Liver tumor models in transgenic zebrafish: An alternative in vivo approach to study hepatocarcinogenes

Future Oncology

Volumn 8, Issue 1, 2012, Pages 21-28

  Huang, Xiaoqian ^a   Zhou, Li ^a   Gong, Zhiyuan ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

anticancer drug; drug screening; HCC; hepatocellular carcinoma; mifepristone; Tet On; tetracycline; transgenic; zebrafish

Indexed keywords

GREEN FLUORESCENT PROTEIN;

ARTICLE; DRUG SCREENING; IN VIVO STUDY; LIVER TUMOR; NONHUMAN; PRIORITY JOURNAL; TRANSGENIC ANIMAL; TUMOR MODEL; ZEBRA FISH;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; ANTINEOPLASTIC AGENTS; CELL TRANSFORMATION, NEOPLASTIC; DISEASE MODELS, ANIMAL; DRUG SCREENING ASSAYS, ANTITUMOR; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ENGINEERING; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIVER NEOPLASMS, EXPERIMENTAL; ZEBRAFISH;

EID: 83655196930     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.2217/fon.11.137     Document Type: Article

References (63)

1. Hawkins WE, Overstreet RM, Fournie JW, Walker WW. Development of aquarium fish models for environmental carcinogenesis: tumor induction in seven species. J. Appl. Toxicol. 5(4), 261-264 (1985). (Pubitemid 15233810)
2. Spitsbergen JM, Kent ML. The state of the art of the zebrafish model for toxicology and toxicologic pathology research - advantages and current limitations. Toxicol. Pathol. 31(Suppl.), 62-87 (2003). (Pubitemid 36169407)
3. Spitsbergen JM, Tsai HW, Reddy A et al. Neoplasia in zebrafish (Danio rerio) treated with N-methyl-N'-nitro-N-nitrosoguanidine by three exposure routes at different developmental stages. Toxicol. Pathol. 28(5), 716-725 (2000).
4. Spitsbergen JM, Tsai HW, Reddy A et al. Neoplasia in zebrafish (Danio rerio) treated with 7,12 dimethylbenz[a]anthracene by two exposure routes at different developmental stages. Toxicol. Pathol. 28(5), 705-715 (2000).
5. Mizgireuv IV, Majorova IG, Gorodinskaya VM, Khudoley VV, Revskoy SY. Carcinogenic effect of N nitrosodimethylamine on diploid and triploid zebrafish (Danio rerio). Toxicol. Pathol. 32(5), 514-518 (2004). (Pubitemid 39258456)
6. Lam SH, Wu YL, Vega VB et al. Conservation of gene expression signatures between zebrafish and human liver tumors and tumor progression. Nat. Biotechnol. 24(1), 73-75 (2006). (Pubitemid 43083168)
7. Ung CY, Lam SH, Gong Z. Comparative transcriptome analyses revealed conserved biological and transcription factor target modules between the zebrafish and human tumors. Zebrafish 6(4), 425-431 (2009).
8. Gong ZY, Koh CHV, Nguyen AT et al. The zebrafish model for liver carcinogenesis. In: Molecular Genetics of Liver Neoplasia. Wang X, Grisham J, Thorgeirsson S (Eds). Springer, NY, USA, 197-217 (2010).
9. Jessen JR, Jessen TN, Vogel SS, Lin S. Concurrent expression of recombination activating genes 1 and 2 in zebrafish olfactory sensory neurons. Genesis 29(4), 156-162 (2001). (Pubitemid 32417238)
10. Langenau DM, Traver D, Ferrando AA et al. Myc-induced T cell leukemia in transgenic zebrafish. Science 299(5608), 887-890 (2003). (Pubitemid 36182446)
11. Yang HW, Kutok JL, Lee NH et al. Targeted expression of human MYCN selectively causes pancreatic neuroendocrine tumors in transgenic zebrafish. Cancer Res. 64(20), 7256-7262 (2004). (Pubitemid 39372062)
12. Park SW, Davison JM, Rhee J, Hruban RH, Maitra A, Leach SD. Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology 134(7), 2080-2090 (2008). (Pubitemid 351783259)
13. Langenau DM, Keefe MD, Storer NY et al. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev. 21(11), 1382-1395 (2007). (Pubitemid 46871041)
14. Patton EE, Widlund HR, Kutok JL et al. BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr. Biol. 15(3), 249-254 (2005). (Pubitemid 40205706)
15. Ceol CJ, Houvras Y, Jane-Valbuena J et al. The histone methyltransferase SETDB1 is recurrently amplified in melanoma and accelerates its onset. Nature 471(7339), 513-517 (2011).
16. White RM, Cech J, Ratanasirintrawoot S et al. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature 471(7339), 518-522 (2011).
17. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW. nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126(17), 3757-3767 (1999). (Pubitemid 29440475)
18. White RM, Sessa A, Burke C et al. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2(2), 183-189 (2008). (Pubitemid 351168711)
19. Banerjee D, Harfouche R, Sengupta S. Nanotechnology-mediated targeting of tumor angiogenesis. Vascular Cell 3(1), 3 (2011).
20. Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev. Biol. 248(2), 307-318 (2002). (Pubitemid 35002091)
21. Stoletov K, Montel V, Lester RD, Gonias SL, Klemke R. High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc. Natl Acad. Sci. USA 104(44), 17406-17411 (2007). (Pubitemid 350219851)
22. Stoletov K, Kato H, Zardouzian E et al. Visualizing extravasation dynamics of metastatic tumor cells. J. Cell Sci. 123(Pt 13), 2332-2341 (2010).
23. Jin SW, Beis D, Mitchell T, Chen JN, Stainier DY. Cellular and molecular analyses of vascular tube and lumen formation in zebrafish. Development 132(23), 5199-5209 (2005). (Pubitemid 43020175)
24. Zhao C, Wang X, Zhao Y et al. A novel xenograft model in zebrafish for high-resolution investigating dynamics of neovascularization in tumors. PLoS ONE 6(7), E21768 (2011).
25. Zhang S, Cao Z, Tian H et al. SKLB1002, a novel potent inhibitor of VEGF receptor 2 signaling, inhibits angiogenesis and tumor growth in vivo. Clin. Cancer Res. 17(13), 4439-4450 (2011).
26. Villanueva A, Minguez B, Forner A, Reig M, Llovet JM. Hepatocellular carcinoma: novel molecular approaches for diagnosis, prognosis, and therapy. Ann. Rev. Med. 61, 317-328 (2010).
27. Gomaa AI, Khan SA, Toledano MB, Waked I, Taylor-Robinson SD. Hepatocellular carcinoma: epidemiology, risk factors and pathogenesis. World J. Gastroenterol. 14(27), 4300-4308 (2008).
28. Lu JW, Hsia Y, Tu HC et al. Liver development and cancer formation in zebrafish. Birth Defects Res. C Embryo Today 93(2), 157-172 (2011).
29. Vucur M, Roderburg C, Bettermann K et al. Mouse models of hepatocarcinogenesis: what can we learn for the prevention of human hepatocellular carcinoma? Oncotarget 1(5), 373-378 (2010).
30. Ingham PW. The power of the zebrafish for disease analysis. Hum. Mol. Genet. 18(R1), R107-R112 (2009).
31. Kari G, Rodeck U, Dicker AP. Zebrafish: an emerging model system for human disease and drug discovery. Clin. Pharmacol. Ther. 82(1), 70-80 (2007). (Pubitemid 46944200)
32. Lieschke GJ, Currie PD. Animal models of human disease: zebrafish swim into view. Nat. Rev. Genet. 8(5), 353-367 (2007). (Pubitemid 46625809)
33. Lam SH, Gong ZY. Fish as a model for human disease. In: Human Genetics (4th Edition). Vogel F, Motulsky AG (Eds). Springer Verlag, Heidelberg, Germany, 827-843 (2010).
34. Feitsma H, Cuppen E. Zebrafish as a cancer model. Mol. Cancer Res. 6(5), 685-694 (2008).
35. Stoletov K, Klemke R. Catch of the day: zebrafish as a human cancer model. Oncogene 27(33), 4509-4520 (2008).
36. Sukardi H, Chng HT, Chan EC, Gong Z, Lam SH. Zebrafish for drug toxicity screening: bridging the in vitro cell-based models and in vivo mammalian models. Expert Opin. Drug Metab. Toxicol. 7(5), 579-589 (2011).
37. Evensen L, Link W, Lorens JB. Imaged-based high-throughput screening for anti-angiogenic drug discovery. Curr. Pharm. Des. 16(35), 3958-3963 (2010).
38. Rubinstein AL, Tran TC, Sneed B et al. Automated, quantitative screening assay for antiangiogenic compounds using transgenic zebrafish. Cancer Res. 67(23), 11386-11392 (2007). (Pubitemid 350248566)
39. Chen S, Zhu Y, Xia W, Xia S, Xu X. Automated analysis of zebrafish images for phenotypic changes in drug discovery. J. Neurosci. Methods 200(2), 229-236 (2011).
40. Nguyen AT, Emelyanov A, Koh CH et al. A high level of liver-specific expression of oncogenic KrasV12 drives robust liver tumorigenesis in transgenic zebrafish. Dis. Models Mech. 4(6), 801-813 (2011).
41. Zender L, Spector MS, Xue W et al. Identification and validation of oncogenes in liver cancer using an integrative oncogenomic approach. Cell 125(7), 1253-1267 (2006). (Pubitemid 43929093)
42. Villanueva A, Llovet JM. Targeted therapies for hepatocellular carcinoma. Gastroenterology 140(5), 1410-1426 (2011).
43. Karnoub AE, Weinberg RA. Ras oncogenes: split personalities. Nat. Rev. Mol. Cell Biol. 9(7), 517-531 (2008). (Pubitemid 351881844)
44. Gossen M, Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl Acad. Sci. USA 89(12), 5547-5551 (1992).
45. Urlinger S, Baron U, Thellmann M, Hasan MT, Bujard H, Hillen W. Exploring the sequence space for tetracycline-dependent transcriptional activators: novel mutations yield expanded range and sensitivity. Proc. Natl Acad. Sci. USA 97(14), 7963-7968 (2000). (Pubitemid 30460756)
46. Emelyanov A, Parinov S. Mifepristone-inducible LexPR system to drive and control gene expression in transgenic zebrafish. Dev. Biol. 320(1), 113-121 (2008).
47. Li Z, Huang X, Zhan H et al. Inducible and repressable oncogenic-addicted hepatocellular carcinoma in Tet On xmrk transgenic zebrafish. J. Hepatol. doi:10.1016/j. jhep.2011.07.025 (2011) (Epub ahead of print).
48. Schartl M. Homology of melanoma-inducing loci in the genus Xiphophorus. Genetics 126(4), 1083-1091 (1990).
49. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Parinov S, Gong Z. An inducible kras V12 transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis. Model Mech. doi:10.1242/ dmm.008367 (2011) (Epub ahead of print).
50. Weinstein IB. Cancer. Addiction to oncogenes - the Achilles heal of cancer. Science 297(5578), 63-64 (2002). (Pubitemid 34743088)
51. Mirbahai L, Williams TD, Zhan H, Gong Z, Chipman JK. Comprehensive profiling of zebrafish hepatic proximal promoter CpG island methylation and its modification during chemical carcinogenesis. BMC Genomics 12, 3 (2011).
52. Zon LI, Bowman TV. Swimming into the future of drug discovery: in vivo chemical screens in zebrafish. ACS Chem. Biol. 5(2), 159-161 (2010).
53. North TE, Goessling W, Walkley CR et al. Prostaglandin E2 regulates vertebrate haematopoietic stem cell homeostasis. Nature 447(7147), 1007-1011 (2007). (Pubitemid 46975751)
54. Sabaawy HE, Azuma M, Embree LJ, Tsai HJ, Starost MF, Hickstein DD. TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proc. Natl Acad. Sci. USA 103(41), 15166-15171 (2006). (Pubitemid 44583182)
55. Chen J, Jette C, Kanki JP, Aster JC, Look AT, Griffin JD. NOTCH1-induced T cell leukemia in transgenic zebrafish. Leukemia 21(3), 462-471 (2007).
56. Zhuravleva J, Paggetti J, Martin L et al. MOZ/TIF2-induced acute myeloid leukaemia in transgenic fish. Br. J. Haematol. 143(3), 378-382 (2008).
57. Dovey M, White RM, Zon LI. Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish 6(4), 397-404 (2009).
58. Ju B, Spitsbergen J, Eden CJ, Taylor MR, Chen W. Co-activation of hedgehog and AKT pathways promote tumorigenesis in zebrafish. Mol. Cancer 8, 40 (2009).
59. Chen YH, Wang YH, Yu TH, Wu HJ, Pai CW. Transgenic zebrafish line with over-expression of Hedgehog on the skin: a useful tool to screen Hedgehog-inhibiting compounds. Transgenic Res. 18(6), 855-864 (2009).
60. Santoriello C, Gennaro E, Anelli V et al. Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLoS ONE 5(12), e15170 (2010).
61. Liu NA, Jiang H, Ben-Shlomo A et al. Targeting zebrafish and murine pituitary corticotroph tumors with a cyclin-dependent kinase (CDK) inhibitor. Proc. Natl Acad. Sci. USA 108(20), 8414-8419 (2011).
62. Gutierrez A, Grebliunaite R, Feng H et al. Pten mediates Myc oncogene dependence in a conditional zebrafish model of T cell acute lymphoblastic leukemia. J. Exp. Med. 208(8), 1595-1603 (2011).
63. Korzh V, Korzh S, Pan XF et al. Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish. BMC Dev. Biol. 8, 84 (2008).