Ewa Snaar-Jagalska
Professor of Cellular tumor biology
- Name
- Prof.dr. B.E. Snaar-Jagalska
- Telephone
- +31 71 527 4980
- b.e.snaar-jagalska@biology.leidenuniv.nl
- ORCID iD
- 0000-0002-3772-047x
I obtained my PhD at Leiden University (NL) in 1988 on G-protein and RAS mediated signal transduction in Dictyostelium. After a postdoctoral fellowship at the Johns Hopkins University, Medical School in Baltimore (USA) I returned to Leiden and was appointed as assistant professor in the workgroup Cell Biology and Genetics.
More information about Ewa Snaar-Jagalska
Postdocs
News
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Fighting gliobastoma brain tumours with two grants -
Chemotherapy without side effects? It’s possible, with light -
Leiden: The scene of the Zebrafish Disease Models conference 2018 -
Hunt for fundamental insight into and treatment for cancer -
Ewa Snaar-Jagalska appointed as Professor in the field of cellular tumor biology -
Aggressiveness of cancer cells halted -
Completion of the Science Campus -
New zebrafish study to understand human cancer
Former PhD candidates
I studied molecular signal transduction processes controlling chemotactic cell movements in the eukaryotic model Dictyostelium. I developed expertise in different aspects of signalling topics like G-protein coupled receptors (GPCRs), G-proteins, RAS, protein kinases and 14-3-3 proteins to answer the important open question: how can cells detect gradients of chemoattractants and translate this information into a chemotactic response? In 2000 I joined the Molecular Cell Biology section of IBL headed by Prof. H.P. Spaink, where I currently work as associate professor. In collaboration with Prof. T. Schmidt (Leiden Institute of Physics) we developed a new research line on the dynamic reorganization of plasma membrane interactions on single-molecule stimulation in vivo. This recently led to a breakthrough in the understanding of directional sensing of migrating cells. In 2003, I made a switch to a vertebrate model, the zebrafish. Currently my research focuses on the signalling dynamics underlying cancer and microenvironment interaction in zebrafish embryonic and transgenic models and in particular the role of innate immunity responses to cancer cells during angiogenesis and metastasis. In addition, I coordinate the ZF-CANCER project (2008-2011), an EU network for development of high-throughput bioassays for human cancers in zebrafish, with the ultimate aim of establishing zebrafish as a key vertebrate model for rapid, preclinical anticancer drug target discovery and lead compound selection. I also participate(d) in other previous (ZF-TOOLS, ZF-MODELS) and ongoing (ZF-HEALTH, SmartMix) international and national zebrafish research networks and co-organized several workshops on cancer and inflammation disease in zebrafish. The success of this new research line is shown by obtaining a medical grant for cancer research in the zebrafish model from the KIKA foundation (collaboration with several clinical research groups at the LUMC such as Molecular Cell Biology, Orthopedics, Pediatric Oncology and Pathology) as well as a NOW-TOP grant (collaboration with Prof. P. Hogendoorn (LUMC), Prof. T. Schmidt (LION) and Dr. A. H. Meijer (MCB-IBL)). I serve/served on the editorial board of several journals and am/was council member of various national and international organizations.
Research
I am interested in the signalling dynamics underlying cancer progression using zebrafish embryonic and transgenic models. The zebrafish is an excellent model system for this purpose: zebrafish form spontaneous tumors with similar histopathological and gene profiling features as human tumors; xeno-transplantation with human carcinoma cells is possible; and angiogenesis and immune response can be studied in vivo within the developing tumor.
The main focus of my research is on: directional cell migration and chemotaxis in cancer; the role of innate immunity responses to cancer cells during angiogenesis and metastasis; and human cancer modeling in zebrafish with the ultimate aim of establishing zebrafish as a key model for rapid discovery and assessment of cancer genetic targets (biomarkers) and drugs to develop strategies for cancer therapies. I closely collaborate with other groups at the Science Faculty and the LUMC and with other staff members of the Molecular Cell Biology group on development and application of high-throughput screening strategies for identifying novel anti-cancer drugs and cancer gene targets (with Prof. Herman Spaink) and on interaction between cancer and the immune system (with Dr. Annemarie Meijer). The research is funded by ZF-CANCER (EU FP7), ZF-HEALTH (EU FP7), SmartMix, KIKA foundation and NWO-TOP.
I have three main research themes:
Directional cell migration and chemotaxis in cancer
Cell migration is involved in vital physiological processes including embryogenesis and the immune response. However, it is likewise closely related to pathological conditions such as in cancer and chronic inflammatory responses. In many cases such cell migration is directional as determined by extracellular gradients of chemokines. Chemotaxis, the process of cell migration in chemokine gradients, is divided into the process of detection of the chemical gradient, the initial gradient sensing, and the subsequent translation of this gradient information into processes leading to physical movement and cell motility. Currently, little is known about the molecular mechanisms that control chemokine gradient sensing and migration of immune, endothelial and tumor cells. Fortunately, the molecular mechanisms that regulate these fundamental aspects of chemotaxis appear to be evolutionarily conserved and studies in the lower eukaryotic model system Dictyostelium discoideum in collaboration with Prof. Dr. Thomas Schmidt from Leiden Institute of the Physics have allowed us to form novel concepts, uncover molecular components, develop new single-molecule techniques, and test models of chemotaxis over the past years. In our earlier studies we found that a graded response in receptor mobility within the membrane, a distinct physical amplification mechanism towards downstream G proteins, and a high degree of membrane organization into signaling platforms does finally lead to a faithful signaling cascade and ultimately towards directed cellular motility.
Importantly, chemokines and chemokine receptors direct the migration of leukocytes to sites of inflammation and control leukocyte infiltration in cancer. In addition, chemokines also affect tumor growth by their angiogenic or angiostatic activity. Angiogenesis, the formation of new blood vessels from existing ones, is important in tumorigenesis to provide oxygen and nutrients and to stimulate the process of metastasis. Tumor growth occurs when the equilibrium between angiogenic and angiostatic factors is disturbed in favor of the angiogenic factors. The balance between angiostatic and angiogenic chemokines and their receptors expressed on the endothelial cell layer has to be strictly regulated. How this balance is regulated is still elusive.
In the current multidisciplinary project (NWO-TOP) we want to further develop, explore, and experimentally test concepts and molecular components of chemokine gradient sensing that leads to migration of immune, endothelial and tumor cells during tumor progression and angiogenesis in Ewing’s sarcoma using in vitro and zebrafish cancer models. The project aims at a molecular/mechanistic view of gradient sensing in tumor development. The fundamental knowledge generated in the course of the project has potential for application in anti-tumor immunity and anti-angiogenetic therapies for cancer treatment.
Group members involved: Sandra de Keijzer (PHD student, NWO-CW), Claudia Tulotta (PHD student, NOW-TOP) and Wietske van der Ent (PHD student on collaborative project with LUMC, funded by KIKA).
Collaborations: Prof. Pancras Hogendoorn (LUMC), Prof. Dr. Thomas Schmidt (LION) Dr. Annemarie Meijer (MCB-IBL), Prof. Herman Spaink (MCB-IBL).
Microenvironmental regulation of cancer angiogenesis and metastasis
How tumor cells interact with their microenvironment during tumor progression is a critical question in cancer biology. Answering this question requires live imaging of tumor-microenvironment interactions at the cellular level – a process severely limited in current animal models. To overcome this limitation, we established a xenograft model by injecting tumor cells into the blood circulation of transparent zebrafish embryos. This reproducibly results in rapid simultaneous formation of a localized tumor and micrometastasis, allowing time-resolved imaging at single-cell resolution. Roles of myeloid cells in critical tumorigenesis steps such as vascularization and invasion were revealed by genetic and pharmaceutical approaches. We discovered that the physiological migration of neutrophils controlled tumor invasion by conditioning the collagen matrix and forming the metastatic niche. Administration of VEGFR inhibitors enhanced migration of neutrophils, which in turn promoted tumor invasion. This work demonstrates the in vivo cooperativeness between VEGF signaling and myeloid cells in metastasis and provides a new mechanism underlying the recent findings that VEGFR targeting can promote tumor invasiveness (see figure above).
Currently we also study the role of immune cells in different aspects of cancer progression using novel transgenic lines with fluorescently marked immune cell population to facilitate real-time imaging. We attempt to unravel novel mechanisms of cancer inflammation and angiogenesis for the development of novel anti-tumor therapies based on targeting of vasculature and tumor-associated myeloid cells.
Group members involved: Shuning He (postdoc, ZF-CANCER project), Wietske van der Ent (PHD student on collaborative project with LUMC, funded by KIKA), Chao Cui (PHD student, SmartMix project) and Claudia Tulotta (PHD student, NOW-TOP).
Collaborations: Dr. Annemarie Meijer (MCB-IBL), Prof. Herman Spaink (MCB-IBL), Prof. Pancras Hogendoorn, Prof. Peter ten Dijke (LUMC), Drs. Jan-Willem Beenakker (PHD student LION), Drs. Veerander Ghotra (PHD student LACDR, ZF-CANCER) and Dr. Erik Danen (LACDR).
Human cancer modeling in zebrafish
Investigation of tumor migration and metastatic mechanisms are technically demanding (whole animal imaging) and expensive (instrumentation, animals). Replacement of small animals with a Danio rerio (zebrafish) embryo model is an alternative for these experiments. Because of the availability of transgenics, fluorescent reporter lines for vascular system and immune cells, and optical transparency, zebrafish is an excellent vertebrate model that allows the simultaneous in vivo imaging of cancer progression hallmarks. Recently we developed zebrafish xeno-transplantation assays to monitor cancer cell proliferation, migration, immune response, angiogenesis and metastasis formation within one week. The visual, non-invasive monitoring of cancer cells in transparent host embryos coupled with RNA interference and screens with chemical compounds enables the identification of novel gene targets and new compounds relevant for human cancer therapy, with the potential for commercial development. The zebrafish provides a fast, sensitive in vivo vertebrate model for identifying novel mechanisms of cancer progression and for development of medium to high-throughput application in preclinical target discovery and drug lead identification in a time- and cost-effective manner.
Group members involved: Shuning He (postdoc, ZF-CANCER project), Hanan Rian (PHD student, ZF-CANCER and ZF-HEALTH), Wietske van der Ent (PHD student on collaborative project with LUMC, funded by KIKA) and Claudia Tulotta (PHD student, NOW-TOP).
Collaborations: Prof. Herman Spaink (MCB-IBL), Prof. Pancras Hogendoorn (LUMC), Prof. Peter ten Dijke (LUMC), Prof. Clemens Lowik (LUMC), Drs. Veerander Ghotra (PHD student LACDR, ZF-CANCER) and Dr. Erik Danen (LACDR).
Professor of Cellular tumor biology
- Science
- Instituut Biologie Leiden
- IBL Animal Sciences
- Groenewoud A., Yin J., Gelmi M.C., Alsafadi S., Nemati F., Decaudin D., Roman-Roman S., Kalirai H., Coupland S.E., Jochemsen A.G., Jager M.J. & Snaar B.E. (2023), Patient derived zebrafish xenograft models reveal ferroptosis as a fatal and druggable weakness in metastatic uveal melanoma, Cell Death Discovery 9: 183.
- Li C., Ma J., Groenewoud A., Ren J., Liu S., Snaar-Jagalska B.E. & Dijke P. ten (2022), Establishment of embryonic zebrafish xenograft assays to investigate TGF-β family signaling in human breast cancer progression. In: Zi Z. & Liu X. (Eds.) TGF-Beta signaling. Methods in Molecular Biology no. 2488 New York: Humana. 67-80.
- Chen Q., Cuello-Garibo J.A., Bretin L.R., Zhang L., Ramu V., Aydar Y., Batsiun Y., Bronkhorst S., Husiev Y., Beztsinna N., Chen L., Zhou X.Q., Schmidt C., Ott I., Jager M.J., Brouwer A.M., Snaar-Jagalska B.E. & Bonnet S.A. (2022), Photosubstitution in a trisheteroleptic ruthenium complex inhibits conjunctival melanoma growth in a zebrafish orthotopic xenograft model, Chemical Science 13(23): 6899-6919.
- Glinkina K., Groenewoud A., Teunisse A.F.A.S., Snaar-Jagalska B.E. & Jochemsen A.G. (2022), Novel treatments of uveal melanoma identified with a synthetic lethal CRISPR/Cas9 screen, Cancers 14(13): 3186.
- Groenewoud A., Forn-Cuní G., Engel B. & Snaar-Jagalska B.E. (2022), XePhIR: the zebrafish xenograft phenotype interactive repository, Database 2022: baac028.
- Groenewoud A., Yin J. & Snaar-Jagalska B.E. (2021), Ortho- and ectopic zebrafish xeno-engraftment of ocular melanoma to recapitulate primary tumor and experimental metastasis development, Journal of visualized experiments 175: e62356.
- Kong L., Chen Q., Campbell F., Snaar‐Jagalska E. & Kros A. (2020), LighttTriggered cancer cell specific targeting and liposomal drug delivery in a zebrafish xenograft model, Advanced Healthcare Materials 9(6): 1901489.
- Chen Q.C., Ramu V., Aydar Y., Groenewoud A., Zhou X.Q., Jager M.J., Cole H., Cameron C.G., McFarland S.A., Bonnet S. & Snaar-Jagalska B.E. (2020), TLD1433 photosensitizer inhibits conjunctival melanoma cells in zebrafish ectopic and orthotopic tumour models, Cancers 12(3): 587.
- Kong L., Chen Q., Campbell F., Snaar‐Jagalska E. & Kros A. (2020), Light‐triggered cancer cell specific targeting and liposomal drug delivery in a zebrafish xenograft model, Advanced Healthcare Materials 9(6): 1901489.
- Berning P., Hennemann C., Tulotta C., Schaefer C., Lechtape B., Hotfilder M., El Gourari Y., Jürgens H., Snaar-Jagalska B.E., Hempel G., Dirksen U. & Potratz J. (2020), The receptor tyrosine kinase RON and its isoforms as therapeutic targets in Ewing sarcoma, Cancers 12(4): 904.
- Gennaro A. di, Damiano V., Brisotto G., Armellin M., Perin T., Zucchetto A., Guardascione M., Spaink H.P., Doglioni C., Snaar-Jagalska B.E., Santarosa M. & Maestro R. (2019), Correction to: A p53/miR-30a/ZEB2 axis controls triple negative breast cancer aggressiveness, Cell Death & Differentiation 26: 2493.
- Henderson F., Johnston H., Badrock A., Jones E., Forster D., Nagaraju R., Evangelou C., Kamarashev J., Green M., Fairclough M., Barinaga-Rementeria Ramirez I., He S., Snaar-Jagalska B.E., Hollywood K., Dunn W., Spaink H.P., Smith M., Lorigan P., Claude E., Williams K., McMahon A. & Hurlstone A. (2019), Enhanced fatty acid scavenging and glycerophospholipid metabolism accompany melanocyte neoplasia progression in zebrafish, Cancer Research 79(9): 2136-2151.
- Heitzer E., Groenewoud A., Meditz K., Lohberger B., Liegl-Atzwanger B., Prokesch A., Kashofer K., Behrens D., Haybaeck J., Kolb-Lenz D., Koefeler H., Riedl S., Schaider H., Fischer C., Snaar-Jagalska B.E., Jong D. de, Szuhai K., Zweytick D. & Rinner B. (2019), Human melanoma brain metastases cell line MUG-Mel1, isolated clones and their detailed characterization, Scientific Reports 9: 4096.
- Tulotta C., Stefanescu C., Chen Q., Torraca V., Meijer A.M. & Snaar-Jagalska B.E. (2019), CXCR4 signaling regulates metastatic onset by controlling neutrophil motility and response to malignant cells, Scientific Reports 9: 2399.
- Chen L., De Menna M., Groenewoud A., Thalmann G.N., Kruithof-de Julio M. & Snaar-Jagalska B.E. (2019), A NF-ĸB-Activin A signaling axis enhances prostate cancer metastasis, Oncogene : .
- Tulotta C. & Snaar-Jagalska B.E. (2019), CXCR4 signalling, metastasis and immunotherapy: zebrafish xenograft model as translational tool for anti-cancer discovery, Journal of Cancer Metastasis and Treatment 5: 74.
- Tulotta C., Groenewoud A., Snaar-Jagalska B.E. & Ottewell P. (2019), Animal models of breast cancer bone metastasis. In: Idris A.I. (Ed.), Bone Research Protocols. Methods in Molecular Biology no. 1914. New York, NY, U.S.A.: Humana Press. 309-330.
- Olszewski M.B., Pruszko M., Snaar-Jagalska B.E., Zylicz A. & Zylicz M. (2019), Diverse and cancer type‑specific roles of the p53 R248Q gain‑of‑function mutation in cancer migration and invasiveness, International Journal of Oncology 54(4): 1168-1182.
- Zoni E., Astrologo L., Ng Ch.K.Y., Piscuoglio S., Melsen J., Grosjean J., Klima I., Chen L., Snaar-Jagalska B.E., Flanagan K., Pluijm G. van der, Kloen P., Cecchini M., Kruithof-de-Julio M. & Thalmann G. (2019), Therapeutic targeting of CD146/MCAM reduces bone metastasis in prostate cancer, Molecular Cancer Research 17(5): 1013.
- Kiener M., Chen L., Krebs M., Grosjean J., Klima I., Kalogirou Ch., Riedmiller H., Kneitz B., Thalmann G.N., Snaar-Jagalska B.E., Spahn M., Kruithof-de Julio M. & Zoni E. (2019), miR-221-5p regulates proliferation and migration in human prostate cancer cells and reduces tumor growth in vivo, BMC Cancer 19: 627.
- Helm D. van der, Groenewoud A., Jonge-Muller E.S.M. de, Barnhoorn M.C., Schoonderwoerd M.J.A., Coenraad M.J., Hawinkels L.J.A.C., Snaar-Jagalska B.E., Hoek B. van & Verspaget H.W. (2018), Mesenchymal stromal cells prevent progression of liver fibrosis in a novel zebrafish embryo model, Scientific Reports 8(1): 16005.
- Paauwe M., Schoonderwoerd M.J.A., Helderman R.F.C.P., Harryvan T.J., Groenewoud A., Pelt G.W. van, Bor R., Hemmer D.M., Versteeg H.H., Snaar-Jagalska B.E., Theuer C.P., Hardwick J.C.H., Sier C.F.M., Dijke P. ten & Hawinkels L.J.A.C. (2018), Endoglin Expression on Cancer-Associated Fibroblasts Regulates Invasion and Stimulates Colorectal Cancer Metastasis, Clinical Cancer Research 24(24): 6331-6344.
- Hill D., Chen L., Snaar-Jagalska B.E. & Chaudhry B. (2018), Embryonic zebrafish xenograft assay of human cancer metastasis, F1000Research 7: 1682.
- Karkampouna S., Helm D. van der, Gray P.C., Chen L., Klima I., Grosjean J., Burgmans M.C., Farina-Sarasqueta A., Snaar-Jagalska B.E., Stroka D.M., Terracciano L., Hoek B. van, Schaapherder A.F., Osanto S., Thalmann G.N., Verspaget H.W., Coenraad M.J. & Kruithof-de Julio M. (2018), CRIPTO promotes an aggressive tumour phenotype and resistance to treatment in hepatocellular carcinoma, Journal of Pathology 245(3): 297-310.
- Gennaro A. di, Damiano V., Brisotto G., Armellin M., Perin T., Zucchetto A., Guardascione M., Spaink H.P., Doglioni C., Snaar-Jagalska B.E., Santarosa M. & Maestro R. (2018), A p53/miR-30a/ZEB2 axis controls triple negative breast cancer aggressiveness, Cell Death & Differentiation 25(12): 2165-2180.
- Cao J., Pontes K.C.S., Heijkants R.C., Brouwer N.J., Groenewoud A., Jordanova E.S., Marinkovic M., Duinen S. van, Teunisse A.F.A.S., Verdijk R.M., Snaar-Jagalska B.E., Jochemsen A.G. & Jager M.J. (2018), Overexpression of EZH2 in conjunctival melanoma offers a new therapeutic target, Journal of Pathology 245(4): 433-444.
- Torraca V., Tulotta C., Snaar-Jagalska B.E. & Meijer A.H. (2017), The chemokine receptor CXCR4 promotes granuloma formation by sustaining a mycobacteria-induced angiogenesis programme, Scientific Reports 7: 45061.
- Liverani C., La Manna F., Groenewoud A., Mercatali L., Pluijm G. van der, Pieri F., Cavaliere D., Vita A. de, Spadazzi C., Miserocchi G., Bongiovanni A., Recine F., Riva D., Amadori D., Snaar-Jagalska B.E. & Ibrahim T. (2017), Innovative approaches to establish and characterize primary cultures: an ex vivo 3D system and the zebrafish model, Biology Open 6: 133-140.
- Franzetti G.A., Laud-Duval K., Ent W. van der, Brisac A., Irondelle M., Aubert S., Dirksen U., Bouvier C., Pinieux G. de, Snaar-Jagalska B.E., Chavrier P. & Delattre O. (2017), Cell-to-cell heterogeneity of EWSR1-FLI1 activity determines proliferation/migration choices in Ewing sarcoma cells, Oncogene 36: 3505-3514.
- Drabsch Y., Snaar-Jagalska B.E. & Dijke P. ten (2017), Fish Tales: The Use of Zebrafish Xenograft Human Cancer Cell Models, Histology and Histopathology 32: 673-686.
- Zoni E., Chen L., Karkampouna S., Granchi Z., Verhoef E.I., La Manna F., Kelber J., Pelger R.C.M., Henry M.D., Snaar-Jagalska B.E., Leenders G.J.L.H. van, Beimers L., Kloen P., Gray P.C., Pluijm G. van der & Kruithof-de Julio M. (2017), CRIPTO and its signaling partner GRP78 drive the metastatic phenotype in human osteotropic prostate cancer, Oncogene 36: 4739-4749.
- Chen L., Groenewoud A., Tulotta C., Zoni E., Kruithof-de Julio M., Horst G. van der, Pluijm G. van der & Snaar-Jagalska B.E. (2017), A Zebrafish Xenograft Model for Studying Human Cancer Stem Cells in distant metastasis and therapy response, Methods in Cell Biology 138: 471-494.
- Sousa Pontes K.C. de, Groenewoud A., Cao J., Ataide L.M.S., Snaar-Jagalska B.E. & Jager M.J. (2017), Evaluation of (fli:GFP) Casper Zebrafish Embryos as a Model for Human Conjunctival Melanoma, Investigative Ophthalmology & Visual Science 58(14): 6065-6071.
- Yang J., Shimada Y., Olsthoorn R.R.C.L., Snaar-Jagalska B.E., Spaink H.P. & Kros A. (2016), Application of Coiled Coil Peptides in Liposomal Anti-Cancer Drug Delivery Using a Zebrafish Xenograft Model, ACS Nano 10(8): 7428-7435.
- Tulotta C., He S., Ent W. van der, Chen L., Groenewoud A., Spaink H.P. & Snaar-Jalaska B.E. (2016), Imaging Cancer Angiogenesis and Metastasis in a Zebrafish Embryo Model. In: Langenau D. (Ed.), Cancer and Zebrafish. Advances in Experimental Medicine and Biology no. 916. Cham: Springer. 239-263.
- Tulotta C., He S., Chen L., Groenewoud A., Ent W. van der, Meijer A.H., Spaink H.P. & Snaar-Jagalska B.E. (2016), Imaging of human cancer cell proliferation, invasion, and micrometastasis in a zebrafish xenogeneic engraftment model. In: Kawakami K., Patton E.E. & Orger M. (Eds.), Zebrafish. Methods in Molecular Biology no. 1451. New York: Springer. 155-169.
- Chen L., Groenewoud A., Pluijm G. van der & Snaar-Jagalska B.E. (2016), A zebrafish xenograft model for studying human cancer stem cells in distant metastasis and therapy response, Methods in Cell Biology 138: 471–496.
- Beletkaia E., Fenz S.A., Pomp W., Snaar-Jagalska B.E., Hogendoorn P.W.C. & Schmidt T. (2016), CXCR4 signaling is controlled by immobilization at the plasma membrane, Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1863(4): 607–616.
- Ent W. van der, Veneman W.J., Groenewoud A., Chen L., Tulotta C., Hogendoorn P.C., Spaink H.P. & Snaar-Jagalska B.E. (2016), Automation of Technology for Cancer Research. In: Langenau D. (Ed.), Cancer and Zebrafish. Advances in Experimental Medicine and Biology no. 916. Cham: Springer. 315-332.
- Tulotta C., Stefanescu C., Beletkaia E., Bussmann J., Tarbashevich K., Schmidt T. & Snaar-Jagalska B.E. (2016), Inhibition of signaling between human CXCR4 and zebrafish ligands by the small molecule IT1t impairs the formation of triple-negative breast cancer early metastases in a zebrafish xenograft model, Disease Models & Mechanisms 9(2): 141-153.
- Dhomen N., Marais R., Jager M.J., Snaar-Jagalska B.E., Coupland S., Romanowska-Dixon B., Mione M.C., Valente A., Ryll B., Ruijtenbeek R., Prestat A., Vinolo E. & Roman-Roman S. (2016), UM Cure 2020-A consortium of European experts in uveal melanoma to identify new therapies for patients with metastatic disease. European Journal of Cancer. 24th Biennial Congress of the European Association for Cancer Research, Manchester. 9 July 2016 - 12 July 2019. [conference poster].
- Kovar H., Amatruda J., Brunet E., Burdach S., Cidre-Aranaz F., Alava E. de, Dirksen U., Ent W. van der, Grohar P., Grünewald T.G., Helman L., Houghton P., Iljin K., Korsching E., Ladanyi M., Lawlor E., Lessnick S., Ludwig J., Meltzer P., Metzler M., Mora J., Moriggl R., Nakamura T., Papamarkou T., Radic Sarikas B., Rédini F., Richter G.H., Rossig C., Schadler K., Schäfer B.W., Scotlandi K., Sheffield N.C., Shelat A., Snaar B.E., Sorensen P., Stegmaier K., Stewart E., Sweet-Cordero A., Szuhai K., Tirado O.M., Tirode F., Toretsky J., Tsafou K., Üren A., Zinovyev A. & Delattre O. (2016), The second European interdisciplinary Ewing sarcoma research summit--A joint effort to deconstructing the multiple layers of a complex disease, OncoTarget 7(8): 8613-8624.
- Mercatali L., La Manna F., Groenewoud A., Casadei R., Recine F., Miserocchi G., Pieri F., Liverani C., Bongiovanni A., Spadazzi C., Vita A. de, Pluijm G. van der, Giorgini A., Biagini R., Amadori D., Ibrahim T. & Snaar-Jagalska B.E. (2016), Development of a Patient-Derived Xenograft (PDX) of Breast Cancer Bone Metastasis in a Zebrafish Model, International Journal of Molecular Sciences 17(8): 1375.
- Zoni E., Horst G. van der, Merbel A.F. van de, Chen L., Rane J.K., Pelger R.C.M., Collins A.T., Visakorpi T., Snaar-Jagalska B.E., Maitland N.J. & Pluijm G. van der (2015), miR-25 Modulates Invasiveness and Dissemination of Human Prostate Cancer Cells via Regulation of v- and 6-Integrin Expression, Cancer Research 75(11): 2326-2336.
- Ent W. van der, Burrello C., Lange M.J. de, Velden P.A. van der, Jochemsen A.G., Jager M.J. & Snaar-Jagalska B.E. (2015), Embryonic Zebrafish: Different Phenotypes after Injection of Human Uveal Melanoma Cells, Ocular Oncology and Pathology 1(3): 170-181.
- Sand L.G.L., Scotlandi K., Berghuis D., Snaar-Jagalska B.E., Picci P., Schmidt T., Szuhai K. & Hogendoorn P.C.W. (2015), CXCL14, CXCR7 expression and CXCR4 splice variant ratio associate with survival and metastases in Ewing sarcoma patients, European Journal of Cancer 51(17): 2624–2633.
- Ghotra V.P.S., He S., Horst G. van der, Nijhoff S., Bont H. de, Lekkerkerker A., Janssen R., Jenster G., Leenders G.J.L.H. van, Hoogland A., Marije M., Verhoef Esther I., Baranski Madrigal Z., Xiong J., Water B. van de, Pluijm G. van den, Snaar-Jagalska B.E. & Danen E.H.J. (2015), SYK is a candidate kinase target for the treatment of advanced prostate cancer, Cancer Research 75(1): 230-240.
- Evensen L., Johansen P.L., Koster G., Zhu K., Hefindal L., Speth M., Fenaroli F., Hildahl J., Bagherifam S., Tulota C., Prasmickaite L., Malandsmo G., Snaar-Jagalska B.E. & Griffiths G. (2015), Zebrafish as a model system for characterization of nanoparticles against cancer, Nanoscale 8(2): 862-877.
- Ent W. van der, Burrello C., Teunisse A.F.A.S., Ksander B.R., Velden P.A. van der, Jager M.J., Jochemsen A.G. & Snaar-Jagalska B.E. (2014), Modeling of Human Uveal Melanoma in Zebrafish Xenograft Embryos, Investigative Ophthalmology & Visual Science 55(10): 6612-6622.
- Truong H.H., Xiong J., Ghotra V.P.S., Nirmala E., Haazen L., Le Dévédec S.E., Balcioglu H.E., He S., Snaar-Jagalska B.E., Vreugdenhil E., Meerman J.H.N., Water B. van de & Danen E.H.J. (2014), beta(1) Integrin Inhibition Elicits a Prometastatic Switch Through the TGF beta-miR-200-ZEB Network in E-Cadherin-Positive Triple-Negative Breast Cancer, Science Signaling 7(312): ra15.
- Truong H.H., Xiong J., Ghotra V.P, Nirmala .E, Haazen L.C.J.M., Dévédec S.E. le, Balcioğlu H.E., He S., Snaar-Jagalska B.E., Vreugdenhil E., Meerman J.H.N., Water B. van de & Danen E.H. (2014), β1 integrin inhibition elicits a prometastatic switch through the TGFβ-miR-200-ZEB network in E-cadherin-positive triple-negative breast cancer, Science Signaling 7(312): ra15.
- Ent W. van der, Jochemsen A.G., Teunisse A.F., Krens S.G., Szuhai K., Spaink H.P., Hogendoorn P.C. & Snaar-Jagalska B.E. (2014), Ewing sarcoma inhibition by disruption of EWSR1-FLI1 transcriptional activity and reactivation of p53, Journal of Pathology 223(4): 415-424.
- Ban J., Aryee D.N., Fourtouna A., Ent W. van der, Kauer M., Niedan S., Machado I., Rodriguez-Galindo C., Tirado O.M., Schwentner R., Picci P., Flanagan A.M., Berg V., Strauss S.J., Scotlandi K., Snaar-Jagalska B.E., Lawlor E.R., Kovar H. & Llombart-Bosch A. (2014), Suppression of deacetylase SIRT1 mediates tumor-suppressive NOTCH response and offers a novel treatment option in metastatic Ewing sarcoma, Cancer Research 74(22): 6578-6588.
- Naber H.P., Drabsch Y.S., Snaar-Jagalska B.E., Dijke P. ten & Laar T. van (2013), Snail and Slug, key regulators of TGF-β-induced EMT, are sufficient for the induction of single-cell invasion, Biochemical and Biophysical Research Communications 435(1): 58-63.
- Snaar-Jagalska B.E., Cambi A., Schmidt T. & Keijzer S. de (2013), Single molecule imaging techniques to study the dynamic regulation of GPCR function in the plasma membrane, Methods in Enzymology 521: 47-67.
- Drabsch Y.S., He S., Zhang L., Snaar-Jagalska B.E. & Dijke P. ten (2013), Transforming growth factor-ß signalling controls human breast cancer metastasis in a zebrafish xenograft model, Breast Cancer Research 15: R106.
- Rian H., Krens S.F.G., Spaink H.P. & Snaar-Jagalska B.E. (2013), Generation of Constitutive Active ERK Mutants as Tools for Cancer Research in Zebrafish, ISRN Cell Biology 2013: 867613.
- Spaink H.P., Cui C., Wiweger M.I., Jansen H.J., Veneman W.J., Marin-Juez R., Sonneville J. de, Ordas A.K., Torraca V., Ent W. van der, Leenders W.P., Meijer A.H., Snaar-Jagalska B.E. & Dirks R.P.H. (2013), Robotic injection of zebrafish embryos for high-throughput screening in disease models, Methods 62(3): 246-254.
- Zhang L., Zhou F., Drabsch Y., Gao R., Snaar-Jagalska B.E., Mickanin C., Huang H., Sheppard K.A., Porter J.A. & Dijke P. ten (2012), USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-β type I receptor, Nature Cell Biology 14(7): 717-726.
- He S., Lamers G.E.M., Beenakker J.W.M., Cui C., Ghotra V.P., Danen E.H.J., Meijer A.H., Spaink H.P. & Snaar-Jagalska B.E. (2012), Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model, Journal of Pathology 227(4): 431-452.
- Ghotra V.P., He S., Bont H.J.G.M. de, Ent W. van der, Spaink H.P., Water B. van de, Snaar-Jagalska B.E. & Danen E.H.J. (2012), Automated whole animal bio-imaging assay for human cancer dissemination, PLOS ONE 7(2): e31281.
- Camus S., Quevedo S., Menendez S., Paramonov I., Janssen R.A., Rueb S., He S., Snaar-Jagalska B.E., Laricchia-Robbio L. & Izpisua Belmonte I.C. (2012), Identification of phosphorylase kinase as a novel therapeutic target through high-throughput screening for anti-angioooogenesis compounds in zebrafish, Oncogene 31: 4333-4342.
- He S., Krens S.F.G., Zhan H., Gong Z., Hogendoorn P.C.W., Spaink H.P. & Snaar-Jagalska B.E. (2011), A deltaRaf1-ER inducible oncogenic zebrafish liver cell model identifies hepatocellular carcinoma signatures, Journal of Pathology 225(1): 19-28.
- Serge A., Keijzer S. de, Hemert F. van, Hickman M., Hereld D., Spaink H.P., Schmidt T. & Snaar B.E. (2011), Quantification of GPCR internalization by single-molecule microscopy in living cells, Integrative Biology 3(6): 675-683.
- Kabli S., Shuning H., Spaink H.P., Hurlstone A., Snaar-Jagalska B.E., Groot H.J.M. de & Alia A. (2010), In vivo magnetic resonance imaging to detect malignant melanoma in adult zebrafish, Zebrafish 7(2): 143-148.
- Hemert F. van, Lazova M., Snaar-Jagalska B.E. & Schmidt T. (2010), Mobility of G proteins is heterogeneous and polarized during chemotaxis, Journal of Cell Science 123: 2922-2930.
- Mione M., Meijer A.H., Snaar-Jagalska B.E., Spaink H.P. & Trede N.S. (2009), Disease modeling in zebrafish: cancer and immune responses. second international workshop on Zebrafish Models of Cancer and the Immune Response 20 July 2009 - 22 July 2009. Zebrafish 445-451.
- Schaaf M., Koopmans W., Meckel T.M., Noort S.J.T. van, Snaar-Jagalska B.E., Schmidt T. & Spaink H.P. (2009), Single-molecule microscopy reveals membrane microdomain organization of cells in a living vertebrate, Biophysical Journal 97(4): 1206-1214.
- Snaar-Jagalska B.E. (2009), ZF-CANCER: Developing High-Throughput Bioassays for Human Cancers in Zebrafish, Zebrafish 6(4): 441-443.
- Krens S.F.G., He S., Lamers G.E.M., Meijer A.H., Bakkers J., Schmidt T., Spaink H.P. & Snaar-Jagalska B.E. (2008), Distinct functions for ERK1 and ERK2 in cell migration processes during zebrafish gastrulation, Developmental Biology 319(2): 370-383.
- Keijzer S. de, Sergé A., Hemert F. van, Lommerse P., Lamers G.E.M., Spaink H.P., Schmidt T. & Snaar-Jagalska B.E. (2008), A spatially restricted increase in receptor mobility is involved in directional sensing during Dictyostelium discoideum chemotaxis, Journal of Cell Science 121(10): 1750-1757.
- Krens S.F.G., Corredor-Adámez M., He S., Snaar-Jagalska B.E. & Spaink H.P. (2008), ERK1 and ERK2 MAPK are key regulators of distinct gene sets in zebrafish embryogenesis, BMC Genomics 9: 196.
- Keijzer S. de, Snaar-Jagalska B.E., Spaink H.P. & Schmidt T. (2008), Single molecule imaging of cellular signaling. In: Rigler R. & Vogel H. (Eds.), Single Molecules and Nanotechnology. Biophysics no. 12. Berlin, Heidelberg: Springer-Verlag. 107-129.
- Haupt B.J., Osbourn M., Spanhoff R., Keijzer S. de, Müller-Taubenberger A., Snaar-Jagalska B.E. & Schmidt T. (2007), Asymmetric elastic properties of Dictyostelium discoideum in relation to chemotaxis, Langmuir 23(18): 9352-9357.
- Trede N., Meijer A.H., Snaar-Jagalska B.E. & Spaink H.P. (2007), Model systems for infectious disease and cancer in zebrafish, EMBO workshop. EMBO Workshop 16 July 2007 - 18 July 2007. Zebrafish 287-292.
- He S., Salas-Vidal E., Rueb S., Krens S.F.G., Meijer A.H., Snaar-Jagalska B.E. & Spaink H.P. (2006), Genetic and transcriptome characterization of model zebrafish cell lines, Zebrafish 3(4): 441-453.
- Krens S.F.G., Spaink H.P. & Snaar-Jagalska B.E. (2006), Functions of the MAPK family in vertebrate development, FEBS Letters 580(21): 4984-4990.
- Krens S.F.G., He S., Spaink H.P. & Snaar-Jagalska B.E. (2006), Characterization and expression patterns of the MAPK family in zebrafish, Gene Expression Patterns 6(8): 1019-1026.
- Spaink H.P., Snaar-Jagalska B.E. & Meijer A.H. (2006), The innate immune system of vertebrates: challenges for future research. In: Sanchez F., Quinto C., Lopez-Lara I.M. & Geiger O. (Eds.), Biology of Plant-Microbe Interactions. St.Paul: I.S. for Molecular Plant-Microbe Interactions. 674-680.
- Lommerse P.H., Snaar-Jagalska B.E., Spaink H.P. & Schmidt T. (2005), Single-molecule diffusion measurements of H-Ras at the plasma membrane of live cells reveal microdomain localization upon activation, Journal of Cell Science 118(9): 1799-1809.
- Lommerse P.H., Blab G.A., Cognet L., Harms G.S., Snaar-Jagalska B.E., Spaink H.P. & Schmidt T. (2004), Single-molecule imaging of the h-ras membrane-anchor reveals domains in the cytoplasmic leaflet of the cell membrane, Biophysical Journal 86(1): 609-616.
- Meijer A.H., Krens S.F.G., Medina Rodriguez I.A., He S., Bitter W., Snaar-Jagalska B.E. & Spaink H.P. (2004), Expression analysis of the Toll-like receptor and TIR domain adaptor families of zebrafish, Molecular Immunology 40(11): 773-783.
- Snaar-Jagalska B.E., Krens S.F.G., Robina I., Wang L.X. & Spaink H.P. (2003), Specific activation of ERK pathways by chitin oligosaccharides in embryonic zebrafish cell lines, Glycobiology 13(10): 725-732.
- Schenk P.W., Epskamp S.J.P., Knetsch M.L.W., Harten V., Lagendijk E.L., Duijn B. van & Snaar-Jagalska B.E. (2001), Lysophosphatidic acid- and G beta-dependent activation of Dictyostelium MAP kinase ERK2, Biochemical and Biophysical Research Communications 282(3): 765-772.
- Schenk P.W. & Snaar-Jagalska B.E. (1999), Signal perception and transduction: the role of protein kinases, Biochimica et Biophysica Acta 1449(1): 1-24.
- Schenk P.W., Nebl T., Fisher P.R. & Snaar-Jagalska B.E. (1999), A serpentine receptor-dependent, G beta- and Ca2+ influx-independent pathway regulates mitogen-activated protein kinase ERK2 in Dictyostelium, Biochemical and Biophysical Research Communications 260(2): 504-509.
- Knetsch M.L.W., Heusden G.P.H. van, Ennis H.L., Shaw D.R., Epskamp S.J.P. & Snaar-Jagalska B.E. (1998), Isolation of a Dictyostelium discoideum 14-3-3 homologue which can replace the essential yeast BMH1 and BMH2 genes, Biochimica et Biophysica Acta (BBA) - Molecular Cell Research 1357(2): 243-248.
- Knetsch M.L., Epskamp S.J., Schenk P.W., Wang Y., Segall J.E. & Snaar-Jagalska B.E. (1996), Dual role of cAMP and involvement of both G-proteins and ras in regulation of ERK2 in Dictyostelium discoideum, The EMBO Journal 15(13): 3361-3368.
- Knetsch M., Wang M., Snaar-Jagalska B.E. & Heimovaara-Dijkstra S. (1996), Abscisic Acid Induces Mitogen-Activated Protein Kinase Activation in Barley Aleurone Protoplasts, The Plant Cell 8(6): 1061-1067.
- Snaar-Jagalska B.E. & Haastert P.J. van (1994), G-protein assays in Dictyostelium, Methods in Enzymology 237: 387-408.
- Wang M., Sedee N.J., Heidekamp F. & Snaar-Jagalska B.E. (1993), Detection of GTP-binding proteins in barley aleurone protoplasts, FEBS Letters 329(3): 245-248.
- Peters D.J., Snaar-Jagalska B.E., Haastert P.J. van & Schaap P. (1992), Lithium, an inhibitor of cAMP-induced inositol 1,4,5-trisphosphate accumulation in Dictyostelium discoideum, inhibits activation of guanine-nucleotide-binding regulatory proteins, reduces activation of adenylylcyclase, but potentiates activation of guanylyl cyclase by cAMP, European Journal of Biochemistry 209(1): 299-304.
- Ludérus M.E., Kesbeke F., Knetsch M.L., Driel R. van, Reymond C.D. & Snaar-Jagalska B.E. (1992), Ligand-independent reduction of cAMP receptors in Dictyostelium discoideum cells over-expressing a mutated ras gene, European Journal of Biochemistry 208(2): 235-240.
- Schenk P.W., Es S. van, Kesbeke F. & Snaar-Jagalska B.E. (1991), Involvement of cyclic AMP cell surface receptors and G-proteins in signal transduction during slug migration of Dictyostelium discoideum, Developmental Biology 145(1): 110-118.
- Snaar-Jagalska B.E., Es S. van, Kesbeke F. & Haastert P.J. van (1991), Activation of a pertussis-toxin-sensitive guanine-nucleotide-binding regulatory protein during desensitization of Dictyostelium discoideum cells to chemotactic signals, FEBS Journal 195(3): 715-721.
- Bominaar A.A., Kesbeke F., Snaar-Jagalska B.E., Peters D.J., Schaap P. & Haastert P.J. van (1991), Abberant chemotaxis and differentiation in Dictyostelium mutant fgdC with a defective regulation of receptor-stimulated phosphoinositidase C, Journal of Cell Science 100(4): 825-831.
- Peters D.J., Bominaar A.A., Snaar-Jagalska B.E., Brandt R., Haastert P.J. van, Ceccarelli A., Williams J.G. & Schaap P. (1991), Selective induction of gene expression and second-messenger accumulation in Dictyostelium discoideum by the partial chemotactic antagonist 8-p-chlorophenylthioadenosine 3',5'-cyclic monophosphate, Proceedings of the National Academy of Sciences 88(20): 9219-9223.
- Snaar-Jagalska B.E. & Haastert P.J. van (1990), Pertussis toxin inhibits cAMP-induced desensitization of adenylate cyclase in Dictyostelium discoideum, Molecular and Cellular Biochemistry 92(2): 177-189.
- Bominaar A.A., Kaay J. van der, Kesbeke F., Snaar-Jagalska B.E. & Haastert P.J. van (1990), G-proteins and the inositol cycle in Dictyostelium discoideum, Biochemical Society Symposia 56: 71-80.
- Haastert P.J.M. van, Bominaar A.A., Kaay J. van der, Drayer R., Penning L.C., Roovers E., Vries M.M. de, Vink A.A., Kesbeke F. & Snaar-Jagalska B.E. (1990), The inositolcycle of Dictyostelium discoideum. In: Konijn T.M., Houslay M.D. & Haastert P.J.M. van (Eds.), Activation and Desensitization of Transducing Pathways no. NATO ASI Series H Cell Biology. Berlin, Heidelberg: Springer Verlag. 41-59.
- Kesbeke F., Haastert P.J.M. van, Wit R.J.W. de & Snaar-Jagalska B.E. (1990), Chemotaxis to cyclic AMP and folic acid is mediated by different G proteins in Dictyostelium discoideum, Journal of Cell Science 96: 669-673.
- Bominaar A.A., Snaar-Jagalska B.E., Kesbeke F. & Haastert P.J.M. van (1989), Signal-transducing G-proteins in Dictyostelium discoideum. In: Bosch L., Kraal B. & Parmeggiani A. (Eds.), The Guanine Nucleotide Binding Proteins. Common Structural and Functional Properties no. NATO ASI Series A. Boston, MA: Springer. 369-375.
- Snaar-Jagalska B.E., Devreotes P.N. & Haastert P.J.M. van (1988), Ligand-induced modification of a surface cAMP receptor of Dictyostelium discoideum does not require its occupancy, Journal of Biological Chemistry 263(2): 897-901.
- Snaar-Jagalska B.E., Kesbeke F.M.H.N. & Haastert P.J. van (1988), G-proteins in the signal-transduction pathways of Dictyostelium discoideum, Genesis 9(4-5): 215-226.
- Snaar-Jagalska B.E., Jakobs K.H. & Haastert P.J. van (1988), Agonist-stimulated high-affinity GTPase in Dictyostelium membranes, FEBS Letters 236(1): 139-144.
- Kesbeke F., Snaar-Jagalska B.E. & Haastert P.J. van (1988), Signal transduction in Dictyostelium fgd A mutants with a defective interaction between surface cAMP receptors and a GTP-binding regulatory protein, Journal of Cell Biology 107(2): 521-528.
- Snaar-Jagalska B.E., Wit R.J. de & Haastert P.J. van (1988), Pertussis toxin inhibits cAMP surface receptor-stimulated binding of [35S]GTP gamma S to Dictyostelium discoideum membranes, FEBS Letters 232(1): 148-152.
- Snaar-Jagalska B.E., Kesbeke F., Pupillo M. & Haastert P.J. van (1988), Immunological detection of G-protein alpha-subunits in Dictyostelium discoideum, Biochemical and Biophysical Research Communications 156(2): 757-761.
- Snaar-Jagalska B.E. & Haastert P.J.M. van (1988), Dictyostelium discoideum mutant synag 7 with altered G-protein-adenylate cyclase interaction, Journal of Cell Science 91: 287-294.
- Haastert P.J.M. van, Wit R.J.W. de, Janssens P.M.W., Kesbeke F., Snaar-Jagalska B.E., Lookeren Campagne M.M. van & Konijn T.M. (1987), Adaptation of Dictostelium discoideum cells to chemotactic signals. In: Konijn T.M., Haastert P.J.M. van, Starre H. van der, Wel H. van der & Houslay M.D. (Eds.), Molecular mechanisms of desensitization to signal molecules. NATO ASI Series (Series H: Cell Biology) no. Volume 6. Heidelberg, F.R.G.: Springer Verlag. 25-42.
- Haastert P.J. van, Snaar-Jagalska B.E. & Janssens P.M. (1987), The regulation of adenylate cyclase by guanine nucleotides in Dictyostelium discoideum membranes, European Journal of Biochemistry 162(2): 251-258.
- Franssen J.M., Snaar-Jagalska B.E. & Hulst C.T.C. van der (1986), The development of Elisa to determine abscisic acid and indole-3-acetic acid in bulbous crops, Acta Horticulturae 177: 563-567.
- Wit R.J. de & Snaar-Jagalska B.E. (1985), Folate and cAMP modulate GTP binding to isolated membranes of Dictyostelium discoideum. Functional coupling between cell surface receptors and G-proteins, Biochemical and Biophysical Research Communications 129(1): 11-17.
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