Mismatch repair protein hMSH2-hMSH6 recognizes mismatches and forms sliding clamps within a D-loop recombination intermediate

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 3, 2014, Pages

  Honda, Masayoshi ^a   Okuno, Yusuke ^b,e   Hengel, Sarah R ^a   Martín López, Juana V ^c   Cook, Christopher P ^c,f   Amunugama, Ravindra ^c,g   Soukup, Randal J ^c   Subramanyam, Shyamal ^a,b   Fishel, Richard ^c,d   Spies, Maria ^a  

^a UNIVERSITY OF IOWA   (United States)

^b UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^c OHIO STATE UNIVERSITY   (United States)

^d OHIO STATE UNIVERSITY   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

^g HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Homeologous recombination; Homologous recombination; Mismatch dna repair; Single molecule; Total internal reflection fluorescence microscopy

Indexed keywords

ADENOSINE TRIPHOSPHATE DERIVATIVE; DOUBLE STRANDED DNA; HETERODUPLEX; MISMATCH REPAIR PROTEIN; PROTEIN HMSH 6; PROTEIN MSH2; REPLICATION FACTOR A; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BIOTIN; HETERODIMER; PROTEIN MSH6; RAD51 PROTEIN; SLIDING CLAMP PROTEIN; STREPTAVIDIN;

ARTICLE; BINDING AFFINITY; BINDING SITE; DISSOCIATION; DISSOCIATION CONSTANT; DNA BINDING; DNA RECOMBINATION; DNA STRAND; DNA SUPERCOILING; GEL MOBILITY SHIFT ASSAY; HUMAN; HYDROLYSIS; MISMATCH REPAIR; PRIORITY JOURNAL; ASSOCIATION RATE CONSTANT; BINDING KINETICS; BLEACHING; D LOOP RECOMBINATION; DNA EXTRACTION; DOWNSTREAM PROCESSING; EC50; HISTOGRAM; HOMOLOGOUS RECOMBINATION; INDEL MUTATION; PROTEIN CONFORMATION; SURFACE PLASMON RESONANCE;

HOMEOLOGOUS RECOMBINATION; HOMOLOGOUS RECOMBINATION; MISMATCH DNA REPAIR; SINGLE-MOLECULE; TOTAL INTERNAL REFLECTION FLUORESCENCE MICROSCOPY;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BASE PAIR MISMATCH; BIOTINYLATION; DNA; DNA MISMATCH REPAIR; DNA-BINDING PROTEINS; HUMANS; HYDROLYSIS; KINETICS; MUTS HOMOLOG 2 PROTEIN; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; REPLICATION PROTEIN A;

EID: 84892931767     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1312988111     Document Type: Article

References (66)

1. Modrich P, Lahue R (1996) Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem 65:101-133.
2. Petit MA, Dimpfl J, Radman M, Echols H (1991) Control of large chromosomal duplications in Escherichia coli by the mismatch repair system. Genetics 129(2):327-332.
3. Jiricny J (2006) The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7(5):335-346.
4. Peltomäki P (2003) Role of DNA mismatch repair defects in the pathogenesis of human cancer. J Clin Oncol 21(6):1174-1179.
5. Kolodner RD, Marsischky GT (1999) Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9(1):89-96.
6. Hombauer H, Campbell CS, Smith CE, Desai A, Kolodner RD (2011) Visualization of eukaryotic DNA mismatch repair reveals distinct recognition and repair intermediates. Cell 147(5):1040-1053.
7. Su SS, Lahue RS, Au KG, Modrich P (1988) Mispair specificity of methyl-directed DNA mismatch correction in vitro. J Biol Chem 263(14):6829-6835.
8. Iyer RR, Pluciennik A, Burdett V, Modrich PL (2006) DNA mismatch repair: Functions and mechanisms. Chem Rev 106(2):302-323.
9. Fishel R, Wilson T (1997) MutS homologs in mammalian cells. Curr Opin Genet Dev 7(1):105-113.
10. Gorbalenya AE, Koonin EV (1990) Superfamily of UvrA-related NTP-binding proteins. Implications for rational classification of recombination/repair systems. J Mol Biol 213(4):583-591.
11. Warren JJ, et al. (2007) Structure of the human MutSalpha DNA lesion recognition complex. Mol Cell 26(4):579-592.
12. Obmolova G, Ban C, Hsieh P, Yang W (2000) Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 407(6805):703-710.
13. Lamers MH, et al. (2000) The crystal structure of DNA mismatch repair protein MutS binding to a G x T mismatch. Nature 407(6805):711-717.
14. Jeong C, et al. (2011) MutS switches between two fundamentally distinct clamps during mismatch repair. Nat Struct Mol Biol 18(3):379-385.
15. Spies M (2013) There and back again: New single-molecule insights in the motion of DNA repair proteins. Curr Opin Struct Biol 23(1):154-160.
16. Qiu R, et al. (2012) Large conformational changes in MutS during DNA scanning, mismatch recognition and repair signalling. EMBO J 31(11):2528-2540.
17. Gorman J, et al. (2012) Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. Proc Natl Acad Sci USA 109(45):E3074-E3083.
18. Cho WK, et al. (2012) ATP alters the diffusion mechanics of MutS on mismatched DNA. Structure 20(7):1264-1274.
19. Gorman J, Plys AJ, Visnapuu ML, Alani E, Greene EC (2010) Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat Struct Mol Biol 17(8):932-938.
20. Gorman J, et al. (2007) Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol Cell 28(3):359-370.
21. Gradia S, et al. (1999) hMSH2-hMSH6 forms a hydrolysis-independent sliding clamp on mismatched DNA. Mol Cell 3(2):255-261.
22. Grilley M, Welsh KM, Su SS, Modrich P (1989) Isolation and characterization of the Escherichia coli mutL gene product. J Biol Chem 264(2):1000-1004.
23. Acharya S, Foster PL, Brooks P, Fishel R (2003) The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol Cell 12(1):233-246.
24. Kadyrov FA, et al. (2007) Saccharomyces cerevisiae MutLalpha is a mismatch repair endonuclease. J Biol Chem 282(51):37181-37190.
25. San Filippo J, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77:229-257.
26. Heyer WD (2007) Biochemistry of eukaryotic homologous recombination. Top Curr Genet 17:95-133.
27. Holliday R (1964) A mechanism for gene conversion in fungi. Genet Res 5:282-304.
28. Jones M, Wagner R, Radman M (1987) Mismatch repair and recombination in E. coli. Cell 50(4):621-626.
29. Rayssiguier C, Thaler DS, Radman M (1989) The barrier to recombination between Escherichia coli and Salmonella typhimurium is disrupted in mismatch-repair mutants. Nature 342(6248):396-401.
30. Sugawara N, Goldfarb T, Studamire B, Alani E, Haber JE (2004) Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc Natl Acad Sci USA 101(25):9315-9320.
31. Harfe BD, Jinks-Robertson S (2000) DNA mismatch repair and genetic instability. Annu Rev Genet 34:359-399.
32. Putnam CD, Hayes TK, Kolodner RD (2009) Specific pathways prevent duplicationmediated genome rearrangements. Nature 460(7258):984-989.
33. Worth L, Jr., Clark S, Radman M, Modrich P (1994) Mismatch repair proteins MutS and MutL inhibit RecA-catalyzed strand transfer between diverged DNAs. Proc Natl Acad Sci USA 91(8):3238-3241.
34. Tham KC, et al. (2013) Mismatch repair inhibits homeologous recombination via coordinated directional unwinding of trapped DNA structures. Mol Cell 51(3):326-337.
35. Acharya S, et al. (1996) hMSH2 forms specific mispair-binding complexes with hMSH3 and hMSH6. Proc Natl Acad Sci USA 93(24):13629-13634.
36. Drummond JT, Li GM, Longley MJ, Modrich P (1995) Isolation of an hMSH2-p160 heterodimer that restores DNA mismatch repair to tumor cells. Science 268(5219):1909-1912.
37. Mazurek A, Johnson CN, Germann MW, Fishel R (2009) Sequence context effect for hMSH2-hMSH6 mismatch-dependent activation. Proc Natl Acad Sci USA 106(11):4177-4182.
38. Gradia S, Acharya S, Fishel R (1997) The human mismatch recognition complex hMSH2-hMSH6 functions as a novel molecular switch. Cell 91(7):995-1005.
39. Fishel R (1998) Mismatch repair, molecular switches, and signal transduction. Genes Dev 12(14):2096-2101.
40. Kolodner RD (1995) Mismatch repair: Mechanisms and relationship to cancer susceptibility. Trends Biochem Sci 20(10):397-401.
41. Snowden T, Acharya S, Butz C, Berardini M, Fishel R (2004) hMSH4-hMSH5 recognizes Holliday Junctions and forms a meiosis-specific sliding clamp that embraces homologous chromosomes. Mol Cell 15(3):437-451.
42. Heinen CD, et al. (2011) Human MSH2(hMSH2) protein controls ATP processing by hMSH2-hMSH6. J Biol Chem 286 (46):40287-40295.
43. Selmane T, Schofield MJ, Nayak S, Du C, Hsieh P (2003) Formation of a DNA mismatch repair complex mediated by ATP. J Mol Biol 334(5):949-965.
44. Heo SD, Cho M, Ku JK, Ban C (2007) Steady-state ATPase activity of E. coli MutS modulated by its dissociation from heteroduplex DNA. Biochem Biophys Res Commun 364(2):264-269.
45. Wold MS (1997) Replication protein A: A heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu Rev Biochem 66:61-92.
46. Fan J, Pavletich NP (2012) Structure and conformational change of a replication protein A heterotrimer bound to ssDNA. Genes Dev 26(20):2337-2347.
47. Haghighat Jahromi A, Honda M, Zimmerman SC, Spies M (2013) Single-molecule study of the CUG repeat-MBNL1 interaction and its inhibition by small molecules. Nucleic Acids Res 41(13):6687-6697.
48. Gourse RL, Landick R (2012) CoSMoS unravels mysteries of transcription initiation. Cell 148(4):635-637.
49. Krejci L, Altmannova V, Spirek M, Zhao X (2012) Homologous recombination and its regulation. Nucleic Acids Res 40(13):5795-5818.
50. Holthausen JT, Wyman C, Kanaar R (2010) Regulation of DNA strand exchange in homologous recombination. DNA Repair (Amst) 9(12):1264-1272.
51. Shim KS, et al. (2006) Magnesium influences the discrimination and release of ADP by human RAD51. DNA Repair (Amst) 5(6):704-717.
52. Amunugama R, et al. (2012) RAD51 protein ATP cap regulates nucleoprotein filament stability. J Biol Chem 287(12):8724-8736.
53. Evans E, Alani E (2000) Roles for mismatch repair factors in regulating genetic recombination. Mol Cell Biol 20(21):7839-7844.
54. Vernole P, et al. (2011) Common fragile sites in colon cancer cell lines: Role of mismatch repair, RAD51 and poly (ADP-ribose) polymerase-1. Mutat Res 712(1-2):40-48.
55. Solinger JA, Kiianitsa K, Heyer WD (2002) Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol Cell 10(5):1175-1188.
56. Javaid S, et al. (2009) Nucleosome remodeling by hMSH2-hMSH6. Mol Cell 36(6):1086-1094.
57. Hopfner KP, et al. (2000) Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell 101(7):789-800.
58. Koroleva O, Makharashvili N, Courcelle CT, Courcelle J, Korolev S (2007) Structural conservation of RecF and Rad50: Implications for DNA recognition and RecF function. EMBO J 26(3):867-877.
59. Lee JH, Paull TT (2005) ATM activation by DNA double-strand breaks through the Mre11-Rad50-Nbs1 complex. Science 308(5721):551-554.
60. Myung K, Datta A, Chen C, Kolodner RD (2001) SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat Genet 27(1):113-116.
61. Spell RM, Jinks-Robertson S (2004) Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 168(4):1855-1865.
62. Evans E, Sugawara N, Haber JE, Alani E (2000) The Saccharomyces cerevisiae Msh2 mismatch repair protein localizes to recombination intermediates in vivo. Mol Cell 5(5):789-799.
63. Saydam N, et al. (2007) Physical and functional interactions between Werner syndrome helicase and mismatch-repair initiation factors. Nucleic Acids Res 35(17):5706-5716.
64. Pedrazzi G, et al. (2003) The Bloom's syndrome helicase interacts directly with the human DNA mismatch repair protein hMSH6. Biol Chem 384(8):1155-1164.
65. Peng M, et al. (2007) The FANCJ/MutLalpha interaction is required for correction of the cross-link response in FA-J cells. EMBO J 26(13):3238-3249.
66. Honda M, Okuno Y, Yoo J, Ha T, Spies M (2011) Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. EMBO J 30(16):3368-3382.