Journal of Genetics

, Volume 75, Issue 2, pp 181–192 | Cite as

Mismatch repair genes of eukaryotes

  • R. Geeta Vani
  • M. R. S. Rao
Review Article

Abstract

Mismatches that arise during replication or genetic recombination or owing to damage to DNA by chemical agents are recognized by mismatch repair systems. The pathway has been characterized in detail inEscherichia coll. Several homologues of the genes encoding the proteins of this pathway have been identified in the yeastSaccharomyces cerevisiae and in human cells. Mutations in the human geneshMSH2, hMLH1, hPMS1 andhPMS2 have been linked to hereditary nonpolyposis colon cancer (HNPCC) and to some sporadic tumours. Mismatch repair also plays an antirecombinogenic role and is implicated in speciation.

Keywords

Mismatch repair eukaryotes cancer 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Aaltonen A. L., Peltomaki P., Leach R. S., Sistonen P., Pylkkanen L., Mecklin J. P., Jarvinen H., Powell S M., Jen J., Hamilton S. R.et al. 1993 Clues to the pathogenesis of familial colorectal cancer.Science 260: 812–816PubMedCrossRefGoogle Scholar
  2. Baker M. S., Bronner E. C., Zhang L., Plug W. A., Robatzek M., Warren G., Elliott A. E., Yu J., Ashley T., Arnheim N., Flavell A. R. and Liskay M. R. 1995 Male mice defective in the DNA mismatch repair genePMS2 exhibit abnormal chromosome synapsis in meiosis.Cell 82: 309–319PubMedCrossRefGoogle Scholar
  3. Bishop D. K., Williamson M. S., Fogel S. and Kolodner R. D. 1987 The role of heteroduplex correction in gene conversion inSaccharomyces cerevisiae.Nature 328: 362–364PubMedCrossRefGoogle Scholar
  4. Bronner C. E., Baker S. M., Morrison P. T., Warren G., Smith L. G., Lescoe M. K., Kane M., Earabino G., Lipford X., Lindblom A.et al. 1994 Mutation in the DNA mismatch repair gene homologuehMLHl is associated with hereditary nonpolyposis colon cancer.Nature 368: 258–261PubMedCrossRefGoogle Scholar
  5. Cheng K. C. and Loeb L. A. 1993 Genomic instability and tumor progression: mechanistic considerations.Adv. Cancer Res. 60: 121–156PubMedCrossRefGoogle Scholar
  6. Claverys J. P. and Lacks S. A. 1986 Heteroduplex deoxyribonucleic acid base mismatch repair in bacteria.Microbiol. Rev. 50: 133–165PubMedGoogle Scholar
  7. De Wind Niels, Dekker M., Berns A., Radman M. and Riele H. 1995 Inactivation of the mouseMSH2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination and predisposition to cancer.Cell 82: 321–330CrossRefGoogle Scholar
  8. Drummond T. J., Minli G., Longley J. M. and Modrich P. 1995 Isolation of a hMSH2-pl 60 heterodimer that restores DNA mismatch repair to tumor cells.Science 268: 1909–1912PubMedCrossRefGoogle Scholar
  9. Fishel R., Lescoe M. K., Rao M. R. S., Copeland M., Jenkins N., Garber J., Kan N. and Kolodner R. D. 1993 The human mutator gene homologMSH2 and its association with hereditary nonpolyposis colon cancer.Cell 75: 1027–1038PubMedCrossRefGoogle Scholar
  10. Fishel R., Ewel A. and Lescoe M. K. 1994a Purified human MSH2 protein binds to DNA containing mismatched nucleotides.Cancer Res. 54: 5539PubMedGoogle Scholar
  11. Fishel R., Ewel A., Lee S., Lescoe K. M. and Griffin J. 1994b Binding of mismatched microsatellite DNA sequences by the human MSH2 protein.Science 266: 1403–1405PubMedCrossRefGoogle Scholar
  12. Freidberg E. C. 1985DNA repair (New York: W. H. Freeman)Google Scholar
  13. Freidberg E. C., Walker G. C. and Siede W. 1995DNA repair and mutagenesis (Washington, DC: ASM Press) pp. 396–399Google Scholar
  14. Fuji H. and Shimada T. 1989 Isolation and characterization of cDNA clones from the divergently transcribed gene in the region upstream from the human dihydrofolate reductase gene.J. Biol. Chem. 264: 10057–10064Google Scholar
  15. Geeta Vani R. and Rao M. R. S. 1996 Cloning of the cDNA encoding rat homologue of the mismatch repair geneMSH2 and its expression during spermatogenesis. (in press)Google Scholar
  16. Glebov O. K., McKenzie K. E., White C. A. and Sukumar S. 1994 Frequent p53 gene mutations and novel alleles in familial breast cancer.Cancer Res. 54: 3703–3709PubMedGoogle Scholar
  17. Han H. J., Yanagisawa A., Kato Y., Park J. G. and Nakamura Y. 1993 Genetic instability in pancreatic cancer and poorly differentiated type of gastric cancer.Cancer Res. 53: 5087–5089PubMedGoogle Scholar
  18. Hare D., Shapiro L. and Patel D. X. 1986 Wobble dG-dT pairing in right handed DNA: Solution conformation of d(C-G-T-G-A-A-T-T-C-G-C-G) deduced from distance geometry analysis of NOESY spectra.Biochemistry 25: 7445–7456PubMedCrossRefGoogle Scholar
  19. Hennecke F. H., Kolmar K., Brundl K. and Fritz H. J. 1991 Thevsr gene product ofE. coli K-12 is a strand and sequence-specific DNA mismatch endonuclease.Nature 353: 776–778PubMedCrossRefGoogle Scholar
  20. Hollingsworth M. N., Ponte L. and Halsey C. 1995 MSH5, a novel MutS homolog, facilitates meiotic reciprocal recombination between homologs inSaccharomyces cerevisiae but not mismatch repair.Genes Dev. 9: 1728–1739PubMedCrossRefGoogle Scholar
  21. Holmes J. J., Clark S. and Modrich P. 1990 Strand-specific mismatch correction in nuclear extracts of human andDrosophila melanogaster cell lines.Proc. Natl. Acad. Sci. USA 87: 5837–5841PubMedCrossRefGoogle Scholar
  22. Jeyaprakash A., Welch J. W. and Fogel S. 1994 Mutagenesis of yeast MW 104-1B strain has identified the uncharacterizedPMS6 DNA mismatch repair gene locus and additional alleles of existingPMS1, PMS2 andMSH2 genes.Mutat. Res. 325: 21–29PubMedCrossRefGoogle Scholar
  23. Jones M., Wagner R. and Radman M. 1987 Mismatch repair and recombination inE. coli.Cell 50: 621–626PubMedCrossRefGoogle Scholar
  24. Kolodner R. D. 1995 Mismatch repair: Mechanisms and relationship to cancer susceptibility.Trends Biochem. Sci. 20: 397–401PubMedCrossRefGoogle Scholar
  25. Kolodner R. D., Hall N. R., Lipford J., Kane M. F., Rao M. R. S., Morrison P., Wirth L., Finan P. J., Burn J., Chapman P.et al. 1994 Structure of the humanMSH2 locus and analysis of two Muir-Torre kindreds formsh2 mutations.Genomics 24: 516–526PubMedCrossRefGoogle Scholar
  26. Kolodner R. D., Hall N. R., Lipford J., Kane M. F., Morrison P., Finan P. J., Burn J., Chapman P., Earabino C., Merchant E.et al. 1995 Structure of the humanMLH1 locus and analysis of a large HNPCC kindred forMLH1 mutations.Cancer Res. 55: 242–248PubMedGoogle Scholar
  27. Kramer W., Kramer B., Williamson M. S. and Fogel S. 1989 Cloning and nucleotide sequence of DNA mismatch repair genePMS1 fromSaccharomyces cerevisiae: homology of PMS1 to procaryotic MutL and HexB.J. Bacteriol. 171: 5339–5346PubMedGoogle Scholar
  28. Lahue R. S., Au K. G. and Modrich P. 1989 DNA mismatch correction in a defined system.Science 245: 160–164PubMedCrossRefGoogle Scholar
  29. Leach F. S., Nicolaides N., C., Papadopoulos N., Liu B., Jen J., Parsons R., Peltomaki P., Sistonen P., Aaltonen L. A., Nystrom-Lahti M.et al. 1993 Mutations of a mutS homolog in hereditary nonpolyposis colorectal cancer.Cell 75: 1215–1225PubMedCrossRefGoogle Scholar
  30. Li G. and Modrich P. 1995 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: 1950–1954PubMedCrossRefGoogle Scholar
  31. Lindblom A., Tannergard P., Werelies B. and Nordenskjold M. 1993 Genetic mapping of a second locus predisposing to hereditary nonpolyposis colon cancer.Nat. Genet. 5: 279–282PubMedCrossRefGoogle Scholar
  32. Linton J. P., Yen J. Y. J., Selby E., Chen Z., Chinsky J. M., Liu K., Kellens R. E. and Crouse G. F. 1989 Dual bidirectional promoters at the mouseDHFR locus: cloning and characterization of two mRNA classes of the divergently transcribedRep-1 gene.Mol. Cell. Biol. 9: 3058–3072PubMedGoogle Scholar
  33. Liu B., Parsons R. E., Hamilton S. R., Petersen G. M., Lynch H. T., Watson P., Markowitz S., Wilson J. K., Green J., Chapelle A.et al. 1994hMSH2 mutations in hereditary nonpolyposis colorectal cancer kindreds.Cancer Res. 54: 4590–4594PubMedGoogle Scholar
  34. Liu B., Nicolaides N. C., Markowitz S., Willson J. K. V., Parsons R. E., Jen J., Papadopoulos N., Peltomaki P., Chapelle A., Hamilton S. R., Kinzler K. W. and Vogelstein B. 1995 Mismatch repair gene defects in sporadic colorectal cancers with microsatellite instability.Nat. Genet. 9: 48–55PubMedCrossRefGoogle Scholar
  35. Loeb L. A. and Kunkel T. A. 1982 Fidelity of DNA synthesis.Annu. Rev. Biochem. 51: 429–457PubMedCrossRefGoogle Scholar
  36. Markowitz S., Wang J., Myreoff L., Parsons R., Sun L., Lutterbaugh J.et al. 1995 Inactivation of the type II TGF-β receptor in colon cancer cells with microsatellite instability.Science 268: 1336–1338PubMedCrossRefGoogle Scholar
  37. Matic I., Rayssiguier C. and Radman M. 1995 Interspecies gene exchange in bacteria: The role of SOS and mismatch repair systems in evolution of species.Cell 80: 507–515PubMedCrossRefGoogle Scholar
  38. Merlo A., Mabry M., Gabrielson E., Vollmer R., Baylin S. B. and Sidransky D. 1994 Frequent microsatellite instability in primary small cell lung cancer.Cancer Res. 54: 2098–2101PubMedGoogle Scholar
  39. Michaels M. L., Tchou J., Grollman A. P. and Miller J. H. 1992 A repair system for 8-oxo-7,8-dihyd-rodeoxyguanine.Biochemistry 31: 10964–10968PubMedCrossRefGoogle Scholar
  40. Modrich P. 1991 Mechanisms and biological effects of mismatch repair.Annu. Rev. Genet. 25: 229–253PubMedCrossRefGoogle Scholar
  41. Nai-Wen Chi and Kolodner R. D. 1994 Purification and characterization of MSH1, a yeast mitochondrial protein that binds to DNA mismatches.J. Biol. Chem. 269: 29984–29992Google Scholar
  42. New L., Liu K. and Crouse F. G. 1993 The yeast geneMSH3 defines a new class of eukaryoticmutS homologues.Mol. Gen. Genet. 239: 97–108PubMedGoogle Scholar
  43. 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.et al. 1994 Mutations of twoPMS homologues in hereditary nonpolyposis colon cancer.Nature 371: 75–80PubMedCrossRefGoogle Scholar
  44. Palombo F., Gallinari P., Laccarino I., Leltieri T., Hughes M., D’Arrigo A., Truong O., Hsuan J. J. and Jiricny J. 1995 GTBP, a 160 kilodalton protein essential for mismatch-binding activity in human cells.Science 268: 1912–1914PubMedCrossRefGoogle Scholar
  45. Papadopoulos N., Nicolaides N. C., Wei Y.-F., Ruben S. M., Carter K. C., Rosen C. A., Haseltine W. A., Fleischman R. D., Fraser C. M., Adams M. D.et al. 1994 Mutation of amutL homolog in hereditary colon cancer.Science 263: 1625–1629PubMedCrossRefGoogle Scholar
  46. Papadopoulos N., Nicolaides N. C., Liu B., Parsons R., Lengauer C., Palombo F., D’Arrigo A., Markowitz S., Wilson J. K. V., Kinzler K. W.et al. 1995 Mutations of GTBP in genetically unstable cells.Science 268: 1915–1917PubMedCrossRefGoogle Scholar
  47. Parsons R., Li G. M., Longley J. M., Fang W., Papadopoulos N., Jen J., Chapelle A., Kinzler N. K., Vogelstein B. and Modrich P. 1993 Hypermutability and mismatch repair deficiency in RER+ tumor cells.Cell 75: 1227–1236PubMedCrossRefGoogle Scholar
  48. Patel D. J., Kozlowski S. A., Ikuta S. and Itakurat 1984 Dynamics of DNA duplexes containing G-T, G-A, A-C and T-C pairs: hydrogen exchange at and adjacent to mismatch sites.Fed. Proc. 43: 2663–2670PubMedGoogle Scholar
  49. Peltomaki P., Aaltonen A. L., Sistonen P., Pylkkanen L., Mecklin P. J., Jarvinen H., Green S. J., Jass R. J., Weber C. J., Leach F. S., Petersen M. G., Hamilton R. S., Chapelle A. and Vogelstein B. 1993 Genetic mapping of a locus predisposing to human colorectal cancer.Science 260: 810–812PubMedCrossRefGoogle Scholar
  50. Prudhomme M., Mejean V., Martin B. and Claverys J. P. 1991 Mismatch repair genes ofStreptococcus pneumoniae: HexA confers a mutator phenotype inEscherichia coli by negative complementation.J. Bacteriol. 173: 7196–7203PubMedGoogle Scholar
  51. Radman M. and Wagner R. 1993 Mismatch recognition in chromosomal interactions and speciation.Chromosoma 102: 369–373PubMedCrossRefGoogle Scholar
  52. Rayssiguier C., Thaler D. S. and Radman M. 1989 The barrier to recombination betweenEscherichia coli andSalmonella typhimurium is disrupted in mismatch repair mutants.Nature 342: 396–401PubMedCrossRefGoogle Scholar
  53. Reenan R. A. G. and Kolodner R. D. 1992a Isolation and characterization of twoSaccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins.Genetics 132: 963–973PubMedGoogle Scholar
  54. Reenan R. A. G. and Kolodner R. D. 1992b Characterization of insertion mutations in theSaccharomyces cerevisiae MSH1 andMSH2 genes: evidence for separate mitochondrial and nuclear functions.Genetics 132: 975–985PubMedGoogle Scholar
  55. Reitmar A. H., Schmits R., Ewel A., Bapat B., Redston M., Mitri A., Waterhouse P., Mittrucker H. W., Wakeham A., Liu B., Thomason A., Griesser H., Gallinger S., Balljausen W. G., Fishel R. and Mak T. W. 1995 MSH2 deficient mice are viable and susceptible to lymphoid tumours.Nat. Genet. 11: 64–70CrossRefGoogle Scholar
  56. Ross-Macdonald P. and Roeder G. S. 1994 Mutation of a meiosis specific MutS homolog decreases crossing over but not mismatch correction.Cell 79: 1069–1080PubMedCrossRefGoogle Scholar
  57. Selva E. M., New L. and Lahue R. S. 1995 Mismatch correction acts as a barrier to homeologous recombination inSaccharomyces cerevisiae.Genetics 139: 1175–1181PubMedGoogle Scholar
  58. Strand M., Prolla T. A., Liskay R. M. and Peter T. D. 1993 Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair.Nature 365: 274–276PubMedCrossRefGoogle Scholar
  59. Thibodeau S. N., Bren G., Schaid 1993 Microsatellite instability in cancer of the proximal colon.Science 260: 816–819PubMedCrossRefGoogle Scholar
  60. Thomas D. C., Roberts J. D. and Kunkel T. A. 1991 Heteroduplex repair in extracts of human HeLa cells.J. Biol. Chem. 266: 3744–3751PubMedGoogle Scholar
  61. Tsai-Wu J. J., Liu H. L. and Lu A. L. 1992E. coli MutY protein has both N-glycosylase and apurinic-apyrimidinic endonuclease activities on A.C and A.G mispairs.Proc. Natl. Acad. Sci. USA 89: 8779–8783PubMedCrossRefGoogle Scholar
  62. Varlet J., Radman M. and Brooks P. 1990 DNA mismatch repair inXenopus egg extracts: Repair efficiency and DNA repair and synthesis for single base-pair mismatches.Proc. Natl. Acad. Sci. USA 87: 7883–7887PubMedCrossRefGoogle Scholar
  63. Varlet J., Pallard C., Radman M., Moreau J. and Niels de Wind 1994 Cloning and expression ofXenopus and mouse MSH2 DNA mismatch repair genes.Nucl. Acids Res. 22: 5723–5728PubMedCrossRefGoogle Scholar
  64. Vogelstein B. and Kinzler K. W. 1994 Colorectal cancer and the intersection between basic and clinical research.Cold Spring Harbor Symp. Quant. Biol. 59: 517–521PubMedGoogle Scholar
  65. Willamson M. S., Game J. C. and Fogel S. 1985 Meiotic gene conversion mutants inSaccharomyces cerevisiae: isolation and characterization of pmsl-1 and pmsl-2.Genetics 110: 609–646Google Scholar
  66. Worth L., Clark S., Radman M. and Modrich P. 1994 Mismatch repair proteins MutS and MutL inhibit RecA catalyzed strand transfer between diverged DNAs.Proc. Natl. Acad. Sci. USA 91: 3238–3241PubMedCrossRefGoogle Scholar

Copyright information

© Indian Academy of Sciences 1996

Authors and Affiliations

  • R. Geeta Vani
    • 1
  • M. R. S. Rao
    • 1
  1. 1.Department of BiochemistryIndian Institute of ScienceBangaloreIndia

Personalised recommendations