Mouse models in liver cancer research: A review of current literature

World Journal of Gastroenterology

Volumn 14, Issue 45, 2008, Pages 6915-6923

  Leenders, Martijn W H ^a   Nijkamp, Maarten W ^a   Borel Rinkes, Inne H M ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

Author keywords

Genetically engineered mice; Hepatocellular carcinoma; Mouse model; Primary liver cancer

Indexed keywords

AFLATOXIN B1; ALCOHOL; ANTINEOPLASTIC AGENT; BETA CATENIN; DIETHYLNITROSAMINE; MYC PROTEIN; ORAL CONTRACEPTIVE AGENT; PHENOBARBITAL; PROTEIN P53; RETINOBLASTOMA PROTEIN; VIRUS ENVELOPE PROTEIN; VIRUS PROTEIN; VIRUS T ANTIGEN; WNT PROTEIN;

ANTINEOPLASTIC ACTIVITY; CANCER MODEL; CANCER RESEARCH; CHEMICAL CARCINOGENESIS; DISEASE ASSOCIATION; EXPERIMENTAL MOUSE; GENETIC ENGINEERING; GENOTOXICITY; HEPATITIS B; HEPATITIS C; HUMAN; LIVER CANCER; LIVER CARCINOGENESIS; LIVER CELL CARCINOMA; NONHUMAN; REVIEW; TRANSGENIC MOUSE; TUMOR XENOGRAFT;

EID: 63449084376     PISSN: 10079327     EISSN: None     Source Type: Journal    
DOI: 10.3748/wjg.14.6915     Document Type: Review

References (80)

1. American Cancer Society. Global Cancer Facts & Figures 2007. Available from: URL: http://www.cancer.org/docroot/STT/ stt_0_2007asp?sitearea=STT&level=1
2. Farazi PA, DePinho RA. Hepatocellular carcinoma pathogenesis: from genes to environment. Nat Rev Cancer 2006; 6: 674-687
3. Llovet JM, Burroughs A, Bruix J. Hepatocellular carcinoma. Lancet 2003; 362: 1907-1917
4. Frese KK, Tuveson DA. Maximizing mouse cancer models. Nat Rev Cancer 2007; 7: 645-658
5. Naugler WE, Sakurai T, Kim S, Maeda S, Kim K, Elsharkawy AM, Karin M. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production. Science 2007; 317: 121-124
6. Chen CJ, Yu MW, Liaw YF. Epidemiological characteristics and risk factors of hepatocellular carcinoma. J Gastroenterol Hepatol 1997; 12: S294-S308
7. Buchmann A, Bauer-Hofmann R, Mahr J, Drinkwater NR, Luz A, Schwarz M. Mutational activation of the c-Ha-ras gene in liver tumors of different rodent strains: correlation with susceptibility to hepatocarcinogenesis. Proc Natl Acad Sci USA 1991; 88: 911-915
8. Lee GH. Paradoxical effects of phenobarbital on mouse hepatocarcinogenesis. Toxicol Pathol 2000; 28: 215-225
9. Hann B, Balmain A. Building 'validated' mouse models of human cancer. Curr Opin Cell Biol 2001; 13: 778-784
10. Wogan GN. Impacts of chemicals on liver cancer risk. Semin Cancer Biol 2000; 10: 201-210
11. Williams GM. Chemicals with carcinogenic activity in the rodent liver; mechanistic evaluation of human risk. Cancer Lett 1997; 117: 175-188
12. Seitz HK, Stickel F. Molecular mechanisms of alcohol-mediated carcinogenesis. Nat Rev Cancer 2007; 7: 599-612
13. Gonzalez FJ. The peroxisome proliferator-activated receptor alpha (PPARalpha): role in hepatocarcinogenesis. Mol Cell Endocrinol 2002; 193: 71-79
14. Huff J, Cirvello J, Haseman J, Bucher J. Chemicals associated with site-specific neoplasia in 1394 long-term carcinogenesis experiments in laboratory rodents. Environ Health Perspect 1991; 93: 247-270
15. Vesselinovitch SD, Mihailovich N. Kinetics of diethylnitrosamine hepatocarcinogenesis in the infant mouse. Cancer Res 1983; 43: 4253-4259
16. Vesselinovitch SD, Koka M, Mihailovich N, Rao KV. Carcinogenicity of diethylnitrosamine in newborn, infant, and adult mice. J Cancer Res Clin Oncol 1984; 108: 60-65
17. Vesselinovitch SD. Infant mouse as a sensitive bioassay system for carcinogenicity of N-nitroso compounds. IARC Sci Publ 1980; 645-655
18. Anisimov VN, Ukraintseva SV, Yashin AI. Cancer in rodents: does it tell us about cancer in humans? Nat Rev Cancer 2005; 5: 807-819
19. Hirst GL, Balmain A. Forty years of cancer modelling in the mouse. Eur J Cancer 2004; 40: 1974-1980
20. Troiani T, Schettino C, Martinelli E, Morgillo F, Tortora G, Ciardiello F. The use of xenograft models for the selection of cancer treatments with the EGFR as an example. Crit Rev Oncol Hematol 2008; 65: 200-211
21. Killion JJ, Radinsky R, Fidler IJ. Orthotopic models are necessary to predict therapy of transplantable tumors in mice. Cancer Metastasis Rev 1998; 17: 279-284
22. Heijstek MW, Kranenburg O, Borel Rinkes IH. Mouse models of colorectal cancer and liver metastases. Dig Surg 2005; 22: 16-25
23. Clarke R. Human breast cancer cell line xenografts as models of breast cancer. The immunobiologies of recipient mice and the characteristics of several tumorigenic cell lines. Breast Cancer Res Treat 1996; 39: 69-86
24. Bankert RB, Egilmez NK, Hess SD. Human-SCID mouse chimeric models for the evaluation of anti-cancer therapies. Trends Immunol 2001; 22: 386-393
25. Tang ZY, Sun FX, Tian J, Ye SL, Liu YK, Liu KD, Xue Q, Chen J, Xia JL, Qin LX, Sun SL, Wang L, Zhou J, Li Y, Ma ZC, Zhou XD, Wu ZQ, Lin ZY, Yang BH. Metastatic human hepatocellular carcinoma models in nude mice and cell line with metastatic potential. World J Gastroenterol 2001; 7: 597-601
26. Jonkers J, Berns A. Conditional mouse models of sporadic cancer. Nat Rev Cancer 2002; 2: 251-265
27. Khanna C, Hunter K. Modeling metastasis in vivo. Carcinogenesis 2005; 26: 513-523
28. Bibby MC. Orthotopic models of cancer for preclinical drug evaluation: advantages and disadvantages. Eur J Cancer 2004; 40: 852-857
29. Becher OJ, Holland EC. Genetically engineered models have advantages over xenografts for preclinical studies. Cancer Res 2006; 66: 3355-8335, discussion 3358-3359
30. Shuldiner AR. Transgenic animals. N Engl J Med 1996; 334: 653-655
31. Palmiter RD, Brinster RL, Hammer RE, Trumbauer ME, Rosenfeld MG, Birnberg NC, Evans RM. Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 1982; 300: 611-615
32. Buendia MA. Genetics of hepatocellular carcinoma. Semin Cancer Biol 2000; 10: 185-200
33. Colnot S, Decaens T, Niwa-Kawakita M, Godard C, Hamard G, Kahn A, Giovannini M, Perret C. Liver-targeted disruption of Apc in mice activates beta-catenin signaling and leads to hepatocellular carcinomas. Proc Natl Acad Sci USA 2004; 101: 17216-17221
34. Ali SH, DeCaprio JA. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin Cancer Biol 2001; 11: 15-23
35. Ahuja D, Saenz-Robles MT, Pipas JM. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 2005; 24: 7729-7745
36. Dubois N, Bennoun M, Allemand I, Molina T, Grimber G, Daudet-Monsac M, Abelanet R, Briand P. Time-course development of differentiated hepatocarcinoma and lung metastasis in transgenic mice. J Hepatol 1991; 13: 227-239
37. Kitagawa T, Hino O, Lee GH, Li H, Liu J, Nomura K, Ohtake K, Furuta Y, Aizawa S. Multistep hepatocarcinogenesis in transgenic mice harboring SV40 T-antigen gene. Princess Takamatsu Symp 1991; 22: 349-360
38. Sepulveda AR, Finegold MJ, Smith B, Slagle BL, DeMayo JL, Shen RF, Woo SL, Butel JS. Development of a transgenic mouse system for the analysis of stages in liver carcinogenesis using tissue-specific expression of SV40 large T-antigen controlled by regulatory elements of the human alpha-1-antitrypsin gene. Cancer Res 1989; 49: 6108-6117
39. Murakami H, Sanderson ND, Nagy P, Marino PA, Merlino G, Thorgeirsson SS. Transgenic mouse model for synergistic effects of nuclear oncogenes and growth factors in tumorigenesis: interaction of c-myc and transforming growth factor alpha in hepatic oncogenesis. Cancer Res 1993; 53: 1719-1723
40. Santoni-Rugiu E, Nagy P, Jensen MR, Factor VM, Thorgeirsson SS. Evolution of neoplastic development in the liver of transgenic mice co-expressing c-myc and transforming growth factor-alpha. Am J Pathol 1996; 149: 407-428
41. Lewis BC, Klimstra DS, Socci ND, Xu S, Koutcher JA, Varmus HE. The absence of p53 promotes metastasis in a novel somatic mouse model for hepatocellular carcinoma. Mol Cell Biol 2005; 25: 1228-1237
42. Lou DQ, Molina T, Bennoun M, Porteu A, Briand P, Joulin V, Vasseur-Cognet M, Cavard C. Conditional hepatocarcinogenesis in mice expressing SV 40 early sequences. Cancer Lett 2005; 229: 107-114
43. Harada N, Oshima H, Katoh M, Tamai Y, Oshima M, Taketo MM. Hepatocarcinogenesis in mice with beta-catenin and Ha-ras gene mutations. Cancer Res 2004; 64: 48-54
44. Parkin DM. The global health burden of infection-associated cancers in the year 2002. Int J Cancer 2006; 118: 3030-3044
45. Fattovich G, Stroffolini T, Zagni I, Donato F. Hepatocellular carcinoma in cirrhosis: incidence and risk factors. Gastroenterology 2004; 127: S35-S50
46. Dandri M, Volz TK, Lutgehetmann M, Petersen J. Animal models for the study of HBV replication and its variants. J Clin Virol 2005; 34 Suppl 1: S54-S62
47. Kremsdorf D, Brezillon N. New animal models for hepatitis C viral infection and pathogenesis studies. World J Gastroenterol 2007; 13: 2427-2435
48. Singh M, Kumar V. Transgenic mouse models of hepatitis B virus-associated hepatocellular carcinoma. Rev Med Virol 2003; 13: 243-253
49. Cougot D, Neuveut C, Buendia MA. HBV induced carcinogenesis. J Clin Virol 2005; 34 Suppl 1: S75-S78
50. Brechot C. Pathogenesis of hepatitis B virus-related hepatocellular carcinoma: old and new paradigms. Gastroenterology 2004; 127: S56-S61
51. Park NH, Song IH, Chung YH. Chronic hepatitis B in hepatocarcinogenesis. Postgrad Med J 2006; 82: 507-515
52. Liang TJ, Heller T. Pathogenesis of hepatitis C-associated hepatocellular carcinoma. Gastroenterology 2004; 127: S62-S71
53. Guidotti LG, Chisari FV. Immunobiology and pathogenesis of viral hepatitis. Annu Rev Pathol 2006; 1: 23-61
54. Lee TH, Finegold MJ, Shen RF, DeMayo JL, Woo SL, Butel JS. Hepatitis B virus transactivator X protein is not tumorigenic in transgenic mice. J Virol 1990; 64: 5939-5947
55. Chisari FV, Pinkert CA, Milich DR, Filippi P, McLachlan A, Palmiter RD, Brinster RL. A transgenic mouse model of the chronic hepatitis B surface antigen carrier state. Science 1985; 230: 1157-1160
56. Babinet C, Farza H, Morello D, Hadchouel M, Pourcel C. Specific expression of hepatitis B surface antigen (HBsAg) in transgenic mice. Science 1985; 230: 1160-1163
57. Akbar SK, Onji M. Hepatitis B virus (HBV)-transgenic mice as an investigative tool to study immunopathology during HBV infection. Int J Exp Pathol 1998; 79: 279-291
58. Chisari FV, Klopchin K, Moriyama T, Pasquinelli C, Dunsford HA, Sell S, Pinkert CA, Brinster RL, Palmiter RD. Molecular pathogenesis of hepatocellular carcinoma in hepatitis B virus transgenic mice. Cell 1989; 59: 1145-1156
59. Reifenberg K, Lohler J, Pudollek HP, Schmitteckert E, Spindler G, Kock J, Schlicht HJ. Long-term expression of the hepatitis B virus core-e- and X-proteins does not cause pathologic changes in transgenic mice. J Hepatol 1997; 26: 119-130
60. Kim CM, Koike K, Saito I, Miyamura T, Jay G. HBx gene of hepatitis B virus induces liver cancer in transgenic mice. Nature 1991; 351: 317-320
61. Yu DY, Moon HB, Son JK, Jeong S, Yu SL, Yoon H, Han YM, Lee CS, Park JS, Lee CH, Hyun BH, Murakami S, Lee KK. Incidence of hepatocellular carcinoma in transgenic mice expressing the hepatitis B virus X-protein. J Hepatol 1999; 31: 123-132
62. Chandra M, Frith CH. Spontaneous neoplasms in aged CD-1 mice. Toxicol Lett 1992; 61: 67-74
63. Bagis H, Arat S, Mercan HO, Aktoprakligil D, Caner M, Turanli ET, Baysal K, Turgut G, Sekmen S, Cirakoglu B. Stable transmission and expression of the hepatitis B virus total genome in hybrid transgenic mice until F10 generation. J Exp Zoolog A Comp Exp Biol 2006; 305: 420-427
64. Guidotti LG, Matzke B, Schaller H, Chisari FV. High-level hepatitis B virus replication in transgenic mice. J Virol 1995; 69: 6158-6169
65. Ghebranious N, Sell S. Hepatitis B injury, male gender, aflatoxin, and p53 expression each contribute to hepatocarcinogenesis in transgenic mice. Hepatology 1998; 27: 383-391
66. Sell S, Hunt JM, Dunsford HA, Chisari FV. Synergy between hepatitis B virus expression and chemical hepatocarcinogens in transgenic mice. Cancer Res 1991; 51: 1278-1285
67. Kaplanski C, Chisari FV, Wild CP. Minisatellite rearrangements are increased in liver tumours induced by transplacental aflatoxin B1 treatment of hepatitis B virus transgenic mice, but not in spontaneously arising tumours. Carcinogenesis 1997; 18: 633-639
68. Jakubczak JL, Chisari FV, Merlino G. Synergy between transforming growth factor alpha and hepatitis B virus surface antigen in hepatocellular proliferation and carcinogenesis. Cancer Res 1997; 57: 3606-3611
69. Terradillos O, Billet O, Renard CA, Levy R, Molina T, Briand P, Buendia MA. The hepatitis B virus X gene potentiates c-myc-induced liver oncogenesis in transgenic mice. Oncogene 1997; 14: 395-404
70. Di Bisceglie AM. Hepatitis C and hepatocellular carcinoma. Hepatology 1997; 26: 34S-38S
71. Koike K, Tsutsumi T, Fujie H, Shintani Y, Kyoji M. Molecular mechanism of viral hepatocarcinogenesis. Oncology 2002; 62 Suppl 1: 29-37
72. Moriya K, Yotsuyanagi H, Shintani Y, Fujie H, Ishibashi K, Matsuura Y, Miyamura T, Koike K. Hepatitis C virus core protein induces hepatic steatosis in transgenic mice. J Gen Virol 1997; 78 (Pt 7): 1527-1531
73. Moriya K, Fujie H, Shintani Y, Yotsuyanagi H, Tsutsumi T, Ishibashi K, Matsuura Y, Kimura S, Miyamura T, Koike K. The core protein of hepatitis C virus induces hepatocellular carcinoma in transgenic mice. Nat Med 1998; 4: 1065-1067
74. Lerat H, Honda M, Beard MR, Loesch K, Sun J, Yang Y, Okuda M, Gosert R, Xiao SY, Weinman SA, Lemon SM. Steatosis and liver cancer in transgenic mice expressing the structural and nonstructural proteins of hepatitis C virus. Gastroenterology 2002; 122: 352-365
75. Kamegaya Y, Hiasa Y, Zukerberg L, Fowler N, Blackard JT, Lin W, Choe WH, Schmidt EV, Chung RT. Hepatitis C virus acts as a tumor accelerator by blocking apoptosis in a mouse model of hepatocarcinogenesis. Hepatology 2005; 41: 660-667
76. Kato T, Miyamoto M, Date T, Yasui K, Taya C, Yonekawa H, Ohue C, Yagi S, Seki E, Hirano T, Fujimoto J, Shirai T, Wakita T. Repeated hepatocyte injury promotes hepatic tumorigenesis in hepatitis C virus transgenic mice. Cancer Sci 2003; 94: 679-685
77. Jhappan C, Stahle C, Harkins RN, Fausto N, Smith GH, Merlino GT. TGF alpha overexpression in transgenic mice induces liver neoplasia and abnormal development of the mammary gland and pancreas. Cell 1990; 61: 1137-1146
78. Lee GH, Merlino G, Fausto N. Development of liver tumors in transforming growth factor alpha transgenic mice. Cancer Res 1992; 52: 5162-5170
79. Conner EA, Lemmer ER, Omori M, Wirth PJ, Factor VM, Thorgeirsson SS. Dual functions of E2F-1 in a transgenic mouse model of liver carcinogenesis. Oncogene 2000; 19: 5054-5062
80. Calvisi DF, Conner EA, Ladu S, Lemmer ER, Factor VM, Thorgeirsson SS. Activation of the canonical Wnt/beta-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer. J Hepatol 2005; 42: 842-849