Mammalian DNA mismatch repair protects cells from UVB-induced DNA damage by facilitating apoptosis and p53 activation

DNA Repair

Volumn 2, Issue 4, 2003, Pages 427-435

  Peters, Anthea C ^a   Young, Leah C ^a   Maeda, Tomoko ^b   Tron, Victor A ^a,b   Andrew, Susan E ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

Apoptosis; MMR; Mouse embryonic fibroblasts; Msh2; p53 activation; UVB

Indexed keywords

PROTEIN P53;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CELL TRANSFORMATION; CONTROLLED STUDY; DNA DAMAGE; FIBROBLAST; GROWTH INHIBITION; MISMATCH REPAIR; MOUSE; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; ULTRAVIOLET B RADIATION; WILD TYPE;

MAMMALIA;

EID: 0037414342     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1568-7864(03)00003-X     Document Type: Article

References (48)

1. Bellacosa A. Functional interactions and signaling properties of mammalian DNA mismatch repair proteins. Cell Death Differ. 8:2001;1076-1092.
2. Duckett D.R., Drummond J.T., Murchie A.I., Reardon J.T., Sancar A., Lilley D.M., Modrich P. Human MutSalpha recognizes damaged DNA base pairs containing O6-methylguanine, O4-methylthymine, or the cisplatin-d(GpG) adduct. Proc. Natl. Acad. Sci. USA. 93:1996;6443-6447.
3. Reitmair A.H., Risley R., Bristow R.G., Wilson T., Ganesh A., Jang A., Peacock J., Benchimol S., Hill R.P., Mak T.W., Fishel R., Meuth M. Mutator phenotype in Msh2-deficient murine embryonic fibroblasts. Cancer Res. 57:1997;3765-3771.
4. de Wind N., Dekker M., Berns A., Radman M., Te R.H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell. 82:1995;321-330.
5. Mu D., Tursun M., Duckett D.R., Drummond J.T., Modrich P., Sancar A. Recognition and repair of compound DNA lesions (base damage and mismatch) by human mismatch repair and excision repair systems. Mol. Cell Biol. 17:1997;760-769.
6. Gong J.G., Costanzo A., Yang H.Q., Melino G., Kaelin W.G. Jr., Levrero M., Wang J.Y. The tyrosine kinase c-Abl regulates p73 in apoptotic response to cisplatin-induced DNA damage. Nature. 399:1999;806-809.
7. Hickman M.J., Samson L.D. Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents. Proc. Natl. Acad. Sci. USA. 96:1999;10764-10769.
8. Hardman R.A., Afshari C.A., Barrett J.C. Involvement of mammalian MLH1 in the apoptotic response to peroxide-induced oxidative stress. Cancer Res. 61:2001;1392-1397.
9. Ananthaswamy H.N., Loughlin S.M., Cox P., Evans R.L., Ullrich S.E., Kripke M.L. Sunlight and skin cancer: inhibition of p53 mutations in UV-irradiated mouse skin by sunscreens. Nat. Med. 3:1997;510-514.
10. Meyers M., Wagner M.W., Hwang H.S., Kinsella T.J., Boothman D.A. Role of the hMLH1 DNA mismatch repair protein in fluoropyrimidine-mediated cell death and cell cycle responses. Cancer Res. 61:2001;5193-5201.
11. Lan Z., Sever-Chroneos Z., Strobeck M.W., Park C.H., Baskaran R., Edelmann W., Leone G., Knudsen E.S. DNA damage invokes mismatch repair-dependent cyclin D1 attenuation and retinoblastoma signaling pathways to inhibit CDK2. J. Biol. Chem. 277:2002;8372-8381.
12. Davis T.W., Wilson-Van Patten C., Meyers M., Kunugi K.A., Cuthill S., Reznikoff C., Garces C., Boland C.R., Kinsella T.J., Fishel R., Boothman D.A. Defective expression of the DNA mismatch repair protein, MLH1, alters G2-M cell cycle checkpoint arrest following ionizing radiation. Cancer Res. 58:1998;767-778.
13. Hawn M.T., Umar A., Carethers J.M., Marra G., Kunkel T.A., Boland C.R., Koi M. Evidence for a connection between the mismatch repair system and the G2 cell cycle checkpoint. Cancer Res. 55:1995;3721-3725.
14. Wang H., Lawrence C.W., Li G.M., Hays J.B. Specific binding of human MSH2.MSH6 mismatch-repair protein heterodimers to DNA incorporating thymine- or uracil-containing UV light photoproducts opposite mismatched bases. J. Biol. Chem. 274:1999;16894-16900.
15. Li G., Ho V.C. p53-dependent DNA repair and apoptosis respond differently to high- and low-dose ultraviolet radiation. Br. J. Dermatol. 139:1998;3-10.
16. Sweder K.S., Verhage R.A., Crowley D.J., Crouse G.F., Brouwer J., Hanawalt P.C. Mismatch repair mutants in yeast are not defective in transcription- coupled DNA repair of UV-induced DNA damage. Genetics. 143:1996;1127-1135.
17. Leadon S.A., Avrutskaya A.V. Requirement for DNA mismatch repair proteins in the transcription- coupled repair of thymine glycols in Saccharomyces cerevisiae. Mutat. Res. 407:1998;177-187.
18. Sonneveld E., Vrieling H., Mullenders L.H., van Hoffen A. Mouse mismatch repair gene Msh2 is not essential for transcription-coupled repair of UV-induced cyclobutane pyrimidine dimers. Oncogene. 20:2001;538-541.
19. Bartek J., Lukas J. Pathways governing G1/S transition and their response to DNA damage. FEBS Lett. 490:2001;117-122.
20. Mellon I., Rajpal D.K., Koi M., Boland C.R., Champe G.N. Transcription-coupled repair deficiency and mutations in human mismatch repair genes. Science. 272:1996;557-560.
21. Rochette P.J., Bastien N., McKay B.C., Therrien J.P., Drobetsky E.A., Drouin R. Human cells bearing homozygous mutations in the DNA mismatch repair genes hMLH1 or hMSH2 are fully proficient in transcription-coupled nucleotide excision repair. Oncogene. 21:2002;5743-5752.
22. Meira L.B., Reis A.M., Cheo D.L., Nahari D., Burns D.K., Friedberg E.C. Cancer predisposition in mutant mice defective in multiple genetic pathways: uncovering important genetic interactions. Mutat. Res. 477:2001;51-58.
23. Wikonkal N.M., Brash D.E. Ultraviolet radiation induced signature mutations in photocarcinogenesis. J. Investig. Dermatol. Symp. Proc. 4:1999;6-10.
24. Li G., Tron V., Ho V. Induction of squamous cell carcinoma in p53-deficient mice after ultraviolet irradiation. J. Invest. Dermatol. 110:1998;72-75.
25. de Boer J., Hoeijmakers J.H. Nucleotide excision repair and human syndromes. Carcinogenesis. 21:2000;453-460.
26. Appella E., Anderson C.W. Post-translational modifications and activation of p53 by genotoxic stresses. Eur. J. Biochem. 268:2001;2764-2772.
27. Bertrand P., Tishkoff D.X., Filosi N., Dasgupta R., Kolodner R.D. Physical interaction between components of DNA mismatch repair and nucleotide excision repair. Proc. Natl. Acad. Sci. USA. 95:1998;14278-14283.
28. Wu J., Gu L., Wang H., Geacintov N.E., Li G.M. Mismatch repair processing of carcinogen-DNA adducts triggers apoptosis. Mol. Cell Biol. 19:1999;8292-8301.
29. Li G.M. The role of mismatch repair in DNA damage-induced apoptosis. Oncol. Res. 11:1999;393-400.
30. Duckett D.R., Bronstein S.M., Taya Y., Modrich P. hMutSalpha- and hMutLalpha-dependent phosphorylation of p53 in response to DNA methylator damage. Proc. Natl. Acad. Sci. USA. 96:1999;12384-12388.
31. Reitmair A.H., Schmits R., Ewel A., Bapat B., Redston M., Mitri A., Waterhouse P., Mittrucker H.W., Wakeham A., Liu B. MSH2 deficient mice are viable and susceptible to lymphoid tumours. Nat. Genet. 11:1995;64-70.
32. Fritzell J.A., Narayanan L., Baker S.M., Bronner C.E., Andrew S.E., Prolla T.A., Bradley A., Jirik F.R., Liskay R.M., Glazer P.M. Role of DNA mismatch repair in the cytotoxicity of ionizing radiation. Cancer Res. 57:1997;5143-5147.
33. Baross-Francis A., Andrew S.E., Penney J.E., Jirik F.R. Tumors of DNA mismatch repair-deficient hosts exhibit dramatic increases in genomic instability. Proc. Natl. Acad. Sci. USA. 95:1998;8739-8743.
34. McKay B.C., Becerril C., Ljungman M. P53 plays a protective role against UV- and cisplatin-induced apoptosis in transcription-coupled repair proficient fibroblasts. Oncogene. 20:2001;6805-6808.
35. Leadon S.A., Avrutskaya A.V. Differential involvement of the human mismatch repair proteins, hMLH1 and hMSH2, in transcription-coupled repair. Cancer Res. 57:1997;3784-3791.
36. Andrew S.E., McKinnon M., Cheng B.S., Francis A., Penney J., Reitmair A.H., Mak T.W., Jirik F.R. Tissues of MSH2-deficient mice demonstrate hypermutability on exposure to a DNA methylating agent. Proc. Natl. Acad. Sci. USA. 95:1998;1126-1130.
37. Ban C., Junop M., Yang W. Transformation of MutL by ATP binding and hydrolysis: a switch in DNA mismatch repair. Cell. 97:1999;85-97.
38. Kulms D., Schwarz T. Mechanisms of UV-induced signal transduction. J. Dermatol. 29:2002;189-196.
39. Cole S.L., Tevethia M.J. Simian virus 40 large T antigen and two independent T-antigen segments sensitize cells to apoptosis following genotoxic damage. J. Virol. 76:2002;8420-8432.
40. Ali S.H., DeCaprio J.A. Cellular transformation by SV40 large T antigen: interaction with host proteins. Semin. Cancer Biol. 11:2001;15-23.
41. Tibbetts R.S., Brumbaugh K.M., Williams J.M., Sarkaria J.N., Cliby W.A., Shieh S.Y., Taya Y., Prives C., Abraham R.T. A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13:1999;152-157.
42. Wang Y., Cortez D., Yazdi P., Neff N., Elledge S.J., Qin J. BASC, a super complex of BRCA1-associated proteins involved in the recognition and repair of aberrant DNA structures. Genes Dev. 14:2000;927-939.
43. Brown K.D., Rathi A., Kamath R., Beardsley D.I., Zhan Q., Mannino J.L., Baskaran R. The mismatch repair system is required for S-phase checkpoint activation. Nat. Genet. 3:2003;80-84.
44. Ochs K., Kaina B. Apoptosis induced by DNA damage O6-methylguanine is Bcl-2 and caspase-9/3 regulated and Fas/caspase-8 independent. Cancer Res. 60:2000;5815-5824.
45. Zhang H., Richards B., Wilson T., Lloyd M., Cranston A., Thorburn A., Fishel R., Meuth M. Apoptosis induced by overexpression of hMSH2 or hMLH1. Cancer Res. 59:1999;3021-3027.
46. Christmann M., Tomicic M.T., Kaina B. Phosphorylation of mismatch repair proteins MSH2 and MSH6 affecting MutSalpha mismatch-binding activity. Nucleic Acids Res. 30:2002;1959-1966.
47. Denning M.F., Wang Y., Nickoloff B.J., Wrone-Smith T. Protein kinase C δ is activated by caspase-dependent proteolysis during ultraviolet radiation induced apoptosis of human keratinocytes. J. Biol. Chem. 273:1998;29995-30002.
48. Cheo D.L., Meira L.B., Burns D.K., Reis A.M., Issac T., Friedberg E.C. Ultraviolet B radiation-induced skin cancer in mice defective in the Xpc, Trp53, and Apex (HAP1) genes: genotype-specific effects on cancer predisposition and pathology of tumors. Cancer Res. 60:2000;1580-1584.