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1. FACS-based protocol to assess cytotoxicity and clonogenic potential of colorectal cancer stem cells using a Wnt/β-catenin signaling pathway reporter

Author

Miriam Gaggianesi, Le Zhang, Jan Paul Medema, Simone Di Franco, Giorgio Stassi, Melania Lo Iacono, Simone Di Franco, Le Zhang, Miriam Gaggianesi, Melania Lo Iacono, Jan Paul Medema, Giorgio Stassi, Center of Experimental and Molecular Medicine, Graduate School, CCA - Cancer biology and immunology, CCA - Imaging and biomarkers, Amsterdam Gastroenterology Endocrinology Metabolism, and Radiotherapy

Subjects
Science (General), Colorectal cancer, Tumor initiation, Biology, General Biochemistry, Genetics and Molecular Biology, Q1-390, Cancer stem cell, medicine, Protocol, Humans, Flow Cytometry/Mass Cytometry, Clonogenic assay, Wnt Signaling Pathway, Cancer, General Immunology and Microbiology, General Neuroscience, Stem Cells, Wnt signaling pathway, Cell Biology, medicine.disease, Flow Cytometry, Molecular/Chemical Probes, Cancer cell, colorectal cancers, cancer stem cells, FACS, Wnt, Cell isolation, Cancer research, Neoplastic Stem Cells, Cell-based Assays, Stem cell, Settore MED/46 - Scienze Tecniche Di Medicina Di Laboratorio, Colorectal Neoplasms, Signal Transduction
Abstract

Summary Cancer stem cells (CSCs) play a key role in tumor initiation and progression. A real-time tool to evaluate the activation of CSC-specific signaling pathways is crucial for the study of this cancer cell subset. Here, we present a protocol to monitor, in vitro, the activation of Wnt/β-catenin signaling pathway, which is considered a functional biomarker for colorectal CSCs (CR-CSCs). This flow-cytometry-based protocol allows it to isolate CR-CSCs and to evaluate their cytotoxicity upon anti-tumor treatments. For complete details on the use and execution of this protocol, please refer to Di Franco et al. (2021)., Graphical abstract, Highlights • Protocol to investigate the CSC cytotoxicity based on the use of Wnt reporter • Stable lentiviral transduction of colorectal cancer cells with Wnt reporter • Flow cytometry analysis of apotosis induction in Wnt+/– colorectal cancer cells • Extreme limiting dilution analysis (ELDA) on colorectal cancer cells, Cancer stem cells (CSCs) play a key role in tumor initiation and progression. A real-time tool to evaluate the activation of CSC-specific signaling pathways is crucial for the study of this cancer cell subset. Here, we present a protocol to monitor, in vitro, the activation of Wnt/β-catenin signaling pathway, which is considered a functional biomarker for colorectal CSCs (CR-CSCs). This flow-cytometry-based protocol allows it to isolate CR-CSCs and to evaluate their cytotoxicity upon anti-tumor treatments.

Published
2021

2. A RAC-GEF network critical for early intestinal tumourigenesis

Author

Jim Cassidy, Owen J. Sansom, William C. Clark, Luis Serrano, Volker M. Stucke, Martin J Drysdale, Martin R Turner, Arafath Kaja Najumudeen, R.P. Fordham, Karen Pickering, Lucas B. Zeiger, Ewan J. McGhee, Saskia M. Brachmann, Ann Hedley, Andrew D. Campbell, Kathryn Gilroy, Jeanette A. Johansson, Maureen M. Bain, David F. Vincent, Kevin Myant, Christina Kiel, Kurt I. Anderson, Benjamin LeRoy Miller, Angeliki Malliri, S.R. van Hoof, Sigrid K. Fey, Jan Paul Medema, E.B. Unal, Anna-Karin E. Johnsson, Catherine Nixon, Laura M. Machesky, Douglas Strathdee, Center of Experimental and Molecular Medicine, Radiotherapy, CCA - Cancer biology and immunology, Najumudeen, AK [0000-0002-3764-5721], Zeiger, LB [0000-0002-8712-3112], Gay, DM [0000-0002-7407-1245], Machesky, LM [0000-0002-7592-9856], Nixon, C [0000-0002-8085-2160], Johnsson, AE [0000-0002-0018-700X], Strathdee, D [0000-0003-2959-4327], Anderson, KI [0000-0002-9324-9598], Malliri, A [0000-0001-6848-090X], Turner, M [0000-0002-3801-9896], Serrano, L [0000-0002-5276-1392], Myant, K [0000-0001-8017-1093], Campbell, AD [0000-0003-3930-1276], Sansom, OJ [0000-0001-9540-3010], Apollo - University of Cambridge Repository, Najumudeen, A. K. [0000-0002-3764-5721], Zeiger, L. B. [0000-0002-8712-3112], Gay, D. M. [0000-0002-7407-1245], Machesky, L. M. [0000-0002-7592-9856], Nixon, C. [0000-0002-8085-2160], Johnsson, A. E. [0000-0002-0018-700X], Strathdee, D. [0000-0003-2959-4327], Anderson, K. I. [0000-0002-9324-9598], Malliri, A. [0000-0001-6848-090X], Turner, M. [0000-0002-3801-9896], Serrano, L. [0000-0002-5276-1392], Myant, K. [0000-0001-8017-1093], Campbell, A. D. [0000-0003-3930-1276], and Sansom, O. J. [0000-0001-9540-3010]

Subjects
0301 basic medicine, VAV3, rac1 GTP-Binding Protein, VAV2, Carcinogenesis, Homeòstasi, General Physics and Astronomy, Imaging, 0302 clinical medicine, Guanine Nucleotide Exchange Factors, Homeostasis, T-Lymphoma Invasion and Metastasis-inducing Protein 1, Wnt Signaling Pathway, Mice, Knockout, Multidisciplinary, Wnt signaling pathway, article, Phenotype, Up-Regulation, Colon cancer, Intestines, Organ Specificity, 030220 oncology & carcinogenesis, 64/60, Signal transduction, 631/67/70, Signal Transduction, Science, Adenomatous Polyposis Coli Protein, RAC1, 13/106, 631/67/1504/1885/1393, Biology, General Biochemistry, Genetics and Molecular Biology, 38/91, Proto-Oncogene Proteins p21(ras), 03 medical and health sciences, Downregulation and upregulation, 14/33, Animals, Proto-Oncogene Proteins c-vav, Cancer models, Tumors, General Chemistry, 030104 developmental biology, Mutation, 13/51, Cancer research, Intestins -- Càncer, Genètica
Abstract

RAC1 activity is critical for intestinal homeostasis, and is required for hyperproliferation driven by loss of the tumour suppressor gene Apc in the murine intestine. To avoid the impact of direct targeting upon homeostasis, we reasoned that indirect targeting of RAC1 via RAC-GEFs might be effective. Transcriptional profiling of Apc deficient intestinal tissue identified Vav3 and Tiam1 as key targets. Deletion of these indicated that while TIAM1 deficiency could suppress Apc-driven hyperproliferation, it had no impact upon tumourigenesis, while VAV3 deficiency had no effect. Intriguingly, deletion of either gene resulted in upregulation of Vav2, with subsequent targeting of all three (Vav2−/− Vav3−/− Tiam1−/−), profoundly suppressing hyperproliferation, tumourigenesis and RAC1 activity, without impacting normal homeostasis. Critically, the observed RAC-GEF dependency was negated by oncogenic KRAS mutation. Together, these data demonstrate that while targeting RAC-GEF molecules may have therapeutic impact at early stages, this benefit may be lost in late stage disease., Loss of small GTPase RAC1 suppresses intestinal tumorigenesis caused by APC loss, but impacts normal intestinal homeostasis. Here, the authors provide an alternative method of reducing RAC1 activity by the combined targeting of three RAC-GEFs and show that this approach delays intestinal tumorigenesis without the detrimental effects on normal intestinal architecture.

Published
2021
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3. Correction for Ebbing et al., Stromal-derived interleukin 6 drives epithelial-to-mesenchymal transition and therapy resistance in esophageal adenocarcinoma

Author

Hanneke W. M. van Laarhoven, Simone Hermsen, Michelle Klein, Aafke Creemers, Suzanne S. Gisbertz, Anne Steins, Eva A. Ebbing, Maarten F. Bijlsma, Amber P. van der Zalm, Rosa Rentenaar, Otto M. van Delden, Cornelis J. A. Punt, Gerrit K. J. Hooijer, Cynthia Waasdorp, Sybren L. Meijer, Kausilia K. Krishnadath, Maarten C.C.M. Hulshof, Jan Paul Medema, and Mark I. van Berge Henegouwen

Subjects
IL-6, Multidisciplinary, Stromal cell, Medical Sciences, biology, Transition (genetics), therapy resistance, esophageal adenocarcinoma, business.industry, Mesenchymal stem cell, tumor stroma, Esophageal adenocarcinoma, Biological Sciences, Cancer research, biology.protein, Medicine, epithelial-to-mesenchymal transition, Treatment resistance, business, Interleukin 6
Abstract

Significance We found that cancer-associated fibroblasts, the most abundant noncancer cell type in esophageal cancer tissue, contribute to the resistance of tumors against currently applicable treatments. These cancer-associated fibroblasts do so by producing and secreting IL-6. IL-6 induces a mesenchymal, resistant tumor cell state. Inhibition of IL-6 reverted the mesenchymal cell state and resensitized tumor cells to therapy. Serum-borne proxies for the presence of IL-6–producing fibroblasts were identified and found to be predictive for the response to neoadjuvant therapy., Esophageal adenocarcinoma (EAC) has a dismal prognosis, and survival benefits of recent multimodality treatments remain small. Cancer-associated fibroblasts (CAFs) are known to contribute to poor outcome by conferring therapy resistance to various cancer types, but this has not been explored in EAC. Importantly, a targeted strategy to circumvent CAF-induced resistance has yet to be identified. By using EAC patient-derived CAFs, organoid cultures, and xenograft models we identified IL-6 as the stromal driver of therapy resistance in EAC. IL-6 activated epithelial-to-mesenchymal transition in cancer cells, which was accompanied by enhanced treatment resistance, migratory capacity, and clonogenicity. Inhibition of IL-6 restored drug sensitivity in patient-derived organoid cultures and cell lines. Analysis of patient gene expression profiles identified ADAM12 as a noninflammation-related serum-borne marker for IL-6–producing CAFs, and serum levels of this marker predicted unfavorable responses to neoadjuvant chemoradiation in EAC patients. These results demonstrate a stromal contribution to therapy resistance in EAC. This signaling can be targeted to resensitize EAC to therapy, and its activity can be measured using serum-borne markers.

Published
2021

4. Oncogenic BRAF, unrestrained by TGFβ-receptor signalling, drives right-sided colonic tumorigenesis

Author

Joshua D. G. Leach, Nikola Vlahov, Petros Tsantoulis, Rachel A. Ridgway, Dustin J. Flanagan, Kathryn Gilroy, Nathalie Sphyris, Ester G. Vázquez, David F. Vincent, William J. Faller, Michael C. Hodder, Alexander Raven, Sigrid Fey, Arafath K. Najumudeen, Douglas Strathdee, Colin Nixon, Mark Hughes, William Clark, Robin Shaw, S:CORT consortium, Sander R. van Hooff, David J. Huels, Jan Paul Medema, Simon T. Barry, Margaret C. Frame, Asier Unciti-Broceta, Simon J. Leedham, Gareth J. Inman, Rene Jackstadt, Barry J. Thompson, Andrew D. Campbell, Sabine Tejpar, Owen J. Sansom, Center of Experimental and Molecular Medicine, CCA - Cancer biology and immunology, and Radiotherapy

Subjects
0301 basic medicine, Chemistry(all), MICROSATELLITE INSTABILITY, Carcinogenesis, Colorectal cancer, Cellular differentiation, Receptor, Transforming Growth Factor-beta Type I, General Physics and Astronomy, SESSILE SERRATED ADENOMAS, DISTAL COLON, Kaplan-Meier Estimate, medicine.disease_cause, COLORECTAL-CANCER, 0302 clinical medicine, Transforming Growth Factor beta, Wnt Signaling Pathway, IN-VIVO, Mutation, Multidisciplinary, Cancer stem cells, Wnt signaling pathway, LGR5, Cell Differentiation, Prognosis, Multidisciplinary Sciences, 030220 oncology & carcinogenesis, Colonic Neoplasms, Science & Technology - Other Topics, Stem cell, STEM-CELLS, Signal Transduction, EXPRESSION, Proto-Oncogene Proteins B-raf, Cell Survival, Colon, MAP Kinase Signaling System, Science, INHIBITION, Physics and Astronomy(all), Biology, Article, General Biochemistry, Genetics and Molecular Biology, WNT ACTIVATION, 03 medical and health sciences, Fetus, SDG 3 - Good Health and Well-being, Spheroids, Cellular, medicine, Animals, Progenitor cell, Cancer models, Adaptor Proteins, Signal Transducing, Inflammation, Science & Technology, Biochemistry, Genetics and Molecular Biology(all), INTESTINAL REGENERATION, Epithelial Cells, YAP-Signaling Proteins, General Chemistry, medicine.disease, digestive system diseases, Mice, Inbred C57BL, Wnt Proteins, 030104 developmental biology, Cancer research, Receptors, Transforming Growth Factor beta, Transcription Factors
Abstract

Right-sided (proximal) colorectal cancer (CRC) has a poor prognosis and a distinct mutational profile, characterized by oncogenic BRAF mutations and aberrations in mismatch repair and TGFβ signalling. Here, we describe a mouse model of right-sided colon cancer driven by oncogenic BRAF and loss of epithelial TGFβ-receptor signalling. The proximal colonic tumours that develop in this model exhibit a foetal-like progenitor phenotype (Ly6a/Sca1+) and, importantly, lack expression of Lgr5 and its associated intestinal stem cell signature. These features are recapitulated in human BRAF-mutant, right-sided CRCs and represent fundamental differences between left- and right-sided disease. Microbial-driven inflammation supports the initiation and progression of these tumours with foetal-like characteristics, consistent with their predilection for the microbe-rich right colon and their antibiotic sensitivity. While MAPK-pathway activating mutations drive this foetal-like signature via ERK-dependent activation of the transcriptional coactivator YAP, the same foetal-like transcriptional programs are also initiated by inflammation in a MAPK-independent manner. Importantly, in both contexts, epithelial TGFβ-receptor signalling is instrumental in suppressing the tumorigenic potential of these foetal-like progenitor cells., Right-sided colorectal cancer (rCRC) has a different mutational spectrum to the left-sided counterpart. Here the authors develop a mouse model of rCRC that recapitulates human BRAF-mutant rCRC and show that loss of TGFβ-receptor signalling and inflammation induce the development of colonic tumours with a foetal-like phenotype.

Published
2021
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5. Spatiotemporal regulation of clonogenicity in colorectal cancer xenografts

Author

Erik van Dijk, Jan Paul Medema, Bauke Ylstra, Daniël M. Miedema, Kristiaan J. Lenos, Veronique L. Veenstra, Lisanne E. Nijman, Maartje van der Heijden, Sanne M. van Neerven, Nina E. de Groot, Martin A. Nowak, Douglas J. Winton, Andrea Arricibita Varea, Bartlomiej Waclaw, Edward Morrissey, Maarten F. Bijlsma, Maria C. Lecca, Pramudita R. Prasetyanti, Sophie C. Lodestijn, Louis Vermeulen, Center of Experimental and Molecular Medicine, Graduate School, AGEM - Digestive immunity, AGEM - Re-generation and cancer of the digestive system, CCA - Cancer biology and immunology, Radiotherapy, Pathology, and Molecular cell biology and Immunology

Subjects
cancer stem cells, Colorectal cancer, Cell, Clone (cell biology), Mice, Nude, colorectal cancer, intratumor heterogeneity, Tumor initiation, Biology, Mice, 03 medical and health sciences, Spatio-Temporal Analysis, 0302 clinical medicine, medicine, Animals, Humans, Malignant cells, Cell Lineage, Tumor growth, Solid tumor, 030304 developmental biology, 0303 health sciences, cancer evolution, Multidisciplinary, Cell Biology, Biological Sciences, medicine.disease, Clone Cells, Cell biology, Biophysics and Computational Biology, tumor growth, medicine.anatomical_structure, 030220 oncology & carcinogenesis, Cancer evolution, Physical Sciences, Heterografts, Female, Colorectal Neoplasms, Neoplasm Transplantation
Abstract

Significance Colorectal cancer (CRC) is a heterogeneous disease, with significant variation in genotype and phenotype within each individual tumor. This intratumor heterogeneity emerges during tumor development due to clonal evolution and in part can explain therapy resistance in CRC. However, a detailed understanding of the spatiotemporal development of tumors underlying cancer evolution and intratumor heterogeneity remains absent. Here, we use lineage-tracing experiments of human CRC cells transplanted into immunocompromised mice, in combination with computational modeling, to study the growth mode of CRC. We found that the clonal position is crucial for clonal outgrowth. This demonstrates that, in addition to the genetic composition, the environment and the geometry of tumor growth play a significant role in shaping tumor evolution., Cancer evolution is predominantly studied by focusing on differences in the genetic characteristics of malignant cells within tumors. However, the spatiotemporal dynamics of clonal outgrowth that underlie evolutionary trajectories remain largely unresolved. Here, we sought to unravel the clonal dynamics of colorectal cancer (CRC) expansion in space and time by using a color-based clonal tracing method. This method involves lentiviral red-green-blue (RGB) marking of cell populations, which enabled us to track individual cells and their clonal outgrowth during tumor initiation and growth in a xenograft model. We found that clonal expansion largely depends on the location of a clone, as small clones reside in the center and large clones mostly drive tumor growth at the border. These dynamics are recapitulated in a computational model, which confirms that the clone position within a tumor rather than cell-intrinsic features, is crucial for clonal outgrowth. We also found that no significant clonal loss occurs during tumor growth and clonal dispersal is limited in most models. Our results imply that, in addition to molecular features of clones such as (epi-)genetic differences between cells, clone location and the geometry of tumor growth are crucial for clonal expansion. Our findings suggest that either microenvironmental signals on the tumor border or differences in physical properties within the tumor, are major contributors to explain heterogeneous clonal expansion. Thus, this study provides further insights into the dynamics of solid tumor growth and progression, as well as the origins of tumor cell heterogeneity in a relevant model system.

Published
2019
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6. Isolation, propagation, and clonogenicity of intestinal stem cells

Author

Aleksandar Buryanov Kirov, Jan Paul Medema, Prashanthi Ramesh, David J. Huels, Graduate School, CCA - Cancer biology and immunology, Center of Experimental and Molecular Medicine, and Radiotherapy

Subjects
0301 basic medicine, Colorectal cancer, Cancer, Biology, medicine.disease, medicine.disease_cause, Small intestine, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, medicine.anatomical_structure, Cancer stem cell, 030220 oncology & carcinogenesis, Cancer research, medicine, Organoid, Immunohistochemistry, Stem cell, Carcinogenesis
Abstract

Intestinal stem cell research has greatly aided our understanding of the biology of intestinal self-renewal but has also shed light on the role of cancer stem cells (CSCs) in carcinogenesis, cancer growth, and dissemination. With new possibilities for CSC targeting, there is a need to have established techniques for quantifying (cancer) stem cell clonogenicity, particularly in organoid cultures. Here, we describe a detailed methodology for the isolation and expansion of mouse intestinal crypts from three different locations-the colon, proximal, and distal small intestine. In addition, we describe techniques that allow the measurement of stem cell clonogenicity and its manipulation using two approaches-organoid counting and immunohistochemistry.

Published
2019
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7. Chromosomal copy number heterogeneity predicts survival rates across cancers

Author

Lisanne E. Nijman, Cornelis J A Punt, Khalid El Makrini, Erik van Dijk, Bauke Ylstra, Louis Vermeulen, Rebecca C. Fitzgerald, Daniël M. Miedema, Jurriaan B. Tuynman, Tom van den Bosch, Jan Paul Medema, Geert J. P. L. Kops, Hendrik F. van Essen, Michiel Boekhout, Joris H. Hageman, Kristiaan J. Lenos, Hugo J. Snippert, Nico Lansu, van den Bosch, Tom [0000-0002-5266-8446], Lenos, Kristiaan J [0000-0003-1165-8732], Hageman, Joris H [0000-0002-1386-054X], Fitzgerald, Rebecca C [0000-0002-3434-3568], Snippert, Hugo J G [0000-0002-4189-5213], Kops, Geert J P L [0000-0003-3555-5295], Ylstra, Bauke [0000-0001-9479-3010], Vermeulen, Louis [0000-0002-6066-789X], Miedema, Daniël M [0000-0002-0729-3753], Apollo - University of Cambridge Repository, Center of Experimental and Molecular Medicine, Graduate School, CCA - Cancer biology and immunology, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Oncology, Radiotherapy, Hubrecht Institute for Developmental Biology and Stem Cell Research, Lenos, Kristiaan J. [0000-0003-1165-8732], Hageman, Joris H. [0000-0002-1386-054X], Fitzgerald, Rebecca C. [0000-0002-3434-3568], Snippert, Hugo J. G. [0000-0002-4189-5213], Kops, Geert J. P. L. [0000-0003-3555-5295], Miedema, Daniël M. [0000-0002-0729-3753], Snippert, Hugo JG [0000-0002-4189-5213], Kops, Geert JPL [0000-0003-3555-5295], Internal medicine, Surgery, Amsterdam Gastroenterology Endocrinology Metabolism, and Pathology

Subjects
0301 basic medicine, Oncology, Male, Tumor Microenvironment/genetics, General Physics and Astronomy, Datasets as Topic, Disease, 0302 clinical medicine, Models, Chromosome instability, Neoplasms, 80 and over, Cancer genomics, Tumor Microenvironment, Child, Aged, 80 and over, Multidisciplinary, Genomics, Middle Aged, Prognosis, Neoplasms/genetics, Progression-Free Survival, 3. Good health, Survival Rate, Gene Expression Regulation, Neoplastic, 030220 oncology & carcinogenesis, Female, Adult, medicine.medical_specialty, Adolescent, DNA Copy Number Variations, Science, Tumour heterogeneity, 45/23, 631/67/69, Biology, 631/67/2329, Risk Assessment, General Biochemistry, Genetics and Molecular Biology, Article, 03 medical and health sciences, Genetic Heterogeneity, Young Adult, Genetic, Internal medicine, medicine, Humans, Computer Simulation, Progression-free survival, Risk Assessment/methods, Survival rate, Aged, Neoplastic, Models, Genetic, Genetic heterogeneity, Gene Expression Profiling, Cancer, General Chemistry, medicine.disease, Computational biology and bioinformatics, Gene expression profiling, 030104 developmental biology, Gene Expression Regulation, 14/63, Mutation, 631/114
Abstract

Survival rates of cancer patients vary widely within and between malignancies. While genetic aberrations are at the root of all cancers, individual genomic features cannot explain these distinct disease outcomes. In contrast, intra-tumour heterogeneity (ITH) has the potential to elucidate pan-cancer survival rates and the biology that drives cancer prognosis. Unfortunately, a comprehensive and effective framework to measure ITH across cancers is missing. Here, we introduce a scalable measure of chromosomal copy number heterogeneity (CNH) that predicts patient survival across cancers. We show that the level of ITH can be derived from a single-sample copy number profile. Using gene-expression data and live cell imaging we demonstrate that ongoing chromosomal instability underlies the observed heterogeneity. Analysing 11,534 primary cancer samples from 37 different malignancies, we find that copy number heterogeneity can be accurately deduced and predicts cancer survival across tissues of origin and stages of disease. Our results provide a unifying molecular explanation for the different survival rates observed between cancer types., Intratumour heterogeneity (ITH) is associated with worse prognosis in cancer, and efficient frameworks to measure it are needed. Here the authors develop a method to estimate copy number heterogeneity, and propose that it is driven by chromosomal instability and can predict pan-cancer survival.

Published
2021
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8. The extracellular matrix controls stem cell specification and crypt morphology in the developing and adult gut

Author

Owen J. Sansom, T. Martins Garcia, Rana Ramadan, Vanesa Muncan, Jan Paul Medema, S. van Neerven, David J. Huels, Joshua D.G. Leach, Michele A. Battle, K. S. Carlson, Olivia D. Franklin, Louis Vermeulen, and V. M. Wouters

Subjects
Extracellular matrix, medicine.anatomical_structure, biology, Laminin, Paneth cell, Mesenchymal stem cell, medicine, LGR5, biology.protein, Signal transduction, Stem cell, Intestinal epithelium, Cell biology
Abstract

The rapid renewal of the epithelial gut lining is fuelled by stem cells that reside at the base of intestinal crypts. In recent years, the signal transduction pathways and morphogens that regulate intestinal stem cell self-renewal and differentiation have been extensively characterised. In contrast, although extracellular matrix (ECM) components form an integral part of the intestinal stem cell niche, their direct influence on the cellular composition is less well understood. Here, we set out to systematically compare the effect of two major ECM classes, fibrillar collagen type I and the basement membrane, on the intestinal epithelium. We found that both collagen I and laminin-containing cultures allow growth of small intestinal epithelial cells with all differentiated and undifferentiated cell types present in both cultures, albeit at different ratios. Specific to the collagen culture was a subset of cells with a fetal-like gene expression program. In contrast, laminin, but not collagen IV, increased Lgr5+ stem cells and Paneth cells, and induced crypt-like morphology changes. The transition from a collagen culture to a laminin culture, resembles the gut development in vivo. Here, the ECM is dramatically remodelled by mesenchymal cells, which is accompanied by a specific and local expression of the laminin receptor ITGA6 in the crypt-forming epithelium. This laminin:ITGA6 signalling is essential for the stem cell induction and crypt formation in vitro. Importantly, deletion of laminin in the adult mouse results in a fetal-like epithelium with a marked reduction of adult intestinal stem cells. Overall, our data support the hypothesis that the formation of intestinal crypts is induced by an increased laminin concentration in the ECM.

Published
2021
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9. BH3 Mimetic Sensitivity of Colorectal Cancer Cell Lines in Correlation with Molecular Features Identifies Predictors of Response

Author

Le Zhang, Prashanthi Ramesh, Maxime Steinmetz, Jan Paul Medema, Center of Experimental and Molecular Medicine, Graduate School, AII - Cancer immunology, CCA - Cancer biology and immunology, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, and Radiotherapy

Subjects
BH3 mimetics, Colorectal cancer, medicine.medical_treatment, Apoptosis, Disease, medicine.disease_cause, lcsh:Chemistry, Biomimetics, BCL-XL, lcsh:QH301-705.5, Spectroscopy, Mutation, biology, Cell Death, General Medicine, Computer Science Applications, Gene Expression Regulation, Neoplastic, KRAS, Colorectal Neoplasms, BH3 Interacting Domain Death Agonist Protein, Proto-Oncogene Proteins B-raf, Programmed cell death, BCL-2, Bcl-xL, Antineoplastic Agents, Article, Catalysis, Inorganic Chemistry, Proto-Oncogene Proteins p21(ras), Cell Line, Tumor, medicine, Humans, Physical and Theoretical Chemistry, consensus molecular subtype (CMS), neoplasms, Molecular Biology, Chemotherapy, Dose-Response Relationship, Drug, Organic Chemistry, Molecular Mimicry, Consensus molecular sub-type (CMS), medicine.disease, digestive system diseases, lcsh:Biology (General), lcsh:QD1-999, Cell culture, Cancer research, biology.protein, MCL-1, Apoptosis Regulatory Proteins
Abstract

Colorectal cancer (CRC) is a heterogeneous disease, which in part explains the differential response to chemotherapy observed in the clinic. BH3 mimetics, which target anti-apoptotic BCL-2 family members, have shown potential in the treatment of hematological malignancies and offer promise for the treatment of solid tumors as well. To gain a comprehensive understanding of the response to BH3 mimetics in CRC and the underlying molecular factors predicting sensitivity, we screened a panel of CRC cell lines with four BH3 mimetics targeting distinct anti-apoptotic BCL-2 proteins. Treatment with compounds alone and in combination revealed potent efficacy of combined MCL-1 and BCL-XL inhibition in inducing CRC cell death, irrespective of molecular features. Importantly, expression of the anti-apoptotic protein target of BH3 mimetics on its own did not predict sensitivity. However, the analysis did identify consensus molecular subtype (CMS) specific response patterns, such as higher resistance to single and combined BCL-2 and MCL-1 inhibition in CMS2 cell lines. Furthermore, analysis of mutation status revealed that KRAS mutant cell lines were more resistant to MCL-1 inhibition. Conclusively, we find that CRC cell lines presented with distinct responses to BH3 mimetics that can in part be predicted by their CMS profile and KRAS/BRAF mutations. Overall, almost all CRC lines share sensitivity in the nanomolar range to combined MCL-1 and BCL-XL targeting suggesting that this would be the preferred approach to target these cancers.

Published
2021

10. AKT3 Expression in Mesenchymal Colorectal Cancer Cells Drives Growth and Is Associated with Epithelial-Mesenchymal Transition

Author

Jan Paul Medema, Danielle Dekker, Arezo Torang, Louis Vermeulen, Joan H. de Jong, Sara Vitale, Joyce Y. Buikhuisen, Kate Cameron, Sander R. van Hooff, Patricia M. Gomez Barila, Giorgio Stassi, Mauro A. A. Castro, Center of Experimental and Molecular Medicine, Graduate School, CCA - Cancer biology and immunology, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Radiotherapy, Buikhuisen J.Y., Barila P.M.G., Torang A., Dekker D., de Jong J.H., Cameron K., Vitale S., Stassi G., van Hooff S.R., Castro M.A.A., Vermeulen L., and Medema J.P.

Subjects
0301 basic medicine, Cancer Research, Colorectal cancer, growth, Biology, lcsh:RC254-282, AKT3, Article, 03 medical and health sciences, 0302 clinical medicine, medicine, mesenchymal CRC, Epithelial–mesenchymal transition, CMS, Mesenchymal stem cell, Cell cycle, medicine.disease, lcsh:Neoplasms. Tumors. Oncology. Including cancer and carcinogens, Phenotype, Gene expression profiling, 030104 developmental biology, Oncology, 030220 oncology & carcinogenesis, Cancer cell, Cancer research, Settore MED/46 - Scienze Tecniche Di Medicina Di Laboratorio
Abstract

Simple Summary Colorectal cancer can be subdivided into four distinct subtypes that are characterised by different clinical features and responses to therapies currently used in the clinic to treat this disease. One of those subtypes, called CMS4, is associated with a worse prognosis and poor response to therapies compared to other subtypes. We therefore set out to explore what proteins are differentially expressed and used in CMS4 to find potential new targets for therapy. We found that protein AKT3 is highly expressed in CMS4, and that active AKT3 inhibits a protein that stalls growth of cancer cells (p27KIP1). We can target AKT3 with inhibitors which leads to strongly reduced growth of cancer cell lines that are categorised as CMS4. Furthermore, our data suggests that high AKT3 expression in tumour cells may be used to identify poor prognosis colorectal cancer patients. Future research should point out if high AKT3 expression can be used to select colorectal cancer patients that have a poor prognosis but that could benefit from AKT3-targeted treatment. Abstract Colorectal cancer (CRC) is a heterogeneous disease that can currently be subdivided into four distinct consensus molecular subtypes (CMS) based on gene expression profiling. The CMS4 subtype is marked by high expression of mesenchymal genes and is associated with a worse overall prognosis compared to other CMSs. Importantly, this subtype responds poorly to the standard therapies currently used to treat CRC. We set out to explore what regulatory signalling networks underlie the CMS4 phenotype of cancer cells, specifically, by analysing which kinases were more highly expressed in this subtype compared to others. We found AKT3 to be expressed in the cancer cell epithelium of CRC specimens, patient derived xenograft (PDX) models and in (primary) cell cultures representing CMS4. Importantly, chemical inhibition or knockout of this gene hampers outgrowth of this subtype, as AKT3 controls expression of the cell cycle regulator p27KIP1. Furthermore, high AKT3 expression was associated with high expression of epithelial-mesenchymal transition (EMT) genes, and this observation could be expanded to cell lines representing other carcinoma types. More importantly, this association allowed for the identification of CRC patients with a high propensity to metastasise and an associated poor prognosis. High AKT3 expression in the tumour epithelial compartment may thus be used as a surrogate marker for EMT and may allow for a selection of CRC patients that could benefit from AKT3-targeted therapy.

Published
2021

11. BCL-XL is crucial for progression through the adenoma-to-carcinoma sequence of colorectal cancer

Author

Tamsin R M Lannagan, Prashanthi Ramesh, Owen J. Sansom, Rene Jackstadt, Jan Paul Medema, Geert J. P. L. Kops, Lidia Atencia Taboada, Sanne M. van Neerven, Aleksandar Buryanov Kirov, Pratyaksha Wirapati, Sabine Tejpar, Danielle Dekker, Jessica Pritchard, Nico Lansu, Sander R. van Hooff, Center of Experimental and Molecular Medicine, Graduate School, AII - Cancer immunology, CCA - Cancer biology and immunology, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Radiotherapy, and Hubrecht Institute for Developmental Biology and Stem Cell Research

Subjects
HUMAN COLON, EXPRESSION, Adenoma, Male, Biochemistry & Molecular Biology, Cell biology, Colorectal cancer, bcl-X Protein, Bcl-xL, Apoptosis, MYC, medicine.disease_cause, Article, Mice, Downregulation and upregulation, microRNA, medicine, Animals, Humans, MCL1, Cancer models, Molecular Biology, Science & Technology, biology, MUTATIONS, Cancer stem cells, INHIBITOR, Cancer, Cell Biology, medicine.disease, GENE, Survival Analysis, APOPTOSIS, POLYPOSIS, TARGET, biology.protein, Cancer research, Disease Progression, Female, Stem cell, Carcinogenesis, Colorectal Neoplasms, Life Sciences & Biomedicine, STEM-CELLS
Abstract

Evasion of apoptosis is a hallmark of cancer, which is frequently mediated by upregulation of the antiapoptotic BCL-2 family proteins. In colorectal cancer (CRC), previous work has highlighted differential antiapoptotic protein dependencies determined by the stage of the disease. While intestinal stem cells (ISCs) require BCL-2 for adenoma outgrowth and survival during transformation, ISC-specific MCL1 deletion results in disturbed intestinal homeostasis, eventually contributing to tumorigenesis. Colon cancer stem cells (CSCs), however, no longer require BCL-2 and depend mainly on BCL-XL for their survival. We therefore hypothesized that a shift in antiapoptotic protein reliance occurs in ISCs as the disease progresses from normal to adenoma to carcinoma. By targeting antiapoptotic proteins with specific BH3 mimetics in organoid models of CRC progression, we found that BCL-2 is essential only during ISC transformation while MCL1 inhibition did not affect adenoma outgrowth. BCL-XL, on the other hand, was crucial for stem cell survival throughout the adenoma-to-carcinoma sequence. Furthermore, we identified that the limited window of BCL-2 reliance is a result of its downregulation by miR-17-5p, a microRNA that is upregulated upon APC-mutation driven transformation. Here we show that BCL-XL inhibition effectively impairs adenoma outgrowth in vivo and enhances the efficacy of chemotherapy. In line with this dependency, expression of BCL-XL, but not BCL-2 or MCL1, directly correlated to the outcome of chemotherapy-treated CRC patients. Our results provide insights to enable the rational use of BH3 mimetics in CRC management, particularly underlining the therapeutic potential of BCL-XL targeting mimetics in both early and late-stage disease.

Published
2021

12. PI3K-driven HER2 expression is a potential therapeutic target in colorectal cancer stem cells

Author

Paola Bianca, Melania Lo Iacono, Laura Rosa Mangiapane, Micol E. Fiori, Maria Rita Bongiorno, Matilde Todaro, Luca Fagnocchi, Sven Beyes, Michele Signore, Veronica Veschi, Miriam Gaggianesi, Jan Paul Medema, Gaspare Gulotta, Irene Pillitteri, Annalisa Nicotra, Alice Turdo, Simone Di Franco, Ruggero De Maria, Gloria Ganduscio, Davide Stefano Sardina, Alessio Zippo, Giorgio Stassi, Mangiapane L.R., Nicotra A., Turdo A., Gaggianesi M., Bianca P., Di Franco S., Sardina D.S., Veschi V., Signore M., Beyes S., Fagnocchi L., Fiori M.E., Bongiorno M.R., Lo Iacono M., Pillitteri I., Ganduscio G., Gulotta G., Medema J.P., Zippo A., Todaro M., De Maria R., Stassi G., Center of Experimental and Molecular Medicine, Radiotherapy, and CCA - Cancer biology and immunology

Subjects
0301 basic medicine, Receptor, ErbB-2, Colorectal cancer, Cetuximab, colorectal cancer, medicine.disease_cause, 03 medical and health sciences, Antineoplastic Agents, Immunological, 0302 clinical medicine, Settore MED/04 - PATOLOGIA GENERALE, Cancer stem cell, stem cells, Tumor Cells, Cultured, medicine, Adjuvant therapy, Animals, Humans, Epidermal growth factor receptor, Protein kinase B, PI3K/AKT/mTOR pathway, Phosphoinositide-3 Kinase Inhibitors, Mitogen-Activated Protein Kinase Kinases, drug resistance, biology, business.industry, Gastroenterology, Trastuzumab, medicine.disease, antibody targeted therapy, 030104 developmental biology, Drug Resistance, Neoplasm, 030220 oncology & carcinogenesis, Neoplastic Stem Cells, Cancer research, biology.protein, KRAS, Phosphatidylinositol 3-Kinase, Stem cell, Colorectal Neoplasms, business
Abstract

ObjectiveCancer stem cells are responsible for tumour spreading and relapse. Human epidermal growth factor receptor 2 (HER2) expression is a negative prognostic factor in colorectal cancer (CRC) and a potential target in tumours carrying the gene amplification. Our aim was to define the expression of HER2 in colorectal cancer stem cells (CR-CSCs) and its possible role as therapeutic target in CRC resistant to anti- epidermal growth factor receptor (EGFR) therapy.DesignA collection of primary sphere cell cultures obtained from 60 CRC specimens was used to generate CR-CSC mouse avatars to preclinically validate therapeutic options. We also made use of the ChIP-seq analysis for transcriptional evaluation of HER2 activation and global RNA-seq to identify the mechanisms underlying therapy resistance.ResultsHere we show that in CD44v6-positive CR-CSCs, high HER2 expression levels are associated with an activation of the phosphatidylinositol 3-kinase (PI3K)/AKT pathway, which promotes the acetylation at the regulatory elements of the Erbb2 gene. HER2 targeting in combination with phosphatidylinositol 3-kinase (PI3K) and mitogen-activated protein kinase kinase (MEK) inhibitors induces CR-CSC death and regression of tumour xenografts, including those carrying Kras and Pik3ca mutation. Requirement for the triple targeting is due to the presence of cancer-associated fibroblasts, which release cytokines able to confer CR-CSC resistance to PI3K/AKT inhibitors. In contrast, targeting of PI3K/AKT as monotherapy is sufficient to kill liver-disseminating CR-CSCs in a model of adjuvant therapy.ConclusionsWhile PI3K targeting kills liver-colonising CR-CSCs, the concomitant inhibition of PI3K, HER2 and MEK is required to induce regression of tumours resistant to anti-EGFR therapies. These data may provide a rationale for designing clinical trials in the adjuvant and metastatic setting.

Published
2021

13. Apc-mutant cells act as supercompetitors in intestinal tumour initiation

Author

Edward Morrissey, Leandro F. Moreno, Vaishali Kakkar, Maria C. Lecca, Douglas J. Winton, Przemek M. Krawczyk, Prashanthi Ramesh, Jan Paul Medema, Louis Vermeulen, Arthur S. Aelvoet, Daniël O. Warmerdam, Nina E. de Groot, Milou S. van Driel, Lisanne E. Nijman, Jan Koster, Nicolas Léveillé, Evelien Dekker, Sanne ten Hoorn, Felipe A. Vieira Braga, Sanne M. van Neerven, Lianne Koens, Marouska F. van Boxel, Maarten F. Bijlsma, Delano R. Sanches, Brendon P. Scicluna, Center of Experimental and Molecular Medicine, Graduate School, CCA - Cancer biology and immunology, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Epidemiology and Data Science, Gastroenterology and Hepatology, Pathology, Medical Biology, Oncogenomics, and Radiotherapy

Subjects
0301 basic medicine, Multidisciplinary, Colorectal cancer, Crypt, Mutant, Wnt signaling pathway, Cancer, Biology, medicine.disease, digestive system, Cell biology, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, 030220 oncology & carcinogenesis, medicine, Compartment (development), Stem cell, Function (biology)
Abstract

A delicate equilibrium of WNT agonists and antagonists in the intestinal stem cell (ISC) niche is critical to maintaining the ISC compartment, as it accommodates the rapid renewal of the gut lining. Disruption of this balance by mutations in the tumour suppressor gene APC, which are found in approximately 80% of all human colon cancers, leads to unrestrained activation of the WNT pathway1,2. It has previously been established that Apc-mutant cells have a competitive advantage over wild-type ISCs3. Consequently, Apc-mutant ISCs frequently outcompete all wild-type stem cells within a crypt, thereby reaching clonal fixation in the tissue and initiating cancer formation. However, whether the increased relative fitness of Apc-mutant ISCs involves only cell-intrinsic features or whether Apc mutants are actively involved in the elimination of their wild-type neighbours remains unresolved. Here we show that Apc-mutant ISCs function as bona fide supercompetitors by secreting WNT antagonists, thereby inducing differentiation of neighbouring wild-type ISCs. Lithium chloride prevented the expansion of Apc-mutant clones and the formation of adenomas by rendering wild-type ISCs insensitive to WNT antagonists through downstream activation of WNT by inhibition of GSK3β. Our work suggests that boosting the fitness of healthy cells to limit the expansion of pre-malignant clones may be a powerful strategy to limit the formation of cancers in high-risk individuals.

Published
2021
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14. 499 AT1636, a colon cancer survivor-derived antibody recognizes a previously unidentified truncated, O-mannosylated 70kDa variant of E-cadherin

Author

Veronika Kattler, Hans van Eenennaam, Yvonne Claassen, Jan Paul Medema, Tim Beaumont, Kelly Maijoor, Lina Bartels, Evelien Dekker, Camille Bru, Victorine H. Roos, Sabrina J. Merat, Martijn Kedde, Gemma Moiset, Frank G. J. Kallenberg, Mark J. Kwakkenbos, Martino Bohne, Arjen Q. Bakker, Pauline M. van Helden, Hergen Spits, Paul J. Hensbergen, Dorien van der Berg, and Koen Wagner

Subjects
Antibody-dependent cell-mediated cytotoxicity, Biology, lcsh:Neoplasms. Tumors. Oncology. Including cancer and carcinogens, medicine.disease, BCL6, lcsh:RC254-282, Lynch syndrome, Epitope, medicine.anatomical_structure, Antibody Repertoire, Monoclonal, Cancer research, biology.protein, medicine, Antibody, B cell
Abstract

Background Colorectal cancer (CRC) associated with Lynch syndrome is characterized by an abundance of infiltrating lymphocytes. To study whether tumor-specific antibodies with therapeutic potential can be isolated from these patients, the B-cell repertoire from a patient with Lynch syndrome who recovered from a stage IV colon carcinoma was screened. Here we describe an antibody, AT1636 that recognizes a previously unidentified O-mannosylated 70kDa form of E-cadherin. The intercellular interactions by E-cadherin on tumor cells have for long been recognized as protective in cancer metastasis, and deregulation of E-cadherin is a hallmark for epithelial-mesenchymal transition (EMT). Methods The study protocol was approved by the Medical Ethical Committee of the Academic Medical Centre, Amsterdam, The Netherlands (NL42718.018.12). AIMM’s BCL6 and Bcl-xL immortalization method1 was used to interrogate the human antibody repertoire. From a carrier of a pathogenic gene variant in the MSH6 gene diagnosed with stage IV CRC and liver metastasis that had been treated with avastin, capecitabine and oxaliplatin, peripheral-blood memory B cells were obtained 9 years after last treatment. Antibodies-containing supernatant of cultured B-cells were screened for binding to 3 different CRC cell lines (DLD1, LS174T and COLO205) and absence of binding to fibroblast by flow cytometry. A high-affinity variant of AT1636 (AT1636IYN) was sorted from the original AT1636, AID-expressing B-cell clone.2 Results Antibodies that demonstrated differential binding to CRC cells were characterized and targets recognized by such antibodies were identified using immunoprecipitation and mass-spectrometry. One of the antibodies, AT1636, recognized a previously unidentified O-mannosylated 70kDa E-cadherin variant (ECV). Although the 70kDa ECV is found in all full-length E-cadherin expressing cells, tumor-specific binding of AT1636 is dependent on the O-mannosylation pattern in the antibody epitope on ECV. Using shRNA knock-down AT1636 binding was shown to depend on the transmembrane O-mannosyltransferase targeting cadherins 3 (TMTC3). 3 In accordance, coexpression of TMTC3 and E-cadherin in tumor cells is predictive for AT1636 binding. In addition, we observed that (over)expression of ECV results in a strong de-adhesive, EMT-like phenotype. Although AT1636 by itself is not able to induce ADCC, the CD3-bispecific antibody (single-chain UCHT1) AT1636 format specifically killed CRC cell lines. Conclusions The AT1636 antibody retrieved from a patient with Lynch syndrome binds a previous unidentified cancer-specific O-mannosylated 70kDa form of E-cadherin. This variant might play a role in tumor-cell invasion and metastasis. More importantly, we provide a rationale to advance AT1636 based therapeutics for treatment of CRC. Ethics Approval The study protocol was approved by the Medical Ethical Committee of the Academic Medical Centre, Amsterdam, The Netherlands (NL42718.018.12) References M.J. Kwakkenbos, et al. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nature Medicine 2010;16:123–128. K. Wagner, et al. Bispecific antibody generated with sortase and click chemistry has broad antiinfluenza virus activity. Proc Natl Acad Sci USA 2014; 111: 16820–16825. I.S.B. Larsen, et al. Discovery of an O-mannosylation pathway selectively serving cadherins and protocadherins. Proc Natl Acad Sci USA 2017;114:11163–11168.

Published
2020
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15. High-grade mesenchymal pancreatic ductal adenocarcinoma drives stromal deactivation through CSF-1

Author

Frederike Dijk, Cansu Tekin, Bryan Serrels, Joanne Verheij, Hemant M. Kocher, Anne Steins, Geertjan van Tienhoven, Johanna W. Wilmink, Cynthia Waasdorp, Remy Klaassen, Hanneke W. M. van Laarhoven, Jan Paul Medema, Sandrine G. Goris, Maarten F. Bijlsma, Marc J. van de Vijver, Olivier R. Busch, Marc G. Besselink, Madelaine G. van Mackelenbergh, Joan H. de Jong, Amber P. van der Zalm, Pathology, CCA - Cancer biology and immunology, CCA - Imaging and biomarkers, Radiation Oncology, Internal medicine, VU University medical center, Graduate School, AGEM - Re-generation and cancer of the digestive system, Oncology, Center of Experimental and Molecular Medicine, Surgery, AGEM - Digestive immunity, AGEM - Endocrinology, metabolism and nutrition, Radiotherapy, and CCA -Cancer Center Amsterdam

Subjects
collagen, Pancreatic ductal adenocarcinoma, Stromal cell, endocrine system diseases, CSF‐1, pancreatic stellate cells, Biochemistry, Article, 03 medical and health sciences, 0302 clinical medicine, Stroma, CSF-1, Cell Movement, Cell Line, Tumor, Tumor Microenvironment, Genetics, Humans, News & Views, Receptor, Molecular Biology, Cancer, 030304 developmental biology, 0303 health sciences, biology, Chemistry, Macrophage Colony-Stimulating Factor, Mesenchymal stem cell, Articles, digestive system diseases, Pancreatic Neoplasms, Cell culture, Cancer research, Hepatic stellate cell, biology.protein, Stromal Cells, ACTA2, deactivation, 030217 neurology & neurosurgery, Carcinoma, Pancreatic Ductal
Abstract

Pancreatic ductal adenocarcinoma (PDAC) is characterized by an abundance of stroma. Multiple molecular classification efforts have identified a mesenchymal tumor subtype that is consistently characterized by high‐grade growth and poor clinical outcome. The relation between PDAC stroma and tumor subtypes is still unclear. Here, we aimed to identify how PDAC cells instruct the main cellular component of stroma, the pancreatic stellate cells (PSCs). We found in primary tissue that high‐grade PDAC had reduced collagen deposition compared to low‐grade PDAC. Xenografts and organotypic co‐cultures established from mesenchymal‐like PDAC cells featured reduced collagen and activated PSC content. Medium transfer experiments using a large set of PDAC cell lines revealed that mesenchymal‐like PDAC cells consistently downregulated ACTA2 and COL1A1 expression in PSCs and reduced proliferation. We identified colony‐stimulating factor 1 as the mesenchymal PDAC‐derived ligand that deactivates PSCs, and inhibition of its receptor CSF1R was able to counteract this effect. In conclusion, high‐grade PDAC features stroma that is low in collagen and activated PSC content, and targeting CSF1R offers direct options to maintain a tumor‐restricting microenvironment., This study reveals that PDAC cells counteract mechanical restrictions of tumor stroma by secreting CSF‐1, which could be a potential therapeutic target.

Published
2020
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16. Unsupervised class discovery in pancreatic ductal adenocarcinoma reveals cell-intrinsic mesenchymal features and high concordance between existing classification systems

Author

Veronique L. Veenstra, Eline C. Soer, Marc G. Besselink, Sjors Klompmaker, Xin Wang, Anne Steins, Cynthia Waasdorp, Gerrit K. J. Hooijer, Johannes B G Halfwerk, Frederike Dijk, Jan Koster, Olivier R. Busch, Lan Zhao, Jan Paul Medema, Sander R. van Hooff, Mark P. G. Dings, Johanna A. M. G. Tol, Hanneke W. M. van Laarhoven, Louis Vermeulen, Lennart B. van Rijssen, Hanneke Wilmink, Lieke Welling, Marc J. van de Vijver, Helene Damhofer, Joanne Verheij, Maarten F. Bijlsma, Marco Marzano, Pathology, AII - Cancer immunology, CCA - Cancer biology and immunology, Center of Experimental and Molecular Medicine, AGEM - Re-generation and cancer of the digestive system, Graduate School, Surgery, AGEM - Digestive immunity, AGEM - Endocrinology, metabolism and nutrition, Ear, Nose and Throat, Oncology, Radiotherapy, CCA - Imaging and biomarkers, Oncogenomics, Internal medicine, and VU University medical center

Subjects
Adult, Male, Pancreatic ductal adenocarcinoma, Tumour heterogeneity, Concordance, Transplantation, Heterologous, Cell, lcsh:Medicine, Classification scheme, Kaplan-Meier Estimate, Computational biology, Biology, Article, Functional clustering, Mice, medicine, Animals, Humans, Tumor growth, lcsh:Science, Aged, Proportional Hazards Models, Aged, 80 and over, Multidisciplinary, Sequence Analysis, RNA, lcsh:R, Mesenchymal stem cell, RNA sequencing, Transcript analysis, Pancreatic cancer, Middle Aged, Prognosis, Pancreatic Neoplasms, medicine.anatomical_structure, Invasive growth, Tandem Repeat Sequences, Female, lcsh:Q, Carcinoma, Pancreatic Ductal
Abstract

Pancreatic ductal adenocarcinoma (PDAC) has the worst prognosis of all common cancers. However, divergent outcomes exist between patients, suggesting distinct underlying tumor biology. Here, we delineated this heterogeneity, compared interconnectivity between classification systems, and experimentally addressed the tumor biology that drives poor outcome. RNA-sequencing of 90 resected specimens and unsupervised classification revealed four subgroups associated with distinct outcomes. The worst-prognosis subtype was characterized by mesenchymal gene signatures. Comparative (network) analysis showed high interconnectivity with previously identified classification schemes and high robustness of the mesenchymal subtype. From species-specific transcript analysis of matching patient-derived xenografts we constructed dedicated classifiers for experimental models. Detailed assessments of tumor growth in subtyped experimental models revealed that a highly invasive growth pattern of mesenchymal subtype tumor cells is responsible for its poor outcome. Concluding, by developing a classification system tailored to experimental models, we have uncovered subtype-specific biology that should be further explored to improve treatment of a group of PDAC patients that currently has little therapeutic benefit from surgical treatment.

Published
2020
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17. Stem cell functionality is microenvironmentally defined during tumour expansion and therapy response in colon cancer

Author

Sophie C. Lodestijn, Xavier Romero Ros, Douglas J. Winton, Felipe De Sousa E Melo, Maarten F. Bijlsma, Kristiaan J. Lenos, Jan Paul Medema, Nicolas Léveillé, Filipe C. Lourenco, Lianne Koens, Guillaume Hypolite, Daniël M. Miedema, Maartje van der Heijden, Giorgio Stassi, Lisanne E. Nijman, Scott K. Lyons, Louis Vermeulen, Tom van den Bosch, Joy Otten, Patrick Veerman, Ronja S. Adam, Anita van Oort, Maria C. Lecca, Edward Morrissey, Sanne M. van Neerven, Lenos, Kristiaan J, Miedema, Daniël M, Lodestijn, Sophie C, Nijman, Lisanne E, van den Bosch, Tom, Romero Ros, Xavier, Lourenço, Filipe C, Lecca, Maria C, van der Heijden, Maartje, van Neerven, Sanne M, van Oort, Anita, Leveille, Nicola, Adam, Ronja S, de Sousa E Melo, Felipe, Otten, Joy, Veerman, Patrick, Hypolite, Guillaume, Koens, Lianne, Lyons, Scott K, Stassi, Giorgio, Winton, Douglas J, Medema, Jan Paul, Morrissey, Edward, Bijlsma, Maarten F, Vermeulen, Louis, Center of Experimental and Molecular Medicine, CCA - Cancer biology and immunology, Graduate School, AGEM - Re-generation and cancer of the digestive system, AGEM - Digestive immunity, Pathology, and Radiotherapy

Subjects
0301 basic medicine, Colorectal cancer, Cell, Clone (cell biology), Mice, Nude, Context (language use), Colon cancer, cancer stem cells, tumor microenvironment, Article, 03 medical and health sciences, Cancer stem cell, Cancer Stem Cells, Antineoplastic Combined Chemotherapy Protocols, medicine, Tumor Microenvironment, Animals, Humans, Osteopontin (OPN, Spp1), Osteopontin, Stem Cell Dynamics, Cells, Cultured, Cell Proliferation, biology, Colon Cancer, Gene Expression Profiling, Cancer, Disease Relapse, Tumour growth, Cell Biology, medicine.disease, Xenograft Model Antitumor Assays, Cell biology, Gene Expression Regulation, Neoplastic, Oxaliplatin, Tamoxifen, 030104 developmental biology, medicine.anatomical_structure, Colonic Neoplasms, biology.protein, Neoplastic Stem Cells, Therapy, Stem cell, Cues
Abstract

Solid malignancies have been speculated to depend on cancer stem cells (CSCs) for expansion and relapse after therapy. Here we report on quantitative analyses of lineage tracing data from primary colon cancer xenograft tissue to assess CSC functionality in a human solid malignancy. The temporally obtained clone size distribution data support a model in which stem cell function in established cancers is not intrinsically, but is entirely spatiotemporally orchestrated. Functional stem cells that drive tumour expansion predominantly reside at the tumour edge, close to cancer-associated fibroblasts. Hence, stem cell properties change in time depending on the cell location. Furthermore, although chemotherapy enriches for cells with a CSC phenotype, in this context functional stem cell properties are also fully defined by the microenvironment. To conclude, we identified osteopontin as a key cancer-associated fibroblast-produced factor that drives in situ clonogenicity in colon cancer.

Published
2018

18. Patched-2 functions to limit Patched-1 deficient skin cancer growth

Author

Ilse Dingjan, Jan Paul Medema, Helene Damhofer, Cynthia Waasdorp, Maarten F. Bijlsma, Hanneke W. M. van Laarhoven, Allard C. van der Wal, Veronique L. Veenstra, CCA - Cancer biology and immunology, AGEM - Re-generation and cancer of the digestive system, Graduate School, Center of Experimental and Molecular Medicine, Pathology, ACS - Heart failure & arrhythmias, Oncology, and Radiotherapy

Subjects
0301 basic medicine, Patched, Cancer Research, Skin Neoplasms, Cell Survival, Cancer development and immune defence Radboud Institute for Molecular Life Sciences [Radboudumc 2], Hedgehog signaling, Patched-2 Receptor, Mice, 03 medical and health sciences, All institutes and research themes of the Radboud University Medical Center, Cell Line, Tumor, Animals, Humans, Sonic hedgehog, Hedgehog, Tissue homeostasis, Smoothened, Original Paper, biology, Reverse Transcriptase Polymerase Chain Reaction, Chemistry, General Medicine, Hedgehog signaling pathway, Cell biology, Patched-1 Receptor, PTCH2, 030104 developmental biology, Oncology, PTCH1, Carcinoma, Basal Cell, Basal cell carcinoma, biology.protein, Molecular Medicine, Signal Transduction
Abstract

Purpose Basal cell carcinoma (BCC) is one of the most common skin cancers, and is typically driven by an aberrantly activated Hedgehog (Hh) pathway. The Hh pathway is regulated by interactions between the Patched-1 (Ptch1) and Smoothened (Smo) receptors. Smo is an activating receptor and is subject to inhibition by Ptch1. Following ligand binding to Ptch1, its inhibitory action is relieved and pathway activation occurs. This receptor interaction is pivotal to restraining uncontrolled cellular growth. Both receptors have been found to be frequently mutated in BCCs. Ptch2 is a Ptch1 paralog that exhibits overlapping functions in both normal development and tissue homeostasis. As yet, its contribution to cancer growth is poorly defined. Here we set out to assess how Ptch2 inhibits BCC growth. Methods We used several in vitro readouts for transcriptional and chemotactic Hh signaling in BCC-derived ASZ001 cells, and a novel xenograft model to assess in vivo BCC tumor growth. Gene editing by TALEN was used to untangle the different Ptch2-dependent responses to its ligand sonic hedgehog (Shh). Results We first defined the signaling competence of Ptch2 in Ptch1-deficient ASZ001 cells in vitro, and found that Ptch2 ligand binding drives their migration rather than eliciting a transcriptional response. We found that subsequent targeting of Ptch2 abrogated the chemotaxic effect. Next, we tested the contribution of Ptch2 to in vivo tumor growth using a xenograft model and found that reduced Ptch function results in increased tumor growth, but that selective pressure appatently acts against complete Ptch2 ablation. Conclusions We conclude that like Ptch1, Ptch2 exerts a tumor-suppressive function in BCC cells, and that after targeting of both paralogs, ligand-independent activation of the Hh pathway contributes to tumor growth. Electronic supplementary material The online version of this article (10.1007/s13402-018-0381-9) contains supplementary material, which is available to authorized users.

Published
2018
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19. Consensus molecular subtypes of colorectal cancer are recapitulated in in vitro and in vivo models

Author

Pramudita R. Prasetyanti, Ronald van Leersum, Janneke F. Linnekamp, Louis Vermeulen, Evelyn Fessler, Peter Nürnberg, Marek Franitza, Hans Clevers, Laura Rosa Mangiapane, Raju Kandimalla, Kate Cameron, Sander R. van Hooff, Giorgio Stassi, Kelly A S T Lee, Johan H de Jong, Joyce Y. Buikhuisen, Hans M. Rodermond, Xin Wang, Jan Paul Medema, Prashanthi Ramesh, Grehor G W Bochove, Linnekamp, Janneke F., Van Hooff, Sander R., Prasetyanti, Pramudita R., Kandimalla, Raju, Buikhuisen, Joyce Y., Fessler, Evelyn, Ramesh, Prashanthi, Lee, Kelly A.S.T., Bochove, Grehor G.W., De Jong, Johan H., Cameron, Kate, Van Leersum, Ronald, Rodermond, Hans M., Franitza, Marek, Nürnberg, Peter, Mangiapane, Laura R., Wang, Xin, Clevers, Han, Vermeulen, Loui, Stassi, Giorgio, Medema, Jan Paul, Hubrecht Institute for Developmental Biology and Stem Cell Research, CCA - Cancer biology and immunology, Graduate School, Center of Experimental and Molecular Medicine, Radiotherapy, Other departments, and AGEM - Amsterdam Gastroenterology Endocrinology Metabolism

Subjects
0301 basic medicine, Stromal cell, Colorectal cancer, Cell, Mice, Nude, Antineoplastic Agents, Apoptosis, Computational biology, Biology, Models, Biological, Article, 03 medical and health sciences, Mice, Structure-Activity Relationship, 0302 clinical medicine, In vivo, medicine, Biomarkers, Tumor, Tumor Cells, Cultured, Animals, Humans, Molecular Biology, Cell Proliferation, Regulation of gene expression, Dose-Response Relationship, Drug, Gene Expression Profiling, Mesenchymal stem cell, Microsatellite instability, Cell Differentiation, Neoplasms, Experimental, Cell Biology, medicine.disease, Gene expression profiling, Gene Expression Regulation, Neoplastic, Oxaliplatin, 030104 developmental biology, medicine.anatomical_structure, 030220 oncology & carcinogenesis, Fluorouracil, Drug Screening Assays, Antitumor, Colorectal Neoplasms
Abstract

Colorectal cancer (CRC) is a highly heterogeneous disease both from a molecular and clinical perspective. Several distinct molecular entities, such as microsatellite instability (MSI), have been defined that make up biologically distinct subgroups with their own clinical course. Recent data indicated that CRC can be best segregated into four groups called consensus molecular subtypes (CMS1-4), each of which has a unique biology and gene expression pattern. In order to develop improved, subtype-specific therapies and to gain insight into the molecular wiring and origin of these subtypes, reliable models are needed. This study was designed to determine the heterogeneity and identify the presence of CMSs in a large panel of CRC cell lines, primary cultures and patient-derived xenografts (PDX). We provide a repository encompassing this heterogeneity and moreover describe that a large part of the models can be robustly assigned to one of the four CMSs, independent of the stromal contribution. We subsequently validate our CMS stratification by functional analysis which for instance shows mesenchymal enrichment in CMS4 and metabolic dysregulation in CMS3. Finally, we observe a clear difference in sensitivity to chemotherapy-induced apoptosis, specifically between CMS2 and CMS4. This relates to the in vivo efficacy of chemotherapy, which delays outgrowth of CMS2, but not CMS4 xenografts. Combined our data indicate that molecular subtypes are faithfully modelled in CRC cell cultures and PDXs, representing tumour cell intrinsic and stable features. This repository provides researchers with a platform to study CRC using the existing heterogeneity.

Published
2018
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20. Think About the Environment: Cellular Reprogramming by the Extracellular Matrix

Author

David J. Huels, Jan Paul Medema, CCA - Cancer biology and immunology, Center of Experimental and Molecular Medicine, and Radiotherapy

Subjects
0301 basic medicine, Regeneration (biology), Cell, Signal transducing adaptor protein, Cell Biology, Biology, Epithelium, Cell biology, Extracellular matrix, 03 medical and health sciences, 030104 developmental biology, medicine.anatomical_structure, Genetics, medicine, Molecular Medicine, Stem cell, Reprogramming
Abstract

In this issue of Cell Stem Cell, Yui et al. (2018) show how tissue regeneration is driven by changes in the micro-environment. During intestinal regeneration, the epithelium is reprogrammed into a fetal state by an altered extracellular matrix (ECM), which is dependent on YAP/TAZ activation

Published
2018
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21. RNF43 truncations trap CK1 to drive niche-independent self-renewal in cancer

Author

Michiel Vermeulen, Madelon M. Maurice, Lars Ootes, Maureen Spit, Jeroen M. Bugter, Sylvia F. Boj, Tomasz Witold Radaszkiewicz, Jan Paul Medema, Alba Cristobal, Katerina Hanakova, Max van Osch, Eline Janssen, Vitezslav Bryja, Bon-Kyoung Koo, David Potesil, Zbynek Zdrahal, Kim E. Boonekamp, Rik G.H. Lindeboom, Ingrid Jordens, Nicola Fenderico, Center of Experimental and Molecular Medicine, Radiotherapy, and CCA - Cancer biology and immunology

Subjects
Ubiquitin-Protein Ligases, Endocytosis, General Biochemistry, Genetics and Molecular Biology, Article, 03 medical and health sciences, All institutes and research themes of the Radboud University Medical Center, 0302 clinical medicine, Downregulation and upregulation, Transcription (biology), Neoplasms, Humans, Molecular Biology, Wnt Signaling Pathway, beta Catenin, 030304 developmental biology, Cancer, 0303 health sciences, PORCN inhibitors, General Immunology and Microbiology, biology, cancer mutations, Casein Kinase I, Proteomics and Chromatin Biology, General Neuroscience, Wnt signaling pathway, Articles, Wnt signaling, 3. Good health, Ubiquitin ligase, Cell biology, human colon organoids, HEK293 Cells, RNF43, biology.protein, Phosphorylation, Casein kinase 1, Stem cell, Tumor Suppressor Protein p53, Nanomedicine Radboud Institute for Molecular Life Sciences [Radboudumc 19], 030217 neurology & neurosurgery, Signal Transduction
Abstract

Wnt/β‐catenin signaling is a primary pathway for stem cell maintenance during tissue renewal and a frequent target for mutations in cancer. Impaired Wnt receptor endocytosis due to loss of the ubiquitin ligase RNF43 gives rise to Wnt‐hypersensitive tumors that are susceptible to anti‐Wnt‐based therapy. Contrary to this paradigm, we identify a class of RNF43 truncating cancer mutations that induce β‐catenin‐mediated transcription, despite exhibiting retained Wnt receptor downregulation. These mutations interfere with a ubiquitin‐independent suppressor role of the RNF43 cytosolic tail that involves Casein kinase 1 (CK1) binding and phosphorylation. Mechanistically, truncated RNF43 variants trap CK1 at the plasma membrane, thereby preventing β‐catenin turnover and propelling ligand‐independent target gene transcription. Gene editing of human colon stem cells shows that RNF43 truncations cooperate with p53 loss to drive a niche‐independent program for self‐renewal and proliferation. Moreover, these RNF43 variants confer decreased sensitivity to anti‐Wnt‐based therapy. Our data demonstrate the relevance of studying patient‐derived mutations for understanding disease mechanisms and improved applications of precision medicine., C‐terminal shortening of RNF43 promotes Wnt/β‐catenin by decreasing destruction complex activity without effects on its ubiquitin ligase activity.

Published
2019

22. Stromal-derived interleukin 6 drives epithelial-to-mesenchymal transition and therapy resistance in esophageal adenocarcinoma

Author

Cynthia Waasdorp, Maarten C.C.M. Hulshof, Maarten F. Bijlsma, Gerrit K. J. Hooijer, Anne Steins, Aafke Creemers, Michelle Klein, Amber P. van der Zalm, Jan Paul Medema, Suzanne S. Gisbertz, Simone Hermsen, Rosa Rentenaar, Eva A. Ebbing, Cornelis J. A. Punt, Sybren L. Meijer, Kausilia K. Krishnadath, Hanneke W. M. van Laarhoven, Otto M. van Delden, Mark I. van Berge Henegouwen, Graduate School, CCA - Cancer biology and immunology, AGEM - Re-generation and cancer of the digestive system, APH - Methodology, APH - Quality of Care, Center of Experimental and Molecular Medicine, Pathology, Gastroenterology and Hepatology, Oncology, Surgery, Radiology and Nuclear Medicine, ACS - Amsterdam Cardiovascular Sciences, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, and Radiotherapy

Subjects
0301 basic medicine, Stromal cell, Epithelial-Mesenchymal Transition, Esophageal Neoplasms, ADAM12, Antineoplastic Agents, Adenocarcinoma, Radiation Tolerance, Tissue Culture Techniques, 03 medical and health sciences, Mice, 0302 clinical medicine, Cancer-Associated Fibroblasts, Cell Movement, Cell Line, Tumor, Organoid, medicine, Animals, Humans, Epithelial–mesenchymal transition, Interleukin 6, Multidisciplinary, biology, Dose-Response Relationship, Drug, business.industry, Interleukin-6, Cancer, Correction, Dose-Response Relationship, Radiation, medicine.disease, Xenograft Model Antitumor Assays, Disease Models, Animal, 030104 developmental biology, Cell culture, Drug Resistance, Neoplasm, 030220 oncology & carcinogenesis, Cancer cell, biology.protein, Cancer research, Stromal Cells, business
Abstract

Esophageal adenocarcinoma (EAC) has a dismal prognosis, and survival benefits of recent multimodality treatments remain small. Cancer-associated fibroblasts (CAFs) are known to contribute to poor outcome by conferring therapy resistance to various cancer types, but this has not been explored in EAC. Importantly, a targeted strategy to circumvent CAF-induced resistance has yet to be identified. By using EAC patient-derived CAFs, organoid cultures, and xenograft models we identified IL-6 as the stromal driver of therapy resistance in EAC. IL-6 activated epithelial-to-mesenchymal transition in cancer cells, which was accompanied by enhanced treatment resistance, migratory capacity, and clonogenicity. Inhibition of IL-6 restored drug sensitivity in patient-derived organoid cultures and cell lines. Analysis of patient gene expression profiles identified ADAM12 as a noninflammation-related serum-borne marker for IL-6-producing CAFs, and serum levels of this marker predicted unfavorable responses to neoadjuvant chemoradiation in EAC patients. These results demonstrate a stromal contribution to therapy resistance in EAC. This signaling can be targeted to resensitize EAC to therapy, and its activity can be measured using serum-borne markers.

Published
2019

23. Betulinic Acid Kills Colon Cancer Stem Cells

Author

Jan Paul Medema, Lisette Potze, Jan H. Kessler, Simone Di Franco, Giorgio Stassi, Potze, L., di Franco, S., Kessler, J., Stassi, G., Medema, J., Other departments, Center of Experimental and Molecular Medicine, and Radiotherapy

Subjects
0301 basic medicine, Programmed cell death, Colorectal cancer, Medicine (miscellaneous), Biology, 03 medical and health sciences, chemistry.chemical_compound, 0302 clinical medicine, Cancer stem cell, Betulinic acid, Cell Line, Tumor, medicine, Humans, Enzyme Inhibitors, Clonogenic assay, Cell Death, Stearoyl CoA-desaturase, Cancer, General Medicine, medicine.disease, Triterpenes, Clone Cells, Colon cancer, Tumor resistance, 030104 developmental biology, chemistry, Biochemistry, Cell culture, 030220 oncology & carcinogenesis, Cancer treatment, Colonic Neoplasms, Mutation, Cancer research, Neoplastic Stem Cells, Stem cell, Settore MED/46 - Scienze Tecniche Di Medicina Di Laboratorio, Pentacyclic Triterpenes, Stearoyl-CoA Desaturase
Abstract

Cancer stem cells (CSCs) are considered to be the origin of cancer and it is suggested that they are resistant to chemotherapy. Current therapies fail to eradicate CSCs and therefore selecting a resistant cell subset that is able to facilitate tumor recurrences. Betulinic acid (BetA) is a broad acting natural compound, shown to induce cell death via the inhibition of the stearoyl-CoA- desaturase (SCD- 1). This enzyme converts saturated fatty acids into unsaturated fatty acids and is over-expressed in tumor cells. Here we show that BetA induces rapid cell death in all colon CSCs tested and is able to affect the CSCs directly as shown, via the loss of clonogenic capacity. Similar results were observed with inhibition of SCD-1, suggesting that SCD-1 activity is indeed a vulnerable link in colon CSCs and can be considered an ideal target for therapy in colon cancer.

Published
2016
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24. Human colonic fibroblasts regulate stemness and chemotherapy resistance of colon cancer stem cells

Author

Jan Paul Medema, Selcuk Colak, Other departments, Center of Experimental and Molecular Medicine, and Radiotherapy

Subjects
0301 basic medicine, Colorectal cancer, Cellular differentiation, Green Fluorescent Proteins, Primary Cell Culture, bcl-X Protein, Antineoplastic Agents, Cell Communication, Keratin-20, Biology, Piperazines, Receptors, G-Protein-Coupled, Nitrophenols, Biological Factors, 03 medical and health sciences, Genes, Reporter, Cancer stem cell, Spheroids, Cellular, medicine, Humans, AC133 Antigen, Fibroblast, Clonogenic assay, Molecular Biology, Mucin-2, Sulfonamides, Cell Death, Extra View, Biphenyl Compounds, Cell Differentiation, Cell Biology, Fibroblasts, medicine.disease, Gene Expression Regulation, Neoplastic, 030104 developmental biology, medicine.anatomical_structure, Drug Resistance, Neoplasm, Apoptosis, Culture Media, Conditioned, Colonic Neoplasms, Cancer cell, Immunology, Neoplastic Stem Cells, Cancer research, Stem cell, Biomarkers, Signal Transduction, Developmental Biology
Abstract

There is increasing evidence that cancers are heterogeneous and contain a hierarchical organization consisting of cancer stem cells and their differentiated cell progeny. These cancer stem cells are at the core of the tumor as they represent the clonogenic cells within a tumor. Moreover, these cells are considered to contain selective therapy resistance, which suggests a pivotal role in therapy resistance and tumor relapse. Here we show that differentiated cells can re-acquire stemness through factors secreted from fibroblasts. This induced CSC state also coincides with re-acquisition of resistance to chemotherapy. Resistance induced in newly formed CSCs is mediated by the anti-apoptotic molecule BCLXL and inhibition of BCLXL with the BH3 mimetic ABT-737 sensitizes these cancer cells toward chemotherapy. These data point to an important interplay between tumor cells and their microenvironment in the regulation of stemness and therapy resistance.

Published
2016
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25. CFTR is a tumor suppressor gene in murine and human intestinal cancer

Author

Gerrit A. Meijer, Remond J.A. Fijneman, B L N Than, David A. Largaespada, Robert T. Cormier, A Niemczyk, A Schumann, Janneke F. Linnekamp, Louis Vermeulen, A Rod, Craig A. Hodges, Juan E. Abrahante, Ying Zhang, V Bruner, Michael G. O’Sullivan, Timothy K. Starr, Jan Paul Medema, T Luczak, E Van den Broek, Patricia M. Scott, Other departments, Center of Experimental and Molecular Medicine, Radiotherapy, Amsterdam Gastroenterology Endocrinology Metabolism, Medical oncology, Pathology, CCA - Cancer biology, Pediatric surgery, CCA - Cancer biology and immunology, Graduate School, CCA -Cancer Center Amsterdam, and AGEM - Amsterdam Gastroenterology Endocrinology Metabolism

Subjects
0301 basic medicine, Cancer Research, congenital, hereditary, and neonatal diseases and abnormalities, Tumor suppressor gene, Colon, Cystic Fibrosis Transmembrane Conductance Regulator, Cystic fibrosis, Disease-Free Survival, Article, Mice, 03 medical and health sciences, 0302 clinical medicine, Genetics, medicine, Animals, Humans, Genes, Tumor Suppressor, Molecular Biology, Tissue homeostasis, Regulation of gene expression, biology, Microarray analysis techniques, Wnt signaling pathway, respiratory system, medicine.disease, Cystic fibrosis transmembrane conductance regulator, digestive system diseases, respiratory tract diseases, Gene Expression Regulation, Neoplastic, 030104 developmental biology, 030220 oncology & carcinogenesis, Mutation, Immunology, Knockout mouse, biology.protein, Cancer research, Colorectal Neoplasms, Gene Deletion, Signal Transduction
Abstract

CFTR, the cystic fibrosis (CF) gene, encodes for the CFTR protein that plays an essential role in anion regulation and tissue homeostasis of various epithelia. In the gastrointestinal (GI) tract CFTR promotes chloride and bicarbonate secretion, playing an essential role in ion and acid-base homeostasis. Cftr has been identified as a candidate driver gene for colorectal cancer (CRC) in several Sleeping Beauty DNA transposon-based forward genetic screens in mice. Further, recent epidemiological and clinical studies indicate that CF patients are at high risk for developing tumors in the colon. To investigate the effects of CFTR dysregulation on GI cancer, we generated Apc(Min) mice that carried an intestinal-specific knockout of Cftr. Our results indicate that Cftr is a tumor suppressor gene in the intestinal tract as Cftr mutant mice developed significantly more tumors in the colon and the entire small intestine. In Apc(+/+) mice aged to ~1 year, Cftr deficiency alone caused the development of intestinal tumors in >60% of mice. Colon organoid formation was significantly increased in organoids created from Cftr mutant mice compared with wild-type controls, suggesting a potential role of Cftr in regulating the intestinal stem cell compartment. Microarray data from the Cftr-deficient colon and the small intestine identified dysregulated genes that belong to groups of immune response, ion channel, intestinal stem cell and other growth signaling regulators. These associated clusters of genes were confirmed by pathway analysis using Ingenuity Pathway Analysis and gene set enrichment analysis (GSEA). We also conducted RNA Seq analysis of tumors from Apc(+/+) Cftr knockout mice and identified sets of genes dysregulated in tumors including altered Wnt β-catenin target genes. Finally we analyzed expression of CFTR in early stage human CRC patients stratified by risk of recurrence and found that loss of expression of CFTR was significantly associated with poor disease-free survival.

Published
2016
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26. Abstract 5163: A colon cancer survivor-derived antibody recognizes a previously unidentified truncated, O-mannosylated 70kDa variant of E-cadherin

Author

Camille Bru, Hans van Eenennaam, Jan Paul Medema, Sabrina J. Merat, Arjen Q. Bakker, Victorine H. Roos, Frank G.J. Kallenberg, Pauline M. van Helden, Martino Bohne, Lina Bartels, Veronika Kattler, Paul J. Hensbergen, Koen Wagner, Tim Beaumont, Dorien van de Berg, Mark J. Kwakkenbos, Kelly Maijoor, Evelien Dekker, Hergen Spits, and Martijn Kedde

Subjects
Cancer Research, Oncology, biology, Cadherin, Colorectal cancer, Chemistry, medicine, biology.protein, Cancer research, Antibody, medicine.disease
Abstract

INTRODUCTION Colorectal cancer (CRC) associated with Lynch syndrome is characterized by an abundance of infiltrating lymphocytes. To study whether tumor-specific antibodies with therapeutic potential can be isolated from these patients, the B-cell repertoire from a patient with Lynch syndrome who recovered from a stage IV colon carcinoma was screened. Here we describe a novel human antibody, AT1636 that recognizes a previously unidentified O-mannosylated 70kDa form of E-cadherin. The intercellular interactions by E-cadherin on tumor cells have for long been recognized as protective in cancer metastasis, and deregulation of E-cadherin is a hallmark for epithelial-mesenchymal transition (EMT). METHODS AIMM's BCL6 and Bcl-xL immortalization method[1] was used to interrogate the human antibody repertoire against targets on colon cancer cells. From a carrier of a pathogenic gene variant in the MSH6 gene diagnosed with stage IV CRC and liver metastasis that had been treated with avastin, capecitabine and oxaliplatin, peripheral-blood memory B cells were obtained 9 years after last treatment. Antibodies-containing supernatant of cultured B-cells were screened for binding to 3 different CRC cell lines (DLD1, LS174T and COLO205) and absence of binding to fibroblast by flow cytometry. High-affinity variants of AT1636 (AT1636IYN) were sorted from the AID-expressing immortalized B-cells clone[2]. RESULTS Patient derived antibodies that demonstrated differential binding to CRC cells were further characterized. Targets recognized by such antibodies were identified using immunoprecipitation and mass-spectrometry. AT1636 binds to a previously unidentified single O-mannosylated 70kDa E-cadherin variant (ECV). Although the 70 kDa ECV is found in all cells that express full length E-cadherin, tumor-specific binding of AT1636 is dependent on the single O-mannosylation pattern in the antibody epitope on ECV. Using shRNA knock-down AT1636 binding was shown to depend on the transmembrane O-mannosyltransferase targeting cadherins 3 (TMTC3)[3]. In accordance, coexpression of TMTC3 and E-cadherin in tumor cells is predictive for AT1636 binding. In addition, we observed that (over)expression of ECV results in a strong de-adhesive, EMT-like phenotype. Although AT1636 by itself is not able to induce ADCC, the CD3-bispecific antibody (single-chain UCHT1) AT1636 format specifically killed CRC cell lines. CONCLUSION The AT1636 antibody retrieved from a patient with Lynch syndrome binds a previous unidentified cancer-specific O-mannosylated 70kDa form of E-cadherin. This variant might play a role in tumor-cell invasion and metastasis. More importantly, we provide a rationale to advance AT1636 based therapeutics for treatment of CRC. references 1) Kwakkenbos et al. Generation of stable monoclonal antibody-producing B cell receptor-positive human memory B cells by genetic programming. Nature Medicine 2010 2) Wagner et al. Bispecific antibody generated with sortase and click chemistry has broad antiinfluenza virus activity. PNAS 2014 3) Larsen et al. Discovery of an O-mannosylation pathway selectively serving cadherins and protocadherins. PNAS 2017 Citation Format: Martijn Kedde, Tim Beaumont, Sabrina J. Merat, Mark J. Kwakkenbos, Lina Bartels, Dorien van de Berg, Koen Wagner, Arjen Q. Bakker, Kelly Maijoor, Martino Böhne, Camille Bru, Veronika Kattler, Hans van Eenennaam, Victorine H. Roos, Frank G.J. Kallenberg, Jan Paul Medema, Paul J. Hensbergen, Pauline van Helden, Evelien Dekker, Hergen Spits. A colon cancer survivor-derived antibody recognizes a previously unidentified truncated, O-mannosylated 70kDa variant of E-cadherin [abstract]. In: Proceedings of the Annual Meeting of the American Association for Cancer Research 2020; 2020 Apr 27-28 and Jun 22-24. Philadelphia (PA): AACR; Cancer Res 2020;80(16 Suppl):Abstract nr 5163.

Published
2020
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27. Sequential cancer mutations in cultured human intestinal stem cells

Author

Gerald Schwank, Arjan Buijs, René M. Overmeer, Norman Sachs, Hugo J. Snippert, Cheryl Zimberlin, Ruben van Boxtel, Harry Begthel, Jeroen Korving, Richard H. van Jaarsveld, Marc van de Wetering, Hans Clevers, Jarno Drost, Meike Logtenberg, Jan Paul Medema, Geert J. P. L. Kops, Edwin Cuppen, G. Johan A. Offerhaus, Bas Ponsioen, Radiotherapy, Other departments, CCA -Cancer Center Amsterdam, Center of Experimental and Molecular Medicine, and Hubrecht Institute for Developmental Biology and Stem Cell Research

Subjects
HUMAN COLON, medicine.medical_treatment, medicine.disease_cause, SMAD4, Piperazines, COLORECTAL-CANCER, Mice, Epidermal growth factor, Intestinal Mucosa, Stem Cell Niche, Child, Non-U.S. Gov't, Smad4 Protein, Genetics, Multidisciplinary, Stem Cells, Research Support, Non-U.S. Gov't, Imidazoles, Wnt signaling pathway, Middle Aged, Intestines, Child, Preschool, Heterografts, Intercellular Signaling Peptides and Proteins, Female, KRAS, Stem cell, Colorectal Neoplasms, STRUCTURAL BASIS, Genes, APC, Xenotransplantation, EPITHELIUM, Mutagenesis (molecular biology technique), Biology, Research Support, Proto-Oncogene Proteins p21(ras), ORGANOIDS, ADENOMAS, REVEALS, medicine, Organoid, Journal Article, Animals, Humans, Neoplasm Invasiveness, Noggin, IN-VITRO EXPANSION, Aneuploidy, Genes, p53, TRANSFORMATION, Mutation, Mutagenesis, Site-Directed, Cancer research, CRISPR-Cas Systems, Neoplasm Transplantation
Abstract

Crypt stem cells represent the cells of origin for intestinal neoplasia. Both mouse and human intestinal stem cells can be cultured in medium containing the stem-cell-niche factors WNT, R-spondin, epidermal growth factor (EGF) and noggin over long time periods as epithelial organoids that remain genetically and phenotypically stable. Here we utilize CRISPR/Cas9 technology for targeted gene modification of four of the most commonly mutated colorectal cancer genes (APC, P53 (also known as TP53), KRAS and SMAD4) in cultured human intestinal stem cells. Mutant organoids can be selected by removing individual growth factors from the culture medium. Quadruple mutants grow independently of all stem-cell-niche factors and tolerate the presence of the P53 stabilizer nutlin-3. Upon xenotransplantation into mice, quadruple mutants grow as tumours with features of invasive carcinoma. Finally, combined loss of APC and P53 is sufficient for the appearance of extensive aneuploidy, a hallmark of tumour progression.

Published
2015
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28. Effective Inhibition of Bone Morphogenetic Protein Function by Highly Specific Llama-Derived Antibodies

Author

Jan Paul Medema, Koen Wagner, C. Theo Verrips, Mohamed El Khattabi, Cheryl Zimberlin, Edward Dolk, Hergen Spits, Kausilia K. Krishnadath, Silvia Calpe, Lucy Rutten, Gastroenterology and Hepatology, Radiotherapy, Cancer Center Amsterdam, Center of Experimental and Molecular Medicine, Amsterdam institute for Infection and Immunity, Amsterdam Gastroenterology Endocrinology Metabolism, and Cell Biology and Histology

Subjects
Models, Molecular, Cancer Research, animal structures, Blotting, Western, Antibody Affinity, Bone Morphogenetic Protein 2, Bone Morphogenetic Protein 4, Plasma protein binding, Biology, Bone morphogenetic protein, Bone morphogenetic protein 2, Antibodies, Cell Line, Mice, Antibody Specificity, Neoplasms, Epitope binning, Animals, Humans, Tissue homeostasis, Molecular biology, Protein Structure, Tertiary, BMPR2, Cell biology, Oncology, Bone morphogenetic protein 4, Docking (molecular), Bone Morphogenetic Proteins, embryonic structures, Camelids, New World, HT29 Cells, Protein Binding
Abstract

Bone morphogenetic proteins (BMP) have important but distinct roles in tissue homeostasis and disease, including carcinogenesis and tumor progression. A large number of BMP inhibitors are available to study BMP function; however, as most of these antagonists are promiscuous, evaluating specific effects of individual BMPs is not feasible. Because the oncogenic role of the different BMPs varies for each neoplasm, highly selective BMP inhibitors are required. Here, we describe the generation of three types of llama-derived heavy chain variable domains (VHH) that selectively bind to either BMP4, to BMP2 and 4, or to BMP2, 4, 5, and 6. These generated VHHs have high affinity to their targets and are able to inhibit BMP signaling. Epitope binning and docking modeling have shed light into the basis for their BMP specificity. As opposed to the wide structural reach of natural inhibitors, these small molecules target the grooves and pockets of BMPs involved in receptor binding. In organoid experiments, specific inhibition of BMP4 does not affect the activation of normal stem cells. Furthermore, in vitro inhibition of cancer-derived BMP4 noncanonical signals results in an increase of chemosensitivity in a colorectal cancer cell line. Therefore, because of their high specificity and low off-target effects, these VHHs could represent a therapeutic alternative for BMP4+ malignancies. Mol Cancer Ther; 14(11); 2527–40. ©2015 AACR.

Published
2015
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29. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015

Author

Lorenzo Galluzzi, Thomas Rudel, Hans-Uwe Simon, Vishva M. Dixit, Erwin F. Wagner, Marie-Lise Gougeon, Andreas Linkermann, J M Bravo-San Pedro, Rosario Rizzuto, Cecília M. P. Rodrigues, Gian Maria Fimia, Hidenori Ichijo, Mathieu J.M. Bertrand, Kodi S. Ravichandran, Francis Ka-Ming Chan, Stephen W.G. Tait, Jochen H. M. Prehn, Richard A. Lockshin, Valina L. Dawson, Andreas Villunger, Sharad Kumar, Emily H. Cheng, Carlos López-Otín, Theocharis Panaretakis, Lucia Altucci, Gabriel A. Rabinovich, Michelangelo Campanella, Peter Vandenabeele, Marcus E. Peter, Francesco Cecconi, Noboru Mizushima, Ilio Vitale, Frank Madeo, Mikhail V. Blagosklonny, Zahra Zakeri, Stuart A. Aaronson, Gabriel Núñez, Eric H. Baehrecke, Nektarios Tavernarakis, Gyorgy Szabadkai, Eleonora Candi, Brent R. Stockwell, Dale E. Bredesen, Seamus J. Martin, Thomas Kaufmann, Sonia Melino, Dieter Adam, John M. Abrams, Katiuscia Bianchi, Yufang Shi, Emad S. Alnemri, Klas Blomgren, Pascal Meier, Catherine Brenner, Michael O. Hengartner, Philipp J. Jost, J M Hardwick, Eileen White, T Vanden Berghe, N. Di Daniele, Nicolas G. Bazan, H. L. Tang, Mauro Piacentini, V De Laurenzi, Beth Levine, Margherita Annicchiarico-Petruzzelli, Josef M. Penninger, Walter Malorni, Ted M. Dawson, Carmen Garrido, David W. Andrews, Douglas R. Green, György Hajnóczky, Jerry E. Chipuk, Wafik S. El-Deiry, Christoph Borner, Stuart A. Lipton, John A. Cidlowski, Klaus-Michael Debatin, Junying Yuan, Jan Paul Medema, Bertrand Joseph, Aaron Ciechanover, Ute M. Moll, Hinrich Gronemeyer, Paolo Pinton, Gerry Melino, Daniel J. Klionsky, Simone Fulda, John J. Lemasters, Cristina Muñoz-Pinedo, Hamsa Puthalakath, Navdeep S. Chandel, R De Maria, Jean-Christophe Marine, Richard A. Flavell, Brian David Dynlacht, W. G. Wood, Henning Walczak, David C. Rubinsztein, Guido Kroemer, Oliver Kepp, Richard A. Knight, Andrew Oberst, Enrico Lugli, J-C Martinou, Boris Zhivotovsky, Yoshihide Tsujimoto, Galluzi, L, Bravo-San, Pedro JM, Vitale, I, Aaaronson, SA, Kumar, S, Kroemer, Guido, Galluzzi, L, Bravo San Pedro, J. M, Aaronson, S. A, Abrams, J. M, Adam, D, Alnemri, E. S, Altucci, L, Andrews, D, Annicchiarico Petruzzelli, M, Baehrecke, E. H, Bazan, N. G, Bertrand, M. J, Bianchi, K, Blagosklonny, M. V, Blomgren, K, Borner, C, Bredesen, D. E, Brenner, C, Campanella, M, Candi, E, Cecconi, F, Chan, F. K, Chandel, N. S, Cheng, E. H, Chipuk, J. E, Cidlowski, J. A, Ciechanover, A, Dawson, T. M, Dawson, V. L, De Laurenzi, V, De Maria, R, Debatin, K. M, Di Daniele, N, Dixit, V. M, Dynlacht, B. D, El Deiry, W. S, Fimia, Gian Maria, Flavell, R. A, Fulda, S, Garrido, C, Gougeon, M. L, Green, D. R, Gronemeyer, H, Hajnoczky, G, Hardwick, J. M, Hengartner, M. O, Ichijo, H, Joseph, B, Jost, P. J, Kaufmann, T, Kepp, O, Klionsky, D. J, Knight, R. A, Lemasters, J. J, Levine, B, Linkermann, A, Lipton, S. A, Lockshin, R. A, López Otín, C, Lugli, E, Madeo, F, Malorni, W, Marine, J. C, Martin, S. J, Martinou, J. C, Medema, J. P, Meier, P, Melino, S, Mizushima, N, Moll, U, Muñoz Pinedo, C, Nuñez, G, Oberst, A, Panaretakis, T, Penninger, J. M, Peter, M. E, Piacentini, M, Pinton, P, Prehn, J. H, Puthalakath, H, Rabinovich, G. A, Ravichandran, K. S, Rizzuto, R, Rodrigues, C. M, Rubinsztein, D. C, Rudel, T, Shi, Y, Simon, H. U, Stockwell, B. R, Szabadkai, G, Tait, S. W, Tang, H. L, Tavernarakis, N, Tsujimoto, Y, Vanden Berghe, T, Vandenabeele, P, Villunger, A, Wagner, E. F, Walczak, H, White, E, Wood, W. G, Yuan, J, Zakeri, Z, Zhivotovsky, B, Melino, G, Kroemer, G., Bravo San Pedro, Jm, Aaronson, Sa, Abrams, Jm, Alnemri, E, Altucci, Lucia, Baehrecke, Eh, Bazan, Ng, Bertrand, Mj, Blagosklonny, Mv, Bredesen, De, Chan, Fk, Chandel, N, Cheng, Eh, Chipuk, Je, Cidlowski, Ja, Dawson, Tm, Dawson, Vl, Debatin, Km, Dixit, Vm, Dynlacht, Bd, El Deiry, W, Fimia, Gm, Flavell, Ra, Gougeon, Ml, Green, Dr, Hardwick, Jm, Hengartner, Mo, Jost, Pj, Klionsky, Dj, Knight, Ra, Lemasters, Jj, Lipton, Sa, Lockshin, Ra, Marine, Jc, Martin, Sj, Martinou, Jc, Medema, Jp, Penninger, Jm, Peter, Me, Prehn, Jh, Rabinovich, Ga, Ravichandran, K, Rodrigues, Cm, Rubinsztein, Dc, Simon, Hu, Stockwell, Br, Tait, Sw, Tang, Hl, Wagner, Ef, and Wood, Wg

Subjects
Biochemical Manifestations of Cell Death, ISCHEMIA-REPERFUSION INJURY, Apoptosis, Review, Transduction (genetics), 0302 clinical medicine, CASPASE INHIBITION SWITCHES, Animals, Humans, Terminology as Topic, Signal Transduction, 610 Medicine & health, Caspase, TUMOR-NECROSIS-FACTOR, 0303 health sciences, Settore BIO/17, biology, Settore BIO/11, Neurodegeneration, Settore BIO/13, APOPTOSIS, 3. Good health, Medicina Básica, cell death, 030220 oncology & carcinogenesis, Morphologic Aspects of Cell Death, Signal transduction, DOMAIN-LIKE PROTEIN, Intracellular, Human, Necroptosi, CYTOCHROME-C RELEASE, OUTER-MEMBRANE PERMEABILIZATION, Programmed cell death, CIENCIAS MÉDICAS Y DE LA SALUD, Settore BIO/06, Inmunología, CELL DEATH, NO, Q-VD-OPH, 03 medical and health sciences, Settore MED/04 - PATOLOGIA GENERALE, ddc:570, APOPTOSIS-INDUCING FACTOR, MIXED LINEAGE KINASE, medicine, Molecular Biology, Cell Biology, Settore BIO/10, 030304 developmental biology, Animal, Cell growth, Apoptosi, Biology and Life Sciences, medicine.disease, MITOCHONDRIAL PERMEABILITY TRANSITION, Immunology, biology.protein, Neuroscience
Abstract

Cells exposed to extreme physicochemical or mechanical stimuli die in an uncontrollable manner, as a result of their immediate structural breakdown. Such an unavoidable variant of cellular demise is generally referred to as ?accidental cell death' (ACD). In most settings, however, cell death is initiated by a genetically encoded apparatus, correlating with the fact that its course can be altered by pharmacologic or genetic interventions. "Regulated cell death" (RCD) can occur as part of physiologic programs or can be activated once adaptive responses to perturbations of the extracellular or intracellular microenvironment fail. The biochemical phenomena that accompany RCD may be harnessed to classify it into a few subtypes, which often (but not always) exhibit stereotyped morphologic features. Nonetheless, efficiently inhibiting the processes that are commonly thought to cause RCD, such as the activation of executioner caspases in the course of apoptosis, does not exert true cytoprotective effects in the mammalian system, but simply alters the kinetics of cellular demise as it shifts its morphologic and biochemical correlates. Conversely, bona fide cytoprotection can be achieved by inhibiting the transduction of lethal signals in the early phases of the process, when adaptive responses are still operational. Thus, the mechanisms that truly execute RCD may be less understood, less inhibitable and perhaps more homogeneous than previously thought. Here, the Nomenclature Committee on Cell Death formulates a set of recommendations to help scientists and researchers to discriminate between essential and accessory aspects of cell death Fil: Rabinovich, Gabriel Adrian. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Biología y Medicina Experimental (i); Argentina Fil: Nomenclature Committee on Cell Death. Equipe 11 Apoptose, Cancer et Immunité. Centre de Recherche des Cordeliers; Francia

Published
2015
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30. HDAC1 and HDAC2 collectively regulate intestinal stem cell homeostasis

Author

Gijs R. van den Brink, Jan Paul Medema, Cesare Lancini, Rachel Sno, Chelsea M. McLean, Hanneke Vlaming, Jan-Hermen Dannenberg, Sanne L. Rosekrans, Cheryl Zimberlin, Michael Bots, Radiotherapy, Tytgat Institute for Liver and Intestinal Research, AII - Amsterdam institute for Infection and Immunity, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Gastroenterology and Hepatology, Laboratory for General Clinical Chemistry, CCA -Cancer Center Amsterdam, and Center of Experimental and Molecular Medicine

Subjects
Male, Intestinal stem cell homeostasis, medicine.drug_class, Pyridines, Blotting, Western, Fluorescent Antibody Technique, Histone Deacetylase 2, Histone Deacetylase 1, Mice, Transgenic, Biology, Stem cell marker, Real-Time Polymerase Chain Reaction, Biochemistry, Immunoenzyme Techniques, Mice, Organ Culture Techniques, Genetics, medicine, Organoid, Animals, Homeostasis, Humans, RNA, Messenger, Molecular Biology, Cells, Cultured, Mice, Knockout, Histone deacetylase 2, Reverse Transcriptase Polymerase Chain Reaction, Stem Cells, Histone deacetylase inhibitor, Cell Differentiation, Flow Cytometry, HDAC1, Cell biology, Histone Deacetylase Inhibitors, Intestines, Mice, Inbred C57BL, Immunology, Benzamides, Female, Histone deacetylase, Stem cell, Biomarkers, Biotechnology
Abstract

Histone deacetylases (HDACs) are posttranslational modifiers that deacetylate proteins. Despite their crucial role in numerous biological processes, the use of broad-range HDAC inhibitors (HDACi), has shown clinical efficacy. However, undesired side effects highlight the necessity to better understand the biology of different HDACs and target the relevant HDACs. Using a novel mouse model, in which HDAC1 and HDAC2 can be simultaneously deleted in the intestine of adult mice, we show that the simultaneous deletion of HDAC1 and HDAC2 leads to a rapid loss of intestinal homeostasis. Importantly, this deletion cannot be sustained, and 8 days after initial ablation, stem cells that have escaped HDAC1 or HDAC2 deletion swiftly repopulate the intestinal lining. In vitro ablation of HDAC1 and HDAC2 using intestinal organoid cultures resulted in a down-regulation of multiple intestinal stem cell markers and functional loss of clonogenic capacity. Importantly, treatment of wild-type organoids with class I-specific HDACi MS-275 also induced a similar loss of stemness, providing a possible rationale for the gastrointestinal side effects often observed in HDACi-treated patients. In conclusion, these data show that HDAC1 and HDAC2 have a redundant function and are essential to maintain intestinal homeostasis.

Published
2015
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31. Lipid Droplets: A New Player in Colorectal Cancer Stem Cells Unveiled by Spectroscopic Imaging

Author

Simone Di Franco, Rosanna La Rocca, Enzo Di Fabrizio, Lisette Potze, Jan Paul Medema, Ennio Carbone, Francesco De Angelis, Antonina Benfante, Andrea Falqui, Luca Tirinato, Roberto Marotta, Matilde Todaro, Mario Malerba, Carlo Liberale, Giorgio Stassi, Vijayakumar P. Rajamanickam, Patrizio Candeloro, Roberta Ruffilli, Other departments, CCA -Cancer Center Amsterdam, Center of Experimental and Molecular Medicine, Radiotherapy, Tirinato, L., Liberale, C., Di Franco, S., P, Candeloro, Benfante, A., La Rocca, R., Potze, L., Marotta, R., Ruffilli, R., Rajamanickam, V. P., Malerba, M., De Angelis, F., Falqui, A., Todaro, M., Medema, J. P., Stassi, G., Di Fabrizio, E., Carbone, E, Tirinato, L, Liberale, C, Di Franco, S, Candeloro, P, Benfante, A, La Rocca, R, Potze ,L, Marotta, R, Ruffilli, R, Rajamanickam, VP, Malerba, M, De Angelis, F, Falqui, A, Todaro, M, Medema, JP, Stassi, G, and Di Fabrizio, E

Subjects
Colorectal cancer, Xenotransplantation, medicine.medical_treatment, Biology, Spectrum Analysis, Raman, Mice, Cancer stem cell, Lipid droplet, Organelle, Biomarkers, Tumor, medicine, Animals, Humans, lipid droplets, colon cancer, stem cells, Wnt Signaling Pathway, Settore MED/04 - Patologia Generale, Wnt signaling pathway, Cancer, Lipid Droplets, Cell Biology, medicine.disease, Cell biology, Neoplastic Stem Cells, Molecular Medicine, Stem cell, Colorectal Neoplasms, Developmental Biology
Abstract

The cancer stem cell (CSC) model is describing tumors as a hierarchical organized system and CSCs are suggested to be responsible for cancer recurrence after therapy. The identification of specific markers of CSCs is therefore of paramount importance. Here, we show that high levels of lipid droplets (LDs) are a distinctive mark of CSCs in colorectal (CR) cancer. This increased lipid content was clearly revealed by label-free Raman spectroscopy and it directly correlates with well-accepted CR-CSC markers as CD133 and Wnt pathway activity. By xenotransplantation experiments, we have finally demonstrated that CR-CSCs overexpressing LDs retain most tumorigenic potential. A relevant conceptual advance in this work is the demonstration that a cellular organelle, the LD, is a signature of CSCs, in addition to molecular markers. A further functional characterization of LDs could lead soon to design new target therapies against CR-CSCs. Stem Cells 2015;33:35–44

Published
2014
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32. Guidelines for the use and interpretation of assays for monitoring autophagy (3rd edition)

Author

Daniel J. Klionsky, Kotb Abdelmohsen, Akihisa Abe, Md Joynal Abedin, Hagai Abeliovich, Abraham Acevedo Arozena, Hiroaki Adachi, Christopher M. Adams, Peter D. Adams, Khosrow Adeli, Peter J. Adhihetty, Sharon G. Adler, Galila Agam, Rajesh Agarwal, Manish K. Aghi, Maria Agnello, Patrizia Agostinis, Patricia V. Aguilar, Julio Aguirre Ghiso, Edoardo M. Airoldi, Slimane Ait Si Ali, Takahiko Akematsu, Emmanuel T. Akporiaye, Mohamed Al Rubeai, Guillermo M. Albaiceta, Chris Albanese, Diego Albani, Matthew L. Albert, Jesus Aldudo, Hana Algül, Mehrdad Alirezaei, Iraide Alloza, Alexandru Almasan, Maylin Almonte Beceril, Emad S. Alnemri, Covadonga Alonso, Nihal Altan Bonnet, Dario C. Altieri, Silvia Alvarez, Lydia Alvarez Erviti, Sandro Alves, Giuseppina Amadoro, Atsuo Amano, Consuelo Amantini, Santiago Ambrosio, Ivano Amelio, Amal O. Amer, Mohamed Amessou, Angelika Amon, Zhenyi An, Frank A. Anania, Stig U. Andersen, Usha P. Andley, Catherine K. Andreadi, Nathalie Andrieu Abadie, Alberto Anel, David K. Ann, Shailendra Anoopkumar Dukie, Manuela Antonioli, Hiroshi Aoki, Nadezda Apostolova, Saveria Aquila, Katia Aquilano, Koichi Araki, Eli Arama, Agustin Aranda, Jun Araya, Alexandre Arcaro, Esperanza Arias, Hirokazu Arimoto, Aileen R. Ariosa, Jane L. Armstrong, Thierry Arnould, Ivica Arsov, Katsuhiko Asanuma, Valerie Askanas, Eric Asselin, Ryuichiro Atarashi, Sally S. Atherton, Julie D. Atkin, Laura D. Attardi, Patrick Auberger, Georg Auburger, Laure Aurelian, Riccardo Autelli, Laura Avagliano, Maria Laura Avantaggiati, Limor Avrahami, Suresh Awale, Neelam Azad, Tiziana Bachetti, Jonathan M. Backer, Dong Hun Bae, Jae sung Bae, Ok Nam Bae, Soo Han Bae, Eric H. Baehrecke, Seung Hoon Baek, Stephen Baghdiguian, Agnieszka Bagniewska Zadworna, Hua Bai, Jie Bai, Xue Yuan Bai, Yannick Bailly, Kithiganahalli Narayanaswamy Balaji, Walter Balduini, Andrea Ballabio, Rena Balzan, Rajkumar Banerjee, Gábor Bánhegyi, Haijun Bao, Benoit Barbeau, Maria D. Barrachina, Esther Barreiro, Bonnie Bartel, Alberto Bartolomé, Diane C. Bassham, Maria Teresa Bassi, Robert C. Bast Jr, Alakananda Basu, Maria Teresa Batista, Henri Batoko, Maurizio Battino, Kyle Bauckman, Bradley L. Baumgarner, K. Ulrich Bayer, Rupert Beale, Jean François Beaulieu, George R. Beck Jr, Christoph Becker, J. David Beckham, Pierre André Bédard, Patrick J. Bednarski, Thomas J. Begley, Christian Behl, Christian Behrends, Georg MN Behrens, Kevin E. Behrns, Eloy Bejarano, Amine Belaid, Francesca Belleudi, Giovanni Bénard, Guy Berchem, Daniele Bergamaschi, Matteo Bergami, Ben Berkhout, Laura Berliocchi, Amélie Bernard, Monique Bernard, Francesca Bernassola, Anne Bertolotti, Amanda S. Bess, Sébastien Besteiro, Saverio Bettuzzi, Savita Bhalla, Shalmoli Bhattacharyya, Sujit K. Bhutia, Caroline Biagosch, Michele Wolfe Bianchi, Martine Biard Piechaczyk, Viktor Billes, Claudia Bincoletto, Baris Bingol, Sara W. Bird, Marc Bitoun, Ivana Bjedov, Craig Blackstone, Lionel Blanc, Guillermo A. Blanco, Heidi Kiil Blomhoff, Emilio Boada Romero, Stefan Böckler, Marianne Boes, Kathleen Boesze Battaglia, Lawrence H. Boise, Alessandra Bolino, Andrea Boman, Paolo Bonaldo, Matteo Bordi, Jürgen Bosch, Luis M. Botana, Joelle Botti, German Bou, Marina Bouché, Marion Bouchecareilh, Marie Josée Boucher, Michael E. Boulton, Sebastien G. Bouret, Patricia Boya, Michaël Boyer Guittaut, Peter V. Bozhkov, Nathan Brady, Vania MM Braga, Claudio Brancolini, Gerhard H. Braus, José M. Bravo San Pedro, Lisa A. Brennan, Emery H. Bresnick, Patrick Brest, Dave Bridges, MarieAgnès Bringer, Marisa Brini, Glauber C. Brito, Bertha Brodin, Paul S. Brookes, Eric J. Brown, Karen Brown, Hal E. Broxmeyer, Alain Bruhat, Patricia Chakur Brum, John H. Brumell, Nicola Brunetti Pierri, Robert J. Bryson Richardson, Shilpa Buch, Alastair M. Buchan, Hikmet Budak, Dmitry V. Bulavin, Scott J. Bultman, Geert Bultynck, Vladimir Bumbasirevic, Yan Burelle, Robert E. Burke, Margit Burmeister, Peter Bütikofer, Laura Caberlotto, Ken Cadwell, Monika Cahova, Dongsheng Cai, Jingjing Cai, Qian Cai, Sara Calatayud, Nadine Camougrand, Michelangelo Campanella, Grant R. Campbell, Matthew Campbell, Silvia Campello, Robin Candau, Isabella Caniggia, Lavinia Cantoni, Lizhi Cao, Allan B. Caplan, Michele Caraglia, Claudio Cardinali, Sandra Morais Cardoso, Jennifer S. Carew, Laura A. Carleton, Cathleen R. Carlin, Silvia Carloni, Sven R. Carlsson, Didac Carmona Gutierrez, Leticia AM Carneiro, Oliana Carnevali, Serena Carra, Alice Carrier, Bernadette Carroll, Caty Casas, Josefina Casas, Giuliana Cassinelli, Perrine Castets, Susana Castro Obregon, Gabriella Cavallini, Isabella Ceccherini, Francesco Cecconi, Arthur I. Cederbaum, Valentín Ceña, Simone Cenci, Claudia Cerella, Davide Cervia, CETRULLO, SILVIA, Hassan Chaachouay, Han Jung Chae, Andrei S. Chagin, Chee Yin Chai, Gopal Chakrabarti, Georgios Chamilos, Edmond YW Chan, Matthew TV Chan, Dhyan Chandra, Pallavi Chandra, Chih Peng Chang, Raymond Chuen Chung Chang, Ta Yuan Chang, John C. Chatham, Saurabh Chatterjee, Santosh Chauhan, Yongsheng Che, Michael E. Cheetham, Rajkumar Cheluvappa, Chun Jung Chen, Gang Chen, Guang Chao Chen, Guoqiang Chen, Hongzhuan Chen, Jeff W. Chen, Jian Kang Chen, Min Chen, Mingzhou Chen, Peiwen Chen, Qi Chen, Quan Chen, Shang Der Chen, Si Chen, Steve S. L. Chen, Wei Chen, Wei Jung Chen, Wen Qiang Chen, Wenli Chen, Xiangmei Chen, Yau Hung Chen, Ye Guang Chen, Yin Chen, Yingyu Chen, Yongshun Chen, Yu Jen Chen, Yue Qin Chen, Yujie Chen, Zhen Chen, Zhong Chen, Alan Cheng, Christopher HK Cheng, Hua Cheng, Heesun Cheong, Sara Cherry, Jason Chesney, Chun Hei Antonio Cheung, Eric Chevet, Hsiang Cheng Chi, Sung Gil Chi, Fulvio Chiacchiera, Hui Ling Chiang, Roberto Chiarelli, Mario Chiariello, Marcello Chieppa, Lih Shen Chin, Mario Chiong, Gigi NC Chiu, Dong Hyung Cho, Ssang Goo Cho, William C. Cho, Yong Yeon Cho, Young Seok Cho, Augustine MK Choi, Eui Ju Choi, Eun Kyoung Choi, Jayoung Choi, Mary E. Choi, Seung Il Choi, Tsui Fen Chou, Salem Chouaib, Divaker Choubey, Vinay Choubey, Kuan Chih Chow, Kamal Chowdhury, Charleen T. Chu, Tsung Hsien Chuang, Taehoon Chun, Hyewon Chung, Taijoon Chung, Yuen Li Chung, Yong Joon Chwae, Valentina Cianfanelli, Roberto Ciarcia, Iwona A. Ciechomska, Maria Rosa Ciriolo, Mara Cirone, Sofie Claerhout, Michael J. Clague, Joan Clària, Peter GH Clarke, Robert Clarke, Emilio Clementi, Cédric Cleyrat, Miriam Cnop, Eliana M. Coccia, Tiziana Cocco, Patrice Codogno, Jörn Coers, Ezra EW Cohen, David Colecchia, Luisa Coletto, Núria S. Coll, Emma Colucci Guyon, Sergio Comincini, Maria Condello, Katherine L. Cook, Graham H. Coombs, Cynthia D. Cooper, J. Mark Cooper, Isabelle Coppens, Maria Tiziana Corasaniti, Marco Corazzari, Ramon Corbalan, Elisabeth Corcelle Termeau, Mario D. Cordero, Cristina Corral Ramos, Olga Corti, Andrea Cossarizza, Paola Costelli, Safia Costes, Susan L. Cotman, Ana Coto Montes, Sandra Cottet, Eduardo Couve, Lori R. Covey, L. Ashley Cowart, Jeffery S. Cox, Fraser P. Coxon, Carolyn B. Coyne, Mark S. Cragg, Rolf J. Craven, Tiziana Crepaldi, Jose L. Crespo, Alfredo Criollo, Valeria Crippa, Maria Teresa Cruz, Ana Maria Cuervo, Jose M. Cuezva, Taixing Cui, Pedro R. Cutillas, Mark J. Czaja, Maria F. Czyzyk Krzeska, Ruben K. Dagda, Uta Dahmen, Chunsun Dai, Wenjie Dai, Yun Dai, Kevin N. Dalby, Luisa Dalla Valle, Guillaume Dalmasso, Marcello D'Amelio, Markus Damme, Arlette Darfeuille Michaud, Catherine Dargemont, Victor M. Darley Usmar, Srinivasan Dasarathy, Biplab Dasgupta, Srikanta Dash, Crispin R. Dass, Hazel Marie Davey, Lester M. Davids, David Dávila, Roger J. Davis, Ted M. Dawson, Valina L. Dawson, Paula Daza, Jackie de Belleroche, Paul de Figueiredo, Regina Celia Bressan Queiroz de Figueiredo, José de la Fuente, Luisa De Martino, Antonella De Matteis, Guido RY De Meyer, Angelo De Milito, Mauro De Santi, Wanderley de Souza, Vincenzo De Tata, Daniela De Zio, Jayanta Debnath, Reinhard Dechant, Jean Paul Decuypere, Shane Deegan, Benjamin Dehay, Barbara Del Bello, Dominic P. Del Re, Régis Delage Mourroux, Lea MD Delbridge, Louise Deldicque, Elizabeth Delorme Axford, Yizhen Deng, Joern Dengjel, Melanie Denizot, Paul Dent, Channing J. Der, Vojo Deretic, Benoît Derrien, Eric Deutsch, Timothy P. Devarenne, Rodney J. Devenish, Sabrina Di Bartolomeo, Nicola Di Daniele, Fabio Di Domenico, Alessia Di Nardo, Simone Di Paola, Antonio Di Pietro, Livia Di Renzo, Aaron DiAntonio, Guillermo Díaz Araya, Ines Díaz Laviada, Maria T. Diaz Meco, Javier Diaz Nido, Chad A. Dickey, Robert C. Dickson, Marc Diederich, Paul Digard, Ivan Dikic, Savithrama P. Dinesh Kumar, Chan Ding, Wen Xing Ding, Zufeng Ding, Luciana Dini, Jörg HW Distler, Abhinav Diwan, Mojgan Djavaheri Mergny, Kostyantyn Dmytruk, Renwick CJ Dobson, Volker Doetsch, Karol Dokladny, Svetlana Dokudovskaya, Massimo Donadelli, X. Charlie Dong, Xiaonan Dong, Zheng Dong, Terrence M. Donohue Jr, Kelly S. Doran, Gabriella D'Orazi, Gerald W. Dorn II, Victor Dosenko, Sami Dridi, Liat Drucker, Jie Du, Li Lin Du, Lihuan Du, André du Toit, Priyamvada Dua, Lei Duan, Pu Duann, Vikash Kumar Dubey, Michael R. Duchen, Michel A. Duchosal, Helene Duez, Isabelle Dugail, Verónica I. Dumit, Mara C. Duncan, Elaine A. Dunlop, William A. Dunn Jr, Nicolas Dupont, Luc Dupuis, Raúl V. Durán, Thomas M. Durcan, Stéphane Duvezin Caubet, Umamaheswar Duvvuri, Vinay Eapen, Darius Ebrahimi Fakhari, Arnaud Echard, Leopold Eckhart, Charles L. Edelstein, Aimee L. Edinger, Ludwig Eichinger, Tobias Eisenberg, Avital Eisenberg Lerner, N. Tony Eissa, Wafik S. El Deiry, Victoria El Khoury, Zvulun Elazar, Hagit Eldar Finkelman, Chris JH Elliott, Enzo Emanuele, Urban Emmenegger, Nikolai Engedal, Anna Mart Engelbrecht, Simone Engelender, Jorrit M. Enserink, Ralf Erdmann, Jekaterina Erenpreisa, Rajaraman Eri, Jason L. Eriksen, Andreja Erman, Ricardo Escalante, Eeva Liisa Eskelinen, Lucile Espert, Lorena Esteban Martínez, Thomas J. Evans, Mario Fabri, Gemma Fabrias, Cinzia Fabrizi, Antonio Facchiano, Nils J. Færgeman, Alberto Faggioni, W. Douglas Fairlie, Chunhai Fan, Daping Fan, Jie Fan, Shengyun Fang, Manolis Fanto, Alessandro Fanzani, Thomas Farkas, Mathias Faure, Francois B. Favier, Howard Fearnhead, Massimo Federici, Erkang Fei, Tania C. Felizardo, Hua Feng, Yibin Feng, Yuchen Feng, Thomas A. Ferguson, Álvaro F. Fernández, Maite G. Fernandez Barrena, Jose C. Fernandez Checa, Arsenio Fernández López, Martin E. Fernandez Zapico, Olivier Feron, Elisabetta Ferraro, Carmen Veríssima Ferreira Halder, Laszlo Fesus, Ralph Feuer, Fabienne C. Fiesel, Eduardo C. Filippi Chiela, Giuseppe Filomeni, Gian Maria Fimia, John H. Fingert, Steven Finkbeiner, Toren Finkel, Filomena Fiorito, Paul B. Fisher, Marc Flajolet, FLAMIGNI, FLAVIO, Oliver Florey, Salvatore Florio, R. Andres Floto, Marco Folini, Carlo Follo, Edward A. Fon, Francesco Fornai, Franco Fortunato, Alessandro Fraldi, Rodrigo Franco, Arnaud Francois, Aurélie François, Lisa B. Frankel, Iain DC Fraser, Norbert Frey, Damien G. Freyssenet, Christian Frezza, Scott L. Friedman, Daniel E. Frigo, Dongxu Fu, José M. Fuentes, Juan Fueyo, Yoshio Fujitani, Yuuki Fujiwara, Mikihiro Fujiya, Mitsunori Fukuda, Simone Fulda, Carmela Fusco, Bozena Gabryel, Matthias Gaestel, Philippe Gailly, Malgorzata Gajewska, Sehamuddin Galadari, Gad Galili, Inmaculada Galindo, Maria F. Galindo, Giovanna Galliciotti, Lorenzo Galluzzi, Luca Galluzzi, Vincent Galy, Noor Gammoh, Sam Gandy, Anand K. Ganesan, Swamynathan Ganesan, Ian G. Ganley, Monique Gannagé, Fen Biao Gao, Feng Gao, Jian Xin Gao, Lorena García Nannig, Eleonora García Véscovi, Marina Garcia Macía, Carmen Garcia Ruiz, Abhishek D. Garg, Pramod Kumar Garg, Ricardo Gargini, Nils Christian Gassen, Damián Gatica, Evelina Gatti, Julie Gavard, Evripidis Gavathiotis, Liang Ge, Pengfei Ge, Shengfang Ge, Po Wu Gean, Vania Gelmetti, Armando A. Genazzani, Jiefei Geng, Pascal Genschik, Lisa Gerner, Jason E. Gestwicki, David A. Gewirtz, Saeid Ghavami, Eric Ghigo, Debabrata Ghosh, Anna Maria Giammarioli, Francesca Giampieri, Claudia Giampietri, Alexandra Giatromanolaki, Derrick J. Gibbings, Lara Gibellini, Spencer B. Gibson, Vanessa Ginet, Antonio Giordano, Flaviano Giorgini, Elisa Giovannetti, Stephen E. Girardin, Suzana Gispert, Sandy Giuliano, Candece L. Gladson, Alvaro Glavic, Martin Gleave, Nelly Godefroy, Robert M. Gogal Jr, Kuppan Gokulan, Gustavo H. Goldman, Delia Goletti, Michael S. Goligorsky, Aldrin V. Gomes, Ligia C. Gomes, Hernando Gomez, Candelaria Gomez Manzano, Rubén Gómez Sánchez, Dawit AP Gonçalves, Ebru Goncu, Qingqiu Gong, Céline Gongora, Carlos B. Gonzalez, Pedro Gonzalez Alegre, Pilar Gonzalez Cabo, Rosa Ana González Polo, Ing Swie Goping, Carlos Gorbea, Nikolai V. Gorbunov, Daphne R. Goring, Adrienne M. Gorman, Sharon M. Gorski, Sandro Goruppi, Shino Goto Yamada, Cecilia Gotor, Roberta A. Gottlieb, Illana Gozes, Devrim Gozuacik, Yacine Graba, Martin Graef, Giovanna E. Granato, Gary Dean Grant, Steven Grant, Giovanni Luca Gravina, Douglas R. Green, Alexander Greenhough, Michael T. Greenwood, Benedetto Grimaldi, Frédéric Gros, Charles Grose, Jean Francois Groulx, Florian Gruber, Paolo Grumati, Tilman Grune, Jun Lin Guan, Kun Liang Guan, Barbara Guerra, Carlos Guillen, Kailash Gulshan, Jan Gunst, Chuanyong Guo, Lei Guo, Ming Guo, Wenjie Guo, Xu Guang Guo, Andrea A. Gust, Åsa B. Gustafsson, Elaine Gutierrez, Maximiliano G. Gutierrez, Ho Shin Gwak, Albert Haas, James E. Haber, Shinji Hadano, Monica Hagedorn, David R. Hahn, Andrew J. Halayko, Anne Hamacher Brady, Kozo Hamada, Ahmed Hamai, Andrea Hamann, Maho Hamasaki, Isabelle Hamer, Qutayba Hamid, Ester M. Hammond, Feng Han, Weidong Han, James T. Handa, John A. Hanover, Malene Hansen, Masaru Harada, Ljubica Harhaji Trajkovic, J. Wade Harper, Abdel Halim Harrath, Adrian L. Harris, James Harris, Udo Hasler, Peter Hasselblatt, Kazuhisa Hasui, Robert G. Hawley, Teresa S. Hawley, Congcong He, Cynthia Y. He, Fengtian He, Gu He, Rong Rong He, Xian Hui He, You Wen He, Yu Ying He, Joan K. Heath, Marie Josée Hébert, Robert A. Heinzen, Gudmundur Vignir Helgason, Michael Hensel, Elizabeth P. Henske, Chengtao Her, Paul K. Herman, Agustín Hernández, Carlos Hernandez, Sonia Hernández Tiedra, Claudio Hetz, P. Robin Hiesinger, Katsumi Higaki, Sabine Hilfiker, Bradford G. Hill, Joseph A. Hill, William D. Hill, Keisuke Hino, Daniel Hofius, Paul Hofman, Günter U. Höglinger, Jörg Höhfeld, Marina K. Holz, Yonggeun Hong, David A. Hood, Jeroen JM Hoozemans, Thorsten Hoppe, Chin Hsu, Chin Yuan Hsu, Li Chung Hsu, Dong Hu, Guochang Hu, Hong Ming Hu, Hongbo Hu, Ming Chang Hu, Yu Chen Hu, Zhuo Wei Hu, Fang Hua, Ya Hua, Canhua Huang, Huey Lan Huang, Kuo How Huang, Kuo Yang Huang, Shile Huang, Shiqian Huang, Wei Pang Huang, Yi Ran Huang, Yong Huang, Yunfei Huang, Tobias B. Huber, Patricia Huebbe, Won Ki Huh, Juha J. Hulmi, Gang Min Hur, James H. Hurley, Zvenyslava Husak, Sabah NA Hussain, Salik Hussain, Jung Jin Hwang, Seungmin Hwang, Thomas IS Hwang, Atsuhiro Ichihara, Yuzuru Imai, Carol Imbriano, Megumi Inomata, Takeshi Into, Valentina Iovane, Juan L. Iovanna, Renato V. Iozzo, Nancy Y. Ip, Javier E. Irazoqui, Pablo Iribarren, Yoshitaka Isaka, Aleksandra J. Isakovic, Harry Ischiropoulos, Jeffrey S. Isenberg, Mohammad Ishaq, Hiroyuki Ishida, Isao Ishii, Jane E. Ishmael, Ciro Isidoro, Ken ichi Isobe, Erika Isono, Shohreh Issazadeh Navikas, Koji Itahana, Eisuke Itakura, Andrei I. Ivanov, Anand Krishnan V. Iyer, José M. Izquierdo, Yotaro Izumi, Valentina Izzo, Marja Jäättelä, Nadia Jaber, Daniel John Jackson, William T. Jackson, Tony George Jacob, Thomas S. Jacques, Chinnaswamy Jagannath, Ashish Jain, Nihar Ranjan Jana, Byoung Kuk Jang, Alkesh Jani, Bassam Janji, Paulo Roberto Jannig, Patric J. Jansson, Steve Jean, Marina Jendrach, Ju Hong Jeon, Niels Jessen, Eui Bae Jeung, Kailiang Jia, Lijun Jia, Hong Jiang, Hongchi Jiang, Liwen Jiang, Teng Jiang, Xiaoyan Jiang, Xuejun Jiang, Ying Jiang, Yongjun Jiang, Alberto Jiménez, Cheng Jin, Hongchuan Jin, Lei Jin, Meiyan Jin, Shengkan Jin, Umesh Kumar Jinwal, Eun Kyeong Jo, Terje Johansen, Daniel E. Johnson, Gail VW Johnson, James D. Johnson, Eric Jonasch, Chris Jones, Leo AB Joosten, Joaquin Jordan, Anna Maria Joseph, Bertrand Joseph, Annie M. Joubert, Dianwen Ju, Jingfang Ju, Hsueh Fen Juan, Katrin Juenemann, Gábor Juhász, Hye Seung Jung, Jae U. Jung, Yong Keun Jung, Heinz Jungbluth, Matthew J. Justice, Barry Jutten, Nadeem O. Kaakoush, Kai Kaarniranta, Allen Kaasik, Tomohiro Kabuta, Bertrand Kaeffer, Katarina Kågedal, Alon Kahana, Shingo Kajimura, Or Kakhlon, Manjula Kalia, Dhan V. Kalvakolanu, Yoshiaki Kamada, Konstantinos Kambas, Vitaliy O. Kaminskyy, Harm H. Kampinga, Mustapha Kandouz, Chanhee Kang, Rui Kang, Tae Cheon Kang, Tomotake Kanki, Thirumala Devi Kanneganti, Haruo Kanno, Anumantha G. Kanthasamy, Marc Kantorow, Maria Kaparakis Liaskos, Orsolya Kapuy, Vassiliki Karantza, Md Razaul Karim, Parimal Karmakar, Arthur Kaser, Susmita Kaushik, Thomas Kawula, A. Murat Kaynar, Po Yuan Ke, Zun Ji Ke, John H. Kehrl, Kate E. Keller, Jongsook Kim Kemper, Anne K. Kenworthy, Oliver Kepp, Andreas Kern, Santosh Kesari, David Kessel, Robin Ketteler, Isis do Carmo Kettelhut, Bilon Khambu, Muzamil Majid Khan, Vinoth KM Khandelwal, Sangeeta Khare, Juliann G. Kiang, Amy A. Kiger, Akio Kihara, Arianna L. Kim, Cheol Hyeon Kim, Deok Ryong Kim, Do Hyung Kim, Eung Kweon Kim, Hye Young Kim, Hyung Ryong Kim, Jae Sung Kim, Jeong Hun Kim, Jin Cheon Kim, Jin Hyoung Kim, Kwang Woon Kim, Michael D. Kim, Moon Moo Kim, Peter K. Kim, Seong Who Kim, Soo Youl Kim, Yong Sun Kim, Yonghyun Kim, Adi Kimchi, Alec C. Kimmelman, Tomonori Kimura, Jason S. King, Karla Kirkegaard, Vladimir Kirkin, Lorrie A. Kirshenbaum, Shuji Kishi, Yasuo Kitajima, Katsuhiko Kitamoto, Yasushi Kitaoka, Kaio Kitazato, Rudolf A. Kley, Walter T. Klimecki, Michael Klinkenberg, Jochen Klucken, Helene Knævelsrud, Erwin Knecht, Laura Knuppertz, Jiunn Liang Ko, Satoru Kobayashi, Jan C. Koch, Christelle Koechlin Ramonatxo, Ulrich Koenig, Young Ho Koh, Katja Köhler, Sepp D. Kohlwein, Masato Koike, Masaaki Komatsu, Eiki Kominami, Dexin Kong, Hee Jeong Kong, Eumorphia G. Konstantakou, Benjamin T. Kopp, Tamas Korcsmaros, Laura Korhonen, Viktor I. Korolchuk, Nadya V. Koshkina, Yanjun Kou, Michael I. Koukourakis, Constantinos Koumenis, Attila L. Kovács, Tibor Kovács, Werner J. Kovacs, Daisuke Koya, Claudine Kraft, Dimitri Krainc, Helmut Kramer, Tamara Kravic Stevovic, Wilhelm Krek, Carole Kretz Remy, Roswitha Krick, Malathi Krishnamurthy, Janos Kriston Vizi, Guido Kroemer, Michael C. Kruer, Rejko Kruger, Nicholas T. Ktistakis, Kazuyuki Kuchitsu, Christian Kuhn, Addanki Pratap Kumar, Anuj Kumar, Ashok Kumar, Deepak Kumar, Dhiraj Kumar, Rakesh Kumar, Sharad Kumar, Mondira Kundu, Hsing Jien Kung, Atsushi Kuno, Sheng Han Kuo, Jeff Kuret, Tino Kurz, Terry Kwok, Taeg Kyu Kwon, Yong Tae Kwon, Irene Kyrmizi, Albert R. La Spada, Frank Lafont, Tim Lahm, Aparna Lakkaraju, Truong Lam, Trond Lamark, Steve Lancel, Terry H. Landowski, Darius JR Lane, Jon D. Lane, Cinzia Lanzi, Pierre Lapaquette, Louis R. Lapierre, Jocelyn Laporte, Johanna Laukkarinen, Gordon W. Laurie, Sergio Lavandero, Lena Lavie, Matthew J. LaVoie, Betty Yuen Kwan Law, Helen Ka wai Law, Kelsey B. Law, Robert Layfield, Pedro A. Lazo, Laurent Le Cam, Karine G. Le Roch, Hervé Le Stunff, Vijittra Leardkamolkarn, Marc Lecuit, Byung Hoon Lee, Che Hsin Lee, Erinna F. Lee, Gyun Min Lee, He Jin Lee, Hsinyu Lee, Jae Keun Lee, Jongdae Lee, Juhyun Lee, Jun Hee Lee, Michael Lee, Myung Shik Lee, Patty J. Lee, Sam W. Lee, Seung Jae Lee, Shiow Ju Lee, Stella Y. Lee, Sug Hyung Lee, Sung Sik Lee, Sung Joon Lee, Sunhee Lee, Ying Ray Lee, Yong J. Lee, Young H. Lee, Christiaan Leeuwenburgh, Sylvain Lefort, Renaud Legouis, Jinzhi Lei, Qun Ying Lei, David A. Leib, Gil Leibowitz, Istvan Lekli, Stéphane D. Lemaire, John J. Lemasters, Marius K. Lemberg, Antoinette Lemoine, Shuilong Leng, Guido Lenz, Paola Lenzi, Lilach O. Lerman, Daniele Lettieri Barbato, Julia I. Ju Leu, Hing Y. Leung, Beth Levine, Patrick A. Lewis, Frank Lezoualc'h, Chi Li, Faqiang Li, Feng Jun Li, Jun Li, Ke Li, Lian Li, Min Li, Qiang Li, Rui Li, Sheng Li, Wei Li, Xiaotao Li, Yumin Li, Jiqin Lian, Chengyu Liang, Qiangrong Liang, Yulin Liao, Joana Liberal, Pawel P. Liberski, Pearl Lie, Andrew P. Lieberman, Hyunjung Jade Lim, Kah Leong Lim, Kyu Lim, Raquel T. Lima, Chang Shen Lin, Chiou Feng Lin, Fang Lin, Fangming Lin, Fu Cheng Lin, Kui Lin, Kwang Huei Lin, Pei Hui Lin, Tianwei Lin, Wan Wan Lin, Yee Shin Lin, Yong Lin, Rafael Linden, Dan Lindholm, Lisa M. Lindqvist, Paul Lingor, Andreas Linkermann, Lance A. Liotta, Marta M. Lipinski, Vitor A. Lira, Michael P. Lisanti, Paloma B. Liton, Bo Liu, Chong Liu, Chun Feng Liu, Fei Liu, Hung Jen Liu, Jianxun Liu, Jing Jing Liu, Jing Lan Liu, Ke Liu, Leyuan Liu, Liang Liu, Quentin Liu, Rong Yu Liu, Shiming Liu, Shuwen Liu, Wei Liu, Xian De Liu, Xiangguo Liu, Xiao Hong Liu, Xinfeng Liu, Xu Liu, Xueqin Liu, Yang Liu, Yule Liu, Zexian Liu, Zhe Liu, Juan P. Liuzzi, Gérard Lizard, Mila Ljujic, Irfan J. Lodhi, Susan E. Logue, Bal L. Lokeshwar, Yun Chau Long, Sagar Lonial, Benjamin Loos, Carlos López Otín, Cristina López Vicario, Mar Lorente, Philip L. Lorenzi, Péter Lõrincz, Marek Los, Michael T. Lotze, Penny E. Lovat, Binfeng Lu, Bo Lu, Jiahong Lu, Qing Lu, She Min Lu, Shuyan Lu, Yingying Lu, Frédéric Luciano, Shirley Luckhart, John Milton Lucocq, Paula Ludovico, Aurelia Lugea, Nicholas W. Lukacs, Julian J. Lum, Anders H. Lund, Honglin Luo, Jia Luo, Shouqing Luo, Claudio Luparello, Timothy Lyons, Jianjie Ma, Yi Ma, Yong Ma, Zhenyi Ma, Juliano Machado, Glaucia M. Machado Santelli, Fernando Macian, Gustavo C. MacIntosh, Jeffrey P. MacKeigan, Kay F. Macleod, John D. MacMicking, Lee Ann MacMillan Crow, Frank Madeo, Muniswamy Madesh, Julio Madrigal Matute, Akiko Maeda, Tatsuya Maeda, Gustavo Maegawa, Emilia Maellaro, Hannelore Maes, Marta Magariños, Kenneth Maiese, Tapas K. Maiti, Luigi Maiuri, Maria Chiara Maiuri, Carl G. Maki, Roland Malli, Walter Malorni, Alina Maloyan, Fathia Mami Chouaib, Na Man, Joseph D. Mancias, Eva Maria Mandelkow, Michael A. Mandell, Angelo A. Manfredi, Serge N. Manié, Claudia Manzoni, Kai Mao, Zixu Mao, Zong Wan Mao, Philippe Marambaud, Anna Maria Marconi, Zvonimir Marelja, Gabriella Marfe, Marta Margeta, Eva Margittai, Muriel Mari, Francesca V. Mariani, Concepcio Marin, Sara Marinelli, Guillermo Mariño, Ivanka Markovic, Rebecca Marquez, MARTELLI, ALBERTO MARIA, Sascha Martens, Katie R. Martin, Seamus J. Martin, Shaun Martin, Miguel A. Martin Acebes, Paloma Martín Sanz, Camille Martinand Mari, Wim Martinet, Jennifer Martinez, Nuria Martinez Lopez, Ubaldo Martinez Outschoorn, Moisés Martínez Velázquez, Marta Martinez Vicente, Waleska Kerllen Martins, Hirosato Mashima, James A. Mastrianni, Giuseppe Matarese, Paola Matarrese, Roberto Mateo, Satoaki Matoba, Naomichi Matsumoto, Takehiko Matsushita, Akira Matsuura, Takeshi Matsuzawa, Mark P. Mattson, Soledad Matus, Norma Maugeri, Caroline Mauvezin, Andreas Mayer, Dusica Maysinger, Guillermo D. Mazzolini, Mary Kate McBrayer, Kimberly McCall, Craig McCormick, Gerald M. McInerney, Skye C. McIver, Sharon McKenna, John J. McMahon, Iain A. McNeish, Fatima Mechta Grigoriou, Jan Paul Medema, Diego L. Medina, Klara Megyeri, Maryam Mehrpour, Jawahar L. Mehta, Yide Mei, Ute Christiane Meier, Alfred J. Meijer, Alicia Meléndez, Gerry Melino, Sonia Melino, Edesio Jose Tenorio de Melo, Maria A. Mena, Marc D. Meneghini, Javier A. Menendez, Regina Menezes, Liesu Meng, Ling hua Meng, Songshu Meng, Rossella Menghini, A. Sue Menko, Rubem FS Menna Barreto, Manoj B. Menon, Marco A. Meraz Ríos, Giuseppe Merla, Luciano Merlini, Angelica M. Merlot, Andreas Meryk, Stefania Meschini, Joel N. Meyer, Man tian Mi, Chao Yu Miao, Lucia Micale, Simon Michaeli, Carine Michiels, FRANCO MIGLIACCIO, ANNA RITA, Anastasia Susie Mihailidou, Dalibor Mijaljica, Katsuhiko Mikoshiba, Enrico Milan, Leonor Miller Fleming, Gordon B. Mills, Ian G. Mills, Georgia Minakaki, Berge A. Minassian, Xiu Fen Ming, Farida Minibayeva, Elena A. Minina, Justine D. Mintern, Saverio Minucci, Antonio Miranda Vizuete, Claire H. Mitchell, Shigeki Miyamoto, Keisuke Miyazawa, Noboru Mizushima, Katarzyna Mnich, Baharia Mograbi, Simin Mohseni, Luis Ferreira Moita, Marco Molinari, Maurizio Molinari, Andreas Buch Møller, Bertrand Mollereau, Faustino Mollinedo, Marco Mongillo, Martha M. Monick, Serena Montagnaro, Craig Montell, Darren J. Moore, Michael N. Moore, Rodrigo Mora Rodriguez, Paula I. Moreira, Etienne Morel, Maria Beatrice Morelli, Sandra Moreno, Michael J. Morgan, Arnaud Moris, Yuji Moriyasu, Janna L. Morrison, Lynda A. Morrison, Eugenia Morselli, Jorge Moscat, Pope L. Moseley, Serge Mostowy, Elisa Motori, Denis Mottet, Jeremy C. Mottram, Charbel E. H. Moussa, Vassiliki E. Mpakou, Hasan Mukhtar, Jean M. Mulcahy Levy, Sylviane Muller, Raquel Muñoz Moreno, Cristina Muñoz Pinedo, Christian Münz, Maureen E. Murphy, James T. Murray, Aditya Murthy, Indira U. Mysorekar, Ivan R. Nabi, Massimo Nabissi, Gustavo A. Nader, Yukitoshi Nagahara, Yoshitaka Nagai, Kazuhiro Nagata, Anika Nagelkerke, Péter Nagy, Samisubbu R. Naidu, Sreejayan Nair, Hiroyasu Nakano, Hitoshi Nakatogawa, Meera Nanjundan, Gennaro Napolitano, Naweed I. Naqvi, Roberta Nardacci, Derek P. Narendra, Masashi Narita, Anna Chiara Nascimbeni, Ramesh Natarajan, Luiz C. Navegantes, Steffan T. Nawrocki, Taras Y. Nazarko, Volodymyr Y. Nazarko, Thomas Neill, Luca M. Neri, Mihai G. Netea, Romana T. Netea Maier, Bruno M. Neves, Paul A. Ney, Ioannis P. Nezis, Hang TT Nguyen, Huu Phuc Nguyen, Anne Sophie Nicot, Hilde Nilsen, Per Nilsson, Mikio Nishimura, Ichizo Nishino, Mireia Niso Santano, Hua Niu, Ralph A. Nixon, Vincent CO Njar, Takeshi Noda, Angelika A. Noegel, Elsie Magdalena Nolte, Erik Norberg, Koenraad K. Norga, Sakineh Kazemi Noureini, Shoji Notomi, Lucia Notterpek, Karin Nowikovsky, Nobuyuki Nukina, Thorsten Nürnberger, Valerie B. O'Donnell, Tracey O'Donovan, Peter J. O'Dwyer, Ina Oehme, Clara L. Oeste, Michinaga Ogawa, Besim Ogretmen, Yuji Ogura, Young J. Oh, Masaki Ohmuraya, Takayuki Ohshima, Rani Ojha, Koji Okamoto, Toshiro Okazaki, F. Javier Oliver, Karin Ollinger, Stefan Olsson, Daniel P. Orban, Paulina Ordonez, Idil Orhon, Laszlo Orosz, Eyleen J. O'Rourke, Helena Orozco, Angel L. Ortega, Elena Ortona, Laura D. Osellame, Junko Oshima, Shigeru Oshima, Heinz D. Osiewacz, Takanobu Otomo, Kinya Otsu, Jing hsiung James Ou, Tiago F. Outeiro, Dong yun Ouyang, Hongjiao Ouyang, Michael Overholtzer, Michelle A. Ozbun, P. Hande Ozdinler, Bulent Ozpolat, Consiglia Pacelli, Paolo Paganetti, Guylène Page, Gilles Pages, Ugo Pagnini, Beata Pajak, Stephen C. Pak, Karolina Pakos Zebrucka, Nazzy Pakpour, Zdena Palková, Francesca Palladino, Kathrin Pallauf, Nicolas Pallet, Marta Palmieri, Søren R. Paludan, Camilla Palumbo, Silvia Palumbo, Olatz Pampliega, Hongming Pan, Wei Pan, Theocharis Panaretakis, Aseem Pandey, Areti Pantazopoulou, Zuzana Papackova, Daniela L. Papademetrio, Issidora Papassideri, Alessio Papini, Nirmala Parajuli, Julian Pardo, Vrajesh V. Parekh, Giancarlo Parenti, Jong In Park, Junsoo Park, Ohkmae K. Park, Roy Parker, Rosanna Parlato, Jan B. Parys, Katherine R. Parzych, Jean Max Pasquet, Benoit Pasquier, Kishore BS Pasumarthi, Daniel Patschan, Cam Patterson, Sophie Pattingre, Scott Pattison, Arnim Pause, Hermann Pavenstädt, Flaminia Pavone, Zully Pedrozo, Fernando J. Peña, Miguel A. Peñalva, Mario Pende, Jianxin Peng, Fabio Penna, Josef M. Penninger, Anna Pensalfini, Salvatore Pepe, Gustavo JS Pereira, Paulo C. Pereira, Verónica Pérez de la Cruz, María Esther Pérez Pérez, Diego Pérez Rodríguez, Dolores Pérez Sala, Celine Perier, Andras Perl, David H. Perlmutter, Ida Perrotta, Shazib Pervaiz, Maija Pesonen, Jeffrey E. Pessin, Godefridus J. Peters, Morten Petersen, Irina Petrache, Basil J. Petrof, Goran Petrovski, James M. Phang, Mauro Piacentini, Marina Pierdominici, Philippe Pierre, Valérie Pierrefite Carle, Federico Pietrocola, Felipe X. Pimentel Muiños, Mario Pinar, Benjamin Pineda, Ronit Pinkas Kramarski, Marcello Pinti, Paolo Pinton, Bilal Piperdi, James M. Piret, Leonidas C. Platanias, Harald W. Platta, Edward D. Plowey, Stefanie Pöggeler, Marc Poirot, Peter Polčic, Angelo Poletti, Audrey H. Poon, Hana Popelka, Blagovesta Popova, Izabela Poprawa, Shibu M. Poulose, Joanna Poulton, Scott K. Powers, Ted Powers, Mercedes Pozuelo Rubio, Krisna Prak, Reinhild Prange, Mark Prescott, Muriel Priault, Sharon Prince, Richard L. Proia, Tassula Proikas Cezanne, Holger Prokisch, Vasilis J. Promponas, Karin Przyklenk, Rosa Puertollano, Subbiah Pugazhenthi, Luigi Puglielli, Aurora Pujol, Julien Puyal, Dohun Pyeon, Xin Qi, Wen bin Qian, Zheng Hong Qin, Yu Qiu, Ziwei Qu, Joe Quadrilatero, Frederick Quinn, Nina Raben, Hannah Rabinowich, Flavia Radogna, Michael J. Ragusa, Mohamed Rahmani, Komal Raina, Sasanka Ramanadham, Rajagopal Ramesh, Abdelhaq Rami, Sarron Randall Demllo, Felix Randow, Hai Rao, V. Ashutosh Rao, Blake B. Rasmussen, Tobias M. Rasse, Edward A. Ratovitski, Pierre Emmanuel Rautou, Swapan K. Ray, Babak Razani, Bruce H. Reed, Fulvio Reggiori, Markus Rehm, Andreas S. Reichert, Theo Rein, David J. Reiner, Eric Reits, Jun Ren, Xingcong Ren, Maurizio Renna, Jane EB Reusch, Jose L. Revuelta, Leticia Reyes, Alireza R. Rezaie, Robert I. Richards, Des R. Richardson, Clémence Richetta, Michael A. Riehle, Bertrand H. Rihn, Yasuko Rikihisa, Brigit E. Riley, Gerald Rimbach, Maria Rita Rippo, Konstantinos Ritis, Federica Rizzi, Elizete Rizzo, Peter J. Roach, Jeffrey Robbins, Michel Roberge, Gabriela Roca, Maria Carmela Roccheri, Sonia Rocha, Cecilia MP Rodrigues, Clara I. Rodríguez, Santiago Rodriguez de Cordoba, Natalia Rodriguez Muela, Jeroen Roelofs, Vladimir V. Rogov, Troy T. Rohn, Bärbel Rohrer, Davide Romanelli, Luigina Romani, Patricia Silvia Romano, M. Isabel G. Roncero, Jose Luis Rosa, Alicia Rosello, Kirill V. Rosen, Philip Rosenstiel, Magdalena Rost Roszkowska, Kevin A. Roth, Gael Roué, Mustapha Rouis, Kasper M. Rouschop, Daniel T. Ruan, Diego Ruano, David C. Rubinsztein, Edmund B. Rucker III, Assaf Rudich, Emil Rudolf, Ruediger Rudolf, Markus A. Ruegg, Carmen Ruiz Roldan, Avnika Ashok Ruparelia, Paola Rusmini, David W. Russ, Gian Luigi Russo, Giuseppe Russo, Rossella Russo, Tor Erik Rusten, Victoria Ryabovol, Kevin M. Ryan, Stefan W. Ryter, David M. Sabatini, Michael Sacher, Carsten Sachse, Michael N. Sack, Junichi Sadoshima, Paul Saftig, Ronit Sagi Eisenberg, Sumit Sahni, Pothana Saikumar, Tsunenori Saito, Tatsuya Saitoh, Koichi Sakakura, Machiko Sakoh Nakatogawa, Yasuhito Sakuraba, María Salazar Roa, Paolo Salomoni, Ashok K. Saluja, Paul M. Salvaterra, Rosa Salvioli, Afshin Samali, Anthony MJ Sanchez, José A. Sánchez Alcázar, Ricardo Sanchez Prieto, Marco Sandri, Miguel A. Sanjuan, Stefano Santaguida, Laura Santambrogio, Giorgio Santoni, Claudia Nunes dos Santos, Shweta Saran, Marco Sardiello, Graeme Sargent, Pallabi Sarkar, Sovan Sarkar, Maria Rosa Sarrias, Minnie M. Sarwal, Chihiro Sasakawa, Motoko Sasaki, Miklos Sass, Ken Sato, Miyuki Sato, Joseph Satriano, Niramol Savaraj, Svetlana Saveljeva, Liliana Schaefer, Ulrich E. Schaible, Michael Scharl, Hermann M. Schatzl, Randy Schekman, Wiep Scheper, Alfonso Schiavi, Hyman M. Schipper, Hana Schmeisser, Jens Schmidt, Ingo Schmitz, Bianca E. Schneider, E. Marion Schneider, Jaime L. Schneider, Eric A. Schon, Miriam J. Schönenberger, Axel H. Schönthal, Daniel F. Schorderet, Bernd Schröder, Sebastian Schuck, Ryan J. Schulze, Melanie Schwarten, Thomas L. Schwarz, Sebastiano Sciarretta, Kathleen Scotto, A. Ivana Scovassi, Robert A. Screaton, Mark Screen, Hugo Seca, Simon Sedej, Laura Segatori, Nava Segev, Per O. Seglen, Jose M. Seguí Simarro, Juan Segura Aguilar, Ekihiro Seki, Iban Seiliez, Christian Sell, Clay F. Semenkovich, Gregg L. Semenza, Utpal Sen, Andreas L. Serra, Ana Serrano Puebla, Hiromi Sesaki, Takao Setoguchi, Carmine Settembre, John J. Shacka, Ayesha N. Shajahan Haq, Irving M. Shapiro, Shweta Sharma, Hua She, C. K. James Shen, Chiung Chyi Shen, Han Ming Shen, Sanbing Shen, Weili Shen, Rui Sheng, Xianyong Sheng, Zu Hang Sheng, Trevor G. Shepherd, Junyan Shi, Qiang Shi, Qinghua Shi, Yuguang Shi, Shusaku Shibutani, Kenichi Shibuya, Yoshihiro Shidoji, Jeng Jer Shieh, Chwen Ming Shih, Yohta Shimada, Shigeomi Shimizu, Dong Wook Shin, Mari L. Shinohara, Michiko Shintani, Takahiro Shintani, Tetsuo Shioi, Ken Shirabe, Ronit Shiri Sverdlov, Orian Shirihai, Gordon C. Shore, Chih Wen Shu, Deepak Shukla, Andriy A. Sibirny, Valentina Sica, Christina J. Sigurdson, Einar M. Sigurdsson, Puran Singh Sijwali, Beata Sikorska, Wilian A. Silveira, Sandrine Silvente Poirot, Gary A. 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Szlosarek, Heinrich Taegtmeyer, Marco Tafani, Emmanuel Taillebourg, Stephen WG Tait, Krisztina Takacs Vellai, Yoshinori Takahashi, Szabolcs Takáts, Genzou Takemura, Nagio Takigawa, Nicholas J. Talbot, Elena Tamagno, Jerome Tamburini, Cai Ping Tan, Lan Tan, Mei Lan Tan, Ming Tan, Yee Joo Tan, Keiji Tanaka, Masaki Tanaka, Daolin Tang, Dingzhong Tang, Guomei Tang, Isei Tanida, Kunikazu Tanji, Bakhos A. Tannous, Jose A. Tapia, Inmaculada Tasset Cuevas, Marc Tatar, Iman Tavassoly, Nektarios Tavernarakis, Allen Taylor, Graham S. Taylor, Gregory A. Taylor, J. Paul Taylor, Mark J. Taylor, Elena V. Tchetina, Andrew R. Tee, Fatima Teixeira Clerc, Sucheta Telang, Tewin Tencomnao, Ba Bie Teng, Ru Jeng Teng, Faraj Terro, Gianluca Tettamanti, Arianne L. Theiss, Anne E. Theron, Kelly Jean Thomas, Marcos P. Thomé, Paul G. Thomes, Andrew Thorburn, Jeremy Thorner, Thomas Thum, Michael Thumm, Teresa LM Thurston, Ling Tian, Andreas Till, Jenny Pan yun Ting, Vladimir I. 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Valverde, Greet Van den Berghe, Ludo Van Den Bosch, Gijs R. van den Brink, F. Gisou van der Goot, Ida J. van der Klei, Luc JW van der Laan, Wouter G. van Doorn, Marjolein van Egmond, Kenneth L. van Golen, Luc Van Kaer, Menno van Lookeren Campagne, Peter Vandenabeele, Wim Vandenberghe, Ilse Vanhorebeek, Isabel Varela Nieto, M. Helena Vasconcelos, Radovan Vasko, Demetrios G. Vavvas, Ignacio Vega Naredo, Guillermo Velasco, Athanassios D. Velentzas, Panagiotis D. Velentzas, Tibor Vellai, Edo Vellenga, Mikkel Holm Vendelbo, Kartik Venkatachalam, Natascia Ventura, Salvador Ventura, Patrícia ST Veras, Mireille Verdier, Beata G. Vertessy, Andrea Viale, Michel Vidal, Helena LA Vieira, Richard D. Vierstra, Nadarajah Vigneswaran, Neeraj Vij, Miquel Vila, Margarita Villar, Victor H. Villar, Joan Villarroya, Cécile Vindis, Giampietro Viola, Maria Teresa Viscomi, Giovanni Vitale, Dan T. Vogl, Olga V. Voitsekhovskaja, Clarissa von Haefen, Karin von Schwarzenberg, Daniel E. Voth, Valérie Vouret Craviari, Kristina Vuori, Jatin M. Vyas, Christian Waeber, Cheryl Lyn Walker, Mark J. Walker, Jochen Walter, Lei Wan, Xiangbo Wan, Bo Wang, Caihong Wang, Chao Yung Wang, Chengshu Wang, Chenran Wang, Chuangui Wang, Dong Wang, Fen Wang, Fuxin Wang, Guanghui Wang, Hai jie Wang, Haichao Wang, Hong Gang Wang, Hongmin Wang, Horng Dar Wang, Jing Wang, Junjun Wang, Mei Wang, Mei Qing Wang, Pei Yu Wang, Peng Wang, Richard C. Wang, Shuo Wang, Ting Fang Wang, Xian Wang, Xiao jia Wang, Xiao Wei Wang, Xin Wang, Xuejun Wang, Yan Wang, Yanming Wang, Ying Wang, Ying Jan Wang, Yipeng Wang, Yu Wang, Yu Tian Wang, Yuqing Wang, Zhi Nong Wang, Pablo Wappner, Carl Ward, Diane McVey Ward, Gary Warnes, Hirotaka Watada, Yoshihisa Watanabe, Kei Watase, Timothy E. Full Terms, Conditions of access, use can be found at h.t.t.p.:././.w.w.w. t.a.n.d.f.o.n.l.i.n.e. com/action/journalInformation?journalCode=kaup20 Download by: [Alma Mater Studiorum Università di Bologna] Date: 23 September 2016, At: 06:43 Weaver, Colin D. Weekes, Jiwu Wei, Thomas Weide, Conrad C. Weihl, Günther Weindl, Simone Nardin Weis, Longping Wen, Xin Wen, Yunfei Wen, Benedikt Westermann, Cornelia M. Weyand, Anthony R. White, Eileen White, J. Lindsay Whitton, Alexander J. Whitworth, Joëlle Wiels, Franziska Wild, Manon E. Wildenberg, Tom Wileman, Deepti Srinivas Wilkinson, Simon Wilkinson, Dieter Willbold, Chris Williams, Katherine Williams, Peter R. Williamson, Konstanze F. Winklhofer, Steven S. Witkin, Stephanie E. Wohlgemuth, Thomas Wollert, Ernst J. Wolvetang, Esther Wong, G. William Wong, Richard W. Wong, Vincent Kam Wai Wong, Elizabeth A. Woodcock, Karen L. Wright, Chunlai Wu, Defeng Wu, Gen Sheng Wu, Jian Wu, Junfang Wu, Mian Wu, Min Wu, Shengzhou Wu, William KK Wu, Yaohua Wu, Zhenlong Wu, Cristina PR Xavier, Ramnik J. Xavier, Gui Xian Xia, Tian Xia, Weiliang Xia, Yong Xia, Hengyi Xiao, Jian Xiao, Shi Xiao, Wuhan Xiao, Chuan Ming Xie, Zhiping Xie, Zhonglin Xie, Maria Xilouri, Yuyan Xiong, Chuanshan Xu, Congfeng Xu, Feng Xu, Haoxing Xu, Hongwei Xu, Jian Xu, Jianzhen Xu, Jinxian Xu, Liang Xu, Xiaolei Xu, Yangqing Xu, Ye Xu, Zhi Xiang Xu, Ziheng Xu, Yu Xue, Takahiro Yamada, Ai Yamamoto, Koji Yamanaka, Shunhei Yamashina, Shigeko Yamashiro, Bing Yan, Bo Yan, Xianghua Yan, Zhen Yan, Yasuo Yanagi, Dun Sheng Yang, Jin Ming Yang, Liu Yang, Minghua Yang, Pei Ming Yang, Peixin Yang, Qian Yang, Wannian Yang, Wei Yuan Yang, Xuesong Yang, Yi Yang, Ying Yang, Zhifen Yang, Zhihong Yang, Meng Chao Yao, Pamela J. Yao, Xiaofeng Yao, Zhenyu Yao, Zhiyuan Yao, Linda S. Yasui, Mingxiang Ye, Barry Yedvobnick, Behzad Yeganeh, Elizabeth S. Yeh, Patricia L. Yeyati, Fan Yi, Long Yi, Xiao Ming Yin, Calvin K. Yip, Yeong Min Yoo, Young Hyun Yoo, Seung Yong Yoon, Ken Ichi Yoshida, Tamotsu Yoshimori, Ken H. Young, Huixin Yu, Jane J. Yu, Jin Tai Yu, Jun Yu, Li Yu, W. Haung Yu, Xiao Fang Yu, Zhengping Yu, Junying Yuan, Zhi Min Yuan, Beatrice YJT Yue, Jianbo Yue, Zhenyu Yue, David N. Zacks, Eldad Zacksenhaus, Nadia Zaffaroni, Tania Zaglia, Zahra Zakeri, Vincent Zecchini, Jinsheng Zeng, Min Zeng, Qi Zeng, Antonis S. Zervos, Donna D. Zhang, Fan Zhang, Guo Zhang, Guo Chang Zhang, Hao Zhang, Hong Zhang, Hongbing Zhang, Jian Zhang, Jiangwei Zhang, Jianhua Zhang, Jing pu Zhang, Li Zhang, Lin Zhang, Long Zhang, Ming Yong Zhang, Xiangnan Zhang, Xu Dong Zhang, Yan Zhang, Yang Zhang, Yanjin Zhang, Yingmei Zhang, Yunjiao Zhang, Mei Zhao, Wei Li Zhao, Xiaonan Zhao, Yan G. Zhao, Ying Zhao, Yongchao Zhao, Yu xia Zhao, Zhendong Zhao, Zhizhuang J. Zhao, Dexian Zheng, Xi Long Zheng, Xiaoxiang Zheng, Boris Zhivotovsky, Qing Zhong, Guang Zhou Zhou, Guofei Zhou, Huiping Zhou, Shu Feng Zhou, Xu jie Zhou, Hongxin Zhu, Hua Zhu, Wei Guo Zhu, Wenhua Zhu, Xiao Feng Zhu, Yuhua Zhu, Shi Mei Zhuang, Xiaohong Zhuang, Elio Ziparo, Christos E. Zois, Teresa Zoladek, Wei Xing Zong, Antonio Zorzano, Susu M. Zughaier, Life Sciences Institute and Department of Molecular, Cellular, and Developmental Biology and Biological Chemistry, University of Michigan [Ann Arbor], University of Michigan System-University of Michigan System, Tokyo Medical University, The Hebrew University of Jerusalem (HUJ), Mammalian Genetics Unit, Medical Research Council Harwell, University of Occupational and Environmental Health School of Medicine, Partenaires INRAE, University of Toronto, Ben-Gurion University of the Negev (BGU), University of Colorado [Boulder], Cell Death Research & Therapy (CDRT) Lab, Université Catholique de Louvain = Catholic University of Louvain (UCL), University of Vienna [Vienna], Conway Institute of Biomolecular and Biomedical Research and School of Chemical and Bioprocess Engineering, University College Dublin [Dublin] (UCD), Georgetown University, Candiolo Cancer Institute (IRCCS), Centro de Investigacion Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III [Madrid] (ISC), Ikerbasque - Basque Foundation for Science, Cleveland Clinic, Sidney Kimmel Cancer Center, Jefferson (Philadelphia University + Thomas Jefferson University), Universidad de Buenos Aires (UBA), Department of Clinical Neurosciences, University College of London [London] (UCL)-Institute of Neurology, Thérapie génique, Génomique et Epigénomique (U 1169), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Saclay, Consiglio Nazionale delle Ricerche (CNR), Osaka University, Department of Experimental Medicine and Public Health, University of Camerino, University of Barcelona, Institut Universitaire d'Hématologie (IUH), Université Paris Diderot - Paris 7 (UPD7), Génomique Fonctionnelle des Tumeurs Solides (U1162), Université Paris 13 (UP13)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Université Paris Descartes - Paris 5 (UPD5), Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Physics, Technical University of Denmark [Lyngby] (DTU), University of Zaragoza - Universidad de Zaragoza [Zaragoza], Department of Pharmaco-Biology, Università della Calabria [Arcavacata di Rende] (Unical), Fondation Universitaire Notre Dame de la Paix (FUNDP), Facultés Universitaires Notre Dame de la Paix (FUNDP), USC Neuromuscular Center, Department of Neurology, University of Southern California (USC), Physiopathologie de la survie et de la mort cellulaire et infection virale, Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-IFR50-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Côte d'Azur (UCA), Giannina Gaslini Institute, Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), École pratique des hautes études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Université de Montpellier (UM)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Institut de recherche pour le développement [IRD] : UR226, Inner Mongolia Agricultural University (IMAU), Politecnico di Milano [Milan] (POLIMI), Department of Civil, Geological, and Mining Engineering, École Polytechnique de Montréal (EPM)-NSERC Industrial Chair on Drinking Water, Institut de Recherche sur le Cancer et le Vieillissement (IRCAN), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Côte d'Azur (UCA), Department of Molecular Medicine, Institut Pasteur, Fondation Cenci Bolognetti - Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Università degli Studi di Roma 'La Sapienza' = Sapienza University [Rome], Physiopathologie du système nerveux central - Institut François Magendie, Université Bordeaux Segalen - Bordeaux 2-IFR8-Institut National de la Santé et de la Recherche Médicale (INSERM), Laboratory of Experimental Virology - Department of Medical Microbiology [Amsterdam, The Netherlands], Academic Medical Center - Academisch Medisch Centrum [Amsterdam] (AMC), University of Amsterdam [Amsterdam] (UvA)-University of Amsterdam [Amsterdam] (UvA)-Center for Infection and Immunity Amsterdam - CINIMA [Amsterdam, The Netherlands], Centre de résonance magnétique biologique et médicale (CRMBM), Aix Marseille Université (AMU)-Assistance Publique - Hôpitaux de Marseille (APHM)-Centre National de la Recherche Scientifique (CNRS), Dynamique des interactions membranaires normales et pathologiques (DIMNP), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université Montpellier 1 (UM1), Department of Internal Medicine, Hospital Universitario Infanta Sofía, Celullar and Molecular Medicine, Infection bactérienne, inflammation, et carcinogenèse digestive, University of Edinburgh, Unité de Nutrition Humaine (UNH), Institut National de la Recherche Agronomique (INRA)-Université d'Auvergne - Clermont-Ferrand I (UdA)-Clermont Université, Faculty of Engineering and Natural Sciences, Sabanci University [Istanbul], University of Science and Technology Beijing [Beijing] (USTB), Centre for Computational and Systems Biology (COSBI), Sun Yat-Sen University [Guangzhou] (SYSU), Dynamique Musculaire et Métabolisme (DMEM), Université de Montpellier (UM)-Institut National de la Recherche Agronomique (INRA), CAS Institute of Oceanology (IOCAS), Chinese Academy of Sciences [Beijing] (CAS), Polytechnic University of Marche, Centre de Recherche en Cancérologie de Marseille (CRCM), Aix Marseille Université (AMU)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Cell Biology, Physiology and Immunology, Department of Experimental Oncology and Molecular Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, University of Pisa - Università di Pisa, Dulbecco Telethon Institute/Department of Biology, Fondation de Recherche Cancer et Sang - Hôpital Kirchberg, China University of Petroleum, Unilever R&D, University of Queensland [Brisbane], University of Minnesota [Twin Cities] (UMN), University of Minnesota System, Laboratoire de Génie des Procédés et Matériaux - EA 4038 (LGPM), CentraleSupélec, Institute for Advanced Study [Tsinghua], Tsinghua University [Beijing] (THU), Nanayang Technological University (NTU), Nanayang Technological University, Institute of Microelectronics [Beijing] (IMETU), Laboratoire de photonique et de nanostructures (LPN), Centre National de la Recherche Scientifique (CNRS), Institut de biologie moléculaire des plantes (IBMP), Centre National de la Recherche Scientifique (CNRS)-Université de Strasbourg (UNISTRA), Northwestern Polytechnical University [Xi'an] (NPU), University of Pennsylvania [Philadelphia], City University of Hong Kong (CityU), Department of Mathematics [Berkeley], University of California [Berkeley], University of California-University of California, ZJU-ENS Joint Laboratory of Medicinal Chemistry, Zhejiang University, University of Cincinnati (UC), Réponses immunes : régulation et développement, Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM), The University of New Mexico [Albuquerque], Centre de Recherche de l'Institut du Cerveau et de la Moelle épinière (CRICM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Dipartimento di Scienze Biomediche, Università degli Studi di Modena e Reggio Emilia (UNIMORE), Department of Experimental Medicine and Oncology, University of Turin, Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), CNV, University of Valparaiso, Université Paris 1 Panthéon-Sorbonne - UFR d'Arts plastiques et sciences de l'art (UP1 UFR04), Université Paris 1 Panthéon-Sorbonne (UP1), Department of General, Visceral and Vascular Surgery [Jena], Friedrich-Schiller-Universität Jena, Récepteurs nucléaires, maladies cardiovasculaires et diabète - U 1011 (RNMCD), Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Institut National de la Santé et de la Recherche Médicale (INSERM), Réseau International des Instituts Pasteur (RIIP), Macrophages et Développement de l’Immunité, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Immunobiologie des Cellules Dendritiques, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre d'infectiologie Necker-Pasteur [CHU Necker], Institut Pasteur [Paris]-CHU Necker - Enfants Malades [AP-HP], Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP), Institut Pasteur [Paris], Trafic membranaire et Division cellulaire - Membrane Traffic and Cell Division, Centre National de la Recherche Scientifique (CNRS)-Institut Pasteur [Paris], Cibles thérapeutiques, formulation et expertise pré-clinique du médicament (CITHEFOR), Université de Lorraine (UL), This work was supported in part by the National Institutes of Health, including Public Health Service grant GM053396 to D.J.K. Due to space and other limitations, it is not possible to include all other sources of financial support., In a rapidly expanding and highly dynamic field such as autophagy, it is possible that some authors who should have been included on this article have been missed. D.J.K. extends his apologies to researchers in the field of autophagy who, due to oversight or any other reason, could not be included on this article. I also note that two of our colleagues on this manuscript have passed away: Arlette Darfeuille-Michaud and Wouter van Doorn., Life Sciences Institute [Ann Arbor, MI, USA], Laboratoire de Biogenèse Membranaire, CNRS UMR 5200, Université de Bordeaux, INRA Bordeaux Aquitaine, Villenave d'Ornon, France., Amelio, Ivano [0000-0002-9126-5391], Beale, Rupert [0000-0002-6705-8560], Floto, Andres [0000-0002-2188-5659], Frezza, Christian [0000-0002-3293-7397], Ktistakis, Nicholas [0000-0001-9397-2914], Melino, Gerry [0000-0001-9428-5972], Narita, Masashi [0000-0001-7764-577X], Rubinsztein, David [0000-0001-5002-5263], Underwood, Benjamin [0000-0003-3427-9487], Whitworth, Alex [0000-0002-1154-6629], Apollo - University of Cambridge Repository, Université Catholique de Louvain, Facultés Universitaires Notre-Dame de la Paix, Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR50-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Nice Sophia Antipolis (... - 2019) (UNS), Department of Clinical and Molecular Medicine, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Università degli Studi di Roma 'La Sapienza' [Rome], Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-IFR50-Institut National de la Santé et de la Recherche Médicale (INSERM), Unité de Nutrition Humaine - Clermont Auvergne (UNH), Institut National de la Recherche Agronomique (INRA)-Université Clermont Auvergne (UCA), Sun Yat-Sen University (SYSU), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Aix Marseille Université (AMU), University of Minnesota [Twin Cities], Tsinghua University [Beijing], Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS), Université Panthéon-Sorbonne - UFR d'Arts plastiques et sciences de l'art (UP1 UFR04), Université Panthéon-Sorbonne (UP1), Récepteurs nucléaires, maladies cardiovasculaires et diabète (EGID), Université de Lille, Droit et Santé-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille), CHU Necker - Enfants Malades [AP-HP], Trafic membranaire et Division cellulaire, Institut de Biologie du Développement de Marseille (IBDM), Aix Marseille Université (AMU)-Collège de France (CdF)-Centre National de la Recherche Scientifique (CNRS), Klionsky, D., Abdelmohsen, K., Abe, A., Abedin, M., Abeliovich, H., Acevedo Arozena, A., Adachi, H., Adams, C., Adams, P., Adeli, K., Adhihetty, P., Adler, S., Agam, G., Agarwal, R., Aghi, M., Agnello, M., Agostinis, P., Aguilar, P., Aguirre-Ghiso, J., Airoldi, E., Ait-Si-Ali, S., Akematsu, T., Akporiaye, E., Al-Rubeai, M., Albaiceta, G., Albanese, C., Albani, D., Albert, M., Aldudo, J., Algül, H., Alirezaei, M., Alloza, I., Almasan, A., Almonte-Beceril, M., Alnemri, E., Alonso, C., Altan-Bonnet, N., Altieri, D., Alvarez, S., Alvarez-Erviti, L., Alves, S., Amadoro, G., Amano, A., Amantini, C., Ambrosio, S., Amelio, I., Amer, A., Amessou, M., Amon, A., An, Z., Anania, F., Andersen, S., Andley, U., Andreadi, C., Andrieu-Abadie, N., Anel, A., Ann, D., Anoopkumar-Dukie, S., Antonioli, M., Aoki, H., Apostolova, N., Aquila, S., Aquilano, K., Araki, K., Arama, E., Aranda, A., Araya, J., Arcaro, A., Arias, E., Arimoto, H., Ariosa, A., Armstrong, J., Arnould, T., Arsov, I., Asanuma, K., Askanas, V., Asselin, E., Atarashi, R., Atherton, S., Atkin, J., Attardi, L., Auberger, P., Auburger, G., Aurelian, L., Autelli, R., Avagliano, L., Avantaggiati, M., Avrahami, L., Awale, S., Azad, N., Bachetti, T., Backer, J., Bae, D., Bae, J., Bae, O., Bae, S., Baehrecke, E., Baek, S., Baghdiguian, S., Bagniewska-Zadworna, A., Bai, H., Bai, J., Bai, X., Bailly, Y., Balaji, K., Balduini, W., Ballabio, A., Balzan, R., Banerjee, R., Bánhegyi, G., Bao, H., Barbeau, B., Barrachina, M., Barreiro, E., Bartel, B., Bartolomé, A., Bassham, D., Bassi, M., Bast, R., Basu, A., Batista, M., Batoko, H., Battino, M., Bauckman, K., Baumgarner, B., Bayer, K., Beale, R., Beaulieu, J., Beck, G., Becker, C., Beckham, J., Bédard, P., Bednarski, P., Begley, T., Behl, C., Behrends, C., Behrens, G., Behrns, K., Bejarano, E., Belaid, A., Belleudi, F., Bénard, G., Berchem, G., Bergamaschi, D., Bergami, M., Berkhout, B., Berliocchi, L., Bernard, A., Bernard, M., Bernassola, F., Bertolotti, A., Bess, A., Besteiro, S., Bettuzzi, S., Bhalla, S., Bhattacharyya, S., Bhutia, S., Biagosch, C., Bianchi, M., Biard-Piechaczyk, M., Billes, V., Bincoletto, C., Bingol, B., Bird, S., Bitoun, M., Bjedov, I., Blackstone, C., Blanc, L., Blanco, G., Blomhoff, H., Boada-Romero, E., Böckler, S., Boes, M., Boesze-Battaglia, K., Boise, L., Bolino, A., Boman, A., Bonaldo, P., Bordi, M., Bosch, J., Botana, L., Botti, J., Bou, G., Bouché, M., Bouchecareilh, M., Boucher, M., Boulton, M., Bouret, S., Boya, P., Boyer-Guittaut, M., Bozhkov, P., Brady, N., Braga, V., Brancolini, C., Braus, G., Bravo-San Pedro, J., Brennan, L., Bresnick, E., Brest, P., Bridges, D., Bringer, M., Brini, M., 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Charlie, Dong, Xiaonan, Dong, Zheng, Donohue, Terrence M, Doran, Kelly S, D'Orazi, Gabriella, Dorn, Gerald W, Dosenko, Victor, Dridi, Sami, Drucker, Liat, Du, Jie, Du, Li Lin, Du, Lihuan, du Toit, André, Dua, Priyamvada, Duan, Lei, Duann, Pu, Dubey, Vikash Kumar, Duchen, Michael R, Duchosal, Michel A, Duez, Helene, Dugail, Isabelle, Dumit, Verónica I, Duncan, Mara C, Dunlop, Elaine A, Dunn, William A, Dupont, Nicola, Dupuis, Luc, Durán, Raúl V, Durcan, Thomas M, Duvezin Caubet, Stéphane, Duvvuri, Umamaheswar, Eapen, Vinay, Ebrahimi Fakhari, Dariu, Echard, Arnaud, Eckhart, Leopold, Edelstein, Charles L, Edinger, Aimee L, Eichinger, Ludwig, Eisenberg, Tobia, Eisenberg Lerner, Avital, Eissa, N. Tony, El Deiry, Wafik S, El Khoury, Victoria, Elazar, Zvulun, Eldar Finkelman, Hagit, Elliott, Chris Jh, Emanuele, Enzo, Emmenegger, Urban, Engedal, Nikolai, Engelbrecht, Anna Mart, Engelender, Simone, Enserink, Jorrit M, Erdmann, Ralf, Erenpreisa, Jekaterina, Eri, Rajaraman, Eriksen, Jason L, Erman, Andreja, Escalante, Ricardo, Eskelinen, Eeva Liisa, Espert, Lucile, Esteban Martínez, Lorena, Evans, Thomas J, Fabri, Mario, Fabrias, Gemma, Fabrizi, Cinzia, Facchiano, Antonio, Færgeman, Nils J, Faggioni, Alberto, Fairlie, W. Dougla, Fan, Chunhai, Fan, Daping, Fan, Jie, Fang, Shengyun, Fanto, Manoli, Fanzani, Alessandro, Farkas, Thoma, Faure, Mathia, Favier, Francois B, Fearnhead, Howard, Federici, Massimo, Fei, Erkang, Felizardo, Tania C, Feng, Hua, Feng, Yibin, Feng, Yuchen, Ferguson, Thomas A, Fernández, Álvaro F, Fernandez Barrena, Maite G, Fernandez Checa, Jose C, Fernández López, Arsenio, Fernandez Zapico, Martin E, Feron, Olivier, Ferraro, Elisabetta, Ferreira Halder, Carmen Veríssima, Fesus, Laszlo, Feuer, Ralph, Fiesel, Fabienne C, Filippi Chiela, Eduardo C, Filomeni, Giuseppe, Fimia, Gian Maria, Fingert, John H, Finkbeiner, Steven, Finkel, Toren, Fiorito, Filomena, Fisher, Paul B, Flajolet, Marc, Flamigni, Flavio, Florey, Oliver, Florio, Salvatore, Floto, R. 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Shieh, Jj, Shih, Cm, Shimada, Y, Shimizu, S, Shin, Dw, Shinohara, Ml, Shintani, M, Shintani, T, Shioi, T, Shirabe, K, Shiri Sverdlov, R, Shirihai, O, Shore, Gc, Shu, Cw, Shukla, D, Sibirny, Aa, Sica, V, Sigurdson, Cj, Sigurdsson, Em, Sijwali, P, Sikorska, B, Silveira, Wa, Silvente Poirot, S, Silverman, Ga, Simak, J, Simmet, T, Simon, Ak, Simon, Hu, Simone, C, Simons, M, Simonsen, A, Singh, R, Singh, Sv, Singh, Sk, Sinha, D, Sinha, S, Sinicrope, Fa, Sirko, A, Sirohi, K, Sishi, Bj, Sittler, A, Siu, Pm, Sivridis, E, Skwarska, A, Slack, R, Slaninová, I, Slavov, N, Smaili, S, Smalley, K, Smith, Dr, Soenen, Sj, Soleimanpour, Sa, Solhaug, A, Somasundaram, K, Son, Jh, Sonawane, A, Song, C, Song, F, Song, Hk, Song, Jx, Song, W, Soo, Ky, Sood, Ak, Soong, Tw, Soontornniyomkij, V, Sorice, M, Sotgia, F, Soto Pantoja, Dr, Sotthibundhu, A, Sousa, Mj, Spaink, Hp, Span, Pn, Spang, A, Sparks, Jd, Speck, Pg, Spector, Sa, Spies, Cd, Springer, W, Clair, D, Stacchiotti, A, Staels, B, Stang, Mt, 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Taylor, Ga, Taylor, Jp, Taylor, Mj, Tchetina, Ev, Tee, Ar, Teixeira Clerc, F, Telang, S, Tencomnao, T, Teng, Bb, Teng, Rj, Terro, F, Tettamanti, G, Theiss, Al, Theron, Ae, Thomas, Kj, Thomé, Mp, Thomes, Pg, Thorburn, A, Thorner, J, Thum, T, Thumm, M, Thurston, Tl, Tian, L, Till, A, Ting, Jp, Titorenko, Vi, Toker, L, Toldo, S, Tooze, Sa, Topisirovic, I, Torgersen, Ml, Torosantucci, L, Torriglia, A, Torrisi, Mr, Tournier, C, Towns, R, Trajkovic, V, Travassos, Lh, Triola, G, Tripathi, Dn, Trisciuoglio, D, Troncoso, R, Trougakos, Ip, Truttmann, Ac, Tsai, Kj, Tschan, Mp, Tseng, Yh, Tsukuba, T, Tsung, A, Tsvetkov, A, Tu, S, Tuan, Hy, Tucci, M, Tumbarello, Da, Turk, B, Turk, V, Turner, Rf, Tveita, Aa, Tyagi, Sc, Ubukata, M, Uchiyama, Y, Udelnow, A, Ueno, T, Umekawa, M, Umemiya Shirafuji, R, Underwood, Br, Ungermann, C, Ureshino, Rp, Ushioda, R, Uversky, Vn, Uzcátegui, Nl, Vaccari, T, Vaccaro, Mi, Váchová, L, Vakifahmetoglu Norberg, H, Valdor, R, Valente, Em, Vallette, F, Valverde, Am, Van den Berghe, G, Van Den Bosch, L, van den Brink, Gr, van der Goot, Fg, van der Klei, Ij, van der Laan, Lj, van Doorn, Wg, van Egmond, M, van Golen, Kl, Van Kaer, L, van Lookeren Campagne, M, Vandenabeele, P, Vandenberghe, W, Vanhorebeek, I, Varela Nieto, I, Vasconcelos, Mh, Vasko, R, Vavvas, Dg, Vega Naredo, I, Velasco, G, Velentzas, Ad, Velentzas, Pd, Vellai, T, Vellenga, E, Vendelbo, Mh, Venkatachalam, K, Ventura, N, Ventura, S, Veras, P, Verdier, M, Vertessy, Bg, Viale, A, Vidal, M, Vieira, H, Vierstra, Rd, Vigneswaran, N, Vij, N, Vila, M, Villar, M, Villar, Vh, Villarroya, J, Vindis, C, Viola, G, Viscomi, Mt, Vitale, G, Vogl, Dt, Voitsekhovskaja, Ov, von Haefen, C, von Schwarzenberg, K, Voth, De, Vouret Craviari, V, Vuori, K, Vyas, Jm, Waeber, C, Walker, Cl, Walker, Mj, Walter, J, Wan, L, Wan, X, Wang, B, Wang, C, Wang, Cy, Wang, D, Wang, F, Wang, G, Wang, Hj, Wang, H, Wang, Hg, Wang, Hd, Wang, J, Wang, M, Wang, Mq, Wang, Py, Wang, P, Wang, Rc, Wang, S, Wang, Tf, Wang, X, Wang, Xj, Wang, Xw, Wang, Y, Wang, Yj, Wang, Yt, Wang, Zn, Wappner, P, Ward, C, Ward, Dm, Warnes, G, Watada, H, Watanabe, Y, Watase, K, Weaver, Te, Weekes, Cd, Wei, J, Weide, T, Weihl, Cc, Weindl, G, Weis, Sn, Wen, L, Wen, X, Wen, Y, Westermann, B, Weyand, Cm, White, Ar, White, E, Whitton, Jl, Whitworth, Aj, Wiels, J, Wild, F, Wildenberg, Me, Wileman, T, Wilkinson, D, Wilkinson, S, Willbold, D, Williams, C, Williams, K, Williamson, Pr, Winklhofer, Kf, Witkin, S, Wohlgemuth, Se, Wollert, T, Wolvetang, Ej, Wong, E, Wong, Gw, Wong, Rw, Wong, Vk, Woodcock, Ea, Wright, Kl, Wu, C, Wu, D, Wu, G, Wu, J, Wu, M, Wu, S, Wu, Wk, Wu, Y, Wu, Z, Xavier, Cp, Xavier, Rj, Xia, Gx, Xia, T, Xia, W, Xia, Y, Xiao, H, Xiao, J, Xiao, S, Xiao, W, Xie, Cm, Xie, Z, Xilouri, M, Xiong, Y, Xu, C, Xu, F, Xu, H, Xu, J, Xu, L, Xu, X, Xu, Y, Xu, Zx, Xu, Z, Xue, Y, Yamada, T, Yamamoto, A, Yamanaka, K, Yamashina, S, Yamashiro, S, Yan, B, Yan, X, Yan, Z, Yanagi, Y, Yang, D, Yang, Jm, Yang, L, Yang, M, Yang, Pm, Yang, P, Yang, Q, Yang, W, Yang, Wy, Yang, X, Yang, Y, Yang, Z, Yao, Mc, Yao, Pj, Yao, X, Yao, Z, Yasui, L, Ye, M, Yedvobnick, B, Yeganeh, B, Yeh, E, Yeyati, Pl, Yi, F, Yi, L, Yin, Xm, Yip, Ck, Yoo, Ym, Yoo, Yh, Yoon, Sy, Yoshida, Ki, Yoshimori, T, Young, Kh, Yu, H, Yu, Jj, Yu, Jt, Yu, J, Yu, L, Yu, Wh, Yu, Xf, Yu, Z, Yuan, J, Yuan, Zm, Yue, By, Yue, J, Yue, Z, Zacks, Dn, Zacksenhaus, E, Zaffaroni, N, Zaglia, T, Zakeri, Z, Zecchini, V, Zeng, J, Zeng, M, Zeng, Q, Zervos, A, Zhang, Dd, Zhang, F, Zhang, G, Zhang, Gc, Zhang, H, Zhang, J, Zhang, Jp, Zhang, L, Zhang, My, Zhang, X, Zhang, Xd, Zhang, Y, Zhao, M, Zhao, Wl, Zhao, X, Zhao, Yg, Zhao, Y, Zhao, Yx, Zhao, Z, Zhao, Zj, Zheng, D, Zheng, Xl, Zheng, X, Zhivotovsky, B, Zhong, Q, Zhou, Gz, Zhou, G, Zhou, H, Zhou, Sf, Zhou, Xj, Zhu, H, Zhu, Wg, Zhu, W, Zhu, Xf, Zhu, Y, Zhuang, Sm, Zhuang, X, Ziparo, E, Zois, Ce, Zoladek, T, Zong, Wx, Zorzano, A, Zughaier, Sm, AII - Amsterdam institute for Infection and Immunity, Medical Microbiology and Infection Prevention, Other departments, CCA -Cancer Center Amsterdam, Center of Experimental and Molecular Medicine, Radiotherapy, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Medical Biochemistry, ANS - Cellular & Molecular Mechanisms, Cell Biology and Histology, Gastroenterology and Hepatology, Tytgat Institute for Liver and Intestinal Research, Daniel J Klionsky, Kotb Abdelmohsen, Akihisa Abe, Md Joynal Abedin, Hagai Abeliovich, Abraham Acevedo Arozena, Hiroaki Adachi, Christopher M Adam, Peter D Adam, Khosrow Adeli, Peter J Adhihetty, Sharon G Adler, Galila Agam, Rajesh Agarwal, Manish K Aghi, Maria Agnello, Patrizia Agostini, Patricia V Aguilar, Julio Aguirre-Ghiso, Edoardo M Airoldi, Slimane Ait-Si-Ali, Takahiko Akematsu, Emmanuel T Akporiaye, Mohamed Al-Rubeai, Guillermo M Albaiceta, Chris Albanese, Diego Albani, Matthew L Albert, Jesus Aldudo, Hana Algül, Mehrdad Alirezaei, Iraide Alloza, Alexandru Almasan, Maylin Almonte-Beceril, Emad S Alnemri, Covadonga Alonso, Nihal Altan-Bonnet, Dario C Altieri, Silvia Alvarez, Lydia Alvarez- Erviti, Sandro Alve, Giuseppina Amadoro, Atsuo Amano, Consuelo Amantini, Santiago Ambrosio, Ivano Amelio, Amal O Amer, Mohamed Amessou, Angelika Amon, Zhenyi An, Frank A Anania, Stig U Andersen, Usha P Andley, Catherine K Andreadi, Nathalie Andrieu- Abadie, Alberto Anel, David K Ann, Shailendra Anoopkumar-Dukie, Manuela Antonioli, Hiroshi Aoki, Nadezda Apostolova, Saveria Aquila, Katia Aquilano, Koichi Araki, Eli Arama, Agustin Aranda, Jun Araya, Alexandre Arcaro, Esperanza Aria, Hirokazu Arimoto, Aileen R Ariosa, Jane L Armstrong, Thierry Arnould, Ivica Arsov, Katsuhiko Asanuma, Valerie Askana, Eric Asselin, Ryuichiro Atarashi, Sally S Atherton, Julie D Atkin, Laura D Attardi, Patrick Auberger, Georg Auburger, Laure Aurelian, Riccardo Autelli, Laura Avagliano, Maria Laura Avantaggiati, Limor Avrahami, Suresh Awale, Neelam Azad, Tiziana Bachetti, Jonathan M Backer, Dong- Hun Bae, Jae-sung Bae, Ok-Nam Bae, Soo Han Bae, Eric H Baehrecke, Seung-Hoon Baek, Stephen Baghdiguian, Agnieszka Bagniewska-Zadworna, Hua Bai, Jie Bai, Xue-Yuan Bai, Yannick Bailly, Kithiganahalli Narayanaswamy Balaji, Walter Balduini, Andrea Ballabio, Rena Balzan, Rajkumar Banerjee, Gábor Bánhegyi, Haijun Bao, Benoit Barbeau, Maria D Barrachina, Esther Barreiro, Bonnie Bartel, Alberto Bartolomé, Diane C Bassham, Maria Teresa Bassi, Robert C Bast Jr, Alakananda Basu, Maria Teresa Batista, Henri Batoko, Maurizio Battino, Kyle Bauckman, Bradley L Baumgarner, K Ulrich Bayer, Rupert Beale, Jean-François Beaulieu, George R. Beck Jr, Christoph Becker, J David Beckham, Pierre-André Bédard, Patrick J Bednarski, Thomas J Begley, Christian Behl, Christian Behrend, Georg MN Behren, Kevin E Behrn, Eloy Bejarano, Amine Belaid, Francesca Belleudi, Giovanni Bénard, Guy Berchem, Daniele Bergamaschi, Matteo Bergami, Ben Berkhout, Laura Berliocchi, Amélie Bernard, Monique Bernard, Francesca Bernassola, Anne Bertolotti, Amanda S Be, Sébastien Besteiro, Saverio Bettuzzi, Savita Bhalla, Shalmoli Bhattacharyya, Sujit K Bhutia, Caroline Biagosch, Michele Wolfe Bianchi, Martine Biard-Piechaczyk, Viktor Bille, Claudia Bincoletto, Baris Bingol, Sara W Bird, Marc Bitoun, Ivana Bjedov, Craig Blackstone, Lionel Blanc, Guillermo A Blanco, Heidi Kiil Blomhoff, Emilio Boada-Romero, Stefan Böckler, Marianne Boe, Kathleen Boesze-Battaglia, Lawrence H Boise, Alessandra Bolino, Andrea Boman, Paolo Bonaldo, Matteo Bordi, Jürgen Bosch, Luis M Botana, Joelle Botti, German Bou, Marina Bouché, Marion Bouchecareilh, Marie- Josée Boucher, Michael E Boulton, Sebastien G Bouret, Patricia Boya, Michaël Boyer-Guittaut, Peter V Bozhkov, Nathan Brady, Vania MM Braga, Claudio Brancolini, Gerhard H Brau, José M Bravo-San Pedro, Lisa A Brennan, Emery H Bresnick, Patrick Brest, Dave Bridge, MarieAgnès Bringer, Marisa Brini, Glauber C Brito, Bertha Brodin, Paul S Brooke, Eric J Brown, Karen Brown, Hal E Broxmeyer, Alain Bruhat, Patricia Chakur Brum, John H Brumell, Nicola Brunetti-Pierri, Robert J Bryson-Richardson, Shilpa Buch, Alastair M Buchan, Hikmet Budak, Dmitry V Bulavin, Scott J Bultman, Geert Bultynck, Vladimir Bumbasirevic, Yan Burelle, Robert E Burke, Margit Burmeister, Peter Bütikofer, Laura Caberlotto, Ken Cadwell, Monika Cahova, Dongsheng Cai, Jingjing Cai, Qian Cai, Sara Calatayud, Nadine Camougrand, Michelangelo Campanella, Grant R Campbell, Matthew Campbell, Silvia Campello, Robin Candau, Isabella Caniggia, Lavinia Cantoni, Lizhi Cao, Allan B Caplan, Michele Caraglia, Claudio Cardinali, Sandra Morais Cardoso, Jennifer S Carew, Laura A Carleton, Cathleen R Carlin, Silvia Carloni, Sven R Carlsson, Didac Carmona-Gutierrez, Leticia AM Carneiro, Oliana Carnevali, Serena Carra, Alice Carrier, Bernadette Carroll, Caty Casa, Josefina Casa, Giuliana Cassinelli, Perrine Castet, Susana Castro-Obregon, Gabriella Cavallini, Isabella Ceccherini, Francesco Cecconi, Arthur I Cederbaum, Valentín Ceña, Simone Cenci, Claudia Cerella, Davide Cervia, Silvia Cetrullo, Hassan Chaachouay, Han-Jung Chae, Andrei S Chagin, Chee-Yin Chai, Gopal Chakrabarti, Georgios Chamilo, Edmond YW Chan, Matthew TV Chan, Dhyan Chandra, Pallavi Chandra, Chih-Peng Chang, Raymond Chuen-Chung Chang, Ta Yuan Chang, John C Chatham, Saurabh Chatterjee, Santosh Chauhan, Yongsheng Che, Michael E Cheetham, Rajkumar Cheluvappa, Chun-Jung Chen, Gang Chen, Guang-Chao Chen, Guoqiang Chen, Hongzhuan Chen, Jeff W Chen, Jian-Kang Chen, Min Chen, Mingzhou Chen, Peiwen Chen, Qi Chen, Quan Chen, Shang- Der Chen, Si Chen, Steve S-L Chen, Wei Chen, 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Vincent CO Njar, Takeshi Noda, Angelika A Noegel, Elsie Magdalena Nolte, Erik Norberg, Koenraad K Norga, Sakineh Kazemi Noureini, Shoji Notomi, Lucia Notterpek, Karin Nowikovsky, Nobuyuki Nukina, Thorsten Nürnberger, Valerie B O'Donnell, Tracey O'Donovan, Peter J O'Dwyer, Ina Oehme, Clara L Oeste, Michinaga Ogawa, Besim Ogretmen, Yuji Ogura, Young J Oh, Masaki Ohmuraya, Takayuki Ohshima, Rani Ojha, Koji Okamoto, Toshiro Okazaki, F Javier Oliver, Karin Ollinger, Stefan Olsson, Daniel P Orban, Paulina Ordonez, Idil Orhon, Laszlo Orosz, Eyleen J O'Rourke, Helena Orozco, Angel L Ortega, Elena Ortona, Laura D Osellame, Junko Oshima, Shigeru Oshima, Heinz D Osiewacz, Takanobu Otomo, Kinya Otsu, Jing-hsiung James Ou, Tiago F Outeiro, Dong-yun Ouyang, Hongjiao Ouyang, Michael Overholtzer, Michelle A Ozbun, P Hande Ozdinler, Bulent Ozpolat, Consiglia Pacelli, Paolo Paganetti, Guylène Page, Gilles Page, Ugo Pagnini, Beata Pajak, Stephen C Pak, Karolina Pakos-Zebrucka, Nazzy Pakpour, Zdena 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Subjects
[SDV]Life Sciences [q-bio], autophagosome, Review Article, ddc:616.07, stress, stre, LC3, MESH: Animals, Settore MED/49 - Scienze Tecniche Dietetiche Applicate, Settore BIO/06 - Anatomia Comparata E Citologia, chaperone-mediated autophagy, ComputingMilieux_MISCELLANEOUS, Settore BIO/11, Pharmacology. Therapy, Settore BIO/13, standards [Biological Assay], autolysosome, MESH: Autophagy*/physiology, lysosome, methods [Biological Assay], Biological Assay, Settore BIO/17 - ISTOLOGIA, Erratum, Human, Biochemistry & Molecular Biology, Settore BIO/06, physiology [Autophagy], Chaperonemediated autophagy, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, NO, autophagy, guidelines, molecular biology, ultrastructure, flux, macroautophagy, phagophore, vacuole, MESH: Biological Assay/methods, MESH: Computer Simulation, ddc:570, Autolysosome, Autophagosome, Chaperonemediated autophagy, Flux, LC3, Lysosome, Macroautophagy, Phagophore, Stress, Vacuole, Autophagy, Animals, Humans, Computer Simulation, Settore BIO/10, ddc:612, Biology, MESH: Humans, Animal, 0601 Biochemistry And Cell Biology, MESH: Biological Assay/standards, Human medicine
Abstract

Seuls les 100 premiers auteurs dont les auteurs INRA ont été entrés dans la notice. La liste complète des auteurs et de leurs affiliations est accessible sur la publication.; International audience; In 2008 we published the first set of guidelines for standardizing research in autophagy. Since then, research on this topic has continued to accelerate, and many new scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Accordingly, it is important to update these guidelines for monitoring autophagy in different organisms. Various reviews have described the range of assays that have been used for this purpose. Nevertheless, there continues to be confusion regarding acceptable methods to measure autophagy, especially in multicellular eukaryotes.For example, a key point that needs to be emphasized is that there is a difference between measurements that monitor the numbers or volume of autophagic elements (e.g., autophagosomes or autolysosomes) at any stage of the autophagic process versus those that measure flux through the autophagy pathway (i.e., the complete process including the amount and rate of cargo sequestered and degraded). In particular, a block in macroautophagy that results in autophagosome accumulation must be differentiated from stimuli that increase autophagic activity, defined as increased autophagy induction coupled with increased delivery to, and degradation within, lysosomes (in most higher eukaryotes and some protists such as Dictyostelium) or the vacuole (in plants and fungi). In other words, it is especially important that investigators new to the field understand that the appearance of more autophagosomes does not necessarily equate with more autophagy. In fact, in many cases, autophagosomes accumulate because of a block in trafficking to lysosomes without a concomitant change in autophagosome biogenesis, whereas an increase in autolysosomes may reflect a reduction in degradative activity. It is worth emphasizing here that lysosomal digestion is a stage of autophagy and evaluating its competence is a crucial part of the evaluation of autophagic flux, or complete autophagy.Here, we present a set of guidelines for the selection and interpretation of methods for use by investigators who aim to examine macroautophagy and related processes, as well as for reviewers who need to provide realistic and reasonable critiques of papers that are focused on these processes. These guidelines are not meant to be a formulaic set of rules, because the appropriate assays depend in part on the question being asked and the system being used. In addition, we emphasize that no individual assay is guaranteed to be the most appropriate one in every situation, and we strongly recommend the use of multiple assays to monitor autophagy. Along these lines, because of the potential for pleiotropic effects due to blocking autophagy through genetic manipulation, it is imperative to target by gene knockout or RNA interference more than one autophagy-related protein. In addition, some individual Atg proteins, or groups of proteins, are involved in other cellular pathways implying that not all Atg proteins can be used as a specific marker for an autophagic process. In these guidelines, we consider these various methods of assessing autophagy and what information can, or cannot, be obtained from them. Finally, by discussing the merits and limits of particular assays, we hope to encourage technical innovation in the field.

Published
2016
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33. microRNA 125a Regulates MHC-I Expression on Esophageal Adenocarcinoma Cells, Associated With Suppression of Antitumor Immune Response and Poor Outcomes of Patients

Author

Sybren L. Meijer, Kausilia K. Krishnadath, Jacques J. Bergman, Francesca Milano, Silvia Calpe, Maria del Carmen Sancho Serra, Sanne Hoefnagel, S S Gisbertz, Luigi Mari, Marian van de Meent, Maarten C.C.M. Hulshof, Mirjam H.M. Heemskerk, Jan Paul Medema, Mark I. van Berge Henegouwen, Domenico Zito, Hanneke W. M. van Laarhoven, Peter van Endert, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Graduate School, CCA - Cancer biology and immunology, AGEM - Re-generation and cancer of the digestive system, Center of Experimental and Molecular Medicine, Gastroenterology and Hepatology, Oncology, Radiotherapy, Surgery, and Pathology

Subjects
0301 basic medicine, Member 3, Esophageal Neoplasms, ATP Binding Cassette Transporter, Antigen presentation, Biology, Adaptive Immunity, Adenocarcinoma, Major histocompatibility complex, Cell Line, 03 medical and health sciences, 0302 clinical medicine, Immune system, ATP Binding Cassette Transporter, Subfamily B, Member 3, Cell Line, Tumor, MHC class I, Cytotoxic T cell, Humans, Antitumor Immune Response, Immune Checkpoints, miR-125, miR-148, 3' Untranslated Regions, DNA-Binding Proteins, MicroRNAs, Transcription Factors, Tumor, Hepatology, Gastroenterology, Acquired immune system, Immune checkpoint, 030104 developmental biology, Subfamily B, CTLA-4, 030220 oncology & carcinogenesis, biology.protein, Cancer research
Abstract

Background & Aims Immune checkpoint inhibition may affect growth or progression of highly aggressive cancers, such as esophageal adenocarcinoma (EAC). We investigated the regulation of expression of major histocompatibility complex, class 1 (MHC-I) proteins (encoded by HLA-A, HLA-B, and HLA-C) and the immune response to EACs in patient samples. Methods We performed quantitative polymerase chain reaction array analyses of OE33 cells and OE19 cells, which express different levels of the ATP binding cassette subfamily B member 1 (TAP1) and TAP2, required for antigen presentation by MHC-I, to identify microRNAs (miRNAs) that regulate their expression. We performed luciferase assays to validate interactions between miRNAs and potential targets. We overexpressed candidate miRNAs in OE33, FLO-1, and OACP4 C cell lines and performed quantitative polymerase chain reaction, immunoblot, and flow cytometry analyses to identify changes in messenger RNA (mRNA) and protein expression; we studied the effects of cytotoxic T cells. We performed miRNA in situ hybridization, RNA-sequencing, and immunohistochemical analyses of tumor tissues from 51 untreated patients with EAC in the Netherlands. Clinical and survival data were collected for patients, and EAC subtypes were determined. Results We found OE19 cells to have increased levels of 7 miRNAs. Of these, we found binding sites for miRNA 125a (MIR125a)-5p in the 3′ untranslated region of the TAP2 mRNA and binding sites for MIR148a-3p in 3′ untranslated regions of HLA-A, HLA-B, and HLA-C mRNAs. Overexpression of these miRNAs reduced expression of TAP2 in OE33, FLO-1, and OACP4 C cells, and reduced cell-surface levels of MHC-I. OE33 cells that expressed the viral peptide BZLF1 were killed by cytotoxic T cells, whereas OE33 that overexpressed MIR125a-5p or MIR 148a along with BZLF1 were not. In EAC and nontumor tissues, levels of MIR125a-5p correlated inversely with levels of TAP2 protein. High expression of TAP1 by EAC correlated with significantly shorter overall survival times of patients. EACs that expressed high levels of TAP1 and genes involved in antigen presentation also expressed high levels of genes that regulate the adaptive immune response, PD-L1, PD-L2, and IDO1; these EACs had a poor response to neoadjuvant chemoradiotherapy and associated with shorter overall survival times of patients. Conclusions In studies of EAC cell lines and tumor tissues, we found increased levels of MIR125a-5p and MIR148a-3p to reduce levels of TAP2 and MHC-I, required for antigen presentation. High expression of MHC-I molecules by EAC correlated with markers of an adaptive immune response and significantly shorter overall survival times of patients.

Published
2017

34. Prostate Cancer Patients with Late Radiation Toxicity Exhibit Reduced Expression of Genes Involved in DNA Double-Strand Break Repair and Homologous Recombination

Author

Bregje van Oorschot, Lukas J.A. Stalpers, Perry D. Moerland, L. Uitterhoeve, Jan Paul Medema, Harry Vrieling, Ilja Oomen, Rosemarie ten Cate, Nicolaas A. P. Franken, Center of Experimental and Molecular Medicine, CCA - Cancer biology and immunology, Radiotherapy, CCA -Cancer Center Amsterdam, Other Research, APH - Methodology, APH - Personalized Medicine, and Epidemiology and Data Science

Subjects
0301 basic medicine, Male, Cancer Research, Pathology, medicine.medical_specialty, medicine.medical_treatment, Biology, Histones, 03 medical and health sciences, Prostate cancer, 0302 clinical medicine, Gene expression, medicine, Biomarkers, Tumor, Humans, DNA Breaks, Double-Stranded, Prospective Studies, Prospective cohort study, Homologous Recombination, Radiation Injuries, Aged, Aged, 80 and over, Prostatic Neoplasms, Recombinational DNA Repair, Retrospective cohort study, Middle Aged, medicine.disease, Prognosis, Double Strand Break Repair, Radiation therapy, 030104 developmental biology, DNA Repair Enzymes, Oncology, 030220 oncology & carcinogenesis, Toxicity, Cancer research, Neoplasm Grading, Homologous recombination, Follow-Up Studies
Abstract

Severe late damage to normal tissue is a major limitation of cancer radiotherapy in prostate cancer patients. In a recent retrospective study, late radiation toxicity was found to relate to a decreased decay of γ-H2AX foci and reduced induction of DNA double-strand break repair genes. Here, we report evidence of prognostic utility in prostate cancer for γ-H2AX foci decay ratios and gene expression profiles derived from ex vivo–irradiated patient lymphocytes. Patients were followed ≥2 years after radiotherapy. Clinical characteristics were assembled, and toxicity was recorded using the Common Terminology Criteria (CTCAE) v4.0. No clinical factor was correlated with late radiation toxicity. The γ-H2AX foci decay ratio correlated negatively with toxicity grade, with a significant difference between grade ≥3 and grade 0 patients (P = 0.02). A threshold foci decay ratio, determined in our retrospective study, correctly classified 23 of 28 patients with grade ≥3 toxicity (sensitivity 82%) and 9 of 14 patients with grade 0 toxicity (specificity 64%). Induction of homologous recombination (HR) repair genes was reduced with increasing toxicity grade. The difference in fold induction of the HR gene set was most pronounced between grade 0 and grade ≥3 toxicity (P = 0.008). Notably, reduced responsiveness of HR repair genes to irradiation and inefficient double-strand break repair correlated with severe late radiation toxicity. Using a decay ratio classifier, we correctly classified 82% of patients with grade ≥3 toxicity, suggesting a prognostic biomarker for cancer patients with a genetically enhanced risk for late radiation toxicity to normal tissues after radiotherapy. Cancer Res; 77(6); 1485–91. ©2017 AACR.

Published
2017

35. Expression and Function of Granzymes A and B in Escherichia coli Peritonitis and Sepsis

Author

Jan Paul Medema, Sanne Terpstra, Cornelis van 't Veer, Sandrine Florquin, M. Isabel García-Laorden, Tom van der Poll, Ingrid Stroo, Alex F. de Vos, Pathology, Amsterdam institute for Infection and Immunity, AII - Infectious diseases, Cancer Center Amsterdam, Radiotherapy, Amsterdam Cardiovascular Sciences, Center of Experimental and Molecular Medicine, Infectious diseases, and ACS - Pulmonary hypertension & thrombosis

Subjects
Male, 0301 basic medicine, Proteases, Article Subject, Immunology, Peritonitis, medicine.disease_cause, Granzymes, GZMB, Microbiology, Sepsis, Mice, 03 medical and health sciences, In vivo, Escherichia coli, medicine, Pathology, lcsh:Pathology, Animals, RB1-214, Pathogen, biology, Cell Biology, medicine.disease, Nucleosomes, 3. Good health, Mice, Inbred C57BL, 030104 developmental biology, Neutrophil Infiltration, Granzyme, biology.protein, Female, Research Article, lcsh:RB1-214
Abstract

Escherichia(E.)coliis the most common causative pathogen in peritonitis, the second most common cause of sepsis. Granzymes (gzms) are serine proteases traditionally implicated in cytotoxicity and, more recently, in the inflammatory response. We here sought to investigate the role of gzms in the host response toE. coli-induced peritonitis and sepsis in vivo. For this purpose, we used a murine model ofE. coliintraperitoneal infection, resembling the clinical condition commonly associated with septic peritonitis by this bacterium, in wild-type and gzmA-deficient (gzmA−/−),gzmB−/−, andgzmAxB−/−mice. GzmA and gzmB were predominantly expressed by natural killer cells, and during abdominal sepsis, the percentage of these cells expressing gzms in peritoneal lavage fluid decreased, while the amount of expression in the gzm+cells increased. Deficiency of gzmA and/or gzmB was associated with increased bacterial loads, especially in the case of gzmB at the primary site of infection at late stage sepsis. While gzm deficiency did not impact neutrophil recruitment into the abdominal cavity, it was accompanied by enhanced nucleosome release at the primary site of infection, earlier hepatic necrosis, and more renal dysfunction. These results suggest that gzms influence bacterial growth and the host inflammatory response during abdominal sepsis caused byE. coli.

Published
2017
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36. Intra-tumor heterogeneity from a cancer stem cell perspective

Author

Jan Paul Medema and Pramudita R. Prasetyanti

Subjects
0301 basic medicine, Oncology, Tumor heterogeneity, Cancer Research, medicine.medical_specialty, Epithelial-Mesenchymal Transition, Cancer therapy, Review, Biology, Models, Biological, Epigenesis, Genetic, Genetic Heterogeneity, 03 medical and health sciences, Cancer stem cell, Neoplasms, Internal medicine, medicine, Humans, Stemness, Tumor microenvironment, Cluster of differentiation, Cancer, Cell Differentiation, medicine.disease, Phenotype, 030104 developmental biology, Apoptosis, Disease Progression, Neoplastic Stem Cells, Molecular Medicine
Abstract

Tumor heterogeneity represents an ongoing challenge in the field of cancer therapy. Heterogeneity is evident between cancers from different patients (inter-tumor heterogeneity) and within a single tumor (intra-tumor heterogeneity). The latter includes phenotypic diversity such as cell surface markers, (epi)genetic abnormality, growth rate, apoptosis and other hallmarks of cancer that eventually drive disease progression and treatment failure. Cancer stem cells (CSCs) have been put forward to be one of the determining factors that contribute to intra-tumor heterogeneity. However, recent findings have shown that the stem-like state in a given tumor cell is a plastic quality. A corollary to this view is that stemness traits can be acquired via (epi)genetic modification and/or interaction with the tumor microenvironment (TME). Here we discuss factors contributing to this CSC heterogeneity and the potential implications for cancer therapy.

Published
2017
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37. Decreased mitochondrial priming determines chemoresistance of colon cancer stem cells

Author

Leah Hogdal, Pramudita R. Prasetyanti, Evelyn Fessler, Cheryl Zimberlin, Catarina Grandela, Jan Paul Medema, Selcuk Colak, Anthony Letai, Other departments, Center of Experimental and Molecular Medicine, CCA -Cancer Center Amsterdam, Graduate School, and Radiotherapy

Subjects
Programmed cell death, Colorectal cancer, Cell Survival, medicine.medical_treatment, bcl-X Protein, Priming (immunology), Antineoplastic Agents, Apoptosis, Biology, Cancer stem cell, medicine, Tumor Cells, Cultured, Neoplasm, Humans, Molecular Biology, Chemotherapy, Original Paper, Cell Biology, medicine.disease, Mitochondria, Drug Resistance, Neoplasm, Immunology, Colonic Neoplasms, Cancer research, Neoplastic Stem Cells, Stem cell
Abstract

Tumor heterogeneity is in part determined by the existence of cancer stem cells (CSCs) and more differentiated tumor cells. CSCs are considered to be the tumorigenic root of cancers and suggested to be chemotherapy resistant. Here we exploited an assay that allowed us to measure chemotherapy-induced cell death in CSCs and differentiated tumor cells simultaneously. This confirmed that CSCs are selectively resistant to conventional chemotherapy, which we revealed is determined by decreased mitochondrial priming. In agreement, lowering the anti-apoptotic threshold using ABT-737 and WEHI-539 was sufficient to enhance chemotherapy efficacy, whereas ABT-199 failed to sensitize CSCs. Our data therefore point to a crucial role of BCLXL in protecting CSCs from chemotherapy and suggest that BH3 mimetics, in combination with chemotherapy, can be an efficient way to target chemotherapy-resistant CSCs.

Published
2014
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38. Escape from senescence boosts tumour growth

Author

Jan Paul Medema

Subjects
0301 basic medicine, Senescence, 03 medical and health sciences, 030104 developmental biology, 0302 clinical medicine, Multidisciplinary, 030220 oncology & carcinogenesis, medicine, Cancer research, Cancer, Cellular senescence, Biology, medicine.disease
Abstract

Some chemotherapies block cancer growth by driving tumour cells into a state of cell-division arrest termed senescence. It emerges that such cells have a boosted capacity to drive tumour growth if they exit senescence. Some chemotherapies block cancer growth by driving tumour cells into a state of cell-division arrest termed senescence. It emerges that such cells have a boosted capacity to drive tumour growth if they exit senescence.

Published
2017
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39. Cancer stem cell dynamics in tumor progression and metastasis: Is the microenvironment to blame?

Author

Felipe De Sousa E Melo, Evelyn Fessler, Jan Paul Medema, and Feline E. Dijkgraaf

Subjects
Cancer Research, Stromal cell, Cancer, Cell Differentiation, Biology, medicine.disease, Primary tumor, Metastasis, Oncology, Cancer stem cell, Tumor progression, Neoplasms, Cancer cell, Immunology, Neoplastic Stem Cells, Tumor Microenvironment, medicine, Cancer research, Humans, Stromal Cells, Stem cell
Abstract

Stem cells are defined by their self-renewal capacity and the ability to give rise to all differentiated progeny necessary for one specific organ. These two characteristics are also inherent in cancer stem cells (CSCs), which are thought to be the only subpopulation within a tumor endowed with tumorigenic potential. CSCs combine many features that render cancer one of the leading causes of death in the Western world: metastasis, tumor recurrence, and therapy refractoriness. Strikingly, CSCs are not a fixed entity, but differentiated tumor cells are able to revert to a stem-like state. Thus, CSCs are not only intrinsically programmed to fulfill their detrimental roles, but are orchestrated by stromal cells residing in their vicinity and forming the CSC niche. Yet, this relationship is not a one-way road: CSCs are able to manipulate stromal cells to their needs, not only in the primary tumor, but also in distant organs and thus prime the foreign soil for their arrival by inducing a premetastatic niche. The suggested plasticity between the differentiation states of cancer cells and the regulation by microenvironmental cues provides new starting-points for novel cancer therapies. (C) 2012 Elsevier Ireland Ltd. All rights reserved

Published
2013
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40. Cancer stem cells: the challenges ahead

Author

Jan Paul Medema, CCA -Cancer Center Amsterdam, Center of Experimental and Molecular Medicine, and Radiotherapy

Subjects
Cell Biology, Biology, medicine.disease, medicine.disease_cause, Metastasis, Cell biology, Mice, Cancer stem cell, Neoplasms, Cancer research, medicine, Neoplastic Stem Cells, Animals, Humans, Neoplasm Metastasis, Carcinogenesis
Abstract

Cancer stem cells (CSCs) have been proposed as the driving force of tumorigenesis and the seeds of metastases. However, their existence and role remain a topic of intense debate. Recently, the identification of CSCs in endogenously developing mouse tumours has provided further support for this concept. Here I discuss the challenges in identifying CSCs, their dependency on a supportive niche and their role in metastasis, and propose that stemness is a flexible — rather than fixed — quality of tumour cells that can be lost and gained.

Published
2013
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41. Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions

Author

Ronald van Leersum, Joan H. de Jong, Hans M. Rodermond, Marnix Jansen, Jurriaan B. Tuynman, Maarten F. Bijlsma, Evelien Dekker, Felipe De Sousa E Melo, Maartje van der Heijden, Xin Wang, Louis Vermeulen, Jan Paul Medema, Carel J. M. van Noesel, Laura P M H de Rooij, Anne Trinh, Florian Markowetz, Evelyn Fessler, Onno J. de Boer, Pathology, Center of Experimental and Molecular Medicine, AII - Amsterdam institute for Infection and Immunity, CCA -Cancer Center Amsterdam, ACS - Amsterdam Cardiovascular Sciences, Other departments, Radiotherapy, Graduate School, Surgery, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, and Gastroenterology and Hepatology

Subjects
Colorectal cancer, Colonic Polyps, Disease, Biology, medicine.disease_cause, Bioinformatics, General Biochemistry, Genetics and Molecular Biology, Epidermal growth factor, Cell Line, Tumor, medicine, Adjuvant therapy, Humans, Oligonucleotide Array Sequence Analysis, Mutation, Extra Views, Gene Expression Profiling, Microsatellite instability, General Medicine, medicine.disease, Prognosis, Gene expression profiling, Gene Expression Regulation, Neoplastic, CpG site, Gene Expression Regulation, Colonic Neoplasms, Cancer research, CpG Islands, Microsatellite Instability, Microsatellite Repeats
Abstract

Colon cancer is a clinically diverse disease. This heterogeneity makes it difficult to determine which patients will benefit most from adjuvant therapy and impedes the development of new targeted agents. More insight into the biological diversity of colon cancers, especially in relation to clinical features, is therefore needed. We demonstrate, using an unsupervised classification strategy involving over 1,100 individuals with colon cancer, that three main molecularly distinct subtypes can be recognized. Two subtypes have been previously identified and are well characterized (chromosomal-instable and microsatellite-instable cancers). The third subtype is largely microsatellite stable and contains relatively more CpG island methylator phenotype-positive carcinomas but cannot be identified on the basis of characteristic mutations. We provide evidence that this subtype relates to sessile-serrated adenomas, which show highly similar gene expression profiles, including upregulation of genes involved in matrix remodeling and epithelial-mesenchymal transition. The identification of this subtype is crucial, as it has a very unfavorable prognosis and, moreover, is refractory to epidermal growth factor receptor-targeted therapy.

Published
2013
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42. Cancer heterogeneity--a multifaceted view

Author

Jan Paul Medema, Evelyn Fessler, Louis Vermeulen, and Felipe De Sousa E Melo

Subjects
Gene Expression, Review Article, Biology, Bioinformatics, Biochemistry, Somatic evolution in cancer, Subclass, Clonal Evolution, Genetic Heterogeneity, Cancer stem cell, Neoplasms, Genetics, medicine, Tumor Microenvironment, Humans, Tumor type, Molecular Biology, Tumor microenvironment, Genetic heterogeneity, Cancer, Cell Differentiation, medicine.disease, Clone Cells, Neoplasm Proteins, Homogeneous, Organ Specificity, Mutation, Neoplastic Stem Cells
Abstract

Cancers of various organs have been categorized into distinct subtypes after increasingly sophisticated taxonomies. Additionally, within a seemingly homogeneous subclass, individual cancers contain diverse tumour cell populations that vary in important cancer-specific traits such as clonogenicity and invasive potential. Differences that exist between and within a given tumour type have hampered significantly both the proper selection of patients that might benefit from therapy, as well as the development of new targeted agents. In this review, we discuss the differences associated with organ-specific cancer subtypes and the factors that contribute to intra-tumour heterogeneity. It is of utmost importance to understand the biological causes that distinguish tumours as well as distinct tumour cell populations within malignancies, as these will ultimately point the way to more rational anti-cancer treatments.

Published
2013
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43. Inhibition of homologous recombination by hyperthermia shunts early double strand break repair to non-homologous end-joining

Author

Judith W.J. Bergs, Lukas J.A. Stalpers, Hans M. Rodermond, Jaap Haveman, Tijana Borovski, Nicolaas A. P. Franken, Jeroen Essers, Przemek M. Krawczyk, Rosemarie ten Cate, Roland Kanaar, Chris van Bree, Jan Paul Medema, Jan Stap, Jacob A. Aten, Pediatrics, Radiotherapy, Molecular Genetics, Cancer Center Amsterdam, Cell Biology and Histology, Other departments, Other Research, and Center of Experimental and Molecular Medicine

Subjects
G2 Phase, DNA End-Joining Repair, Hot Temperature, Morpholines, Chromosomal translocation, Biology, Radiation Tolerance, Biochemistry, Translocation, Genetic, Mice, 03 medical and health sciences, chemistry.chemical_compound, 0302 clinical medicine, Cell Line, Tumor, medicine, Animals, Humans, DNA Breaks, Double-Stranded, Homologous Recombination, Molecular Biology, 030304 developmental biology, Cisplatin, 0303 health sciences, fungi, Recombinational DNA Repair, Cell Biology, Molecular biology, Double Strand Break Repair, 3. Good health, Non-homologous end joining, enzymes and coenzymes (carbohydrates), chemistry, Chromones, Gamma Rays, 030220 oncology & carcinogenesis, Premature chromosome condensation, Homologous recombination, DNA, medicine.drug
Abstract

In S and G2 phase mammalian cells DNA double strand breaks (DSBs) can potentially be repaired by homologous recombination (HR) or non-homologous end-joining (NHEJ). Results of several studies suggest that these two mechanistically distinct repair pathways can compete for DNA ends. Because HR and NHEJ differ with respect to error susceptibility, generation of chromosome rearrangements, which are potentially carcinogenic products of DSB repair, may depend on the pathway choice. To investigate this hypothesis, the influence of HR and NHEJ inhibition on the frequencies of chromosome aberrations in G2 phase cells was investigated. SW-1573 and RKO cells were treated with mild (41 °C) hyperthermia in order to disable HR and/or NU7441/cisplatin to inactivate NHEJ and frequencies of chromosomal fragments (resulting from unrepaired DSBs) and translocations (products of erroneous DSB rejoining) were studied using premature chromosome condensation (PCC) combined with fluorescence in situ hybridization (FISH). It is shown here that temporary inhibition of HR by hyperthermia results in increased frequency of ionizing-radiation (IR)-induced chromosomal translocations and that this effect is abrogated by NU7441- or cisplatin-mediated inhibition of NHEJ. The results suggest that in the absence of HR, DSB repair is shifted to the error-prone NHEJ pathway resulting in increased frequencies of chromosomal rearrangements. These results might be of consequence for clinical cancer treatment approaches that aim at inhibition of one or more DSB repair pathways.

Published
2013
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44. Chronic lymphocytic leukemia disease progression is accelerated by APRIL-TACI interaction in the TCL1 transgenic mouse model

Author

Erik Slinger, Jan Paul Medema, Jan G. Schot, Jeroen E. J. Guikema, Valeria Lascano, Marinus H. J. van Oers, Dieuwertje M. Luijks, Eric Eldering, Arnon P. Kater, Steven T. Pals, Thomas J. Kipps, Kate Cameron, Marco Guadagnoli, Michael Hahne, Institut de Génétique Moléculaire de Montpellier (IGMM), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), AII - Amsterdam institute for Infection and Immunity, CCA -Cancer Center Amsterdam, Radiotherapy, Other departments, Pathology, Center of Experimental and Molecular Medicine, 01 Internal and external specialisms, Clinical Haematology, and Experimental Immunology

Subjects
Genetically modified mouse, Time Factors, Transmembrane Activator and CAML Interactor Protein, Chronic lymphocytic leukemia, Tumor Necrosis Factor Ligand Superfamily Member 13, Immunology, Mice, Transgenic, Kaplan-Meier Estimate, Biology, Biochemistry, Somatic evolution in cancer, Mice, 03 medical and health sciences, 0302 clinical medicine, immune system diseases, Proto-Oncogene Proteins, hemic and lymphatic diseases, Tumor Cells, Cultured, medicine, Animals, Humans, [SDV.BBM]Life Sciences [q-bio]/Biochemistry, Molecular Biology, Receptor, 030304 developmental biology, 0303 health sciences, Lymphoid Neoplasia, breakpoint cluster region, Cell Biology, Hematology, medicine.disease, Leukemia, Lymphocytic, Chronic, B-Cell, Mice, Inbred C57BL, Disease Models, Animal, Leukemia, HEK293 Cells, Mutation, Disease Progression, Tumor necrosis factor alpha, CD5, Protein Binding, 030215 immunology
Abstract

Although in vitro studies pointed to the tumor necrosis factor family member APRIL (a proliferation-inducing ligand) in mediating survival of chronic lymphocytic leukemia (CLL) cells, clear evidence for a role in leukemogenesis and progression in CLL is lacking. APRIL significantly prolonged in vitro survival of CD5(+)B220(dull) leukemic cells derived from the murine E mu-TCL1-Tg (TCL1-Tg [transgenic]) model for CLL. APRIL-TCL1 double-Tg mice showed a significantly earlier onset of leukemia and disruption of splenic architecture, and survival was significantly reduced. Interestingly, clonal evolution of CD5(+) B220(dull) cells (judged by BCR clonality) did not seem to be accelerated by APRIL; both mouse strains were oligoclonal at 4 months. Although APRIL binds different receptors, APRIL-mediated leukemic cell survival depended on tumor necrosis factor receptor superfamily member 13B (TACI) ligation. These findings indicate that APRIL has an important role in CLL and that the APRIL-TACI interaction might be a selective novel therapeutic target for human CLL. (Blood. 2013;122(24):3960-3963)

Published
2013
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45. Therapy-resistant tumor microvascular endothelial cells contribute to treatment failure in glioblastoma multiforme

Author

J B Daalhuisen, O. van Tellingen, Tijana Borovski, Martin R. Sprick, P Beke, Joost J.C. Verhoeff, V Lascano, Hans M. Rodermond, Jan Paul Medema, Cancer Center Amsterdam, Radiotherapy, Amsterdam institute for Infection and Immunity, and Center of Experimental and Molecular Medicine

Subjects
Senescence, Cancer Research, Poor prognosis, Therapy resistant, medicine.medical_treatment, Biology, Treatment failure, Mice, Cancer stem cell, Genetics, medicine, Animals, Humans, Treatment Failure, Molecular Biology, Chemotherapy, Brain Neoplasms, Endothelial Cells, medicine.disease, Tumor recurrence, Immunology, Neoplastic Stem Cells, Cancer research, Female, Glioblastoma
Abstract

Glioblastoma multiforme (GBM) is a devastating disease with high mortality and poor prognosis. Cancer stem cells (CSCs) have recently been defined as a fraction of tumor cells highly resistant to therapy and subsequently considered to be responsible for tumor recurrence. These cells have been characterized in GBM and suggested to reside in and be supported by the tumor microvascular niche. Here we evaluated the response of tumor microvascular endothelial cells (tMVECs) to radio- and chemotherapy, and analyzed how this affects their interaction with CSCs. Our data demonstrate that tMVECs exhibit extreme resistance to both therapies, with the main response to irradiation being senescence. Importantly, senescent tMVECs can be detected in human GBM samples as well as in mice upon irradiation. Even though permanently arrested, they are still viable and able to support CSC growth with the same efficacy as non-senescent tMVECs. Intriguingly, GBM CSCs themselves are capable of differentiating into cells with similar features as tMVECs that subsequently undergo senescence when exposed to radiation. This indicates that endothelial-like cells are therapy resistant and, more importantly, support expansion of GBM cells.

Published
2013
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46. Assessment of the stromal contribution to Sonic Hedgehog-dependent pancreatic adenocarcinoma

Author

Jan Paul Medema, Veronique L. Veenstra, Liviu Badea, Henk Roelink, Maarten F. Bijlsma, Irinel Popescu, Helene Damhofer, AII - Amsterdam institute for Infection and Immunity, CCA -Cancer Center Amsterdam, Radiotherapy, Center of Experimental and Molecular Medicine, and Graduate School

Subjects
Male, PLAUR, gene set enrichment analysis, Cancer Research, Pathology, SPOCK1, plasminogen activator, Stroma, HH, SHH, Mice, EDIL3, Sonic hedgehog, Research Articles, ITGB4, Tumor, biology, General Medicine, Cwcv And Kazal-Like Domains Proteoglycan, Neoplasm Proteins, Survival Rate, Sonic Hedgehog, Oncology, Molecular Medicine, Adenocarcinoma, Female, medicine.medical_specialty, Stromal cell, Oncology and Carcinogenesis, pancreatic ductal adenocarcinoma, Development, EGF-like repeats and discoidin I-like domains 3, Disease-Free Survival, Cell Line, Sparc/Osteonectin, Cell Line, Tumor, Pancreatic cancer, integrin beta 4, Genetics, medicine, urokinase receptor, Animals, Humans, Hedgehog Proteins, Oncology & Carcinogenesis, cysteine deaminase, Hedgehog, mRNA-Seq, GSEA, PDAC, medicine.disease, Coculture Techniques, Pancreatic Neoplasms, CDA, Tumor progression, Cancer cell, biology.protein, Stromal Cells
Abstract

Pancreatic ductal adenocarcinoma (PDAC) remains one of the most lethal malignancies. It is typically detected at an advanced stage, at which the therapeutic options are very limited. One remarkable feature of PDAC that contributes to its resilience to treatment is the extreme stromal activation seen in these tumors. Often, the vast majority of tumor bulk consists of non-tumor cells that together provide a tumor-promoting environment. One of the signals that maintains and activates the stroma is the developmental protein Sonic Hedgehog (SHH). As the disease progresses, tumor cells produce increasing amounts of SHH, which activates the surrounding stroma to aid in tumor progression. To better understand this response and identify targets for inhibition, we aimed to elucidate the proteins that mediate the SHH-driven stromal response in PDAC. For this a novel mixed-species coculture model was set up in which the cancer cells are human, and the stroma is modeled by mouse fibroblasts. In conjunction with next-generation sequencing we were able to use the sequence difference between these species to genetically distinguish between the epithelial and stromal responses to SHH. The stromal SHH-dependent genes from this analysis were validated and their relevance for human disease was subsequently determined in two independent patient cohorts. In non-microdissected tissue from PDAC patients, in which a large amount of stroma is present, the targets were confirmed to associate with tumor stroma versus normal pancreatic tissue. Patient survival analysis and immunohistochemistry identified CDA, EDIL3, ITGB4, PLAUR and SPOCK1 as SHH-dependent stromal factors that are associated with poor prognosis in PDAC patients. Summarizing, the presented data provide insight into the role of the activated stroma in PDAC, and how SHH acts to mediate this response. In addition, the study has yielded several candidates that are interesting therapeutic targets for a disease for which treatment options are still inadequate. © 2013 Federation of European Biochemical Societies.

Published
2013
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47. Mechanisms of antibody immunotherapy on clonal islet reactive T cells

Author

Dave L. Roelen, Bart O. Roep, Jan Paul Medema, P. van de Linde, O.M.H. Tysma, Herman Waldmann, Geoff Hale, Cancer Center Amsterdam, and Radiotherapy

Subjects
Daclizumab, CD3 Complex, medicine.drug_class, medicine.medical_treatment, CD3, T-Lymphocytes, Immunology, Apoptosis, Monoclonal antibody, Antibodies, Monoclonal, Humanized, Lymphocyte Activation, medicine, Immunology and Allergy, Humans, IL-2 receptor, Antilymphocyte Serum, Cell Proliferation, Antibody-dependent cell-mediated cytotoxicity, biology, Glutamate Decarboxylase, Immunization, Passive, Antibodies, Monoclonal, General Medicine, Immunotherapy, Clone Cells, Isoenzymes, Cytokine, Diabetes Mellitus, Type 1, Immunoglobulin G, biology.protein, Cytokines, Antibody, medicine.drug
Abstract

Clinical intervention trials evaluating the efficacy of antibody immunotherapy in type 1 diabetes are in progress. We tested effects on prediabetic islet antigen-specific autoreactive T cells of antithymocyte globulin (ATG) and humanized monoclonal antibodies against CD3 (ChAglyCD3) or CD25 (daclizumab) with regard to downmodulation of the target protein, proliferation, cytokine production, complement-dependent cytotoxicity (CDC), antibody-dependent cell cytotoxicity (ADCC), and survival. ATG leads to depletion of autoreactive CD4 + T cells by ADCC, CDC, and apoptosis, whereas anti-CD3 and anti-CD25 inhibited T-cell autoreactivity in a nondepleting fashion. ATG treatment led to a cytokine burst of Th1- and Th2-associated cytokines. Modulation of cytokine release through humanized monoclonal antibodies was moderate and selective: anti-CD25 led to increased release of IL-2 and reduced production of TNFα, whereas anti-CD3 decreased release of interferon-y and IL-5 and increased secretion of IL-10. ATG and the humanized monoclonal antibodies displayed contrasting mechanisms of action.

Published
2016

48. TGFβ signaling directs serrated adenomas to the mesenchymal colorectal cancer subtype

Author

Joep E. G. IJspeert, Felipe De Sousa E Melo, Evelyn Fessler, Marnix Jansen, Peter Nürnberg, Pramudita R. Prasetyanti, Hans Clevers, Jarno Drost, Louis Vermeulen, Carel J. M. van Noesel, Janneke F. Linnekamp, Marek Franitza, Evelien Dekker, Xin Wang, Jan Paul Medema, Sander R. van Hooff, Hubrecht Institute for Developmental Biology and Stem Cell Research, Center of Experimental and Molecular Medicine, Graduate School, Other departments, AGEM - Amsterdam Gastroenterology Endocrinology Metabolism, Gastroenterology and Hepatology, CCA -Cancer Center Amsterdam, Pathology, and Radiotherapy

Subjects
0301 basic medicine, Adenoma, Pathology, medicine.medical_specialty, Colorectal cancer, Carcinogenesis, colorectal cancer, medicine.disease_cause, epithelial–mesenchymal transition, 03 medical and health sciences, 0302 clinical medicine, Transforming Growth Factor beta, medicine, Journal Article, Humans, Epithelial–mesenchymal transition, Research Articles, Cancer, biology, Transforming growth factor beta, medicine.disease, Molecular medicine, digestive system diseases, Gene expression profiling, Organoids, 030104 developmental biology, 030220 oncology & carcinogenesis, sessile serrated adenoma, cancer subtypes, biology.protein, Cancer research, transforming growth factor beta (TGFβ), Molecular Medicine, Colorectal Neoplasms, Digestive System, Sessile serrated adenoma, Research Article, Signal Transduction
Abstract

The heterogeneous nature of colorectal cancer (CRC) complicates prognosis and is suggested to be a determining factor in the efficacy of adjuvant therapy for individual patients. Based on gene expression profiling, CRC is currently classified into four consensus molecular subtypes (CMSs), characterized by specific biological programs, thus suggesting the existence of unifying developmental drivers for each CMS. Using human organoid cultures, we investigated the role of such developmental drivers at the premalignant stage of distinct CRC subtypes and found that TGFβ plays an important role in the development of the mesenchymal CMS4, which is of special interest due to its association with dismal prognosis. We show that in tubular adenomas (TAs), which progress to classical CRCs, the dominating response to TGFβ is death by apoptosis. By contrast, induction of a mesenchymal phenotype upon TGFβ treatment prevails in a genetically engineered organoid culture carrying a BRAFV 600E mutation, constituting a model system for sessile serrated adenomas (SSAs). Our data indicate that TGFβ signaling is already active in SSA precursor lesions and that TGFβ is a critical cue for directing SSAs to the mesenchymal, poor‐prognosis CMS4 of CRC.

Published
2016

49. DNA methylation based biomarkers in colorectal cancer: A systematic review

Author

Kathy Pan, Kevin Lam, Raju Kandimalla, Janneke F. Linnekamp, and Jan Paul Medema

Subjects
0301 basic medicine, Epigenomics, Cancer Research, Colorectal cancer, Biology, Bioinformatics, 03 medical and health sciences, 0302 clinical medicine, Neoplasms, Genetics, medicine, Carcinoma, Biomarkers, Tumor, Humans, Epigenetics, HLTF, Promoter Regions, Genetic, Genome, Human, Methylation, DNA Methylation, medicine.disease, Prognosis, Neoplasm Proteins, 030104 developmental biology, Oncology, 030220 oncology & carcinogenesis, DNA methylation, Human genome
Abstract

Since genetic and epigenetic alterations influence the development of colorectal cancer (CRC), huge potential lies in the use of DNA methylation as biomarkers to improve the current diagnosis, screening, prognosis and treatment prediction. Here we performed a systematic review on DNA methylation-based biomarkers published in CRC, and discussed the current state of findings and future challenges. Based on the findings, we then provide a perspective on future studies. Genome-wide studies on DNA methylation revealed novel biomarkers as well as distinct subgroups that exist in CRC. For diagnostic purposes, the most independently validated genes to study further are VIM, SEPT9, ITGA4, OSM4, GATA4 and NDRG4. These hypermethylated biomarkers can even be combined with LINE1 hypomethylation and the performance of markers should be examined in comparison to FIT further to find sensitive combinations. In terms of prognostic markers, myopodin, KISS1, TMEFF2, HLTF, hMLH1, APAF1, BCL2 and p53 are independently validated. Most prognostic markers published lack both a multivariate analysis in comparison to clinical risk factors and the appropriate patient group who will benefit by adjuvant chemotherapy. Methylation of IGFBP3, mir148a and PTEN are found to be predictive markers for 5-FU and EGFR therapy respectively. For therapy prediction, more studies should focus on finding markers for chemotherapeutic drugs as majority of the patients would benefit. Translation of these biomarkers into clinical utility would require large-scale prospective cohorts and randomized clinical trials in future. Based on these findings and consideration we propose an avenue to introduce methylation markers into clinical practice in near future. For future studies, multi-omics profiling on matched tissue and non-invasive cohorts along with matched cohorts of adenoma to carcinoma is indispensable to concurrently stratify CRC and find novel, robust biomarkers. Moreover, future studies should examine the timing and heterogeneity of methylation as well as the difference in methylation levels between epithelial and stromal tissues.

Published
2016

50. Erratum

Author

Sascha Martens, Masashi Narita, Rajkumar Cheluvappa, Kevin A. Roth, Ta Yuan Chang, Kartik Venkatachalam, Chang-Shen Lin, Sharon G. Adler, Flaminia Pavone, Dianwen Ju, Michelle A. Ozbun, Michael R. Duchen, Shu Feng Zhou, Wei-Guo Zhu, Aaron Di Antonio, Defeng Wu, Taixing Cui, Xu Guang Guo, Zhiping Xie, Lorena García Nannig, Eloy Bejarano, Stéphane D. Lemaire, Petro Starokadomskyy, Hyung Ryong Kim, Mario Pinar, Rebecca T. Marquez, Zvenyslava Husak, Anthony R. White, Joanna Poulton, Antonis S. Zervos, Shweta Sharma, Jochen Walter, Nicholas T. Ktistakis, Christopher H.K. Cheng, Sunhee Lee, Yuen Li Chung, Howard O. Fearnhead, Young J. Oh, Ivano Amelio, Guillermo A. Blanco, Jan Simak, Junfang Wu, Yingying Lu, Mary Kate McBrayer, Soo Han Bae, Ichizo Nishino, Hong-Ming Hu, Benjamin R. Underwood, Tomonori Kimura, Zexian Liu, Savithrama P. Dinesh-Kumar, Qian Yang, Andreas Kern, Hsing Jien Kung, Jan B. Parys, Cam Patterson, Celine Perier, Toshiro Okazaki, Daisuke Koya, Avinash Sonawane, Cédric Cleyrat, Robert I. Richards, Kai Y. Soo, Rodrigo Mora-Rodriguez, Gigi N.C. Chiu, Moon Moo Kim, Vladimir N. Uversky, Shengfang Ge, Matthew T. V. Chan, Irene Kyrmizi, Lara Gibellini, Ángela M. Valverde, Erik Norberg, Fan Zhang, Jan C. Koch, Alec C. Kimmelman, Jingfang Ju, Jie Bai, Lei Duan, Paulina Ordonez, Shuwen Liu, Wolfdieter Springer, Eric Deutsch, Elena Ortona, Jose M. Seguí-Simarro, Vinay Choubey, Leonidas Stefanis, Robert G. Hawley, Claudia Bincoletto, Xian-Hui He, Zhifen Yang, Thomas M. Durcan, Martine Biard-Piechaczyk, Kui Lin, Hongming Pan, Konstantinos Kambas, Cristina Muñoz-Pinedo, Marta Magariños, Yoshinori Takahashi, Adrienne M. Gorman, Philippe Gailly, Takahiko Akematsu, Justine D. Mintern, Liang Xu, Tetsuo Shioi, Luis M. Botana, Yule Liu, Yong Yeon Cho, Jinzhi Lei, Eung Kweon Kim, Alakananda Basu, Vikash Kumar Dubey, Candelaria Gomez-Manzano, Avital Eisenberg-Lerner, Chuan-Ming Xie, Wenjie Dai, Pedro Gonzalez-Alegre, Maria Condello, Zheng-Hong Qin, Zhi-Min Yuan, Catherine Andreadi, Anna Rita Migliaccio, Chong Liu, Michaël Boyer-Guittaut, Melanie Denizot, Esperanza Arias, Greet Van den Berghe, Guomei Tang, Timothy P. Devarenne, Xianyong Sheng, Louis R. Lapierre, J. Wade Harper, Zuzana Storchova, Aileen R. Ariosa, Sug Hyung Lee, Qi Zeng, Godefridus J. Peters, Daniela L. Papademetrio, Alexandre Arcaro, Zhiyuan Yao, Pablo Iribarren, Mario Chiariello, Maria Rosaria Torrisi, Parimal Karmakar, Yong Huang, Sebastiano Sciarretta, Nathalie Andrieu-Abadie, László Fésüs, Patricia Boya, Ruediger Rudolf, Leonor Miller-Fleming, Vasilis J. Promponas, Juan Segura-Aguilar, Paula Daza, Shiow Ju Lee, Songshu Meng, Paul K. Herman, Ludwig Eichinger, Ye-Guang Chen, Kay F. Macleod, Thomas Simmet, Cristina Corral-Ramos, Claudio Brancolini, Jun Ren, Ying Jiang, Benoît Derrien, Xiao Fang Yu, Qing Zhong, Zong Wan Mao, Xingcong Ren, Armando A. Genazzani, Marina Pierdominici, Sanbing Shen, Sandra Moreno, Hana Algül, Maurizio Renna, Ricardo Sánchez-Prieto, Ashok K. Saluja, Yasuo Uchiyama, Pope L. Moseley, Victor E. Dosenko, Chun-Feng Liu, Bakhos A. Tannous, Efthimios Sivridis, Baharia Mograbi, Michiko Shintani, Amanda S. Bess, Rodrigo Portes Ureshino, Avnika A. Ruparelia, Paul Hofman, Eric Chevet, Martha M. Monick, Hong Gang Wang, Daping Fan, Jorge Moscat, Giuseppe Matarese, Consiglia Pacelli, Young Seok Cho, Miriam Cnop, Stefan Böckler, Nikolai V. Gorbunov, Christina J. Sigurdson, Hang T.T. Nguyen, Aurélie François, Katarina Kågedal, Sam Gandy, Silvia Campello, Alain Bruhat, Filomena Fiorito, Hua Feng, Man Tian Mi, Gian Maria Fimia, Masaki Tanaka, Guofei Zhou, José L. Crespo, Heinz Jungbluth, Anna Chiara Nascimbeni, Arianne L. Theiss, Svetlana Dokudovskaya, Mar Lorente, Sergio Lavandero, Yu Xia Zhao, Fangming Lin, Yuchen Feng, Gad Galili, Silvia Cetrullo, Paula I. Moreira, Dhyan Chandra, Dimitrios J. Stravopodis, Roberta A. Gottlieb, Gregory A. Taylor, Longping Wen, Faqiang Li, Marco Sardiello, Umesh K. Jinwal, Francesca Belleudi, Lan Tan, Livia Di Renzo, Tamas Korcsmaros, Xinbing Sui, Douglas R. Green, Guillermo Mazzolini, Hervé Le Stunff, Kelly S. Doran, Mary E. Choi, Carlos S. Subauste, Natalia Rodriguez-Muela, Nicholas J. Talbot, Marta Palmieri, Sonia Hernández-Tiedra, Ligia C. Gomes, Irving M. Shapiro, Makoto Ubukata, Mario P. Tschan, Baris Bingol, Benjamin Loos, Terry Kwok, Luca M. Neri, Sreejayan Nair, Michele Wolfe Bianchi, Ralf Erdmann, Alexander Greenhough, Neeraj Vij, Jeong Hun Kim, Satoaki Matoba, Bo Liu, George R. Beck, Michael Moore, Vrajesh V. Parekh, Kyle A. Bauckman, Li-Lin Du, Mikihiro Fujiya, Yan G. Zhao, Renaud Legouis, Jiangwei Zhang, Kailiang Jia, Nadezda Apostolova, Sehamuddin Galadari, Khosrow Adeli, Ming Yong Zhang, Carmela Fusco, Angel Ortega, Anna Pensalfini, Zsuzsanna Szatmári, Marco Tafani, Isabella Ceccherini, Anne Hamacher-Brady, Kuen Jer Tsai, Anita C. Truttmann, Franco Fortunato, Keisuke Miyazawa, Chunhai Fan, Berge A. Minassian, Jian Zhang, Frank A. Anania, Heesun Cheong, Amal O. Amer, Ing Swie Goping, Won-Ki Huh, Anita Solhaug, Joan Cl ria, Laurent Le Cam, Seungmin Hwang, Karen L. Wright, Antonella De Matteis, Troy T. Rohn, Ivana Bjedov, Subbiah Pugazhenthi, Hal E. Broxmeyer, Xue Yuan Bai, Koenraad Norga, Minnie M. Sarwal, Daniel F. Schorderet, Ioannis P. Nezis, Mei Qing Wang, Jun Hee Lee, Yong J. Lee, David A. Tumbarello, Fernando Macian, Joern Dengjel, Dmitry V. Bulavin, Andrew J. Halayko, Ben Berkhout, Aseem Pandey, Santosh Kesari, Karin Przyklenk, Elena V. Tchetina, Matthew L. Albert, Laura Segatori, Joel N. Meyer, Mustapha Rouis, Éva Margittai, Ashish Jain, David Hahn, Thomas Vaccari, Lori R. Covey, Ghanshyam Swarup, Kuo Yang Huang, Gennaro Napolitano, Sam W. Lee, Seong Who Kim, Alberto Anel, Vladimir V. Rogov, Laura A. Carleton, Amine Belaid, Byoung Kuk Jang, Sheng-Han Kuo, Patricia L. Yeyati, Jae U. Jung, Teresa Zoladek, Sabrina Di Bartolomeo, Clémence Richetta, Peixin Yang, Daniela Trisciuoglio, Hye Seung Jung, Katsumi Higaki, Eui-Bae Jeung, Ivan Topisirovic, Isabella Caniggia, Susan E. Logue, Issidora S. Papassideri, Lynda A. Morrison, Caihong Wang, Graeme Sargent, Beth Levine, Mingxiang Ye, David M. Sabatini, Consuelo Amantini, Julio A. Aguirre-Ghiso, Lawrence H. Boise, Patricia Silvia Romano, Sean T. Sweeney, Takayuki Tsukuba, Reinhard Dechant, Benoit Barbeau, Marta Martinez-Vicente, Kuo How Huang, Edésio José Tenório de Melo, Faustino Mollinedo, José M. Fuentes, Joaquín Jordán, Dong-Hyung Cho, Dexian Zheng, Jeroen J.M. Hoozemans, Zhong Chen, Waleska Kerllen Martins, Abraham Acevedo Arozena, Marcos P. Thomé, Gordon C. Shore, Fabienne C. Fiesel, Teng Jiang, Feng Han, Marc Poirot, Anne Sophie Nicot, Eileen White, Olivier Feron, Arthur I. Cederbaum, Wen Bin Qian, Yingjie Sun, Rejko Krüger, Shingo Kajimura, Jianzhen Xu, Shang Der Chen, Maximiliano G. Gutierrez, Zhengping Yu, Jiaren Sun, Utpal Sen, Giovanna Galliciotti, Hilde Nilsen, Benjamin T. Kopp, Benedikt Westermann, Inmaculada Galindo, Eeva-Liisa Eskelinen, Rubem F. S. Menna-Barreto, Guillermo Mariño, Andrea Ballabio, Izabela Poprawa, Yanjin Zhang, Clay F. Semenkovich, Martin E. Fernandez-Zapico, Helin Vakifahmetoglu-Norberg, Hongchi Jiang, Eugenia Morselli, Angelo A. Manfredi, Marianne Boes, Han-Jung Chae, Covadonga Alonso, Min Chen, Safia Costes, David Kessel, Rakesh Kumar, Yang Zhang, Reinhild Prange, Vassiliki E. Mpakou, Laura Santambrogio, Javier E. Irazoqui, Anna Skwarska, Junichi Sadoshima, Rika Umemiya-Shirafuji, Michael I. Koukourakis, Norma Maugeri, Yuqing Wang, Pedro R. Cutillas, Jiqin Lian, Jiri Stulik, Takashi Ueno, Craig Montell, Rena Balzan, Meiyan Jin, Mara C. Duncan, Cathleen R. Carlin, Yasuo Yanagi, Maite G. Fernandez-Barrena, Yuyan Xiong, Martin Graef, Wei Yuan Yang, Renato V. Iozzo, Mark Screen, Patrick Brest, Haichao Wang, Ming Tan, Werner J. Kovacs, Weili Shen, Alessandro Fraldi, Paul Saftig, Alberto Faggioni, Krisna Prak, Christos E. Zois, Timothy E. Weaver, Marc Lecuit, Yu-Ying He, Michele Caraglia, Walter Balduini, M. Isabel G. Roncero, B. Schneider, Monika Cahova, Mathias Faure, Chihiro Sasakawa, Simon Michaeli, Sandy Giuliano, Dario C. Altieri, Eun-Kyeong Jo, Myung-Shik Lee, Carol Imbriano, John H. Brumell, Gustavo H. Goldman, Yan Wang, Junyan Shi, Quan Chen, Jayanta Debnath, Yonggeun Hong, Mohamed Amessou, Richard W. Wong, Robert E. Burke, Mauro De Santi, Trevor G. Shepherd, Anna Maria Joseph, Wouter G. van Doorn, Erkang Fei, Huey Lan Huang, F. Gisou van der Goot, Xinfeng Liu, Alexandru Almasan, Akiko Maeda, Yu Qiu, Yaohua Wu, Annie Sittler, Wen-Xing Ding, Wenhua Zhu, Hung-Jen Liu, Moisés Martínez-Velázquez, Jeffery S. Cox, Seung Yong Yoon, Concepcio Marin, Wilian A. Silveira, Fulvio Chiacchiera, W. Douglas Fairlie, Jian Xin Gao, Shuilong Leng, Nathan R. Brady, Josef M. Penninger, Puran Singh Sijwali, Florian Gruber, Tibor Vellai, Jiunn-Liang Ko, Laura Korhonen, Slimane Ait-Si-Ali, Hirokazu Arimoto, Alberto M. Martelli, Teresa L. M. Thurston, Chuanshan Xu, Kathrin Pallauf, Eduardo Couve, Shweta Saran, Lionel Blanc, Maylin Almonte-Beceril, Yong-Keun Jung, Lena Lavie, Junsoo Park, Camilla Palumbo, Claire H. Mitchell, Sophie Pattingre, Guillermo Velasco, Steve S.-L. Chen, Xiu-Fen Ming, Xin Qi, Vania Gelmetti, Nicolas Dupont, Soraya S. Smaili, Chinnaswamy Jagannath, Uta Dahmen, Daolin Tang, Rodrigo Franco, John H. Kehrl, Xiaonan Dong, Carsten Sachse, Jeff Kuret, Genzou Takemura, Supawadee Sukseree, Joëlle Botti, W. Haung Yu, Aurelia Lugea, Scott J. Bultman, Divaker Choubey, Frank A. Sinicrope, You-Wen He, Jian Wu, Yoshitaka Isaka, Geert Bultynck, Giuseppe Merla, Luigi Maiuri, Sonia Melino, Hannelore Maes, Daniele Lettieri Barbato, Ian G. Ganley, Zhihong Yang, Daniel Hofius, Kimberly McCall, Peiwen Chen, Istvan Lekli, Alicia Rosello, Eric Ghigo, Atsushi Kuno, Iman Tavassoly, Chris Albanese, Agustín Aranda, Salvatore Pepe, Hong Jiang, Henri Batoko, Giovanna Elvira Granato, Vincent Zecchini, Stephen E. Girardin, Maria T. Diaz-Meco, Philippe Marambaud, G. Amadoro, Sangeeta Khare, Christelle Koechlin-Ramonatxo, Emery H. Bresnick, Christian Behl, Mikio Nishimura, Julien Puyal, Wenjie Guo, Hsinyu Lee, Carolyn M. Sue, Derrick Gibbings, Alina Maloyan, Philippe Pierre, Serge N. Manié, Gerry Melino, Elizabeth A. Woodcock, Roberto Ciarcia, Liwen Jiang, Michael C. Kruer, Vladimir Trajkovic, Yunjiao Zhang, Nina Raben, Beata Pajak, Michael J. Ragusa, Riccardo Autelli, Kelly Jean Thomas, Suzana Gispert, Wei Li Zhao, Cheol Hyeon Kim, Pothana Saikumar, Arsenio Fernández-López, Juliano Machado, Valentina Iovane, Cai Ping Tan, Carmine Settembre, Neelam Azad, Yohta Shimada, Shivendra V. Singh, Hai Rao, Hirosato Mashima, Michael T. Stang, Yasuhito Sakuraba, Gemma Fabriàs, Tuck Wah Soong, Didac Carmona-Gutierrez, Ilse Vanhorebeek, F. Javier Oliver, Mondira Kundu, Alfonso Schiavi, Dan Lindholm, José L. Revuelta, Jason S. King, Susana Castro-Obregón, Paul Digard, Hua Zhu, Komal Raina, Yun Dai, Ruben K. Dagda, Nuria Martinez-Lopez, Andrea A. Gust, Lucia Notterpek, Robert Clarke, Manon E. Wildenberg, Mingzhou Chen, Leticia Reyes, Laura Berliocchi, John J. McMahon, Hongzhuan Chen, E.M. Nolte, Stefan W. Ryter, Fulvio Reggiori, Jiefei Geng, Michael A. Mandell, John H. Fingert, Holger Prokisch, Marina Jendrach, Søren R. Paludan, Elizabeth P. Henske, Ricardo Gargini, Wei-Xing Zong, Susmita Kaushik, Michael Overholtzer, Paul W. Sylvester, Daniel E. Voth, Canhua Huang, Andrea Boman, Gérard Lizard, Rut Valdor, Marc Flajolet, Graham S. Taylor, Nicola Di Daniele, Leonardo H. Travassos, Ying Yang, Anumantha G. Kanthasamy, Hasan Mukhtar, Yuhua Zhu, Noor Gammoh, Ignacio Vega-Naredo, Victoria Ryabovol, Sara W. Bird, Gang Min Hur, Qun-Ying Lei, Fan Yi, Laura Caberlotto, Maria F. Galindo, Bilal Piperdi, Leonidas C. Platanias, P. Hande Özdinler, Régis Delage-Mourroux, Julio Madrigal-Matute, Xu Liu, Nagio Takigawa, Aurora Pujol, Marta Margeta, Hee Jeong Kong, Christian Behrends, Michael Thumm, Shirley Luckhart, Emilio Clementi, John W. Steele, Liliana Schaefer, Philip L. Lorenzi, Chao-Yu Miao, She Min Lu, Jane E. Ishmael, Jin Hyoung Kim, V. Izzo, Yanming Wang, Balindiwe J.N. Sishi, Vincent Galy, Andras Perl, Shouqing Luo, Giovanni Vitale, Yongsheng Che, Rodrigo Troncoso, Liu Yang, Thomas J. Begley, Sebastien G. Bouret, Elizete Rizzo, James M. Piret, Junjun Wang, Herman P. Spaink, Thomas S. Jacques, Robin F. B. Turner, Young H. Lee, Eva Szegezdi, Daphne R. Goring, Manish K. Aghi, Rui Kang, Bart Staels, Midori Umekawa, Delia Goletti, Robert J. Bryson-Richardson, Ubaldo E. Martinez-Outschoorn, Luisa Dalla Valle, Giovanni Luca Gravina, Emad S. Alnemri, Maria Kaparakis-Liaskos, Konstantinos Ritis, Shalmoli Bhattacharyya, Alessandra Bolino, Xiaonan Zhao, Yoshihisa Watanabe, Christian Ungermann, Juan L. Iovanna, Katherine Williams, Ken Shirabe, Teresa S. Hawley, Sara Cherry, Ryuichiro Atarashi, Kozo Hamada, Seamus J. Martin, Shigeru Oshima, Mario Pende, Illana Gozes, Michel A. Duchosal, John J. Shacka, Shunhei Yamashina, Kithiganahalli Narayanaswamy Balaji, Richard L. Proia, Besim Ogretmen, Fang Hua, Koichi Araki, Charles Grose, Jia Luo, Helen K. W. Law, Charles Swanton, Liat Drucker, Guo Zhang, Zhizhuang J. Zhao, Anne K. Kenworthy, Javier A. Menendez, Gary Grant, Stig U. Andersen, Frank Lafont, Aparna Lakkaraju, Taijoon Chung, Leticia A.M. Carneiro, Monique Bernard, Gang Chen, Stephen W.G. 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Tapia, Christoph Becker, Huixin Yu, Pei-Yu Wang, Bertrand Joseph, Zhen Yan, Georgia Minakaki, Ricardo Escalante, Ralph A. Nixon, Katsuhiko Asanuma, M. Helena Vasconcelos, David J. Reiner, Shengkan Jin, David Dávila, Theo Rein, Balakrishna L. Lokeshwar, Antonio Miranda-Vizuete, Carl Ward, Vito Turk, Frederick D. Quinn, Katja Köhler, Masaru Harada, Kathleen Boesze-Battaglia, Fraser P. Coxon, Paulo R. Jannig, Miguel A. Peñalva, Manjula Kalia, Marco Corazzari, Chunjuan Song, Xianghua Yan, Lilach Toker, Benjamin Pineda, Vanessa Ginet, Ye Xu, Chun Jung Chen, Roberto Towns, Amy A. Kiger, Rajagopal Ramesh, Maria Rita Rippo, Joseph A. Hill, Boris Zhivotovsky, Peter Speck, Ya Hua, Peter J. Roach, Fabio Penna, Kasper M.A. Rouschop, Jeng-Jer Shieh, Maria Angeles Mena, Mei Zhao, Sonia Rocha, Xin Wen, Sylvain Lefort, Michael Scharl, Ramnik J. Xavier, Alan Cheng, Marion Bouchecareilh, Stella Y. Lee, Maria Xilouri, Qi Chen, Claudia Spies, Pengfei Ge, Natascia Ventura, Luca Galluzzi, Yau Hung Chen, Jing Pu Zhang, Diego Albani, Dingzhong Tang, Nikolai Engedal, Stefania Meschini, Maria Lyngaas Torgersen, Shibu M. Poulose, Jean-Paul Decuypere, Ziheng Xu, Jocelyn Laporte, Thierry Arnould, Albert Haas, Ida J. van der Klei, Agustín Hernández, Dong Wook Shin, Per E. Stromhaug, Valentín Ceña, Ugo Pagnini, Karolina Pakos-Zebrucka, Blagovesta Popova, Lisa M Lindqvist, Sangita C. Sinha, Yuguang Shi, Zvonimir Marelja, Robin Candau, Xin Wang, Evelina Gatti, Olatz Pampliega, Michael P. Lisanti, Elena Tamagno, Mei Lan Tan, Gary Warnes, Zdena Palková, Shigeomi Shimizu, Ingo Schmitz, Tino Kurz, Soledad Matus, Gopal Chakrabarti, Joseph J.Y. Sung, Beáta G. Vértessy, Giuliana Cassinelli, Giovanni Benard, Yin Chen, Emma Colucci-Guyon, Craig Blackstone, Lizhi Cao, Sebastian Schuck, Qingqiu Gong, Theocharis Panaretakis, Jayoung Choi, Sven R. Carlsson, Libuše Váchová, Raymond Chuen-Chung Chang, Yang Liu, Zheng Dong, Qinghua Shi, Hélène Duez, Tiziana Bachetti, Axel H. Schönthal, Sumit Sahni, Bo Wang, Naomichi Matsumoto, Markus Rehm, Liliana Torosantucci, Toren Finkel, Yi Hsin Tseng, Hsiang Cheng Chi, Fang Lin, Tony George Jacob, Ju-Xian Song, Alessandro Fanzani, Marc Tatar, Paola Costelli, Rubén Gómez-Sánchez, Yunfei Wen, Juha J. Hulmi, Francesca V. Mariani, Min Zeng, Chiung Chyi Shen, Carine Michiels, Yan Burelle, Andreas L. Serra, Goran Petrovski, Kwang Woon Kim, Paula Ludovico, Darius Ebrahimi-Fakhari, Yee Joo Tan, Luisa De Martino, Alvaro Glavic, Pierre Lapaquette, Edmund B. Rucker, Andreas Mayer, Shigeko Yamashiro, Scott K. Powers, Robert M. Gogal, Ebru Goncu, Yuichiro J. Suzuki, Anna Maria Giammarioli, Claudio Hetz, Eric H. Baehrecke, Cheryl L. Walker, Cinzia Lanzi, Deepti S. Wilkinson, Ralph Feuer, Long Yi, Virawudh Soontornniyomkij, Nektarios Tavernarakis, Nobuyuki Nukina, Elisabetta Ferraro, Thomas Wollert, Vassiliki Karantza, Simon Wilkinson, Yong Tae Kwon, Panagiotis D. Velentzas, Jong-In Park, Huu Phuc Nguyen, Miriam J. Schönenberger, Marcello Chieppa, Thomas A. Ferguson, Behzad Yeganeh, Saurabh Chatterjee, Anika Nagelkerke, Ju Hong Jeon, David W. Russ, Jeff W. Chen, Verónica I. Dumit, Chuangui Wang, Stephen C. Pak, Georgios Chamilos, Vijittra Leardkamolkarn, L. Ashley Cowart, Miguel A. Martín-Acebes, Andrea Cossarizza, László Orosz, X. Charlie Dong, Kei Watase, Yasuko Rikihisa, Santiago Rodríguez de Córdoba, Yu Jen Chen, Andrew P. Lieberman, Peter G.H. Clarke, Guylène Page, Babak Razani, Franziska Wild, Guang Zhou Zhou, Tsui-Fen Chou, Gen Sheng Wu, Daniel Johnson, Jiwu Wei, Rani Ojha, Marco Molinari, Manolis Fanto, Yongjun Jiang, Nadine Camougrand, Rong-Rong He, Ivan Dikic, Candece L. Gladson, Naoki Suzuki, Shiming Liu, Felipe X. Pimentel-Muiños, Alicia Meléndez, José Antonio Sánchez-Alcázar, Maho Hamasaki, Carmen Ruiz-Roldán, Hana Schmeisser, Margarita Villar, Vinod Sundaramoorthy, Maria Beatrice Morelli, Naweed I. Naqvi, Jochen Klucken, Nirmala Parajuli, Rodney J. Devenish, Mari L. Shinohara, J. Lindsay Whitton, Marie-Josée Boucher, Jeroen Roelofs, Xiao Hong Liu, Saverio Minucci, Germán Bou, Katie R. Martin, Hermann M. Schätzl, Suresh C. Tyagi, Shengzhou Wu, Michael T. Lotze, Albert R. La Spada, Channing J. Der, Gabriela Roca, Lucile Espert, Elisabeth Corcelle-Termeau, Zhenyu Yue, Sabine Hilfiker, Evripidis Gavathiotis, Truong Lam, Tobias M. Rasse, Kumaravel Somasundaram, Chih-Wen Shu, Tamotsu Yoshimori, Daniel T. Starczynowski, Oliver Florey, Vladimir Kirkin, Dan T. Vogl, Peter Vandenabeele, Allan Tsung, Renwick C. J. Dobson, Serge Mostowy, Nelly Godefroy, Maria Teresa Viscomi, Young Ho Koh, Caroline Mauvezin, Keiji Tanaka, Juan Fueyo, Lih-Shen Chin, Jingjing Cai, Laura D. 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Heinzen, Xiangmei Chen, Nihal Altan-Bonnet, Sung Sik Lee, Hai Jie Wang, Catherine Dargemont, Jie Du, Sofie Claerhout, Edmond Chan, Yi Sun, Xiangbo Wan, Paul Lingor, Shilpa Buch, Gerald M. McInerney, Zhenlong Wu, Guo Chang Zhang, Iain A. McNeish, Suresh Awale, Mark P. Mattson, Srinivasa Subramaniam, Wuhan Xiao, Katsuhiko Mikoshiba, Giancarlo Parenti, Bruno Miguel Neves, Benjamin Dehay, Fatima Teixeira-Clerc, Patricia Huebbe, Calvin K. Yip, Ryan J. Schulze, Pallabi Sarkar, Vladimir I. Titorenko, Johanna Laukkarinen, Martin E. Gleave, Veronika Stoka, Pascal Genschik, Karen Brown, Zhaoliang Su, Walter Malorni, Arlette Darfeuille-Michaud, Vincent C. O. Njar, Jeffrey E. Pessin, Thomas Wileman, Alexander J. Whitworth, Stefano Santaguida, Gustavo A. Nader, Gláucia Maria Machado-Santelli, Marie-Josée Hébert, Skye C. McIver, Scott A. Soleimanpour, Jia-Hong Lu, Fei Liu, Yu Wang, Elisa Motori, Chad A. 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McKenna, Mila Ljujic, Hirotaka Watada, Harry Ischiropoulos, Shile Huang, Udo Hasler, Ke Li, Josefina Casas, Ken-ichi Isobe, Min Li, Muriel Priault, Vincenzo De Tata, Monique Gannagé, Sakineh Kazemi Noureini, Isao Ishii, Sasanka Ramanadham, Valérie Pierrefite-Carle, Chengyu Liang, Louise Deldicque, Gabriella Cavallini, Afshin Samali, Angelika Amon, Kah-Leong Lim, Lavinia Cantoni, Demetrios G. Vavvas, James E. Haber, Alireza R. Rezaie, Regina Celia Bressan Queiroz de Figueiredo, Cynthia D. Cooper, Masaaki Komatsu, Silvia Alvarez, Gemma Triola, Dong-Yun Ouyang, Razaul Karim, Kostyantyn V. Dmytruk, Bassam Janji, Peter Bütikofer, Indira U. Mysorekar, Hana Popelka, E. Marion Schneider, Carlos Guillén, Gaël Roué, Seung-Hoon Baek, Patrick Auberger, Jun Araya, Sandra M. Cardoso, Gu He, Eduardo C. Filippi-Chiela, Patrick A. Lewis, Wei-Pang Huang, Eric Reits, Cécile Vindis, Trond Lamark, Mehrdad Alirezaei, Takao Setoguchi, Alberto Bartolomé, Chih Peng Chang, Andriy A. Sibirny, Mauro Piacentini, Jing Wang, Kuninori Suzuki, Ludo Van Den Bosch, Kevin N. Dalby, Keiran S.M. Smalley, David K. Ann, Luis F. Moita, Anthony Sanchez, Chin Hsu, Guillermo M. Albaiceta, Vassilis Stratoulias, Attila L. Kovács, Charleen T. Chu, Tewin Tencomnao, Audrey H. Poon, Steve Lancel, José C. Fernández-Checa, Hannah Rabinowich, Heinz D. Osiewacz, Sami Dridi, Kate E. Keller, Thorsten Hoppe, Crispin R. Dass, Jekaterina Erenpreisa, Akira Matsuura, Donna D. Zhang, Ying Zhao, Luisa Coletto, Roy Parker, Georg M. N. Behrens, Alessia Di Nardo, Mian Wu, Alberto Jiménez, Magdalena Rost-Roszkowska, Christopher J. H. Elliott, Pamela J. Yao, Damián Gatica, Rafael Linden, Helena L. A. Vieira, Anand K. Ganesan, Wim Martinet, Frank Madeo, Juliann G. Kiang, Helmut Kramer, Lorrie A. Kirshenbaum, Salvador Ventura, Clemens Steegborn, Zahra Zakeri, Marco Antonio Meraz-Ríos, Masaki Ohmuraya, Michael A. Riehle, Congcong He, Federica Sotgia, Shi-Mei Zhuang, Paul Dent, Jürgen Bosch, Xuejun Wang, Kuan-Chih Chow, Carlos Gorbea, Lisa Gerner, Yuzuru Imai, Jan Gunst, Duncan R. Smith, María Esther Pérez-Pérez, N. Tony Eissa, Michel Roberge, Carmen García-Ruiz, Irfan J. Lodhi, Hongjiao Ouyang, Mustapha Kandouz, Alessio Papini, Jun Sun, Takanobu Otomo, David H. Perlmutter, Jae-Sung Kim, Feng Gao, Åsa B. Gustafsson, Paul M. Salvaterra, Michael Klinkenberg, Or Kakhlon, Abhinav Diwan, Takahiro Shintani, Paola Matarrese, Marc D. Meneghini, Jinsheng Zeng, Xu-jie Zhou, Linda S. Yasui, Rui Sheng, Shiqian Huang, Elizabeth Delorme-Axford, Amélie Bernard, Kevin M. Ryan, Cecília M. P. Rodrigues, Jonathan M. Backer, Harald Stenmark, Hiroaki Adachi, Koichi Sakakura, Fatima Mechta-Grigoriou, Zhi Nong Wang, Ramesh Natarajan, Tian Xia, Marco Folini, Robert A. Screaton, Jane J. Yu, Xian Wang, Gerhard H. Braus, Min Wu, John A. Hanover, Anuj Kumar, Charbel Moussa, Shailendra Anoopkumar-Dukie, Edward A. 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De Meyer, Alice Carrier, Yipeng Wang, Serena Montagnaro, Nadeem O. Kaakoush, José de la Fuente, Devrim Gozuacik, Edward D. Plowey, Alastair M. Buchan, John C. Chatham, Daniel J. Klionsky, Cecilia Gotor, Isabelle Hamer, Katarzyna Mnich, Paola Rusmini, Chengshu Wang, Per Nilsson, Lorena Esteban-Martínez, Raúl V. Durán, Dieter Willbold, Hye Won Chung, Janet D. Sparks, John M. Lucocq, Blake B. Rasmussen, Takeshi Matsuzawa, Hagai Abeliovich, Wiep Scheper, Sung Joon Lee, Jennifer S. Carew, Serena Carra, Michael J. Morgan, Nikolai Slavov, Guy Berchem, Tiziana Cocco, Simone Engelender, Jianbo Yue, Yujie Chen, Mario Fabri, Maria F. Czyzyk-Krzeska, Hua Niu, Roger J. Davis, Peter J. Adhihetty, Kishore B.S. Pasumarthi, Jongsook Kim Kemper, Sharon A. Tooze, Antonio Zorzano, Jin Cheon Kim, Jian Xu, Andreas Meryk, Kristina Vuori, Jongdae Lee, Patrizia Agostinis, Diego Ruano, Wim Vandenberghe, Julia I-Ju Leu, Céline Gongora, Bernadette Carroll, Vinoth Kumar Megraj Khandelwal, Bo Lu, Marja Jäättelä, Lorenzo Galluzzi, Ioannis P. Trougakos, Tatsuya Maeda, Marie-Agnès Bringer, Mario Chiong, Hans-Uwe Simon, Lance A. Liotta, Ruth S. Slack, Ina Oehme, Umamaheswar Duvvuri, Shaun Martin, Augustine M.K. Choi, Michel Vidal, Ying Wang, Isis do Carmo Kettelhut, Mojgan Djavaheri-Mergny, Jörn Coers, Massimo Donadelli, Jesus Aldudo, Miyuki Sato, Jianxun Liu, Jörg Höhfeld, Luc Van Kaer, Andrei I. Ivanov, Dohun Pyeon, José M. Bravo-San-Pedro, Jianxin Peng, Xiaoyan Jiang, Dimitri Krainc, Yangqing Xu, Arnaud François, P. Robin Hiesinger, Sagar Lonial, William C. Cho, Caty Casas, Betty Yuen Kwan Law, Hongbing Zhang, Tor Erik Rusten, Erwin Knecht, Honglin Luo, Shi Xiao, Hiromi Sesaki, Enza Maria Valente, Verónica Pérez de la Cruz, Marta M. Lipinski, David A. Hood, Shi-Yong Sun, Luiz Carlos Carvalho Navegantes, Joynal Abedin, Shino Goto-Yamada, Gustavo Maegawa, Takehiko Matsushita, Vitor A. Lira, Clara I. Rodríguez, Ekihiro Seki, Qiang Li, Karin Öllinger, Ted M. Dawson, Ssang-Goo Cho, Wan-Wan Lin, Pramod Kumar Garg, Jeffrey Robbins, Peter R. Williamson, Michael Sacher, Carlo Follo, Bulent Ozpolat, Xiao Jia Wang, Na Man, Hua Cheng, Bing Yan, Tsung-Hsien Chuang, Paul B. Fisher, Rajat Singh, Edward A. Ratovitski, Katsuhiko Kitamoto, Jung Jin Hwang, Shinji Hadano, Che Hsin Lee, Shuo Wang, Einar M. Sigurdsson, Camille Martinand-Mari, Agnieszka Sirko, Katherine R. Parzych, Etienne Morel, Yasushi Kitaoka, Hassan Chaachouay, Patricia Chakur Brum, Dexin Kong, Jerome Tamburini, Kuppan Gokulan, Stefan Olsson, Bilon Khambu, Lea M.D. Delbridge, Daniel P. Orban, David A. Gewirtz, Zhonglin Xie, Joe Quadrilatero, Kunikazu Tanji, Simin Mohseni, Gábor Bánhegyi, Jin Ming Yang, Jinxian Xu, Carmen Veríssima Ferreira-Halder, Addanki P. Kumar, Deok Ryong Kim, Jianjie Ma, Sang Won Suh, Guido Kroemer, Klára Megyeri, Michael N. Sack, Heinrich Taegtmeyer, Gilles Pagès, Gabriella Marfe, Gregg L. Semenza, Karine G. Le Roch, Marisa Brini, Marina Bouché, Oliver Kepp, Vinay V. Eapen, J. David Beckham, Stephan T. Stern, Xudong Zhang, Marcello Pinti, Xiangnan Zhang, Jae Keun Lee, Ana Coto-Montes, Assaf Rudich, Laura D. Attardi, Debabrata Ghosh, Philip Rosenstiel, Sébastien Besteiro, Maria Rosa Sarrias, R. Andres Floto, Xiao Ming Yin, Nicholas W. Lukacs, Hermann Pavenstädt, Matias Simons, Hitoshi Nakatogawa, Sandro Alves, Krisztina Takács-Vellai, Masato Koike, Debasish Sinha, Shoji Notomi, Faraj Terro, Maria Carmela Roccheri, Santiago Ambrosio, K. Ulrich Bayer, Yumin Li, Terje Johansen, Christian Kuhn, Yee Shin Lin, David C. Rubinsztein, Ziwei Qu, Ronit Shiri-Sverdlov, Emmanuel T. Akporiaye, Galila Agam, Hui Ling Chiang, Seung-Jae Lee, Yu Xue, Francesca Giampieri, Markus Damme, Tassula Proikas-Cezanne, Tianwei Lin, Marc Kantorow, Guang-Chao Chen, Qiangrong Liang, Claudia Manzoni, Joan S. Steffan, Emilio Boada-Romero, Damien Freyssenet, Sepp D. Kohlwein, Maria D. Barrachina, Yulin Liao, Jiankang Chen, Erika Isono, Hugo Seca, Mei Wang, Taras Y. Nazarko, Yannick Bailly, Nadya V. Koshkina, Tapas K. Maiti, Bärbel Rohrer, Karin Nowikovsky, James H. Hurley, Gerald W. Dorn, Nils C. Gassen, Kazuhiro Nagata, Eiki Kominami, A. Ivana Scovassi, Ana Maria Cuervo, Adi Kimchi, Minghua Yang, Sylviane Muller, Life Sciences Institute and Department of Molecular, Cellular, and Developmental Biology and Biological Chemistry, University of Michigan [Ann Arbor], University of Michigan System-University of Michigan System, Defense in Plant-Pathogen Interactions [Nagoya, Japan], Nagoya University-Graduate School of Bioagricultural Sciences [Nagoya, Japan], Facultad de Quimica [Santiago], Pontificia Universidad Católica de Chile (UC), Institute of Cancer Sciences [Glasgow, UK] (CR-UK Beatson Institute), University of Glasgow, Cell Death Research & Therapy (CDRT) Lab, Université Catholique de Louvain, Harvard University Statistics Department, Harvard University [Cambridge], Centre épigénétique et destin cellulaire (EDC (UMR_7216)), Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), Conway Institute of Biomolecular and Biomedical Research and School of Chemical and Bioprocess Engineering, University College Dublin [Dublin] (UCD), Immunobiologie des Cellules dendritiques, Institut Pasteur [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Biochemistry and Molecular Biology, Thomas Jefferson University-Sidney Kimmel Cancer Center, Jefferson (Philadelphia University + Thomas Jefferson University)-Jefferson (Philadelphia University + Thomas Jefferson University), Centro de Estudios Farmacológicos y Botánicos [Buenos Aires] (CEFYBO), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET)-Facultad de Medicina [Buenos Aires], Universidad de Buenos Aires [Buenos Aires] (UBA)-Universidad de Buenos Aires [Buenos Aires] (UBA), Thérapie génique, Génomique et Epigénomique (U 1169), Université Paris-Saclay-Institut National de la Santé et de la Recherche Médicale (INSERM)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Sud - Paris 11 (UP11), Department of Experimental Medicine and Public Health, University of Camerino, MRC Toxicology Unit, University of Leicester, Génomique Fonctionnelle des Tumeurs Solides (U1162), Université Paris 13 (UP13)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut de médecine moléculaire de Rangueil (I2MR), Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-IFR150-Institut National de la Santé et de la Recherche Médicale (INSERM), Departamento de Bioquímica y Biología Molecular y Celular, University of Zaragoza - Universidad de Zaragoza [Zaragoza], Department of Pharmaco-Biology, Università della Calabria [Arcavacata di Rende] (Unical), Department of Molecular Genetics [Rehovot, Israël], Weizmann Institute of Science, Fondation Universitaire Notre Dame de la Paix (FUNDP), Facultés Universitaires Notre-Dame de la Paix, Département Advanced Research And Techniques For Multidimensional Imaging Systems (ARTEMIS), Institut Mines-Télécom [Paris] (IMT)-Télécom SudParis (TSP), USC Neuromuscular Center, Department of Neurology, University of Southern California (USC), Centre méditérannéen de médecine moléculaire (C3M), Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM), Giannina Gaslini Institute, Department of Molecular Pharmacology, Albert Einstein College of Medicine, Department of Cancer Biology, University of Massachusetts Medical School [Worcester] (UMASS), University of Massachusetts System (UMASS)-University of Massachusetts System (UMASS), Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École pratique des hautes études (EPHE)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226-Centre National de la Recherche Scientifique (CNRS), Inner Mongolia Agricultural University (IMAU), Franche-Comté Électronique Mécanique, Thermique et Optique - Sciences et Technologies (UMR 6174) (FEMTO-ST), Université de Franche-Comté (UFC)-Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Supérieure de Mécanique et des Microtechniques (ENSMM)-Université de Technologie de Belfort-Montbeliard (UTBM), Indian Institute of Science [Bangalore] (IISc Bangalore), Politecnico di Milano [Milan] (POLIMI), Département des Sciences Biologiques [Montréal], Université du Québec à Montréal (UQAM), Laboratory of Molecular Biology, Scientific Institute E. Medea, Université Catholique de Louvain (UCL), Univ Ancona, Politecn Marche, University of Toronto, Munich Cluster for systems neurology [Munich] (SyNergy), Technische Universität München [München] (TUM)-Ludwig-Maximilians-Universität München (LMU), Institut de Recherche sur le Cancer et le Vieillissement (IRCAN), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA), Department of Clinical and Molecular Medicine, Università degli Studi di Roma 'La Sapienza' [Rome]-Réseau International des Instituts Pasteur (RIIP)-Institut Pasteur, Fondation Cenci Bolognetti - Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Réseau International des Instituts Pasteur (RIIP), Physiopathologie du système nerveux central - Institut François Magendie, Université Bordeaux Segalen - Bordeaux 2-IFR8-Institut National de la Santé et de la Recherche Médicale (INSERM), Laboratoire d'Hémato-Cancérologie Expérimentale, CRP-Santé, Dpt of Neuroscience and Brain Technologies [Genova], NeuroEngineering & bio-arTificial Synergic SystemS Laboratory [Genova] (NetS3 Lab), Istituto Italiano di Tecnologia (IIT)-Istituto Italiano di Tecnologia (IIT), Center for Infection and Immunity Amsterdam (CINIMA), Laboratoire de biogenèse membranaire (LBM), Université Bordeaux Segalen - Bordeaux 2-Centre National de la Recherche Scientifique (CNRS), Centre de résonance magnétique biologique et médicale (CRMBM), Aix Marseille Université (AMU)-Assistance Publique - Hôpitaux de Marseille (APHM)-Centre National de la Recherche Scientifique (CNRS), Régulation de l'expression génétique (REG), Département de Biologie - ENS Paris, École normale supérieure - Paris (ENS Paris)-École normale supérieure - Paris (ENS Paris)-Centre National de la Recherche Scientifique (CNRS), Dynamique des interactions membranaires normales et pathologiques (DIMNP), Université Montpellier 1 (UM1)-Université Montpellier 2 - Sciences et Techniques (UM2)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Institut de Biologie Intégrative de la Cellule (I2BC), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Centre National de la Recherche Scientifique (CNRS)-Université Paris-Saclay, Institut de Recherche en Infectiologie de Montpellier (IRIM), Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS), Department of Microbiology and Immunology, Stanford University School of Medicine [CA, USA], Institut de Myologie, Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Assistance publique - Hôpitaux de Paris (AP-HP) (APHP)-Association française contre les myopathies (AFM-Téléthon)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Department of Dermatology, Brigham and Women's Hospital [Boston], San Raffaele Scientific Institute, Milan, Italy, Laboratory of Molecular Neuroembryology, University of Rome 'Tor Vergeta'-Clinical and Behavioral Neurology - Neuroscienze e riabilitazione, IRCCS Fondazione Santa Lucia [Roma]-Dulbecco Telethon Institute, Department of Pharmacology, Universidade de Santiago de Compostela, Glycobiologie et signalisation cellulaire, Université Paris-Sud - Paris 11 (UP11)-Institut National de la Santé et de la Recherche Médicale (INSERM), Complexo Hospitalario Universitario A Coruña, Mécanismes moléculaires de l'angiogénèse, Université Bordeaux Segalen - Bordeaux 2-Institut National de la Santé et de la Recherche Médicale (INSERM), University of Florida [Gainesville], Centre de Recherche Jean-Pierre AUBERT Neurosciences et Cancer (JPArc - U1172 Inserm), Université Lille Nord de France (COMUE)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Université Lille 2 - Faculté de Médecine, Centro de Investigaciones Biológicas (CSIC), Consejo Superior de Investigaciones Científicas [Spain] (CSIC), Interactions hôte-greffon-tumeur, ingénierie cellulaire et génique - UFC (UMR INSERM 1098) (HOTE GREFFON), Université de Franche-Comté (UFC)-Etablissement français du sang [Bourgogne-France-Comté] (EFS [Bourgogne-France-Comté])-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre de Recherche des Cordeliers (CRC (UMR_S_1138 / U1138)), École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU), Infection bactérienne, inflammation, et carcinogenèse digestive, Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-IFR50-Institut National de la Santé et de la Recherche Médicale (INSERM), Centre des Sciences du Goût et de l'Alimentation [Dijon] (CSGA), Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Centre National de la Recherche Scientifique (CNRS), Universita degli Studi di Padova, University of British Columbia (UBC), University of Edinburgh, Unité de Nutrition Humaine - Clermont Auvergne (UNH), Institut National de la Recherche Agronomique (INRA)-Université Clermont Auvergne (UCA), Australian Regenerative Medicine Institute, Monash University, Clayton, 3800, VIC, Australia, Faculty of Engineering and Natural Sciences, Sabanci University [Istanbul], Department of Biological Sciences [Stanford], Stanford University [Stanford], Université de Montréal (UdeM), Department of Human Genetics, Department of Psychiatry, University of Michigan System-University of Michigan System-Molecular and Behavioral Neuroscience Institute, Centre for Computational and Systems Biology (COSBI), Department of Computer Science [Tsukuba], Graduate School of Systems and Information Engineering [Tsukuba], University of Tsukuba-University of Tsukuba, Institut de biochimie et génétique cellulaires (IBGC), University of Western Ontario (UWO), Genetics, Dynamique Musculaire et Métabolisme (DMEM), Institut National de la Recherche Agronomique (INRA)-Université de Montpellier (UM), Department of Biochemistry and Biophysics, University of Naples Federico II, Lund University [Lund], Institute of Molecular Biosciences, Karl-Franzens University Graz, (IMB), Karl-Franzens-Universität Graz, Polytechnic University of Marche, Centre de Recherche en Cancérologie de Marseille (CRCM), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Aix Marseille Université (AMU), Cell Biology, Physiology and Immunology, Research Unit on BioActive Molecules, Departamento de Química Orgánica Biológica, Instituto de Investigaciones Quimicas y Ambientales de Barcelona, Department of Experimental Oncology and Molecular Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Physiopathologie et thérapie du muscle strié, Université Pierre et Marie Curie - Paris 6 (UPMC)-IFR14-Institut National de la Santé et de la Recherche Médicale (INSERM), The Buck Institute for Age Research, University of Pisa - Università di Pisa, Laboratorio di Genetica Molecolare, Istituto Gaslini, Universidad de Castilla-La Mancha (UCLM), Laboratoire de Biologie Moléculaire et Cellulaire du Cancer, Hôpital Kirchberg, University of Crete [Heraklion] (UOC), Division of Molecular and Cellular Pathology [Birmingham], Department of Medical Research, Taichung Veterans General Hospital, Modélisation et Simulation Numérique en Mécanique et Génie des Procédés (MSNMGP), Université de la Méditerranée - Aix-Marseille 2-Université Paul Cézanne - Aix-Marseille 3-Université de Provence - Aix-Marseille 1-Centre National de la Recherche Scientifique (CNRS), University of Queensland [Brisbane], Dept of Mathematics, Purdue University, Purdue University [West Lafayette], Virologie et Pathologie Humaine (VirPath), École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Laboratoire de chimie de coordination (LCC), Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Institut de Chimie de Toulouse (ICT-FR 2599), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Zhejiang University, Équipe Micro et nanosystèmes HyperFréquences Fluidiques (LAAS-MH2F), Laboratoire d'analyse et d'architecture des systèmes (LAAS), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse 1 Capitole (UT1)-Université Toulouse - Jean Jaurès (UT2J)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Université Toulouse 1 Capitole (UT1)-Université Toulouse - Jean Jaurès (UT2J), King Abdullah University of Science and Technology (KAUST), Southern University of Science and Technology of China (SUSTech), OASE, National University of Tainan, Taiwan (OASE), National Taiwan University [Taiwan] (NTU), Weifang Bureau of Land Resources [Weifang], Department of cardiology [Guy's and St. Thomas ' hospitals] [London], Guy's and St Thomas' Hospital [London]-Guy's Hospital [London], University of Pennsylvania [Philadelphia], CRLCC Eugène Marquis (CRLCC), Emory University School of Medicine, Emory University [Atlanta, GA], Korea University, Cytokines et Immunologie des Tumeurs Humaines (U753), Université Paris-Sud - Paris 11 (UP11)-Institut Gustave Roussy (IGR)-Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Pharmacology [Tartu, Estonie], Institute of Biomedicine and Translational Medicine [Tartu, Estonie], University of Tartu-University of Tartu, Max-Planck-Institut für Biophysikalische Chemie - Max Planck Institute for Biophysical Chemistry [Göttingen], Max-Planck-Gesellschaft, University of Pittsburgh (PITT), Pennsylvania Commonwealth System of Higher Education (PCSHE), University of Cincinnati (UC), Réponses immunes : régulation et développement, Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Experimental Medicine, Oxford University, University of Oxford [Oxford], Division of regenerative Medicine, San Raffaele Scientific Institute, The University of New Mexico [Albuquerque], Université Libre de Bruxelles [Bruxelles] (ULB), Macrophages et Développement de l'Immunité, Institut Pasteur [Paris]-Centre National de la Recherche Scientifique (CNRS), Department of Molecular Microbiology and Immunology, Johns Hopkins Bloomberg School of Public Health [Baltimore], Johns Hopkins University (JHU)-Johns Hopkins University (JHU), Institut du Cerveau et de la Moëlle Epinière = Brain and Spine Institute (ICM), Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pitié-Salpêtrière [APHP]-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Dipartimento di Scienze Biomediche, Università degli Studi di Modena e Reggio Emilia (UNIMORE), Department of Experimental Medicine and Oncology, University of Turin, Institut de Génomique Fonctionnelle (IGF), Université de Montpellier (UM)-Université Montpellier 1 (UM1)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 2 - Sciences et Techniques (UM2)-Centre National de la Recherche Scientifique (CNRS), CNV, University of Valparaiso, Institut Gustave Roussy (IGR), Universidad Autonoma de Madrid (UAM), Cell Signalling & Proteomics Group [Londres, Royayme-Uni], Barts Cancer Institute [Londres, Royayme-Uni], Queen Mary University of London (QMUL)-Queen Mary University of London (QMUL), Department of General, Visceral and Vascular Surgery [Jena], Friedrich-Schiller-Universität Jena, Department of Biomedical Engineering, The University of Texas at Austin, University of Texas at Austin, Microbes, Intestin, Inflammation et Susceptibilité de l'Hôte - Clermont Auvergne (M2iSH), Institut National de la Recherche Agronomique (INRA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Clermont Auvergne (UCA)-Centre de Recherche en Nutrition Humaine d'Auvergne (CRNH d'Auvergne), Fondazione Santa Lucia (IRCCS), Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Jacques Monod (IJM (UMR_7592)), Institute of Biological, Environmental and Rural Sciences (IBERS), Aberystwyth University, Department of Biology, Johns Hopkins University (JHU), Neurogenetics Group, Instituto de Investigación en Recursos Cinegéticos (IREC), Laboratório de Ultraestrutura Celular Hertha Meyer (IBCCF), Universidade Federal do Rio de Janeiro [Rio de Janeiro] (UFRJ), Eidgenössische Technische Hochschule - Swiss Federal Institute of Technology in Zürich [Zürich] (ETH Zürich), Molecular and Cellular Biology, Catholic University of Leuven - Katholieke Universiteit Leuven (KU Leuven), National University of Ireland [Galway] (NUI Galway), Institut des Maladies Neurodégénératives [Bordeaux] (IMN), Université de Bordeaux (UB)-Centre National de la Recherche Scientifique (CNRS), Freiburg Institute for Advanced Studies-LifeNet, Albert-Ludwigs-Universität Freiburg, Groupe de Recherche en Immunopathologies et maladies infectueuses (GRI), Université de La Réunion (UR)-Centre hospitalier Félix-Guyon [Saint-Denis, La Réunion], Brunel University London [Uxbridge], Unité Propre de Recherche 2357, Institution de Biologie Moléculaire des Plantes, Radiothérapie moléculaire (UMR 1030), Department of Chemistry, University of Kentucky, Universidad de Córdoba [Cordoba], Institut Pasteur, Fondation Cenci Bolognetti - Istituto Pasteur Italia, Fondazione Cenci Bolognetti, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Università degli Studi di Roma 'La Sapienza' [Rome], Facultad de Ciencias Químicas y Farmacéuticas, Centro de Estudios Moleculares de la Célula, Biochemistry and Molecular Biology, Goethe-University Frankfurt am Main, Department of Biological and Environmental Sciences and Technologies (DiSTeBA), Università del Salento, Institut Bergonié - Département de médecine, Université Bordeaux Segalen - Bordeaux 2-Centre régional de lutte contre le cancer [CRLCC], Institut National Polytechnique de Lorraine (INPL), Récepteurs nucléaires, maladies cardiovasculaires et diabète (EGID), Université de Lille, Droit et Santé-Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille), Unité de Recherche sur les Maladies Cardiovasculaires, du Métabolisme et de la Nutrition = Institute of cardiometabolism and nutrition (ICAN), Assistance publique - Hôpitaux de Paris (AP-HP) (APHP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pitié-Salpêtrière [APHP]-Sorbonne Université (SU), Institut de recherches sur la catalyse et l'environnement de Lyon (IRCELYON), Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS), Laboratoire de signalisation moléculaire et neurodégénerescence, Université Louis Pasteur - Strasbourg I-IFR37-Institut National de la Santé et de la Recherche Médicale (INSERM), Institut Européen de Chimie et Biologie (IECB), Centre National de la Recherche Scientifique (CNRS)-Université de Bordeaux (UB)-Institut National de la Santé et de la Recherche Médicale (INSERM), Trafic membranaire et Division cellulaire, Landesbetrieb Hessisches Landeslabor, Hematology-Oncology Division, Perelman School of Medicine, University of Pennsylvania [Philadelphia]-University of Pennsylvania [Philadelphia], University of Pavia, Instituto de Investigaciones Biotecnológicas [San Martín] (IIB-INTECH), Universidad Nacional de San Martin (UNSAM)-Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET), University of Helsinki, School of Physics and Astronomy [Exeter], University of Exeter, Department of Biomedicinal Chemistry (CSIC), Institut de Química Avançada de Catalunya, Laboratory of Vascular Pathology (IDI-IRCCS), Istituto Dermopatico dell'Immacolata, Peking University [Beijing], MRC Centre for Developmental Neurobiology, University of Brescia, Immunobiologie fondamentale et clinique, Université de Lyon-Université de Lyon-IFR128-Institut National de la Santé et de la Recherche Médicale (INSERM), CIC régional épidémiologie clinique/essais cliniques - Ile de la Réunion (CIC-EC), University of Rome 'Tor Vergeta', Universidad de Oviedo [Oviedo], Laboratoire des signaux et systèmes (L2S), Université Paris-Sud - Paris 11 (UP11)-CentraleSupélec-Centre National de la Recherche Scientifique (CNRS), Dulbecco Telethon Institute/Department of Biology, Istituto Nazionale di Malattie Infettive 'Lazzaro Spallanzani' (INMI), Rockefeller University [New York], The Babraham Institute, Kansas State University, McGill University, Service d'Anatomie et Cytologie Pathologique [Rouen], CHU Rouen, Normandie Université (NU)-Normandie Université (NU)-Université de Rouen Normandie (UNIROUEN), Normandie Université (NU), Laboratoire Interuniversitaire de Biologie de la Motricité (LIBM ), Université de Lyon-Université de Lyon-Université Jean Monnet [Saint-Étienne] (UJM)-Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry]), Department of Medicine [New York], Icahn School of Medicine at Mount Sinai [New York] (MSSM), ATOS Origin, Department of Developmental Biology and Neurosciences, Graduate School of Life Sciences-Tohoku University [Sendai], Goethe-University, Goethe-Universität Frankfurt am Main, Institute of physiological chemistry, Hannover Medical School [Hannover] (MHH), Department of Physiology, Department of Plant and Environmental Sciences, Apoptose, cancer et immunité (U848), Laboratoire de Biologie du Développement (LBD), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Departments of Neurology and Psychiatry, Alzheimer's Disease Research Center, Institute of Experimental Immunology - IEI [Zürich, Switzerland], Université de Zurich [Switzerland], Digital Enterprise Research Institute (DERI-NUIG), Spanish National Research Council (CSIC), Cell Death Research and Therapy Unit [Leuven, Belgium] ( Department of Cellular and Molecular Medicine), Centre d'Immunologie de Marseille - Luminy (CIML), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU), Signaling in Oncogenesis, Angiogenesis and Permeability - SOAP (CRCINA - Département ONCO - Equipe 15), Centre de recherche de Cancérologie et d'Immunologie / Nantes - Angers (CRCINA), Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN), Department of Medicine [San Francisco], University of California [San Francisco] (UCSF), University of California-University of California, Fondazione Santa Lucia [IRCCS], Clinical and Behavioral Neurology [IRCCS Santa Lucia], Institut de biologie moléculaire des plantes (IBMP), Université de Strasbourg (UNISTRA)-Centre National de la Recherche Scientifique (CNRS), Unité de Recherche sur les Maladies Infectieuses et Tropicales Emergentes (URMITE), Institut de Recherche pour le Développement (IRD)-Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR48, INSB-INSB-Centre National de la Recherche Scientifique (CNRS), Department of Anatomy, Histology, Forensic Medicine and Orthopedic, N.A., Division of Pharmacology and Chemotherapy, Department of Internal Medicine, Pathogénie Microbienne Moléculaire, University of Chile [Santiago], Université de Montpellier (UM), Faculdade de Ciências Farmacêuticas de Ribeirão Preto [São Paulo], Universidade de São Paulo (USP), Centro de Investigación Biomédica en Red en Enfermedades Neurodegenerativas (CIBERNED), Institut de recherche en cancérologie de Montpellier (IRCM - U896 Inserm - UM1), CRLCC Val d'Aurelle - Paul Lamarque-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Montpellier 1 (UM1), Catalan Institute of Oncology, Department of Cell Biology, National Institute for Basic Biology [Okazaki], Instituto de Bioquímica Vegetal y Fotosíntesis (IBVF), Universidad de Sevilla-Centro de Investigaciones Científicas Isla de la Cartuja, The Adams Super Center for Brain Studies, Tel Aviv University [Tel Aviv], Institut de Biologie du Développement de Marseille (IBDM), Aix Marseille Université (AMU)-Collège de France (CdF)-Centre National de la Recherche Scientifique (CNRS), Department of Pharmacology and biochemistry, Virginia Commonwealth University (VCU), Department of Immunology, St Jude Children's Research Hospital, Department of Biology and Biotechnologies 'Charles Darwin', Lettres, Idées, Savoir (LIS), Université Paris-Est Créteil Val-de-Marne - Paris 12 (UPEC UP12), Institute of Biological Chemistry and Nutrition, University of Hohenheim, China Seismological Bureau, Massachusetts Institute of Technology (MIT), Rosenstiel Basic Medical Sciences Research Center [Waltham], Brandeis University, Institut Necker Enfants-Malades (INEM - UM 111 (UMR 8253 / U1151)), Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université de Strasbourg (UNISTRA), Meakins-Christie Laboratories, Sanford Burnham Medical Research Institute, La Jolla, National Institute of Advanced Industrial Science and Technology (AIST), ORIENT ET MÉDITERRANÉE : Textes, Archéologie, Histoire (OM), Université Panthéon-Sorbonne (UP1)-École pratique des hautes études (EPHE)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), David Geffen School of Medicine [Los Angeles], University of California [Los Angeles] (UCLA), Ludwig Institute for Cancer Research, Royal Melbourne Hospital, Centro de Investigacion y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV), Biochemistry and Molecular Biology I, Department of Immunology and Infectious Diseases, Harvard School of Public Health, aDepartment of Plant Biology, Uppsala BioCenter, Swedish University of Agricultural Sciences (SLU), Philipps University of Marburg, Cologne Excellence Cluster on Cellular Stress Responses in Aging-Associated Diseases (CECAD), University of Cologne, Renal Division, University Medical Center Freiburg, Freiburg, Germany, Rural Health Academic Centre, University of Melbourne-Rural Clinical School, Department of Pathology, University of Veterinary and Animal Sciences, Dipartimento di Scienze della Vita [Modena, Italy], Stress Cellulaire, Université de la Méditerranée - Aix-Marseille 2-Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Pathology, Anatomy & Cell Biology [Philadelphia, Pennsylvania, USA], Thomas Jefferson University, Department of Molecular Neuroscience, Departamento de Bioquimica Clinica, Facultad de Ciencias Quimicas, Centro de Investigación en Bioquímica Clínica e Inmunología (CONICET), Universidad Nacional de Córdoba, Córdoba, Argentina, Neuroinflammation Unit, Biotech Research and Innovation Centre-University of Copenhagen = Københavns Universitet (KU), Mathematics and Computing in Automatic Control and Optimization for the User (MIAOU), Inria Sophia Antipolis - Méditerranée (CRISAM), Institut National de Recherche en Informatique et en Automatique (Inria)-Institut National de Recherche en Informatique et en Automatique (Inria), Centre de Recherche des Cordeliers (CRC), Université Paris Diderot - Paris 7 (UPD7)-École pratique des hautes études (EPHE)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Danish Cancer Society, Institute of Cancer Biology, UCL-Institute of Child Health (ICH), Institute of Child Health-Great Ormond Street Hospital for Children [London] (GOSH), Division of Renal Diseases and Hypertension, University of Colorado [Boulder], Institut de biologie et chimie des protéines [Lyon] (IBCP), Joslin Diabetes Center, Universität Ulm - Ulm University [Ulm, Allemagne], Qingdao Institute of Marine Geology, China Geological Survey, Qingdao 266071, China, Université Paris Diderot - Paris 7 (UPD7), Institute of Software, Chinese Academy of Sciences [Beijing] (CAS), Metabolic Engineering Group, Departamento de Microbiologia y Genetica, Edificio Departamental, Campus Miguel de Unamuno, Universidad de Salamanca, University of Minnesota [Twin Cities], University of Minnesota System, Department of Cellular and Molecular Physiology, Yale University School of Medicine, The Arctic University of Norway, Department of Biological Sciences, The Open University [Milton Keynes] (OU), Summit Analytical, CALRG, Institute of Educational Technology, Institute for Neurologic Disabilities Research, Faculty of Health Sciences-University of Pretoria [South Africa], Department of Paediatric Neurology, Guy's and St Thomas' Hospital [London]-Evelina Children's Hospital, Physiologie des Adaptations Nutritionnelles [UMR_A1280] (PhAN), Institut National de la Recherche Agronomique (INRA)-Université de Nantes (UN), Dana-Farber Cancer Institute and the Department of Cell Biology, Harward Medical School, Translational Health Science and Technology Institute [Faridabad] (THSTI), Department of Biomedical Sciences of Cells and Systems, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands, School of Reliability and Systems Engineering [Beijing], Beihang University, Oxford Centre for Integrative Systems Biology, Center for Membrane and Cell Physiology [Charlottesville, VA, USA] (School of Medicine), University of Virginia [Charlottesville], Apoptose, cancer et immunité (Equipe labellisée Ligue contre le cancer - CRC - Inserm U1138), Institut Gustave Roussy (IGR)-Centre de Recherche des Cordeliers (CRC (UMR_S_1138 / U1138)), École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU), St James's University Hospital, Leeds Teaching Hospitals NHS Trust, Karlsruher Institut für Technologie (KIT), Faculty of Pharmaceutical Sciences, Hokkaido University, École normale supérieure - Paris (ENS Paris), School of Electrical Engineering [Seoul] (Korea University), Department of Mathematics and Statistics [Guelph], University of Guelph, Department of Molecular Genetics, Department of Genetics [Stanford, CA, États-Unis], Institute of Immunology, University Hospital Schleswig-Holstein, Arizona Respiratory Center, Okazaki Institute for Integrative Bioscience, ToxAlim (ToxAlim), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Recherche Agronomique (INRA), Newcastle University [Newcastle], JRC Institute for Transuranium Elements [Karlsruhe] (ITU ), European Commission - Joint Research Centre [Karlsruhe] (JRC), Department of Neuroscience, University of Texas Southwestern Medical Center [Dallas], Centre de génétique et de physiologie moléculaire et cellulaire (CGPhiMC), Laboratory of Functional Neurogenomics [Tuebingen, Germany], University of Tuebingen-Center of Neurology and Hertie-Institute for Clinical Brain Research [Tuebingen, Germany], Indian Institute of Technology Bombay (IIT Bombay), European Organization for Nuclear Research (CERN), Harvard Medical School [Boston] (HMS), Indian School of Mines, Department of Computer Science [UIUC] (UIUC), University of Illinois at Urbana-Champaign [Urbana], University of Illinois System-University of Illinois System, Centre for Cancer Biology, Hanson Institute, Adelaide, University of California [San Diego] (UC San Diego), University of California, Centre d’Infection et d’Immunité de Lille (CIIL) - U1019 - UMR 8204 (CIIL), Institut Pasteur de Lille, Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre National de la Recherche Scientifique (CNRS), Department of Biochemistry, University of Bristol, Organisation Nucléaire et Oncogenèse, Institut de génétique et biologie moléculaire et cellulaire (IGBMC), Université Louis Pasteur - Strasbourg I-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), FONDAP Center CEMC Estudios Moleculares de la Célula, Unité de Biologie Fonctionnelle et Adaptative (BFA (UMR_8251 / U1133)), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7), Centre d'infectiologie Necker-Pasteur [CHU Necker], CHU Necker - Enfants Malades [AP-HP], Chungnam National Univesity School of Medicine, Taejon, Korea, Chungnam National Univesity School of Medicine, Micro & Nanobiotechnologies, Institut des Sciences Analytiques (ISA), Centre National de la Recherche Scientifique (CNRS)-Université de Lyon-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-École normale supérieure - Lyon (ENS Lyon)-Centre National de la Recherche Scientifique (CNRS)-Université de Lyon-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-École normale supérieure - Lyon (ENS Lyon), Centre de Recherche en Cancérologie de Lyon (CRCL), Université de Lyon-Université de Lyon-Centre Léon Bérard [Lyon]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre de génétique moléculaire (CGM), Université Paris-Sud - Paris 11 (UP11)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Center for Applied Mathematics, Tsinghua University [Beijing], University of Connecticut School of Medicine, University of Connecticut (UCONN), Laboratoire de Biologie Moléculaire et Cellulaire des Eucaryotes (LBMCE), Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Microenvironnement et Physiopathologie de la Differenciation, Division of Nephrology and Hypertension, Mayo Clinic, Beatson Institute for Cancer Research, Beatson institute for cancer research, Howard Hughes Medical Institute, Howard Hugues Medical Institute, Institut des Maladies Métaboliques et Cardiovasculaires (I2MC), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM), Institute of Computing Technology [Beijing] (ICT), Chinese Academy of Sciences [Changchun Branch] (CAS), School of Electronics and Computer Science (ECS), University of Southampton, Third Hospital, Department of Anesthesiology, Cognitive Interaction Technology [Bielefeld] (CITEC), Universität Bielefeld = Bielefeld University, Procédés, Matériaux et Energie Solaire (PROMES), Université de Perpignan Via Domitia (UPVD)-Centre National de la Recherche Scientifique (CNRS), Faculty of Pharmacy- University of Coimbra, National Neuroscience Institute, Key Laboratory of Molecular Virology & Immunology (LMVI), Institut Pasteur de Shanghai, Académie des Sciences de Chine - Chinese Academy of Sciences (IPS-CAS), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP), Coll Life Sci, Beijing Normal University, Delft University of Technology (TU Delft), Christian-Albrechts-Universität zu Kiel (CAU), Department of Molecular Pathology and Microbiology, Center for Applied Proteomics and Molecular Medicine-George Mason University [Fairfax], Sidney Kimmel Cancer Center, Jefferson (Philadelphia University + Thomas Jefferson University), Institut des Sciences Chimiques de Rennes (ISCR), Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Centre National de la Recherche Scientifique (CNRS)-Ecole Nationale Supérieure de Chimie de Rennes-Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES), Department of Chemistry, University of Pittsburgh, University of Pittsburg, Tianjin University of Science and Technology (TUST), Hunan University of Science and Technology [Xiangtan], Laboratoire de Génie Civil et Génie Mécanique (LGCGM), Université de Rennes 1 (UR1), Université de Rennes (UNIV-RENNES)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées - Rennes (INSA Rennes), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA), China Agricultural University (CAU), Acad Disaster Reduct and Emergency Management, Minist Civil Affairs, Minist Educ, Beijing, Peoples R China, affiliation inconnue, Département Technologie des Polymères et Composites & Ingénierie Mécanique (TPCIM), École des Mines de Douai (Mines Douai EMD), Institut Mines-Télécom [Paris] (IMT)-Institut Mines-Télécom [Paris] (IMT)-Ministère de l'Economie, des Finances et de l'Industrie, MOE Key Laboratory of Bioinformatics, Centre for Plant Biology, School of Life Sciences, Laboratoire d'Informatique Gaspard-Monge (ligm), Université Paris-Est Marne-la-Vallée (UPEM)-École des Ponts ParisTech (ENPC)-ESIEE Paris-Fédération de Recherche Bézout-Centre National de la Recherche Scientifique (CNRS), Laboratoire de Biochimie Moléculaire et Cellulaire (LBMC), Université de Bourgogne (UB), Center for International Blood and Marrow Transplant Research (CIBMTR), Emory University [Atlanta, GA]-Medical College of Wisconsin, Centre de biophysique moléculaire (CBM), Université d'Orléans (UO)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Illman Cancer Center, Pennsylvania Commonwealth System of Higher Education (PCSHE)-Pennsylvania Commonwealth System of Higher Education (PCSHE), Ingénierie des Matériaux Polymères (IMP), Université de Lyon-Université de Lyon-Institut National des Sciences Appliquées de Lyon (INSA Lyon), Université de Lyon-Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Jean Monnet [Saint-Étienne] (UJM)-Centre National de la Recherche Scientifique (CNRS), Université Côte d'Azur (UCA), Department of Medical Microbiology and Immunology, University of California [Davis] (UC Davis), School of Health Sciences, University of Minho [Braga], Équipe Calcul Distribué et Asynchronisme (LAAS-CDA), University of California [Riverside] (UCR), Ohio State University [Columbus] (OSU), Laboratory of Systems Biology, Van Andel Institute [Grand Rapids], Division of Genetics and Cell Biology, National Center for Gender-Specific Medicine, Istituto Superiore di Sanità, Oregon Health and Science University [Portland] (OHSU), Dendrite Differenciation Group [DZNE - Bonn], German Research Center for Neurodegenerative Diseases - Deutsches Zentrum für Neurodegenerative Erkrankungen (DZNE), Equipe 12, Génétique moléculaire, signalisation et cancer (GMSC), Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre de Recherche en Cancérologie de Lyon (CRCL), Université de Lyon-Université de Lyon-Centre Léon Bérard [Lyon]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre Léon Bérard [Lyon]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), University Medical Center [Utrecht], Institut d'Investigacions Biomèdiques August Pi I Sunyer [Barcelona, Spain] (Hospital Clinic ), Department of Genetics, Trinity College Dublin, Fisiopatologia de los procesos inflamatorios, Vall d'Hebron Research Institute, Institució Catalana de Recerca i Estudis Avançats (ICREA), Department of Human Genetics, Nagasaki University, Transduction du signal et oncogénèse, Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Curie, Center for Experimental and Molecular Medicine, Academic Medical Center - Academisch Medisch Centrum [Amsterdam] (AMC), University of Amsterdam [Amsterdam] (UvA)-University of Amsterdam [Amsterdam] (UvA), Department of medical Biochemistry, University of Amsterdam [Amsterdam] (UvA), IDI-IRCCS Biochemistry Laboratory, Università degli Studi di Roma Tor Vergata [Roma], Program Against Cancer Therapeutic Resistance/Metabolism & Cancer Group [Catalonia, Spain] (ProCURE), Catalan Institute of Oncology-Girona (ICO-Girona), Instituto de Tecnologia Química e Biológica António Xavier (ITQB), Universidade Nova de Lisboa (NOVA), Medical Genetics Unit, IRCCS Casa Sollievo della Sofferenza Hospital, CNR, Consiglio Nazionale delle Ricerche (CNR), Biochimie et Physiologie Moléculaire des Plantes (BPMP), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Laboratory for Developmental Neurobiology, RIKEN Brain Science Institute, The Hospital for sick children [Toronto] (SickKids), Universidad de Sevilla, Immunité muqueuse et vaccination, Institut National de la Santé et de la Recherche Médicale (INSERM)-IFR50-Université Nice Sophia Antipolis (... - 2019) (UNS), DIMS, University of Trento [Trento], Laboratoire de Biologie Moléculaire de la Cellule (LBMC), Department of Cellular and Molecular Medicine [Madrid, Spain], Laboratory of Cell Death and Cancer Therapy [Madrid, Spain], Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC) -Centro de Investigaciones Biológicas, Consejo Superior de Investigaciones Científicas (CSIC), Plymouth Marine Laboratory, Prospect Place, The Hoe, Plymouth PL1 3HD, UK, Centre d'Immunologie et de Maladies Infectieuses (CIMI), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Dpt. of Cancer & Cell Biology, Interactions Bactéries-Cellules (UIBC), Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur [Paris]-Institut National de la Recherche Agronomique (INRA), Max planck Institute for Biology of Ageing [Cologne], Euromov (EuroMov), Wellcome Trust Centre for Molecular Parasitology [Glasgow, UK], University of Glasgow- Institute of Infection, Immunity and Inflammation [Glasgow, UK], Immunologie et chimie thérapeutiques (ICT), Cancéropôle du Grand Est-Centre National de la Recherche Scientifique (CNRS), UMR 1599, Centre National de la Recherche Scientifique (CNRS), EA 4100, Histoire culturelle et sociale de l'art (HiCSA), Université Panthéon-Sorbonne (UP1)-Université Panthéon-Sorbonne (UP1), Centre for Astrophysics and Supercomputing (Centre for Astrophysics and Supercomputing), Swinburne University of Technology [Melbourne], Department of Cellular and Physiological Sciences [Vancouver, BC, Canada] (Life Sciences Institute), University of British Columbia (UBC)-Life Sciences Institute [Vancouver, BC, Canada], School of Pharmacy, Department of Experimental Medicine, Dept. Neurosciences, Department of Internal Medicine, Radboud University Medical Center [Nijmegen], Institute of Medical Genetics and Applied Genomics, Radiation Physics, School of Life Science, Department of Basic Biology, The Graduate University for Advanced Studies, CIBER de Enfermedades Neurodegenerativas (CIBERNED), Doshisha University, National Cancer Research Center [Tokyo, Japan], University of Washington [Seattle], Department of Experimental Neurodegeneration [Göttingen, Germany], University Medical Center Göttingen (UMG), Cibles moléculaires et thérapeutiques de la maladie d'Alzheimer (CIMoTHeMA), Université de Poitiers, Laboratoire de Probabilités et Modèles Aléatoires (LPMA), Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Diderot - Paris 7 (UPD7)-Centre National de la Recherche Scientifique (CNRS), BioCeV-Institute of Microbiology, Médecine Personnalisée, Pharmacogénomique, Optimisation Thérapeutique (MEPPOT - U1147), Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Istituto di chimica biologica, Università degli Studi di Verona, Département Image et Traitement Information (ITI), Institut Mines-Télécom [Paris] (IMT)-Université européenne de Bretagne - European University of Brittany (UEB)-Télécom Bretagne, Department of Cell Biology and Biophysics, Università degli Studi di Firenze [Firenze], Cell Immunity in Cancer, Inflammation and infection Group [Zaragoza, Spain] (Biomedical Research Center), Nanoscience Institute of Aragon - INA [Zaragoza, Spain]-Fundación Agencia Aragonesa para la Investigación y el Desarrollo - ARAID [Zaragoza, Spain]-University of Zaragoza - Universidad de Zaragoza [Zaragoza], Department of Pediatrics, Università degli studi di Napoli Federico II, Transfert de Genes a Visee Therapeutique Dans les Cellules Souches, Developpement Normal et Pathologique du Système Immunitaire, Signalisation et physiopathologie des cellules épithéliales, Facultad de Medicina, Universidad de Santiago de Chile [Santiago] (USACH), Departamento de Farmacobiología, Cinvestav-Sede Sur, Centre de recherche Croissance et signalisation (UMR_S 845), College of Life Sciences, Central China Normal University, Institute of Molecular Biotechnology, Austrian Academy of Sciences (OeAW), Laboratory of Cardiac Surgical Research, Monash University [Clayton], Universidade do Minho, Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Neurodegenerative Diseases Research Group (CIBERNED), Vall d'Hebron Research Institute-Center for Networked Biomedical Research on Neurodegenerative Diseases, Barcelona, Department of medicine, Syracuse, NY, USA, State University of New York (SUNY), National University of Singapore (NUS)-Yong Loo Lin School of Medicine-Graduate School for Integrative Sciences and Engineering, McGill University Health Center [Montreal] (MUHC), National Institute for Infectious Diseases, Transporteurs en Imagerie et Radiothérapie en Oncologie (TIRO - UMR E4320), Service Hospitalier Frédéric Joliot (SHFJ), Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-UMR E4320 (TIRO-MATOs), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Université Côte d'Azur (UCA)-Université Côte d'Azur (UCA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Nice Sophia Antipolis (... - 2019) (UNS), Institut Gustave Roussy (IGR)-Centre de Recherche des Cordeliers (CRC), Université Paris Diderot - Paris 7 (UPD7)-École pratique des hautes études (EPHE)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris Diderot - Paris 7 (UPD7)-École pratique des hautes études (EPHE)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Department of Biomedical Sciences, Department of Genetics of Eukaryotic Microorganisms, Georg-August-University [Göttingen]-Institute of Microbiology and Genetics, Sterol metabolism and therapeutic innovations in oncology, Institut Claudius Regaud, CRLCC Institut Claudius Regaud-CRLCC Institut Claudius Regaud-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées, Department of Molecular, Cellular and Developmental Biology, Señalización Celular 4, Institute of integrative biology (Liverpool), University of Liverpool, Department of Human Biology, University of Cape Town, National Institute of Diabetes and Digestive and Kidney Diseases [Bethesda], Department of Molecular Biology, Eberhard Karls Universität Tübingen, Technical University of Munich (TUM), Biophysics and Bioinformatics Laboratory, Department of Cell Biology and Morphology, Université de Lausanne (UNIL), Shenyang Institute of Automation, the Chinese Academy of Sciences (SIA), Key Laboratory of Thermo-Fluid Science and Engineering of Ministry of Education, Xi'an Jiaotong University (Xjtu), Dipartimento di Biologia, Mechanics laboratory , UniversityAmar Telidji, 3000 Laghouat, Algéria., Mechanics laboratory , University Amar Telidji, sans affiliation, Service d'hépatologie [Hôpital Beaujon], Assistance publique - Hôpitaux de Paris (AP-HP) (APHP), University of Waterloo, Waterloo, ON, Canada, Institute of Cell Biology and Immunology, University of Stuttgart, Chaperones Research Group, Institute of Biosciences and Technology [Houston, TX, États-Unis] (IBT), Texas A&M Health Science Center [Houston, TX, États-Unis] (TAMHSC), Texas A&M University Health Science Center-Texas A&M University Health Science Center, Aquatic and Crop Resource Development, National Research Council of Canada (NRC), Cibles thérapeutiques, formulation et expertise pré-clinique du médicament (CITHEFOR), Université de Lorraine (UL), Dipartimento di Scienze Cliniche e Molecolari, Università Politecnica delle Marche [Ancona] (UNIVPM), Department of Biochemistry and Molecular Biology [Indianapolis, IN, USA], Indiana University School of Medicine, Indiana University System-Indiana University System, Wellcome Trust Centre for Gene Regulation and Expression, College of Life Sciences, University of Dundee, iMed.UL, Faculty of Pharmacy, University of Lisbon, CESAM & Biology Department, Universidade de Aveiro, Celullar and Molecular Medicine, Università degli Studi di Perugia (UNIPG), Institute of Clinical Molecular Biology, Kiel University, Apoptose et Système Immunitaire (ASI), Vieillissement Cellulaire Intégré et Inflammation (VCII), Adaptation Biologique et Vieillissement = Biological Adaptation and Ageing (B2A), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Department of Mathematical Sciences [Aalborg], Aalborg University [Denmark] (AAU), Cambridge Institute for Medical Research (CIMR), University of Cambridge [UK] (CAM), Biozentrum, University of Basel (Unibas), Structural and Computational Biology Unit, European Molecular Biology Laboratory [Grenoble] (EMBL), Rutgers New Jersey Medical School (NJMS), Rutgers University System (Rutgers), Université de Perpignan Via Domitia (UPVD), Universidad Pablo de Olavide [Sevilla] (UPO), Department of Neurosciences, Agronomes et Vétérinaires Sans Frontières (AVSF), AVSF, Department of Mathematics [Gakushuin], Gakushuin University, Department of Internal Medicine [Münster, Germany], University of Münster, Neurogenetics laboratory, University Medicine Goettingen, Institut de biologie structurale (IBS - UMR 5075), Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Direction de Recherche Fondamentale (CEA) (DRF (CEA)), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Grenoble Alpes (UGA)-Centre National de la Recherche Scientifique (CNRS), Université d'Uruguay, Laboratoire de Biologie Cellulaire et Moléculaire du Contrôle de la Prolifération (LBCMCP), Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Toulouse III - Paul Sabatier (UT3), Institute for Conservation & Improvement of Valentian Agrodiversity (COMAV), Universitat Politecnica de Valencia (UPV), ICBM, University of Chile [Santiago]-Faculty of Medicine, Nutrition, Métabolisme, Aquaculture (NuMéA), Institut National de la Recherche Agronomique (INRA)-Université de Pau et des Pays de l'Adour (UPPA), Department of Cell Biology, Baltimore, Johns Hopkins University School of Medicine, Baylor College of Medicine (BCM), Baylor University, University of Minnesota Medical School, Beijing Candid soft Technology Co. Ltd, Nanjing University of Information Science and Technology, Department of Hepatobiliary and Pancreatic Surgery [Maebashi, Japan], Gunma University Graduate Schoolof Medicine [Maebashi, Japan], Department of Molecular Genetics [Maastricht, The Netherlands], Maastricht University [The Netherlands], Institute of Cell Biology and Genetic Engineering, National Academy of Sciences of Ukraine (NASU), Institute of Pharmacology of Natural Products and Clinical Pharmacology, Institute of Pharmacology, University of Bern, Imagine - Institut des maladies génétiques (IMAGINE - U1163), Wilmer Eye Institute, Mayo Clinic and Mayo College of Medicine, Rochester, Institute of Biochemistry and Biophysics, Polska Akademia Nauk (PAN)-Sciences, Department of Electrical and Computer Engineering [Waterloo] (ECE), University of Waterloo [Waterloo], Department of Chemistry and Toxicology, Norwegian Veterinary Institute, Department of Gynecologic Oncology, The University of Texas M.D. Anderson Cancer Center [Houston], University of Minho, Friedrich Miescher Laboratory (FML), Charité - Universitätsmedizin Berlin / Charite - University Medicine Berlin, Department of Biomedical Sciences and Biotechnologies, Brescia University, Department of Physiological Chemistry [Bochum], Ruhr-Universität Bochum [Bochum], University of Oslo (UiO), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Saclay, Facultés Universitaires Notre Dame de la Paix (FUNDP), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM), École pratique des hautes études (EPHE)-Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut de recherche pour le développement [IRD] : UR226, Université du Québec à Montréal = University of Québec in Montréal (UQAM), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Paris (ENS Paris), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Association française contre les myopathies (AFM-Téléthon)-Sorbonne Université (SU), Université Lille 2 - Faculté de Médecine -Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Lille Nord de France (COMUE)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille), Institut National de la Santé et de la Recherche Médicale (INSERM)-Etablissement français du sang [Bourgogne-France-Comté] (EFS [Bourgogne-France-Comté])-Université de Franche-Comté (UFC), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-IFR50-Institut National de la Santé et de la Recherche Médicale (INSERM), Aix Marseille Université (AMU)-Institut Paoli-Calmettes, Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Fédération nationale des Centres de lutte contre le Cancer (FNCLCC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Lyon (ENS Lyon), Institut de Chimie de Toulouse (ICT-FR 2599), Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Institut National Polytechnique (Toulouse) (Toulouse INP), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS), Université Toulouse 1 Capitole (UT1)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Institut National des Sciences Appliquées (INSA)-Institut National des Sciences Appliquées (INSA)-Université Toulouse - Jean Jaurès (UT2J)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Toulouse 1 Capitole (UT1)-Institut National des Sciences Appliquées - Toulouse (INSA Toulouse), Université Fédérale Toulouse Midi-Pyrénées, Université libre de Bruxelles (ULB), Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pitié-Salpêtrière [AP-HP], Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS), Universidade Federal do Rio de Janeiro (UFRJ), Institut Bergonié [Bordeaux], UNICANCER, Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pitié-Salpêtrière [AP-HP], Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU), Trafic membranaire et Division cellulaire - Membrane Traffic and Cell Division, Centre National de la Recherche Scientifique (CNRS)-CentraleSupélec-Université Paris-Sud - Paris 11 (UP11), McGill University = Université McGill [Montréal, Canada], Service d'Anatomie et Cytologie Pathologique [CHU Rouen], Centre National de la Recherche Scientifique (CNRS)-Institut de Biologie Paris Seine (IBPS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Centre National de la Recherche Scientifique (CNRS), Signaling in Oncogenesis, Angiogenesis and Permeability (CRCINA-ÉQUIPE 15), Centre de Recherche en Cancérologie et Immunologie Nantes-Angers (CRCINA), Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Nantes - UFR de Médecine et des Techniques Médicales (UFR MEDECINE), Université de Nantes (UN)-Université de Nantes (UN)-Centre hospitalier universitaire de Nantes (CHU Nantes)-Centre National de la Recherche Scientifique (CNRS)-Université d'Angers (UA), Universidad de Chile = University of Chile [Santiago] (UCHILE), Centro de Investigacion Biomédica en Red sobre Enfermedades Neurodegenerativas (CIBERNED), Instituto de Salud Carlos III (ISC), Université Montpellier 1 (UM1)-CRLCC Val d'Aurelle - Paul Lamarque-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Montpellier (UM), Aix Marseille Université (AMU)-Collège de France (CdF (institution))-Centre National de la Recherche Scientifique (CNRS), Université Panthéon-Sorbonne (UP1)-École pratique des hautes études (EPHE)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU)-Collège de France (CdF (institution)), Université Pierre et Marie Curie - Paris 6 (UPMC)-École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Great Ormond Street Hospital for Children [London] (GOSH)-Institute of Child Health, Hokkaido University [Sapporo, Japan], Université Paris sciences et lettres (PSL), Institut National de la Recherche Agronomique (INRA)-Université Toulouse III - Paul Sabatier (UT3), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Ecole Nationale Vétérinaire de Toulouse (ENVT), Université Fédérale Toulouse Midi-Pyrénées-Ecole d'Ingénieurs de Purpan (INPT - EI Purpan), Université de Lyon-Université de Lyon, Centre d’Infection et d’Immunité de Lille (CIIL) - INSERM U1019 - UMR 9017 (CIIL), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Centre National de la Recherche Scientifique (CNRS), Organisation Nucléaire et Oncogenèse - Nuclear Organization and Oncogenesis, Université Paris Diderot - Paris 7 (UPD7)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre de Recherche en Cancérologie de Lyon (UNICANCER/CRCL), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Centre Léon Bérard [Lyon], Centre National de la Recherche Scientifique (CNRS)-Institut de biologie physico-chimique (IBPC (FR_550)), Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Sorbonne Université (SU), The Beatson Institute for Cancer Research, Beijing Normal University (BNU), Institut National des Sciences Appliquées (INSA)-Université de Rennes (UNIV-RENNES)-Institut National des Sciences Appliquées (INSA)-Ecole Nationale Supérieure de Chimie de Rennes-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Fédération de Recherche Bézout-ESIEE Paris-École des Ponts ParisTech (ENPC)-Université Paris-Est Marne-la-Vallée (UPEM), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA), Université de Lyon-Université de Lyon-Centre de Recherche en Cancérologie de Lyon (UNICANCER/CRCL), Université de Lyon-Université de Lyon-Centre Léon Bérard [Lyon]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre Léon Bérard [Lyon], Vall d’Hebron Research Institute (VHIR), Institut Curie [Paris]-Institut National de la Santé et de la Recherche Médicale (INSERM), Universidade Nova de Lisboa = NOVA University of Lisboa (NOVA), Université de Montpellier (UM)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut National de la Recherche Agronomique (INRA)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-École normale supérieure - Lyon (ENS Lyon)-Université Claude Bernard Lyon 1 (UCBL), Doshisha University [Kyoto], Université européenne de Bretagne - European University of Brittany (UEB)-Télécom Bretagne-Institut Mines-Télécom [Paris] (IMT), Università degli Studi di Firenze = University of Florence [Firenze], University of Zaragoza - Universidad de Zaragoza [Zaragoza]-Nanoscience Institute of Aragon - INA [Zaragoza, Spain]-Fundación Agencia Aragonesa para la Investigación y el Desarrollo - ARAID [Zaragoza, Spain], Central China Normal University [Wuhan, China], Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-UMR E4320 (TIRO-MATOs), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Nice Sophia Antipolis (... - 2019) (UNS), COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-COMUE Université Côte d'Azur (2015 - 2019) (COMUE UCA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Université Pierre et Marie Curie - Paris 6 (UPMC)-École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-École pratique des hautes études (EPHE)-Université Paris Diderot - Paris 7 (UPD7)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut Claudius Regaud, Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP), Institut de biologie structurale [1992-2019] (IBS - UMR 5075 [1992-2019]), Université Grenoble Alpes [2016-2019] (UGA [2016-2019])-Centre National de la Recherche Scientifique (CNRS)-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre de Biologie Intégrative (CBI), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Nanjing University of Information Science and Technology (NUIST), Facultad de Medicina [Buenos Aires], Universidad de Buenos Aires [Buenos Aires] (UBA)-Universidad de Buenos Aires [Buenos Aires] (UBA)-Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET), Université de Technologie de Belfort-Montbeliard (UTBM)-Ecole Nationale Supérieure de Mécanique et des Microtechniques (ENSMM)-Centre National de la Recherche Scientifique (CNRS)-Université de Franche-Comté (UFC), Université Clermont Auvergne (UCA)-Institut National de la Recherche Agronomique (INRA), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille, Droit et Santé-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille), Consejo Nacional de Investigaciones Científicas y Técnicas [Buenos Aires] (CONICET)-Universidad Nacional de San Martin (UNSAM), Université Savoie Mont Blanc (USMB [Université de Savoie] [Université de Chambéry])-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Université Jean Monnet [Saint-Étienne] (UJM), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Réseau International des Instituts Pasteur (RIIP)-Réseau International des Instituts Pasteur (RIIP)-Centre National de la Recherche Scientifique (CNRS)-Centre Hospitalier Régional Universitaire [Lille] (CHRU Lille)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université de Lille, George Mason University [Fairfax]-Center for Applied Proteomics and Molecular Medicine, Institut National de la Recherche Agronomique (INRA)-Centre international d'études supérieures en sciences agronomiques (Montpellier SupAgro)-Université de Montpellier (UM)-Centre National de la Recherche Scientifique (CNRS)-Institut national d’études supérieures agronomiques de Montpellier (Montpellier SupAgro), Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro), Institute of Infection, Immunity and Inflammation [Glasgow, UK]-University of Glasgow, Centre National de la Recherche Scientifique (CNRS)-Université Paris Diderot - Paris 7 (UPD7)-Université Pierre et Marie Curie - Paris 6 (UPMC), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université Grenoble Alpes [2016-2019] (UGA [2016-2019])-Institut de Recherche Interdisciplinaire de Grenoble (IRIG), Université Paris-Sud - Paris 11 (UP11)-Commissariat à l'énergie atomique et aux énergies alternatives (CEA)-Université Paris-Saclay-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-AgroSup Dijon - Institut National Supérieur des Sciences Agronomiques, de l'Alimentation et de l'Environnement-Institut National de la Recherche Agronomique (INRA)-Université de Bourgogne (UB), Université Fédérale Toulouse Midi-Pyrénées-Institut de Recherche pour le Développement (IRD)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS), Université de Bordeaux (UB)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université de Rouen Normandie (UNIROUEN), Normandie Université (NU)-Normandie Université (NU)-CHU Rouen, Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Gustave Roussy (IGR)-Université Paris-Sud - Paris 11 (UP11), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Institut National de la Santé et de la Recherche Médicale (INSERM)-Institut Pasteur [Paris], Centre Léon Bérard [Lyon]-Université Claude Bernard Lyon 1 (UCBL), Université de Lyon-Université de Lyon-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre Léon Bérard [Lyon]-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut de Biologie Paris Seine (IBPS), Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Université Fédérale Toulouse Midi-Pyrénées-Université Fédérale Toulouse Midi-Pyrénées-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM), and Centre National de la Recherche Scientifique (CNRS)-Université Paris Descartes - Paris 5 (UPD5)-Institut National de la Santé et de la Recherche Médicale (INSERM)

Subjects
0301 basic medicine, Settore BIO/06, biology, Cell Biology, [SDV.BC]Life Sciences [q-bio]/Cellular Biology, biology.organism_classification, Cell biology, Interpretation (model theory), 03 medical and health sciences, Arama, 030104 developmental biology, Molecular Biology, Humanities, ComputingMilieux_MISCELLANEOUS
Abstract

Author(s): Klionsky, DJ; Abdelmohsen, K; Abe, A; Abedin, MJ; Abeliovich, H; Arozena, AA; Adachi, H; Adams, CM; Adams, PD; Adeli, K; Adhihetty, PJ; Adler, SG; Agam, G; Agarwal, R; Aghi, MK; Agnello, M; Agostinis, P; Aguilar, PV; Aguirre-Ghiso, J; Airoldi, EM; Ait-Si-Ali, S; Akematsu, T; Akporiaye, ET; Al-Rubeai, M; Albaiceta, GM; Albanese, C; Albani, D; Albert, ML; Aldudo, J; Algul, H; Alirezaei, M; Alloza, I; Almasan, A; Almonte-Beceril, M; Alnemri, ES; Alonso, C; Altan-Bonnet, N; Altieri, DC; Alvarez, S; Alvarez-Erviti, L; Alves, S; Amadoro, G; Amano, A; Amantini, C; Ambrosio, S; Amelio, I; Amer, AO; Amessou, M; Amon, A; An, Z; Anania, FA; Andersen, SU; Andley, UP; Andreadi, CK; Andrieu-Abadie, N; Anel, A; Ann, DK; Anoopkumar-Dukie, S; Antonioli, M; Aoki, H; Apostolova, N; Aquila, S; Aquilano, K; Araki, K; Arama, E; Aranda, A; Araya, J; Arcaro, A; Arias, E; Arimoto, H; Ariosa, AR; Armstrong, JL; Arnould, T; Arsov, I; Asanuma, K; Askanas, V; Asselin, E; Atarashi, R; Atherton, SS; Atkin, JD; Attardi, LD; Auberger, P; Auburger, G; Aurelian, L; Autelli, R

Published
2016
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