Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates

Cell

Volumn 147, Issue 5, 2011, Pages 1040-1053

  Hombauer, Hans ^a,b,c   Campbell, Christopher S ^a,c   Smith, Catherine E ^a,b,c   Desai, Arshad ^a,c   Kolodner, Richard D ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FUNGAL DNA; MISMATCH REPAIR PROTEIN PMS2; PROTEIN MLH1; PROTEIN MSH2; PROTEIN MSH6;

ARTICLE; BASE MISPAIRING; CELL CYCLE S PHASE; CONTROLLED STUDY; FLUORESCENCE; GENE LOCATION; GENE REPLICATION; MISMATCH REPAIR; MUTATION RATE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; STOICHIOMETRY;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 81855189485     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2011.10.025     Document Type: Article

References (88)

1. S. Acharya, P.L. Foster, P. Brooks, and R. Fishel The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair Mol. Cell 12 2003 233 246
2. E. Alani The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs Mol. Cell. Biol. 16 1996 5604 5615
3. N.S. Amin, M.N. Nguyen, S. Oh, and R.D. Kolodner exo1-Dependent mutator mutations: model system for studying functional interactions in mismatch repair Mol. Cell. Biol. 21 2001 5142 5155
4. L.J. Blackwell, S. Wang, and P. Modrich DNA chain length dependence of formation and dynamics of hMutSalpha.hMutLalpha.heteroduplex complexes J. Biol. Chem. 276 2001 33233 33240
5. J. Bowers, P.T. Tran, R.M. Liskay, and E. Alani Analysis of yeast MSH2-MSH6 suggests that the initiation of mismatch repair can be separated into discrete steps J. Mol. Biol. 302 2000 327 338
6. E. Cannavo, G. Marra, J. Sabates-Bellver, M. Menigatti, S.M. Lipkin, F. Fischer, P. Cejka, and J. Jiricny Expression of the MutL homologue hMLH3 in human cells and its role in DNA mismatch repair Cancer Res. 65 2005 10759 10766
7. A.B. Clark, F. Valle, K. Drotschmann, R.K. Gary, and T.A. Kunkel Functional interaction of proliferating cell nuclear antigen with MSH2-MSH6 and MSH2-MSH3 complexes J. Biol. Chem. 275 2000 36498 36501
8. A. Datta, A. Adjiri, L. New, G.F. Crouse, and S. Jinks Robertson Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae Mol. Cell. Biol. 16 1996 1085 1093
9. S.M. Deschênes, G. Tomer, M. Nguyen, N. Erdeniz, N.C. Juba, N. Sepúlveda, J.E. Pisani, and R.M. Liskay The E705K mutation in hPMS2 exerts recessive, not dominant, effects on mismatch repair Cancer Lett. 249 2007 148 156
10. D.S. Dimitrova, I.T. Todorov, T. Melendy, and D.M. Gilbert Mcm2, but not RPA, is a component of the mammalian early G1-phase prereplication complex J. Cell Biol. 146 1999 709 722
11. L. Dzantiev, N. Constantin, J. Genschel, R.R. Iyer, P.M. Burgers, and P. Modrich A defined human system that supports bidirectional mismatch-provoked excision Mol. Cell 15 2004 31 41
12. M. Elez, A.W. Murray, L.J. Bi, X.E. Zhang, I. Matic, and M. Radman Seeing mutations in living cells Curr. Biol. 20 2010 1432 1437
13. E. Evans, N. Sugawara, J.E. Haber, and E. Alani The Saccharomyces cerevisiae Msh2 mismatch repair protein localizes to recombination intermediates in vivo Mol. Cell 5 2000 789 799
14. F. Fabre, A. Chan, W.D. Heyer, and S. Gangloff Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication Proc. Natl. Acad. Sci. USA 99 2002 16887 16892
15. W.H. Fang, and P. Modrich Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction J. Biol. Chem. 268 1993 11838 11844
16. H. Flores-Rozas, and R.D. Kolodner The Saccharomyces cerevisiae MLH3 gene functions in MSH3-dependent suppression of frameshift mutations Proc. Natl. Acad. Sci. USA 95 1998 12404 12409
17. H. Flores-Rozas, D. Clark, and R.D. Kolodner Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex Nat. Genet. 26 2000 375 378
18. J. Genschel, and P. Modrich Mechanism of 5′-directed excision in human mismatch repair Mol. Cell 12 2003 1077 1086
19. J. Genschel, S.J. Littman, J.T. Drummond, and P. Modrich Isolation of MutSbeta from human cells and comparison of the mismatch repair specificities of MutSbeta and MutSalpha J. Biol. Chem. 273 1998 19895 19901
20. S. Ghaemmaghami, W.K. Huh, K. Bower, R.W. Howson, A. Belle, N. Dephoure, E.K. O'Shea, and J.S. Weissman Global analysis of protein expression in yeast Nature 425 2003 737 741
21. S. Gradia, D. Subramanian, T. Wilson, S. Acharya, A. Makhov, J. Griffith, and R. Fishel hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA Mol. Cell 3 1999 255 261
22. L. Gu, Y. Hong, S. McCulloch, H. Watanabe, and G.M. Li ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair Nucleic Acids Res. 26 1998 1173 1178
23. Y. Habraken, P. Sung, L. Prakash, and S. Prakash Enhancement of MSH2-MSH3-mediated mismatch recognition by the yeast MLH1-PMS1 complex Curr. Biol. 7 1997 790 793
24. V.V. Hargreaves, S.S. Shell, D.J. Mazur, M.T. Hess, and R.D. Kolodner Interaction between the Msh2 and Msh6 nucleotide-binding sites in the Saccharomyces cerevisiae Msh2-Msh6 complex J. Biol. Chem. 285 2010 9301 9310
25. M.T. Hess, M.L. Mendillo, D.J. Mazur, and R.D. Kolodner Biochemical basis for dominant mutations in the Saccharomyces cerevisiae MSH6 gene Proc. Natl. Acad. Sci. USA 103 2006 558 563
26. P. Hozák, A.B. Hassan, D.A. Jackson, and P.R. Cook Visualization of replication factories attached to nucleoskeleton Cell 73 1993 361 373
27. S.N. Huang, and D.M. Crothers The role of nucleotide cofactor binding in cooperativity and specificity of MutS recognition J. Mol. Biol. 384 2008 31 47
28. I. Iaccarino, G. Marra, F. Palombo, and J. Jiricny hMSH2 and hMSH6 play distinct roles in mismatch binding and contribute differently to the ATPase activity of hMutSalpha EMBO J. 17 1998 2677 2686
29. R.R. Iyer, A. Pluciennik, V. Burdett, and P.L. Modrich DNA mismatch repair: functions and mechanisms Chem. Rev. 106 2006 302 323
30. J. Jiricny, S.S. Su, S.G. Wood, and P. Modrich Mismatch-containing oligonucleotide duplexes bound by the E. coli mutS-encoded protein Nucleic Acids Res. 16 1988 7843 7853
31. A.P. Joglekar, D.C. Bouck, J.N. Molk, K.S. Bloom, and E.D. Salmon Molecular architecture of a kinetochore-microtubule attachment site Nat. Cell Biol. 8 2006 581 585
32. F.A. Kadyrov, L. Dzantiev, N. Constantin, and P. Modrich Endonucleolytic function of MutLalpha in human mismatch repair Cell 126 2006 297 308
33. F.A. Kadyrov, S.F. Holmes, M.E. Arana, O.A. Lukianova, M. O'Donnell, T.A. Kunkel, and P. Modrich Saccharomyces cerevisiae MutLalpha is a mismatch repair endonuclease J. Biol. Chem. 282 2007 37181 37190
34. F.A. Kadyrov, J. Genschel, Y. Fang, E. Penland, W. Edelmann, and P. Modrich A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair Proc. Natl. Acad. Sci. USA 106 2009 8495 8500
35. E. Kitamura, J.J. Blow, and T.U. Tanaka Live-cell imaging reveals replication of individual replicons in eukaryotic replication factories Cell 125 2006 1297 1308
36. H.E. Kleczkowska, G. Marra, T. Lettieri, and J. Jiricny hMSH3 and hMSH6 interact with PCNA and colocalize with it to replication foci Genes Dev. 15 2001 724 736
37. R. Kolodner Biochemistry and genetics of eukaryotic mismatch repair Genes Dev. 10 1996 1433 1442
38. R.D. Kolodner, and G.T. Marsischky Eukaryotic DNA mismatch repair Curr. Opin. Genet. Dev. 9 1999 89 96
39. T.A. Kunkel, and D.A. Erie DNA mismatch repair Annu. Rev. Biochem. 74 2005 681 710
40. G.I. Lang, and A.W. Murray Estimating the per-base-pair mutation rate in the yeast Saccharomyces cerevisiae Genetics 178 2008 67 82
41. R.A. Laskey, and M.A. Madine A rotary pumping model for helicase function of MCM proteins at a distance from replication forks EMBO Rep. 4 2003 26 30
42. P.J. Lau, H. Flores-Rozas, and R.D. Kolodner Isolation and characterization of new proliferating cell nuclear antigen (POL30) mutator mutants that are defective in DNA mismatch repair Mol. Cell. Biol. 22 2002 6669 6680
43. S.D. Lee, and E. Alani Analysis of interactions between mismatch repair initiation factors and the replication processivity factor PCNA J. Mol. Biol. 355 2006 175 184
44. L. Li, K.M. Murphy, U. Kanevets, and L.J. Reha-Krantz Sensitivity to phosphonoacetic acid: a new phenotype to probe DNA polymerase delta in Saccharomyces cerevisiae Genetics 170 2005 569 580
45. M. Lisby, R. Rothstein, and U.H. Mortensen Rad52 forms DNA repair and recombination centers during S phase Proc. Natl. Acad. Sci. USA 98 2001 8276 8282
46. G.T. Marsischky, and R.D. Kolodner Biochemical characterization of the interaction between the Saccharomyces cerevisiae MSH2-MSH6 complex and mispaired bases in DNA J. Biol. Chem. 274 1999 26668 26682
47. G.T. Marsischky, N. Filosi, M.F. Kane, and R. Kolodner Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair Genes Dev. 10 1996 407 420
48. I. Matic, C. Rayssiguier, and M. Radman Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species Cell 80 1995 507 515
49. M.L. Mendillo, D.J. Mazur, and R.D. Kolodner Analysis of the interaction between the Saccharomyces cerevisiae MSH2-MSH6 and MLH1-PMS1 complexes with DNA using a reversible DNA end-blocking system J. Biol. Chem. 280 2005 22245 22257
50. A. Morrison, J.B. Bell, T.A. Kunkel, and A. Sugino Eukaryotic DNA polymerase amino acid sequence required for 3′-5′ exonuclease activity Proc. Natl. Acad. Sci. USA 88 1991 9473 9477
51. A. Morrison, A.L. Johnson, L.H. Johnston, and A. Sugino Pathway correcting DNA replication errors in Saccharomyces cerevisiae EMBO J. 12 1993 1467 1473
52. J. Newport, and H. Yan Organization of DNA into foci during replication Curr. Opin. Cell Biol. 8 1996 365 368
53. S.A. Nick McElhinny, C.M. Stith, P.M. Burgers, and T.A. Kunkel Inefficient proofreading and biased error rates during inaccurate DNA synthesis by a mutant derivative of Saccharomyces cerevisiae DNA polymerase delta J. Biol. Chem. 282 2007 2324 2332
54. S.A. Nick McElhinny, D.A. Gordenin, C.M. Stith, P.M. Burgers, and T.A. Kunkel Division of labor at the eukaryotic replication fork Mol. Cell 30 2008 137 144
55. J. Park, Y. Jeon, D. In, R. Fishel, C. Ban, and J.B. Lee Single-molecule analysis reveals the kinetics and physiological relevance of MutL-ssDNA binding PLoS ONE 5 2010 e15496
56. P. Peltomäki Role of DNA mismatch repair defects in the pathogenesis of human cancer J. Clin. Oncol. 21 2003 1174 1179
57. A. Pluciennik, L. Dzantiev, R.R. Iyer, N. Constantin, F.A. Kadyrov, and P. Modrich PCNA function in the activation and strand direction of MutLα endonuclease in mismatch repair Proc. Natl. Acad. Sci. USA 107 2010 16066 16071
58. T.A. Prolla, Q. Pang, E. Alani, R.D. Kolodner, and R.M. Liskay MLH1, PMS1, and MSH2 interactions during the initiation of DNA mismatch repair in yeast Science 265 1994 1091 1093
59. Z.F. Pursell, I. Isoz, E.B. Lundström, E. Johansson, and T.A. Kunkel Yeast DNA polymerase epsilon participates in leading-strand DNA replication Science 317 2007 127 130
60. C.D. Putnam, T.K. Hayes, and R.D. Kolodner Specific pathways prevent duplication-mediated genome rearrangements Nature 460 2009 984 989
61. C. Schmutte, M.M. Sadoff, K.S. Shim, S. Acharya, and R. Fishel The interaction of DNA mismatch repair proteins with human exonuclease I J. Biol. Chem. 276 2001 33011 33018
62. S.S. Shell, C.D. Putnam, and R.D. Kolodner The N terminus of Saccharomyces cerevisiae Msh6 is an unstructured tether to PCNA Mol. Cell 26 2007 565 578
63. K. Shibahara, and B. Stillman Replication-dependent marking of DNA by PCNA facilitates CAF-1-coupled inheritance of chromatin Cell 96 1999 575 585
64. E.A. Sia, R.J. Kokoska, M. Dominska, P. Greenwell, and T.D. Petes Microsatellite instability in yeast: dependence on repeat unit size and DNA mismatch repair genes Mol. Cell. Biol. 17 1997 2851 2858
65. B.T. Smith, A.D. Grossman, and G.C. Walker Visualization of mismatch repair in bacterial cells Mol. Cell 8 2001 1197 1206
66. D.X. Tishkoff, A.L. Boerger, P. Bertrand, N. Filosi, G.M. Gaida, M.F. Kane, and R.D. Kolodner Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2 Proc. Natl. Acad. Sci. USA 94 1997 7487 7492
67. H.T. Tran, D.A. Gordenin, and M.A. Resnick The 3′->5′ exonucleases of DNA polymerases delta and epsilon and the 5′->3′ exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae Mol. Cell. Biol. 19 1999 2000 2007
68. P.T. Tran, J.A. Simon, and R.M. Liskay Interactions of Exo1p with components of MutLalpha in Saccharomyces cerevisiae Proc. Natl. Acad. Sci. USA 98 2001 9760 9765
69. A. Umar, A.B. Buermeyer, J.A. Simon, D.C. Thomas, A.B. Clark, R.M. Liskay, and T.A. Kunkel Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis Cell 87 1996 65 73
70. H. Wang, and J.B. Hays Mismatch repair in human nuclear extracts. Quantitative analyses of excision of nicked circular mismatched DNA substrates, constructed by a new technique employing synthetic oligonucleotides J. Biol. Chem. 277 2002 26136 26142
71. S. Zanders, X. Ma, A. Roychoudhury, R.D. Hernandez, A. Demogines, B. Barker, Z. Gu, C.D. Bustamante, and E. Alani Detection of heterozygous mutations in the genome of mismatch repair defective diploid yeast using a Bayesian approach Genetics 186 2010 493 503
72. Y. Zhang, F. Yuan, S.R. Presnell, K. Tian, Y. Gao, A.E. Tomkinson, L. Gu, and G.M. Li Reconstitution of 5′-directed human mismatch repair in a purified system Cell 122 2005 693 705
73. H. Zou, and R. Rothstein Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism Cell 90 1997 87 96
74. Amin, N.S., Nguyen, M.N., Oh, S., and Kolodner, R.D. (2001). exo1-dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol. Cell. Biol. 21, 5142-5155.
75. Hargreaves, V.V., Shell, S.S., Mazur, D.J., Hess, M.T., and Kolodner, R.D. (2010). Interaction between the Msh2 and Msh6 nucleotide-binding sites in the Saccharomyces cerevisiae Msh2-Msh6 complex. J. Biol. Chem. 285, 9301-9310.
76. Hess, M.T., Gupta, R.D., and Kolodner, R.D. (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, 25545-25553.
77. Janke, C., Magiera, M.M., Rathfelder, N., Taxis, C., Reber, S., Maekawa, H., Moreno-Borchart, A., Doenges, G., Schwob, E., Schiebel, E., and Knop, M. (2004). A versatile toolbox for PCR-based tagging of yeast genes: new fluorescent proteins, more markers and promoter substitution cassettes. Yeast 21, 947-962.
78. Joglekar, A.P., Bouck, D.C., Molk, J.N., Bloom, K.S., and Salmon, E.D. (2006). Molecular architecture of a kinetochore-microtubule attachment site. Nat. Cell Biol. 8, 581-585.
79. Lau, P.J., Flores-Rozas, H., and Kolodner, R.D. (2002). Isolation and characterization of new proliferating cell nuclear antigen (POL30) mutator mutants that are defective in DNA mismatch repair. Mol. Cell. Biol. 22, 6669-6680.
80. Lea, D.E., and Coulson, C.A. (1948). The distribution of the numbers of mutants in bacterial populations. J. Genet. 49, 264-285.
81. Li, L., Murphy, K.M., Kanevets, U., and Reha-Krantz, L.J. (2005). Sensitivity to phosphonoacetic acid: a new phenotype to probe DNA polymerase delta in Saccharomyces cerevisiae. Genetics 170, 569-580.
82. Marsischky, G.T., Filosi, N., Kane, M.F., and Kolodner, R. (1996). Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10, 407-420.
83. Morrison, A., Bell, J.B., Kunkel, T.A., and Sugino, A. (1991). Eukaryotic DNA polymerase amino acid sequence required for 3′-5′ exonuclease activity. Proc. Natl. Acad. Sci. USA 88, 9473-9477.
84. Morrison, A., Johnson, A.L., Johnston, L.H., and Sugino, A. (1993). Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J. 12, 1467-1473.
85. Pursell, Z.F., Isoz, I., Lundström, E.B., Johansson, E., and Kunkel, T.A. (2007). Yeast DNA polymerase epsilon participates in leading-strand DNA replication. Science 317, 127-130.
86. Shell, S.S., Putnam, C.D., and Kolodner, R.D. (2007). The N terminus of Saccharomyces cerevisiae Msh6 is an unstructured tether to PCNA. Mol. Cell 26, 565-578.
87. Tran, H.T., Keen, J.D., Kricker, M., Resnick, M.A., and Gordenin, D.A. (1997). Hypermutability of homonucleotide runs in mismatch repair and DNA polymerase proofreading yeast mutants. Mol. Cell. Biol. 17, 2859-2865.
88. Wach, A., Brachat, A., Pöhlmann, R., and Philippsen, P. (1994). New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast 10, 1793-1808.