There and back again: New single-molecule insights in the motion of DNA repair proteins

Current Opinion in Structural Biology

Volumn 23, Issue 1, 2013, Pages 154-160

  Spies, Maria ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; BRCA1 PROTEIN; BRCA2 PROTEIN; DOUBLE STRANDED DNA; POLYDEOXYRIBONUCLEOTIDE SYNTHASE; PROTEIN MSH2; PROTEIN MSH6; PROTEIN MUTS; RAD52 PROTEIN; RECA PROTEIN; SINGLE STRANDED DNA; SINGLE STRANDED DNA BINDING PROTEIN;

DNA BINDING; DNA DAMAGE; DNA MODIFICATION; DNA REPAIR; FLUORESCENCE MICROSCOPY; MISMATCH REPAIR; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN HYDROLYSIS; PROTEIN PHOSPHORYLATION; REVIEW;

DNA REPAIR; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; PROTEIN BINDING; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; REC A RECOMBINASES;

EID: 84873526052     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2012.11.008     Document Type: Review

References (60)

1. de Duve C. The onset of selection. Nature 2005, 433:581-582.
2. Kanaar R., Hoeijmakers J.H., van Gent D.C. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 1998, 8:483-489.
3. Kolodner R.D., Putnam C.D., Myung K. Maintenance of genome stability in Saccharomyces cerevisiae. Science 2002, 297:552-557.
4. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
5. Campisi J. Cancer, aging and cellular senescence. In Vivo 2000, 14:183-188.
6. Borges H.L., Linden R., Wang J.Y. DNA damage-induced cell death: lessons from the central nervous system. Cell Res. 2008, 18:17-26.
7. Lans H., Hoeijmakers J.H. Cell biology: ageing nucleus gets out of shape. Nature 2006, 440:32-34.
8. Joo C., Balci H., Ishitsuka Y., Buranachai C., Ha T. Advances in single-molecule fluorescence methods for molecular biology. Annu. Rev. Biochem. 2008, 77:51-76.
9. Hilario J., Kowalczykowski S.C. Visualizing protein-DNA interactions at the single-molecule level. Curr. Opin. Chem. Biol. 2010, 14:15-22.
10. van Oijen A.M. Single-molecule approaches to characterizing kinetics of biomolecular interactions. Curr. Opin. Biotechnol. 2011, 22:75-80.
11. Berg O.G., Winter R.B., von Hippel P.H. Diffusion-driven mechanisms of protein translocation on nucleic acids. 1. Models and theory. Biochemistry 1981, 20:6929-6948.
12. Winter R.B., Berg O.G., von Hippel P.H. Diffusion-driven mechanisms of protein translocation on nucleic acids. 3. The Escherichia coli lac repressor-operator interaction: kinetic measurements and conclusions. Biochemistry 1981, 20:6961-6977.
13. Gowers D.M., Halford S.E. Protein motion from non-specific to specific DNA by three-dimensional routes aided by supercoiling. EMBO J. 2003, 22:1410-1418.
14. Riggs A.D., Bourgeois S., Cohn M. The lac repressor-operator interaction. 3. Kinetic studies. J. Mol. Biol. 1970, 53:401-417.
15. Halford S.E., Szczelkun M.D. How to get from A to B: strategies for analysing protein motion on DNA. Eur. Biophys. J. 2002, 31:257-267.
16. Tafvizi A., Huang F., Leith J.S., Fersht A.R., Mirny L.A., van Oijen A.M. Tumor suppressor p53 slides on DNA with low friction and high stability. Biophys. J. 2008, 95:L01-L03.
17. Blainey P.C., Luo G., Kou S.C., Mangel W.F., Verdine G.L., Bagchi B., Xie X.S. Nonspecifically bound proteins spin while diffusing along DNA. Nat. Struct. Mol. Biol. 2009, 16:1224-1229.
18. Elf J., Li G.W., Xie X.S. Probing transcription factor dynamics at the single-molecule level in a living cell. Science 2007, 316:1191-1194.
19. Hammar P., Leroy P., Mahmutovic A., Marklund E.G., Berg O.G., Elf J. The lac repressor displays facilitated diffusion in living cells. Science 2012, 336:1595-1598.
20. Billen D. Spontaneous DNA damage and its significance for the "negligible dose" controversy in radiation protection. Radiat. Res. 1990, 124:242-245.
21. Ciccia A., Elledge S.J. The DNA damage response: making it safe to play with knives. Mol. Cell 2010, 40:179-204.
22. Lamers M.H., Perrakis A., Enzlin J.H., Winterwerp H.H., de Wind N., Sixma T.K. The crystal structure of DNA mismatch repair protein MutS binding to a G×T mismatch. Nature 2000, 407:711-717.
23. Obmolova G., Ban C., Hsieh P., Yang W. Crystal structures of mismatch repair protein MutS and its complex with a substrate DNA. Nature 2000, 407:703-710.
24. Warren J.J., Pohlhaus T.J., Changela A., Iyer R.R., Modrich P.L., Beese L.S. Structure of the human MutSalpha DNA lesion recognition complex. Mol. Cell 2007, 26:579-592.
25. 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 1999, 3:255-261.
26. Vale R.D. Switches, latches, and amplifiers: common themes of G proteins and molecular motors. J. Cell Biol. 1996, 135:291-302.
27. Goody R.S., Hofmann-Goody W. Exchange factors, effectors, GAPs and motor proteins: common thermodynamic and kinetic principles for different functions. Eur. Biophys. J. 2002, 31:268-274.
28. Allen D.J., Makhov A., Grilley M., Taylor J., Thresher R., Modrich P., Griffith J.D. MutS mediates heteroduplex loop formation by a translocation mechanism. EMBO J. 1997, 16:4467-4476.
29. Gorman J., Chowdhury A., Surtees J.A., Shimada J., Reichman D.R., Alani E., Greene E.C. Dynamic basis for one-dimensional DNA scanning by the mismatch repair complex Msh2-Msh6. Mol. Cell 2007, 28:359-370.
30. Gorman J., Plys A.J., Visnapuu M.-L., Alani E., Greene E.C. Visualizing one-dimensional diffusion of eukaryotic DNA repair factors along a chromatin lattice. Nat. Struct. Mol. Biol. 2010, 17:932-938.
31. Jeong C., Cho W.K., Song K.M., Cook C., Yoon T.Y., Ban C., Fishel R., Lee J.B. MutS switches between two fundamentally distinct clamps during mismatch repair. Nat. Struct. Mol. Biol. 2011, 18:379-385.
32. Cho W.K., Jeong C., Kim D., Chang M., Song K.M., Hanne J., Ban C., Fishel R., Lee J.B. ATP alters the diffusion mechanics of MutS on mismatched DNA. Structure 2012, 20:1264-1274.
33. Gorman J., Wang F., Redding S., Plys A.J., Fazio T., Wind S., Alani E.E., Greene E.C. Single-molecule imaging reveals target-search mechanisms during DNA mismatch repair. Proc. Natl. Acad. Sci. U. S. A. 2012.
34. Spies M., Ha T. Inching over hurdles: how DNA helicases move on crowded lattices. Cell Cycle 2010, 9:1742-1749.
35. Forties R.A., North J.A., Javaid S., Tabbaa O.P., Fishel R., Poirier M.G., Bundschuh R. A quantitative model of nucleosome dynamics. Nucleic Acids Res. 2011, 39:8306-8313.
36. Slutsky M., Mirny L.A. Kinetics of protein-DNA interaction: facilitated target location in sequence-dependent potential. Biophys. J. 2004, 87:4021-4035.
37. Qiu R., DeRocco V.C., Harris C., Sharma A., Hingorani M.M., Erie D.A., Weninger K.R. Large conformational changes in MutS during DNA scanning, mismatch recognition and repair signalling. EMBO J. 2012, 31:2528-2540.
38. Liu J., Heyer W.-D. Who's who in human recombination: BRCA2 and RAD52. Proc. Natl. Acad. Sci. U. S. A. 2011, 108:441-442.
39. Lok B.H., Powell S.N. Molecular pathways: understanding the role of Rad52 in homologous recombination for therapeutic advancement. Clin. Cancer Res. 2012.
40. Honda M., Okuno Y., Yoo J., Ha T., Spies M. Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding. EMBO J. 2011, 30:3368-3382.
41. Grimme J.M., Honda M., Wright R., Okuno Y., Rothenberg E., Mazin A.V., Ha T., Spies M. Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Nucleic Acids Res. 2010, 38:2917-2930.
42. Grimme J.M., Spies M. FRET-based assays to monitor DNA binding and annealing by Rad52 recombination mediator protein. Methods Mol. Biol. 2011, 745:463-483.
43. Rothenberg E., Grimme J.M., Spies M., Ha T. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:20274-20279.
44. Kagawa W., Kurumizaka H., Ishitani R., Fukai S., Nureki O., Shibata T., Yokoyama S. Crystal structure of the homologous-pairing domain from the human Rad52 recombinase in the undecameric form. Mol. Cell 2002, 10:359-371.
45. Singleton M.R., Wentzell L.M., Liu Y., West S.C., Wigley D.B. Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13492-13497.
46. Lloyd J.A., McGrew D.A., Knight K.L. Identification of residues important for DNA binding in the full-length human Rad52 protein. J. Mol. Biol. 2005, 345:239-249.
47. Stasiak A.Z., Larquet E., Stasiak A., Muller S., Engel A., Van Dyck E., West S.C., Egelman E.H. The human Rad52 protein exists as a heptameric ring. Curr. Biol. 2000, 10:337-340.
48. Li X., Heyer W.D. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 2008, 18:99-113.
49. Moynahan M.E., Jasin M. Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat. Rev. Mol. Cell Biol. 2010, 11:196-207.
50. Holthausen J.T., Wyman C., Kanaar R. Regulation of DNA strand exchange in homologous recombination. DNA Repair 2011, 9:1264-1272.
51. Forget A.L., Kowalczykowski S.C. Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol. 2010, 20:269-276.
52. Holthausen J.T., Wyman C., Kanaar R. Regulation of DNA strand exchange in homologous recombination. DNA Repair 2010, 9:1264-1272.
53. Forget A.L., Kowalczykowski S.C. Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search. Nature 2012, 482:423-427.
54. Ragunathan K., Joo C., Ha T. Real-time observation of strand exchange reaction with high spatiotemporal resolution. Structure 2011, 19:1064-1073.
55. Ragunathan K, Liu C, Ha T: RecA filament sliding on DNA facilitates homology search. eLife 2012, in press.
56. Comstock M.J., Ha T., Chemla Y.R. Ultrahigh-resolution optical trap with single-fluorophore sensitivity. Nat. Meth. 2011, 8:335-340.
57. Henzler-Wildman K.A., Thai V., Lei M., Ott M., Wolf-Watz M., Fenn T., Pozharski E., Wilson M.A., Petsko G.A., Karplus M., et al. Intrinsic motions along an enzymatic reaction trajectory. Nature 2007, 450:838-844.
58. Brunger A.T., Strop P., Vrljic M., Chu S., Weninger K.R. Three-dimensional molecular modeling with single molecule FRET. J. Struct. Biol. 2011, 173:497-505.
59. 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 2001, 7:1-12.
60. Chen Z., Yang H., Pavletich N.P. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 2008, 453:489-494.