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1. The EMT transcription factor ZEB1 governs a fitness-promoting but vulnerable DNA replication stress response

Author

Schuhwerk, Harald, Kleemann, Julia, Gupta, Pooja, van Roey, Ruthger, Armstark, Isabell, Kreileder, Martina, Feldker, Nora, Ramesh, Vignesh, Hajjaj, Yussuf, Fuchs, Kathrin, Mahapatro, Mousumi, Hribersek, Mojca, Volante, Marco, Groenewoud, Arwin, Engel, Felix B., Ceppi, Paolo, Eckstein, Markus, Hartmann, Arndt, Müller, Fabian, Kroll, Torsten, Stemmler, Marc P., Brabletz, Simone, and Brabletz, Thomas

Published
2022
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5. Zeb1 mediates EMT/plasticity-associated ferroptosis sensitivity in cancer cells by regulating lipogenic enzyme expression and phospholipid composition

Author

Schwab, Annemarie, Rao, Zhigang, Zhang, Jie, Gollowitzer, André, Siebenkäs, Katharina, Bindel, Nino, D’Avanzo, Elisabetta, van Roey, Ruthger, Hajjaj, Yussuf, Özel, Ece, Armstark, Isabell, Bereuter, Leonhard, Su, Fengting, Grander, Julia, Bonyadi Rad, Ehsan, Groenewoud, Arwin, Engel, Felix B., Bell, George W., Henry, Whitney S., Angeli, José Pedro Friedmann, Stemmler, Marc P., Brabletz, Simone, Koeberle, Andreas, and Brabletz, Thomas

Abstract

Therapy resistance and metastasis, the most fatal steps in cancer, are often triggered by a (partial) activation of the epithelial–mesenchymal transition (EMT) programme. A mesenchymal phenotype predisposes to ferroptosis, a cell death pathway exerted by an iron and oxygen-radical-mediated peroxidation of phospholipids containing polyunsaturated fatty acids. We here show that various forms of EMT activation, including TGFβ stimulation and acquired therapy resistance, increase ferroptosis susceptibility in cancer cells, which depends on the EMT transcription factor Zeb1. We demonstrate that Zeb1 increases the ratio of phospholipids containing pro-ferroptotic polyunsaturated fatty acids over cyto-protective monounsaturated fatty acids by modulating the differential expression of the underlying crucial enzymes stearoyl-Co-A desaturase 1 (SCD), fatty acid synthase (FASN), fatty acid desaturase 2 (FADS2), elongation of very long-chain fatty acid 5 (ELOVL5) and long-chain acyl-CoA synthetase 4 (ACSL4). Pharmacological inhibition of selected lipogenic enzymes (SCD and FADS2) allows the manipulation of ferroptosis sensitivity preferentially in high-Zeb1-expressing cancer cells. Our data are of potential translational relevance and suggest a combination of ferroptosis activators and SCD inhibitors for the treatment of aggressive cancers expressing high Zeb1.

Published
2024
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6. Mechano-signaling of prostate tumor initiating cells facilitates their tropism to stiff metastatic niche

Author

Chen, Lanpeng, primary, Zhao, Gangyin, additional, De Menna, Marta, additional, Coppola, Stefano, additional, Groenewoud, Arwin, additional, Landman, Nick, additional, Schieven, Sebastiaan, additional, Thalmann, George N., additional, Schmidt, Thomas, additional, de Vrie, Jelle, additional, Kruithof-de Julio, Marianna, additional, and Snaar, Ewa B, additional

Published
2023
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9. Patient-derived zebrafish xenografts of uveal melanoma reveal ferroptosis as a drug target

Author

Groenewoud, Arwin, primary, Yin, Jie, additional, Gelmi, Maria Chiara, additional, Alsafadi, Samar, additional, Nemati, Fariba, additional, Decaudin, Didier, additional, Roman-Roman, Sergio, additional, Kalirai, Helen, additional, Coupland, Sarah E., additional, Jochemsen, Aart G., additional, Jager, Martine J., additional, Engel, Felix B., additional, and Snaar-Jagalska, B. E., additional

Published
2023
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12. Human melanoma brain metastases cell line MUG-Mel1, isolated clones and their detailed characterization

Author

Heitzer, Ellen, Groenewoud, Arwin, Meditz, Katharina, Lohberger, Birgit, Liegl-Atzwanger, Bernadette, Prokesch, Andreas, Kashofer, Karl, Behrens, Diana, Haybaeck, Johannes, Kolb-Lenz, Dagmar, Koefeler, Harald, Riedl, Sabrina, Schaider, Helmut, Fischer, Carina, Snaar-Jagalska, B. Ewa, de’Jong, Danielle, Szuhai, Karoly, Zweytick, Dagmar, and Rinner, Beate

Published
2019
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13. Supplementary figure S4 from Endoglin Expression on Cancer-Associated Fibroblasts Regulates Invasion and Stimulates Colorectal Cancer Metastasis

Author

Paauwe, Madelon, primary, Schoonderwoerd, Mark J.A., primary, Helderman, Roxan F.C.P., primary, Harryvan, Tom J., primary, Groenewoud, Arwin, primary, van Pelt, Gabi W., primary, Bor, Rosalie, primary, Hemmer, Danielle M., primary, Versteeg, Henri H., primary, Snaar-Jagalska, B. Ewa, primary, Theuer, Charles P., primary, Hardwick, James C.H., primary, Sier, Cornelis F.M., primary, ten Dijke, Peter, primary, and Hawinkels, Lukas J.A.C., primary

Published
2023
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14. Supplementary table S4 from Endoglin Expression on Cancer-Associated Fibroblasts Regulates Invasion and Stimulates Colorectal Cancer Metastasis

Author

Paauwe, Madelon, primary, Schoonderwoerd, Mark J.A., primary, Helderman, Roxan F.C.P., primary, Harryvan, Tom J., primary, Groenewoud, Arwin, primary, van Pelt, Gabi W., primary, Bor, Rosalie, primary, Hemmer, Danielle M., primary, Versteeg, Henri H., primary, Snaar-Jagalska, B. Ewa, primary, Theuer, Charles P., primary, Hardwick, James C.H., primary, Sier, Cornelis F.M., primary, ten Dijke, Peter, primary, and Hawinkels, Lukas J.A.C., primary

Published
2023
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15. Patient-derived zebrafish xenografts of uveal melanoma reveal ferroptosis as a drug target

Author

Groenewoud, Arwin, primary, Yin, Jie, additional, Gelmi, Maria-Chiara, additional, Alsafadi, Samar, additional, Nemati, Fariba, additional, Decaudin, Didier, additional, Roman-Roman, Sergio, additional, Kalirai, Helen, additional, Coupland, Sarah, additional, Jochemsen, Aart, additional, Jager, Martine, additional, Engel, Felix, additional, and Snaar-Jagalska, Ewa, additional

Published
2022
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18. Automation of Technology for Cancer Research

Author

van der Ent, Wietske, primary, Veneman, Wouter J., additional, Groenewoud, Arwin, additional, Chen, Lanpeng, additional, Tulotta, Claudia, additional, Hogendoorn, Pancras C. W., additional, Spaink, Herman. P., additional, and Snaar-Jagalska, B. Ewa, additional

Published
2016
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20. Patient-derived zebrafish xenograft models reveal ferroptosis as a fatal and druggable weakness in metastatic uveal melanoma

Author

Groenewoud, Arwin, primary, Yin, Jie, additional, Gelmi, Maria Chiara, additional, Alsafadi, Samar, additional, Nemati, Fariba, additional, Decaudin, Didier, additional, Roman-Roman, Sergio, additional, Kalirai, Helen, additional, Coupland, Sarah E, additional, Jochemsen, Aart G, additional, Jager, Martine J, additional, and Snaar-Jagalska, Ewa, additional

Published
2021
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24. Extracellular mycobacterial DNA drives disease progression by triggering Caspase-11-dependent pyroptosis of infected macrophages

Author

Varela, Monica, van der Vaart, Michiel, Groenewoud, Arwin, and Meijer, Annemarie H.

Subjects
0303 health sciences, Pyroptosis, Inflammasome, Inflammation, Caspase-11, Biology, medicine.disease, 3. Good health, Cell biology, 03 medical and health sciences, 0302 clinical medicine, Granuloma, medicine, Macrophage, Secretion, medicine.symptom, 030304 developmental biology, 030215 immunology, Phagosome, medicine.drug
Abstract

Deregulated inflammation is a serious complication of life-threatening microbial infections, including tuberculosis (TB). The pathological hallmark of TB, the granuloma, is an inflammatory structure crucial for containing infection. However, excessive inflammation in granulomas can cause tissue damage and promote bacterial proliferation and dissemination. The assembly of multiprotein inflammasome complexes is an important trigger of inflammation, but it remains unknown how inflammasome activation impacts TB granuloma progression. Here, by in vivo imaging using the zebrafish TB model, we found that inflammasomes and ensuing pyroptotic cell death of infected macrophages drive granuloma expansion and disease progression. We show that different types of inflammasomes are activated during granuloma formation, with host-protective roles for Asc-dependent inflammasome activation and Il1b secretion. In contrast, an Asc-independent pathway induces macrophage pyroptosis and impairs host resistance. Complementary research in ASC-deficient murine macrophages reveals that extracellular bacterial DNA induces CASP11-dependent pyroptosis in a manner dependent on phagosome permeabilization. Finally, we show that mycobacteria induce pyroptosis to escape from cell-in-cell structures that form within granulomas when living infected cells are engulfed by newly attracted macrophages. This study provides new insights into the role of pyroptosis in TB pathogenesis and unravels a novel link between nucleic acid sensing and CASP11-dependent pyroptosis.

Published
2019
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27. Endoglin Expression on Cancer-Associated Fibroblasts Regulates Invasion and Stimulates Colorectal Cancer Metastasis

Author

Paauwe, Madelon, primary, Schoonderwoerd, Mark J.A., additional, Helderman, Roxan F.C.P., additional, Harryvan, Tom J., additional, Groenewoud, Arwin, additional, van Pelt, Gabi W., additional, Bor, Rosalie, additional, Hemmer, Danielle M., additional, Versteeg, Henri H., additional, Snaar-Jagalska, B. Ewa, additional, Theuer, Charles P., additional, Hardwick, James C.H., additional, Sier, Cornelis F.M., additional, ten Dijke, Peter, additional, and Hawinkels, Lukas J.A.C., additional

Published
2018
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30. Overexpression of EZH2 in conjunctival melanoma offers a new therapeutic target

Author

Cao, Jinfeng, primary, Pontes, Kelly CS, additional, Heijkants, Renier C, additional, Brouwer, Niels J, additional, Groenewoud, Arwin, additional, Jordanova, Ekaterina S, additional, Marinkovic, Marina, additional, van Duinen, Sjoerd, additional, Teunisse, Amina FAS, additional, Verdijk, Robert M, additional, Snaar-Jagalska, Ewa, additional, Jochemsen, Aart G, additional, and Jager, Martine J, additional

Published
2018
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31. UM Cure 2020: New therapies for uveal melanoma

Author

Roman-Roman, Sergio, primary, Stern, Marc-Henri, additional, Alsafadi, Samar, additional, Jager, Martine J., additional, Dogrusöz, Mehmet, additional, Coupland, Sarah E., additional, Mione, Maria Caterina, additional, Anelli, Viviana, additional, Precazzini, Francesca, additional, Mobuchon, Lenha, additional, Nemati, Fariba, additional, Decaudin, Didier, additional, Rodrigues, Manuel, additional, Lantz, Olivier, additional, Barnhill, Raymond, additional, Piperno-Neumann, Sophie, additional, Cassoux, Nathalie, additional, Desjardins, Laurence, additional, Gezgin, Gulçin, additional, Wierenga, Annemijn, additional, Jochemsen, Aart J., additional, Glinkina, Kseniya A., additional, van der Velden, Pieter A., additional, Nell, Rogier J., additional, Groenewoud, Arwin, additional, Snaar-Jagalska, B.E., additional, Marais, Richard, additional, Mahal, Katharina, additional, Hascoet, Pauline, additional, Kalirai, Helen, additional, Elas, Martyna, additional, Romanowska-Dixon, Bozena, additional, Ruijtenbeek, Rob, additional, van den Heuvel, Dianne, additional, Houkes, Liesbeth, additional, Lebel-Binay, Sophie, additional, Prestat, Antoine, additional, Sengenés, Jennifer, additional, Ryll, Bettina, additional, Valente, André, additional, and Vinolo, Emilie, additional

Published
2018
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33. CORRECTION: Innovative approaches to establish and characterize primary cultures: an ex vivo 3D system and the zebrafish model

Author

Liverani, Chiara, primary, La Manna, Federico, additional, Groenewoud, Arwin, additional, Mercatali, Laura, additional, Van Der Pluijm, Gabri, additional, Pieri, Federica, additional, Cavaliere, Davide, additional, De Vita, Alessandro, additional, Spadazzi, Chiara, additional, Miserocchi, Giacomo, additional, Bongiovanni, Alberto, additional, Recine, Federica, additional, Riva, Nada, additional, Amadori, Dino, additional, Tasciotti, Ennio, additional, Snaar-Jagalska, Ewa, additional, and Ibrahim, Toni, additional

Published
2017
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34. Development of a Patient-Derived Xenograft (PDX) of Breast Cancer Bone Metastasis in a Zebrafish Model

Author

Mercatali, Laura, primary, La Manna, Federico, additional, Groenewoud, Arwin, additional, Casadei, Roberto, additional, Recine, Federica, additional, Miserocchi, Giacomo, additional, Pieri, Federica, additional, Liverani, Chiara, additional, Bongiovanni, Alberto, additional, Spadazzi, Chiara, additional, de Vita, Alessandro, additional, van der Pluijm, Gabri, additional, Giorgini, Andrea, additional, Biagini, Roberto, additional, Amadori, Dino, additional, Ibrahim, Toni, additional, and Snaar-Jagalska, Ewa, additional

Published
2016
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35. Innovative approaches to establish and characterize primary cultures: an ex vivo 3D system and the zebrafish model

Author

Liverani, Chiara, primary, La Manna, Federico, additional, Groenewoud, Arwin, additional, Mercatali, Laura, additional, Van Der Pluijm, Gabri, additional, Pieri, Federica, additional, Cavaliere, Davide, additional, De Vita, Alessandro, additional, Spadazzi, Chiara, additional, Miserocchi, Giacomo, additional, Bongiovanni, Alberto, additional, Recine, Federica, additional, Riva, Nada, additional, Amadori, Dino, additional, Tasciotti, Ennio, additional, Snaar-Jagalska, Ewa, additional, and Ibrahim, Toni, additional

Published
2016
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36. Correlation of breast cancer susceptibility loci with patient characteristics, metastasis-free survival, and mRNA expression of the nearest genes

Author

Riaz, Muhammad, primary, Berns, Els M. J. J., additional, Sieuwerts, Anieta M., additional, Ruigrok-Ritstier, Kirsten, additional, de Weerd, Vanja, additional, Groenewoud, Arwin, additional, Uitterlinden, Andrè G., additional, Look, Maxime P., additional, Klijn, Jan G. M., additional, Sleijfer, Stefan, additional, Foekens, John A., additional, and Martens, John W. M., additional

Published
2011
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37. Establishment of Embryonic Zebrafish Xenograft Assays to Investigate TGF-β Family Signaling in Human Breast Cancer Progression.

Author

Li C, Ma J, Groenewoud A, Ren J, Liu S, Snaar-Jagalska BE, and Ten Dijke P

Subjects
Animals, Female, Heterografts, Humans, Neoplasm Transplantation, Signal Transduction, Tumor Microenvironment, Breast Neoplasms pathology, TGF-beta Superfamily Proteins metabolism, Zebrafish metabolism
Abstract

Transforming growth factor-β (TGF-β) family members have pivotal functions in controlling breast cancer progression, acting not only on cancer cells but also on other cells within the tumor microenvironment. Here we describe embryonic zebrafish xenograft assays to investigate how TGF-β family signaling controls breast cancer cell intravasation, extravasation and regulates tumor angiogenesis. Fluorescently mCherry-labeled breast cancer cells are injected in the perivitelline space or Duct of Cuvier of Tg (fli:EGFP) transgenic Casper zebrafish embryos, in which the zebrafish express enhanced green fluorescent protein in the entire vasculature. The dynamic responses of migratory and invasive human cancer cells, and the induction of new blood vessel formation by the cancer cells in zebrafish host, are visualized using a fluorescent microscope. These assays provide efficient, reliable, low-cost models to investigate the effect of (epi)genetic modulators and pharmacological compounds that perturb the activity of TGF-β family signaling components on breast cancer cell metastasis and angiogenesis., (© 2022. The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature.)

Published
2022
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38. Animal Models of Breast Cancer Bone Metastasis.

Author

Tulotta C, Groenewoud A, Snaar-Jagalska BE, and Ottewell P

Subjects
Animals, Bone Neoplasms diagnostic imaging, Bone Neoplasms pathology, Bone and Bones diagnostic imaging, Bone and Bones pathology, Breast Neoplasms diagnostic imaging, Cell Line, Tumor, Embryo, Nonmammalian, Female, Humans, Luciferases chemistry, Luminescent Measurements instrumentation, Luminescent Measurements methods, Mice, Mice, Nude, Mice, SCID, Optical Imaging instrumentation, Optical Imaging methods, Xenograft Model Antitumor Assays instrumentation, Zebrafish, Bone Neoplasms secondary, Breast Neoplasms pathology, Disease Models, Animal, Xenograft Model Antitumor Assays methods
Abstract

This chapter is designed to provide a comprehensive overview outlining the different in vivo models available for research into breast cancer bone metastasis. The main focus is to guide the researcher through the methodological processes required to establish and utilize these models within their own laboratory. These detailed methods are designed to enable the acquisition of accurate and meaningful results that can be used for publication and future translation into clinical benefit for women with breast cancer-induced bone metastasis.

Published
2019
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39. Innovative approaches to establish and characterize primary cultures: an ex vivo 3D system and the zebrafish model.

Author

Liverani C, La Manna F, Groenewoud A, Mercatali L, Van Der Pluijm G, Pieri F, Cavaliere D, De Vita A, Spadazzi C, Miserocchi G, Bongiovanni A, Recine F, Riva N, Amadori D, Tasciotti E, Snaar-Jagalska E, and Ibrahim T

Abstract

Patient-derived specimens are an invaluable resource to investigate tumor biology. However, in vivo studies on primary cultures are often limited by the small amount of material available, while conventional in vitro systems might alter the features and behavior that characterize cancer cells. We present our data obtained on primary dedifferentiated liposarcoma cells cultured in a 3D scaffold-based system and injected into a zebrafish model. Primary cells were characterized in vitro for their morphological features, sensitivity to drugs and biomarker expression, and in vivo for their engraftment and invasiveness abilities. The 3D culture showed a higher enrichment in cancer cells than the standard monolayer culture and a better preservation of liposarcoma-associated markers. We also successfully grafted primary cells into zebrafish, showing their local migratory and invasive abilities. Our work provides proof of concept of the ability of 3D cultures to maintain the original phenotype of ex vivo cells, and highlights the potential of the zebrafish model to provide a versatile in vivo system for studies with limited biological material. Such models could be used in translational research studies for biomolecular analyses, drug screenings and tumor aggressiveness assays., (© 2016. Published by The Company of Biologists Ltd.)

Published
2017
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40. Imaging of Human Cancer Cell Proliferation, Invasion, and Micrometastasis in a Zebrafish Xenogeneic Engraftment Model.

Author

Tulotta C, He S, Chen L, Groenewoud A, van der Ent W, Meijer AH, Spaink HP, and Snaar-Jagalska BE

Subjects
Animals, Cell Line, Tumor, Cell Proliferation genetics, Cell Proliferation physiology, Disease Models, Animal, Embryo, Nonmammalian cytology, Embryo, Nonmammalian metabolism, Embryo, Nonmammalian pathology, Humans, Mice, Neoplasm Micrometastasis, Transplantation, Heterologous, Zebrafish embryology, Neoplasms metabolism, Neoplasms pathology, Zebrafish metabolism
Abstract

The xenograft model, using the early life stages of the zebrafish, allows imaging of tumor cell behavior both on a single cell and whole organism level, over time, within a week. This robust and reproducible assay can be used as an intermediate step between in vitro techniques and the expensive, and time consuming, murine models of cancer invasion and metastasis.In this chapter, a detailed protocol to inject human cancer cells into the blood circulation of a zebrafish embryo is described; the engraftment procedure is then followed by visualization and quantification methods of tumor cell proliferation, invasion, and micrometastasis formation during subsequent larval development. Interaction with the host microenvironment is also considered.

Published
2016
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