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1. A subset of Kupffer cells regulates metabolism through the expression of CD36

Author

Guochen Wan, Nicholas Ang, Shanshan W. Howland, Svetoslav Chakarov, Evan W. Newell, Gregoire Gessain, Wan Ting Kong, Cecilia Morgantini, Olivier N. F. Cexus, Bernett Lee, Zhaoyuan Liu, Xenia Ficht, Ping Chen, Giorgia De Simone, Emelie Barreby, Josephine Lum, Nicolas Venteclef, Francesco Andreata, Ahad Khalilnezhad, Myriam Aouadi, Jinmiao Chen, Connie Xu, Xiaomeng Zhang, Ivy Low, Foo Shihui, Garett Dunsmore, Anis Larbi, Laurent Yvan-Charvet, Camille Blériot, Wei Guo, Rhea Pai, Muhammad Faris Bin Mohd Kairi, Benoit Malleret, Radoslaw M. Sobota, Wint Wint Phoo, Florent Ginhoux, Lai Guan Ng, Valerio Azzimato, Marc Bajénoff, Raphaelle Ballaire, Matteo Iannacone, Valeria Fumagalli, Ankur Sharma, Akhila Balachander, Singapore Immunology Network (SIgN), Biomedical Sciences Institute (BMSI), Karolinska Institute, Institut Gustave Roussy (IGR), Immunologie anti-tumorale et immunothérapie des cancers (ITIC), Institut Gustave Roussy (IGR)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Université Paris-Saclay, Inovarion, IRCCS San Raffaele Scientific Institute [Milan, Italie], Universita Vita Salute San Raffaele = Vita-Salute San Raffaele University [Milan, Italie] (UniSR), Equipe Electronique - Laboratoire GREYC - UMR6072, Groupe de Recherche en Informatique, Image et Instrumentation de Caen (GREYC), Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Normandie Université (NU)-École Nationale Supérieure d'Ingénieurs de Caen (ENSICAEN), Normandie Université (NU)-Centre National de la Recherche Scientifique (CNRS)-Université de Caen Normandie (UNICAEN), Normandie Université (NU)-Centre National de la Recherche Scientifique (CNRS), Karolinska Institutet [Stockholm], Shangaï Jiao Tong University [Shangaï], Genome Institute of Singapore (GIS), National University of Singapore (NUS), University of Surrey (UNIS), Agency for science, technology and research [Singapore] (A*STAR), Aix Marseille Université (AMU), Centre méditerranéen de médecine moléculaire (C3M), Université Nice Sophia Antipolis (1965 - 2019) (UNS), 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)-Université Côte d'Azur (UCA), Immunité et métabolisme dans le diabète = IMmunity and MEtabolism in DIABetes [CRC] (IMMEDIAB Lab), Centre de Recherche des Cordeliers (CRC (UMR_S_1138 / U1138)), École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris Cité (UPCité)-École Pratique des Hautes Études (EPHE), Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Sorbonne Université (SU)-Université Paris Cité (UPCité), Istituto di Ricovero e Cura a Carattere Scientifico (IRCCS San Raffaele Pisana), Shanghai Jiao Tong University [Shanghai], Clinical Research Center, Department of Laboratory Medicine, Karolinska Institutet, Karolinska University Hospital Huddinge, Huddinge, Sweden, Karolinska Institutet [Stockholm]-Karolinska University Hospital [Stockholm], Inserm Avenir Group, Institut National de la Santé et de la Recherche Médicale (INSERM), Centre d'Immunologie de Marseille - Luminy (CIML), Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), INSERM U1015, Unit of Immunology, Rheumatology, Allergy and Rare diseases, Milan (IRCCS San Raffaele Scientific Institute), E-institute of Shanghai University Immunology Division, Shanghai University, University of Surrey, - Biosciences and Medicine, Faculty of Health and Medical Sciences, Guildford, SingMass National Laboratory - Singapore, Bleriot, C., Barreby, E., Dunsmore, G., Ballaire, R., Chakarov, S., Ficht, X., De Simone, G., Andreata, F., Fumagalli, V., Guo, W., Wan, G., Gessain, G., Khalilnezhad, A., Zhang, X. M., Ang, N., Chen, P., Morgantini, C., Azzimato, V., Kong, W. T., Liu, Z., Pai, R., Lum, J., Shihui, F., Low, I., Xu, C., Malleret, B., Kairi, M. F. M., Balachander, A., Cexus, O., Larbi, A., Lee, B., Newell, E. W., Ng, L. G., Phoo, W. W., Sobota, R. M., Sharma, A., Howland, S. W., Chen, J., Bajenoff, M., Yvan-Charvet, L., Venteclef, N., Iannacone, M., Aouadi, M., Ginhoux, F., Bleriot, C, Barreby, E, Dunsmore, G, Ballaire, R, Chakarov, S, Ficht, X, De Simone, G, Andreata, F, Fumagalli, V, Guo, W, Wan, G, Gessain, G, Khalilnezhad, A, Zhang, X, Ang, N, Chen, P, Morgantini, C, Azzimato, V, Kong, W, Liu, Z, Pai, R, Lum, J, Shihui, F, Low, I, Xu, C, Malleret, B, Kairi, M, Balachander, A, Cexus, O, Larbi, A, Lee, B, Newell, E, Ng, L, Phoo, W, Sobota, R, Sharma, A, Howland, S, Chen, J, Bajenoff, M, Yvan-Charvet, L, Venteclef, N, Iannacone, M, Aouadi, M, Ginhoux, F, and Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU)

Subjects
CD36 Antigens, Kupffer Cells, CD36, [SDV]Life Sciences [q-bio], Immunology, Population, Kupffer cell, macrophage, liver, 03 medical and health sciences, chemistry.chemical_compound, Mice, 0302 clinical medicine, Immune system, scRNA-seq, medicine, Immunology and Allergy, Gene silencing, Macrophage, Animals, Obesity, education, ComputingMilieux_MISCELLANEOUS, 030304 developmental biology, 0303 health sciences, education.field_of_study, biology, Fatty acid metabolism, high fat diet, medicine.disease, Phenotype, Cell biology, macrophages, single cell, Oxidative Stress, Infectious Diseases, chemistry, CD206, Liver, 030220 oncology & carcinogenesis, biology.protein, Steatosis, heterogeneity, metabolism
Abstract

Tissue macrophages are immune cells whose phenotypes and functions are dictated by origin and niches. However, tissues are complex environments, and macrophage heterogeneity within the same organ has been overlooked so far. Here, we used high-dimensional approaches to characterize macrophage populations in the murine liver. We identified two distinct populations among embryonically derived Kupffer cells (KCs) sharing a core signature while differentially expressing numerous genes and proteins: a major CD206loESAM– population (KC1) and a minor CD206hiESAM+ population (KC2). KC2 expressed genes involved in metabolic processes, including fatty acid metabolism both in steady-state and in diet-induced obesity and hepatic steatosis. Functional characterization by depletion of KC2 or targeted silencing of the fatty acid transporter Cd36 highlighted a crucial contribution of KC2 in the liver oxidative stress associated with obesity. In summary, our study reveals that KCs are more heterogeneous than anticipated, notably describing a subpopulation wired with metabolic functions.

Published
2021

2. Identification of a Kupffer cell subset capable of reverting the T cell dysfunction induced by hepatocellular priming

Author

Xenia Ficht, Marc Bajénoff, Alexandre P. Benechet, Matteo Iannacone, Federica Moalli, Svetoslav Chakarov, José M. Garcia-Manteiga, Paola Zordan, Pietro Di Lucia, Francesco Andreata, Chiara Laura, Luca G. Guidotti, Marta Mainetti, Giorgia De Simone, Camille Blériot, Elisa Bono, Gioia Ambrosi, Leonardo Giustini, Valeria Fumagalli, Stefano Gilotto, Micol Ravà, Federico F. De Ponti, Florent Ginhoux, Universita Vita Salute San Raffaele = Vita-Salute San Raffaele University [Milan, Italie] (UniSR), IRCCS San Raffaele Scientific Institute [Milan, Italie], Singapore Immunology Network (SIgN), Biomedical Sciences Institute (BMSI), Centre d'Immunologie de Marseille - Luminy (CIML), Aix Marseille Université (AMU)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS), School of Medicine [Shanghai Jiaotong University], Shanghai Jiaotong University, Agency for science, technology and research [Singapore] (A*STAR), De Simone, G., Andreata, F., Bleriot, C., Fumagalli, V., Laura, C., Garcia-Manteiga, J. M., Di Lucia, P., Gilotto, S., Ficht, X., De Ponti, F. F., Bono, E. B., Giustini, L., Ambrosi, G., Mainetti, M., Zordan, P., Benechet, A. P., Rava, M., Chakarov, S., Moalli, F., Bajenoff, M., Guidotti, L. G., Ginhoux, F., Iannacone, M., De Simone, G, Andreata, F, Bleriot, C, Fumagalli, V, Laura, C, Garcia-Manteiga, J, Di Lucia, P, Gilotto, S, Ficht, X, De Ponti, F, Bono, E, Giustini, L, Ambrosi, G, Mainetti, M, Zordan, P, Benechet, A, Rava, M, Chakarov, S, Moalli, F, Bajenoff, M, Guidotti, L, Ginhoux, F, Iannacone, M, Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Aix Marseille Université (AMU), and Bajenoff, Marc

Subjects
[SDV]Life Sciences [q-bio], hepatitis B viru, Priming (immunology), CD8-Positive T-Lymphocytes, [SDV.IMM.II]Life Sciences [q-bio]/Immunology/Innate immunity, ACTIVATION, Mice, 0302 clinical medicine, Immunology and Allergy, Cytotoxic T cell, Kupffer cells, T cell dysfunction, RNA-SEQ, Antigen Presentation, 0303 health sciences, tolerance, CD8(+) T cells, Effector, MED/04 - PATOLOGIA GENERALE, Kupffer cell, imaging, Hepatitis B, single cell, 3. Good health, Infectious Diseases, medicine.anatomical_structure, [SDV.IMM.IA]Life Sciences [q-bio]/Immunology/Adaptive immunology, [SDV.IMM.IA] Life Sciences [q-bio]/Immunology/Adaptive immunology, 030220 oncology & carcinogenesis, CD8+ T cell, medicine.drug, EXPRESSION, Interleukin 2, Kupffer Cells, Immunology, FATE, T cells, Mice, Transgenic, Biology, +, liver, Major histocompatibility complex, DENDRITIC CELLS, Article, 03 medical and health sciences, Cross-Priming, Antigen, scRNA-seq, Immune Tolerance, medicine, Animals, [SDV.IMM.II] Life Sciences [q-bio]/Immunology/Innate immunity, 030304 developmental biology, IL-2, Biology and Life Sciences, CD8, CROSS, Cancer research, biology.protein, CD8+ T cells, Interleukin-2, interleukin-2, hepatitis B virus, RESPONSES
Abstract

Summary Kupffer cells (KCs) are highly abundant, intravascular, liver-resident macrophages known for their scavenger and phagocytic functions. KCs can also present antigens to CD8+ T cells and promote either tolerance or effector differentiation, but the mechanisms underlying these discrepant outcomes are poorly understood. Here, we used a mouse model of hepatitis B virus (HBV) infection, in which HBV-specific naive CD8+ T cells recognizing hepatocellular antigens are driven into a state of immune dysfunction, to identify a subset of KCs (referred to as KC2) that cross-presents hepatocellular antigens upon interleukin-2 (IL-2) administration, thus improving the antiviral function of T cells. Removing MHC-I from all KCs, including KC2, or selectively depleting KC2 impaired the capacity of IL-2 to revert the T cell dysfunction induced by intrahepatic priming. In summary, by sensing IL-2 and cross-presenting hepatocellular antigens, KC2 overcome the tolerogenic potential of the hepatic microenvironment, suggesting new strategies for boosting hepatic T cell immunity., Graphical abstract, Highlights • KCs are required for in vivo reinvigoration of intrahepatically primed T cells by IL-2 • KCs respond to IL-2 and cross-present hepatocellular Ags • Single-cell RNA-seq identifies two distinct populations of KCs • KC2s have enriched IL-2 sensing machinery and Ag presentation capacity, De Simone et al. delineate the mechanisms by which hepatocellularly primed HBV-specific CD8+ T cells acquire antiviral effector functions following IL-2 administration. These mechanisms rely on KCs and, in particular, on a hitherto unidentified KC subset, referred to as KC2, that is poised to respond to IL-2 and cross-present viral antigens.

Published
2021

3. Making friends in out-of-the-way places: how cells of the immune system get together and how they conduct their business as revealed by intravital imaging

Author

Hai Qi, Jackson G. Egen, Flora Castellino, Masaru Ishii, Alex Yee-Chen Huang, Ronald N. Germain, Marcello Chieppa, Lily Koo, Marc Bajénoff, Germain, R. N., Bajenoff, M., Castellino, F., Chieppa, M., Egen, J. G., Huang, A. Y. C., Ishii, M., Koo, L. Y., and Qi, H.

Subjects
Diagnostic Imaging, Stromal cell, Immunology, Inflammation, Biology, Immune system, Cell trafficking, medicine, Immunology and Allergy, Animals, Humans, Antigens, B cell, Microscopy, Animal, T cell, Cell migration, Dendritic cell, T lymphocyte, Cell biology, Haematopoiesis, Antigen, Immune System, In vivo imaging, medicine.symptom, Intravital microscopy, Human
Abstract

A central characteristic of the immune system is the constantly changing location of most of its constituent cells. Lymphoid and myeloid cells circulate in the blood, and subsets of these cells enter, move, and interact within, then leave organized lymphoid tissues. When inflammation is present, various hematopoietic cells also exit the vasculature and migrate within non-lymphoid tissues, where they carry out effector functions that support host defense or result in autoimmune pathology. Effective innate and adaptive immune responses involve not only the action of these individual cells but also productive communication among them, often requiring direct membrane contact between rare antigen-specific or antigen-bearing cells. Here, we describe our ongoing studies using two-photon intravital microscopy to probe the in situ behavior of the cells of the immune system and their interactions with non-hematopoietic stromal elements. We emphasize the importance of non-random cell migration within lymphoid tissues and detail newly established mechanisms of traffic control that operate at multiple organizational scales to facilitate critical cell contacts. We also describe how the methods we have developed for imaging within lymphoid sites are being applied to other tissues and organs, revealing dynamic details of host-pathogen interactions previously inaccessible to direct observation. © 2008 The Authors.

Published
2008

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