Protein dynamics during presynaptic-complex assembly on individual single-stranded DNA molecules

Nature Structural and Molecular Biology

Volumn 21, Issue 10, 2014, Pages 893-900

  Gibb, Bryan ^a   Ye, Ling F ^a   Kwon, Youngho ^b   Niu, Hengyao ^b   Sung, Patrick ^b   Greene, Eric C ^a  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

RAD51 PROTEIN; RAD52 PROTEIN; REPLICATION FACTOR A; SINGLE STRANDED DNA; PROTEIN BINDING; RAD51 PROTEIN, S CEREVISIAE; RAD52 PROTEIN, S CEREVISIAE; RFA1 PROTEIN, S CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; GENE CLUSTER; GENE REPRESSION; INTERSPERSED REPEAT; MOLECULAR DYNAMICS; NONHUMAN; PRESYNAPTIC COMPLEX; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DNA BINDING; PROTEIN DNA INTERACTION; PROTEIN FUNCTION; PROTEIN METABOLISM; REGULATORY DNA SEQUENCE; REGULATORY MECHANISM; SACCHAROMYCES CEREVISIAE; SPATIOTEMPORAL ANALYSIS; BINDING SITE; DOUBLE STRANDED DNA BREAK; GENETICS; HOMOLOGOUS RECOMBINATION; METABOLISM; RECOMBINATION REPAIR;

SACCHAROMYCES CEREVISIAE;

BINDING SITES; DNA BREAKS, DOUBLE-STRANDED; DNA, SINGLE-STRANDED; HOMOLOGOUS RECOMBINATION; PROTEIN BINDING; RAD51 RECOMBINASE; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATIONAL DNA REPAIR; REPLICATION PROTEIN A; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84919774962     PISSN: 15459993     EISSN: 15459985     Source Type: Journal    
DOI: 10.1038/nsmb.2886     Document Type: Article

References (61)

1. Mazon, G., Mimitou, E.P., Symington, L.S. SnapShot: homologous recombination in DNA double-strand break repair. Cell 142, 646, 646.e1 (2010).
2. San Filippo, J., Sung, P., Klein, H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 77, 229-257 (2008).
3. Krogh, B.O., Symington, L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38, 233-271 (2004).
4. Cromie, G.A., Connelly, J.C., Leach, D.R. Recombination at double-strand breaks and DNA ends: conserved mechanisms from phage to humans. Mol. Cell 8, 1163-1174 (2001).
5. Cejka, P. et al. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature 467, 112-116 (2010).
6. Chen, X. et al. The Fun30 nucleosome remodeller promotes resection of DNA double-strand break ends. Nature 489, 576-580 (2012).
7. Mimitou, E.P., Symington, L.S. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455, 770-774 (2008).
8. Niu, H. et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature 467, 108-111 (2010).
9. Zhu, Z., Chung, W.H., Shim, E.Y., Lee, S.E., Ira, G. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134, 981-994 (2008).
10. Wold, M.S. Replication protein A: a heterotrimeric, single-stranded DNA-binding protein required for eukaryotic DNA metabolism. Annu. Rev. Biochem. 66, 61-92 (1997).
11. Broderick, S., Rehmet, K., Concannon, C., Nasheuer, H.P. Eukaryotic single-stranded DNA binding proteins: central factors in genome stability. Subcell. Biochem. 50, 143-163 (2010).
12. Mimitou, E.P., Symington, L.S. DNA end resection:unraveling the tail. DNA Repair (Amst.) 10, 344-348 (2011).
13. Lisby, M., Rothstein, R. Choreography of recombination proteins during the DNA damage response. DNA Repair (Amst.) 8, 1068-1076 (2009).
14. Symington, L.S., Gautier, J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 45, 247-271 (2011).
15. Choi, J.H. et al. Reconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling. Proc. Natl. Acad. Sci. USA 107, 13660-13665 (2010).
16. Maréchal, A. et al. PRP19 Transforms into a sensor of RPA-ssDNA after DNA damage and drives ATR activation via a ubiquitin-mediated circuitry. Mol. Cell 53, 235-246 (2014).
17. Gasior, S.L., Wong, A.K., Kora, Y., Shinohara, A., Bishop, D.K. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 12, 2208-2221 (1998).
18. Hays, S.L., Firmenich, A.A., Massey, P., Banerjee, R., Berg, P. Studies of the interaction between Rad52 protein and the yeast single-stranded DNA binding protein RPA. Mol. Cell. Biol. 18, 4400-4406 (1998).
19. Oakley, G.G., Patrick, S.M. Replication protein A: directing traffic at the intersection of replication and repair. Front. Biosci. (Landmark Ed) 15, 883-900 (2010).
20. Plate, I. et al. Interaction with RPA is necessary for Rad52 repair center formation and for its mediator activity. J. Biol. Chem. 283, 29077-29085 (2008).
21. Conway, A.B. et al. Crystal structure of a Rad51 filament. Nat. Struct. Mol. Biol. 11, 791-796 (2004).
22. Ogawa, T., Yu, X., Shinohara, A., Egelman, E.H. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science 259, 1896-1899 (1993).
23. Heyer, W.D., Ehmsen, K.T., Liu, J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44, 113-139 (2010).
24. Symington, L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 66, 630-670 (2002).
25. West, S.C. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4, 435-445 (2003).
26. Bianco, P.R., Tracy, R.B., Kowalczykowski, S.C. DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci. 3, D570-D603 (1998).
27. Sung, P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272, 28194-28197 (1997).
28. Shinohara, A., Ogawa, T. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature 391, 404-407 (1998).
29. New, J.H., Sugiyama, T., Zaitseva, E., Kowalczykowski, S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature 391, 407-410 (1998).
30. Benson, F.E., Baumann, P., West, S.C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature 391, 401-404 (1998).
31. Lao, J.P., Oh, S.D., Shinohara, M., Shinohara, A., Hunter, N. Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol. Cell 29, 517-524 (2008).
32. McIlwraith, M.J., West, S.C. DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell 29, 510-516 (2008).
33. Nimonkar, A.V., Sica, R.A., Kowalczykowski, S.C. Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. Proc. Natl. Acad. Sci. USA 106, 3077-3082 (2009).
34. Sugiyama, T., Kantake, N., Wu, Y., Kowalczykowski, S.C. Rad52-mediated DNA annealing after Rad51-mediated DNA strand exchange promotes second ssDNA capture. EMBO J. 25, 5539-5548 (2006).
35. Lisby, M., Barlow, J.H., Burgess, R.C., Rothstein, R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118, 699-713 (2004).
36. Lisby, M., Rothstein, R., Mortensen, U.H. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98, 8276-8282 (2001).
37. Feng, Z. et al. Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl. Acad. Sci. USA 108, 686-691 (2011).
38. Jensen, R.B., Carreira, A., Kowalczykowski, S.C. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature 467, 678-683 (2010).
39. Gibb, B. et al. Concentration-dependent exchange of replication protein A on single-stranded DNA revealed by single-molecule imaging. PLoS ONE 9, e87922 (2014).
40. Deng, S.K., Gibb, B., de Almeida, M.J., Greene, E.C., Symington, L.S. RPA antagonizes microhomology-mediated repair of DNA double-strand breaks. Nat. Struct. Mol. Biol. 21, 405-412 (2014).
41. Gibb, B., Silverstein, T.D., Finkelstein, I.J., Greene, E.C. Single-stranded DNA curtains for real-time single-molecule visualization of protein-nucleic acid interactions. Anal. Chem. 84, 7607-7612 (2012).
42. Visnapuu, M.L., Fazio, T., Wind, S., Greene, E.C. Parallel arrays of geometric nanowells for assembling curtains of DNA with controlled lateral dispersion. Langmuir 24, 11293-11299 (2008).
43. Sugiyama, T., Kowalczykowski, S.C. Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 277, 31663-31672 (2002).
44. Sugiyama, T., Kantake, N. Dynamic regulatory interactions of Rad51, Rad52, and replication protein-A in recombination intermediates. J. Mol. Biol. 390, 45-55 (2009).
45. Sugiyama, T., New, J.H., Kowalczykowski, S.C. DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl. Acad. Sci. USA 95, 6049-6054 (1998).
46. Shinohara, A., Shinohara, M., Ohta, T., Matsuda, S., Ogawa, T. Rad52 forms ring structures and co-operates with RPA in single-strand DNA annealing. Genes Cells 3, 145-156 (1998).
47. 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. USA 99, 13492-13497 (2002).
48. Stasiak, A.Z. et al. The human Rad52 protein exists as a heptameric ring. Curr. Biol. 10, 337-340 (2000).
49. Graham, J.S., Johnson, R.C., Marko, J.F. Concentration-dependent exchange accelerates turnover of proteins bound to double-stranded DNA. Nucleic Acids Res. 39, 2249-2259 (2011).
50. Sing, C.E., Olvera de la Cruz, M., Marko, J.F. Multiple-binding-site mechanism explains concentration-dependent unbinding rates of DNA-binding proteins. Nucleic Acids Res. 42, 3783-3791 (2014).
51. Sung, P., Klein, H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 7, 739-750 (2006).
52. Wang, X., Haber, J.E. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLoS Biol. 2, E21 (2004).
53. Miyazaki, T., Bressan, D.A., Shinohara, M., Haber, J.E., Shinohara, A. In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. EMBO J. 23, 939-949 (2004).
54. Miné-Hattab, J., Rothstein, R. Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol. 14, 510-517 (2012).
55. Efron, B., Tibshirani, R. An Introduction to the Bootstrap (Champman and Hall, New York, 1993).
56. Antúnez de Mayolo, A. et al. Multiple start codons and phosphorylation result in discrete Rad52 protein species. Nucleic Acids Res. 34, 2587-2597 (2006).
57. Galletto, R., Amitani, I., Baskin, R.J., Kowalczykowski, S.C. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443, 875-878 (2006).
58. Krejci, L. et al. Interaction with Rad51 is indispensable for recombination mediator function of Rad52. J. Biol. Chem. 277, 40132-40141 (2002).
59. Busygina, V. et al. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 22, 786-795 (2008).
60. Kwon, Y., Zhao, W., Sung, P. Biochemical studies on human Rad51-mediated homologous recombination. Methods Mol. Biol. 745, 421-435 (2011).
61. Greene, E.C., Wind, S., Fazio, T., Gorman, J., Visnapuu, M.L. DNA curtains for high-throughput single-molecule optical imaging. Methods Enzymol. 472, 293-315 (2010).