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Annual Review of Genetics

Volume 49, 2015

Eukaryotic Mismatch Repair in Relation to DNA Replication

Abstract

Three processes act in series to accurately replicate the eukaryotic nuclear genome. The major replicative DNA polymerases strongly prevent mismatch formation, occasional mismatches that do form are proofread during replication, and rare mismatches that escape proofreading are corrected by mismatch repair (MMR). This review focuses on MMR in light of increasing knowledge about nuclear DNA replication enzymology and the rate and specificity with which mismatches are generated during leading- and lagging-strand replication. We consider differences in MMR efficiency in relation to mismatch recognition, signaling to direct MMR to the nascent strand, mismatch removal, and the timing of MMR. These studies are refining our understanding of relationships between generating and repairing replication errors to achieve accurate replication of both DNA strands of the nuclear genome.

Keyword(s): DNA mismatch repair, genome instability, mutation rate, mutator, replication fidelity
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2015-11-23
2024-04-25
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Literature Cited

  1. Amin NS, Nguyen MN, Oh S, Kolodner RD. 1.  2001. exo1-Dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol. Cell. Biol. 21:5142–55 [Google Scholar]
  2. Antony E, Khubchandani S, Chen S, Hingorani MM. 2.  2006. Contribution of Msh2 and Msh6 subunits to the asymmetric ATPase and DNA mismatch binding activities of Saccharomyces cerevisiae Msh2-Msh6 mismatch repair protein. DNA Repair 5:153–62 [Google Scholar]
  3. Balakrishnan L, Bambara RA. 3.  2013. Okazaki fragment metabolism. Cold Spring Harb. Perspect. Biol. 5:pii:a010173 [Google Scholar]
  4. Begum R, Martin S. 4.  2015. Targeting mismatch repair defects: a novel strategy for personalized cancer treatment. DNA Repair. In press
  5. Blackwell LJ, Martik D, Bjornson KP, Bjornson ES, Modrich P. 5.  1998. Nucleotide-promoted release of hMutSα from heteroduplex DNA is consistent with an ATP-dependent translocation mechanism. J. Biol. Chem. 273:32055–62 [Google Scholar]
  6. Buckland RJ, Watt DL, Chittoor B, Nilsson AK, Kunkel TA, Chabes A. 6.  2014. Increased and imbalanced dNTP pools symmetrically promote both leading and lagging strand replication infidelity. PLOS Genet. 10:e1004846 [Google Scholar]
  7. Campbell CS, Hombauer H, Srivatsan A, Bowen N, Gries K. 7.  et al. 2014. Mlh2 is an accessory factor for DNA mismatch repair in Saccharomyces cerevisiae. PLOS Genet. 10:e1004327 [Google Scholar]
  8. 8. Cancer Genome Atlas Netw 2012. Comprehensive molecular characterization of human colon and rectal cancer. Nature 487:330–37 [Google Scholar]
  9. Cerritelli SM, Crouch RJ. 9.  2009. Ribonuclease H: the enzymes in eukaryotes. FEBS J. 276:1494–505 [Google Scholar]
  10. Church DN, Briggs SE, Palles C, Domingo E, Kearsey SJ. 10.  et al. 2013. DNA polymerase ε and δ exonuclease domain mutations in endometrial cancer. Hum. Mol. Genet. 22:2820–28 [Google Scholar]
  11. Clausen AR, Lujan SA, Burkholder AB, Orebaugh CD, Williams JS. 11.  et al. 2015. Tracking replication enzymology in vivo by genome-wide mapping of ribonucleotide incorporation. Nat. Struct. Mol. Biol. 22:185–91 [Google Scholar]
  12. Crouse G. 12.  2016. Non-canonical actions of mismatch repair. DNA Repair. In press
  13. Daigaku Y, Keszthelyi A, Müller C, Miyabe I, Brookls T. 13.  et al. 2015. A global profile of replicative polymerase usage. Nat. Struct. Mol. Biol. 22:192–98 [Google Scholar]
  14. DeRocco V, Anderson T, Piehler J, Erie DA, Weninger K. 14.  2010. Four-color single-molecule fluorescence with noncovalent dye labeling to monitor dynamic multimolecular complexes. BioTechniques 49:807–16 [Google Scholar]
  15. Deschenes SM, Tomer G, Nguyen M, Erdeniz N, Juba NC. 15.  et al. 2007. The E705K mutation in hPMS2 exerts recessive, not dominant, effects on mismatch repair. Cancer Lett. 249:148–56 [Google Scholar]
  16. Dowen JM, Putnam CD, Kolodner RD. 16.  2010. Functional studies and homology modeling of Msh2-Msh3 predict that mispair recognition involves DNA bending and strand separation. Mol. Cell. Biol. 30:3321–28 [Google Scholar]
  17. Drake JW. 17.  1999. The distribution of rates of spontaneous mutation over viruses, prokaryotes, and eukaryotes. Ann. N. Y. Acad. Sci. 870:100–7 [Google Scholar]
  18. Earley MC, Crouse GF. 18.  1998. The role of mismatch repair in the prevention of base pair mutations in Saccharomyces cerevisiae. PNAS 95:15487–91 [Google Scholar]
  19. Edelbrock MA, Kaliyaperumal S, Williams KJ. 19.  2013. Structural, molecular and cellular functions of MSH2 and MSH6 during DNA mismatch repair, damage signaling and other noncanonical activities. Mutat. Res. 743–44:53–66 [Google Scholar]
  20. Lee K, Tosti E, Edelmann W. 20.  2016. Mouse models of DNA mismatch repair in cancer research.. DNA Repair. In press
  21. Elez M, Radman M, Matic I. 21.  2012. Stoichiometry of MutS and MutL at unrepaired mismatches in vivo suggests a mechanism of repair. Nucleic Acids Res. 40:3929–38 [Google Scholar]
  22. Elsayed FA, Kets CM, Ruano D, van den Akker B, Mensenkamp AR. 22.  et al. 2015. Germline variants in POLE are associated with early onset mismatch repair deficient colorectal cancer. Eur. J. Hum. Genet. 23:1080–84 [Google Scholar]
  23. Erdeniz N, Nguyen M, Deschenes SM, Liskay RM. 23.  2007. Mutations affecting a putative MutLα endonuclease motif impact multiple mismatch repair functions. DNA Repair 6:1463–70 [Google Scholar]
  24. Erie DA, Weninger KR. 24.  2014. Single molecule studies of DNA mismatch repair. DNA Repair 20:71–81 [Google Scholar]
  25. Fortune JM, Pavlov YI, Welch CM, Johansson E, Burgers PM, Kunkel TA. 25.  2005. Saccharomyces cerevisiae DNA polymerase delta: high fidelity for base substitutions but lower fidelity for single- and multi-base deletions. J. Biol. Chem. 280:29980–87 [Google Scholar]
  26. Gad H, Koolmeister T, Jemth AS, Eshtad S, Jacques SA. 26.  et al. 2014. MTH1 inhibition eradicates cancer by preventing sanitation of the dNTP pool. Nature 508:215–21 [Google Scholar]
  27. Georgescu RE, Langston L, Yao NY, Yurieva O, Zhang D. 27.  et al. 2014. Mechanism of asymmetric polymerase assembly at the eukaryotic replication fork. Nat. Struct. Mol. Biol. 21:664–70 [Google Scholar]
  28. Ghaemmaghami S, Huh W-K, Bower K, Howson RW, Belle A. 28.  et al. 2003. Global analysis of protein expression in yeast. Nature 425:737–41 [Google Scholar]
  29. Ghodgaonkar MM, Lazzaro F, Olivera-Pimentel M, Artola-Boran M, Cejka P. 29.  et al. 2013. Ribonucleotides misincorporated into DNA act as strand-discrimination signals in eukaryotic mismatch repair. Mol. Cell 50:323–32 [Google Scholar]
  30. Glaab WE, Risinger JI, Umar A, Kunkel TA, Barrett JC, Tindall KR. 30.  1998. Characterization of distinct human endometrial carcinoma cell lines deficient in mismatch repair that originated from a single tumor. J. Biol. Chem. 273:26662–69 [Google Scholar]
  31. Goellner EM, Smith CE, Campbell CS, Hombauer H, Desai A. 31.  et al. 2014. PCNA and Msh2-Msh6 activate an Mlh1-Pms1 endonuclease pathway required for Exo1-independent mismatch repair. Mol. Cell 55:291–304 [Google Scholar]
  32. Groothuizen FS, Fish A, Petoukhov MV, Reumer A, Manelyte L. 32.  et al. 2013. Using stable MutS dimers and tetramers to quantitatively analyze DNA mismatch recognition and sliding clamp formation. Nucleic Acids Res. 41:8166–81 [Google Scholar]
  33. Groothuizen F, Sixma T. 33.  2015. The conserved molecular machinery in DNA mismatch repair structures. DNA Repair. In press
  34. Gupta S, Gellert M, Yang W. 34.  2012. Mechanism of mismatch recognition revealed by human MutSβ bound to unpaired DNA loops. Nat. Struct. Mol. Biol. 19:72–78 [Google Scholar]
  35. Hall MC, Shcherbakova PV, Fortune JM, Borchers CH, Dial JM. 35.  et al. 2003. DNA binding by yeast Mlh1 and Pms1: implications for DNA mismatch repair. Nucleic Acids Res. 31:2025–34 [Google Scholar]
  36. Haracska L, Yu SL, Johnson RE, Prakash L, Prakash S. 36.  2000. Efficient and accurate replication in the presence of 7,8-dihydro-8-oxoguanine by DNA polymerase η. Nat. Genet. 25:458–61 [Google Scholar]
  37. Harfe BD, Jinks-Robertson S. 37.  2000. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34:359–99 [Google Scholar]
  38. Harfe BD, Jinks-Robertson S. 38.  2000. Sequence composition and context effects on the generation and repair of frameshift intermediates in mononucleotide runs in Saccharomyces cerevisiae. Genetics 156:571–78 [Google Scholar]
  39. Harrington JM, Kolodner RD. 39.  2007. Saccharomyces cerevisiae Msh2-Msh3 acts in repair of base-base mispairs. Mol. Cell. Biol. 27:6546–54 [Google Scholar]
  40. Hawk JD, Stefanovic L, Boyer JC, Petes TD, Farber RA. 40.  2005. Variation in efficiency of DNA mismatch repair at different sites in the yeast genome. PNAS 102:8639–43 [Google Scholar]
  41. Heinen CD. 41.  2015. Mismatch repair defects and Lynch Syndrome: the role of the basic scientist in the battle against cancer. DNA Repair. In press
  42. Hess MT, Gupta RD, Kolodner RD. 42.  2002. Dominant Saccharomyces cerevisiae msh6 mutations cause increased mispair binding and decreased dissociation from mispairs by Msh2-Msh6 in the presence of ATP. J. Biol. Chem. 277:25545–53 [Google Scholar]
  43. Hingorani MM. 43.  2016. Mismatch binding, ADP-ATP exchange and intramolecular signalling during mismatch repair. DNA Repair. In press
  44. Schmidt TT, Hombauer H. 44.  2016. Visualization of mismatch repair complexes using fluorescence microscopy. DNA Repair. In press
  45. Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD. 45.  2011. Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147:1040–53 [Google Scholar]
  46. Hombauer H, Srivatsan A, Putnam CD, Kolodner RD. 46.  2011. Mismatch repair, but not heteroduplex rejection, is temporally coupled to DNA replication. Science 334:1713–16 [Google Scholar]
  47. Hsieh P, Yamane K. 47.  2008. DNA mismatch repair: molecular mechanism, cancer, and ageing. Mech. Ageing Dev. 129:391–407 [Google Scholar]
  48. Iyer RR, Pluciennik A, Burdett V, Modrich PL. 48.  2006. DNA mismatch repair: functions and mechanisms. Chem. Rev. 106:302–23 [Google Scholar]
  49. Iyer RR, Pluciennik A, Genschel J, Tsai MS, Beese LS, Modrich P. 49.  2010. MutLα and proliferating cell nuclear antigen share binding sites on MutSβ. J. Biol. Chem. 285:11730–39 [Google Scholar]
  50. Jiricny J. 50.  2013. Postreplicative mismatch repair. Cold Spring Harb. Perspect. Biol. 5:a012633 [Google Scholar]
  51. Johansson E, Dixon N. 51.  2013. Replicative DNA polymerases. Cold Spring Harb. Perspect. Biol. doi: 10.1101/cshperspect.a012799
  52. Johnson RE, Kovvali GK, Prakash L, Prakash S. 52.  1995. Requirement of the yeast RTH1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science 269:238–40 [Google Scholar]
  53. Kadyrova LY, Kadyrov FA. 53.  2015. Endonuclease activities of MutLα and its homologs in mismatch repair. DNA Repair. In press
  54. Kadyrov FA, Dzantiev L, Constantin N, Modrich P. 54.  2006. Endonucleolytic function of MutLα in human mismatch repair. Cell 126:297–308 [Google Scholar]
  55. Kadyrov FA, Genschel J, Fang Y, Penland E, Edelmann W, Modrich P. 55.  2009. A possible mechanism for exonuclease 1–independent eukaryotic mismatch repair. PNAS 106:8495–500 [Google Scholar]
  56. Kadyrov FA, Holmes SF, Arana ME, Lukianova OA, O'Donnell M. 56.  et al. 2007. Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease. J. Biol. Chem. 282:37181–90 [Google Scholar]
  57. Kim TM, Laird PW, Park PJ. 57.  2013. The landscape of microsatellite instability in colorectal and endometrial cancer genomes. Cell 155:858–68 [Google Scholar]
  58. Koh KD, Balachander S, Hesselberth JR, Storici F. 58.  2015. Ribose-seq: global mapping of ribonucleotides embedded in genomic DNA. Nat. Methods 12:251–57 [Google Scholar]
  59. Kolodner RD. 59.  2016. A personal historical view of DNA mismatch repair with an emphasis on eukaryotic DNA mismatch repair. DNA Repair. In press
  60. Kolodner RD, Marsischky GT. 60.  1999. Eukaryotic DNA mismatch repair. Curr. Opin. Genet. Dev. 9:89–96 [Google Scholar]
  61. Kow YW, Bao G, Reeves JW, Jinks-Robertson S, Crouse GF. 61.  2007. Oligonucleotide transformation of yeast reveals mismatch repair complexes to be differentially active on DNA replication strands. PNAS 104:11352–57 [Google Scholar]
  62. Kroutil LC, Register K, Bebenek K, Kunkel TA. 62.  1996. Exonucleolytic proofreading during replication of repetitive DNA. Biochemistry 35:1046–53 [Google Scholar]
  63. Kumar C, Piacente SC, Sibert J, Bukata AR, O'Connor J. 63.  et al. 2011. Multiple factors insulate Msh2–Msh6 mismatch repair activity from defects in Msh2 domain I. J. Mol. Biol. 411:765–80 [Google Scholar]
  64. Kumar D, Abdulovic AL, Viberg J, Nilsson AK, Kunkel TA, Chabes A. 64.  2011. Mechanisms of mutagenesis in vivo due to imbalanced dNTP pools. Nucleic Acids Res. 39:1360–71 [Google Scholar]
  65. Kunkel TA. 65.  1993. Nucleotide repeats. Slippery DNA and diseases. Nature 365:207–8 [Google Scholar]
  66. Kunkel TA. 66.  2009. Evolving views of DNA replication (in)fidelity. Cold Spring Harb. Symp. Quant. Biol. 74:91–101 [Google Scholar]
  67. Kunkel TA, Burgers PM. 67.  2008. Dividing the workload at a eukaryotic replication fork. Trends Cell Biol. 18:521–27 [Google Scholar]
  68. Kunkel TA, Burgers PM. 68.  2014. Delivering nonidentical twins. Nat. Struct. Mol. Biol. 21:649–51 [Google Scholar]
  69. Kunkel TA, Erie DA. 69.  2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681–710 [Google Scholar]
  70. Lamers MH, Perrakis A, Enzlin JH, Winterwerp HH, de Wind N, Sixma TK. 70.  2000. The crystal structure of DNA mismatch repair protein MutS binding to a G × T mismatch. Nature 407:711–17 [Google Scholar]
  71. Lang GI, Parsons L, Gammie AE. 71.  2013. Mutation rates, spectra, and genome-wide distribution of spontaneous mutations in mismatch repair deficient yeast. G3 Bethesda 3:1453–65 [Google Scholar]
  72. Tham KC, Kanaar R, Lebbink JHG. 72.  2016. Mismatch repair and homeologous recombination. DNA Repair In press
  73. Lee JB, Cho WK, Park J, Jeon Y, Kim D. 73.  et al. 2014. Single-molecule views of MutS on mismatched DNA. DNA Repair 20:82–93 [Google Scholar]
  74. Lee JB, Fishel R. 74.  2014. Single molecule views of MutS on mismatched DNA. DNA Repair 20:82–93 [Google Scholar]
  75. Li F, Ortega J, Gu L, Li G-M. 75.  2015. Regulation of mismatch repair by histone code and posttranslational modifications in eukaryotic cells. DNA Repair. In press
  76. Friedhoff P, Li P, Gotthardt J. 76.  2016. Protein-protein interactions in DNA mismatch repair. DNA Repair. In press
  77. Li Z, Pearlman AH, Hsieh P. 77.  2015. DNA mismatch repair and the DNA damage response. DNA Repair. In press
  78. Liberti SE, Larrea AA, Kunkel TA. 78.  2012. Exonuclease 1 preferentially repairs mismatches generated by DNA polymerase α. DNA Repair 12:92–96 [Google Scholar]
  79. Loeb LA. 79.  1991. Mutator phenotype may be required for multistage carcinogenesis. Cancer Res. 51:3075–79 [Google Scholar]
  80. Loeb LA, Kunkel TA. 80.  1982. Fidelity of DNA synthesis. Annu. Rev. Biochem. 51:429–57 [Google Scholar]
  81. Longley MJ, Pierce AJ, Modrich P. 81.  1997. DNA polymerase δ is required for human mismatch repair in vitro. J. Biol. Chem. 272:10917–21 [Google Scholar]
  82. Lujan SA, Clausen AR, Clark AB, MacAlpine HK, MacAlpine DM. 82.  et al. 2014. Heterogeneous polymerase fidelity and mismatch repair bias genome variation and composition. Genome Res. 24:1751–64 [Google Scholar]
  83. Lujan SA, Williams JS, Clausen AR, Clark AB, Kunkel TA. 83.  2013. Ribonucleotides are signals for mismatch repair of leading-strand replication errors. Mol. Cell 50:437–43 [Google Scholar]
  84. Lujan SA, Williams JS, Pursell ZF, Abdulovic-Cui AA, Clark AB. 84.  et al. 2012. Mismatch repair balances leading and lagging strand DNA replication fidelity. PLOS Genet. 8:e1003016 [Google Scholar]
  85. Ma X, Rogacheva MV, Nishant KT, Zanders S, Bustamante CD, Alani E. 85.  2012. Mutation hot spots in yeast caused by long-range clustering of homopolymeric sequences. Cell Rep. 1:36–42 [Google Scholar]
  86. Manhart CM, Alani E. 86.  2015. Roles for mismatch repair family proteins in promoting meiotic crossing over. DNA Repair. In press
  87. Marinus MG. 87.  1976. Adenine methylation of Okazaki fragments in Escherichia coli. J. Bacteriol. 128:853–54 [Google Scholar]
  88. Mazur DJ, Mendillo ML, Kolodner RD. 88.  2006. Inhibition of Msh6 ATPase activity by mispaired DNA induces a Msh2(ATP)-Msh6(ATP) state capable of hydrolysis-independent movement along DNA. Mol. Cell 22:39–49 [Google Scholar]
  89. Mazurek A, Johnson CN, Germann MW, Fishel R. 89.  2009. Sequence context effect for hMSH2-hMSH6 mismatch-dependent activation. PNAS 106:4177–82 [Google Scholar]
  90. McCulloch SD, Kokoska RJ, Chilkova O, Welch CM, Johansson E. 90.  et al. 2004. Enzymatic switching for efficient and accurate translesion DNA replication. Nucleic Acids Res. 32:4665–75 [Google Scholar]
  91. Meister P, Taddei A, Ponti A, Baldacci G, Gasser SM. 91.  2007. Replication foci dynamics: replication patterns are modulated by S-phase checkpoint kinases in fission yeast. EMBO J. 26:1315–26 [Google Scholar]
  92. Mendelman LV, Boosalis MS, Petruska J, Goodman MF. 92.  1989. Nearest neighbor influences on DNA polymerase insertion fidelity. J. Biol. Chem. 264:14415–23 [Google Scholar]
  93. Modrich P. 93.  1987. DNA mismatch correction. Annu. Rev. Biochem. 56:435–66 [Google Scholar]
  94. Modrich P. 94.  1991. Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25:229–53 [Google Scholar]
  95. Natrajan G, Lamers MH, Enzlin JH, Winterwerp HH, Perrakis A, Sixma TK. 95.  2003. Structures of Escherichia coli DNA mismatch repair enzyme MutS in complex with different mismatches: a common recognition mode for diverse substrates. Nucleic Acids Res. 31:4814–21 [Google Scholar]
  96. Ni TT, Marsischky GT, Kolodner RD. 96.  1999. MSH2 and MSH6 are required for removal of adenine misincorporated opposite 8-oxo-guanine in S. cerevisiae. Mol. Cell 4:439–44 [Google Scholar]
  97. Nick McElhinny SA, Kissling GE, Kunkel TA. 97.  2010. Differential correction of lagging-strand replication errors made by DNA polymerases α and δ. PNAS 107:21070–75 [Google Scholar]
  98. Nick McElhinny SA, Kumar D, Clark AB, Watt DL, Watts BE. 98.  et al. 2010. Genome instability due to ribonucleotide incorporation into DNA. Nat. Chem. Biol. 6:774–81 [Google Scholar]
  99. Nick McElhinny SA, Pavlov YI, Kunkel TA. 99.  2006. Evidence for extrinsic exonucleolytic proofreading. Cell Cycle 5:958–62 [Google Scholar]
  100. Nick McElhinny SA, Watts BE, Kumar D, Watt DL, Lundstrom EB. 100.  et al. 2010. Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. PNAS 107:4949–54 [Google Scholar]
  101. O'Donnell M, Langston L, Stillman B. 101.  2013. Principles and concepts of DNA replication in bacteria, archaea, and eukarya. Cold Spring Harb. Perspect. Biol. 5:pii: a010108 [Google Scholar]
  102. Obmolova G, Ban C, Hsieh P, Yang W. 102.  2000. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407:703–10 [Google Scholar]
  103. Owen BAL H, Lang W, McMurray CT. 103.  2009. The nucleotide binding dynamics of human MSH2–MSH3 are lesion dependent. Nat. Struct. Mol. Biol. 16:550–57 [Google Scholar]
  104. Palles C, Cazier JB, Howarth KM, Domingo E, Jones AM. 104.  et al. 2013. Germline mutations affecting the proofreading domains of POLE and POLD1 predispose to colorectal adenomas and carcinomas. Nat. Genet. 45:136–44 [Google Scholar]
  105. Pavlov YI, Frahm C, Nick McElhinny SA, Niimi A, Suzuki M, Kunkel TA. 105.  2006. Evidence that errors made by DNA polymerase alpha are corrected by DNA polymerase delta. Curr. Biol. 16:202–7 [Google Scholar]
  106. Pavlov YI, Mian IM, Kunkel TA. 106.  2003. Evidence for preferential mismatch repair of lagging strand DNA replication errors in yeast. Curr. Biol. 13:744–48 [Google Scholar]
  107. Pavlov YI, Shcherbakova PV. 107.  2010. DNA polymerases at the eukaryotic fork: 20 years later. Mutat. Res. 685:45–53 [Google Scholar]
  108. Schmidt MHM, Pearson CE. 108.  2016. Repeat-associated disease and mismatch repair: sometimes, less is more. DNA Repair. In press
  109. Peňa-Diaz J, Rasmussen L. 109.  2015. Approaches to diagnose mismatch repair gene defects in cancer. DNA Repair. In press
  110. Perrino FW, Loeb LA. 110.  1990. Hydrolysis of 3′-terminal mispairs in vitro by the 3′–5′ exonuclease of DNA polymerase δ permits subsequent extension by DNA polymerase α. Biochemistry 29:5226–31 [Google Scholar]
  111. Pluciennik A, Burdett V, Baitinger C, Iyer RR, Shi K, Modrich P. 111.  2013. Extrahelical (CAG)/(CTG) triplet repeat elements support proliferating cell nuclear antigen loading and MutLα endonuclease activation. PNAS 110:12277–82 [Google Scholar]
  112. Pluciennik A, Dzantiev L, Iyer RR, Constantin N, Kadyrov FA, Modrich P. 112.  2010. PCNA function in the activation and strand direction of MutLα endonuclease in mismatch repair. PNAS 107:16066–71 [Google Scholar]
  113. Pukkila PJ, Peterson J, Herman G, Modrich P, Meselson M. 113.  1983. Effects of high levels of DNA adenine methylation on methyl-directed mismatch repair in Escherichia coli. Genetics 104:571–82 [Google Scholar]
  114. Putnam CD. 113a.  2016. Evolution of the methyl directed mismatch repair system in Escherichia coli. DNA Repair. In press
  115. Qiu R, DeRocco VC, Harris C, Sharma A, Hingorani MM. 114.  et al. 2012. Large conformational changes in MutS during DNA scanning, mismatch recognition and repair signalling. EMBO J. 31:2528–40 [Google Scholar]
  116. Reha-Krantz LJ. 115.  2010. DNA polymerase proofreading: multiple roles maintain genome stability. Biochim. Biophys. Acta 1804:1049–63 [Google Scholar]
  117. Reijns MAM, Kemp H, Ding J, Marion de Proce S, Jackson AP, Taylor MS. 116.  2015. Lagging strand replication shapes the mutational landscape of the genome. Nature 518:502–6 [Google Scholar]
  118. Romanova NV, Crouse GF. 117.  2013. Different roles of eukaryotic MutS and MutL complexes in repair of small insertion and deletion loops in yeast. PLOS Genet. 9:e1003920 [Google Scholar]
  119. Russo MT, Blasi MF, Chiera F, Fortini P, Degan P. 118.  et al. 2004. The oxidized deoxynucleoside triphosphate pool is a significant contributor to genetic instability in mismatch repair–deficient cells. Mol. Cell. Biol. 24:465–74 [Google Scholar]
  120. Sabouri N, Viberg J, Goyal DK, Johansson E, Chabes A. 119.  2008. Evidence for lesion bypass by yeast replicative DNA polymerases during DNA damage. Nucleic Acids Res. 36:5660–67 [Google Scholar]
  121. Sacho EJ, Kadyrov FA, Modrich P, Kunkel TA, Erie DA. 120.  2008. Direct visualization of asymmetric adenine-nucleotide-induced conformational changes in MutLα. Mol. Cell 29:112–21 [Google Scholar]
  122. Schaaper RM. 121.  1993. Base selection, proofreading, and mismatch repair during DNA replication in Escherichia coli. J. Biol. Chem. 268:23762–65 [Google Scholar]
  123. Schaaper RM, Radman M. 122.  1989. The extreme mutator effect of Escherichia coli mutD5 results from saturation of mismatch repair by excessive DNA replication errors. EMBO J. 8:3511–16 [Google Scholar]
  124. Serero A, Jubin C, Loeillet S, Legoix-Ne P, Nicolas AG. 123.  2014. Mutational landscape of yeast mutator strains. PNAS 111:1897–902 [Google Scholar]
  125. Shibutani S, Takeshita M, Grollman AP. 124.  1991. Insertion of specific bases during DNA synthesis past the oxidation-damaged base 8-oxodG. Nature 349:431–14 [Google Scholar]
  126. Shinbrot E, Henninger EE, Weinhold N, Covington KR, Goksenin AY. 125.  et al. 2014. Exonuclease mutations in DNA polymerase epsilon reveal replication strand specific mutation patterns and human origins of replication. Genome Res. 24:1740–50 [Google Scholar]
  127. Sia EA, Kokoska RJ, Dominska M, Greenwell P, Petes TD. 126.  1997. Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes. Mol. Cell. Biol. 17:2851–58 [Google Scholar]
  128. Sijmons RH, Hofstra RMW. 127.  2015. Clinical aspects of hereditary DNA mismatch repair gene defects. DNA Repair. In press
  129. Sparks JL, Chon H, Cerritelli SM, Kunkel TA, Johansson E. 128.  et al. 2012. RNase H2-initiated ribonucleotide excision repair. Mol. Cell 47:980–86 [Google Scholar]
  130. Srivatsan A, Bowen N, Kolodner RD. 129.  2014. Mispair-specific recruitment of the Mlh1-Pms1 complex identifies repair substrates of the Saccharomyces cerevisiae Msh2-Msh3 complex. J. Biol. Chem. 289:9352–64 [Google Scholar]
  131. Strand M, Earley MC, Crouse GF, Petes TD. 130.  1995. Mutations in the MSH3 gene preferentially lead to deletions within tracts of simple repetitive DNA in Saccharomyces cerevisiae. PNAS 92:10418–21 [Google Scholar]
  132. Su SS, Lahue RS, Au KG, Modrich P. 131.  1988. Mispair specificity of methyl-directed DNA mismatch correction in vitro. J. Biol. Chem. 263:6829–35 [Google Scholar]
  133. Surtees JA, Alani E. 132.  2006. Mismatch repair factor MSH2-MSH3 binds and alters the conformation of branched DNA structures predicted to form during genetic recombination. J. Mol. Biol. 360:523–36 [Google Scholar]
  134. Szankasi P, Smith GR. 133.  1995. A role for exonuclease I from S. pombe in mutation avoidance and mismatch correction. Science 267:1166–69 [Google Scholar]
  135. Tessmer I, Yang Y, Zhai J, Du C, Hsieh P. 134.  et al. 2008. Mechanism of MutS searching for DNA mismatches and signaling repair. J. Biol. Chem. 283:36646–54 [Google Scholar]
  136. Tian L, Hou C, Tian K, Holcomb NC, Gu L, Li GM. 135.  2009. Mismatch recognition protein MutS does not hijack (CAG)n hairpin repair in vitro. J. Biol. Chem. 284:20452–56 [Google Scholar]
  137. Tishkoff DX, Boerger AL, Bertrand P, Filosi N, Gaida GM. 136.  et al. 1997. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. PNAS 94:7487–92 [Google Scholar]
  138. Tome S, Simard JP, Slean MM, Holt I, Morris GE. 137.  et al. 2013. Tissue-specific mismatch repair protein expression: MSH3 is higher than MSH6 in multiple mouse tissues. DNA Repair 12:46–52 [Google Scholar]
  139. Tran HT, Gordenin DA, Resnick MA. 138.  1999. The 3′→5′ exonucleases of DNA polymerases δ and ε and the 5′→3′ exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:2000–7 [Google Scholar]
  140. Tran HT, Keen JD, Kricker M, Resnick MA, Gordenin DA. 139.  1997. Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17:2859–65 [Google Scholar]
  141. Tran PT, Erdeniz N, Symington LS, Liskay RM. 140.  2004. EXO1-A multi-tasking eukaryotic nuclease. DNA Repair 3:1549–59 [Google Scholar]
  142. van Oers JM, Roa S, Werling U, Liu Y, Genschel J. 141.  et al. 2010. PMS2 endonuclease activity has distinct biological functions and is essential for genome maintenance. PNAS 107:13384–89 [Google Scholar]
  143. Vo AT, Zhu F, Wu X, Yuan F, Gao Y. 142.  et al. 2005. hMRE11 deficiency leads to microsatellite instability and defective DNA mismatch repair. EMBO Rep. 6:438–44 [Google Scholar]
  144. Wagner R Jr, Meselson M. 143.  1976. Repair tracts in mismatched DNA heteroduplexes. PNAS 73:4135–39 [Google Scholar]
  145. Wang H, Yang Y, Schofield MJ, Du C, Fridman Y. 144.  et al. 2003. DNA bending and unbending by MutS govern mismatch recognition and specificity. PNAS 100:14822–27 [Google Scholar]
  146. Warren JJ, Pohlhaus TJ, Changela A, Iyer RR, Modrich PL, Beese LS. 145.  2007. Structure of the human MutSα DNA lesion recognition complex. Mol. Cell 26:579–92 [Google Scholar]
  147. Wei K, Clark AB, Wong E, Kane MF, Mazur DJ. 146.  et al. 2003. Inactivation of Exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 17:603–14 [Google Scholar]
  148. Yoshida R, Miyashita K, Inoue M, Shimamoto A, Yan Z. 147.  et al. 2011. Concurrent genetic alterations in DNA polymerase proofreading and mismatch repair in human colorectal cancer. Eur. J. Hum. Genet. 19:320–25 [Google Scholar]
  149. Yu C, Gan H, Han J, Zhou ZX, Jia S. 148.  et al. 2014. Strand-specific analysis shows protein binding at replication forks and PCNA unloading from lagging strands when forks stall. Mol. Cell 56:551–63 [Google Scholar]
  150. Zanders S, Ma X, Roychoudhury A, Hernandez RD, Demogines A. 149.  et al. 2010. Detection of heterozygous mutations in the genome of mismatch repair defective diploid yeast using a Bayesian approach. Genetics 186:493–503 [Google Scholar]
  151. Zanotti KJ, Gearhart PJ. 150.  2016. Antibody diversification caused by disrupted mismatch repair and promiscuous DNA polymerases. DNA Repair. In press
  152. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y. 151.  et al. 2005. Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 122:693–705 [Google Scholar]
  153. Zheng L, Shen B. 152.  2011. Okazaki fragment maturation: nucleases take centre stage. J. Mol. Cell Biol. 3:23–30 [Google Scholar]
/content/journals/10.1146/annurev-genet-112414-054722
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Eukaryotic Mismatch Repair in Relation to DNA Replication
Annual Review of Genetics 49, 291 (2015); https://doi.org/10.1146/annurev-genet-112414-054722
/content/journals/10.1146/annurev-genet-112414-054722
/content/journals/10.1146/annurev-genet-112414-054722
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