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. 1999 Feb 15;338(Pt 1):1–13.

Recognition of DNA alterations by the mismatch repair system.

G Marra 1, P Schär 1
PMCID: PMC1220017  PMID: 9931291

Abstract

Misincorporation of non-complementary bases by DNA polymerases is a major source of the occurrence of promutagenic base-pairing errors during DNA replication or repair. Base-base mismatches or loops of extra bases can arise which, if left unrepaired, will generate point or frameshift mutations respectively. To counteract this mutagenic potential, organisms have developed a number of elaborate surveillance and repair strategies which co-operate to maintain the integrity of their genomes. An important replication-associated correction function is provided by the post-replicative mismatch repair system. This system is highly conserved among species and appears to be the major pathway for strand-specific elimination of base-base mispairs and short insertion/deletion loops (IDLs), not only during DNA replication, but also in intermediates of homologous recombination. The efficiency of repair of different base-pairing errors in the DNA varies, and appears to depend on multiple factors, such as the physical structure of the mismatch and sequence context effects. These structural aspects of mismatch repair are poorly understood. In contrast, remarkable progress in understanding the biochemical role of error-recognition proteins has been made in the recent past. In eukaryotes, two heterodimers consisting of MutS-homologous proteins have been shown to share the function of mismatch recognition in vivo and in vitro. A first MutS homologue, MSH2, is present in both heterodimers, and the specificity for mismatch recognition is dictated by its association with either of two other MutS homologues: MSH6 for recognition of base-base mismatches and small IDLs, or MSH3 for recognition of IDLs only. Mismatch repair deficiency in cells can arise through mutation, transcriptional silencing or as a result of imbalanced expression of these genes.

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Selected References

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  1. 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. Clues to the pathogenesis of familial colorectal cancer. Science. 1993 May 7;260(5109):812–816. doi: 10.1126/science.8484121. [DOI] [PubMed] [Google Scholar]
  2. Aboul-ela F., Koh D., Tinoco I., Jr, Martin F. H. Base-base mismatches. Thermodynamics of double helix formation for dCA3XA3G + dCT3YT3G (X, Y = A,C,G,T). Nucleic Acids Res. 1985 Jul 11;13(13):4811–4824. doi: 10.1093/nar/13.13.4811. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Acharya S., Wilson T., Gradia S., Kane M. F., Guerrette S., Marsischky G. T., Kolodner R., Fishel R. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci U S A. 1996 Nov 26;93(24):13629–13634. doi: 10.1073/pnas.93.24.13629. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aebi S., Kurdi-Haidar B., Gordon R., Cenni B., Zheng H., Fink D., Christen R. D., Boland C. R., Koi M., Fishel R. Loss of DNA mismatch repair in acquired resistance to cisplatin. Cancer Res. 1996 Jul 1;56(13):3087–3090. [PubMed] [Google Scholar]
  5. Alani E., Chi N. W., Kolodner R. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and insertions. Genes Dev. 1995 Jan 15;9(2):234–247. doi: 10.1101/gad.9.2.234. [DOI] [PubMed] [Google Scholar]
  6. Alani E., Sokolsky T., Studamire B., Miret J. J., Lahue R. S. Genetic and biochemical analysis of Msh2p-Msh6p: role of ATP hydrolysis and Msh2p-Msh6p subunit interactions in mismatch base pair recognition. Mol Cell Biol. 1997 May;17(5):2436–2447. doi: 10.1128/mcb.17.5.2436. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Alani E. The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs. Mol Cell Biol. 1996 Oct;16(10):5604–5615. doi: 10.1128/mcb.16.10.5604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Allen D. J., Makhov A., Grilley M., Taylor J., Thresher R., Modrich P., Griffith J. D. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 1997 Jul 16;16(14):4467–4476. doi: 10.1093/emboj/16.14.4467. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Anthoney D. A., McIlwrath A. J., Gallagher W. M., Edlin A. R., Brown R. Microsatellite instability, apoptosis, and loss of p53 function in drug-resistant tumor cells. Cancer Res. 1996 Mar 15;56(6):1374–1381. [PubMed] [Google Scholar]
  10. Armstrong M. J., Galloway S. M. Mismatch repair provokes chromosome aberrations in hamster cells treated with methylating agents or 6-thioguanine, but not with ethylating agents. Mutat Res. 1997 Feb 3;373(2):167–178. doi: 10.1016/s0027-5107(96)00234-5. [DOI] [PubMed] [Google Scholar]
  11. Au K. G., Welsh K., Modrich P. Initiation of methyl-directed mismatch repair. J Biol Chem. 1992 Jun 15;267(17):12142–12148. [PubMed] [Google Scholar]
  12. Barry M. A., Behnke C. A., Eastman A. Activation of programmed cell death (apoptosis) by cisplatin, other anticancer drugs, toxins and hyperthermia. Biochem Pharmacol. 1990 Nov 15;40(10):2353–2362. doi: 10.1016/0006-2952(90)90733-2. [DOI] [PubMed] [Google Scholar]
  13. Basu A. K., Essigmann J. M. Site-specifically alkylated oligodeoxynucleotides: probes for mutagenesis, DNA repair and the structural effects of DNA damage. Mutat Res. 1990 Nov-Dec;233(1-2):189–201. doi: 10.1016/0027-5107(90)90162-w. [DOI] [PubMed] [Google Scholar]
  14. Bawa S., Xiao W. A mutation in the MSH5 gene results in alkylation tolerance. Cancer Res. 1997 Jul 1;57(13):2715–2720. [PubMed] [Google Scholar]
  15. Bedford P., Fichtinger-Schepman A. M., Shellard S. A., Walker M. C., Masters J. R., Hill B. T. Differential repair of platinum-DNA adducts in human bladder and testicular tumor continuous cell lines. Cancer Res. 1988 Jun 1;48(11):3019–3024. [PubMed] [Google Scholar]
  16. Bishop D. K., Andersen J., Kolodner R. D. Specificity of mismatch repair following transformation of Saccharomyces cerevisiae with heteroduplex plasmid DNA. Proc Natl Acad Sci U S A. 1989 May;86(10):3713–3717. doi: 10.1073/pnas.86.10.3713. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Branch P., Aquilina G., Bignami M., Karran P. Defective mismatch binding and a mutator phenotype in cells tolerant to DNA damage. Nature. 1993 Apr 15;362(6421):652–654. doi: 10.1038/362652a0. [DOI] [PubMed] [Google Scholar]
  18. Branch P., Hampson R., Karran P. DNA mismatch binding defects, DNA damage tolerance, and mutator phenotypes in human colorectal carcinoma cell lines. Cancer Res. 1995 Jun 1;55(11):2304–2309. [PubMed] [Google Scholar]
  19. Brooks P., Dohet C., Almouzni G., Méchali M., Radman M. Mismatch repair involving localized DNA synthesis in extracts of Xenopus eggs. Proc Natl Acad Sci U S A. 1989 Jun;86(12):4425–4429. doi: 10.1073/pnas.86.12.4425. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Brown T. C., Jiricny J. A specific mismatch repair event protects mammalian cells from loss of 5-methylcytosine. Cell. 1987 Sep 11;50(6):945–950. doi: 10.1016/0092-8674(87)90521-6. [DOI] [PubMed] [Google Scholar]
  21. Brown T. C., Jiricny J. Different base/base mispairs are corrected with different efficiencies and specificities in monkey kidney cells. Cell. 1988 Aug 26;54(5):705–711. doi: 10.1016/s0092-8674(88)80015-1. [DOI] [PubMed] [Google Scholar]
  22. Brown T., Hunter W. N., Kneale G., Kennard O. Molecular structure of the G.A base pair in DNA and its implications for the mechanism of transversion mutations. Proc Natl Acad Sci U S A. 1986 Apr;83(8):2402–2406. doi: 10.1073/pnas.83.8.2402. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Bruhn S. L., Pil P. M., Essigmann J. M., Housman D. E., Lippard S. J. 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 U S A. 1992 Mar 15;89(6):2307–2311. doi: 10.1073/pnas.89.6.2307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Calsou P., Frit P., Salles B. Repair synthesis by human cell extracts in cisplatin-damaged DNA is preferentially determined by minor adducts. Nucleic Acids Res. 1992 Dec 11;20(23):6363–6368. doi: 10.1093/nar/20.23.6363. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Chu G. Cellular responses to cisplatin. The roles of DNA-binding proteins and DNA repair. J Biol Chem. 1994 Jan 14;269(2):787–790. [PubMed] [Google Scholar]
  26. Ciccarelli R. B., Solomon M. J., Varshavsky A., Lippard S. J. In vivo effects of cis- and trans-diamminedichloroplatinum(II) on SV40 chromosomes: differential repair, DNA-protein cross-linking, and inhibition of replication. Biochemistry. 1985 Dec 17;24(26):7533–7540. doi: 10.1021/bi00347a005. [DOI] [PubMed] [Google Scholar]
  27. Claverys J. P., Lacks S. A. Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria. Microbiol Rev. 1986 Jun;50(2):133–165. doi: 10.1128/mr.50.2.133-165.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Cooper D. L., Lahue R. S., Modrich P. Methyl-directed mismatch repair is bidirectional. J Biol Chem. 1993 Jun 5;268(16):11823–11829. [PubMed] [Google Scholar]
  29. Cornelis A. G., Haasnoot J. H., den Hartog J. F., de Rooij M., van Boom J. H., Cornelis A. Local destabilisation of a DNA double helix by a T--T wobble pair. Nature. 1979 Sep 20;281(5728):235–236. doi: 10.1038/281235a0. [DOI] [PubMed] [Google Scholar]
  30. Cox E. C. Bacterial mutator genes and the control of spontaneous mutation. Annu Rev Genet. 1976;10:135–156. doi: 10.1146/annurev.ge.10.120176.001031. [DOI] [PubMed] [Google Scholar]
  31. Cryer J. E., Johnson S. W., Engelsberg B. N., Billings P. C. Analysis of HMG protein binding to DNA modified with the anticancer drug cisplatin. Cancer Chemother Pharmacol. 1996;38(2):163–168. doi: 10.1007/s002800050465. [DOI] [PubMed] [Google Scholar]
  32. Detloff P., Sieber J., Petes T. D. Repair of specific base pair mismatches formed during meiotic recombination in the yeast Saccharomyces cerevisiae. Mol Cell Biol. 1991 Feb;11(2):737–745. doi: 10.1128/mcb.11.2.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Dohet C., Wagner R., Radman M. Repair of defined single base-pair mismatches in Escherichia coli. Proc Natl Acad Sci U S A. 1985 Jan;82(2):503–505. doi: 10.1073/pnas.82.2.503. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Drummond J. T., Anthoney A., Brown R., Modrich P. Cisplatin and adriamycin resistance are associated with MutLalpha and mismatch repair deficiency in an ovarian tumor cell line. J Biol Chem. 1996 Aug 16;271(33):19645–19648. doi: 10.1074/jbc.271.33.19645. [DOI] [PubMed] [Google Scholar]
  35. Drummond J. T., Genschel J., Wolf E., Modrich P. DHFR/MSH3 amplification in methotrexate-resistant cells alters the hMutSalpha/hMutSbeta ratio and reduces the efficiency of base-base mismatch repair. Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10144–10149. doi: 10.1073/pnas.94.19.10144. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Drummond J. T., Li G. M., Longley M. J., Modrich P. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science. 1995 Jun 30;268(5219):1909–1912. doi: 10.1126/science.7604264. [DOI] [PubMed] [Google Scholar]
  37. 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 U S A. 1996 Jun 25;93(13):6443–6447. doi: 10.1073/pnas.93.13.6443. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Eastman A. Characterization of the adducts produced in DNA by cis-diamminedichloroplatinum(II) and cis-dichloro(ethylenediamine)platinum(II). Biochemistry. 1983 Aug 2;22(16):3927–3933. doi: 10.1021/bi00285a031. [DOI] [PubMed] [Google Scholar]
  39. Eastman A., Schulte N. Enhanced DNA repair as a mechanism of resistance to cis-diamminedichloroplatinum(II). Biochemistry. 1988 Jun 28;27(13):4730–4734. doi: 10.1021/bi00413a022. [DOI] [PubMed] [Google Scholar]
  40. Eastman A. The formation, isolation and characterization of DNA adducts produced by anticancer platinum complexes. Pharmacol Ther. 1987;34(2):155–166. doi: 10.1016/0163-7258(87)90009-x. [DOI] [PubMed] [Google Scholar]
  41. Echols H., Goodman M. F. Fidelity mechanisms in DNA replication. Annu Rev Biochem. 1991;60:477–511. doi: 10.1146/annurev.bi.60.070191.002401. [DOI] [PubMed] [Google Scholar]
  42. Fang W. H., Modrich P. Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction. J Biol Chem. 1993 Jun 5;268(16):11838–11844. [PubMed] [Google Scholar]
  43. Fink D., Zheng H., Nebel S., Norris P. S., Aebi S., Lin T. P., Nehmé A., Christen R. D., Haas M., MacLeod C. L. In vitro and in vivo resistance to cisplatin in cells that have lost DNA mismatch repair. Cancer Res. 1997 May 15;57(10):1841–1845. [PubMed] [Google Scholar]
  44. Fishel R., Ewel A., Lee S., Lescoe M. K., Griffith J. Binding of mismatched microsatellite DNA sequences by the human MSH2 protein. Science. 1994 Nov 25;266(5189):1403–1405. doi: 10.1126/science.7973733. [DOI] [PubMed] [Google Scholar]
  45. Fishel R., Ewel A., Lescoe M. K. Purified human MSH2 protein binds to DNA containing mismatched nucleotides. Cancer Res. 1994 Nov 1;54(21):5539–5542. [PubMed] [Google Scholar]
  46. Fishel R., Lescoe M. K., Rao M. R., Copeland N. G., Jenkins N. A., Garber J., Kane M., Kolodner R. The human mutator gene homolog MSH2 and its association with hereditary nonpolyposis colon cancer. Cell. 1993 Dec 3;75(5):1027–1038. doi: 10.1016/0092-8674(93)90546-3. [DOI] [PubMed] [Google Scholar]
  47. Fram R. J. Cisplatin and platinum analogues: recent advances. Curr Opin Oncol. 1992 Dec;4(6):1073–1079. doi: 10.1097/00001622-199212000-00012. [DOI] [PubMed] [Google Scholar]
  48. Fujii H., 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. 1989 Jun 15;264(17):10057–10064. [PubMed] [Google Scholar]
  49. Galloway S. M., Greenwood S. K., Hill R. B., Bradt C. I., Bean C. L. A role for mismatch repair in production of chromosome aberrations by methylating agents in human cells. Mutat Res. 1995 Apr;346(4):231–245. doi: 10.1016/0165-7992(95)90040-3. [DOI] [PubMed] [Google Scholar]
  50. Glazer P. M., Sarkar S. N., Chisholm G. E., Summers W. C. DNA mismatch repair detected in human cell extracts. Mol Cell Biol. 1987 Jan;7(1):218–224. doi: 10.1128/mcb.7.1.218. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Goldmacher V. S., Cuzick R. A., Jr, Thilly W. G. 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. 1986 Sep 25;261(27):12462–12471. [PubMed] [Google Scholar]
  52. Gradia S., Acharya S., Fishel R. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell. 1997 Dec 26;91(7):995–1005. doi: 10.1016/s0092-8674(00)80490-0. [DOI] [PubMed] [Google Scholar]
  53. Grilley M., Welsh K. M., Su S. S., Modrich P. Isolation and characterization of the Escherichia coli mutL gene product. J Biol Chem. 1989 Jan 15;264(2):1000–1004. [PubMed] [Google Scholar]
  54. Gu L., Hong Y., McCulloch S., Watanabe H., Li G. M. ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair. Nucleic Acids Res. 1998 Mar 1;26(5):1173–1178. doi: 10.1093/nar/26.5.1173. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Guild W. R., Shoemaker N. B. Mismatch correction in pneumococcal transformation: donor length and hex-dependent marker efficiency. J Bacteriol. 1976 Jan;125(1):125–135. doi: 10.1128/jb.125.1.125-135.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Haber L. T., Pang P. P., Sobell D. I., Mankovich J. A., Walker G. C. Nucleotide sequence of the Salmonella typhimurium mutS gene required for mismatch repair: homology of MutS and HexA of Streptococcus pneumoniae. J Bacteriol. 1988 Jan;170(1):197–202. doi: 10.1128/jb.170.1.197-202.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Haber L. T., Walker G. C. Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities. EMBO J. 1991 Sep;10(9):2707–2715. doi: 10.1002/j.1460-2075.1991.tb07815.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Habraken Y., Sung P., Prakash L., Prakash S. Binding of insertion/deletion DNA mismatches by the heterodimer of yeast mismatch repair proteins MSH2 and MSH3. Curr Biol. 1996 Sep 1;6(9):1185–1187. doi: 10.1016/s0960-9822(02)70686-6. [DOI] [PubMed] [Google Scholar]
  59. Habraken Y., Sung P., Prakash L., Prakash S. Enhancement of MSH2-MSH3-mediated mismatch recognition by the yeast MLH1-PMS1 complex. Curr Biol. 1997 Oct 1;7(10):790–793. doi: 10.1016/s0960-9822(06)00337-x. [DOI] [PubMed] [Google Scholar]
  60. Hare D., Shapiro L., Patel D. J. Extrahelical adenosine stacks into right-handed DNA: solution conformation of the d(C-G-C-A-G-A-G-C-T-C-G-C-G) duplex deduced from distance geometry analysis of nuclear Overhauser effect spectra. Biochemistry. 1986 Nov 18;25(23):7456–7464. doi: 10.1021/bi00371a030. [DOI] [PubMed] [Google Scholar]
  61. 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. 1995 Sep 1;55(17):3721–3725. [PubMed] [Google Scholar]
  62. Heiger-Bernays W. J., Essigmann J. M., Lippard S. J. Effect of the antitumor drug cis-diamminedichloroplatinum(II) and related platinum complexes on eukaryotic DNA replication. Biochemistry. 1990 Sep 11;29(36):8461–8466. doi: 10.1021/bi00488a037. [DOI] [PubMed] [Google Scholar]
  63. Herman G. E., Modrich P. Escherichia coli K-12 clones that overproduce dam methylase are hypermutable. J Bacteriol. 1981 Jan;145(1):644–646. doi: 10.1128/jb.145.1.644-646.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Ho P. S., Frederick C. A., Quigley G. J., van der Marel G. A., van Boom J. H., Wang A. H., Rich A. G.T wobble base-pairing in Z-DNA at 1.0 A atomic resolution: the crystal structure of d(CGCGTG). EMBO J. 1985 Dec 16;4(13A):3617–3623. doi: 10.1002/j.1460-2075.1985.tb04125.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Hoffmann J. S., Locker D., Villani G., Leng M. HMG1 protein inhibits the translesion synthesis of the major DNA cisplatin adduct by cell extracts. J Mol Biol. 1997 Jul 25;270(4):539–543. doi: 10.1006/jmbi.1997.1143. [DOI] [PubMed] [Google Scholar]
  66. Hoffmann J. S., Pillaire M. J., Maga G., Podust V., Hübscher U., Villani G. DNA polymerase beta bypasses in vitro a single d(GpG)-cisplatin adduct placed on codon 13 of the HRAS gene. Proc Natl Acad Sci U S A. 1995 Jun 6;92(12):5356–5360. doi: 10.1073/pnas.92.12.5356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Holmes J., Jr, Clark S., Modrich P. Strand-specific mismatch correction in nuclear extracts of human and Drosophila melanogaster cell lines. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5837–5841. doi: 10.1073/pnas.87.15.5837. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Hughes E. N., Engelsberg B. N., Billings P. C. Purification of nuclear proteins that bind to cisplatin-damaged DNA. Identity with high mobility group proteins 1 and 2. J Biol Chem. 1992 Jul 5;267(19):13520–13527. [PubMed] [Google Scholar]
  69. Hughes M. J., Jiricny J. The purification of a human mismatch-binding protein and identification of its associated ATPase and helicase activities. J Biol Chem. 1992 Nov 25;267(33):23876–23882. [PubMed] [Google Scholar]
  70. Hunter W. N., Brown T., Anand N. N., Kennard O. Structure of an adenine-cytosine base pair in DNA and its implications for mismatch repair. Nature. 1986 Apr 10;320(6062):552–555. doi: 10.1038/320552a0. [DOI] [PubMed] [Google Scholar]
  71. Iaccarino I., Marra G., Palombo F., Jiricny J. hMSH2 and hMSH6 play distinct roles in mismatch binding and contribute differently to the ATPase activity of hMutSalpha. EMBO J. 1998 May 1;17(9):2677–2686. doi: 10.1093/emboj/17.9.2677. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Iaccarino I., Palombo F., Drummond J., Totty N. F., Hsuan J. J., Modrich P., Jiricny J. MSH6, a Saccharomyces cerevisiae protein that binds to mismatches as a heterodimer with MSH2. Curr Biol. 1996 Apr 1;6(4):484–486. doi: 10.1016/s0960-9822(02)00516-x. [DOI] [PubMed] [Google Scholar]
  73. Ionov Y., Peinado M. A., Malkhosyan S., Shibata D., Perucho M. Ubiquitous somatic mutations in simple repeated sequences reveal a new mechanism for colonic carcinogenesis. Nature. 1993 Jun 10;363(6429):558–561. doi: 10.1038/363558a0. [DOI] [PubMed] [Google Scholar]
  74. Jiricny J., Hughes M., Corman N., Rudkin B. B. A human 200-kDa protein binds selectively to DNA fragments containing G.T mismatches. Proc Natl Acad Sci U S A. 1988 Dec;85(23):8860–8864. doi: 10.1073/pnas.85.23.8860. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Jiricny J. Mismatch repair and cancer. Cancer Surv. 1996;28:47–68. [PubMed] [Google Scholar]
  76. Jiricny J., Su S. S., Wood S. G., Modrich P. Mismatch-containing oligonucleotide duplexes bound by the E. coli mutS-encoded protein. Nucleic Acids Res. 1988 Aug 25;16(16):7843–7853. doi: 10.1093/nar/16.16.7843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  77. Johnson R. E., Kovvali G. K., Prakash L., Prakash S. Requirement of the yeast MSH3 and MSH6 genes for MSH2-dependent genomic stability. J Biol Chem. 1996 Mar 29;271(13):7285–7288. doi: 10.1074/jbc.271.13.7285. [DOI] [PubMed] [Google Scholar]
  78. Jones M., Wagner R., Radman M. Mismatch repair and recombination in E. coli. Cell. 1987 Aug 14;50(4):621–626. doi: 10.1016/0092-8674(87)90035-3. [DOI] [PubMed] [Google Scholar]
  79. Jones M., Wagner R., Radman M. Mismatch repair of deaminated 5-methyl-cytosine. J Mol Biol. 1987 Mar 5;194(1):155–159. doi: 10.1016/0022-2836(87)90724-8. [DOI] [PubMed] [Google Scholar]
  80. Karran P., Bignami M. Drug-related killings: a case of mistaken identity. Chem Biol. 1996 Nov;3(11):875–879. doi: 10.1016/s1074-5521(96)90175-1. [DOI] [PubMed] [Google Scholar]
  81. Karran P., Bignami M. Self-destruction and tolerance in resistance of mammalian cells to alkylation damage. Nucleic Acids Res. 1992 Jun 25;20(12):2933–2940. doi: 10.1093/nar/20.12.2933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Karran P., Marinus M. G. Mismatch correction at O6-methylguanine residues in E. coli DNA. Nature. 1982 Apr 29;296(5860):868–869. doi: 10.1038/296868a0. [DOI] [PubMed] [Google Scholar]
  83. Kat A., Thilly W. G., Fang W. H., Longley M. J., Li G. M., Modrich P. An alkylation-tolerant, mutator human cell line is deficient in strand-specific mismatch repair. Proc Natl Acad Sci U S A. 1993 Jul 15;90(14):6424–6428. doi: 10.1073/pnas.90.14.6424. [DOI] [PMC free article] [PubMed] [Google Scholar]
  84. Koi M., Umar A., Chauhan D. P., Cherian S. P., Carethers J. M., Kunkel T. A., 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. 1994 Aug 15;54(16):4308–4312. [PubMed] [Google Scholar]
  85. Kolodner R. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev. 1996 Jun 15;10(12):1433–1442. doi: 10.1101/gad.10.12.1433. [DOI] [PubMed] [Google Scholar]
  86. Kramer B., Kramer W., Fritz H. J. Different base/base mismatches are corrected with different efficiencies by the methyl-directed DNA mismatch-repair system of E. coli. Cell. 1984 Oct;38(3):879–887. doi: 10.1016/0092-8674(84)90283-6. [DOI] [PubMed] [Google Scholar]
  87. Kramer B., Kramer W., Williamson M. S., Fogel S. Heteroduplex DNA correction in Saccharomyces cerevisiae is mismatch specific and requires functional PMS genes. Mol Cell Biol. 1989 Oct;9(10):4432–4440. doi: 10.1128/mcb.9.10.4432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Lacks S. A., Dunn J. J., Greenberg B. Identification of base mismatches recognized by the heteroduplex-DNA-repair system of Streptococcus pneumoniae. Cell. 1982 Dec;31(2 Pt 1):327–336. doi: 10.1016/0092-8674(82)90126-x. [DOI] [PubMed] [Google Scholar]
  89. Laengle-Rouault F., Maenhaut-Michel G., Radman M. GATC sequence and mismatch repair in Escherichia coli. EMBO J. 1986 Aug;5(8):2009–2013. doi: 10.1002/j.1460-2075.1986.tb04457.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  90. Lahue R. S., Au K. G., Modrich P. DNA mismatch correction in a defined system. Science. 1989 Jul 14;245(4914):160–164. doi: 10.1126/science.2665076. [DOI] [PubMed] [Google Scholar]
  91. Leach F. S., Nicolaides N. C., Papadopoulos N., Liu B., Jen J., Parsons R., Peltomäki P., Sistonen P., Aaltonen L. A., Nyström-Lahti M. Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer. Cell. 1993 Dec 17;75(6):1215–1225. doi: 10.1016/0092-8674(93)90330-s. [DOI] [PubMed] [Google Scholar]
  92. Liu K., Niu L., Linton J. P., Crouse G. F. Characterization of the mouse Rep-3 gene: sequence similarities to bacterial and yeast mismatch-repair proteins. Gene. 1994 Sep 30;147(2):169–177. doi: 10.1016/0378-1119(94)90062-0. [DOI] [PubMed] [Google Scholar]
  93. Longley M. J., Pierce A. J., Modrich P. DNA polymerase delta is required for human mismatch repair in vitro. J Biol Chem. 1997 Apr 18;272(16):10917–10921. doi: 10.1074/jbc.272.16.10917. [DOI] [PubMed] [Google Scholar]
  94. Lu A. L., Clark S., Modrich P. Methyl-directed repair of DNA base-pair mismatches in vitro. Proc Natl Acad Sci U S A. 1983 Aug;80(15):4639–4643. doi: 10.1073/pnas.80.15.4639. [DOI] [PMC free article] [PubMed] [Google Scholar]
  95. Längle-Rouault F., Maenhaut-Michel G., Radman M. GATC sequences, DNA nicks and the MutH function in Escherichia coli mismatch repair. EMBO J. 1987 Apr;6(4):1121–1127. doi: 10.1002/j.1460-2075.1987.tb04867.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  96. Mamenta E. L., Poma E. E., Kaufmann W. K., Delmastro D. A., Grady H. L., Chaney S. G. Enhanced replicative bypass of platinum-DNA adducts in cisplatin-resistant human ovarian carcinoma cell lines. Cancer Res. 1994 Jul 1;54(13):3500–3505. [PubMed] [Google Scholar]
  97. Marinus M. G., Morris N. R. Pleiotropic effects of a DNA adenine methylation mutation (dam-3) in Escherichia coli K12. Mutat Res. 1975 Apr;28(1):15–26. doi: 10.1016/0027-5107(75)90309-7. [DOI] [PubMed] [Google Scholar]
  98. Marra G., Boland C. R. Hereditary nonpolyposis colorectal cancer: the syndrome, the genes, and historical perspectives. J Natl Cancer Inst. 1995 Aug 2;87(15):1114–1125. doi: 10.1093/jnci/87.15.1114. [DOI] [PubMed] [Google Scholar]
  99. Marra G., Iaccarino I., Lettieri T., Roscilli G., Delmastro P., Jiricny J. Mismatch repair deficiency associated with overexpression of the MSH3 gene. Proc Natl Acad Sci U S A. 1998 Jul 21;95(15):8568–8573. doi: 10.1073/pnas.95.15.8568. [DOI] [PMC free article] [PubMed] [Google Scholar]
  100. Marsischky G. T., Filosi N., Kane M. F., Kolodner R. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 1996 Feb 15;10(4):407–420. doi: 10.1101/gad.10.4.407. [DOI] [PubMed] [Google Scholar]
  101. Mello J. A., Acharya S., Fishel R., Essigmann J. M. The mismatch-repair protein hMSH2 binds selectively to DNA adducts of the anticancer drug cisplatin. Chem Biol. 1996 Jul;3(7):579–589. doi: 10.1016/s1074-5521(96)90149-0. [DOI] [PubMed] [Google Scholar]
  102. Miret J. J., Milla M. G., Lahue R. S. Characterization of a DNA mismatch-binding activity in yeast extracts. J Biol Chem. 1993 Feb 15;268(5):3507–3513. [PubMed] [Google Scholar]
  103. Miret J. J., Parker B. O., Lahua R. S. Recognition of DNA insertion/deletion mismatches by an activity in Saccharomyces cerevisiae. Nucleic Acids Res. 1996 Feb 15;24(4):721–729. doi: 10.1093/nar/24.4.721. [DOI] [PMC free article] [PubMed] [Google Scholar]
  104. Modrich P. Mechanisms and biological effects of mismatch repair. Annu Rev Genet. 1991;25:229–253. doi: 10.1146/annurev.ge.25.120191.001305. [DOI] [PubMed] [Google Scholar]
  105. Modrich P. Strand-specific mismatch repair in mammalian cells. J Biol Chem. 1997 Oct 3;272(40):24727–24730. doi: 10.1074/jbc.272.40.24727. [DOI] [PubMed] [Google Scholar]
  106. Moggs J. G., Szymkowski D. E., Yamada M., Karran P., Wood R. D. Differential human nucleotide excision repair of paired and mispaired cisplatin-DNA adducts. Nucleic Acids Res. 1997 Feb 1;25(3):480–491. doi: 10.1093/nar/25.3.480. [DOI] [PMC free article] [PubMed] [Google Scholar]
  107. Moggs J. G., Yarema K. J., Essigmann J. M., Wood R. D. Analysis of incision sites produced by human cell extracts and purified proteins during nucleotide excision repair of a 1,3-intrastrand d(GpTpG)-cisplatin adduct. J Biol Chem. 1996 Mar 22;271(12):7177–7186. doi: 10.1074/jbc.271.12.7177. [DOI] [PubMed] [Google Scholar]
  108. 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. 1997 Feb;17(2):760–769. doi: 10.1128/mcb.17.2.760. [DOI] [PMC free article] [PubMed] [Google Scholar]
  109. Nevers P., Spatz H. C. Escherichia coli mutants uvr D and uvr E deficient in gene conversion of lambda-heteroduplexes. Mol Gen Genet. 1975 Aug 27;139(3):233–243. doi: 10.1007/BF00268974. [DOI] [PubMed] [Google Scholar]
  110. O'Regan N. E., Branch P., Macpherson P., Karran P. hMSH2-independent DNA mismatch recognition by human proteins. J Biol Chem. 1996 Jan 19;271(3):1789–1796. doi: 10.1074/jbc.271.3.1789. [DOI] [PubMed] [Google Scholar]
  111. Palombo F., Gallinari P., Iaccarino I., Lettieri T., Hughes M., D'Arrigo A., Truong O., Hsuan J. J., Jiricny J. GTBP, a 160-kilodalton protein essential for mismatch-binding activity in human cells. Science. 1995 Jun 30;268(5219):1912–1914. doi: 10.1126/science.7604265. [DOI] [PubMed] [Google Scholar]
  112. Palombo F., Hughes M., Jiricny J., Truong O., Hsuan J. Mismatch repair and cancer. Nature. 1994 Feb 3;367(6462):417–417. doi: 10.1038/367417a0. [DOI] [PubMed] [Google Scholar]
  113. Palombo F., Iaccarino I., Nakajima E., Ikejima M., Shimada T., Jiricny J. hMutSbeta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr Biol. 1996 Sep 1;6(9):1181–1184. doi: 10.1016/s0960-9822(02)70685-4. [DOI] [PubMed] [Google Scholar]
  114. Papadopoulos N., Nicolaides N. C., Liu B., Parsons R., Lengauer C., Palombo F., D'Arrigo A., Markowitz S., Willson J. K., Kinzler K. W. Mutations of GTBP in genetically unstable cells. Science. 1995 Jun 30;268(5219):1915–1917. doi: 10.1126/science.7604266. [DOI] [PubMed] [Google Scholar]
  115. Parker B. O., Marinus M. G. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli. Proc Natl Acad Sci U S A. 1992 Mar 1;89(5):1730–1734. doi: 10.1073/pnas.89.5.1730. [DOI] [PMC free article] [PubMed] [Google Scholar]
  116. Perucho M. Cancer of the microsatellite mutator phenotype. Biol Chem. 1996 Nov;377(11):675–684. [PubMed] [Google Scholar]
  117. Pil P. M., Lippard S. J. Specific binding of chromosomal protein HMG1 to DNA damaged by the anticancer drug cisplatin. Science. 1992 Apr 10;256(5054):234–237. doi: 10.1126/science.1566071. [DOI] [PubMed] [Google Scholar]
  118. Pinto A. L., Lippard S. J. Binding of the antitumor drug cis-diamminedichloroplatinum(II) (cisplatin) to DNA. Biochim Biophys Acta. 1985;780(3):167–180. doi: 10.1016/0304-419x(85)90001-0. [DOI] [PubMed] [Google Scholar]
  119. Priebe S. D., Hadi S. M., Greenberg B., Lacks S. A. Nucleotide sequence of the hexA gene for DNA mismatch repair in Streptococcus pneumoniae and homology of hexA to mutS of Escherichia coli and Salmonella typhimurium. J Bacteriol. 1988 Jan;170(1):190–196. doi: 10.1128/jb.170.1.190-196.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  120. Pukkila P. J., Peterson J., Herman G., Modrich P., Meselson M. Effects of high levels of DNA adenine methylation on methyl-directed mismatch repair in Escherichia coli. Genetics. 1983 Aug;104(4):571–582. doi: 10.1093/genetics/104.4.571. [DOI] [PMC free article] [PubMed] [Google Scholar]
  121. Radicella J. P., Clark E. A., Fox M. S. Some mismatch repair activities in Escherichia coli. Proc Natl Acad Sci U S A. 1988 Dec;85(24):9674–9678. doi: 10.1073/pnas.85.24.9674. [DOI] [PMC free article] [PubMed] [Google Scholar]
  122. Rasouli-Nia A., Sibghat-Ullah, Mirzayans R., Paterson M. C., Day R. S., 3rd On the quantitative relationship between O6-methylguanine residues in genomic DNA and production of sister-chromatid exchanges, mutations and lethal events in a Mer- human tumor cell line. Mutat Res. 1994 Mar;314(2):99–113. doi: 10.1016/0921-8777(94)90074-4. [DOI] [PubMed] [Google Scholar]
  123. Reenan R. A., Kolodner R. D. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics. 1992 Dec;132(4):975–985. doi: 10.1093/genetics/132.4.975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  124. Rydberg B. Bromouracil mutagenesis and mismatch repair in mutator strains of Escherichia coli. Mutat Res. 1978 Oct;52(1):11–24. doi: 10.1016/0027-5107(78)90091-x. [DOI] [PubMed] [Google Scholar]
  125. Schär P., Baur M., Schneider C., Kohli J. Mismatch repair in Schizosaccharomyces pombe requires the mutL homologous gene pms1: molecular cloning and functional analysis. Genetics. 1997 Aug;146(4):1275–1286. doi: 10.1093/genetics/146.4.1275. [DOI] [PMC free article] [PubMed] [Google Scholar]
  126. Schär P., Munz P., Kohli J. Meiotic mismatch repair quantified on the basis of segregation patterns in Schizosaccharomyces pombe. Genetics. 1993 Apr;133(4):815–824. doi: 10.1093/genetics/133.4.815. [DOI] [PMC free article] [PubMed] [Google Scholar]
  127. Sibghat-Ullah, Day R. S., 3rd Incision at O6-methylguanine:thymine mispairs in DNA by extracts of human cells. Biochemistry. 1992 Sep 1;31(34):7998–8008. doi: 10.1021/bi00149a034. [DOI] [PubMed] [Google Scholar]
  128. Stephenson C., Karran P. Selective binding to DNA base pair mismatches by proteins from human cells. J Biol Chem. 1989 Dec 15;264(35):21177–21182. [PubMed] [Google Scholar]
  129. Strand M., Earley M. C., Crouse G. F., Petes T. D. Mutations in the MSH3 gene preferentially lead to deletions within tracts of simple repetitive DNA in Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1995 Oct 24;92(22):10418–10421. doi: 10.1073/pnas.92.22.10418. [DOI] [PMC free article] [PubMed] [Google Scholar]
  130. Su S. S., Modrich P. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc Natl Acad Sci U S A. 1986 Jul;83(14):5057–5061. doi: 10.1073/pnas.83.14.5057. [DOI] [PMC free article] [PubMed] [Google Scholar]
  131. Szankasi P., Smith G. R. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science. 1995 Feb 24;267(5201):1166–1169. doi: 10.1126/science.7855597. [DOI] [PubMed] [Google Scholar]
  132. Szymkowski D. E., Yarema K., Essigmann J. M., Lippard S. J., Wood R. D. An intrastrand d(GpG) platinum crosslink in duplex M13 DNA is refractory to repair by human cell extracts. Proc Natl Acad Sci U S A. 1992 Nov 15;89(22):10772–10776. doi: 10.1073/pnas.89.22.10772. [DOI] [PMC free article] [PubMed] [Google Scholar]
  133. Thibodeau S. N., Bren G., Schaid D. Microsatellite instability in cancer of the proximal colon. Science. 1993 May 7;260(5109):816–819. doi: 10.1126/science.8484122. [DOI] [PubMed] [Google Scholar]
  134. Thomas D. C., Roberts J. D., Kunkel T. A. Heteroduplex repair in extracts of human HeLa cells. J Biol Chem. 1991 Feb 25;266(6):3744–3751. [PubMed] [Google Scholar]
  135. Tiraby J. G., Fox M. S. Marker discrimination in transformation and mutation of pneumococcus. Proc Natl Acad Sci U S A. 1973 Dec;70(12):3541–3545. doi: 10.1073/pnas.70.12.3541. [DOI] [PMC free article] [PubMed] [Google Scholar]
  136. Tishkoff D. X., Boerger A. L., Bertrand P., Filosi N., Gaida G. M., Kane M. F., Kolodner R. D. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7487–7492. doi: 10.1073/pnas.94.14.7487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  137. Umar A., Boyer J. C., Kunkel T. A. DNA loop repair by human cell extracts. Science. 1994 Nov 4;266(5186):814–816. doi: 10.1126/science.7973637. [DOI] [PubMed] [Google Scholar]
  138. Umar A., Buermeyer A. B., Simon J. A., Thomas D. C., Clark A. B., Liskay R. M., Kunkel T. A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 1996 Oct 4;87(1):65–73. doi: 10.1016/s0092-8674(00)81323-9. [DOI] [PubMed] [Google Scholar]
  139. WITKIN E. M., SICURELLA N. A. PURE CLONES OF LACTOSE-NEGATIVE MUTANTS OBTAINED IN ESCHERICHIA COLI AFTER TREATMENT WITH 5-BROMOURACIL. J Mol Biol. 1964 Apr;8:610–613. doi: 10.1016/s0022-2836(64)80017-6. [DOI] [PubMed] [Google Scholar]
  140. Wagner R., Jr, Meselson M. Repair tracts in mismatched DNA heteroduplexes. Proc Natl Acad Sci U S A. 1976 Nov;73(11):4135–4139. doi: 10.1073/pnas.73.11.4135. [DOI] [PMC free article] [PubMed] [Google Scholar]
  141. Wells J., Held P., Illenye S., Heintz N. H. Protein-DNA interactions at the major and minor promoters of the divergently transcribed dhfr and rep3 genes during the Chinese hamster ovary cell cycle. Mol Cell Biol. 1996 Feb;16(2):634–647. doi: 10.1128/mcb.16.2.634. [DOI] [PMC free article] [PubMed] [Google Scholar]
  142. Welsh K. M., Lu A. L., Clark S., Modrich P. Isolation and characterization of the Escherichia coli mutH gene product. J Biol Chem. 1987 Nov 15;262(32):15624–15629. [PubMed] [Google Scholar]
  143. Werntges H., Steger G., Riesner D., Fritz H. J. Mismatches in DNA double strands: thermodynamic parameters and their correlation to repair efficiencies. Nucleic Acids Res. 1986 May 12;14(9):3773–3790. doi: 10.1093/nar/14.9.3773. [DOI] [PMC free article] [PubMed] [Google Scholar]
  144. Wiebauer K., Jiricny J. In vitro correction of G.T mispairs to G.C pairs in nuclear extracts from human cells. Nature. 1989 May 18;339(6221):234–236. doi: 10.1038/339234a0. [DOI] [PubMed] [Google Scholar]
  145. Wiebauer K., Neddermann P., Hughes M., Jiricny J. The repair of 5-methylcytosine deamination damage. EXS. 1993;64:510–522. doi: 10.1007/978-3-0348-9118-9_23. [DOI] [PubMed] [Google Scholar]
  146. Xiao W., Rathgeber L., Fontanie T., Bawa S. DNA mismatch repair mutants do not increase N-methyl-N'-nitro-N-nitrosoguanidine tolerance in O6-methylguanine DNA methyltransferase-deficient yeast cells. Carcinogenesis. 1995 Aug;16(8):1933–1939. doi: 10.1093/carcin/16.8.1933. [DOI] [PubMed] [Google Scholar]
  147. Yamada M., O'Regan E., Brown R., Karran P. Selective recognition of a cisplatin-DNA adduct by human mismatch repair proteins. Nucleic Acids Res. 1997 Feb 1;25(3):491–496. doi: 10.1093/nar/25.3.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  148. Yeh Y. C., Chang D. Y., Masin J., Lu A. L. Two nicking enzyme systems specific for mismatch-containing DNA in nuclear extracts from human cells. J Biol Chem. 1991 Apr 5;266(10):6480–6484. [PubMed] [Google Scholar]
  149. Zamble D. B., Lippard S. J. Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem Sci. 1995 Oct;20(10):435–439. doi: 10.1016/s0968-0004(00)89095-7. [DOI] [PubMed] [Google Scholar]
  150. Zamble D. B., Mu D., Reardon J. T., Sancar A., Lippard S. J. Repair of cisplatin--DNA adducts by the mammalian excision nuclease. Biochemistry. 1996 Aug 6;35(31):10004–10013. doi: 10.1021/bi960453+. [DOI] [PubMed] [Google Scholar]

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