The nucleotide binding dynamics of human MSH2-MSH3 are lesion dependent

Nature Structural and Molecular Biology

Volumn 16, Issue 5, 2009, Pages 550-557

  Owen, Barbara A L ^a,b   H Lang, Walter ^c   McMurray, Cynthia T ^a,b,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b MAYO CLINIC   (United States)

^c LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; PROTEIN MSH2; PROTEIN MSH3; PROTEIN MSH6; DNA; DNA BINDING PROTEIN; MSH2 PROTEIN, HUMAN; MSH3 PROTEIN, HUMAN; NUCLEOTIDE; PROTEIN SUBUNIT;

ANISOTROPY; ARTICLE; DNA BINDING; HYDROLYSIS; MISMATCH REPAIR; PRIORITY JOURNAL; PROTEIN PURIFICATION; CHEMICAL STRUCTURE; DNA DAMAGE; HUMAN; METABOLISM; PROTEIN BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SACCHAROMYCES CEREVISIAE; SOLUTION AND SOLUBILITY; STATISTICS;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DNA; DNA DAMAGE; DNA-BINDING PROTEINS; HUMANS; HYDROLYSIS; MODELS, MOLECULAR; MUTS HOMOLOG 2 PROTEIN; NUCLEOTIDES; PROTEIN BINDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; PROTEIN SUBUNITS; SACCHAROMYCES CEREVISIAE; SOLUTIONS; STOCHASTIC PROCESSES;

EID: 66149115286     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.1596     Document Type: Article

References (32)

1. Iyer, R.R., Pluciennik, A., Burdett, V. & Modrich, P.L. DNA mismatch repair: functions and mechanisms. Chem. Rev. 106, 302-323 (2006).
2. Kunkel, T.A. & Erie, D.A. DNA mismatch repair. Annu. Rev. Biochem. 74, 681-710 (2005).
3. Schofield, M.J. & Hsieh, P. DNA mismatch repair: molecular mechanisms and biological function. Annu. Rev. Microbiol. 57, 579-608 (2003).
4. Surtees, J.A. & Alani, E. Mismatch repair factor Msh2/Msh3 binds and alters the conformation of branched DNA structures predicted to form during genetic recombination. J. Mol. Biol. 360, 523-536 (2006).
5. Kovtun, I.V. & McMurray, C.T. Crosstalk of DNA glycosylases with pathways other than base excision repair. DNA Repair (Amst.) 6, 517-529 (2007).
6. Fishel, R. The selection for mismatch repair defects in hereditary nonpolyposis colorectal cancer: revising the mutator hypothesis. Cancer Res. 61, 7369-7374 (2001).
7. Peltomaki, P. Deficient DNA mismatch repair: a common etiologic factor for colon cancer. Hum. Mol. Genet. 10, 735-740 (2001).
8. Wei, K., Kucherlapati, R. & Edelmann, W. Mouse models for human DNA mismatch-repair gene defects. Trends Mol. Med. 8, 346-353 (2002).
9. Obmolova, G., Ban, C, Hsieh, P. & Yang, W. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407, 703-710 (2000).
10. Lamers, M.H. et al. The crystal structure of DNA mismatch repair protein MutS binding to a G × T mismatch. Nature 407, 711-717 (2000).
11. Warren, J.J. et al. Structure of the human MutSα DNA lesion recognition complex. Mol. Cell 26, 579-592 (2007).
12. Alani, E. et al. Crystal structure and biochemical analysis of the MutS-ADP-beryllium fluoride complex suggest a conserved mechanism for ATP interactions in mismatch repair. J. Biol. Chem. 278, 16088-16094 (2003).
13. Yamamoto, A., Schofield, M.J., Biswas, I. & Hsieh, P. Requirement for Phe36 for DNA binding and mismatch repair by Escherichia coli MutS protein. Nucleic Acids Res 28, 3564-3569 (2000).
14. Blackwell, L.J., Bjornson, K.P., Allen, D.J. & Modrich, P. Distinct MutS DNA-binding modes that are differentially modulated by ATP binding and hydrolysis. J. Biol. Chem. 276, 34339-34347 (2001).
15. Iaccarino, I., Marra, G., Palombo, F. & Jiricny, J. hMsh2 and hMsh6 play distinct roles in mismatch binding and contribute differently to the ATPase activity of hMutSα. EMBO J. 17, 2677-2686 (1998).
16. Gradia, S. et al. hMsh2/Msh6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol. Cell 3, 255-261 (1999).
17. Mendillo, M.L., Mazur, D.J. & Kolodner, R.D. Analysis of the interaction between the Saccharomyces cervisiae Msh2/Msh6 and MLH1-PMS1 complexes with DNA using a reversible DNA end-blocking system. J. Biol. Chem. 280, 22245-22257 (2005).
18. Mazur, D.J., Mendillo, M.L. & Kolodner, R.D. Inhibition of Msh6 ATPase activity by mispaired DNA induces a Msh2(ATP)-Msh6(ATP) state capable of hydrolysis-independent movement along DNA. Mol. Cell 22, 39-49 (2006).
19. Acharya, S. et al. hMsh2 forms specific mispair-binding complexes with hMsh3 and hMsh6. Proc. Natl. Acad. Sci. USA 93, 13629-13634 (1996).
20. Gradia, S., Acharya, S. & Fishel, R. The role of mismatched nucleotides in activating the hMsh2-hMsh6 molecular switch. J. Biol. Chem. 275, 3922-3930 (2000).
21. Marsischky, G.T. & Kolodner, R.D. Biochemical characterization of the interaction between the Saccharomyces cerevisiae Msh2/Msh6 complex and mispaired bases in DNA. J. Biol. Chem. 274, 26668-26682 (1999).
22. Harrington, J.M. & Kolodner, R.D. Saccharomyces cerevisiae Msh2/Msh3 acts in repair of base-base mispairs. Mol. Cell. Biol. 27, 6546-6554 (2007).
23. Wilson, T., Guerrette, S. & Fishel, R. Dissociation of mismatch recognition and ATPase activity by hMsh2-hMsh3. J. Biol. Chem. 274, 21659-21664 (1999).
24. Palombo, F et al. hMutSβ, a heterodimer of hMsh2 and hMsh3, binds to insertion/ deletion loops in DNA. Curr. Biol. 6, 1181-1184 (1996).
25. Shell, S.S., Putnam, CD. & Kolodner, R.D. Chimeric Saccharomyces cerevisiae Msh6 protein with an Msh3 mispair-binding domain combines properties of both proteins. Proc. Natl. Acad. Sci. USA 104, 10956-10961 (2007).
26. Lee, S.D., Surtees, J.A. & Alani, E. Saccharomyces cerevisiae Msh2/Msh3 and Msh2/Msh6 complexes display distinct requirements for DNA binding domain I in mismatch recognition. J. Mol. Biol. 366, 53-66 (2007).
27. Martik, D., Baitinger, C. & Modrich, P. Differential specificities and simultaneous occupancy of human MutSa nucleotide binding sites. J. Biol. Chem. 279, 28402-28410 (2004).
28. Lamers, M.H., Winterwerp, H.H.K. & Sixma, T.K. The alternating ATPase domains of MutS control DNA mismatch repair. EMBO J. 22, 746-756 (2003).
29. Bjornson, K.P. & Modrich, P. Differential and simultaneous adenosine di- and triphosphate binding by MutS. J. Biol. Chem. 278, 18557-18562 (2003).
30. n-hairpin DNA binds to Msh2/Msh3 and changes properties of mismatch recognition. Nat. Struct. Mol. Biol. 12, 663-670 (2005).
31. n be used as an indicator of cell viability, necrosis and apoptosis. J. Immunol. Methods 240, 79-92 (2000).
32. Junop, M.S., Obmolova, G., Rausch, K., Hsieh, P. & Yang, W. Composite active site of an ABC ATPaseMutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol. Cell 7, 1-12 (2001).