Defective DNA strand break repair causes chromosomal instability and accelerates liver carcinogenesis in mice

Hepatology

Volumn 47, Issue 6, 2008, Pages 2078-2088

  Teoh, Narci C ^a   Yock, Young Dan ^b   Swisshelm, Karen ^c   Lehman, Stacey ^c   Wright, Jocelyn H ^c   Haque, Jamil ^c   Gu, Yansong ^c   Fausto, Nelson ^c  

^a The Australian National University   (Australia)

^b NATIONAL UNIVERSITY HOSPITAL   (Singapore)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATR PROTEIN; AURORA A KINASE; CELL NUCLEUS ANTIGEN; CYCLIN D1; PROTEIN P53; ACTIN; AURORA KINASE; CARCINOGEN; DIETHYLNITROSAMINE; DNA BINDING PROTEIN; HISTONE; KU ANTIGEN; MDM2 PROTEIN, MOUSE; PROTEIN MDM2; PROTEIN SERINE THREONINE KINASE; UBIQUITIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL PROLIFERATION; CHROMOSOMAL INSTABILITY; CONTROLLED STUDY; DISEASE ASSOCIATION; DNA STRAND BREAKAGE; KARYOTYPE; LIVER CARCINOGENESIS; LIVER CELL; LIVER CELL CARCINOMA; LIVER TUMOR; MALE; MITOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UBIQUITINATION; ANIMAL; CELL CULTURE; CHEMICALLY INDUCED DISORDER; DISEASE MODEL; DOUBLE STRANDED DNA BREAK; GENETICS; METABOLISM; MOUSE MUTANT; PATHOLOGY;

ACTINS; ANIMALS; ANTIGENS, NUCLEAR; CARCINOGENS; CARCINOMA, HEPATOCELLULAR; CELL PROLIFERATION; CELLS, CULTURED; CHROMOSOMAL INSTABILITY; DIETHYLNITROSAMINE; DISEASE MODELS, ANIMAL; DNA BREAKS, DOUBLE-STRANDED; DNA-BINDING PROTEINS; HEPATOCYTES; HISTONES; LIVER NEOPLASMS; MALE; MICE; MICE, KNOCKOUT; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-MDM2; TUMOR SUPPRESSOR PROTEIN P53; UBIQUITIN;

EID: 46249134069     PISSN: 02709139     EISSN: None     Source Type: Journal    
DOI: 10.1002/hep.22194     Document Type: Article

References (47)

1. Bruix J, Boix J, Sala M, Llovet JM. Focus on hepatocellular carcinoma. Cancer Cell 2004;5:215-219.
2. Bosch FX, Riles J, Diaz M, Cleries R. Primary liver cancer worldwide incidence and trends. Gastroenterology 2004;127:S5-S16.
3. Nishimura T, Nishida N, Komeda T, Fukuda Y, Nakao K. Genotype stability and clonal evolution of hepatocellular carcinoma assessed by autopsy-based genome-wide microsatellite analysis. Cancer Genet Cytogenet 200;161:164-169.
4. Fausto N. Mouse liver tumorigenesis: models, mechanisms and relevance to human disease. Semin Liver Dis 1999;19:243-252.
5. Aihara T, Noguchi S, Sasaki Y, Nakano H, Monden M, Imaoka S. Clonal analysis of precancerous lesions of hepatocellular carcinoma. Gastroenterology 1996;111:455-461.
6. 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.
7. Geissler M. Molecular mechanisms of hepatocarcinogenesis. In: Liver Cancer. Edinburgh, UK: Churchill Livingstone; 1997:59-88.
8. Khanna KK, Jackson SP. DNA double-strand breaks: signaling, repair and the cancer connection. Nat Genet 2001;27:247-254.
9. Van Gent DC, Hoeijmakers JHJ, Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat Rev Genet 2001;2:196-206.
10. Gu Y, Seidl K, Rathbun GA, Zhu C, Manis JP, van der Stoep N, et al. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity 1997;7:653-665.
11. Durocher D, Jackson SP. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr Opin Cell Biol 2001;13:225-231.
12. Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003;3:155-168.
13. Pierce RH, Vail ME, Ralph L, Campbell JS, Fausto N. Bcl-2 expression inhibits liver carcinogenesis and delays the development of proliferating foci. Am J Pathol 2002;160:1550-1560.
14. Franklin CC, Krejsa CM, Pierce RH, White CC, Fausto N, Kavanagh TJ. Caspase-3-dependent cleavage of the glutamate-L-cysteine ligase catalytic subunit during apoptotic cell death. Am J Pathol 2002;160;1887-1894.
15. Strahl BD, Allis CD. The language of covalent histone modifications. Nature 2000;403:41-45.
16. Vogelstein B, Lane D, Levine AJ. Surfing the p53 network. Nature 2000;408:307-310.
17. Vousden KH, Lu X. Live or let die: The cell's response to p53. Nat Rev Cancer 2002;2:594-604.
18. Meraldi P, Honda R, Nigg EA. Aurora kinases link chromosome segregation and cell division to cancer susceptibility. Curr Opin Genet Dev 2004;14:29-36.
19. Carmena M, Earnshaw WC. The cellular geography of Aurora kinases. Nature 2003;4:842-854.
20. Meraldi P, Honda R, Nigg E. Aurora A overexpression reveals tetraploidization as a major route to centrosome amplification in p53-/- cells. EMBO J 2002;21:483-492.
21. Lee J-S, Chu I-S, Mikaelyan A, Calvisi DF, Heo J, Reddy JK, et al. Application of comparative functional genomics to identify best-fit mouse models to study human cancer. Nat Genet 2004;36:1306-1311.
22. Zimonjic DB, Keck CL, Thorgeisson SS, Popescu NC. Novel current genetic imbalances in human hepatocellular carcinoma cell lines identified by comparative genomic hybridisation. HEPATOLOGY 1999;29:1208-1214.
23. Collis SJ, De Weese TL, Jeggo PA, Parker AR. The life and death of DNA-PK. Oncogene 2005;24:949-961.
24. Sengupta S, Harris CC. p53: traffic cop at the crossroads of DNA repair and recombination. Nat Rev Mol Cell Biol 2005;6:44-55.
25. Bellamy COC, Clarke AR, Wyllie AH, Harrison DJ. p53 deficiency in liver reduces local control of survival and proliferation, but does not affect apoptosis after DNA damage. FASEB J 1997;11:591-599.
26. Michael D, Oren M. The p53-mdm2 module and the ubiquitin system. Semin Cancer Biol 2003;13:49-58.
27. Zhou BP, Liao Y, Xia W, Zou Y, Spohn B, Hung MC. HER-2/neu induces p53 ubiquitination via Akt-mediated Mdm2 phosphorylation. Nat Cell Biol 2001;3:973-982.
28. Muller S, Ledl A, Schmidt D. SUMO: a regulator of gene expression and genome integrity. Oncogene 2004;23:1998-2008.
29. Moschos SJ, Mo YY. Role of SUMO/Ubc9 in DNA damage repair and tumorigenesis. J Mol Histol 2006;37:309-319.
30. Lee CG, Ren J, Cheong IS, Ban HK, Ooi LL, Yong Tan S, et al. Expression of FAT10 gene is highly upregulated in hepatocellular carcinoma and other gastrointestinal and gynecological cancers. Oncogene 2003;22:2592-2603.
31. Lim CB, Zhang D, Lee CGL. FAT10, a gene upregulated in various cancers, is cell-cycle regulated. Cell Div 2006;1:20.
32. Ren J, Kan A, Leong SH, London LPJO, Jeang KT, Chong SS, et al. FAT10 plays a role in the regulation of chromosomal stability. J Biol Chem 2006;281:11413-11421.
33. Princiotta MF, Schubert U, Chen W, Bennick JR, Myung J, Crews CM, et al. Cells adapted to proteasome inhibitor 4-hydroxy-5-iodo-3-nitrophenylacetyl-Leu- Leu-leucinal-vinyl sulfone require enzymatically active proteasomes for continued survival. Proc Natl Acad Sci U S A 2001;98:513-518.
34. Vassilev LT, Binh TV, Graves B, Carvajal D, Podlaski F, Filipovic Z, et al. In vivo activation of the p53 pathway by small-molecule antagonists of MDM2. Science 2003;303:844-848.
35. Barak Y, Juven T, Haffner R, Oren M. Mdm2 expression is induced by wildtype p53 activity. EMBO J 1993;12:46-68.
36. Finnberg N, Silins I, Stenius U, Hogberg J. Characterizing the role of MDM2 in diethlynitrosamine induced acute liver damage and development of pre-neoplastic lesions. Carcinogenesis 2004;25:113-122.
37. Momand J, Zambettie GP, Olson DC, George D, Levine AJ. The Mdm2 oncogene product forms a complex with the p53 protein and inhibits p53-mediated transactivation. Cell 1992;69:1237-1245.
38. Inoue T, Geyer RK, Yu ZK, Maki CG. MDM2 can promote the ubiquitination, nuclear export, and degradation of p53 in the absence of direct binding. J Biol Chem 2001;276:45255-45260.
39. Vousden KH, Prives C. p53 and prognosis: new insights and further complexity. Cell 2005;120:7-10.
40. Van Gijssell HE, Ohlson LCE, Torndal U-B, Mulder GJ, Eriksson LC, Porsch-Hällstöm I, et al. Loss of nuclear p53 protein in preneoplastic rat hepatocytes is accompanied by Mdm2 and Bcl-2 overexpression and by defective response to DNA damage in vivo. HEPATOLOGY 2000;32:701-710.
41. Staib F, Hussain P, Hofseth LJ, Wang XW, Harris CC. TP53 and liver carcinogenesis. Hum Mutat 2003;21:201-216.
42. Kress S, Konig J, Schweizer J, Lohrke, H, Bauer-Hossman R, Schwarz M. p53 mutations are absent from carcinogen-induced liver tumors but occur in cell lines established from these tumors. Mol Carcinog 1992;6:148-158.
43. Sandgren EP. Transgenic models of hepatic growth regulation and hepatocarcinogenesis. In Liver Regeneration and Carcinogenesis. San Diego, CA: Academic Press; 1995:257-300.
44. Marx J. Building better mouse models for studying cancer. Science 2003;299:1972-1975.
45. Feldser DM, Hackett JA, Greider CW. Telomere dysfunction and the initiation of genome instability. Nat Rev Cancer 2003;3:623-627.
46. Yang Y, Li CC, Weissman AM. Regulating the p53 system through ubiquitination. Oncogene 2004;23:2096-2106.
47. Shirahashi H, Sakaida I, Terai S, Hironaka K, Kusano N, Okita K. Ubiquitin is a possible new predictive marker for the recurrence of human hepatocellular carcinoma. Liver 2002;22:413-418.