1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Cancer Biology
  4. Volume 5, 2021
  5. Article

Annual Review of Cancer Biology

Volume 5, 2021

Reeling in the Zebrafish Cancer Models

Abstract

Zebrafish are rapidly becoming a leading model organism for cancer research. The genetic pathways driving cancer are highly conserved between zebrafish and humans, and the ability to easily manipulate the zebrafish genome to rapidly generate transgenic animals makes zebrafish an excellent model organism. Transgenic zebrafish containing complex, patient-relevant genotypes have been used to model many cancer types. Here we present a comprehensive review of transgenic zebrafish cancer models as a resource to the field and highlight important areas of cancer biology that have yet to be studied in the fish. The ability to image cancer cells and niche biology in an endogenous tumor makes zebrafish an indispensable model organism in which we can further understand the mechanisms that drive tumorigenesis and screen for potential new cancer therapies.

Keyword(s): cancer, genetics, modeling, transgenic, tumor, zebrafish
Loading

Article metrics loading...

/content/journals/10.1146/annurev-cancerbio-051320-014135
2021-03-04
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/cancerbio/5/1/annurev-cancerbio-051320-014135.html?itemId=/content/journals/10.1146/annurev-cancerbio-051320-014135&mimeType=html&fmt=ahah

Literature Cited

  1. Ablain J, Durand EM, Yang S, Zhou Y, Zon LI 2015. A CRISPR/Cas9 vector system for tissue-specific gene disruption in zebrafish. Dev. Cell 32:6756–64
     [Google Scholar]
  2. Ablain J, Xu M, Rothschild H, Jordan RC, Mito JK et al. 2018. Human tumor genomics and zebrafish modeling identify SPRED1 loss as a driver of mucosal melanoma. Science 362:64181055–60
     [Google Scholar]
  3. Ablain J, Zon LI. 2016. Tissue-specific gene targeting using CRISPR/Cas9. Methods Cell Biol 135:189–202
     [Google Scholar]
  4. ACS (Am. Cancer Soc.) 2020. Cancer facts and figures 2020 Tech. Rep., Am. Cancer Soc Atlanta, GA:
  5. Alghisi E, Distel M, Malagola M, Anelli V, Santoriello C et al. 2013. Targeting oncogene expression to endothelial cells induces proliferation of the myelo-erythroid lineage by repressing the Notch pathway. Leukemia 27:2229–41
     [Google Scholar]
  6. Amsterdam A, Sadler KC, Lai K, Farrington S, Bronson RT et al. 2004. Many ribosomal protein genes are cancer genes in zebrafish. PLOS Biol 2:5e139
     [Google Scholar]
  7. Anelli V, Villefranc JA, Chhangawala S, Martinez-McFaline R, Riva E et al. 2017. Oncogenic BRAF disrupts thyroid morphogenesis and function via twist expression. eLife 6:e20728
     [Google Scholar]
  8. Basten SG, Davis EE, Gillis AJM, van Rooijen E, Stoop H et al. 2013. Mutations in LRRC50 predispose zebrafish and humans to seminomas. PLOS Genet 9:4e1003384
     [Google Scholar]
  9. Blackburn JS, Liu S, Raiser DM, Martinez SA, Feng H et al. 2012. Notch signaling expands a pre-malignant pool of T-cell acute lymphoblastic leukemia clones without affecting leukemia-propagating cell frequency. Leukemia 26:2069–78
     [Google Scholar]
  10. Blackburn JS, Liu S, Wilder JL, Dobrinski KP, Lobbardi R et al. 2014. Clonal evolution enhances leukemia-propagating cell frequency in T cell acute lymphoblastic leukemia through Akt/mTORC1 pathway activation. Cancer Cell 25:366–78
     [Google Scholar]
  11. Borga C, Park G, Foster C, Burroughs-Garcia J, Marchesin M et al. 2019. Simultaneous B and T cell acute lymphoblastic leukemias in zebrafish driven by transgenic MYC: implications for oncogenesis and lymphopoiesis. Leukemia 33:333–47
     [Google Scholar]
  12. Callahan SJ, Tepan S, Zhang YM, Lindsay H, Burger A et al. 2018. Cancer modeling by transgene electroporation in adult zebrafish (TEAZ). Dis. Model. Mech. 11:9dmm034561
     [Google Scholar]
  13. Ceol CJ, Houvras Y, Jane-Valbuena J, Bilodeau S, Orlando DA et al. 2011. The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471:7339513–18
     [Google Scholar]
  14. Chaturantabut S, Shwartz A, Evason KJ, Cox AG, Labella K et al. 2019. Estrogen activation of G-protein-coupled estrogen receptor 1 regulates phosphoinositide 3-kinase and mTOR signaling to promote liver growth in zebrafish and proliferation of human hepatocytes. Gastroenterology 156:61788–804.e13
     [Google Scholar]
  15. Chen EY, DeRan MT, Ignatius MS, Grandinetti KB, Clagg R et al. 2014. Glycogen synthase kinase 3 inhibitors induce the canonical WNT/β-catenin pathway to suppress growth and self-renewal in embryonal rhabdomyosarcoma. PNAS 111:145349–54
     [Google Scholar]
  16. Chen J, Jette C, Kanki JP, Aster JC, Look AT, Griffin JD 2007. NOTCH1-induced T-cell leukemia in transgenic zebrafish. Leukemia 21:462–71
     [Google Scholar]
  17. Chu CY, Chen CF, Rajendran RS, Shen CN, Chen TH et al. 2012. Overexpression of Akt1 enhances adipogenesis and leads to lipoma formation in zebrafish. PLOS ONE 7:5e36474
     [Google Scholar]
  18. Ciarlo C, Kaufman CK, Kinikoglu B, Michael J, Yang S et al. 2017. A chemical screen in zebrafish embryonic cells establishes that Akt activation is required for neural crest development. eLife 6:e29145
     [Google Scholar]
  19. Dang M, Henderson RE, Garraway LA, Zon LI 2016. Long-term drug administration in the adult zebrafish using oral gavage for cancer preclinical studies. Dis. Model. Mech. 9:7811–20
     [Google Scholar]
  20. Deveau AP, Forrester AM, Coombs AJ, Wagner GS, Grabher C et al. 2015. Epigenetic therapy restores normal hematopoiesis in a zebrafish model of NUP98–HOXA9-induced myeloid disease. Leukemia 29:2086–97
     [Google Scholar]
  21. Dovey M, White RM, Zon LI 2009. Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 6:4397–404
     [Google Scholar]
  22. Drummond IA, Davidson AJ. 2010. Zebrafish kidney development. Methods in Cell Biology, Vol. 100 HW Detrich 3rd, M Westerfield, LI Zon 233–60 Burlington, MA: Academic
     [Google Scholar]
  23. Durinck K, Goossens S, Peirs S, Wallaert A, Van Loocke W et al. 2015. Novel biological insights in T-cell acute lymphoblastic leukemia. Exp. Hematol. 43:625–39
     [Google Scholar]
  24. Evason KJ, Francisco MT, Juric V, Balakrishnan S, del Pilar Lopez Pazmino M et al. 2015. Identification of chemical inhibitors of β-catenin-driven liver tumorigenesis in zebrafish. PLOS Genet 11:7e1005305
     [Google Scholar]
  25. Feng H, Langenau DM, Madge JA, Quinkertz A, Gutierrez A et al. 2007. Heat-shock induction of T-cell lymphoma/leukaemia in conditional Cre/lox-regulated transgenic zebrafish. Br. J. Haematol. 138:2169–75
     [Google Scholar]
  26. Feng H, Stachura DL, White RM, Gutierrez A, Zhang L et al. 2010. T-lymphoblastic lymphoma cells express high levels of BCL2, S1P1, and ICAM1, leading to a blockade of tumor cell intravasation. Cancer Cell 18:353–66
     [Google Scholar]
  27. Ferrara F, Schiffer CA. 2013. Acute myeloid leukaemia in adults. Lancet 381:9865484–95
     [Google Scholar]
  28. Forrester AM, Grabher C, McBride ER, Boyd ER, Vigerstad MH et al. 2011. NUP98-HOXA9-transgenic zebrafish develop a myeloproliferative neoplasm and provide new insight into mechanisms of myeloid leukaemogenesis. Br. J. Haematol. 155:2167–81
     [Google Scholar]
  29. Garcia EG, Iyer S, Garcia SP, Loontiens S, Sadreyev RI et al. 2018. Cell of origin dictates aggression and stem cell number in acute lymphoblastic leukemia. Leukemia 32:1860–65
     [Google Scholar]
  30. Gill JA, Lowe L, Nguyen J, Liu PP, Blake T et al. 2010. Enforced expression of simian virus 40 large T-antigen leads to testicular germ cell tumors in zebrafish. Zebrafish 7:4333–41
     [Google Scholar]
  31. Gjini E, Chang-Bin J, Nguyen AT, Reyon D, Gans E et al. 2019. Disruption of asxl1 results in myeloproliferative neoplasms in zebrafish. Dis. Model. Mech. 12:5dmm035790
     [Google Scholar]
  32. Gutierrez A, Feng H, Stevenson K, Neuberg DS, Calzada O et al. 2014a. Loss of function tp53 mutations do not accelerate the onset of myc-induced T-ALL in the zebrafish. Br. J. Haematol. 166:184–90
     [Google Scholar]
  33. Gutierrez A, Grebliunaite R, Feng H, Kozakewich E, Zhu S et al. 2011a. Pten mediates Myc oncogene dependence in a conditional zebrafish model of T cell acute lymphoblastic leukemia. J. Exp. Med. 208:81595–603
     [Google Scholar]
  34. Gutierrez A, Look AT, Aster JC 2014b. Phenothiazines induce PP2A-mediated apoptosis in T cell acute lymphoblastic leukemia. J. Clin. Investig. 124:2644–55
     [Google Scholar]
  35. Gutierrez A, Snyder EL, Marino-Enriquez A, Zhang YX, Sioletic S et al. 2011b. Aberrant AKT activation drives well-differentiated liposarcoma. PNAS 108:3916386–91
     [Google Scholar]
  36. Haramis APG, Hurlstone A, van der Velden Y, Begthel H, van den Born M et al. 2006. Adenomatous polyposis coli-deficient zebrafish are susceptible to digestive tract neoplasia. EMBO Rep 7:4444–49
     [Google Scholar]
  37. Hayes MN, Langenau DM. 2017. Discovering novel oncogenic pathways and new therapies using zebrafish models of sarcoma. Methods in Cell Biology, Vol. 138 HW Detrich 3rd, M Westerfield, LI Zon 525–61 Burlington, MA: Academic
     [Google Scholar]
  38. Hayes MN, McCarthy K, Jin A, Oliveira ML, Iyer S et al. 2018. Vangl2/RhoA signaling pathway regulates stem cell self-renewal programs and growth in rhabdomyosarcoma. Cell Stem Cell 22:3414–27.e6
     [Google Scholar]
  39. He S, Mansour MR, Zimmerman MW, Ki DH, Layden HM et al. 2016. Synergy between loss of NF1 and overexpression of MYCN in neuroblastoma is mediated by the GAP-related domain. eLife 5:e14713
     [Google Scholar]
  40. Heilmann S, Ratnakumar K, Langdon E, Kansler E, Kim I et al. 2015. A quantitative system for studying metastasis using transparent zebrafish. Cancer Res 75:204272–82
     [Google Scholar]
  41. Hong WY, Kutok JL, Nam HL, Hui YP, Fletcher CDM et al. 2004. Targeted expression of human MYCN selectively causes pancreatic neuroendocrine tumors in transgenic zebrafish. Cancer Res 64:207256–62
     [Google Scholar]
  42. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C et al. 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503
     [Google Scholar]
  43. Huang SJ, Cheng CL, Chen JR, Gong HY, Liu W, Wu JL 2017. Inducible liver-specific overexpression of gankyrin in zebrafish results in spontaneous intrahepatic cholangiocarcinoma and hepatocellular carcinoma formation. Biochem. Biophys. Res. Commun. 490:31052–58
     [Google Scholar]
  44. Ignatius MS, Chen E, Elpek NM, Fuller AZ, Tenente IM et al. 2012. In vivo imaging of tumor-propagating cells, regional tumor heterogeneity, and dynamic cell movements in embryonal rhabdomyosarcoma. Cancer Cell 21:5680–93
     [Google Scholar]
  45. Ignatius MS, Hayes MN, Lobbardi R, Chen EY, McCarthy KM et al. 2017. The NOTCH1/SNAIL1/MEF2C pathway regulates growth and self-renewal in embryonal rhabdomyosarcoma. Cell Rep 19:112304–18
     [Google Scholar]
  46. Ignatius MS, Hayes MN, Moore FE, Tang Q, Garcia SP et al. 2018. tp53 deficiency causes a wide tumor spectrum and increases embryonal rhabdomyosarcoma metastasis in zebrafish. eLife 7:e37202
     [Google Scholar]
  47. Ju B, Chen W, Orr BA, Spitsbergen JM, Jia S et al. 2015. Oncogenic KRAS promotes malignant brain tumors in zebrafish. Mol. Cancer 14:18
     [Google Scholar]
  48. Jung IH, Leem GL, Jung DE, Kim MH, Kim EY et al. 2013. Glioma is formed by active Akt1 alone and promoted by active Rac1 in transgenic zebrafish. Neuro-Oncology 15:3290–304
     [Google Scholar]
  49. Kalev-Zylinska ML, Horsfield JA, Flores MVC, Postlethwait JH, Vitas MR et al. 2002. Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1-CBF2T1 transgene advances a model for studies of leukemogenesis. Development 129:2015–30
     [Google Scholar]
  50. Kaufman CK, Mosimann C, Fan ZP, Yang S, Thomas A et al. 2016. A zebrafish melanoma model reveals emergence of neural crest identity during melanoma initiation. Science 351:6272aad2197
     [Google Scholar]
  51. Kendall GC, Watson S, Xu L, Lavigne CA, Murchison W et al. 2018. PAX3-FOXO1 transgenic zebrafish models identify HES3 as a mediator of rhabdomyosarcoma tumorigenesis. eLife 7:e33800
     [Google Scholar]
  52. Ki DH, He S, Rodig S, Look AT 2017. Overexpression of PDGFRA cooperates with loss of NF1 and p53 to accelerate the molecular pathogenesis of malignant peripheral nerve sheath tumors. Oncogene 36:81058–68
     [Google Scholar]
  53. Kinkel MD, Eames SC, Philipson LH, Prince VE 2010. Intraperitoneal injection into adult zebrafish. J. Vis. Exp. 42:2126
     [Google Scholar]
  54. Langenau DM, Feng H, Berghmans S, Kanki JP, Kutok JL, Look AT 2005. Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. PNAS 102:176068–73
     [Google Scholar]
  55. Langenau DM, Keefe MD, Storer NY, Guyon JR, Kutok JL et al. 2007. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev 21:111382–95
     [Google Scholar]
  56. Langenau DM, Traver D, Ferrando AA, Kutok JL 2003. Myc-induced T cell leukemia in transgenic zebrafish. Science 299:5608887–90
     [Google Scholar]
  57. Le X, Langenau DM, Keefe MD, Kutok JL, Neuberg DS, Zon LI 2007. Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish. PNAS 104:229410–15
     [Google Scholar]
  58. Le X, Pugach EK, Hettmer S, Storer NY, Liu J et al. 2013. A novel chemical screening strategy in zebrafish identifies common pathways in embryogenesis and rhabdomyosarcoma development. Development 140:112354–64
     [Google Scholar]
  59. Leacock SW, Basse AN, Chandler GL, Kirk AM, Rakheja D, Amatruda JF 2012. A zebrafish transgenic model of Ewing's sarcoma reveals conserved mediators of EWS-FLI1 tumorigenesis. Dis. Model. Mech. 5:95–106
     [Google Scholar]
  60. Lee E, Wei Y, Zou Z, Tucker K, Rakheja D et al. 2016. Genetic inhibition of autophagy promotes p53 loss-of-heterozygosity and tumorigenesis. Oncotarget 7:4267919–33
     [Google Scholar]
  61. Lewis RS, Stephenson SEM, Ward AC 2006. Constitutive activation of zebrafish Stat5 expands hematopoietic cell populations in vivo. Exp. Hematol. 34:179–87
     [Google Scholar]
  62. Li H, Lu JW, Huo X, Li Y, Li Z, Gong Z 2019. Effects of sex hormones on liver tumor progression and regression in Myc/xmrk double oncogene transgenic zebrafish. Gen. Comp. Endocrinol. 277:112–21
     [Google Scholar]
  63. Li Z, Huang X, Zhan H, Zeng Z, Li C et al. 2012. Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J. Hepatol. 56:2419–25
     [Google Scholar]
  64. Li Z, Zheng W, Wang Z, Zeng Z, Zhan H et al. 2013. A transgenic zebrafish liver tumor model with inducible Myc expression reveals conserved Myc signatures with mammalian liver tumors. Dis. Model. Mech. 6:2414–23
     [Google Scholar]
  65. Lister JA, Robertson PC, Lepage T, Johnson SL, Raible DW 1999. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757–67
     [Google Scholar]
  66. Litchfield K, Levy M, Dudakia D, Proszek P, Shipley C et al. 2016. Rare disruptive mutations in ciliary function genes contribute to testicular cancer susceptibility. Nat. Commun. 7:13840
     [Google Scholar]
  67. Lo J, Fisher DE. 2014. The melanoma revolution: from UV carcinogenesis to a new era in therapeutics. Science 346:6212945–49
     [Google Scholar]
  68. Lobbardi R, Pinder J, Martinez-Pastor B, Theodorou M, Blackburn JS et al. 2017. TOX regulates growth, DNA repair, and genomic instability in T-cell acute lymphoblastic leukemia. Cancer Discov 7:111336–53
     [Google Scholar]
  69. Lu J, Hou H, Hsieh M, Tien H, Lin L 2016. Overexpression of FLT3-ITD driven by spi-1 results in expanded myelopoiesis with leukemic phenotype in zebrafish. Leukemia 30:2098–101
     [Google Scholar]
  70. Lutterbach B, Hiebert SW. 2000. Role of the transcription factor AML-1 in acute leukemia and hematopoietic differentiation. Blood 106:51519–24
     [Google Scholar]
  71. Maher ER, Kaelin WG. 1997. von Hippel-Lindau disease. Medicine 76:381–91
     [Google Scholar]
  72. Martins Metelo A, Noonan HR, Li X, Jin Y, Baker R et al. 2015. Pharmacological HIF2a inhibition improves VHL disease-associated phenotypes in zebrafish model. J. Clin. Investig. 125:51987–97
     [Google Scholar]
  73. Mayrhofer M, Gourain V, Reischl M, Affaticati P, Jenett A et al. 2017. A novel brain tumour model in zebrafish reveals the role of YAP activation in MAPK- and PI3K-induced malignant growth. Dis. Model. Mech. 10:15–28
     [Google Scholar]
  74. McConnell AM, Mito JK, Ablain J, Dang M, Formichella L et al. 2019. Neural crest state activation in NRAS driven melanoma, but not in NRAS-driven melanocyte expansion. Dev. Biol. 449:107–13
     [Google Scholar]
  75. Modzelewska K, Boer EF, Mosbruger TL, Picard D, Anderson D et al. 2016. MEK inhibitors reverse growth of embryonal brain tumors derived from oligoneural precursor cells. Cell Rep 17:51255–64
     [Google Scholar]
  76. Molinaro AM, Taylor JW, Wiencke JK, Wrensch MR 2019. Genetic and molecular epidemiology of adult diffuse glioma. Nat. Rev. Neurol. 15:7405–17
     [Google Scholar]
  77. Morita K, He S, Nowak RP, Wang J, Zimmerman MW et al. 2020. Allosteric activators of protein phosphatase 2A display broad antitumor activity mediated by dephosphorylation of MYBL2. Cell 181:702–15.e20
     [Google Scholar]
  78. Mort RL, Jackson IJ, Patton EE 2015. The melanocyte lineage in development and disease. Development 142:4620–32
     [Google Scholar]
  79. Neumann JC, Chandler GL, Damoulis VA, Fustinoa NJ, Lillard K et al. 2011. Mutation in the type IB bone morphogenetic protein receptor alk6b impairs germ-cell differentiation and causes germ-cell tumors in zebrafish. PNAS 108:3213153–58
     [Google Scholar]
  80. Neumann JC, Dovey JS, Chandler GL, Carbajal L, Amatruda JF 2009. Identification of a heritable model of testicular germ cell tumor in the zebrafish. Zebrafish 6:4319–27
     [Google Scholar]
  81. Nguyen AT, Emelyanov A, Koh CHV, Spitsbergen JM, Lam SH et al. 2011. A high level of liver-specific expression of oncogenic KrasV12 drives robust liver tumorigenesis in transgenic zebrafish. Dis. Model. Mech. 4:6801–13
     [Google Scholar]
  82. Nguyen AT, Emelyanov A, Koh CHV, Spitsbergen JM, Parinov S, Gong Z 2012. An inducible krasV12 transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis. Model. Mech. 5:63–72
     [Google Scholar]
  83. Nguyen AT, Koh V, Spitsbergen JM, Gong Z 2016. Development of a conditional liver tumor model by mifepristone-inducible Cre recombination to control oncogenic krasV12 expression in transgenic zebrafish. Sci. Rep. 6:19559
     [Google Scholar]
  84. Noonan HR, Metelo AM, Kamei CN, Peterson RT, Drummond IA, Iliopoulos O 2016. Loss of vhl in the zebrafish pronephros recapitulates early stages of human clear cell renal cell carcinoma. Dis. Model. Mech. 9:8873–84
     [Google Scholar]
  85. Oh S, Park JT. 2019. Zebrafish model of KRAS-initiated pancreatic endocrine tumor. Anim. Cells Syst. 23:3209–18
     [Google Scholar]
  86. Oppel F, Tao T, Shi H, Ross KN, Zimmerman MW et al. 2019. Loss of atrx cooperates with p53-deficiency to promote the development of sarcomas and other malignancies. PLOS Genet 15:4e1008039
     [Google Scholar]
  87. Park H, Galbraith R, Turner T, Mehojah J, Azuma M 2016. Loss of Ewing sarcoma EWS allele promotes tumorigenesis by inducing chromosomal instability in zebrafish. Sci. Rep. 6:32297
     [Google Scholar]
  88. Park JT, Johnson N, Liu S, Levesque M, Wang YJ et al. 2015. Differential in vivo tumorigenicity of diverse KRAS mutations in vertebrate pancreas: a comprehensive survey. Oncogene 34:212801–6
     [Google Scholar]
  89. Park SW, Davison JM, Rhee J, Hruban RH, Maitra A, Leach SD 2008. Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology 134:72080–90
     [Google Scholar]
  90. Patton EE, Widlund HR, Kutok JL, Kopani KR, Amatruda JF et al. 2005. BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr. Biol. 15:3249–54
     [Google Scholar]
  91. Provost E, Bailey JM, Aldrugh S, Liu S, Iacobuzio-Donahue C, Leach SD 2014. The tumor suppressor rpl36 restrains KRASG12V-induced pancreatic cancer. Zebrafish 11:6551–59
     [Google Scholar]
  92. Pugach EK, Li P, White R, Zon L 2009. Retro-orbital injection in adult zebrafish. J. Vis. Exp. 34:1645
     [Google Scholar]
  93. Rekha RD, Amali AA, Her GM, Yeh YH, Gong HY et al. 2008. Thioacetamide accelerates steatohepatitis, cirrhosis and HCC by expressing HCV core protein in transgenic zebrafish Danio rerio. . Toxicology 243:1–211–22
     [Google Scholar]
  94. Reynolds C, Roderick JE, Labelle JL, Bird G, Mathieu R et al. 2014. Repression of BIM mediates survival signaling by MYC and AKT in high-risk T-cell acute lymphoblastic leukemia. Leukemia 28:1819–27
     [Google Scholar]
  95. Ridges S, Heaton WL, Joshi D, Choi H, Eiring A et al. 2012. Zebrafish screen identifies novel compound with selective toxicity against leukemia. Blood 119:245621–31
     [Google Scholar]
  96. Robertson AL, Avagyan S, Gansner JM, Zon LI 2016. Understanding the regulation of vertebrate hematopoiesis and blood disorders: big lessons from a small fish. FEBS Lett 590:224016–33
     [Google Scholar]
  97. Rudner L, Brown K, Dobrinski K, Bradley D, Garcia M et al. 2011. Shared acquired genomic changes in zebrafish and human T-ALL. Oncogene 30:4289–96
     [Google Scholar]
  98. Sabaawy HE, Azuma M, Embree LJ, Tsai H-J, Starost MF, Hickstein DD 2006. TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. PNAS 103:4115166–71
     [Google Scholar]
  99. Sanchez A, Amatruda JF. 2016. Zebrafish germ cell tumors. Adv. Exp. Med. Biol. 916:479–94
     [Google Scholar]
  100. Sanchez A, Xu L, Pierce JL, Lafin JT, Abe D et al. 2019. Identification of testicular cancer driver genes by a cross-species comparative oncology approach. Andrology 7:545–54
     [Google Scholar]
  101. Santhakumar K, Judson EC, Elks PM, McKee S, Elworthy S et al. 2012. A zebrafish model to study and therapeutically manipulate hypoxia signaling in tumorigenesis. Cancer Res 72:164017–27
     [Google Scholar]
  102. Santoriello C, Gennaro E, Anelli V, Distel M, Kelly A et al. 2010. Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLOS ONE 5:12e15170
     [Google Scholar]
  103. Santoriello C, Sporrij A, Yang S, Flynn RA, Henriques T et al. 2020. RNA helicase DDX21 mediates nucleotide stress responses in neural crest and melanoma cells. Nat. Cell Biol. 22:372–79
     [Google Scholar]
  104. Shen L-J, Chen F-Y, Zhang Y, Cao L-F, Kuang Y et al. 2013. MYCN transgenic zebrafish model with the characterization of acute myeloid leukemia and altered hematopoiesis. PLOS ONE 8:3e59070
     [Google Scholar]
  105. Shi X, He B-L, Ma ACH, Guo Y, Chi Y et al. 2015. Functions of idh1 and its mutation in the regulation of developmental hematopoiesis in zebrafish. Blood 125:192974–84
     [Google Scholar]
  106. Shimizu N, Matsuda M. 2019. Identification of a novel zebrafish mutant line that develops testicular germ cell tumors. Zebrafish 16:115–28
     [Google Scholar]
  107. Shin J, Padmanabhan A, de Groh ED, Lee J-S, Haidar S et al. 2012. Zebrafish neurofibromatosis type 1 genes have redundant functions in tumorigenesis and embryonic development. Dis. Model. Mech. 5:6881–94
     [Google Scholar]
  108. Shive HR, West RR, Embree LJ, Golden CD, Hickstein DD 2014. brca2 and tp53 collaborate in tumorigenesis in zebrafish. PLOS ONE 9:1e87177
     [Google Scholar]
  109. Storer NY, White RM, Uong A, Price E, Nielsen GP et al. 2013. Zebrafish rhabdomyosarcoma reflects the developmental stage of oncogene expression during myogenesis. Development 140:143040–50
     [Google Scholar]
  110. Tao T, Sondalle SB, Shi H, Zhu S, Perez-Atayde AR et al. 2017. The pre-rRNA processing factor DEF is rate limiting for the pathogenesis of MYCN-driven neuroblastoma. Oncogene 36:273852–67
     [Google Scholar]
  111. TCGA (Cancer Genome Atlas Res. Netw.) 2013. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499:43–49
     [Google Scholar]
  112. TCGA (Cancer Genome Atlas Res. Netw.) 2015. Genomic classification of cutaneous melanoma. Cell 161:71681–96
     [Google Scholar]
  113. Tenente IM, Hayes MN, Ignatius MS, McCarthy K, Yohe M et al. 2017. Myogenic regulatory transcription factors regulate growth in rhabdomyosarcoma. eLife 6:e19214
     [Google Scholar]
  114. Tregnago C, Manara E, Zampini M, Bisio V, Borga C et al. 2016. CREB engages C/EBPδ to initiate leukemogenesis. Leukemia 30:1887–96
     [Google Scholar]
  115. Van Rooijen E, Voest EE, Logister I, Bussmann J, Korving J et al. 2010. von Hippel-Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish. Dis. Model. Mech. 3:343–53
     [Google Scholar]
  116. Van Rooijen E, Voest EE, Logister I, Korving J, Schwerte T et al. 2009. Zebrafish mutants in the von Hippel-Lindau tumor suppressor display a hypoxic response and recapitulate key aspects of Chuvash polycythemia. Blood 113:256449–60
     [Google Scholar]
  117. Venkatesan AM, Vyas R, Gramann AK, Dresser K, Gujja S et al. 2018. Ligand-activated BMP signaling inhibits cell differentiation and death to promote melanoma. J. Clin. Investig. 128:1294–308
     [Google Scholar]
  118. Wang J, Leng X, Wang G, Wan X, Cao H 2017. The construction of intrahepatic cholangiocarcinoma model in zebrafish. Sci. Rep. 7:13419
     [Google Scholar]
  119. White LA, Sexton JM, Shive HR 2017. Histologic and immunohistochemical analyses of soft tissue sarcomas from brca2-mutant/tp53-mutant zebrafish are consistent with neural crest (Schwann cell) origin. Vet. Pathol. 54:2320–27
     [Google Scholar]
  120. White R, Rose K, Zon L 2013. Zebrafish cancer: the state of the art and the path forward. Nat. Rev. Cancer 13:9624–36
     [Google Scholar]
  121. White RM, Cech J, Ratanasirintrawoot S, Lin CY, Rahl PB et al. 2011. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 471:7339518–22
     [Google Scholar]
  122. Wrighton PJ, Oderberg IM, Goessling W 2019. There is something fishy about liver cancer: zebrafish models of hepatocellular carcinoma. Cell. Mol. Gastroenterol. Hepatol. 8:3347–63
     [Google Scholar]
  123. Xu M, Ye Y, Ye Z, Xu S, Liu W et al. 2020. Human BCR/ABL1 induces chronic myeloid leukemia-like disease in zebrafish. Haematologica 105:3674–86
     [Google Scholar]
  124. Yan C, Huo X, Wang S, Feng Y, Gong Z 2015. Stimulation of hepatocarcinogenesis by neutrophils upon induction of oncogenic kras expression in transgenic zebrafish. J. Hepatol. 63:2420–28
     [Google Scholar]
  125. Yan C, Yang Q, Huo X, Li H, Zhou L, Gong Z 2017. Chemical inhibition reveals differential requirements of signaling pathways in krasV12- and Myc-induced liver tumors in transgenic zebrafish. Sci. Rep. 7:45796
     [Google Scholar]
  126. Yang Q, Yan C, Gong Z 2018. Interaction of hepatic stellate cells with neutrophils and macrophages in the liver following oncogenic kras activation in transgenic zebrafish. Sci. Rep. 8:8495
     [Google Scholar]
  127. Yeh J-RJ, Munson KM, Chao YL, Peterson QP, MacRae CA, Peterson RT 2008. AML1-ETO reprograms hematopoietic cell fate by downregulating scl expression. Development 135:401–10
     [Google Scholar]
  128. Zhang GJ, Hoersch S, Amsterdam A, Whittaker CA, Beert E et al. 2013. Comparative oncogenomic analysis of copy number alterations in human and zebrafish tumors enables cancer driver discovery. PLOS Genet 9:8e1003734
     [Google Scholar]
  129. Zhang GJ, Hoersch S, Amsterdam A, Whittaker CA, Lees JA, Hopkins N 2010. Highly aneuploid zebrafish malignant peripheral nerve sheath tumors have genetic alterations similar to human cancers. PNAS 107:3916940–45
     [Google Scholar]
  130. Zhang M, Di Martino JS, Bowman RL, Campbell NR, Baksh SC et al. 2018. Adipocyte-derived lipids mediate melanoma progression via FATP proteins. Cancer Discov 8:81006–25
     [Google Scholar]
  131. Zhang X, Dong Z, Zhang C, Ung CY, He S et al. 2017. Critical role for GAB2 in neuroblastoma pathogenesis through the promotion of SHP2/MYCN cooperation. Cell Rep 18:122932–42
     [Google Scholar]
  132. Zhao F, Shi Y, Huang Y, Zhan Y, Zhou L et al. 2018. Irf8 regulates the progression of myeloproliferative neoplasm-like syndrome via Mertk signaling in zebrafish. Leukemia 32:149–58
     [Google Scholar]
  133. Zhao Y, Huang X, Ding TW, Gong Z 2016. Enhanced angiogenesis, hypoxia and neutrophil recruitment during Myc-induced liver tumorigenesis in zebrafish. Sci. Rep. 6:31952
     [Google Scholar]
  134. Zheng W, Li Z, Nguyen AT, Li C, Emelyanov A, Gong Z 2014. Xmrk, Kras and Myc transgenic zebrafish liver cancer models share molecular signatures with subsets of human hepatocellular carcinoma. PLOS ONE 9:3e91179
     [Google Scholar]
  135. Zhu S, Lee JS, Guo F, Shin J, Perez-Atayde AR et al. 2012. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell 21:3362–73
     [Google Scholar]
  136. Zhu S, Zhang X, Weichert-Leahey N, Dong Z, Zhang C et al. 2017. LMO1 synergizes with MYCN to promote neuroblastoma initiation and metastasis. Cancer Cell 32:3310–23.e5
     [Google Scholar]
  137. Zhuravleva J, Paggetti J, Martin L, Hammann A, Solary E et al. 2008. MOZ/TIF2-induced acute myeloid leukaemia in transgenic fish. Br. J. Haematol. 143:3378–82
     [Google Scholar]
  138. Zimmerman MW, Liu Y, He S, Durbin AD, Abraham BJ et al. 2018. MYC drives a subset of high-risk pediatric neuroblastomas and is activated through mechanisms including enhancer hijacking and focal enhancer amplification. Cancer Discov 8:3320–35
     [Google Scholar]
/content/journals/10.1146/annurev-cancerbio-051320-014135
Loading
Reeling in the Zebrafish Cancer Models
Annual Review of Cancer Biology 5, 331 (2021); https://doi.org/10.1146/annurev-cancerbio-051320-014135
/content/journals/10.1146/annurev-cancerbio-051320-014135
/content/journals/10.1146/annurev-cancerbio-051320-014135
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error