Alkylation-induced colon tumorigenesis in mice deficient in the Mgmt and Msh6 proteins

Oncogene

Volumn 28, Issue 5, 2009, Pages 734-741

  Bugni, J M ^a   Meira, L B ^a   Samson, L D ^a  

^a Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Azoxymethane; Colorectal cancer; Mgmt; Mismatch repair; Msh6

Indexed keywords

APC PROTEIN; AZOXYMETHANE; DEXTRAN SULFATE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; PROTEIN MSH6;

ALKYLATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COLON CARCINOGENESIS; COLORECTAL ADENOMA; CONTROLLED STUDY; FEMALE; GENE INTERACTION; GENE MUTATION; GENETIC ASSOCIATION; MALE; MISMATCH REPAIR; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR SUPPRESSOR GENE;

ALKYLATING AGENTS; ALKYLATION; ANIMALS; APOPTOSIS; AZOXYMETHANE; CARCINOGENS; CARCINOMA; COLONIC NEOPLASMS; DEXTRAN SULFATE; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; GENES, APC; GENETIC PREDISPOSITION TO DISEASE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; TUMOR SUPPRESSOR PROTEINS;

MUS;

EID: 59649091620     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2008.426     Document Type: Article

References (43)

1. Acharya S, Wilson T, Gradia S, Kane MF, Guerrette S, Marsischky GT et al. (1996). hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci USA 93: 13629-13634.
2. Aquilina G, Biondo R, Dogliotti E, Meuth M, Bignami M. (1992). Expression of the endogenous O6-methylguanine-DNA-methyltransferase protects Chinese hamster ovary cells from spontaneous G:C to A:T transitions. Cancer Res 52: 6471-6475.
3. -/-;Min mice. Cancer Res 58: 1087-1089.
4. Edelmann W, Yang K, Kuraguchi M, Heyer J, Lia M, Kneitz B et al. (1999). Tumorigenesis in Mlh1 and Mlh1/Apc1638N mutant mice. Cancer Res 59: 1301-1307.
5. Edelmann W, Yang K, Umar A, Heyer J, Lau K, Fan K et al. (1997). Mutation in the mismatch repair gene Msh6 causes cancer susceptibility. Cell 91: 467-477.
6. Esteller M, Corn PG, Baylin SB, Herman JG. (2001). A gene hypermethylation profile of human cancer. Cancer Res 61: 3225-3229.
7. Fang Q, Kanugula S, Pegg AE. (2005). Function of domains of human O6-alkylguanine-DNA alkyltransferase. Biochemistry 44: 15396-15405.
8. Fox EJ, Leahy DT, Geraghty R, Mulcahy HE, Fennelly D, Hyland JM et al. (2006). Mutually exclusive promoter hypermethylation patterns of hMLH1 and O6-methylguanine DNA methyltransferase in colorectal cancer. J Mol Diagn 8: 68-75.
9. Glassner BJ, Weeda G, Allan JM, Broekhof JLM, Carls NHE, Donker I et al. (1999). DNA repair methyltransferase (Mgmt) knockout mice are sensitive to the lethal effects of chemotherapeutic alkylating agents. Mutagenesis 14: 339-347.
10. Haigis KM, Caya JG, Reichelderfer M, Dove WF. (2002). Intestinal adenomas can develop with a stable karyotype and stable microsatellites. Proc Natl Acad Sci USA 99: 8927-8931.
11. Harris LC, Potter PM, Tano K, Shiota S, Mitra S, Brent TP. (1991). Characterization of the promoter region of the human O6-methylguanine-DNA methyltransferase gene. Nucleic Acids Res 19: 6163-6167.
12. Hecht SS. (1999). DNA adduct formation from tobacco-specific N-nitrosamines. Mutat Res 424: 127-142.
13. Hickman MJ, Samson LD. (1999). Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents. Proc Natl Acad Sci USA 96: 10764-10769.
14. Jiricny J. (2006). The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7: 335-346.
15. Kaina B. (2003). DNA damage-triggered apoptosis: critical role of DNA repair, double-strand breaks, cell proliferation and signaling. Biochem Pharmacol 66: 1547-1554.
16. Kaina B, Ziouta A, Ochs K, Coquerelle T. (1997). Chromosomal instability, reproductive cell death and apoptosis induced by O6-methylguanine in Mex-, Mex+ and methylation-tolerant mismatch repair compromised cells: facts and models. Mutat Res 381: 227-241.
17. Karran P, Bignami M. (1992). Self-destruction and tolerance in resistance of mammalian cells to alkylation damage. Nucleic Acids Res 20: 2933-2940.
18. Kat A, Thilly WG, Fang WH, Longley MJ, Li GM, Modrich P. (1993). An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc Natl Acad Sci USA 90: 6424-6428.
19. Kawate H, Sakumi K, Tsuzuki T, Nakatsuru Y, Ishikawa T, Takahashi S et al. (1998). Separation of killing and tumorigenic effects of an alkylating agent in mice defective in two of the DNA repair genes. Proc Natl Acad Sci USA 95: 5116-5120.
20. Kellett M, Potten CS, Rew DA. (1992). A comparison of in vivo cell proliferation measurements in the intestine of mouse and man. Epithelial Cell Biol 1: 147-155.
21. Kohonen-Corish MR, Daniel JJ, te Riele H, Buffinton GD, Dahlstrom JE. (2002). Susceptibility of Msh2-deficient mice to inflammation-associated colorectal tumors. Cancer Res 62: 2092-2097.
22. Kuraguchi M, Yang K, Wong E, Avdievich E, Fan K, Kolodner RD et al. (2001). The distinct spectra of tumor-associated Apc mutations in mismatch repair-deficient Apc1638N mice define the roles of MSH3 and MSH6 in DNA repair and intestinal tumorigenesis. Cancer Res 61: 7934-7942.
23. Larson K, Sahm J, Shenkar R, Strauss B. (1985). Methylation-induced blocks to in vitro DNA replication. Mutat Res 150: 77-84.
24. Lind GE, Thorstensen L, Lovig T, Meling GI, Hamelin R, Rognum TO et al. (2004). A CpG island hypermethylation profile of primary colorectal carcinomas and colon cancer cell lines. Mol Cancer 3: 28.
25. Millar CB, Guy J, Sansom OJ, Selfridge J, MacDougall E, Hendrich B et al. (2002). Enhanced CpG mutability and tumorigenesis in MBD4-deficient mice. Science 297: 403-405.
26. Myrnes B, Norstrand K, Giercksky KE, Sjunneskog C, Krokan H. (1984). A simplified assay for O6-methylguanine-DNA methyltransferase activity and its application to human neoplastic and nonneoplastic tissues. Carcinogenesis 5: 1061-1064.
27. Nagasaka T, Goel A, Notohara K, Takahata T, Sasamoto H, Uchida T et al. (2008). Methylation pattern of the O6-methylguanine-DNA methyltransferase gene in colon during progressive colorectal tumorigenesis. Int J Cancer 122: 2429-2436.
28. Reitmair AH, Cai JC, Bjerknes M, Redston M, Cheng H, Pind MT et al. (1996). MSH2 deficiency contributes to accelerated APC-mediated intestinal tumorigenesis. Cancer Res 56: 2922-2926.
29. Sakumi K, Shiraishi A, Shimizu S, Tsuzuki T, Ishikawa T, Sekiguchi M. (1997). Methylnitrosourea-induced tumorigenesis in MGMT gene knockout mice. Cancer Res 57: 2415-2418.
30. Sandercock LE, Kwok MC, Luchman HA, Mark SC, Giesbrecht JL, Samson LD et al. (2004). Mutational-reporter transgenes rescued from mice lacking either Mgmt, or both Mgmt and Msh6 suggest that O6-alkylguanine-induced miscoding does not contribute to the spontaneous mutational spectrum. Oncogene 23: 5931-5940.
31. Sedgwick B. (1997). Nitrosated peptides and polyamines as endogenous mutagens in O6-alkylguanine-DNA alkyltransferase deficient cells. Carcinogenesis 18: 1561-1567.
32. Sieber OM, Howarth KM, Thirlwell C, Rowan A, Mandir N, Goodlad RA et al. (2004). Myh deficiency enhances intestinal tumorigenesis in multiple intestinal neoplasia (ApcMin/+) mice. Cancer Res 64: 8876-8881.
33. Snow ET, Foote RS, Mitra S. (1984). Base-pairing properties of O6-methylguanine in template DNA during in vitro DNA replication. J Biol Chem 259: 8095-8100.
34. Sohn OS, Fiala ES, Requeijo SP, Weisburger JH, Gonzalez FJ. (2001). Differential effects of CYP2E1 status on the metabolic activation of the colon carcinogens azoxymethane and methylazoxymethanol. Cancer Res 61: 8435-8440.
35. Stojic L, Brun R, Jiricny J. (2004). Mismatch repair and DNA damage signalling. DNA Repair (Amst) 3: 1091-1101.
36. Taniguchi K, Kakinuma S, Tokairin Y, Arai M, Kohno H, Wakabayashi K et al. (2006). Mild inflammation accelerates colon carcinogenesis in Mlh1-deficient mice. Oncology 71: 124-130.
37. Toft NJ, Sansom OJ, Brookes RA, Arends MJ, Wood M, Margison GP et al. (2000). In vivo administration of O(6)-benzylguanine does not influence apoptosis or mutation frequency following DNA damage in the murine intestine, but does inhibit P450-dependent activation of dacarbazine. Carcinogenesis 21: 593-598.
38. Toft NJ, Winton DJ, Kelly J, Howard LA, Dekker M, te Riele H et al. (1999). Msh2 status modulates both apoptosis and mutation frequency in the murine small intestine. Proc Natl Acad Sci USA 96: 3911-3915.
39. Vogelstein B, Kinzler KW. (1993). The multistep nature of cancer. Trends Genet 9: 138-141.
40. Wali RK, Skarosi S, Hart J, Zhang Y, Dolan ME, Moschel RC et al. (1999). Inhibition of O(6)-methylguanine-DNA methyltransferase increases azoxymethane-induced colonic tumors in rats. Carcinogenesis 20: 2355-2360.
41. Xiao W, Samson L. (1993). In vivo evidence for endogenous DNA alkylation damage as a source of spontaneous mutation in eukaryotic cells. Proc Natl Acad Sci USA 90: 2117-2121.
42. (6)-alkylguanine-DNA alkyltransferase. Carcinogenesis 23: 823-830.
43. Zaidi NH, Pretlow TP, O'Riordan MA, Dumenco LL, Allay E, Gerson SL. (1995). Transgenic expression of human MGMT protects against azoxymethane-induced aberrant crypt foci and G to A mutations in the K-ras oncogene of mouse colon. Carcinogenesis 16: 451-456.