Potential role of MLH1 in the induction of p53 and apoptosis by blocking transcription on damaged DNA templates

Molecular Cancer Research

Volumn 1, Issue 10, 2003, Pages 747-754

  Yanamadala, Sunitha ^a   Ljungman, Mats ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; HYDROGEN PEROXIDE; PROTEIN MLH1; PROTEIN P53; RNA POLYMERASE II;

APOPTOSIS; ARTICLE; CELL CYCLE S PHASE; CHROMOSOME 3; COLON CARCINOMA; DNA DAMAGE; DNA REPLICATION; DNA STRAND BREAKAGE; DNA TEMPLATE; GENETIC STABILITY; HUMAN; HUMAN CELL; MESSENGER RNA SYNTHESIS; MISMATCH REPAIR; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; TRANSCRIPTION REGULATION;

ADENOCARCINOMA; ALKYLATING AGENTS; APOPTOSIS; CARRIER PROTEINS; CELL CYCLE; CELL LINE, TUMOR; COLORECTAL NEOPLASMS; DNA DAMAGE; HUMANS; HYDROGEN PEROXIDE; NEOPLASM PROTEINS; NUCLEAR PROTEINS; OXIDATIVE STRESS; PEROXIDES; PHOSPHORYLATION; RNA, MESSENGER; TEMPLATES, GENETIC; TRANSCRIPTION, GENETIC; TUMOR SUPPRESSOR PROTEIN P53;

EID: 0041928171     PISSN: 15417786     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (59)

1. Modrich, P. and Lahue, R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem., 65: 101-133, 1996.
2. Kolodner, R. D. and Marsischky, G. T. Eukaryotic DNA mismatch repair. Curr. Opin. Genet. Dev., 9: 89-96, 1999.
3. Mellon, I., Rajpal, D. K., Koi, M., Boland, C. R., and Champe, G. N. Transcription-coupled repair deficiency and mutations in human mismatch repair genes. Science, 272: 557-560, 1996.
4. Sonneveld, E., Vrieling, H., Mullenders, L. H., and van Hoffen, A. Mouse mismatch repair gene Msh2 is not essential for transcription-coupled repair of UV-induced cyclobutane pyrimidine dimers. Oncogene, 20: 538-541, 2001.
5. Rochette, P. J., Bastien, N., McKay, B. C., Therrien, J. P., Drobetsky, E. A., and 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: 5743-5752, 2002.
6. D'Atri, S., Tentori, L., Lacal, P. M., Graziani, G., Pagani, E., Benincasa, E., Zambruno, G., Bonmassar, E., and Jiricny, J. Involvement of the mismatch repair system in temozolomide-induced apoptosis. Mol. Pharmacol., 54: 334-341, 1998.
7. Duckett, D. R., Bronstein, S. M., Taya, Y., and Modrich, P. hMutS α- and hMutL α-dependent phosphorylation of p53 in response to DNA methylator damage. Proc. Natl. Acad. Sci. USA, 96: 12384-12388, 1999.
8. Hickman, M. J. and Samson, L. D. Role of DNA mismatch repair and p53 in signaling induction of apoptosis by alkylating agents. Proc. Natl. Acad. Sci. USA, 96: 10764-10769, 1999.
9. Wu, J. X., Gu, L. Y., Wang, H. X., Geacintov, N. E., and Li, G. M. Mismatch repair processing of carcinogen-DNA adducts triggers apoptosis. Mol. Cell. Biol., 19: 8292-8301, 1999.
10. Bardelli, A., Cahill, D. P., Lederer, G., Speicher, M. R., Kinzler, K. W., Vogelstein, B., and Lengauer, C. Carcinogen-specific induction of genetic instability. Proc. Natl. Acad. Sci. USA, 98: 5770-5775, 2001.
11. Aebi, S., Kurdi-Haidar, B., Gordon, R., Cenni, B., Zheng, H., Fink, D., Christen, R. D., Boland, C. R., Koi, M., Fishel, R., and Howell, S. B. Loss of DNA mismatch repair in acquired resistance to cisplatin. Cancer Res., 56: 3087-3090, 1996.
12. Koi, M., Umar, A., Chauhan, D., Cherian, S., Carethers, J., Kunkel, T., and Boland, C. Human chromosome 3 corrects mismatch repair deficiency and microsatellite instability and reduces N-methyl-N′ -nitro-N-nitrosoguanidine tolerance in colon tumor cells with homozygous hMLH1 mutation. Cancer Res., 54: 4308-4312, 1994.
13. Frouin, I., Prosperi, E., Denegri, M., Negri, C., Donzelli, M., Rossi, L., Riva, F., Stefanini, M., and Seovassi, A. I. Different effects of methotrexate on DNA mismatch repair proficient and deficient cells. Eur. J. Cancer, 37: 1173-1180, 2001.
14. Fedier, A., Schwarz, V. A., Walt, H., Carpini, R. D., Haller, U., and Fink, D. Resistance to topoisomerase poisons due to loss of DNA mismatch repair. Int. J. Cancer, 93: 571-576, 2001.
15. Hardman, R. A., Afshari, C. A., and Barrett, J. C. Involvement of mammalian MLH1 in the apoptotic response to peroxide-induced oxidative stress. Cancer Res., 61: 1392-1397, 2001.
16. DeWeese, T. L., Shipman, J. M., Larrier, N. A., Buckley, N. M., Kidd, L. R., Groopman, J. D., Cutler, R. G., te Riele, H., and Nelson, W. G. Mouse embryonic stem cells carrying one or two defective Msh2 alleles respond abnormally to oxidative stress inflicted by low-level radiation. Proc. Natl. Acad. Sci. USA, 95: 11915-11920, 1998.
17. Meyers, M., Wagner, M. W., Hwang, H. S., Kinsella, T. J., and Boothman, D. A. Role of the hMLH1 DNA mismatch repair protein in fluoropyrimidine-mediated cell death and cell cycle responses. Cancer Res., 61: 5193-5201, 2001.
18. Bellacosa, A. Functional interactions and signaling properties of mammalian DNA mismatch repair proteins. Cell Death Differ., 8: 1076-1092, 2001.
19. Karran, P. Mechanisms of tolerance to DNA damaging therapeutic drugs. Carcinogenesis, 22: 1931-1937, 2001.
20. Fishel, R. The selection for mismatch repair defects in hereditary nonpolyposis colorectal cancer: revising the mutator hypothesis. Cancer Res., 61: 7369-7374, 2001.
21. Ljungman, M. and Zhang, F. Blockage of RNA polymerase as a possible trigger for UV light-induced apoptosis. Oncogene, 13: 823-831, 1996.
22. Ljungman, M., Zhang, F. F., Chen, F., Rainbow, A. J., and McKay, B. C. Inhibition ofRNA polymerase II as a trigger for the p53 response. Oncogene, 18: 583-592, 1999.
23. McKay, B. C., Ljungman, M., and Rainbow, A. J. Persistent DNA damage induced by ultraviolet light inhibits p21(waf1) and bax expression: implications for DNA repair, UV sensitivity and the induction of apoptosis. Oncogene, 17: 545-555, 1998.
24. McKay, B. and Ljungman, M. Role for p53 in the recovery of transcription and protection against apoptosis induced by ultraviolet light. Neoplasia, 1: 276-284, 1999.
25. Ljungman, M. Dial 9-1-1 for p53: mechanisms of p53 activation by cellular stress. Neoplasia, 2: 208-225, 2000.
26. McKay, B. C., Chen, F., Perumalswami, C. R., Zhang, F. F., and Ljungman, M. The tumor suppressor p53 can both stimulate and inhibit ultraviolet light-induced apoptosis. Mol. Biol. Cell, 11: 2543-2551, 2000.
27. McKay, B. C., Becerril, C., and Ljungman, M. P53 plays a protective role against UV- and cisplatin-induced apoptosis in transcription-coupled repair proficient fibroblasts. Oncogene, 20: 6805-6808, 2001.
28. Ljungman, M., O'Hagan, H. M., and Paulsen, M. T. Induction of ser15 and lys382 modifications of p53 by blockage of transcription elongation. Oncogene, 20: 5964-5971, 2001.
29. Jacob, S., Aguado, M., Fallik, D., and Praz, F. The role of the DNA mismatch repair system in the cytotoxicity of the topoisomerase inhibitors camptothecin and etoposide to human colorectal cancer cells. Cancer Res., 61: 6555-6562, 2001.
30. 6-methylguanine. Mutagenesis, 17: 483-487, 2002.
31. 6-alkylguanine by alkyltransferases. Mutat. Res., 462: 462: 83-100, 2000.
32. 6-benzylguanine-mediated enhancement of chemotherapy. Mol. Cancer Ther., 1: 943-948, 2002.
33. 4-methylthymine, or the cisplatin-d(GpG) adduct. Proc. Natl. Acad. Sci. USA, 93: 6443-6447, 1996.
34. 2 cell cycle checkpoint. Cancer Res., 55: 3721-3725, 1995.
35. Yamaizumi, M. and Sugano, T. UV-induced nuclear accumulation of p53 is evoked through DNA damage of actively transcribed genes independent of the cell cycle. Oncogene, 9: 2775-2784, 1994.
36. Dumaz, N., Duthu, A., Ehrhart, J. C., Drougard, C., Appella, E., Anderson, C. W., May, P., Sarasin, A., and DayaGrosjean, L. Prolonged p53 protein accumulation in trichothiodystrophy fibroblasts dependent on unrepaired pyrimidine dimers on the transcribed strands of cellular genes. Mol. Carcinog., 20: 340-347, 1997.
37. Brash, D. E., Wikonkal, N. M., Remenyik, E., van der Horst, G. T. J., Friedberg, E. C., Cheo, D. L., van Steeg, H., Westerman, A., and van Krancn, H. J. The DNA damage signal for Mdm2 regulation, Trp53 induction, and sunburn cell formation in vivo originates from actively transcribed genes. J. Invest. Dermatol., 117: 1234-1240, 2001.
38. Blattner, C., Bender, K., Herrlich, P., and Rahmsdorf, H. Photoproducts in transcriptionally active DNA induce signal transduction to delay UV-responsive genes for collagenase and metallothionein. Oncogene, 16: 2827-2834, 1998.
39. Donahue, B. A., Yin, S., Taylor, J. S., Reines, D., and Hanawalt, P. C. Transcript cleavage by RNA polymerase II arrested by a cyclobutane pyrimidine dimer in the DNA template. Proc. Natl. Acad. Sci. USA, 91: 8502-8506, 1994.
40. Tornaletti, S., Reines, D., and Hanawalt, P. C. Structural characterization of RNA polymerase II complexes arrested by a cyclobutane pyrimidine dimer in the transcribed strand of template DNA. J. Biol. Chem., 274: 24124-24130, 1999.
41. Viswanathan, A. and Doetsch, P. W. Effects of nonbulky DNA base damages on Escherichia coli RNA polymerase-mediated elongation and promoter clearance. J. Biol. Chem., 273: 21276-21281, 1998.
42. Glaab, W. E., Hill, R. B., and Skopek, T. R. Suppression of spontaneous and hydrogen peroxide-induced mutagenesis by the antioxidant ascorbate in mismatch repair-deficient human colon cancer cells. Carcinogenesis, 22: 1709-1713, 2001.
43. Canman, C. E., Lim, D. S., Cimprich, K. A., Taya, Y., Tamai, K., Sakaguchi, K., Appella, E., Kastan, M. B., and Siliciano, J. D. Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science, 281: 1677-1679, 1998.
44. Banin, S., Moyal, L., Shieh, S. Y., Taya, Y., Anderson, C. W., Chessa, L., Smorodinsky, N. I., Prives, C., Reiss, Y., Shiloh, Y., and Ziv, Y. Enhanced phosphorylation of p53 by ATN in response to DNA damage. Science, 281: 1674-1677, 1998.
45. Xie, S. Q., Wang, Q., Wu, H. Y., Cogswell, J., Lu, L., Jhanwar-Uniyal, M., and Dai, W. Reactive oxygen species-induced phosphorylation of p53 on serine 20 is mediated in part by polo-like kinase-3. J. Biol. Chem., 276: 36194-36199, 2001.
46. Friedberg, E., Walker, G., and Siede, W. DNA Repair and Mutagenesis. Washington, DC: ASM Press, 1995.
47. Tornaletti, S., Maeda, L. S., Lloyd, D. R., Reines, D., and Hanawalt, P. C. Effect of thymine glycol on transcription elongation by T7 RNA polymerase and mammalian RNA polymerase II. J. Biol. Chem., 276: 45367-45371, 2001.
48. Kuraoka, I., Endou, M., Yamaguchi, Y., Wada, T., Handa, H., and Tanaka, K. Effects of endogenous DNA base lesions on transcription elongation by mammalian RNA polymerase II - implications for transcription-coupled DNA repair and transcriptional mutagenesis. J. Biol. Chem., 278: 7294-7299, 2003.
49. Le Page, F., Kwoh, E. E., Avrutskaya, A., Gentil, A., Leadon, S. A., Sarasin, A., and Cooper, P. K. Transcription-coupled repair of 8-oxoguanine: requirement for XPG, TFIIH, and CSB and implications for Cockayne syndrome. Cell, 101: 159-171, 2000.
50. Brown, K. D., Rathi, A., Kamath, R., Beardsley, D. I., Zhan, Q. M., Mannino, J. L., and Baskaran, R. The mismatch repair system is required for S-phase checkpoint activation. Nat. Genet., 33: 80-84, 2003.
51. Adamson, A. W., Kim, W. J., Shangary, S., Baskaran, R., and Brown, K. D. ATM is activated in response to N-methyl-N′-nitro-N-nitrosoguanidine-induced DNA alkylation. J. Biol. Chem., 277: 38222-38229, 2002.
52. 6-ethylguanine in transcribed and nontranscribed genes of the rat. J. Biol. Chem., 269: 1681-1686, 1994.
53. 6-methylguanine lesion. Mol. Cell. Biol., 18: 1660-1669, 1998.
54. Leadon, S. A. and Cooper, P. K. Preferential repair of ionizing radiation-induced damage in the transcribed strand of an active human gene is defective in Cockayne syndrome. Proc. Natl. Acad. Sci. USA, 90: 10499-10503, 1993.
55. Le Page, E., Randrianarison, V., Marot, D., Cabannes, J., Perricaudet, M., Feunteun, J., and Sarasin, A. BRCA1 and BRCA2 are necessary for the transcription-coupled repair of the oxidative 8-oxoguanine lesion in human cells. Cancer Res., 60: 5548-5552, 2000.
56. Ljungman, M. and Paulsen, M. T. The cyclin-dependent kinase inhibitor roscovitine inhibits RNA synthesis and triggers nuclear accumulation of p53 that is unmodified at Ser15 and Lys382. Mol. Pharmacol., 60: 785-789, 2001.
57. Kolodner, R. D. Mismatch repair: mechanisms and relationship to cancer susceptibility. Trends Biochem. Sci., 20: 397-401, 1995.
58. Jiricny, J. and Nystrom-Lahti, M. Mismatch repair defects in cancer. Curr. Opin. Genet. Dev., 10: 157-161, 2000.
59. Chen, F., Chang, D., Goh, M., Klibanov, S. A., and Ljungman, M. Role of p53 in cell cycle regulation and apoptosis following exposure to proteasome inhibitors. Cell Growth & Differ., 11: 239-246, 2000.