Activation of the canonical Wnt/β-catenin pathway confers growth advantages in c-Myc/E2F1 transgenic mouse model of liver cancer

Journal of Hepatology

Volumn 42, Issue 6, 2005, Pages 842-849

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

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

Catenin; C Myc; E2F1; Hepatic tumors; Transgenic mouse models

Indexed keywords

AXIN; BETA CATENIN; FRIZZLED PROTEIN; FRIZZLED PROTEIN 1; FRIZZLED PROTEIN 2; GLUTAMATE AMMONIA LIGASE; GLUTAMATE TRANSPORTER; GLYCOGEN SYNTHASE KINASE 3BETA; MYC PROTEIN; PROTEIN; PROTEIN DISHEVELLED 1; PROTEIN WISP 1; UNCLASSIFIED DRUG; VESICULAR GLUTAMATE TRANSPORTER 1; WNT1 PROTEIN;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER GROWTH; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; ENZYME INACTIVATION; GENE LOCUS; GENE MUTATION; GENE TARGETING; INTERMETHOD COMPARISON; LIVER CANCER; LIVER CARCINOGENESIS; MICROSATELLITE INSTABILITY; MICROSATELLITE MARKER; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; STATISTICAL SIGNIFICANCE; TRANSGENIC MOUSE; TUMOR VOLUME; WESTERN BLOTTING;

ANIMALS; BETA CATENIN; CELL CYCLE PROTEINS; CELL DIVISION; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; DNA-BINDING PROTEINS; E2F TRANSCRIPTION FACTORS; E2F1 TRANSCRIPTION FACTOR; FEMALE; GENE EXPRESSION PROFILING; GENES, MYC; GLYCOGEN SYNTHASE KINASE 3; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; LIVER NEOPLASMS, EXPERIMENTAL; MALE; MICE; MICE, TRANSGENIC; MICROSATELLITE REPEATS; PRECANCEROUS CONDITIONS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; WNT PROTEINS; WNT1 PROTEIN;

EID: 18844402131     PISSN: 01688278     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhep.2005.01.029     Document Type: Article

References (57)

1. J.W. Harbour, and D.C. Dean The Rb/E2F pathway: expanding roles and emerging paradigms Genes Dev 14 2000 2393 2409
2. R.A. Weinberg The retinoblastoma protein and cell cycle control Cell 81 1995 323 330
3. J.R. Nevins E2F: a link between the Rb tumor suppressor protein and viral oncoproteins Science 258 1992 424 429
4. E. Tabor Tumor suppressor genes, growth factor genes, and oncogenes in hepatitis B virus-associated hepatocellular carcinoma J Med Virol 42 1994 357 365
5. T. Moroy, A. Marchio, J. Etiemble, C. Trepo, P. Tiollais, and M.A. Buendia Rearrangement and enhanced expression of c-myc in hepatocellular carcinoma of hepatitis virus infected woodchucks Nature 324 1986 76 279
6. H. Murakami, N.D. Sanderson, P. Nagy, P.A. Marino, G. Merlino, and S.S. Thorgeirsson 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 53 1993 1719 1723
7. E.A. Conner, E.R. Lemmer, M. Omori, P.J. Wirth, V.M. Factor, and S.S. Thorgeirsson Dual functions of E2F-1 in a transgenic mouse model of liver carcinogenesis Oncogene 19 2000 5054 5062
8. T.K. Blackwell, L. Kretzner, E.M. Blackwood, R.N. Eisenman, and H. Weintraub Sequence-specific DNA binding by the c-Myc protein Science 250 1990 149 151
9. E.M. Blackwood, and R.N. Eisenman Max: a helix-loop-helix zipper protein that forms a sequence-specific DNA-binding complex with Myc Science 251 1991 1211 1217
10. N. Dyson The regulation of E2F by pRB-family proteins Genes Dev 12 1998 2245 2262
11. J.R. Nevins, G. Leone, J. DeGregori, and L. Jakoi Role of the Rb/E2F pathway in cell growth control J Cell Physiol 173 1997 233 236
12. J. DeGregori, G. Leone, A. Miron, L. Jakoi, and J.R. Nevins Distinct roles for E2F proteins in cell growth control and apoptosis Proc Natl Acad Sci USA 94 1997 7245 7250
13. D.G. Johnson, J.K. Schwarz, W.D. Cress, and J.R. Nevins Expression of transcription factor E2F1 induces quiescent cells to enter S phase Nature 365 1993 349 352
14. L. Kaczmarek, J.K. Hyland, R. Watt, M. Rosenberg, and R. Baserga Microinjected c-myc as a competence factor Science 228 1985 1313 1315
15. H. Hermeking, and D. Eick Mediation of c-Myc-induced apoptosis by p53 Science 265 1994 2091 2093
16. T.F. Kowalik, J. DeGregori, G. Leone, L. Jakoi, and J.R. Nevins E2F1-specific induction of apoptosis and p53 accumulation, which is blocked by Mdm2 Cell Growth Differ 9 1998 13 118
17. X. Wu, and A.J. Levine p53 and E2F-1 cooperate to mediate apoptosis Proc Natl Acad Sci USA 91 1994 3602 3606
18. S.W. Hiebert, M. Lipp, and J.R. Nevins E1A-dependent trans-activation of the human MYC promoter is mediated by the E2F factor Proc Natl Acad Sci USA 86 1989 3594 3598
19. G. Leone, R. Sears, E. Huang, R. Rempel, F. Nuckolls, and C.H. Park Myc requires distinct E2F activities to induce S phase and apoptosis Mol Cell 8 2001 105 113
20. M.J. Elliott, Y.B. Dong, H. Yang, and K.M. McMasters E2F-1 up-regulates c-Myc and p14 (ARF) and induces apoptosis in colon cancer cells Clin Cancer Res 7 2001 3590 3597
21. E. Santoni-Rugiu, D. Duro, T. Farkas, I.S. Mathiasen, M. Jaattela, and J. Bartek E2F activity is essential for survival of Myc-overexpressing human cancer cells Oncogene 21 2002 6498 6509
22. Z. You, D. Saims, S. Chen, Z. Zhang, D.C. Guttridge, and K.L. Guan Wnt signaling promotes oncogenic transformation by inhibiting c-Myc-induced apoptosis J Cell Biol 157 2002 429 440
23. A. De La Coste, B. Romagnolo, P. Billuart, C.A. Renard, M.A. Buendia, and O. Soubranes Somatic mutations of the beta-catenin gene are frequent in mouse and human hepatocellular carcinomas Proc Natl Acad Sci USA 95 1998 8847 8851
24. D.F. Calvisi, V.M. Factor, R. Loi, and S.S. Thorgeirsson Activation of beta-catenin during hepatocarcinogenesis in transgenic mouse models: relationship to phenotype and tumor grade Cancer Res 61 2001 2085 2091
25. Y. Miyoshi, K. Iwao, Y. Nagasawa, T. Aihara, Y. Sasaki, and S. Imaoka Activation of the β-catenin gene in primary hepatocellular carcinomas by somatic alterations involving Exon 3 Cancer Res 58 1998 2524 2527
26. P. Polakis The oncogenic activation of β-catenin Curr Opin Genet Dev 9 1999 15 21
27. S. Munemitsu, I. Albert, B. Souza, B. Rubinfeld, and P. Polakis Regulation of intracellular β-catenin levels by the adenomatous polyposis coli (APC) tumor-suppressor protein Proc Natl Acad Sci USA 92 1995 3046 3050
28. S. Ikeda, S. Kishida, H. Yamamoto, H. Murai, S. Koyama, and A. Kikuchi Axin, a negative regulator of the Wnt signaling pathway, forms a complex with GSK-3beta and beta-catenin and promotes GSK-3beta-dependent phosphorylation of beta-catenin Eur Mol Biol Org J 17 1998 1371 1384
29. J. Behrens, B.A. Jerchow, M. Wurtele, J. Grimm, C. Asbrand, and R. Wirtz Functional interaction of an axin homolog, conductin, with beta-catenin, APC, and GSK3beta Science 280 1998 596 599
30. P. Polakis More than one way to skin a catenin Cell 105 2001 563 566
31. E.A. Conner, E.R. Lemmer, A. Sanchez, V.M. Factor, and S.S. Thorgeirsson E2F1 blocks and c-Myc accelerates hepatic ploidy in transgenic mouse models Biochem Biophys Res Commun 302 2003 114 120
32. M.M. Simile, M.R. De Miglio, M.R. Muroni, M. Frau, G. Asara, and S. Serra Down-regulation of c-myc and Cyclin D1 genes by antisense oligodeoxy nucleotides inhibits the expression of E2F1 and in vitro growth of HepG2 and Morris 5123 liver cancer cells Carcinogenesis 25 2004 333 341
33. D.F. Calvisi, V.M. Factor, S. Ladu, E.A. Conner, and S.S. Thorgeirsson Disruption of beta-catenin pathway or genomic instability define two distinct categories of liver cancer in transgenic mice Gastroenterology 126 2004 1374 1386
34. C.H. Frith, J.M. Ward, and V.S. Turusov Tumours of the liver V. Turusov U. Mohr Pathology of tumours in laboratory animals vol. 2 1994 IARC Scientific Publications Lyon, France 223 270
35. P.W. Laird, A. Zijderveld, K. Linders, M.A. Rudnicki, R. Jaenisch, and A. Berns Simplified mammalian DNA isolation procedure Nucleic Acids Res 19 1991 4293
36. H. Aydinlik, T.D. Nguyen, O. Moennikes, A. Buchmann, and M. Schwarz Selective pressure during tumor promotion by phenobarbital leads to clonal outgrowth of beta-catenin mutated mouse liver tumors Oncogene 20 2001 7812 7816
37. D. Yan, M. Wiesmann, M. Rohan, V. Chan, A.B. Jefferson, and L. Guo Elevated expression of axin2 and hnkd mRNA provides evidence that Wnt/beta-catenin signaling is activated in human colon tumors Proc Natl Acad Sci USA 98 2001 14973 14978
38. B. Lustig, B. Jerchow, M. Sachs, S. Weiler, T. Pietsch, and U. Karsten Negative feedback loop of Wnt signaling through upregulation of conductin/axin2 in colorectal and liver tumors Mol Cell Biol 22 2002 1184 1193
39. J.Y. Leung, F.T. Kolligs, R. Wu, Y. Zhai, R. Kuick, S. Hanash, and K.R. Cho Activation of AXIN2 expression by beta-catenin/TCF: a feedback repressor pathway regulating Wnt signaling J Biol Chem 277 2002 21657 21665
40. J. Papkoff, B. Rubinfeld, B. Schryver, and P. Polakis Wnt-1 regulates free pools of catenins and stabilizes APC-catenin complexes Mol Cell Biol 16 1996 2128 2134
41. D. Cook, M.J. Fry, K. Hughes, R. Sumathipala, J.R. Woodgett, and T.C. Dale Wingless inactivates glycogen synthase kinase-3 via an intracellular signalling pathway which involves a protein kinase C Eur Mol Biol Org J 15 1996 4526 4536
42. S. Chen, D.C. Guttridge, Z. You, Z. Zhang, A. Fribley, and M.W. Mayo Wnt-1 signaling inhibits apoptosis by activating beta-catenin/T cell factor-mediated transcription J Cell Biol 152 2001 87 96
43. H.S. Melkonyan, W.C. Chang, J.P. Shapiro, M. Mahadevappa, P.A. Fitzpatrick, and M.C. Kiefer SARPs: a family of secreted apoptosis-related proteins Proc Natl Acad Sci USA 94 1997 13636 13641
44. A. Cadoret, C. Ovejero, B. Terris, E. Souil, L. Levy, and W.H. Lamers New targets of beta-catenin signaling in the liver are involved in the glutamine metabolism Oncogene 21 2002 8293 8301
45. A. Cadoret, C. Ovejero, S. Saadi-Kheddouci, E. Souil, M. Fabre, and B. Romagnolo Hepatomegaly in transgenic mice expressing an oncogenic form of beta-catenin Cancer Res 61 2001 3245 3249
46. C.H. Anna, M. Iida, R.C. Sills, and T.R. Devereux Expression of potential beta-catenin targets, cyclin D1, c-Jun, c-Myc, E-cadherin, and EGFR in chemically induced hepatocellular neoplasms from B6C3F1 mice Toxicol Appl Pharmacol 190 2003 135 145
47. S. Colnot, T. Decaens, M. Niwa-Kawakita, C. Godard, G. Hamard, and A. Kahn Liver-targeted disruption of Apc in mice activates beta-catenin signaling and leads to hepatocellular carcinomas Proc Natl Acad Sci USA 101 2004 17216 17221
48. K. Yasui, H. Okamoto, S. Arii, and J. Inazawa Association of over-expressed TFDP1 with progression of hepatocellular carcinomas J Hum Genet 48 2003 609 613
49. S.Y. Peng, P.L. Lai, and M.C. Hsu Activation of the c-myc gene in human hepatocellular carcinoma: biologic significance J Formos Med Assoc 92 1993 866 870
50. E. Santoni-Rugiu, M.R. Jensen, and S.S. Thorgeirsson Disruption of the pRb/E2F pathway and inhibition of apoptosis are major oncogenic events in liver constitutively expressing c-myc and transforming growth factor alpha Cancer Res 58 1998 123 134
51. R.M. Pascale, M.M. Simile, M.R. De Miglio, M.R. Muroni, D.F. Calvisi, and G. Asara Cell cycle deregulation in liver lesions of rats with and without genetic predisposition to hepatocarcinogenesis Hepatology 35 2002 1341 1350
52. K. Taniguchi, L.R. Roberts, I.N. Aderca, X. Dong, C. Qian, and L.M. Murphy Mutational spectrum of beta-catenin, AXIN1, and AXIN2 in hepatocellular carcinomas and hepatoblastomas Oncogene 21 2002 4863 4871
53. Y. Ishizaki, S. Ikeda, M. Fujimori, Y. Shimizu, T. Kurihara, and T. Itamoto Immunohistochemical analysis and mutational analyses of beta-catenin, Axin family and APC genes in hepatocellular carcinomas Int J Oncol 24 2004 1077 1083
54. H. Suzuki, D.N. Watkins, K.W. Jair, K.E. Schuebel, S.D. Markowitz, and W. Dong Chen Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer Nat Genet 36 2004 417 422
55. S.P. Monga, H.K. Monga, X. Tan, K. Mule, P. Pediaditakis, and G.K. Michalopoulos Beta-catenin antisense studies in embryonic liver cultures: role in proliferation, apoptosis, and lineage specification Gastroenterology 124 2003 202 216
56. N. Harada, H. Miyoshi, N. Murai, H. Oshima, Y. Tamai, and M. Oshima Lack of tumorigenesis in the mouse liver after adenovirus-mediated expression of a dominant stable mutant of beta-catenin Cancer Res 62 2002 1971 1977
57. D.F. Calvisi, S. Ladu, V.M. Factor, and S.S. Thorgeirsson Activation of β-catenin provides proliferative and invasive advantages in c-myc/TGF-α hepatocarcinogenesis promoted by phenobarbital Carcinogenesis 25 2004 901 908