A transgenic zebrafish model expressing KIT-D816V recapitulates features of aggressive systemic mastocytosis

British Journal of Haematology

Volumn 167, Issue 1, 2014, Pages 48-61

  Balci, Tugce B ^a,b   Prykhozhij, Sergey V ^a   Teh, Evelyn M ^a   Da'as, Sahar I ^a   Mcbride, Eileen ^a,c   Liwski, Robert ^d   Chute, Ian C ^e   Leger, Daniel ^e   Lewis, Stephen M ^d,e,f,g   Berman, Jason N ^a,d  

^a IWK HEALTH CENTRE   (Canada)

^b UNIVERSITY OF OTTAWA   (Canada)

^c Hopital Montfort Hospital   (Canada)

^d DALHOUSIE UNIVERSITY   (Canada)

^e ATLANTIC CANCER RESEARCH INSTITUTE   (Canada)

^f UNIVERSITY OF NEW BRUNSWICK   (Canada)

^g UNIVERSITÉ DE MONCTON   (Canada)

Author keywords

KIT D816V; Receptor tyrosine kinase; Systemic mastocytosis; Transgenesis; Zebrafish

Indexed keywords

DNA METHYLTRANSFERASE 1; EPITHELIAL CELL ADHESION MOLECULE; CELL ADHESION MOLECULE; DNA (CYTOSINE 5) METHYLTRANSFERASE; DNMT1 PROTEIN, ZEBRAFISH; PEPTIDE HYDROLASE; STEM CELL FACTOR RECEPTOR; TUMOR ANTIGEN; TUMOR-ASSOCIATED ANTIGEN GA733; ZEBRAFISH PROTEIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL CYCLE; DISEASE MODEL; DNMT1 GENE; DOWN REGULATION; EMBRYO; EPCAM GENE; FEMALE; GENE; GENE EXPRESSION; GENE MUTATION; IN VIVO STUDY; KIT GENE; MAST CELL; MYELOPROLIFERATIVE DISORDER; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SYSTEMIC MASTOCYTOSIS; TRANSGENIC ZEBRAFISH; ANIMAL; ANIMAL EMBRYO; APOPTOSIS; ENZYMOLOGY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE ORDER; GENE VECTOR; GENETICS; HEMATOPOIESIS; HUMAN; KIDNEY; MASTOCYTOSIS; METABOLISM; MUTATION; PATHOLOGY; PHENOTYPE; TRANSGENIC ANIMAL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTIGENS, NEOPLASM; APOPTOSIS; CELL ADHESION MOLECULES; CELL CYCLE; DISEASE MODELS, ANIMAL; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; EMBRYO, NONMAMMALIAN; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE ORDER; GENETIC VECTORS; HEMATOPOIESIS; HUMANS; KIDNEY; MAST CELLS; MASTOCYTOSIS; MASTOCYTOSIS, SYSTEMIC; MUTATION; PEPTIDE HYDROLASES; PHENOTYPE; PROTO-ONCOGENE PROTEINS C-KIT; ZEBRAFISH; ZEBRAFISH PROTEINS;

EID: 84909972068     PISSN: 00071048     EISSN: 13652141     Source Type: Journal    
DOI: 10.1111/bjh.12999     Document Type: Article

References (51)

1. Berman, J., Hsu, K. & Look, A.T. (2003) Zebrafish as a model organism for blood diseases. British Journal of Haematology, 123, 568-576.
2. Burns, C.G., Milan, D.J., Grande, E.J., Rottbauer, W., MacRae, C.A. & Fishman, M.C. (2005) High-throughput assay for small molecules that modulate zebrafish embryonic heart rate. Nature Chemical Biology, 1, 263-264.
3. Chen, E.Y. & Langenau, D.M. (2011) Zebrafish models of rhabdomyosarcoma. Methods in Cell Biology, 105, 383-402.
4. Da'as, S., Teh, E.M., Dobson, J.T., Nasrallah, G.K., McBride, E.R., Wang, H., Neuberg, D.S., Marshall, J.S., Lin, T.-J. & Berman, J.N. (2011) Zebrafish mast cells possess an Fce{open}RI-like receptor and participate in innate and adaptive immune responses. Developmental and Comparative Immunology, 35, 125-134.
5. Da'as, S.I., Coombs, A.J., Balci, T.B., Grondin, C.A, Ferrando, A.A & Berman, J.N. (2012) The zebrafish reveals dependence of the mast cell lineage on Notch signaling in vivo. Blood, 119, 3585-3594.
6. Dahlem, T.J., Hoshijima, K., Jurynec, M.J., Gunther, D., Starker, C.G., Locke, A.S., Weis, A.M., Voytas, D.F. & Grunwald, D.J. (2012) Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genetics, 8, e1002861. Available at: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3420959&tool=pmcentrez&rendertype=abstract [Accessed April 30, 2014].
7. D'ambrosio, C., Akin, C., Wu, Y., Magnusson, M.K. & Metcalfe, D.D. (2003) Gene expression analysis in mastocytosis reveals a highly consistent profile with candidate molecular markers. The Journal of Allergy and Clinical Immunology, 112, 1162-1170.
8. Deveau, A., Forrester, A.M., Grabher, C., Coombs, A.J., Chute, I., Leger, D., Lewis, S., Look, A.T. & Berman, J.N. (2012) Epigenetic therapy inhibits NUP98-HOXA9-mediated myeloid disease - decitabine and valproic acid work synergistically to rescue normal hematopoiesis in transgenic zebrafish. Blood (ASH Annual Meeting Abstracts), 120, 2391.
9. Dobson, J.T., Seibert, J., Teh, E.M., Da'as, S., Fraser, R.B., Paw, B.H., Lin, T.-J. & Berman, J.N. (2008) Carboxypeptidase A5 identifies a novel mast cell lineage in the zebrafish providing new insight into mast cell fate determination. Blood, 112, 2969-2972.
10. Forrester, A.M., Grabher, C., McBride, E.R., Boyd, E.R., Vigerstad, M.H., Edgar, A., Kai, F.-B., Da'as, S.I., Payne, E., Look, A.T. & Berman, J.N. (2011) NUP98-HOXA9-transgenic zebrafish develop a myeloproliferative neoplasm and provide new insight into mechanisms of myeloid leukaemogenesis. British Journal of Haematology, 155, 167-181.
11. Gerbaulet, A., Wickenhauser, C., Scholten, J., Peschke, K., Drube, S., Horny, H.-P., Kamradt, T., Naumann, R., Müller, W., Krieg, T., Waskow, C., Hartmann, K. & Roers, A. (2011) Mast cell hyperplasia, B-cell malignancy, and intestinal inflammation in mice with conditional expression of a constitutively active kit. Blood, 117, 2012-2021.
12. Gerlach, G.F., Schrader, L.N. & Wingert, R.A. (2011) Dissection of the adult zebrafish kidney. Journal of Visualized Experiments: JoVE, 54, 1-5.
13. Jette, C.A., Flanagan, A.M., Ryan, J., Pyati, U.J., Carbonneau, S., Stewart, R.A., Langenau, D.M., Look, A.T. & Letai, A. (2008) BIM and other BCL-2 family proteins exhibit cross-species conservation of function between zebrafish and mammals. Cell Death and Differentiation, 15, 1063-1072.
14. Jing, L. & Zon, L.I. (2011) Zebrafish as a model for normal and malignant hematopoiesis. Disease Models & Mechanisms, 4, 433-438.
15. Kwan, K.M., Fujimoto, E., Grabher, C., Mangum, B.D., Hardy, M.E., Campbell, D.S., Parant, J.M., Yost, H.J., Kanki, J.P. & Chien, C.-B. (2007) The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 236, 3088-3099.
16. Langenau, D.M., Traver, D., Ferrando, A.A., Kutok, J.L., Aster, J.C., Kanki, J.P., Lin, S., Prochownik, E., Trede, N.S., Zon, L.I. & Look, A.T. (2003) Myc-induced T cell leukemia in transgenic zebrafish. Science, 299, 887-890.
17. Longley, J.B., Tyrell, L., Lu, S.-Z., Ma, Y.-S., Langley, K., Ding, T., Duffy, T., Jacobs, P., Tang, L.H. & Modlin, I. (1996) Somatic c-KIT activating mutation in urticaria pigmentosa and aggressive mastocytosis: establishment of clonality ina human mast cell neoplasm. Nature Genetics, 12, 312-314.
18. Martin, P. & Feng, Y. (2009) Inflammation: wound healing in zebrafish. Nature, 459, 921-923.
19. Metcalfe, D.D. (2008) ASH 50th anniversary review Mast cells and mastocytosis. Blood, 112, 946-956.
20. Metcalfe, D.D. & Akin, C. (2001) Mastocytosis: molecular mechanisms and clinical disease heterogeneity. Leukemia Research, 25, 577-582.
21. Nagata, H., Worobec, A.S., Oh, C.K., Chowdhury, B.A., Tannenbaum, S., Suzuki, Y. & Metcalfe, D.D. (1995) Identification of a point mutation in the catalytic domain of the protooncogene c-kit in peripheral blood mononuclear cells of patients who have mastocytosis with an associated hematologic disorder. Proceedings of the National Academy of Sciences of the United States of America, 92, 10560-10564.
22. Ng, J.M.Y., Vermeulen, W., van der Horst, G.T.J., Bergink, S., Sugasawa, K., Vrieling, H. & Hoeijmakers, J.H.J. (2003) A novel regulation mechanism of DNA repair by damage-induced and RAD23-dependent stabilization of xeroderma pigmentosum group C protein. Genes & Development, 17, 1630-1645.
23. North, T.E., Goessling, W., Walkley, C.R., Lengerke, C., Kopani, K.R., Lord, A.M., Weber, G.J., Bowman, T.V., Jang, I.-H., Grosser, T., Fitzgerald, G.A., Daley, G.Q., Orkin, S.H. & Zon, L.I. (2007) Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature, 447, 1007-1011.
24. Ogi, T., Limsirichaikul, S., Overmeer, R.M., Volker, M., Takenaka, K., Cloney, R., Nakazawa, Y., Niimi, A., Miki, Y., Jaspers, N.G., Mullenders, L.H.F., Yamashita, S., Fousteri, M.I. & Lehmann, A.R. (2010) Three DNA polymerases, recruited by different mechanisms, carry out NER repair synthesis in human cells. Molecular Cell, 37, 714-727.
25. Pardanani, A. (2012) Systemic mastocytosis in adults: 2012 update on diagnosis, risk stratification, and management. American Journal of Hematology, 87, 401-411.
26. Patnaik, M.M., Rindos, M., Kouides, P.A, Tefferi, A. & Pardanani, A. (2007) Systemic mastocytosis: a concise clinical and laboratory review. Archives of Pathology & Laboratory Medicine, 131, 784-791.
27. Patton, E.E., Widlund, H.R., Kutok, J.L., Kopani, K.R., Amatruda, J.F., Murphey, R.D., Berghmans, S., Mayhall, E.A., Traver, D., Fletcher, C.D.M., Aster, J.C., Granter, S.R., Look, A.T., Lee, C., Fisher, D.E. & Zon, L.I. (2005) BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Current Biology: CB, 15, 249-254.
28. Peterson, R.T., Link, B.A., Dowling, J.E. & Schreiber, S.L. (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proceedings of the National Academy of Sciences of the United States of America, 97, 12965-12969.
29. Pontarin, G., Ferraro, P., Bee, L., Reichard, P. & Bianchi, V. (2012) Mammalian ribonucleotide reductase subunit p53R2 is required for mitochondrial DNA replication and DNA repair in quiescent cells. Proceedings of the National Academy of Sciences of the United States of America, 109, 13302-13307.
30. Renshaw, S.A. & Trede, N.S. (2012) A model 450 million years in the making: zebrafish and vertebrate immunity. Disease Models & Mechanisms, 5, 38-47.
31. Ribatti, D., Crivellato, E., Roccaro, A.M., Ria, R. & Vacca, A. (2004) Mast cell contribution to angiogenesis related to tumour progression. Clinical and Experimental Allergy: Journal of the British Society for Allergy and Clinical Immunology, 34, 1660-1664.
32. Ribatti, D., Crivellato, E. & Molica, S. (2009) Mast cells and angiogenesis in haematological malignancies. Leukemia Research, 33, 876-879.
33. Robyn, J. & Metcalfe, D.D. (2006) Systemic mastocytosis. Advances in Immunology, 89, 169-243.
34. Sabaawy, H.E., Azuma, M., Embree, L.J., Tsai, H. J., Starost, M.F. & Hickstein, D.D. (2006) TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proceedings of the National Academy of Sciences of the United States of America, 103, 15166-15171.
35. Santoriello, C., Gennaro, E., Anelli, V., Distel, M., Kelly, A., Köster, R.W., Hurlstone, A. & Mione, M. (2010) Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLoS One, 5, e15170.
36. Schnell, U., Cirulli, V. & Giepmans, B.N.G. (2013) EpCAM: structure and function in health and disease. Biochimica et Biophysica Acta, 1828, 1989-2001.
37. Shepard, J.L., Stern, H.M., Pfaff, K.L. & Amatruda, J.F. (2004) Analysis of the cell cycle in zebrafish embryos. Methods in Cell Biology, 76, 109-125.
38. Sidi, S., Sanda, T., Kennedy, R.D., Hagen, A.T., Jette, C.A., Hoffmans, R., Pascual, J., Imamura, S., Kishi, S., Amatruda, J.F., Kanki, J.P., Green, D.R., D'Andrea, A.A. & Look, A.T. (2008) Chk1 suppresses a caspase-2 apoptotic response to DNA damage that bypasses p53, Bcl-2, and caspase-3. Cell, 133, 864-877.
39. Swindell, W.R. (2011) Metallothionein and the biology of aging. Ageing Research Reviews, 10, 132-145.
40. Takemoto, C.M., Lee, Y.-N., Jegga, A.G., Zablocki, D., Brandal, S., Shahlaee, A., Huang, S., Ye, Y., Gowrisankar, S., Huynh, J. & McDevitt, M.A. (2009) Mast cell transcriptional networks. Blood Cells, Molecules & Diseases, 41, 82-90.
41. Theoharides, T.C. & Kalogeromitros, D. (2006) The critical role of mast cells in allergy and inflammation. Annals of the New York Academy of Sciences, 1088, 78-99.
42. Traver, D., Herbomel, P., Patton, E.E., Murphey, R.D., Yoder, J.A., Litman, G.W., Catic, A., Amemiya, C.T., Zon, L.I. & Trede, N.S. (2003) The zebrafish as a model organism to study development of the immune system. Advances in Immunology, 81, 253-330.
43. Trowbridge, J.J., Snow, J.W., Kim, J. & Orkin, S.H. (2009) DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell, 5, 442-449.
44. Trowbridge, J.J., Sinha, A.U., Zhu, N., Li, M., Armstrong, S.A. & Orkin, S.H. (2012) Haploinsufficiency of Dnmt1 impairs leukemia stem cell function through derepression of bivalent chromatin domains. Genes & Development, 26, 344-349.
45. Tsang, M. (2010) Zebrafish: a tool for chemical screens. Birth Defects Research Part C, Embryo Today: Reviews, 90, 185-192.
46. Ustun, C., DeRemer, D.L. & Akin, C. (2011) Tyrosine kinase inhibitors in the treatment of systemic mastocytosis. Leukemia Research, 35, 1143-1152.
47. Villablanca, E.J., Renucci, A., Sapède, D., Lec, V., Soubiran, F., Sandoval, P.C., Dambly-Chaudière, C., Ghysen, A. & Allende, M.L. (2006) Control of cell migration in the zebrafish lateral line: implication of the gene "tumour-associated calcium signal transducer", tacstd. Developmental Dynamics: An Official Publication of the American Association of Anatomists, 235, 1578-1588.
48. Westerfield, M. (2007) The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), 5th edn. The University of Oregon Press, Eugene, OR.
49. Yeh, J.-R.J., Munson, K.M., Elagib, K.E., Goldfarb, A.N., Sweetser, D.A. & Peterson, R.T. (2009) Discovering chemical modifiers of oncogene-regulated hematopoietic differentiation. Nature Chemical Biology, 5, 236-243.
50. Yoo, S.K., Starnes, T.W., Deng, Q. & Huttenlocher, A. (2011) Lyn is a redox sensor that mediates leukocyte wound attraction in vivo. Nature, 480, 109-112.
51. Zappulla, J.P., Dubreuil, P., Desbois, S., Létard, S., Hamouda, N.B., Daëron, M., Delsol, G., Arock, M. & Liblau, R.S. (2005) Mastocytosis in mice expressing human Kit receptor with the activating Asp816Val mutation. The Journal of Experimental Medicine, 202, 1635-1641.