Dominant Mutations in S. cerevisiae PMS1 Identify the Mlh1-Pms1 Endonuclease Active Site and an Exonuclease 1-Independent Mismatch Repair Pathway

PLoS Genetics

Volumn 9, Issue 10, 2013, Pages

  Smith, Catherine E ^a   Mendillo, Marc L ^a,d   Bowen, Nikki ^a   Hombauer, Hans ^a,e   Campbell, Christopher S ^a   Desai, Arshad ^a,b   Putnam, Christopher D ^a,c   Kolodner, Richard D ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^d WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

^e GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDONUCLEASE; EXONUCLEASE; FUNGAL ENZYME; MLH1 PMS1 ENDONUCLEASE; UNCLASSIFIED DRUG; CARRIER PROTEIN; DNA BINDING PROTEIN; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I; MLH1 PROTEIN, S CEREVISIAE; PMS1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

AMINO ACID SUBSTITUTION; ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INACTIVATION; FRAMESHIFT MUTATION; FUNGAL GENE; GENE MUTATION; MISMATCH REPAIR; MISSENSE MUTATION; MOLECULAR MODEL; MUTAGENESIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPE; PLASMID; PMS1 GENE; POINT MUTATION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; SITE DIRECTED MUTAGENESIS; GENETICS; GROWTH, DEVELOPMENT AND AGING; HEREDITARY NONPOLYPOSIS COLORECTAL CANCER; HUMAN; METABOLISM; MUTATION; PATHOLOGY; PROTEIN TERTIARY STRUCTURE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; CARRIER PROTEINS; CATALYTIC DOMAIN; COLORECTAL NEOPLASMS, HEREDITARY NONPOLYPOSIS; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; EXODEOXYRIBONUCLEASES; HUMANS; MUTATION; PROTEIN STRUCTURE, TERTIARY; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION;

EID: 84887274666     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1003869     Document Type: Article

References (72)

1. de la Chapelle A, (2004) Genetic predisposition to colorectal cancer. Nat Rev Cancer 4: 769-780.
2. Peltomaki P, Vasen HF, (1997) Mutations predisposing to hereditary nonpolyposis colorectal cancer: database and results of a collaborative study. The International Collaborative Group on Hereditary Nonpolyposis Colorectal Cancer. Gastroenterology 113: 1146-1158.
3. Borresen AL, Lothe RA, Meling GI, Lystad S, Morrison P, et al. (1995) Somatic mutations in the hMSH2 gene in microsatellite unstable colorectal carcinomas. Hum Mol Genet 4: 2065-2072.
4. Kane MF, Loda M, Gaida GM, Lipman J, Mishra R, et al. (1997) Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. Cancer Res 57: 808-811.
5. Network TCGA (2012) Comprehensive molecular characterization of human colon and rectal cancer. Nature 487: 330-337.
6. Network TCGA (2013) Integrated genomic characterization of endometrial carcinoma. Nature 497: 67-73.
7. Peltomaki P, (2003) Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21: 1174-1179.
8. Datta A, Adjiri A, New L, Crouse GF, Jinks Robertson S, (1996) Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae. Mol Cell Biol 16: 1085-1093.
9. Matic I, Rayssiguier C, Radman M, (1995) Interspecies gene exchange in bacteria: the role of SOS and mismatch repair systems in evolution of species. Cell 80: 507-515.
10. Putnam CD, Hayes TK, Kolodner RD, (2009) Specific pathways prevent duplication-mediated genome rearrangements. Nature 460: 984-989.
11. Iyer RR, Pluciennik A, Burdett V, Modrich PL, (2006) DNA mismatch repair: functions and mechanisms. Chem Rev 106: 302-323.
12. Kolodner RD, Marsischky GT, (1999) Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9: 89-96.
13. Kunkel TA, Erie DA, (2005) DNA mismatch repair. Annu Rev Biochem 74: 681-710.
14. Lahue RS, Au KG, Modrich P, (1989) DNA mismatch correction in a defined system. Science 245: 160-164.
15. Lamers MH, Perrakis A, Enzlin JH, Winterwerp HH, de Wind N, et al. (2000) The crystal structure of DNA mismatch repair protein MutS binding to a G×T mismatch. Nature 407: 711-717.
16. Obmolova G, Ban C, Hsieh P, Yang W, (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407: 703-710.
17. Acharya S, Foster PL, Brooks P, Fishel R, (2003) The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol Cell 12: 233-246.
18. Welsh KM, Lu AL, Clark S, Modrich P, (1987) Isolation and characterization of the Escherichia coli mutH gene product. J Biol Chem 262: 15624-15629.
19. Burdett V, Baitinger C, Viswanathan M, Lovett ST, Modrich P, (2001) In vivo requirement for RecJ, ExoVII, ExoI, and ExoX in methyl-directed mismatch repair. Proc Natl Acad Sci U S A 98: 6765-6770.
20. Acharya S, Wilson T, Gradia S, Kane MF, Guerrette S, et al. (1996) hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci U S A 93: 13629-13634.
21. Marsischky GT, Filosi N, Kane MF, Kolodner R, (1996) Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev 10: 407-420.
22. Prolla TA, Pang Q, Alani E, Kolodner RD, Liskay RM, (1994) MLH1, PMS1, and MSH2 interactions during the initiation of DNA mismatch repair in yeast. Science 265: 1091-1093.
23. Mendillo ML, Mazur DJ, Kolodner RD, (2005) 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: 22245-22257.
24. Blackwell LJ, Wang S, Modrich P, (2001) DNA chain length dependence of formation and dynamics of hMutSalpha.hMutLalpha.heteroduplex complexes. J Biol Chem 276: 33233-33240.
25. Kadyrov FA, Dzantiev L, Constantin N, Modrich P, (2006) Endonucleolytic function of MutLalpha in human mismatch repair. Cell 126: 297-308.
26. Kadyrov FA, Holmes SF, Arana ME, Lukianova OA, O'Donnell M, et al. (2007) Saccharomyces cerevisiae MutLalpha is a mismatch repair endonuclease. J Biol Chem 282: 37181-37190.
27. Amin NS, Nguyen MN, Oh S, Kolodner RD, (2001) exo1-Dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol Cell Biol 21: 5142-5155.
28. Tishkoff DX, Boerger AL, Bertrand P, Filosi N, Gaida GM, et al. (1997) Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A 94: 7487-7492.
29. Wei K, Clark AB, Wong E, Kane MF, Mazur DJ, 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: 603-614.
30. Constantin N, Dzantiev L, Kadyrov FA, Modrich P, (2005) Human mismatch repair: reconstitution of a nick-directed bidirectional reaction. J Biol Chem 280: 39752-39761.
31. Flores-Rozas H, Clark D, Kolodner RD, (2000) Proliferating cell nuclear antigen and Msh2p-Msh6p interact to form an active mispair recognition complex. Nat Genet 26: 375-378.
32. Lin YL, Shivji MK, Chen C, Kolodner R, Wood RD, et al. (1998) The evolutionarily conserved zinc finger motif in the largest subunit of human replication protein A is required for DNA replication and mismatch repair but not for nucleotide excision repair. J Biol Chem 273: 1453-1461.
33. Umar A, Buermeyer AB, Simon JA, Thomas DC, Clark AB, et al. (1996) Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell 87: 65-73.
34. Zhang Y, Yuan F, Presnell SR, Tian K, Gao Y, et al. (2005) Reconstitution of 5′-directed human mismatch repair in a purified system. Cell 122: 693-705.
35. Xie Y, Counter C, Alani E, (1999) Characterization of the repeat-tract instability and mutator phenotypes conferred by a Tn3 insertion in RFC1, the large subunit of the yeast clamp loader. Genetics 151: 499-509.
36. Dzantiev L, Constantin N, Genschel J, Iyer RR, Burgers PM, et al. (2004) A defined human system that supports bidirectional mismatch-provoked excision. Mol Cell 15: 31-41.
37. Longley MJ, Pierce AJ, Modrich P, (1997) DNA polymerase delta is required for human mismatch repair in vitro. J Biol Chem 272: 10917-10921.
38. Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD, (2011) Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147: 1040-1053.
39. Hombauer H, Srivatsan A, Putnam CD, Kolodner RD, (2011) Mismatch repair, but not heteroduplex rejection, is temporally coupled to DNA replication. Science 334: 1713-1716.
40. Langston LD, O'Donnell M, (2006) DNA replication: keep moving and don't mind the gap. Mol Cell 23: 155-160.
41. Benkovic SJ, Valentine AM, Salinas F, (2001) Replisome-mediated DNA replication. Annu Rev Biochem 70: 181-208.
42. Liberti SE, Larrea AA, Kunkel TA, (2013) Exonuclease 1 preferentially repairs mismatches generated by DNA polymerase alpha. DNA Repair (Amst) 12: 92-96.
43. Pluciennik A, Dzantiev L, Iyer RR, Constantin N, Kadyrov FA, et al. (2010) PCNA function in the activation and strand direction of MutLalpha endonuclease in mismatch repair. Proc Natl Acad Sci U S A 107: 16066-16071.
44. Genschel J, Modrich P, (2003) Mechanism of 5′-directed excision in human mismatch repair. Mol Cell 12: 1077-1086.
45. Kadyrov FA, Genschel J, Fang Y, Penland E, Edelmann W, et al. (2009) A possible mechanism for exonuclease 1-independent eukaryotic mismatch repair. Proc Natl Acad Sci U S A 106: 8495-8500.
46. Gueneau E, Dherin C, Legrand P, Tellier-Lebegue C, Gilquin B, et al. (2013) Structure of the MutLalpha C-terminal domain reveals how Mlh1 contributes to Pms1 endonuclease site. Nat Struct Mol Biol 20: 461-468.
47. Namadurai S, Jain D, Kulkarni DS, Tabib CR, Friedhoff P, et al. (2010) The C-terminal domain of the MutL homolog from Neisseria gonorrhoeae forms an inverted homodimer. PLoS One 5: e13726.
48. Pillon MC, Lorenowicz JJ, Uckelmann M, Klocko AD, Mitchell RR, et al. (2010) Structure of the endonuclease domain of MutL: unlicensed to cut. Mol Cell 39: 145-151.
49. Tran PT, Erdeniz N, Symington LS, Liskay RM, (2004) EXO1-A multi-tasking eukaryotic nuclease. DNA Repair (Amst) 3: 1549-1559.
50. Tran PT, Erdeniz N, Dudley S, Liskay RM, (2002) Characterization of nuclease-dependent functions of Exo1p in Saccharomyces cerevisiae. DNA Repair (Amst) 1: 895-912.
51. Pang Q, Prolla TA, Liskay RM, (1997) Functional domains of the Saccharomyces cerevisiae Mlh1p and Pms1p DNA mismatch repair proteins and their relevance to human hereditary nonpolyposis colorectal cancer-associated mutations. Mol Cell Biol 17: 4465-4473.
52. Nick McElhinny SA, Stith CM, Burgers PM, Kunkel TA, (2007) Inefficient proofreading and biased error rates during inaccurate DNA synthesis by a mutant derivative of Saccharomyces cerevisiae DNA polymerase delta. J Biol Chem 282: 2324-2332.
53. Nick McElhinny SA, Kumar D, Clark AB, Watt DL, Watts BE, et al. (2010) Genome instability due to ribonucleotide incorporation into DNA. Nat Chem Biol 6: 774-781.
54. Nick McElhinny SA, Watts BE, Kumar D, Watt DL, Lundstrom EB, et al. (2010) Abundant ribonucleotide incorporation into DNA by yeast replicative polymerases. Proc Natl Acad Sci U S A 107: 4949-4954.
55. Pursell ZF, Isoz I, Lundstrom EB, Johansson E, Kunkel TA, (2007) Regulation of B family DNA polymerase fidelity by a conserved active site residue: characterization of M644W, M644L and M644F mutants of yeast DNA polymerase epsilon. Nucleic Acids Res 35: 3076-3086.
56. Deschenes SM, Tomer G, Nguyen M, Erdeniz N, Juba NC, et al. (2007) The E705K mutation in hPMS2 exerts recessive, not dominant, effects on mismatch repair. Cancer Lett 249: 148-156.
57. Zakharyevich K, Tang S, Ma Y, Hunter N, (2012) Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase. Cell 149: 334-347.
58. Brown MS, Lim E, Chen C, Nishant KT, Alani E, (2013) Genetic Analysis of mlh3 Mutations Reveals Interactions Between Crossover Promoting Factors During Meiosis in Baker's Yeast. G3 (Bethesda) 3: 9-22.
59. Hunter N, Borts RH, (1997) Mlh1 is unique among mismatch repair proteins in its ability to promote crossing-over during meiosis. Genes Dev 11: 1573-1582.
60. Duppatla V, Bodda C, Urbanke C, Friedhoff P, Rao DN, (2009) The C-terminal domain is sufficient for endonuclease activity of Neisseria gonorrhoeae MutL. Biochem J 423: 265-277.
61. Fukui K, Nishida M, Nakagawa N, Masui R, Kuramitsu S, (2008) Bound nucleotide controls the endonuclease activity of mismatch repair enzyme MutL. J Biol Chem 283: 12136-12145.
62. Iino H, Kim K, Shimada A, Masui R, Kuramitsu S, et al. (2011) Characterization of C- and N-terminal domains of Aquifex aeolicus MutL endonuclease: N-terminal domain stimulates the endonuclease activity of C-terminal domain in a zinc-dependent manner. Biosci Rep 31: 309-322.
63. Kosinski J, Plotz G, Guarne A, Bujnicki JM, Friedhoff P, (2008) The PMS2 subunit of human MutLalpha contains a metal ion binding domain of the iron-dependent repressor protein family. J Mol Biol 382: 610-627.
64. Hargreaves VV, Shell SS, Mazur DJ, Hess MT, Kolodner RD, (2010) Interaction between the Msh2 and Msh6 nucleotide-binding sites in the Saccharomyces cerevisiae Msh2-Msh6 complex. J Biol Chem 285: 9301-9310.
65. Umezu K, Sugawara N, Chen C, Haber JE, Kolodner RD, (1998) Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics 148: 989-1005.
66. Gerik KJ, Gary SL, Burgers PM, (1997) Overproduction and affinity purification of Saccharomyces cerevisiae replication factor C. J Biol Chem 272: 1256-1262.
67. Ayyagari R, Impellizzeri KJ, Yoder BL, Gary SL, Burgers PM, (1995) A mutational analysis of the yeast proliferating cell nuclear antigen indicates distinct roles in DNA replication and DNA repair. Mol Cell Biol 15: 4420-4429.
68. Fien K, Stillman B, (1992) Identification of replication factor C from Saccharomyces cerevisiae: a component of the leading-strand DNA replication complex. Mol Cell Biol 12: 155-163.
69. Brunger AT, Adams PD, Clore GM, DeLano WL, Gros P, et al. (1998) Crystallography & NMR system: A new software suite for macromolecular structure determination. Acta Crystallogr D Biol Crystallogr 54: 905-921.
70. McRee DE, (1999) XtalView/Xfit-A versatile program for manipulating atomic coordinates and electron density. J Struct Biol 125: 156-165.
71. Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA, (2008) Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins 70: 611-625.
72. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539.