(CAG)n-hairpin DNA binds to Msh2-Msh3 and changes properties of mismatch recognition

Nature Structural and Molecular Biology

Volumn 12, Issue 8, 2005, Pages 663-670

  Owen, Barbara A L ^a   Yang, Zungyoon ^b   Lai, Maoyi ^a   Gajek, Maciez ^c   Badger II, John D ^a   Hayes, Jeffrey J ^b   Edelmann, Winfried ^d   Kucherlapati, Raju ^e   Wilson, Teresa M ^c   McMurray, Cynthia T ^a  

^a MAYO GRADUATE SCHOOL   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^c UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^e LABORATORY FOR MOLECULAR MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; DNA; PROTEIN MSH2; PROTEIN MSH3; TRINUCLEOTIDE; DNA BINDING PROTEIN; MSH2 PROTEIN, MOUSE; MSH3 PROTEIN, MOUSE; ONCOPROTEIN; PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; CONTROLLED STUDY; DNA STRUCTURE; ENZYME ACTIVITY; MISMATCH REPAIR; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; ANIMAL; BASE MISPAIRING; BASE PAIRING; BIOLOGICAL MODEL; COMPARATIVE STUDY; DNA REPAIR; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; MOLECULAR GENETICS; PROTEIN BINDING; TRANSGENIC MOUSE; TRINUCLEOTIDE REPEAT;

ANIMALIA;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; BASE PAIR MISMATCH; BASE PAIRING; BASE SEQUENCE; DNA; DNA REPAIR; DNA-BINDING PROTEINS; ELECTROPHORETIC MOBILITY SHIFT ASSAY; MICE; MICE, TRANSGENIC; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTS HOMOLOG 2 PROTEIN; PROTEIN BINDING; PROTEINS; PROTO-ONCOGENE PROTEINS; TRINUCLEOTIDE REPEAT EXPANSION;

EID: 25844468819     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb965     Document Type: Article

References (48)

1. Alani, E. The Saccharomyces cerevisiae Msh2 and Msh6 proteins form a complex that specifically binds to duplex oligonucleotides containing mismatched DNA base pairs. Mol. Cell. Biol. 16, 5604-5615 (1996).
2. Acharya, S. et al. hMSH2 forms specific mispair-binding complexes with hMsh3 and hMsh6. Proc. Natl. Acad. Sci. USA 93, 13629-13634 (1996).
3. Blackwell, L.J., Bjornson, K.P. & Modrich, P. DNA dependent activation of the hMutSalpha ATPase. J. Biol. Chem. 273, 32049-32054 (1998).
4. Modrich, P. & LaHue, R.S. Mismatch repair in replication fidelity, genetic recombination and cancer biology. Annu. Rev. Biochem. 65, 101-113 (1996).
5. Genschel, J., Littman, S.J., Drummond, J.T. & Modrich, P. Isolation of MutSβ from human cells and comparison of the mismatch repair specificities of MutSβ and Mutsα. J. Biol. Chem. 273, 19895-19901 (1998).
6. Johnson, R.E., Kowali, G.K., Prakash, L. & Prakash, S. Requirement of the yeast Msh3 and Msh6 genes for Msh2-dependent genomic stability. J. Biol. Chem. 271, 7285-7288 (1996).
7. Marsischky, G.T., Filosi, N., Kane, M.F. & Kolodner, R.D. Redundancy of Saccharomyces cerevisiae MSH3 and MSH6 in MSH2-dependent mismatch repair. Genes Dev. 10, 407-420 (1996).
8. Palombo, F. et al. hMurSbeta, a heterodimer of hMSH2 and hMSH3, binds to insertion/deletion loops in DNA. Curr. Biol. 6, 1181-1184 (1996).
9. Gradia, S. et al. hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol. Cell 3, 255-261 (1999).
10. Wilson, T., Guerrette, S. & Fishel, R. Dissociation of mismatch recognition and ATPase activity by hMSH2-MSH3. J. Biol. Chem. 274, 21659-21664 (1999).
11. Allen, D.J. et al. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 16, 4467-4476 (1997).
12. 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).
13. Gradia, S., Acharya, S. & Fishel, R. The role of mismatched oligonucleotides in activating the hMSH2-MSH6 molecular switch. J. Biol. Chem. 275, 3922-3930 (2000).
14. Martik, D., Baitinger, C. & Modrich, P. Differential specificities and simultaneous occupancy of human MutSα nucleotide binding. J. Biol. Chem. 279, 28402-28410 (2004).
15. van den Broek, W.J. et al. Somatic expansion behavior of the (CTG)n repeat in myotonic dystrophy knock-in mice is differentially affected by Msh3 and Msh6 mismatch-repair proteins. Hum. Mol. Genet. 11, 191-199 (2002).
16. Dufner, P., Marra, G., Raschle, M. & Jiricny, J. Mismatch recognition and DNA-dependent stimulation of the ATPase activity of hMutSα is abolished by a single mutation in the hMSH6 subunit. J. Biol. Chem. 275, 36550-36555 (2000).
17. Junop, M.S., Obmolova, G., Rausch, K., Hsieh, P. & Yang, W. Composite active site of an ABC ATPase: MutS uses ATP to verify mismatch recognition and authorize DNA repair. Mol. Cell 7, 1-12 (2001).
18. Drotschmann, K., Yang, W. & Kunkel, T.A. Evidence for sequential action of two ATPase active sites in yeast MSH2-MSH6. DNA Repair (Amst.) 1, 743-753 (2002).
19. Lamers, M.H., Winterwerp, H.H. & Sixma, T.K. The alternating ATPase domains of MutS control DNA mismatch repair. EMBO J. 22, 746-756 (2003).
20. Baitinger, C., Burdett, V. & Modrich, P. Hydrolytically deficient MutS E694A is defective in the MutL-dependent activation of MutH and in the mismatch-dependent assembly of the MutS.MutL.heteroduplex complex. J. Biol. Chem. 278, 49505-49511 (2003).
21. Selmane, T., Schofield, M.J., Nayak, S., Du, C. & Hsieh, P. Formation of a DNA mismatch repair complex mediated by ATP. J. Mol. Biol. 334, 949-965 (2003).
22. Bjornson, K.P. & Modrich, P. Differential and simultaneous adenosine di- and triphosphate binding by MutS. J. Biol. Chem. 278, 18557-18562 (2003).
23. Cummings, C.J. & Zoghbi, H.Y. Fourteen and counting; unraveling trinucleotide repeat diseases. Hum. Mol. Genet. 9, 909-916 (2000).
24. Lahue, R.S. & Slater, D.L. DNA repair and trinucleotide repeat instability. Front. Biosci. 8, s653-s666 (2003).
25. McMurray, C.T. DNA secondary structure: A common and causative factor for expansion in human disease. Proc. Natl. Acad. Sci. USA 96, 1823-1825 (1999).
26. Manley, K., Shirley, T.L., Flaherty, L. & Messer, A. MSH2 deficiency prevents in vivo somatic instability of the CAG repeat in Huntington disease transgenic mice. Nat. Genet. 23, 471-473 (1999).
27. Kovtun, I.V. & McMurray, C.T. Trinucleotide expansion in haploid germ cells by gap repair. Nat. Genet. 27, 407-411 (2001).
28. Seznec, H. et al. Transgenic mice carrying large human genomic sequences with expanded CTG repeat mimic closely the DM CTG repeat intergenerational and somatic instability. Hum. Mol. Genet. 9, 1185-1194 (2000).
29. Iyer, R.R. & Wells, R.D. Expansion and deletion of triplet repeat sequences in Escherichia coli occur on the leading strand of DNA replication. J. Biol. Chem. 274, 3865-3877 (1999).
30. Kang, S., Jaworski, A., Ohshima, K. & Wells, R.D. Expansion and deletion of CTG repeats from human disease genes are determined by the direction of replication in E. coli. Nat. Genet. 10, 213-218 (1995).
31. Miret, J.J., Pessoa-Brandao, L. & Lahue, R.S. Orientation-dependent and sequence-specific expansion of CTG/CAG trinucleotide repeats in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 95, 12438-12443 (1998).
32. Gacy, A.M., Goellner, G., Juranic, N., Macura, S. & McMurray, CT. Trinucleotide repeats that expand in human disease form hairpin structures in vitro. Cell 81, 533-540 (1995).
33. Freudenreich, C.H., Kantrow, S.M. & Zakian, V.A. Expansion and length- dependent fragility of CTG repeats in yeast. Science 279, 853-856 (1998).
34. Fortune, M.T., Vassilopoulos, C., Coolbaugh, M.I., Siciliano, M.J. & Monckton, D.G. Dramatic, expansion-biased, age-dependent, tissue-specific somatic mosaicism in a transgenic mouse model of triplet instability. Hum. Mol. Genet. 9, 439-445 (2000).
35. Chong, S.S. et al. Contribution of DNA sequence and CAG size to mutation frequencies of intermediate alleles for Huntington disease: evidence from single sperm analysis. Hum. Mol. Genet. 6, 301-309 (1997).
36. Freudenreich, C.H., Stavenhagen, J.B. & Zakian, V.A. Stability of a CTG/CAG trinucleotide repeat in yeast is dependent on its orientation in the genome. Mol. Cell. Biol. 17, 2090-2097 (1997).
37. Miret, J.J., Pessoa-Brandão, L. & Lahue, R.S. Instability of CAG and CTG trinucleotide repeats in Sacchammyces cerevesiae. Mol. Cell. Biol. 17, 3382-3387 (1997).
38. Moore, H., Greewell, P.W., Liu, C.-P., Arnheim, N. & Petes, T.D. Triplet repeats form secondary structures that escape DNA repair in yeast. Proc. Natl. Acad. Sci. USA 96, 1504-1509 (1999).
39. Pearson, C.E., Ewel, A., Acharya, S., Fishel, R.A. & Sinden, R.R. Human MSH2 binds to trinucleotide repeat DNA structures associated with neurodegenerative diseases. Hum. Mol. Genet. 6, 1117-1123 (1997).
40. Gacy, A.M. & McMurray, C.T. Influence of hairpins on template reannealing at trinucleotide repeat duplexes: a model for slipped DNA. Biochemistry 37, 9426-9434 (1998).
41. Acharya, S., Foster, P.L., Brooks, P. & Fishel, R. The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol. Cell 12, 233-246 (2003).
42. Dzantiev, L. et al. A defined human system that supports bidirectional mismatch-provoked excision. Mol. Cell 15, 31-41 (2004).
43. Zuker, M. Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res. 31, 3406-3415 (2003).
44. Goellner, G.M. et al. Different mechanisms underlie DNA instability in Huntington disease and colorectal cancer. Am. J. Hum. Genet. 60, 879-890 (1997).
45. Muller, A. & Fishel, R. Mismatch repair and the hereditary non-polyposis colorectal cancer syndrome (HNPCC). Cancer Invest. 20, 102-109 (2002).
46. Peltomaki, P. Deficient DNA mismatch repair: a common etiologic factor for colon cancer. Hum. Mol. Genet. 10, 735-740 (2001).
47. Mangiarini, L. et al. Exon 1 of the HD gene with an expanded CAG repeat is sufficient to cause a progressive neurological phenotype in transgenic mice. Cell 87, 493-506 (1996).
48. Owen, B.A.L., Sullivan, W.P., Felts, S.J. & Toft, D.O. Regulation of heat shock protein 90 ATPase activity by sequences in the carboxyl terminus. J. Biol. Chem. 277, 7086-7091 (2002).