Disruption of β-Catenin Pathway or Genomic Instability Define Two Distinct Categories of Liver Cancer in Transgenic Mice

Gastroenterology

Volumn 126, Issue 5, 2004, Pages 1374-1386

  Calvisi, Diego F ^a   Factor, Valentina M ^a   Ladu, Sara ^a   Conner, Elizabeth A ^a   Thorgeirsson, Snorri S ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; MYC PROTEIN; TRANSCRIPTION FACTOR E2F1; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CHROMOSOMAL LOCALIZATION; CHROMOSOME 1; CHROMOSOME 12; CHROMOSOME 14; CHROMOSOME 2; CHROMOSOME 4; CHROMOSOME 6; CHROMOSOME 7; CHROMOSOME 9; CONTROLLED STUDY; GENE DELETION; GENE DISRUPTION; GENE LOCUS; GENE MUTATION; GENETIC STABILITY; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LIVER CANCER; LIVER CELL CARCINOMA; LIVER TUMOR; MICROSATELLITE MARKER; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROGNOSIS; PROTEIN EXPRESSION; RANDOM AMPLIFIED POLYMORPHIC DNA; TRANSGENIC MOUSE; X CHROMOSOME;

EID: 2142812377     PISSN: 00165085     EISSN: None     Source Type: Journal    
DOI: 10.1053/j.gastro.2004.02.014     Document Type: Article

References (78)

1. Simonetti RG, Camma C, Fiorello F, Politi F, D'Amico G, Pagliaro L. Hepatocellular carcinoma. A worldwide problem and the major risk factors. Dig Dis Sci 1991;36:962-972.
2. Thorgeirsson SS, Grisham JW. Molecular pathogenesis of human hepatocellular caminoma. Nat Genet 2002;31:339-346.
3. Hanahan D, Weinberg RA. The hallmarks of cancer. Cell 2000; 100:57-70.
4. Loeb LA. A mutator phenotype in cancer. Cancer Res 2001;61: 3230-3239.
5. Loeb LA, Loeb KR, Anderson JP. Multiple mutations and cancer. Proc Natl Acad Sci U S A 2003;100:776-781.
6. Nagai H, Pineau P, Tiollais P, Buendia MA, Dejean A. Comprehensive allelotyping of human hepatocellular carcinoma. Oncogene 1997;14:2927-2933.
7. Murakami Y, Hayashi K, Hirohashi S, Sekiya T. Aberrations of the tumor suppressor p53 and retinoblastoma genes in human hepatocellular carcinomas. Cancer Res 1991;51:5520-5525.
8. De Souza AT, Hankins GR, Washington MK, Orton TC, Jirtle RL. M6P/IGF2R gene is mutated in human hepatocellular carcinomas with loss of heterozygosity. Nat Genet 1995;11:447-449.
9. Kanai Y, Ushijima S, Hui AM, Ochiai A, Tsuda H, Sakamoto M, Hirohashi S. The E-cadherin gene is silenced by CpG methylation in human hepatocellular carcinomas. Int J Cancer 1997;71:355-359.
10. Peng SY, Lai PL, Hsu HC. Amplification of the c-myc gene in human hepatocellular carcinoma: biologic significance. J Formos Med Assoc 1993;92:866-870.
11. Nishida N, Fukuda Y, Komeda T, Kita R, Sando T, Furukawa M, Amenomori M, Shibagaki I, Nakao K, Ikenaga M, Ishizaki K. Amplification and overexpression of the cyclin D1 gene in aggressive human hepatocellular carcinoma. Cancer Res 1994;54: 3107-3110.
12. De La Coste A, Romagnolo B, Billuart P, Renard CA, Buendia MA, Soubrane O, Fabre M, Chelly J, Beldjord C, Kahn A, Perret C. Somatic mutations of the β-catenin gene are frequent in mouse and human hepatocellular carcinomas. Proc Natl Acad Sci U S A 1998;95:8847-8851.
13. Miyoshi Y, Iwao K, Nagasawa Y, Aihara T, Sasaki Y, Imaoka S, Murata M, Shimano T, Nakamura Y. Activation of the beta-catenin gene in primary hepatocellular carcinomas by somatic alterations involving exon 3. Cancer Res 1998;58:2524-2527.
14. Yamada Y, Yoshimi N, Sugie S, Suzui M, Matsunaga K, Kawabata K, Hara A, Mori H. β-Catenin (Ctnnb1) gene mutations in diethylnitrosamine (DEN)-induced liver tumors in male F344 rats. Jpn J Cancer Res 1999;90:824-828.
15. Anna CH, Sills RC, Foley JF, Stockton PS, Ton TV, Devereux TR. Beta-catenin mutations and protein accumulation in all hepatoblastomas examined from B6C3F1 mice treated with anthraquinone or oxazepam. Cancer Res 2000;60:2864-2868.
16. Renard CA, Fourel G, Bralet MP, Degott C, De La Coste A, Perret C, Tiollais P, Buendia MA. Hepatocellular carcinoma in WHV/N-myc2 transgenic mice: oncogenic mutations of beta-catenin and synergistic effect of p53 null alleles. Oncogene 2000;19;2678-2686.
17. Gumbiner BM. Signal transduction by β-catenin. Curr Opin Cell Biol 1995;7:634-640.
18. Polakis P. Wnt signaling and cancer. Genes Dev 2000;14:1837-1851.
19. Satoh S, Daigo Y, Furukawa Y, Kato T, Miwa N, Nishiwaki T, Kawasoe T, Ishiguro H, Fujita M, Tokino T, Sasaki Y, Imaoka S, Murata M, Shimano T, Yamaoka Y, Nakamura Y. AXIN1 mutations in hepatocellular carcinomas, and growth suppression in cancer cells by virus-mediated transfer of AXIN1. Nat Genet 2000;24:245-250.
20. Taniguchi K, Roberts LR, Aderca IN, Dong X, Qian C, Murphy LM, Nagomey DM, Burgart LJ, Roche PC, Smith DI, Ross JA, Liu W. Mutational spectrum of β-catenin, AXIN1, and AXIN2 in hepatocellular carcinomas and hepatoblastomas. Oncogene 2002;21: 4863-4871.
21. Laurent-Puig P, Legoix P, Bluteau O, Belghiti J, Franco D, Binot F, Monges G, Thomas G, Bioulac Bloulac-Sage P, Zucman-Rossi J. Genetic alterations associated with hepatocellular carcinomas define distinct pathways of hepatocarcinogenesis. Gastroenterology 2001; 120:1763-1773.
22. Legoix P, Bluteau O, Bayer J, Perret C, Balabaud C, Belghiti J, Franco D, Thomas G, Laurent-Puig P, Zucman-Rossi J. β-Catenin mutations in hepatocellular carcinoma correlate with a low rate of loss of heterozygosity. Oncogene 1999;18:4044-4046.
23. Conner EA, Lemmer ER, Sanchez A, Factor VM, Thorgeirsson SS. E2F1 blocks and c-Myc accelerates hepatic ploidy in transgenic mouse models. Biochem Biophys Res Commun 2003;302:114-120.
24. 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-α in hepatic oncogenesis. Cancer Res 1993;53:1719-1723.
25. 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.
26. Calvisi DF, Factor VM, Loi R, Thorgeirsson SS. Activation of β-catenin during hepatocarcinogenesis in transgenic mouse models: relationship to phenotype and tumor grade. Cancer Res 2001;61:2085-2091.
27. Sargent LM, Zhou X, Keck CL, Sanderson ND, Zimonjic DB, Popescu NC, Thorgeirsson SS. Nonrandom cytogenetic alterations in hepatocellular carcinoma from transgenic mice overexpressing c-myc and transforming growth factor-α in the liver. Am J Pathol 1999;154:1047-1055.
28. Lee GH, Merlino G, Fausto N. Development of liver tumors in transforming growth factor alpha transgenic mice. Cancer Res 1992;52:5162-5170.
29. Frith CH, Ward JM, Turusov VS. Tumours of the liver. In: Turusov V, Mohr U, eds. Pathology of tumors in laboratory animals. Volume 2. Lyon, France: IARC Scientific Publications, 1994:223-270.
30. Laird PW, Zijderveld A, Linders K, Rudnicki MA, Jaenisch R, Bems A. Simplified mammalian DNA isolation procedure. Nucleic Acids Res 1991;19:4293.
31. Woodward SR, Sudweeks J, Teuscher C. Random sequence oligonucleotide primers detect polymorphic DNA products which segregate in inbred strains of mice. Mamm Genome 1992;3:73-78.
32. Luceri C, De Filippo C, Cademi G, Gambacciani L, Salvadori M, Giannini A, Dolara P. Detection of somatic DNA alterations in azoxymethane-induced F344 rat colon tumors by random amplified polymorphic DNA analysis. Carcinogenesis 2000;21:1753-1756.
33. Dietrich WF, Miller J, Steen R, Merchant MA, Damron-Boles D, Husain Z, Dredge R, Daly MJ, Ingalls KA, O'Connor TJ, Evans CA, DeAngelis MM, Levinson DM, Kruglyak L, Goodman N, Copeland NG, Jenkins NA, Hawkins TL, Stein L, Page DC, Lander ES. A comprehensive genetic map of the mouse genome. Nature 1996;380:149-152.
34. Aydinlik H, Nguyen TD, Moennikes O, Buchmann A, Schwarz M. Selective pressure during tumor promotion by phenobarbital leads to clonal outgrowth of beta-catenin-mutated mouse liver tumors. Oncogene 2001;20:7812-7816.
35. Grisham JW. Interspecies comparison of liver carcinogenesis: implications for cancer risk assessment. Carcinogenesis 1997; 18:59-81.
36. Tangkijvanich P, Anukulkarnkusol N, Suwangool P, Lertmaharit S, Hanvivatvong O, Kullavanijaya P, Poovorawan Y. Clinical characteristics and prognosis of hepatocellular carcinoma: analysis based on alpha-fetoprotein levels. J Clin Gastroenterol 2000;31: 301-308.
37. Yao WJ, Chang TT, Wang ST, Chow NH, Lin PW, Chang YC, Tu DG, Chlu NT. Clinicopathologic correlation of serum tissue polypeptide specific antigen in hepatocellular carcinoma. Oncology 2001;61:64-70.
38. Qin LX, Tang ZY. The prognostic significance of clinical and pathological features in hepatocellular carcinoma. World J Gastroenterol 2002;8:193-199.
39. Miyamoto Y, Maitra A, Ghosh B, Zechner U, Argani P, Iacobuzio-Donahue CA, Sriuranpong V, Iso T, Meszoely IM, Wolfe MS, Hruban RH, Ball DW, Schmid RM, Leach SD. Notch mediates TGF alpha-induced changes in epithelial differentiation during pancreatic tumorigenesis. Cancer Cell 2003;3:565-576.
40. Melkonyan HS, Chang WC, Shapiro JP, Mahadevappa M, Fitzpatrick PA, Kiefer MC, Tomei LD, Umansky SR. SARPs: a family of secreted apoptosis-related proteins. Proc Natl Acad Sci U S A 1997;94:13636-13641.
41. Ryu DY, Pratt VS, Davis CD, Schut HAJ, Snyderwine EG. In vivo mutagenicity and hepatocarcinogenicity of 2-amino-3, 8-dimethylimidazoquinoxaline (MelQx) in bitransgenic c-myc/lambda lacZ mice. Cancer Res 1999;59:2587-2592.
42. Calvisi DF, Ladu S, Factor VM, Thorgeirsson SS. Activation of β-catenin provides proliferative and invasive advantages in c-myc/TGF-α hepatocarcinogenesis promoted by phenobarbital. Carcinogenesis (in press).
43. Ogawa K, Yamada Y, Kishibe K, Ishizaki K, Tokusashi Y. Beta-catenin mutations are frequent in hepatocellular carcinomas but absent in adenomas induced by diethylnitrosamine in B6C3F1 mice. Cancer Res 1999;59:1830-1833.
44. Voeller HJ, Truica CI, Gelmann EP. Beta-catenin mutations in human prostate cancer. Cancer Res 1998;58:2520-2523.
45. Torbenson M, Lee JH, Choti M, Gage W, Abraham SC, Montgomery E, Boitnott J, Wu TT. Hepatic adenomas: analysis of sex steroid receptor status and the Wnt signaling pathway. Mod Pathol 2002;15:189-196.
46. Hsu HC, Jeng YM, Mao TL, Chu JS, Lai PL, Peng SY. Beta-catenin mutations are associated with a subset of low-stage hepatocellular carcinoma negative for hepatitis B virus and with favorable prognosis. Am J Pathol 2000;157:763-770.
47. Mao TL, Chu JS, Jeng YM, Lai PL, Hsu HC. Expression of mutant nuclear beta-catenin correlates with non-invasive hepatocellular carcinoma, absence of portal vein spread, and good prognosis. J Pathol 2001;193:95-101.
48. Wong CM, Fan ST, Ng IO. Beta-catenin mutation and overexpression in hepatocellular carcinoma: clinicopathologic and prognostic significance. Cancer 2001;92:136-145.
49. Inagawa S, Itabashi M, Adachi S, Kawamoto T, Hori M, Shimazaki J, Yoshimi F, Fukao K. Expression and prognostic roles of beta-catenin in hepatocellular carcinoma: correlation with tumor progression and postoperative survival. Clin Cancer Res 2002;8: 450-456.
50. Factor VM, Kiss A, Woitach JT, Wirth PJ, Thorgeirsson SS. Disruption of redox homeostasis in the transforming growth factor-alpha/c-myc transgenic mouse model of accelerated hepatocarcinogenesis. J Biol Chem 1998;273:15846-15853.
51. Hironaka K, Factor VM, Calvisi DF, Conner EA, Thorgeirsson SS. Dysregulation of DNA repair pathways in a transforming growth factor alpha/ c-myc transgenic mouse model of accelerated hepatocarcinogenesis. Lab Invest 2003;83:643-654.
52. Lee JS, Thorgeirsson SS. Functional and genomic implications of global gene expression profiles in cell lines from human hepatocellular cancer. Hepatology 2002;35:1134-1143.
53. Li Q, Dang CV. c-myc overexpression uncouples DNA replication from mitosis. Mol Cell Biol 1999;19:5339-5351.
54. Weaver ZA, McCormack SJ, Liyanage M, du Manoir S, Coleman A, Schrock E, Dickson RB, Ried T. A recurring pattern of chromosomal aberrations in mammary gland tumors of MMTV/c-myc transgenic mice. Genes Chromosomes Cancer 1999;25:251-260.
55. Felsher DW, Bishop JM. Reversible tumorigenesis by MYC in hematopoiatic lineages. Mol Cell 1999;4:199-207.
56. Wu Y, Renard CA, Apiou F, Huerre M, Tiollais P, Dutrillaux B, Buendia MA. Recurrent allelic deletions at mouse chromosomes 4 and 14 in Myc-induced liver tumors. Oncogene 2002;21:1518-1526.
57. Menssen A, Hermeking H. Characterization of the c-myc-regulated transcriptome by SAGE: identification and analysis of c-myc target genes. Proc Natl Acad Sci U S A 2002;99:6274-6279.
58. Yin XY, Grove L, Datta NS, Long MW, Prochownik EV. C-myc overexpression and p53 loss cooperate to promote genomic instability. Oncogene 1999;18:1177-1184.
59. Hofferer M, Wirbelauer C, Humar B, Krek W. Increased levels of E2F-1-dependent DNA binding activity after UV- or gamma-irradiation. Nucleic Acids Res 1999;27:491-495.
60. Blattner C, Sparks A, Lane D. Transcription factor E2F-1 is upregulated in response to DNA damage in a manner analogous to that of p53. Mol Cell Biol 1999;19:3704-3713.
61. Polager S, Kalma Y, Berkovich E, Ginsberg D. E2Fs up-regulate expression of genes involved in DNA replication, DNA repair and mitosis. Oncogene 2002;21:437-446.
62. Durkin ME, Keck-Waggoner CL, Popescu NC, Thorgeirsson SS. Integration of a c-myc transgene results in disruption of the mouse Gtf2ird1 gene, the homologue of the human GTF2IRD1 gene hemizygously deleted in Williams-Beuren syndrome. Genomics 2001;73:20-27.
63. Moen CJ, Groot PC, Hart AA, Snoek M, Demant P. Fine mapping of colon tumor susceptibility (Scc) genes in the mouse, different from the genes known to be somatically mutated in colon cancer. Proc Natl Acad Sci U S A 1996;93:1082-1086.
64. Davis LM, Caspary WJ, Sakallah SA, Maronpot R, Wiseman R, Barrett JC, Elliott R, Hozier JC. Loss of heterozygosity in spontaneous and chemically induced tumors of the B6C3F1 mouse. Carcinogenesis 1994;15:1637-1645.
65. Lawler J. The functions of thrombospondin-1 and -2. Curr Opin Cell Biol 2000;12:634-640.
66. Ritland SR, Rowse GJ, Chang Y, Gendler SJ. Loss of heterozygosity analysis in primary mammary tumors and lung metastases of MMTV-MTAg and MMTV-neu transgenic mice. Cancer Res 1997;57:3520-3525.
67. Gariboldi M, Manenti G, Canzian F, Falvella FS, Pierottl MA, Della Porta G, Bineill G, Drigani TA. Chromosome mapping of murine susceptibility loci to liver carcinogenesis. Cancer Res 1993;53: 209-211.
68. Fujimoto Y, Hampton LL, Wirth PJ, Wang NJ, Xie JP, Thorgeirsson SS. Alterations of tumor suppressor genes and allelic losses in human hepatocellular carcinomas in China. Cancer Res 1994; 54:281-285.
69. Spurr NK, Gough AC, Lee MG. Cloning of the mouse homologue of the yeast cell cycle control gene cdc2. DNA Seq 1990;1:49-54.
70. Pineau P, Nagai H, Prigent S, Wei Y, Gyapay G, Weissenbach J, Tiollais P, Buendia MA, Dejean A. Identification of three distinct regions of allelic deletions on the short arm of chromosome 8 in hepatocellular carcinoma. Oncogene 1999;18:3127-3134.
71. Tanaka S, Sugimachi K, Yamashita Yi Y, Ohga T, Shirabe K, Shimada M, Wands JR, Sugimachi K. Tie2 vascular endothelial receptor expression and function in hepatocellular carcinoma. Hepatology 2002;35:861-867.
72. Garrod D, Chidgey M, North A. Desmosomes: differentiation, development, dynamics and disease. Curr Opin Cell Biol 1996; 8:670-678.
73. Ihara A, Koizumi H, Hashizume R, Uchikoshi T. Expression of epithelial cadherin and alpha- and beta-catenins in nontumoral livers and hepatocellular carcinomas. Hepatology 1996;23:1441-1447.
74. Kozyraki R, Scoazec JY, Flejou JF, D'Errico A, Bedossa P, Terris B, Fiorentino M, Bringuier AF, Grigioni WF, Feldmann G. Expression of cadherins and alpha-catenin in primary epithelial tumors of the liver. Gastroenterology 1996;110:1137-1149.
75. Hayashi Y, Wang W, Ninomiya T, Nagano H, Ohta K, Itoh H. Liver enriched transcription factors and differentiation of hepatocellular carcinoma. Mol Pathol 1999;52:19-24.
76. Ma XD, Ma X, Sui YF, Wang WL. Expression of gapjunction genes connexin32 and connexin43 mRNAs and proteins, and their role in hepatocarcinogenesis. World J Gastroenterol 2002;8:64-68.
77. Fitzgerald DJ, Mesnil M, Oyamada M, Tsuda H, Ito N, Yamasaki H. Changes in gap junction protein (connexin 32) gene expression during rat liver carcinogenesis. J Cell Biochem 1989;41:97-102.
78. Temme A, Buchmann A, Gabriel HD, Nelles E, Schwarz M, Willecke K. High incidence of spontaneous and chemically induced liver tumors in mice deficient for connexin32. Curr Biol 1997;7: 713-716.