Characterization of a highly conserved binding site of Mlhl required for exonuclease I-dependent mismatch repair

Molecular and Cellular Biology

Volumn 29, Issue 3, 2009, Pages 907-918

  Dherin, Claudine ^a,b   Gueneau, Emeric ^b,c   Francin, Mathilde ^a,b,h   Nunez, Marcela ^b,c   Miron, Simona ^d,e   Liberti, Sascha Emilie ^f   Rasmussen, Lene Juel ^f   Zinn Justin, Sophie ^b,c   Gilquin, Bernard ^b,c   Charbonnier, Jean Baptiste ^b,c,g   Boiteux, Serge ^a,b  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

^b CNRS   (France)

^c SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

^d INSTITUT CURIE   (France)

^e Centre Universitaire   (France)

^f ROSKILDE UNIVERSITY   (Denmark)

^g DIF   (France)

^h INRA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOM SYNDROME HELICASE; EXONUCLEASE; FUNGAL PROTEIN; MISMATCH REPAIR PROTEIN; MISMATCH REPAIR PROTEIN EXO1; MISMATCH REPAIR PROTEIN NTG2; MISMATCH REPAIR PROTEIN SGS1; PEPTIDE; PROTEIN MLH1; UNCLASSIFIED DRUG; AMINO ACID; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I; MLH1 PROTEIN, HUMAN; MLH1 PROTEIN, S CEREVISIAE; NUCLEAR PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN; SIGNAL TRANSDUCING ADAPTOR PROTEIN;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CONSERVATION GENETICS; CONTROLLED STUDY; DIMERIZATION; FUNGAL STRAIN; HISTOGRAM; HUMAN; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS; AMINO ACID SEQUENCE; CALORIMETRY; CHEMICAL STRUCTURE; CHEMISTRY; ENZYMOLOGY; GENE DELETION; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN BINDING; PROTEIN MOTIF; SPECIES DIFFERENCE; STRUCTURE ACTIVITY RELATION; TWO HYBRID SYSTEM;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; AMINO ACIDS; BINDING SITES; CALORIMETRY; CONSERVED SEQUENCE; DIMERIZATION; DNA MISMATCH REPAIR; EXODEOXYRIBONUCLEASES; HUMANS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR PROTEINS; PEPTIDES; PROTEIN BINDING; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SEQUENCE DELETION; SPECIES SPECIFICITY; STRUCTURE-ACTIVITY RELATIONSHIP; TWO-HYBRID SYSTEM TECHNIQUES;

EID: 59249089352     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00945-08     Document Type: Article

References (54)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Amin, N. S., M. N. Nguyen, S. Oh, and R. D. Kolodner. 2001. exoi-Dependent mutator mutations: model system for studying functional interactions in mismatch repair. Mol. Cell. Biol. 21:5142-5155.
3. Argueso, J. L., A. W. Kijas, S. Sarin, J. Heck, M. Waase, and E. Alani. 2003. Systematic mutagenesis of the Saccharomyces cerevisiae MLH1 gene reveals distinct roles for Mlh1p in meiotic crossing over and in vegetative and meiotic mismatch repair. Mol. Cell. Biol. 23:873-886.
4. Baker, S. M., A. W. Plug, T. A. Prolla, C. E. Bronner, A. C. Harris, X. Yao, D. M. Christie, C. Monell, N. Arnheim, A. Bradley, T. Ashley, and R. M. Liskay. 1996. Involvement of mouse Mlh1 in DNA mismatch repair and meiotic crossing over. Nat. Genet. 13:336-342.
5. Baudin, A., O. Ozier-Kalogeropoulos, A. Denouel, F. Lacroute, and C. Cullin. 1993. A simple and efficient method for direct gene deletion in Saccharomyces cerevisiae. Nucleic Acids Res. 21:3329-3330.
6. Cannavo, E., B. Gerrits, G. Marra, R. Schlapbach, and J. Jiricny. 2007. Characterization of the interactome of the human MutL homologues MLH1, PMS1, and PMS2. J. Biol. Chem. 282:2976-2986.
7. Edelmann, W., P. E. Cohen, M. Kane, K. Lau, B. Morrow, S. Bennett, A. Umar, T. Kunkel, G. Cattoretti, R. Chaganti, J. W. Pollard, R. D. Kolodner, and R. Kucherlapati. 1996. Meiotic pachytene arrest in MLH1-deficient mice. Cell 85:1125-1134.
8. Edgar, R. C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
9. Erdeniz, N., M. Nguyen, S. M. Deschenes, and R. M. Liskay. 2007. Mutations affecting a putative MutLα endonuclease motif impact multiple mismatch repair functions. DNA Repair 6:1463-1470.
10. Fiser, A., and A. Sali. 2003. Modeller: generation and refinement of homology-based protein structure models. Methods Enzymol. 374:461-491.
11. Fromont-Racine, M., J. C. Rain, and P. Legrain. 1997. Toward a functional analysis of the yeast genome through exhaustive two-hybrid screens. Nat. Genet. 16:277-282.
12. Gellon, L., M. Werner, and S. Boiteux. 2002. Ntg2p, a Saccharomyces cerevisiae DNA N-glycosylase/apurinic or apyrimidinic lyase involved in base excision repair of oxidative DNA damage, interacts with the DNA mismatch repair protein Mlh1p. Identification of a Mlh1p binding motif. J. Biol. Chem. 277:29963-29972.
13. Gietz, D., A. St. Jean, R. A. Woods, and R. H. Schiestl. 1992. Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20:1425.
14. Guarne, A., S. Ramon-Maiques, E. M. Wolff, R. Ghirlando, X. Hu, J. H. Miller, and W. Yang. 2004. Structure of the MutL C-terminal domain: a model of intact MutL and its roles in mismatch repair. EMBO J. 23:4134-4145.
15. Hall, M. C., P. V. Shcherbakova, J. M. Fortune, C. H. Borchers, J. M. Dial, K. B. Tomer, and T. A. Kunkel. 2003. DNA binding byyeast Mlh1 and Pms1:implications for DNA mismatch repair. Nucleic Acids Res. 31:2025-2034.
16. Jager, A. C., M. Rasmussen, H. C. Bisgaard, K. K. Singh, F. C. Nielsen, and L. J. Rasmussen. 2001. HNPCC mutations in the human DNA mismatch repair gene hMLH1 influence assembly of hMutLα and hMLH1-hEXO1 complexes. Oncogene 20:3590-3595.
17. Jiricny, J. 2006. The multifaceted mismatch-repair system. Nat. Rev. Mol. Cell. Biol. 7:335-346.
18. Kadyrov, F. A., L. Dzantiev, N. Constantin, and P. Modrich. 2006. Endonucleolytic function of MutLα in human mismatch repair. Cell 126:297-308.
19. Kadyrov, F. A., S. F. Holmes, M. E. Arana, O. A. Lukianova, M. O'Donnell, T. A. Kunkel, and P. Modrich. 2007. Saccharomyces cerevisiae MutLα is a mismatch repair endonuclease. J. Biol. Chem. 282:37181-37190.
20. Keskin, O., A. Gursoy, B. Ma, and R. Nussinov. 2008. Principles of protein- protein interactions: what are the preferred ways for proteins to interact? Chem. Rev. 108:1225-1244.
21. Kosinski, J., I. Steindorf, J. M. Bujnicki, L. Giron-Monzon, and P. Friedhoff. 2005. Analysis of the quaternary structure of the MutL C-terminal domain. J. Mol. Biol. 351:895-909.
22. Kunkel, T. A., and D. A. Erie. 2005. DNA mismatch repair. Annu. Rev. Biochem. 74:681-710.
23. Lagerstedt Robinson, K., T. Liu, J. Vandrovcova, B. Halvarsson, M. Clendenning, T. Frebourg, N. Papadopoulos, K. W. Kinzler, B. Vogelstein, P. Peltomaki, R. D. Kolodner, M. Nilbert, and A. Lindblom. 2007. Lynch syndrome (hereditary nonpolyposis colorectal cancer) diagnostics. J. Natl. Cancer Inst. 99:291-299.
24. Landau, M., I. Mayrose, Y. Rosenberg, F. Glaser, E. Martz, T. Pupko, and N. Ben-Tal. 2005. ConSurf 2005: the proiection of evolutionary conservation scores of residues on protein structures. Nucleic Acids Res. 33:W299-W302.
25. Langland, G., J. Kordich, J. Creaney, K. H. Goss, K. Lillard-Wetherell, K. Bebenek, T. A. Kunkel, and J. Groden. 2001. The Bloom's syndrome protein (BLM) interacts with MLH1 but is not required for DNA mismatch repair. J. Biol. Chem. 276:30031-30035.
26. Lea, D. E., and D. A. Coulson. 1949. The distribution of the numbers of mutants in bacterial populations. J. Genet. 49:264-285.
27. Lee, S. D., and E. Alani. 2006. Analysis of interactions between mismatch repair initiation factors and the replication processivity factor PCNA. J. Mol. Biol. 355:175-184.
28. Longtine, M. S., A. McKenzie III, D. J. Demarini, N. G. Shah, A. Wach, A. Brachat, P. Philippsen, and J. R. Pringle. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Sac- charomyces cerevisiae. Yeast 14:953-961.
29. Lutzen, A., S. E. Liberti, and L. J. Rasmussen. 2004. Cadmium inhibits human DNA mismatch repair in vivo. Biochem. Biophys. Res. Commun. 321:21-25.
30. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. McGuffin, L. J., K. Bryson, and D. T. Jones. 2000. The PSIPRED protein structure prediction server. Bioinformatics 16:404-405.
32. Modrich, P. 2006. Mechanisms in eukaryotic mismatch repair. J. Biol. Chem. 281:30305-30309.
33. Moldovan, G. L., B. Pfander, and S. Jentsch. 2007. PCNA, the maestro of the replication fork. Cell 129:665-679.
34. Nielsen, F. C., A. C. Jager, A. Lutzen, J. R. Bundgaard, and L. J. Rasmussen. 2004. Characterization of human exonuclease 1 in complex with mismatch repair proteins, subcellular localization and association with PCNA. Oncogene 23:1457-1468.
35. Pedrazzi, G., C. Perrera, H. Blaser, P. Kuster, G. Marra, S. L. Davies, G. H. Ryu, R. Freire, I. D. Hickson, J. Jiricny, and I. Stagljar. 2001. Direct association of Bloom's syndrome gene product with the human mismatch repair protein MLH1. Nucleic Acids Res. 29:4378-4386.
36. Peng, M., R. Litman, J. Xie, S. Sharma, R. M. Brosh, Jr., and S. B. Cantor. 2007. The FANCJ/MutLα interaction is required for correction of the crosslink response in FA-J. cells. EMBO J. 26:3238-3249.
37. Plotz, G., C. Welsch, L. Giron-Monzon, P. Friedhoff, M. Albrecht, A. Piiper, R. M. Biondi, T. Lengauer, S. Zeuzem, and J. Raedle. 2006. Mutations in the MutSa interaction interface of MLH1 can abolish DNA mismatch repair. Nucleic Acids Res. 34:6574-6586.
38. Rasmussen, L. J., M. Rasmussen, B. Lee, A. K. Rasmussen, D. M. Wilson III, F. C. Nielsen, and H. C. Bisgaard. 2000. Identification of factors interacting with hMSH2 in the fetal liver utilizing the yeast two-hybrid system. In vivo interaction through the C-terminal domains of hEXO1 and hMSH2 and comparative expression analysis. Mutat. Res. 460:41-52.
39. Resnick, M. A., J. C. Game, and S. Stasiewicz. 1983. Genetic effects of UV irradiation on excision-proficient and -deficient yeast during meiosis. Genetics 104:603-618.
40. Schmutte, C., R. C. Marinescu, M. M. Sadoff, S. Guerrette, J. Overhauser, and R. Fishel. 1998. Human exonuclease I interacts with the mismatch repair protein hMSH2. Cancer Res. 58:4537-4542.
41. Schmutte, C., M. M. Sadoff, K. S. Shim, S. Acharya, and R. Fishel. 2001. The interaction of DNA mismatch repair proteins with human exonuclease I. J. Biol. Chem. 276:33011-33018.
42. Schuster-Bockler, B., J. Schultz, and S. Rahmann. 2004. HMM Logos for visualization of protein families. BMC Bioinform. 5:7.
43. Shcherbakova, P. V., M. C. Hall, M. S. Lewis, S. E. Bennett, K. J. Martin, P. R. Bushel, C. A. Afshari, and T. A. Kunkel. 2001. Inactivation of DNA mismatch repair by increased expression of yeast MLH1. Mol. Cell. Biol. 21:940-951.
44. Shcherbakova, P. V., and T. A. Kunkel. 1999. Mutator phenotypes conferred by MLH1 overexpression and by heterozygosity for mlh1 mutations. Mol. Cell. Biol. 19:3177-3183.
45. Sherman, F., and J. Hicks. 1991. Micromanipulation and dissection of asci. Methods Enzymol. 194:21-37.
46. Takahashi, M., H. Shimodaira, C. Andreutti-Zaugg, R. Iggo, R. D. Kolodner, and C. Ishioka. 2007. Functional analysis of human MLH1 variants using yeast and in vitro mismatch repair assays. Cancer Res. 67:4595-4604.
47. Tishkoff, D. X., A. L. Boerger, P. Bertrand, N. Filosi, G. M. Gaida, M. F. Kane, and R. D. Kolodner. 1997. Identification and characterization of Sacchawmyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc. Natl. Acad. Sci. USA 94:7487-7492.
48. Tran, H. T., D. A. Gordenin, and M. A. Resnick. 1999. The 3′ → 5′ exonucleases of DNA polymerases delta and epsilon and the 5′→ 3′ exonuclease Exo1 have maior roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol. Cell. Biol. 19:2000-2007.
49. Tran, P. T., J. P. Fey, N. Erdeniz, L. Gellon, S. Boiteux, and R. M. Liskay. 2007. A mutation in EXO1 defines separable roles in DNA mismatch repair and post-replication repair. DNA Repair 6:1572-1583.
50. Tran, P. T., and R. M. Liskay. 2000. Functional studies on the candidate ATPase domains of Saccharomyces cerevisiae MutLα. Mol. Cell. Biol. 20:6390-6398.
51. Tran, P. T., J. A. Simon, and R. M. Liskay. 2001. Interactions of Exo1p with components of MutLα in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 98:9760-9765.
52. Umar, A., A. B. Buermeyer, J. A. Simon, D. C. Thomas, A. B. Clark, R. M. Liskay, and T. A. Kunkel. 1996. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell 87:65-73.
53. Wang, T. F., N. Kleckner, and N. Hunter. 1999. Functional specificity of MutL homologs in yeast: evidence for three Mlh1-based heterocomplexes with distinct roles during meiosis in recombination and mismatch correction. Proc. Natl. Acad. Sci. USA 96:13914-13919.
54. Wei, K., A. B. Clark, E. Wong, M. F. Kane, D. J. Mazur, T. Parris, N. K. Kolas, R. Russell, H. Hou, Jr., B. Kneitz, G. Yang, T. A. Kunkel, R. D. Kolodner, P. E. Cohen, and W. Edelmann. 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.