The role of DNA mismatch repair in drug resistance

Clinical Cancer Research

Volumn 4, Issue 1, 1998, Pages 1-6

  Fink, Daniel ^a   Aebi, Stefan ^a   Howell, Stephen B ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKYLATING AGENT; ANTIMETABOLITE; ANTINEOPLASTIC AGENT; BUSULFAN; CARBOPLATIN; CISPLATIN; DNA TOPOISOMERASE INHIBITOR; DOXORUBICIN; ETOPOSIDE; MERCAPTOPURINE; PLATINUM DERIVATIVE; PROCARBAZINE; TEMOZOLOMIDE; TIOGUANINE;

APOPTOSIS; BASE MISPAIRING; CELL CYCLE G2 PHASE; DNA DAMAGE; DNA REPAIR; GENE MUTATION; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ALKYLATING AGENTS; ANIMALS; ANTINEOPLASTIC AGENTS; CELL CYCLE; DNA REPAIR; DRUG RESISTANCE, NEOPLASM; HUMANS; ORGANOPLATINUM COMPOUNDS; THIOGUANINE;

EID: 0031906084     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (75)

1. Wildenberg, J., and Meselson, M. Mismatch repair in heteroduplex DNA. Proc. Natl. Acad. Sci. USA, 72: 2202-2206, 1975.
2. Su, S. S., and Modrich, P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc. Natl. Acad. Sci. USA, 83: 5057-5061, 1986.
3. Fishel, R., Lescoe, M. K., Rao, M. R. S., Copeland, N. G., Jenkins, N. A., Garber, J., Kane, M., and Kolodner, R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell, 75: 1027-1038, 1993.
4. Leach, F. S., Nicolaides, N. C., Papadopoulos, N., Liu, B., Jen, J., Parsons, R., Peltomäki, P., Sistonen, P., Aaltonen, L. A., Nyström-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., Järvinen, 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. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell, 75: 1215-1225, 1993.
5. Fujii, H., and Shimada, T. Isolation and characterization of cDNA clones derived from the divergently transcribed gene in the region upstream from the human dihydrofolate reductase gene. J. Biol. Chem., 264: 10057-10064, 1989.
6. Risinger, J. I., Umar, A., Boyd, J., Berchuck, A., Kunkel, T. A., and Barrett, J. C. Mutation of MSH3 in endometrial cancer and evidence for its functional role in heteroduplex repair. Nat. Genet., 14: 102-105, 1996.
7. Palombo, F., Gallinari, P., Iaccarino, I., Lettieri, T., Hughes, M., D'Arrigo, A., Truong, O., Hsuan, J. J., and Jiricny, J. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science (Washington DC), 268: 1912-1914, 1995.
8. Drummond, J. T., Li, G-M., Longley, M. J., and Modrich, P. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science (Washington DC), 268: 1909-1912, 1995.
9. 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. Mutations of a mutL homolog in hereditary colon cancer. Science (Washington DC), 263: 1625-1629, 1994.
10. 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. Mutation in the DNA mismatch repair gene homologue hMLH1 is associated with hereditary nonpolyposis colon cancer. Nature (Lond.), 368: 258-261, 1994.
11. Nicolaides, N. C., Papadopoulos, N., Liu, B., Wei, Y-F., Carter, K. C., Ruben, S. M., Rosen, C. A., Haseltine, W. A., Fleischmann, R. D., Fraser, C. M., Adams, M. D., Venter, J. C., Dunlop, M. G., Hamilton, S. R., Petersen, G. M., de la Chapelle, A., Vogelstein, B., and Kinzler, K. W. Mutations of two PMS homologues in hereditary non-polyposis colon cancer. Nature (Lond.), 371: 75-80, 1994.
12. Kolodner, R. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev., 10: 1433-1442, 1996.
13. Fishel, R., Ewel, A., and Lescoe, M. K. Purified human MSH2 protein binds to DNA containing mismatched nucleotides. Cancer Res., 54: 5539-5542, 1994.
14. Acharya, S., Wilson, T., Gradia, S., Kane, M. F., Guerrette, S., Marsischky, G. T., Kolodner, R., and Fishel, R. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc. Natl. Acad. Sci. USA, 93: 13629-13634, 1996.
15. Li, G-M., and Modrich, P. Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc. Natl. Acad. Sci. USA, 92: 1950-1954, 1995.
16. Aaltonen, L. A., Peltomäki, P., Leach, F. S., Sistonen, P., Pylkkänen, L., Mecklin, J-P., Järvinen, H., Powell, S. M., Jen, J., Hamilton, S. R., Petersen, G. M., Kinzler, K. W., Vogelstein, B., and de la Chapelle, A. Clues to the pathogenesis of familial colorectal cancer. Science (Washington DC), 260: 812-816, 1993.
17. Thibodeau, S. N., Bren, G., and Schaid, D. Microsatellite instability in cancer of the proximal colon. Science (Washington DC), 260: 816-819, 1993.
18. Bhattacharyya, N. P., Skandalis, A., Ganesh, A., Groden, J., and Meuth, M. Mutator phenotypes in human colorectal carcinoma cell lines. Proc. Natl. Acad. Sci. USA, 91: 6319-6323, 1994.
19. Hess, P., Aquilina, G., Dogliotti, E., and Bignami, M. Spontaneous mutations at aprt locus in a mammalian cell line defective in mismatch recognition. Somatic Cell Mol. Genet., 20: 409-421, 1994.
20. Huang, J., Papadopoulos, N., McKinley, A. J., Farrington, S. M., Curtis, L. J., Wyllie, A. H., Zheng, S., Willson, J. K. V., Markowitz, S. D., Morin, P., Kinzler, K. W., Vogelstein, B., and Dunlop, M. G. APC mutations in colorectal tumors with mismatch repair deficiency. Proc. Natl. Acad. Sci. USA, 93: 9049-9054, 1996.
21. Markowitz, S., Wang, J., Myeroff, L., Parsons, R. E., Sun, L., Lutterbaugh, J., Fan, R. S., Zborowska, E., Kinzler, K. W., Vogelstein, B., Brattain, M., and Willson, J. K. V. Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability. Science (Washington DC), 268: 1336-1338, 1995.
22. Rampino, N., Yamamoto, H., Ionov, Y., Li, Y., Sawai, H., Reed, J. C., and Perucho, M. Somatic frameshift mutations in the BAX gene in colon cancers of the microsatellite mutator phenotype. Science (Washington DC), 275: 967-969, 1997.
23. Hemminki, A., Peltomäki, P., Mecklin, J-P., Järvinen, H., Salovaara, R., Nyström-Lahti, M., de la Chapelle, A., and Aaltonen, L. A. Loss of the wild type MLH1 gene is a feature of hereditary nonpolyposis colorectal cancer. Nat. Genet., 8: 405-410, 1994.
24. Liu, B., Parsons, R., Papadopoulos, N., Nicolaides, N. C., Lynch, H. T., Watson, P., Jass, J. R., Dunlop, M., Wyllie, A., Peltomäki, P., de la Chapelle, A., Hamilton, S. R., Vogelstein, B., and Kinzler, K. W. Analysis of mismatch repair genes in hereditary non-polyposis colorectal cancer patients. Nat. Med., 2: 169-174, 1996.
25. Risinger, J. I., Berchuck, A., Kohler, M. F., Watson, P., Lynch, H. T., and Boyd, J. Genetic instability of microsatellites in endometrial carcinoma. Cancer Res., 53: 5100-5103, 1993.
26. Merlo, A., Mabry, M., Gabrielson, E., Vollmer, R., Baylin, S. B., and Sidransky, D. Frequent microsatellite instability in primary small cell lung cancer. Cancer Res., 54: 2098-2101, 1994.
27. Shridhar, V., Siegfried, J., Hunt, J., del Mar Alonso, M., and Smith D. I. Genetic instability of microsatellite sequences in many non-small cell lung carcinomas. Cancer Res., 54: 2084-2087, 1994.
28. Han, H-J., Yanagisawa, A., Kato, Y., Park, J-G., and Nakamura, Y. Genetic instability in pancreatic cancer and poorly differentiated type of gastric cancer. Cancer Res., 53: 5087-5089, 1993.
29. Wooster, R., Cleton-Jansen, A-M., Collins, N., Mangion, J., Cornelis, R. S., Cooper, C. S., Gusterson, B. A., Ponder, B. A. J., von Deimling, A., Wiestler, O. D., Cornelisse, C. J., Devilee, P., and Stratton, M. R. Instability of short tandem repeats (microsatellites) in human cancers. Nat. Genet., 6: 152-156, 1994.
30. Baker, S. M., Plug, A. W., Prolla, T. A., Bronner, C. E., Harris, A. C., Yao, X., Christie, D-M., Monell, C., Arnheim, N., Bradley, A., Ashley, T., and Liskay, R. M. Involvement of mouse MLH1 in DNA mismatch repair and meiotic crossing over. Nat. Genet., 13: 336-342, 1996.
31. de Wind, N., Dekker, M., Berns, A., Radman, M., and te Riele, H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell, 82: 321-330, 1995.
32. Reitmair, A. H., Schmits, R., Ewel, A., Bapat, B., Redston, M., Mitri, A., Waterhouse, P., Mittrücker, H-W., Wakeham, A., Liu, B., Thomason, A., Griesser, H., Gallinger, S., Ballhausen, W. G., Fishel, R., and Mak, T. W. MSH2 deficient mice are viable and susceptible to lymphoid tumours. Nat. Genet., 11: 64-70, 1995.
33. Baker, S. M., Bronner, C. E., Zhang, L., Plug, A. W., Robatzek, M., Warren, G., Elliott, E. A., Yu, J., Ashley, T., Arnheim, N., Flavell, R. A., and Liskay, R. M. Male mice defective in the DNA mismatch repair gene PMS2 exhibit abnormal chromosome synapsis in meiosis. Cell, 82: 309-319, 1995.
34. + tumor cells. Cell, 75: 1227-1236, 1993.
35. Boyer, J. C., Umar, A., Risinger, J. I., Lipford, J. R., Kane, M., Yin, S., Barrett, J. C., Kolodner, R. D., and Kunkel, T. A. Microsatellite instability, mismatch repair deficiency, and genetic defects in human cancer cell lines. Cancer Res., 55: 6063-6070, 1995.
36. Koi, M., Umar, A., Chauhan, D. P., Cherian, S. P., Carethers, J. M., Kunkel, T. A., and Boland, C. R. 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.
37. Umar, A., Koi, M., Risinger, J. I., Glaab, W. E., Tindall, K. R., Kolodner, R. D., Boland, C. R., Barrett, J. C., and Kunkel, T. A. Correction of hypermutability, N-methyl-N′-nitro-N-nitrosoguanidine resistance, and defective DNA mismatch repair by introducing chromosome 2 into human tumor cells with mutations in MSH2 and. MSH6. Cancer Res., 57: 3949-3955, 1997.
38. Risinger, J. I., Umar, A., Barrett, J. C., and Kunkel, T. A. A hPMS2 mutant cell line is defective in strand-specific mismatch repair. J. Biol. Chem., 270: 18183-18186, 1995.
39. Moggs, J. G., Szymkowski, D. E., Yamada, M., Karran, P., and Wood, R. D. Differential human nucleotide excision repair of paired and mispaired cisplatin-DNA adducts. Nucleic Acids Res., 25: 480-490, 1997.
40. Griffin, S., Branch, P., Xu, Y-Z., and Karran, P. DNA mismatch binding and incision at modified guanine bases by extracts of mammalian cells: implications for tolerance to DNA methylation damage. Biochemistry, 33: 4787-4793, 1994.
41. Karran, P., and Bignami, M. DNA damage tolerance, mismatch repair and genome instability. Bioessays, 16: 833-839, 1994.
42. Kat, A., Thilly, W. G., Fang, W-H., Longley, M. J., Li, G-M., and Modrich, P. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc. Natl. Acad. Sci. USA, 90: 6424-6428, 1993.
43. Branch, P., Aquilina, G., Bignami, M., and Karran, P. Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature (Lond.), 362: 652-654, 1993.
44. Liu, L., Markowitz, S., and Gerson, S. L. Mismatch repair mutations override alkyltransferase in conferring resistance to temozolomide but not to 1,3-bis(2-chloroethyl)nitrosourea. Cancer Res., 56: 5375-5379, 1996.
45. D'Atri, S., Graziani, G., Lacal, P. M., Tentori, L., Bonmassar, E., Pagani, E., and Jiricny, J. Role of mismatch repair in apoptosis induced by methyltriazenes. Proc. Am. Assoc. Cancer Res., 38: 1, 1997.
46. Friedman, H. S., Johnson, S. P., Dong, Q., Schold, S. C., Rasheed, B. K. A., Bigner, S. H., Ali-Osman, F., Dolan, E., Colvin, O. M., Houghton, P., Germain, G., Drummond, J. T., Keir, S., Marcelli, S., Bigner, D. D., and Modrich, P. Methylator resistance mediated by mismatch repair deficiency in a glioblastoma multiforme xenograft. Cancer Res., 57: 2933-2936, 1997.
47. 6-benzylguanine. Biochemistry, 32: 11998-12006, 1993.
48. Rode, P., Kupiec, N., Teicher, B., Emi, Y., and Bubley, G. The effect of a homozygous hMLH1 mutation on antitumor alkylating agent sensitivity. Proc. Am. Assoc. Cancer Res., 37: 380, 1996.
49. Aebi, S., Fink, D., Gordon, R., Kim, H. K., Zheng, H., Fink, J. L., and Howell, S. B. Resistance to cytotoxic drugs in DNA mismatch repair-deficient cells. Clin. Cancer Res., 3: 1763-1767, 1997.
50. Elion, G. B. The purine path to chemotherapy. Science (Washington DC), 244: 41-47, 1989.
51. Tidd, D. M., and Paterson, A. R. P. A biochemical mechanism for the delayed cytotoxic reaction of 6-mercaptopurine. Cancer Res., 34: 738-746, 1974.
52. Bodell, W. J. Molecular dosimetry of sister chromatid exchange induction in 9L cells treated with 6-thioguanine. Mutagenesis, 6: 175-177, 1991.
53. 2 cell cycle checkpoint. Cancer Res., 55: 3721-3725, 1995.
54. Swann, P. F., Waters, T. R., Moulton, D. C., Xu, Y-Z., Zheng, Q., Edwards, M., and Mace, R. Role of postreplicative DNA mismatch repair in the cytotoxic action of thioguanine. Science (Washington DC), 273: 1109-1111, 1996.
55. 6-methylthioguanine. Biochemistry, 36: 2501-2506, 1997.
56. Rappaport, H. P. Replication of the base pair 6-thioguanine/5-methyl-2-pyrimidinone with the large Klenow fragment of Escherichia coli DNA polymerase I. Biochemistry, 32: 3047-3057, 1993.
57. Eastman, A. Activation of programmed cell death by anticancer agents - cisplatin as a model system. Cancer Cells (Cold Spring Harbor), 2: 275-280, 1990.
58. Fram, R. J., Cusick, P. S., Wilson, J. M., and Marinus, M. G. Mismatch repair of cis-diamminedichloroplatinum(II)-induced DNA damage. Mol. Pharmacol., 28: 51-55, 1985.
59. Anthoney, D. A., McIlwrath, A. J., Gallagher, W. M., Edlin, A. R. M., and Brown, R. Microsatellite instability, apoptosis, and loss of p53 function in drug-resistant tumor cells. Cancer Res., 56: 1374-1381, 1996.
60. 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.
61. Drummond, J. T., Anthoney, A., Brown, R., and Modrich, P. Cisplatin and Adriamycin resistance are associated with MutLα and mismatch repair deficiency in an ovarian tumor cell line. J. Biol. Chem., 271: 19645-19648, 1996.
62. Fink, D., Nebel, S., Aebi, S., Zheng, H., Cenni, B., Nehmé, A., Christen, R. D., and Howell, S. B. The role of DNA mismatch repair in platinum drug resistance. Cancer Res., 56: 4881-4886, 1996.
63. Naredi, P., Heath, D. D., Enns, R. E., and Howell, S. B. Cross-resistance between cisplatin, antimony potassium tartrate, and arsenite in human tumor cells. J. Clin. Invest., 95: 1193-1198, 1995.
64. Mello, J. A., Acharya, S., Fishel, R., and Essigmann, J. M. The mismatch-repair protein hMSH2 binds selectively to DNA adducts of the anticancer drug cisplatin. Chem. Biol., 3: 579-589, 1996.
65. 4-methylthymine, or the cisplatin-d(GpG) adduct. Proc. Natl. Acad. Sci. USA, 93: 6443-6447, 1996.
66. Yamada, M., O'Regan, E., Brown, R., and Karran, P. Selective recognition of a cisplatin-DNA adduct by human mismatch repair proteins. Nucleic Acids Res., 25: 491-495, 1997.
67. 2-terminal kinase and c-Ab1 kinase in DNA mismatch repair-proficient and -deficient cells exposed to cisplatin. Cancer Res., 57: 3253-3257, 1997.
68. Chen, A. Y., and Liu, L. F. DNA topoisomerases: essential enzymes and lethal targets. Annu. Rev. Pharmacol. Toxicol., 36: 191-218, 1994.
69. Carethers, J. M., Hawn, M. T., Chauhan, D. P., Luce, M. C., Marra, G., Koi, M., and Boland, C. R. Competency in mismatch repair prohibits clonal expansion of cancer cells treated with N-methyl-N′-nitro-N-nitrosoguanidine. J. Clin. Invest., 98: 199-206, 1996.
70. King, R. W., Jackson, P. K., and Kirschner, M. W. Mitosis in transition. Cell, 79: 563-571, 1994.
71. Brown, R., Hirst, G. L., Gallagher, W. M., McIlwrath, A. J., Margison, G. P., van der Zee, A. G. J., and Anthoney, D. A. hMLH1 expression and cellular responses of ovarian tumour cells to treatment with cytotoxic anticancer agents. Oncogene, 15: 45-52, 1997.
72. Fink, D., Zheng, H., Nebel, S., Norris, P. S., Aebi, S., Lin, T-P., Nehmé, A., Christen, R. D., Hass, M., MacLeod, C. L., and Howell, S. B. In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair. Cancer Res., 57: 1841-1845, 1997.
73. Tomlinson, I. P. M., Novelli, M. R., and Bodmer, W. F. The mutation rate and cancer. Proc. Natl. Acad. Sci. USA, 93: 14800-14803, 1996.
74. Loeb, L. A. Microsatellite instability: marker of a mutator phenotype in cancer. Cancer Res., 54: 5059-5063, 1994.
75. Ben-Yehuda, D., Krichevsky, S., Caspi, O., Rund, D., Polliack, A., Abeliovich, D., Zelig, O., Yahalom, V., Paltiel, O., Or, R., Peretz, T., Ben-Neriah, S., Yehuda, O., and Rachmilewitz, E. A. Microsatellite instability and p53 mutations in therapy-related leukemia suggest mutator phenotype. Blood, 88: 4296-4303, 1996.