The mismatch-repair protein hMSH2 binds selectively to DNA adducts of the anticancer drug cisplatin

Chemistry and Biology

Volumn 3, Issue 7, 1996, Pages 579-589

  Mello, Jill A ^a   Acharya, Samir ^b   Fishel, Richard ^b   Essigmann, John M ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

cisplatin; cisplatin binding proteins; hMSH2; mismatch repair

Indexed keywords

ESCHERICHIA;

EID: 0030198880     PISSN: 10745521     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-5521(96)90149-0     Document Type: Article

References (59)

1. Loehrer, P.J. & Einhorn, L.H. (1984). Cisplatin. Ann. Intern. Med. 100, 704-713.
2. Brunn, S.L., Toney, J.H. & Lippard, S.J. (1990). Biological processing of DNA modified by platinum compounds. Prog. Inorg. Chem. 38, 477-516.
3. Eastman, A. (1983). Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cis-dichloro(ethylenediamine)platinum(II). Biochemistry 22, 3927-3933.
4. Fichtinger-Schepman, A.M.J., van der Veer, J.L., den Hartog, J.H., Lohman, P.M. & Reedijk, J. (1985). Adducts of the antitumor drug cis-diamminedichloroplatinum(II) with DNA: formation, identification, and quantitation. Biochemistry 24, 707-713.
5. 2 phase and cell death induced by cisplatin. J. Natl Cancer Inst. 82, 749-755.
6. Chu, G. (1994). Cellular responses to cisplatin. J. Biol. Chem. 269, 787-790.
7. Bruhn, S.L., Pil, P.M., Essigmann, J.M., Housman, D.E. & Lippard, S.J. (1992). Isolation and characterization of human cDNA clones encoding a high mobility group box protein that recognizes structural distortions to DNA caused by binding of the anticancer agent cisplatin. Proc. Natl. Acad. Sci. USA 89, 2307-2311.
8. Pil, P.M. & Lippard, S.J. (1992). Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. Science 256, 234-237.
9. Brown, S.J., Kellett, P.J. & Lippard, S.J. (1993). Ixr1, a yeast protein that binds to platinated DNA and confers sensitivity to cisplatin. Science 261, 603-605.
10. Toney, J.H., Donahue, B.A., Kellett, P.J., Bruhn, S.L., Essigmann, J.M. & Lippard, S.J. (1989). Isolation of cDNAs encoding a human protein that binds selectively to DNA modified by the anticancer drug cis-diamminedichloroplatinum(II). Proc. Natl. Acad. Sci. USA 86, 8328-8332.
11. Bianchi, M.E., Falciola, L., Ferrari, S. & Lilley, D.M.J. (1992). The DNA binding site of HMG1 protein is composed of two similar segments (HMG boxes), both of which have counterparts in other eukaryotic regulatory proteins. EMBO J. 11, 1055-1063.
12. Ferrari, S., Harley, V.R., Pontiggia, A., Goodfellow, P.N., Lovell-Badge, R. & Bianchi, M.E. (1992). SRY, like HMG1, recognizes sharp angles in DNA. EMBO J. 11, 4497-4506.
13. Lilley, D.M.J. (1992). HMG has DNA wrapped up. Nature 357, 282-283.
14. +. Biophys. Chem. 35, 179-188.
15. Bellon, S.F., Coleman, J.H. & Lippard, S.J. (1991). DNA unwinding produced by site-specific intrastrand cross-links of the antitumor drug cis-diamminedichloroplatinum(II). Biochemistry 30, 8026-8035.
16. Donahue, B.A., et al., & Essigmann, J.M. (1990). Characterization of a DNA damage-recognition protein from mammalian cells that binds specifically to intrastrand d(GpG) and d(ApG) DNA adducts of the anticancer drug cisplatin. Biochemistry 29, 5872-5880.
17. Huang, J.-C., Zamble, D.B., Reardon, J.T., Lippard, S.J. & Sancar, A. (1994). HMG-domain proteins specifically inhibit the repair of the major DNA adduct of the anticancer drug cisplatin by human excision nuclease. Proc. Natl. Acad. Sci. USA 91, 10394-10398.
18. McA'Nulty, M.M. & Lippard, S.J. (1996). The HMG-domain protein Ixr1 blocks excision repair of cisplatin-DNA adducts in yeast. Mutat. Res. 362, 75-86.
19. Treiber, D.K., Zhai, X., Jantzen, H.-M. & Essigmann, J.M. (1994). Cisplatin-DNA adducts are molecular decoys for the ribosomal RNA transcription factor hUBF (human upstream binding factor). Proc. Natl. Acad. Sci. USA 91, 5672-5676.
20. Wilson, T.M., et al., & Kelley, M.R. (1995). Differential cellular expression of the human MSH2 repair enzyme in small and large intestine. Cancer Res. 55, 5146-5150.
21. Fishel, R., et al., & Kolodner, R. (1993). The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell 75, 1027-1038.
22. Leach, F.S., et al., & Vogelstein, B. (1993). Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell 75, 1215-1225.
23. Fram, R.J., Cusick, P.S., Wilson, J.M. & Marinus, M.G. (1985). Mismatch repair of cis-diamminedichloroplatinum(II)-induced DNA damage. Mol. Pharmacol. 28, 51-55.
24. Fishel, R., Ewel, A. & Lescoe, M.K. (1994). Purified human MSH2 protein binds to DNA containing mismatched nucleotides. Cancer Res. 54, 5539-5542.
25. Fishel, R., Ewel, A., Lee, S., Lescoe, M.K. & Griffith, J. (1994). Binding of mismatched microsatellite DNA sequences by the human MSH2 protein. Science 266, 1403-1405.
26. Alani, E., Chi, N.-W. & Kolodner, R. (1995). The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions. Genes Dev. 9, 234-247.
27. Kasparková, J. & Brabec, V. (1995). Recognition of DNA interstrand cross-links of cis-diamminedichloroplatinum(II) and its trans isomer by DNA-binding proteins. Biochemistry 34, 12379-12387.
28. Palombo, F., et al., & Jiricny, J. (1995). GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science 268, 1912-1914.
29. Drummond, J.T., Li, G.-M., Longley, M.J. & Modrich, R (1995). Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268, 1909-1912.
30. Papadopoulos, N., et al., & Vogelstein, B. (1995). Mutations of GTBP in genetically unstable cells. Science 268, 1915-1917.
31. Marsischky, G.T., Filosi, N., Kane, M.F. & Kolodner, R. (1996). Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10, 407-420.
32. Mellon, I. & Champe, G.N. (1996). Products of DNA mismatch repair genes mutS and mutL are required for transcription-coupled nucleotide-excision repair of the lactose operon in Escherichia coli. Proc. Natl. Acad. Sci. USA 93, 1292-1297.
33. Mellon, I., Rajpal, D.K., Koi, M., Boland, C.R. & Champe, G.N. (1996). Transcription-coupled repair deficiency and mutations in human mismatch repair genes. Science 272, 557-560.
34. 6-methylguanine residues in E. coli DNA. Nature 296, 868-869.
35. Jones, M. & Wagner, R. (1981). N-Methyl-N′-nitro-N-nitrosoguanidine sensitivity of E. coli mutants deficient in DNA methylation and mismatch repair. Mol. Gen. Genet. 184, 562-563.
36. Goldmacher, V.S., Cuzick Jr, R.A. & Thilly, W.G. (1986). Isolation and partial characterization of human cell mutants differing in sensitivity to killing and mutation by methylnitrosourea and N-methyl-N′-nitro-N-nitrosoguanidine. J. Biol. Chem. 261, 12462-12471.
37. Kat, A., Thilly, W.G., Fang, W.-H., Longley, M.J., Li, G.-M. & Modrich, P. (1993). An alykylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc. Natl. Acad. Sci. USA 90, 6424-6428.
38. Karran, P. & Bignami, M. (1992). Self-destruction and tolerance in resistance of mammalian cells to alkylation damage. Nucleic Acids Res. 20, 2933-2940.
39. Branch, P., Aquilina, G., Bignami, M. & Karran, P. (1993). Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature 362, 652-654.
40. Branch, P., Hampson, R. & Karran, P. (1995). DNA mismatch binding defects, DNA damage tolerance, and mutator phenotypes in human colorectal carcinoma cell lines. Cancer Res. 55, 2304-2309.
41. Aquilina, G., Hess, P., Fiumicino, S., Ceccotti, S. & Bignami, M. (1995). A mutator phenotype characterizes one of two complementation groups in human cells tolerant to methylation damage. Cancer Res. 55, 2569-2575.
42. Griffin, S., Branch, P., Xu, Y.-Z. & Karran, P. (1994). 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.
43. 6-Methylguanine residues elicit DNA repair synthesis by human cell extracts. J. Biol. Chem. 268, 15878-15886.
44. 2 arrest and DNA double-strand breaks. Cancer Res. 48, 4484-4488.
45. Roussel, P., André, C., Masson, C., Géraud, G. & Hernandez-Verdun, D. (1993). Localization of the RNA polymerase I transcription factor hUBF during the cell cycle. J. Cell Sci. 104, 327-337.
46. Leach, F.S., et al., & Vogelstein, B. (1996). Expression of the human mismatch repair gene hMSH2 in normal and neoplastic tissues. Cancer Res. 56, 235-240.
47. Aebi, S., et al., & Howell, S.B. (1996). Loss of DNA mismatch repair in acquired resistance to cisplatin. Cancer Res., in press.
48. Anthoney, D.A., McIlwrath, A.J., Gallagher, W.M., Edlin, A.R.M. & Brown, R. (1996). Microsatellite instability, apoptosis, and loss of p53 function in drug-resistant tumor cells. Cancer Res. 56, 1374-1381.
49. 2 cell cycle checkpoint. Cancer Res. 55, 3721-3725.
50. Sorenson, C.M. & Eastman, A. (1988). Influence of cis-diamminedichloroplatinum(II) on DNA synthesis and cell cycle progression in excision repair proficient and deficient Chinese hamster ovary cells. Cancer Res. 48, 6703-6707.
51. Piacentini, M., Fesus, L. & Melino, G. (1993). Multiple cell cycle access to the apoptotic death programme in human neuroblastoma cells. FEBS Lett. 320, 150-154.
52. Evans, D.L. & Dive, C. (1993). Effects of cisplatin on the induction of apoptosis in proliferating hepatoma cells and nonproliferating immature thymocytes. Cancer Res. 53, 2133-2139.
53. Shinomiya, N., Shinomiya, M., Wakiyama, H., Katsura, Y. & Rokutanda, M. (1994). Enhancement of CDDP cytotoxicity by caffeine is characterized by apoptotic cell death. Exp. Cell Res. 210, 236-242.
54. Feuer, E.J., Brown, L.M. and Kaplan, R.S. (1993) in SEER Cancer Statistics Review: 1973-1990 (Miller, BA., et al., & Edwards, B.K., eds) pp. XXIV.1-XXIV.13, NIH Publication No. 93-2789: National Cancer Institute, Bethesda, MD.
55. Watt, G.W. & Cude, W.A. (1968). Diethylenetriamine complexes of platinum(II) halides. Inorg. Chem. 7, 335-338.
56. 2]. Indian J. Chem. 8, 193-194.
57. Lippard, S.J., Ushay, H.M., Merkel, C.M. & Poirier, M.C. (1983). Use of antibodies to probe the stereochemistry of antitumor platinum drug binding to deoxyribonucleic acid. Biochemistry 22, 5165-5168.
58. Creighton, T.E. (1993). Interactions with other molecules. In Proteins: Structures and Molecular Properties. (2nd edn), pp. 367-382, Freeman and Company, New York.
59. Dignam, J.D., Lebovitz, R.M. & Roeder, R.G. (1983). Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 11, 1475-1489.