Mechanism of 5′-directed excision in human mismatch repair

Molecular Cell

Volumn 12, Issue 5, 2003, Pages 1077-1086

  Genschel, Jochen ^a   Modrich, Paul ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL EXTRACT; DNA BINDING PROTEIN; PROTEIN; PROTEIN EXOI; PROTEIN MUTL ALPHA; PROTEIN MUTS ALPHA; UNCLASSIFIED DRUG; ADENOSINE TRIPHOSPHATASE; BACTERIAL PROTEIN; DNA; ESCHERICHIA COLI PROTEIN; EXO1 PROTEIN, HUMAN; EXODEOXYRIBONUCLEASE; EXODEOXYRIBONUCLEASE I; MUTL PROTEIN, E COLI; MUTS PROTEIN, E COLI; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MUTS; REPLICATION PROTEIN A; RPA1 PROTEIN, HUMAN;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; DNA STRAND BREAKAGE; EXCISION REPAIR; FEMALE; HELA CELL; HUMAN; HUMAN CELL; MISMATCH REPAIR; MOLECULAR DYNAMICS; NONHUMAN; PROTEIN FUNCTION; PURIFICATION; BASE MISPAIRING; CELL NUCLEUS; CHEMISTRY; DNA REPAIR; ENZYME ACTIVATION; GENETICS; METABOLISM;

ADENOSINE TRIPHOSPHATASES; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEINS; BASE PAIR MISMATCH; CELL NUCLEUS; DNA; DNA REPAIR; DNA REPAIR ENZYMES; DNA-BINDING PROTEINS; ENZYME ACTIVATION; ESCHERICHIA COLI PROTEINS; EXODEOXYRIBONUCLEASES; HELA CELLS; HUMANS; MUTS DNA MISMATCH-BINDING PROTEIN; REPLICATION PROTEIN A;

EID: 0345276522     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(03)00428-3     Document Type: Article

References (42)

1. Amin N.S., Nguyen M.N., Oh S., Kolodner R.D. exo1-dependent mutator mutations. model system for studying functional interactions in mismatch repair Mol. Cell. Biol. 21:2001;5142-5155.
2. Au K.G., Welsh K., Modrich P. Initiation of methyl-directed mismatch repair. J. Biol. Chem. 267:1992;12142-12148.
3. Blackwell L.J., Martik D., Bjornson K.P., Bjornson E.S., Modrich P. Nucleotide-promoted release of hMutSα from heteroduplex DNA is consistent with an ATP-dependent translocation mechanism. J. Biol. Chem. 273:1998;32055-32062.
4. Blackwell L.J., Wang S., Modrich P. DNA chain length dependence of formation and dynamics of hMutSα•hMutLα•heteroduplex complexes. J. Biol. Chem. 276:2001;33233-33240.
5. Buermeyer A.B., Deschenes S.M., Baker S.M., Liskay R.M. Mammalian DNA mismatch repair. Annu. Rev. Genet. 33:1999;533-564.
6. Cooper D.L., Lahue R.S., Modrich P. Methyl-directed mismatch repair is bidirectional. J. Biol. Chem. 268:1993;11823-11829.
7. Dao V., Modrich P. Mismatch, MutS, MutL, and helicase II-dependent unwinding from the single-strand break of an incised heteroduplex. J. Biol. Chem. 273:1998;9202-9207.
8. Drummond J.T., Li G.-M., Longley M.J., Modrich P. Isolation of an hMSH2•p160 heterodimer that restores mismatch repair to tumor cells. Science. 268:1995;1909-1912.
9. Drummond J.T., Anthoney A., Brown R., Modrich P. Cisplatin and adriamycin resistance are associated with MutLα and mismatch repair deficiency in an ovarian tumor cell line. J. Biol. Chem. 271:1996;19645-19648.
10. Ellis L.A., Taylor G.R., Baumberg S. MutS binding protects heteroduplex DNA from exonuclease digestion in vitro. a simple method for detecting mutations Nucleic Acids Res. 22:1994;2710-2711.
11. Fang W.-h., Modrich P. Human strand-specific mismatch repair occurs by a bidirectional mechanism similar to that of the bacterial reaction. J. Biol. Chem. 268:1993;11838-11844.
12. Genschel J., Bazemore L.R., Modrich P. Human exonuclease I is required for 5′ and 3′ mismatch repair. J. Biol. Chem. 277:2002;13302-13311.
13. Gradia S., Subramanian D., Wilson T., Acharya S., Makhov A., Griffith J., Fishel R. hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol. Cell. 3:1999;255-261.
14. Harfe B.D., Jinks-Robertson S. DNA mismatch repair and genetic instability. Annu. Rev. Genet. 34:2000;359-399.
15. Henricksen L.A., Umbricht C.B., Wold M.S. Recombinant replication protein A. expression, complex formation, and functional characterization J. Biol. Chem. 269:1994;11121-11132.
16. Herman J.G., Umar A., Polyak K., Graff J.R., Ahuja N., Issa J.P., Markowitz S., Willson J.K., Hamilton S.R., Kinzler K.W., et al. Incidence and functional consequences of hMLH1 promoter hypermethylation in colorectal carcinoma. Proc. Natl. Acad. Sci. USA. 95:1998;6870-6875.
17. Jager A.C., Rasmussen M., Bisgaard H.C., Singh K.K., Nielsen F.C., Rasmussen L.J. HNPCC mutations in the human DNA mismatch repair gene hMLH1 influence assembly of hMutLalpha and hMLH1-hEXO1 complexes. Oncogene. 20:2001;3590-3595.
18. Jagmohan-Changur S., Poikonen T., Vilkki S., Launonen V., Wikman F., Orntoft T.F., Moller P., Vasen H., Tops C., Kolodner R.D., et al. EXO1 variants occur commonly in normal population. evidence against a role in hereditary nonpolyposis colorectal cancer Cancer Res. 63:2003;154-158.
19. Jiricny J. Eukaryotic mismatch repair. an update Mutat. Res. 409:1998;107-121.
20. Kane M.F., Loda M., Gaida G.M., Lipman J., Mishra R., Goldman H., Jessup J.M., Kolodner R. 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. 57:1997;808-811.
21. Kolodner R. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev. 10:1996;1433-1442.
22. Li G.-M., Modrich P. Restoration of mismatch repair to nuclear extracts of H6 colorectal tumor cells by a heterodimer of human MutL homologs. Proc. Natl. Acad. Sci. USA. 92:1995;1950-1954.
23. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 65:1996;101-133.
24. Papadopoulos N., Nicolaides N.C., Wei Y.-F., Ruben S.M., Carter K.C., Rosen C.A., Haseltine W.A., Fleischmann R.D., Fraser C.M., Adams M.D., et al. Mutation of a mutL homolog in hereditary colon cancer. Science. 263:1994;1625-1629.
25. Ramilo C., Gu L., Guo S., Zhang X., Patrick S.M., Turchi J.J., Li G.M. Partial reconstitution of human DNA mismatch repair in vitro. characterization of the role of human replication protein A Mol. Cell. Biol. 22:2002;2037-2046.
26. Rasmussen L.J., Rasmussen M., Lee B., Rasmussen A.K., Wilson D.M., Nielsen F.C., Bisgaard H.C. 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. 460:2000;41-52.
27. Schmutte C., Marinescu R.C., Sadoff M.M., Guerrette S., Overhauser J., Fishel R. Human exonuclease I interacts with the mismatch repair protein hMSH2. Cancer Res. 58:1998;4537-4542.
28. Schmutte C., Sadoff M.M., Shim K.S., Acharya S., Fishel R. The interaction of DNA mismatch repair proteins with human exonuclease I. J. Biol. Chem. 276:2001;33011-33018.
29. Sokolsky T., Alani E. EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics. 155:2000;589-599.
30. Strathdee G., MacKean M.J., Illand M., Brown R. A role for methylation of the hMLH1 promoter in loss of hMLH1 expression and drug resistance in ovarian cancer. Oncogene. 18:1999;2335-2341.
31. Sun X., Zheng L., Shen B. Functional alterations of human exonuclease 1 mutants identified in atypical hereditary nonpolyposis colorectal cancer syndrome. Cancer Res. 62:2002;6026-6030.
32. Szankasi P., Smith G.R. A DNA exonuclease induced during meiosis of Schizosaccharomyces pombe. J. Biol. Chem. 267:1992;3014-3023.
33. Tishkoff D.X., Boerger A.L., Bertrand P., Filosi N., Gaida G.M., Kane M.F., Kolodner R.D. 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.
34. Tishkoff D.X., Amin N.S., Viars C.S., Arden K.C., Kolodner R.D. Identification of a human gene encoding a homologue of Saccharomyces cerevisiae EXO1, an exonuclease implicated in mismatch repair and recombination. Cancer Res. 58:1998;5027-5031.
35. Tran P.T., Simon J.A., Liskay R.M. Interactions of Exo1p with components of MutLalpha in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA. 98:2001;9760-9765.
36. Umar A., Buermeyer A.B., Simon J.A., Thomas D.C., Clark A.B., Liskay R.M., Kunkel T.A. Requirement for PCNA in DNA mismatch repair at a step preceding DNA resynthesis. Cell. 87:1996;65-73.
37. Veigl M.L., Kasturi L., Olechnowicz J., Ma A.H., Lutterbaugh J.D., Periyasamy S., Li G.M., Drummond J., Modrich P.L., Sedwick W.D., Markowitz S.D. Biallelic inactivation of hMLH1 by epigenetic gene silencing, a novel mechanism causing human MSI cancers. Proc. Natl. Acad. Sci. USA. 95:1998;8698-8702.
38. Viswanathan M., Burdett V., Baitinger C., Modrich P., Lovett S.T. Redundant exonuclease involvement in Escherichia coli methyl-directed mismatch repair. J. Biol. Chem. 276:2001;31053-31058.
39. Wang H., Hays J.B. 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.
40. Wei K., Clark A.B., Wong E., Kane M.F., Mazur D.J., Parris T., Kolas N.K., Russell R., Hou H. Jr., Kneitz B., et al. Inactivation of exonuclease 1 in mice results in DNA mismatch repair defects, increased cancer susceptibility, and male and female sterility. Genes Dev. 17:2003;603-614.
41. Wilson D.M. III, Carney J.P., Coleman M.A., Adamson A.W., Christensen M., Lamerdin J.E. Hex1. a new human Rad2 nuclease family member with homology to yeast exonuclease 1 Nucleic Acids Res. 26:1998;3762-3768.
42. Wu Y., Berends M.J., Post J.G., Mensink R.G., Verlind E., Van Der Sluis T., Kempinga C., Sijmons R.H., van der Zee A.G., Hollema H., et al. Germline mutations of EXO1 gene in patients with hereditary nonpolyposis colorectal cancer (HNPCC) and atypical HNPCC forms. Gastroenterology. 120:2001;1580-1587.