Zebrafish models of cancer: Progress and future challenges

Current Opinion in Genetics and Development

Volumn 24, Issue 1, 2014, Pages 38-45

  Yen, Jennifer ^a   White, Richard M ^b   Stemple, Derek L ^a  

^a WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CANCER GENETICS; CANCER MODEL; CANCER THERAPY; CHEMICAL ANALYSIS; COMPARATIVE GENOMIC HYBRIDIZATION; EMBRYONAL RHABDOMYOSARCOMA; GENE EXPRESSION; GENETIC ANALYSIS; GENETIC HETEROGENEITY; HEMATOLOGIC MALIGNANCY; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MELANOMA; METASTASIS; MUTAGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SOLID TUMOR; TRANSGENIC ANIMAL; TRANSGENICS; ZEBRA FISH;

ANIMALS; DISEASE MODELS, ANIMAL; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION, NEOPLASTIC; GENOMICS; HUMANS; NEOPLASMS; ZEBRAFISH;

EID: 84891086559     PISSN: 0959437X     EISSN: 18790380     Source Type: Journal    
DOI: 10.1016/j.gde.2013.11.003     Document Type: Review

References (76)

1. 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., et al. Myc-induced T cell leukemia in transgenic zebrafish. Science 2003, 299:887-890.
2. Yang H.W., Kutok J.L., Lee N.H., Piao H.Y., Fletcher C.D.M., Kanki J.P., Look A.T. Targeted expression of human MYCN selectively causes pancreatic neuroendocrine tumors in transgenic zebrafish. Cancer Res 2004, 64:7256-7262.
3. Berghmans S., Look T.A. tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci U S A 2005, 102:407-412.
4. Sabaawy H.E., Azuma M., Embree L.J., Tsai H.-J., Starost M.F., Hickstein D.D. TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proc Natl Acad Sci U S A 2006, 103:15166-15171.
5. Faucherre A., Taylor G.S., Overvoorde J., Dixon J.E., Hertog J.D. Zebrafish pten genes have overlapping and non-redundant functions in tumorigenesis and embryonic development. Oncogene 2007, 27:1079-1086.
6. Chen J., Jette C., Kanki J.P., Aster J.C., Look A.T., Griffin J.D. NOTCH1-induced T-cell leukemia in transgenic zebrafish. Leukemia 2007, 21:462-471.
7. 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. BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr Biol 2005, 15:249-254.
8. Dovey M., White R.M., Zon L.I. Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 2009, 6:397-404.
9. Neumann J.C., Dovey J.S., Chandler G.L., Carbajal L., Amatruda J.F. Identification of a heritable model of testicular germ cell tumor in the zebrafish. Zebrafish 2009, 6:319-327.
10. Frazer J.K., Meeker N.D., Rudner L., Bradley D.F., Smith A.C.H., Demarest B., Joshi D., Locke E.E., Hutchinson S.A., Tripp S., et al. Heritable T-cell malignancy models established in a zebrafish phenotypic screen. Leukemia 2009, 23:1825-1835.
11. Langenau D.M., Keefe M.D., Storer N.Y., Guyon J.R., Kutok J.L., Le X., Goessling W., Neuberg D.S., Kunkel L.M., Zon L.I. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev 2007, 21:1382-1395.
12. Santoriello C., Gennaro E., Anelli V., Distel M., Kelly A., Köster R.W., Hurlstone A., Mione M. Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLoS ONE 2010, 5:e15170.
13. Liu S., Leach S.D. Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system. Methods in Cell Biology 2011, 367-381. Academic Press, New York, (Chapter 15). H. William Detrich, M. Westerfield, L.I. Zon (Eds.).
14. Nguyen A.T., Emelyanov A., Koh C.H.V., Spitsbergen J.M., Parinov S., Gong Z. An inducible krasV12 transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis Model Mech 2011, 5:63-72.
15. Shin J., Padmanabhan A., de Groh E.D., Lee J.-S., Haidar S., Dahlberg S., Guo F., He S., Wolman M.A., Granato M., et al. Zebrafish neurofibromatosis type 1 genes have redundant functions in tumorigenesis and embryonic development. Dis Model Mech 2012, 5:881-894.
16. Leacock S., Basse A., Chandler G., Kirk A., Rakheja D., Amatruda J. A zebrafish transgenic model of Ewing's sarcoma reveals conserved mediators of EWS-FLI1 tumorigenesis. Dis Model Mech 2012, 5:95-106.
17. Feng H., Stachura D.L., White R.M., Gutierrez A., Zhang L., Sanda T., Jette C.A., Testa J.R., Neuberg D.S., Langenau D.M., et al. T-lymphoblastic lymphoma cells express high levels of BCL2, S1P1, and ICAM1, leading to a blockade of tumor cell intravasation. Cancer Cell 2010, 18:353-366.
18. Ridges S., Heaton W.L., Joshi D., Choi H., Eiring A., Batchelor L., Choudhry P., Manos E.J., Sofla H., Sanati A., et al. Zebrafish screen identifies novel compound with selective toxicity against leukemia. Blood 2012, 119:5621-5631.
19. Zhuravleva J., Paggetti J., Martin L., Hammann A., Solary E., Bastie J.-N., Delva L. MOZ/TIF2-induced acute myeloid leukaemia in transgenic fish. Br J Haematol 2008, 143:378-382.
20. Le X., Langenau D., Keefe M., Kutok J., Neuberg D., Zon L. Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish. Proc Natl Acad Sci U S A 2007, 104:9410-9415.
21. 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., et al. NUP98-HOXA9-transgenic zebrafish develop a myeloproliferative neoplasm and provide new insight into mechanisms of myeloid leukaemogenesis. Br J Haematol 2011, 155:167-181.
22. Yeh J.R.J., Munson K.M., Chao Y.L., Peterson Q.P., MacRae C.A., Peterson R.T. AML1-ETO reprograms hematopoietic cell fate by downregulating scl expression. Development 2007, 135:401-410.
23. Yeh J.-R.J., Munson K.M., Elagib K.E., Goldfarb A.N., Sweetser D.A., Peterson R.T. Discovering chemical modifiers of oncogene-regulated hematopoietic differentiation. Nat Chem Biol 2009, 5:236-243.
24. Haramis A.-P.G., Hurlstone A., van der Velden Y., Begthel H., van den Born M., Offerhaus G.J.A., Clevers H.C. Adenomatous polyposis coli-deficient zebrafish are susceptible to digestive tract neoplasia. EMBO Rep 2006, 7:444-449.
25. Davies H., Bignell G.R., Cox C., Stephens P., Edkins S., Clegg S., Teague J., Woffendin H., Garnett M.J., Bottomley W., et al. Mutations of the BRAF gene in human cancer. Nature 2002, 417:949-954.
26. Pollock P.M., Harper U.L., Hansen K.S., Yudt L.M., Stark M., Robbins C.M., Moses T.Y., Hostetter G., Wagner U., Kakareka J., et al. High frequency of BRAF mutations in nevi. Nat Genet 2002, 33:19-20.
27. Brose M.S., Volpe P., Feldman M., Kumar M., Rishi I., Gerrero R., Einhorn E., Herlyn M., Minna J., Nicholson A., et al. BRAF and RAS mutations in human lung cancer and melanoma. Cancer Res 2002, 62:6997-7000.
28. Ceol C.J., Houvras Y., Jane-Valbuena J., Bilodeau S., Orlando D.A., Battisti V., Fritsch L., Lin W.M., Hollmann T.J., Ferré F., et al. The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 2011, 471:513-517.
29. Garraway L.A., Widlund H.R., Rubin M.A., Getz G., Berger A.J., Ramaswamy S., Beroukhim R., Milner D.A., Granter S.R., Du J., et al. Integrative genomic analyses identify MITF as a lineage survival oncogene amplified in malignant melanoma. Nature 2005, 436:117-122.
30. White R.M., Cech J., Ratanasirintrawoot S., Lin C.Y., Rahl P.B., Burke C.J., Langdon E., Tomlinson M.L., Mosher J., Kaufman C., et al. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 2011, 471:518-522.
31. Taylor K.L., Lister J.A., Zeng Z., Ishizaki H., Anderson C., Kelsh R.N., Jackson I.J., Patton E.E. Differentiated melanocyte cell division occurs in vivo and is promoted by mutations in Mitf. Development 2011, 138:3579-3589.
32. Lister J.A., Capper A., Zeng Z., Mathers M.E., Richardson J., Paranthaman K., Jackson I.J., Patton E.E. A conditional Zebrafish MITF mutation reveals MITF levels are critical for melanoma promotion versus regression in vivo. J Investig Dermatol 2013, 10.1038/jid.2013.293.
33. Ignatius M.S., Chen E., Elpek N.M., Fuller A.Z., Tenente I.M., Clagg R., Liu S., Blackburn J.S., Linardic C.M., Rosenberg A.E., et al. In vivo imaging of tumor-propagating cells, regional tumor heterogeneity, and dynamic cell movements in embryonal rhabdomyosarcoma. Cancer Cell 2012, 21:680-693.
34. Storer N.Y., White R.M., Uong A., Price E., Nielsen G.P., Langenau D.M., Zon L.I. Zebrafish rhabdomyosarcoma reflects the developmental stage of oncogene expression during myogenesis. Development 2013, 140:3040-3050.
35. Hettmer S., Liu J., Miller C.M., Lindsay M.C., Sparks C.A., Guertin D.A., Bronson R.T., Langenau D.M., Wagers A.J. Sarcomas induced in discrete subsets of prospectively isolated skeletal muscle cells. Proc Natl Acad Sci U S A 2011, 108:20002-20007.
36. Shive H.R., West R.R., Embree L.J., Azuma M., Sood R., Liu P., Hickstein D.D. brca2 in zebrafish ovarian development, spermatogenesis, and tumorigenesis. Proc Natl Acad Sci U S A 2010, 107:19350-19355.
37. Albacker C.E., Storer N.Y., Langdon E.M., DiBiase A., Zhou Y., Langenau D.M., Zon L.I. The histone methyltransferase SUV39H1 suppresses embryonal rhabdomyosarcoma formation in Zebrafish. PLoS ONE 2013, 8:e64969.
38. Le X., Pugach E.K., Hettmer S., Storer N.Y., Liu J., Wills A.A., DiBiase A., Chen E.Y., Ignatius M.S., Poss K.D., et al. A novel chemical screening strategy in zebrafish identifies common pathways in embryogenesis and rhabdomyosarcoma development. Development 2013, 140:2354-2364.
39. He S., Lamers G.E., Beenakker J.-W.M., Cui C., Ghotra V.P., Danen E.H., Meijer A.H., Spaink H.P., Snaar-Jagalska B.E. Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model. J Pathol 2012, 227:431-445.
40. White R., Rose K., Zon L. Zebrafish cancer: the state of the art and the path forward. Nature 2013, 13:624-636.
41. Liu S., Leach S.D. Zebrafish models for cancer. Annu Rev Pathol Mech Dis 2011, 6:71-93.
42. Chen E.Y., Langenau D.M. Zebrafish models of rhabdomyosarcoma. Methods in cell biology 2011, 383-402. Academic Press, New York, (Chapter 16). H. William Detrich, M. Westerfield, L.I. Zon (Eds.).
43. Mione M.C., Trede N.S. The zebrafish as a model for cancer. Dis Model Mech 2010, 3:517-523.
44. Park S.W., Davison J.M., Rhee J., Hruban R.H., Maitra A., Leach S.D. Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology 2008, 134:2080-2090.
45. Rudner L.A., Brown K.H., Dobrinski K.P., Bradley D.F., Garcia M.I., Smith A.C.H., Downie J.M., Meeker N.D., Look A.T., Downing J.R., et al. Shared acquired genomic changes in zebrafish and human T-ALL. Oncogene 2011, 30:4289-4296.
46. Zhang G., Hoersch S., Amsterdam A., Whittaker C.A., Beert E., Catchen J.M., Farrington S., Postlethwait J.H., Legius E., Hopkins N., et al. Comparative oncogenomic analysis of copy number alterations in human and zebrafish tumors enables cancer driver discovery. PLoS Genet 2013, 9:e1003734.
47. Howe K., Clark M.D., Torroja C.F., Torrance J., Berthelot C., Muffato M., Collins J.E., Humphray S., McLaren K., Matthews L., et al. The zebrafish reference genome sequence and its relationship to the human genome. Nature 2013, 496:498-503.
48. Brown K.H., Dobrinski K.P., Lee A.S., Gokcumen O., Mills R.E., Shi X., Chong W.W.S., Chen J.Y.H., Yoo P., David S., et al. Extensive genetic diversity and substructuring among zebrafish strains revealed through copy number variant analysis. Proc Natl Acad Sci U S A 2012, 109:529-534.
49. Bedell V.M., Wang Y., Campbell J.M., Poshusta T.L., Starker C.G., Krug R.G., Tan W., Penheiter S.G., Ma A.C., Leung A.Y.H., et al. In vivo genome editing using a high-efficiency TALEN system. Nature 2013, 490:114-118.
50. Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Tsai S.Q., Sander J.D., Peterson R.T., Yeh J-RJ, Joung J.K. Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 2013, 31:227-229.
51. Hwang W.Y., Fu Y., Reyon D., Maeder M.L., Kaini P., Sander J.D., Joung J.K., Peterson R.T., Yeh J.-R.J. Heritable and precise zebrafish genome editing using a CRISPR-Cas system. PLoS ONE 2013, 8:e68708.
52. Jao L.-E., Wente S.R., Chen W. Efficient multiplex biallelic zebrafish genome editing using a CRISPR nuclease system. Proc Natl Acad Sci U S A 2013, 110:13904-13909.
53. White R.M., Sessa A., Burke C., Bowman T., LeBlanc J., Ceol C., Bourque C., Dovey M., Goessling W., Burns C.E., et al. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2008, 2:183-189.
54. Kettleborough R.N.W., Busch-Nentwich E.M., Harvey S.A., Dooley C.M., de Bruijn E., van Eeden F., Sealy I., White R.J., Herd C., Nijman I.J., et al. A systematic genome-wide analysis of zebrafish protein-coding gene function. Nature 2014, 496:494-497.
55. Adatto I., Lawrence C., Thompson M., Zon L.I. A new system for the rapid collection of large numbers of developmentally staged zebrafish embryos. PLoS ONE 2011, 6:e21715.
56. Beckwith L.G., Moore J.L., Tsao-Wu G.S., Harshbarger J.C., Cheng K.C. Ethylnitrosourea induces neoplasia in zebrafish (Danio rerio). Lab Invest 2000, 80:379-385.
57. Goessling W., North T.E., Lord A.M., Ceol C., Lee S., Weidinger G., Bourque C., Strijbosch R., Haramis A.-P., Puder M. APC mutant zebrafish uncover a changing temporal requirement for wnt signaling in liver development. Dev Biol 2008, 320:161-174.
58. Amsterdam A., Burgess S., Golling G., Chen W., Sun Z., Townsend K., Farrington S., Haldi M., Hopkins N. A large-scale insertional mutagenesis screen in zebrafish. Genes Dev 1999, 13:2713-2724.
59. Amsterdam A., Sadler K.C., Lai K., Farrington S., Bronson R.T., Lees J.A., Hopkins N. Many ribosomal protein genes are cancer genes in zebrafish. PLoS Biol 2004, 2:e139.
60. Kawakami K., Shima A., Kawakami N. Identification of a functional transposase of the Tol2 element, an Ac-like element from the Japanese medaka fish, and its transposition in the zebrafish germ lineage. Proc Natl Acad Sci U S A 2000, 97:11403-11408.
61. Suster M.L., Kikuta H., Urasaki A., Asakawa K., Kawakami K. Transgenesis in zebrafish with the tol2 transposon system. Methods Mol Biol 2009, 561:41-63.
62. Kawakami K., Takeda H., Kawakami N., Kobayashi M., Matsuda N., Mishina M. A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 2004, 7:133-144.
63. Anelli V., Santoriello C., Distel M., Köster R., Ciccarelli F., Mione M. Global repression of cancer gene expression in a zebrafish model of melanoma is linked to epigenetic regulation. Zebrafish 2009, 6:417-424.
64. Birling M.-C., Gofflot F., Warot X. Site-specific recombinases for manipulation of the mouse genome. Methods Mol Biol 2009, 561:245-263.
65. Thummel R., Burket C.T., Brewer J.L., Sarras M.P.J., Li L., Perry M., McDermott J.P., Sauer B., Hyde D.R., Godwin A.R. Cre-mediated site-specific recombination in zebrafish embryos. Dev Dyn 2005, 233:1366-1377.
66. Langenau D.M., Feng H., Berghmans S., Kanki J.P., Kutok J.L., Look A.T. Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. Proc Natl Acad Sci U S A 2005, 102:6068-6073.
67. Feng H., Langenau D.M., Madge J.A., Quinkertz A., Gutierrez A., Neuberg D.S., Kanki J.P., Thomas Look A. Heat-shock induction of T-cell lymphoma/leukaemia in conditional Cre/lox-regulated transgenic zebrafish. B J Haematol 2007, 138:169-175.
68. Huang C.-J., Jou T.-S., Ho Y.-L., Lee W.-H., Jeng Y.-T., Hsieh F.-J., Tsai H.-J. Conditional expression of a myocardium-specific transgene in zebrafish transgenic lines. Dev Dyn 2005, 233:1294-1303.
69. Li Z., Huang X., Zhan H., Zeng Z., Li C., Spitsbergen J.M., Meierjohann S., Schartl M., Gong Z. Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J Hepatol 2012, 56:419-425.
70. Emelyanov A., Parinov S. Mifepristone-inducible LexPR system to drive and control gene expression in transgenic zebrafish. Dev Biol 2008, 320:113-121.
71. Huang P., Xiao A., Zhou M., Zhu Z., Lin S., Zhang B. Heritable gene targeting in zebrafish using customized TALENs. Nat Biotechnol 2011, 29:699-700.
72. Moore F.E., Reyon D., Sander J.D., Martinez S.A., Blackburn J.S., Khayter C., Ramirez C.L., Joung J.K., Langenau D.M. Improved somatic mutagenesis in zebrafish using transcription activator-like effector nucleases (TALENs). PLoS ONE 2012, 7:e37877.
73. Meng X., Noyes M.B., Zhu L.J., Lawson N.D., Wolfe S.A. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 2008, 26:695-701.
74. Doyon Y., McCammon J.M., Miller J.C., Faraji F., Ngo C., Katibah G.E., Amora R., Hocking T.D., Zhang L., Rebar E.J., et al. Heritable targeted gene disruption in zebrafish using designed zinc-finger nucleases. Nat Biotechnol 2008, 26:702-708.
75. Sood R., Carrington B., Bishop K., Jones M., Rissone A., Candotti F., Chandrasekharappa S.C., Liu P. Efficient methods for targeted mutagenesis in zebrafish using zinc-finger nucleases: data from targeting of nine genes using CompoZr or CoDA ZFNs. PLoS ONE 2013, 8:e57239.
76. Yen J., White R.M., Wedge D.C., Van Loo P., de Ridder J., Capper A., Richardson J., Jones D., Raine K., Watson I.R., et al. The genetic heterogeneity and mutational burden of engineered melanomas in zebrafish models. Genome Biology 2013, 14:R113.