A defect in a single allele of the Mlh1 gene causes dissociation of the killing and tumorigenic actions of an alkylating carcinogen in methyltransferase-deficient mice

Carcinogenesis

Volumn 21, Issue 2, 2000, Pages 301-305

  Kawate, Hisaya ^a,b   Itoh, Riyoko ^a,e   Sakumi, Kunihiko ^a   Nakabeppu, Yusaku ^a   Tsuzuki, Teruhisa ^b   Ide, Fumio ^c   Ishikawa, Takatoshi ^c   Noda, Tetsuo ^d   Nawata, Hajime ^b   Sekiguchi, Mutsuo ^e  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

^d CANCER INSTITUTE   (Japan)

^e FUKUOKA DENTAL COLLEGE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; CARCINOGEN; METHYLNITROSOUREA; METHYLTRANSFERASE; PROTEIN;

ALLELE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CARCINOGENESIS; CONTROLLED STUDY; DNA REPAIR; ENZYME DEFICIENCY; GENE EXPRESSION; GENE MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; THYMUS LYMPHOMA; TUMOR; TUMOR GROWTH;

EID: 0033955906     PISSN: 01433334     EISSN: None     Source Type: Journal    
DOI: 10.1093/carcin/21.2.301     Document Type: Article

References (38)

1. Loveless, A. (1969) Possible relevance of O-6 alkylation of deoxyguanosine to the mutagenicity and carcinogenicity of nitrosamines and nitrosamides. Nature, 223, 206-207.
2. 6-ethylguanine in rat-brain DNA: correlation with nervous system-specific carcinogenesis by ethylnitrosourea. Proc. Natl Acad. Sci. USA, 71, 639-643.
3. Coulonidre, C. and Miller, J.H. (1977) Genetic studies of the lac repressor. IV. Mutagenic specificity in the lacl gene of Escherichia coli. J. Mol. Biol., 117, 577-606.
4. Ito, T., Nakamura, T., Maki, H. and Sekiguchi, M. (1994) Roles of transcription and repair in alkylation mutagenesis. Mutat. Res., 314, 273-285.
5. 6-methylguanine-DNA methyltransferase. J. Biol. Chem., 257, 13776-13780.
6. Sekiguchi, M., Nakabeppu, Y., Sakumi, K. and Tsuzuki, T. (1996) DNA-repair methyltransferase as a molecular device for preventing mutation and cancer. J. Cancer Res. Clin. Oncol., 122, 199-206.
7. 4-methylthymine in DNA. Carcinogenesis, 16, 1595-1602.
8. 6-alkylguanine-DNA alkyltransferase activity based on cellular DNA content in human, rat and mouse tissues. Carcinogenesis, 7, 745-749.
9. Ishibashi, T. Nakabeppu, Y., Kawate, H., Sakumi, K., Hayakawa, H. and Sekiguchi, M. (1994) Intracellular localization and function of DNA repair methyltransferase in human cells. Mutat. Res., 315, 199-212.
10. Day, R.S., Ziolkowski, C.H., Scudiero, D.A., Meyer, S.A., Lubiniecki, A.S., Girardi, A.J., Galloway, S.M. and Bynum, G.D. (1980) Defective repair of alkylated DNA by human tumour and SV40-transformed human cell strains. Nature, 288, 724-727.
11. 6-methylguanine DNA methyltransferase (MGMT) gene correlates with MGMT expression in human glioma cells. J. Biol. Chem., 269, 17228-17237.
12. 6-methylguanine-DNA methyltransferase hy promoter hypermethylation is a common event in primary human neoplasia. Cancer Res., 59, 793-797.
13. 6-methylguanine-DNA methyltransferase. Mutat. Res., 293, 119-132.
14. 6-methylguanine-DNA methyltransferase. Carcinogenesis, 13, 289-296.
15. Iwakuma, T., Shiraishi, A., Fukuhara, M., Kawate, H. and Sekiguchi, M. (1996) Organization and expression of the mouse gene for DNA repair methyltransferase. DNA Cell Biol., 15, 863-872.
16. Tsuzuki, T., Sakumi, K., Shiraishi, A., Kawate, H., Igarashi, H., Iwakuma, T., Tominaga, Y., Zhang, S., Shimizu, S., Ishikawa, T., Nakamura, K., Nakao, K., Katsuki, M. and Sekiguchi, M. (1996) Targeted disruption of the DNA repair methyltransferase gene renders mice hypersensitive to alkylating agent. Carcinogenesis, 17, 1215-1220.
17. Sakumi, K., Shiraishi, A., Shimizu, S., Tsuzuki, T., Ishikawa, T. and Sekiguchi, M. (1997) Methylnitrosourea-induced tumorigenesis in MGMT gene knockout mice. Cancer Res., 57, 2415-2418.
18. Iwakuma, T., Sakumi, K., Nakatsuru, Y., Kawate, H., Igarashi, H., Shiraishi, A., Tsuzuki, T., Ishikawa, T. and Sekiguchi, M. (1993) High incidence of nitrosamine-induced tumorigenesis in mice lacking DNA repair methyltransferase. Carcinogenesis, 18, 1631-1635.
19. Branch, P., Aquilina, G., Bignami, M. and Karran, P. (1993) Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature, 362, 652-654.
20. Kat, A., Thilly, W.G., Fang, W.H., Longley, M.J., Li, G.M. and 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.
21. de Wind, N., Dekker, M., Berns, A., Radman, M. and te Riele, H. (1995) Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination and predisposition to cancer. Cell, 82, 321-330.
22. Kawate, H., Sakumi, K., Tsuzuki, T., Nakatsuru, Y., Ishikawa, T., Takahashi, S., Takano, H., Noda, T. and Sekiguchi, M. (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.
23. de Wind, N., Dekker, M., van Rossum, A., van der Valk, M. and te Riele, H. (1998) Mouse models for hereditary nonpolyposis colorectal cancer. Cancer Res., 58, 248-255.
24. Prolla, T.A., Baker, S.M., Harris, A.C., Tsao, J.L., Yao, X., Bronner, C.E., Zheng, B., Gordon, M., Reneker, J., Arnheim, N., Shibata, D., Bradley, A. and Liskay, R.M. (1998) Tumour susceptibility and spontaneous mutation in mice deficient in Mlhl, Pmsl and Pms2 DNA mismatch repair. Nature Genet., 18, 276-279.
25. Leach, F.S., Nicolaides, N.C., Papadopoulos, N., Liu, B., Jen, J., Parsons, R., Peltomäki, P., Sistonen, P., Aaltonen, L.A., Nystrom-Lahti, M., Guan, X.-Y., Zhang, J., Meltzer, P.S., Yu, J.-W., Kao, F.-T., Chen, D.J., Cerosaletti, K.M., Fournier, R.E.K., Todd, S., Lewis, T., Leach, R.J., Naylor, S.L., Weissenbach, J., Mecklin, J.-P., Jarvinen, H., Petersen, G.M., Hamilton, S.R., Green, J., Jass, J., Watson, P., Lynch, H.T., Trent, J.M., de la Chapelle, A., Kinzler, K.W. and Vogelstein, B. (1993) Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell, 75, 1215-1225.
26. Bronner, C.E., Baker, S.M., Morrison, P.T., Warren, G., Smith, L.G., Lescoe, M.K., Kane, M., Earabino, C., Lipford, J., Lindblom, A., Tannergard, P. Bollag, R.J., Godwin, A.R., Ward, D.C., Nordenskjold, M., Fishel, R., Kolodner, R. and Liskay, R.M. (1994) Mutation in the DNA mismatch repair gene homologue hMLHI is associated with hereditary non-polyposis colon cancer. Nature, 368, 258-261.
27. Papadopoulos, N., Nicolaides, N.C., Wei, Y.F., Ruben, S.M., Carter, K.C., Rosen, C.A., Haseltine, W.A., Fleischmann, R.D., Fraser, C.M., Adams, M.D., Venter, J.C., Hamilton, S.R., Petersen, G.M., Watson, P., Lynch, H.T., Peltomäki, P. Mecklin, J.-P. de la Chapelle, A., Kinzler, K.W. and Vogelstein, B. (1994) Mutation of a mutL homolog in hereditary colon cancer. Science, 263, 1625-1629.
28. Kolodner, R.D., Hall, N.R., Lipford, J., Kane, M.F., Morrison, P.T., Finan, P.J., Burn, J., Chapman, P., Earabino, C., Merchant, E. and Bishop, T. (1995) Structure of the human MLHI locus and analysis of a large hereditary nonpolyposis colorectal carcinoma kindred for mlhl mutations. Cancer Res., 55, 242-248.
29. Modrich, P. and Lahue, R. (1996) Mismatch repair in replication fidelity, genetic recombination and cancer biology. Annu. Rev. Biochem., 65, 101-133.
30. Papadopoulos, N. and Lindblom, A. (1997) Molecular basis of HNPCC: mutations of MMR genes. Hum. Mutat., 10, 89-99.
31. Jirieny, J. (1998) Eukaryotic mismatch repair: an update. Mutat. Res., 409, 107-121.
32. 6-methylguanine-DNA methyltransferase activity revealed by saturation mutagenesis with negative and positive screening. Mol. Gen. Genet., 243, 379-389.
33. Koera, K., Nakamura, K., Nakao, K., Miyoshi, J., Toyoshima, K., Hatta, T., Otani, H., Aiba, A. and Katsuki, M. (1997) K-ras is essential tor the development of the mouse embryo. Oncogene, 15, 1151-1158.
34. Newcomb, E.W., Steinberg, J.J. and Pellicer, A. (1988) ras oncogenes and phenotypic staging in N-methylnitrosourea-and gamma-irradiation-induced thymic lymphomas in C57BL/6J mice. Cancer Res., 48, 5514-5521.
35. Romach, E., Moore, J., Rummel, S. and Richie, E. (1994) Influence of sex and carcinogen treatment protocol on tumor latency and frequency of K-ras mutations in N-methyl-N-nitrosourea-induced lymphomas. Carcinogenesis, 15, 2275-2280.
36. Tominaga, Y., Tsuzuki, T., Shiraishi, A., Kawate, H. and Sekiguchi, M. (1997) Alkylation-induced apoptosis of embryonic stem cells in which the gene for DNA-repair, methyltransferase, had been disrupted by gene targeting. Carcinogenesis, 18, 889-896.
37. Edelmann, W., Yang, K., Kuraguchi, M., Heyer, J., Lia, M., Kneitz, B., Fan, K., Brown, A.M., Lipkin, M. and Kucherlapati, R. (1999) Tumorigenesis in Mlhl and MlhllApc1638N mutant mice. Cancer Res., 59, 1301-1307.
38. Shcherbakova, P.V. and Kunkel, T.A. (1999) Mutator phenotypes conferred by MLHI overexpression and by heterozygosity for mlhl mutations. Mol. Cell. Biol., 19, 3177-3183.