Saccharomyces cerevisiae Msh2p and Msh6p ATPase activities are both required during mismatch repair

Molecular and Cellular Biology

Volumn 18, Issue 12, 1998, Pages 7590-7601

  Studamire, Barbara ^a   Quach, Tony ^a   Alani, Eric ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE;

ARTICLE; BASE MISPAIRING; DNA REPAIR; ENZYME ACTIVITY; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 0031784272     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.12.7590     Document Type: Article

References (62)

1. Acharya, S., T. Wilson, S. Gradia, M. F. Kane, S. Guerrette, G. T. Marsischky, R. Kolodner, and R. Fishel. 1996. hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc. Natl. Acad. Sci. USA 93:13629-13634.
2. Alani, E. 1996. The Saccharomyces cerevisiae Msh2p and Msh6p form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs. Mol. Cell. Biol. 16:5604-5615.
3. Alani, E., N. W. Chi, and R. D. Kolodner. 1995. The Saccharomyces cerevisiae Msh2 protein specifically binds to duplex oligonucleotides containing mismatched DNA base pairs and loop insertions. Genes Dev. 9:234-247.
4. Alani, E., R. A. G. Reenan, and R. D. Kolodner. 1994. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics 137:19-39.
5. Alani, E., T. Sokolsky, B. Studamire, J. J. Miret, and R. S. Lahue. 1997. Genetic and biochemical analysis of Msh2p-Msh6p: role of ATP hydrolysis and Msh2p-Msh6p subunit interactions in mismatch base pair recognition. Mol. Cell. Biol. 17:2436-2447.
6. Allen, D. J., A. Makhov, M. Grilley, J. Taylor, R. Thresher, P. Modrich, and J. D. Griffith. 1997. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 16:4467-4476.
7. Au, K. G., K. Welsh, and P. Modrich. 1992. Initiation of methyl-directed mismatch repair. J. Biol. Chem. 267:12142-12148.
8. Bhattacharyya, G. K., and R. A. Johnson. 1977. Statistical concepts and methods. John Wiley & Sons, New York, N.Y.
9. Biswas, I., and P. Hsieh. 1996. Identification and characterization of a thermostable MutS homolog from Thermus aquaticus. J. Biol. Chem. 271: 5040-5048.
10. Bjornson, K. P., I. Wong, and T. M. Lohman. 1996. ATP hydrolysis stimulates binding and release of single stranded DNA from alternating subunits of the dimeric E. coli Rep helicase: implications for ATP-driven helicase translocation. J. Mol. Biol. 263:411-422.
11. Bjornson, K. P., J. Hsieh, M. Amaratunga, and T. M. Lohman. 1998. Kinetic mechanism for the sequential binding of two single-stranded oligodeoxynucleotides to the Escherichia coli Rep helicase dimer. Biochemistry 37:891-899.
12. Bowers, J., and E. Alani. Unpublished data.
13. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
14. Chi, N., and R. D. Kolodner. 1994. The effect of DNA mismatches on the ATPase activity of Msh1, a protein in yeast mitochondria that recognizes DNA mismatches. J. Biol. Chem. 269:29993-29997.
15. Christianson, T. W., R. S. Sikorski, M. Dante, J. H. Shero, and P. Hieter. 1992. Multifunctional yeast high-copy-number shuttle vectors. Gene 110: 119-122.
16. Crouse, G. F. 1996. Mismatch repair systems in Saccharomyces cerevisiae, p. 411-448. In J. Nickoloff and M. Hoekstra (ed.), DNA damage and repair -biochemistry, genetics and cell biology. Humana Press, Clifton, N.J.
17. Drotschmann, K., A. Aronshtam, H. J. Fritz, and M. G. Marinus. 1998. The E. coli MutL protein stimulates binding of VSR and MutS to heteroduplex DNA. Nucleic Acids Res. 26:948-953.
18. Drummond, J. T., G.-M. Li, M. J. Longley, and P. Modrich. 1995. Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268:1909-1912.
19. Geitz, R. D., and R. H. Schiestl. 1991. Applications of high efficiency lithium acetate transformation of intact yeast cells using single-stranded nucleic acids as carrier. Yeast 7:253-263.
20. Gradia, S., S. Acharya, and R. Fishel. 1997. The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 91:995-1005.
21. Grilley, M., K. M. Welsh, S.-S. Su, and P. Modrich. 1989. Isolation and characterization of the Escherichia coli mutL gene product. J. Biol. Chem. 264:1000-1004.
22. Gu, L., Y. Hong, S. McCulloch, H. Watanabe, and G. M. Li. 1998. ATP-dependent interaction of human mismatch repair proteins and dual role of PCNA in mismatch repair. Nucleic Acids Res. 26:1173-1178.
23. Haber, L. T., and G. C. Walker. 1991. Altering the conserved nucleotide binding motif in the Salmonella typhimurium MutS mismatch repair protein affects both its ATPase and mismatch binding activities. EMBO J. 10:2707-2715.
24. Habraken, Y., P. Sung, L. Prakash, and S. Prakash. 1996. Binding of insertion/deletion DNA mismatches by the heterodimer of yeast mismatch repair proteins MSH2 and MSH3. Curr. Biol. 6:1185-1187.
25. Habraken, Y., P. Sung, L. Prakash, and S. Prakash. 1997. Enhancement of MSH2-MSH3-mediated mismatch recognition by the yeast MLH1-PMS1 complex. Curr. Biol. 7:790-793.
26. Habraken, Y., P. Sung, L. Prakash, and S. Prakash. 1998. ATP-dependent assembly of a ternary complex consisting of a DNA mismatch and the yeast MSH2-MSH6 and MLH1-PMS1 protein complexes. J. Biol. Chem. 273: 9837-9841.
27. Harlow, E., and D. Lane. 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
28. Henderson, S. T., and T. D. Petes. 1992. Instability of simple sequence DNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 12:2749-2757.
29. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
30. Hughes, M. J., and J. Jiricny. 1992. The purification of a human mismatch-binding protein and identification of its associated ATPase and helicase activities. J. Biol. Chem. 267:23876-23882.
31. Iaccarino, I., G. Marra, F. Palombo, and J. Jiricny. 1998. hMSH2 and hMSH6 play distinct roles in mismatch binding and contribute differently to the ATPase activity of hMutSα. EMBO J. 17:2677-2686.
32. Iaccarino, I., F. Palombo, J. Drummond, N. F. Totty, J. J. Hsuan, P. Modrich, and J. Jiricny. 1996. MSH6, a Saccharomyces cerevisiae protein that binds to mismatches as a heterodimer with MSH2. Curr. Biol. 6:484-486.
33. Jiricny, J., S. Su, S. G. Wood, and P. Modrich. 1988. Mismatch-containing oligonucleotide duplexes bound by the E. coli mutS-encoded protein. Nucleic Acids Res. 16:7843-7853.
34. Johnson, R. E., G. K. Kovvali, L. Prakash, and S. Prakash. 1996. Requirement of the yeast MSH3 and MSH6 genes for MSH2 dependent genomic stability. J. Biol. Chem. 271:7285-7288.
35. Kolodner, R. 1996. Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev. 10:1433-1442.
36. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
37. Lahue, R. S., K. G. Au, and P. Modrich. 1989. DNA mismatch correction in a defined system. Science 245:160-164.
38. Maniatis, T., E. F. Fritsch, and J. Sambrook. 1982. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
39. Marsischky, G. T., N. Filosi, M. F. Kane, and R. Kolodner. 1996. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10:407-420.
40. McEntee, K., G. Weinstock, and I. R. Lehman. 1980. recA protein-catalyzed strand assimilation: stimulation by Escherichia coli single-stranded DNA-binding protein. Proc. Natl. Acad. Sci. USA 77:857-861.
41. Miller, J. 1972. Experiments in molecular genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
42. Modrich, P. 1997. Strand-specific mismatch repair in mammalian cells. J. Biol. Chem. 272:24727-24730.
43. Modrich, P., and R. S. Lahue. 1996. Mismatch repair in replication fidelity, genetic recombination and cancer biology. Annu. Rev. Biochem. 65:101-133.
44. Palombo, F., P. Gallinari, I. Iaccarino, T. Lettieri, M. Hughes, A. D'Arrigo, O. Truong, J. J. Hsuan, and J. Jiricny. 1995. GTBP, a 160 kD protein essential for mismatch binding activity in human cells. Science 268:1912-1914.
45. Palombo, F., I. Iaccarino, E. Nakajima, M. Ikejima, T. Shimada, and J. Jiricny. 1996. hMutSβ, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr. Biol. 6:1181-1184.
46. Parker, B. O., and M. G. Marinus. 1992. Repair of DNA heteroduplexes containing small heterologous sequences in Escherichia coli. Proc. Natl. Acad. Sci. USA 89:1730-1734.
47. Prolla, T. A., D. M. Christie, and R. M. Liskay. 1994. Dual requirement in yeast DNA mismatch repair for MLH1 and PMS1, two homologs of the bacterial mutL gene. Mol. Cell. Biol. 14:407-415.
48. Prolla, T. A., Q. Pang, E. Alani, R. D. Kolodner, and R. M. Liskay. 1994. MLH1, PMS1, and MSH2 interactions during the initiation of DNA mismatch repair in yeast. Science 265:1091-1093.
49. Reenan, R. A. G., and R. D. Kolodner. 1992. Characterization of insertion mutations in the Saccharomyces cerevisiae MSH1 and MSH2 genes: evidence for separate mitochondrial and nuclear functions. Genetics 132:975-985.
50. Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
51. Sancar, A., and J. E. Hearst. 1993. Molecular matchmakers. Science 259: 1415-1420.
52. Segel, I. H. 1976. Biochemical calculations. John Wiley & Sons, New York. N.Y.
53. Sokolsky, T., and E. Alani. Unpublished data.
54. Strand, M., M. C. Earley, G. F. Crouse, and T. D. Petes. 1995. Mutations in the MSH3 gene preferentially lead to deletions within tracts of simple repetitive DNA in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 92: 10418-10421.
55. Studamire, B., and E. Alani. Unpublished data.
56. Su, S.-S., R. S. Lahue, K. G. Au, and P. Modrich. 1988. Mispair specificity of methyl-directed DNA mismatch correction in vitro. J. Biol. Chem. 263:6829-6835.
57. Su, S.-S., and P. Modrich. 1986. Escherichia coli mutS-encoded protein binds to mismatched DNA base pairs. Proc. Natl. Acad. Sci. USA 83:5057-5061.
58. Sung, P., D. Higgins, L. Prakash, and S. Prakash. 1988. Mutation of lysine-48 to arginine in the yeast RAD3 protein abolishes its ATPase and DNA helicase activities but not the ability to bind ATP. EMBO J. 7:3263-3269.
59. Tipton, K. F. 1992. Principles of enzyme assay and kinetic studies, p. 1-58. In R. Eisenthal and M. J. Danson (ed.), Enzyme assays: a practical approach. Oxford University Press, Oxford, England.
60. Welsh, K. M., A.-L. Lu, S. Clark, and P. Modrich. 1987. Isolation and characterization of the Escherichia coli mutH gene product. J. Biol. Chem. 262:15624-15629.
61. Winston, F., C. Dollard, and S. L. Ricupero-Hovasse. 1995. Construction of a set of convenient Saccharomyces cerevisiae strains that are isogenic to S288C. Yeast 11:53-55.
62. Wu, T.-H., and M. G. Marinus. 1994. Dominant negative mutator mutations in the mutS gene of Escherichia coli. J. Bacteriol. 176:5393-5400.