Rad51 Paralogs Remodel Pre-synaptic Rad51 Filaments to Stimulate Homologous Recombination

Cell

Volumn 162, Issue 2, 2015, Pages 271-286

  Taylor, Martin R G ^a   Špírek, Mário ^b,c   Chaurasiya, Kathy R ^d   Ward, Jordan D ^a,e   Carzaniga, Raffaella ^a   Yu, Xiong ^f   Egelman, Edward H ^f   Collinson, Lucy M ^a   Rueda, David ^d   Krejčí, Lumir ^b,c   Boulton, Simon J ^a  

^a THE FRANCIS CRICK INSTITUTE   (United Kingdom)

^b MASARYK UNIVERSITY   (Czech Republic)

^c ST ANNE S UNIVERSITY HOSPITAL   (Czech Republic)

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e GENENTECH INC   (United States)

^f UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; BRCA2 PROTEIN; DOUBLE STRANDED DNA; HETERODIMER; RAD51 PROTEIN; RECEPTOR INTERACTING PROTEIN 1; RECOMBINANT PROTEIN; RFS 1 PROTEIN; SINGLE STRANDED DNA; UNCLASSIFIED DRUG; CAENORHABDITIS ELEGANS PROTEIN; CARRIER PROTEIN; DNA BINDING PROTEIN; NUCLEOPORIN; NUP42 PROTEIN, S CEREVISIAE; RAD-51 PROTEIN, C ELEGANS; RFS-1 PROTEIN, C ELEGANS; RIP-1 PROTEIN, C ELEGANS; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; CONFORMATIONAL TRANSITION; DNA PROTEIN COMPLEX; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVITY; GEL PERMEATION CHROMATOGRAPHY; HOMOLOGOUS RECOMBINATION; NONHUMAN; PARALOGY; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN PROTEIN INTERACTION; YEAST CELL; ANIMAL; CAENORHABDITIS ELEGANS; GENETICS; HEK293 CELL LINE; HUMAN; METABOLISM; MUTATION; SACCHAROMYCES CEREVISIAE;

ANIMALS; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; CARRIER PROTEINS; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; HEK293 CELLS; HOMOLOGOUS RECOMBINATION; HUMANS; MUTATION; NUCLEAR PORE COMPLEX PROTEINS; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84937217157     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.06.015     Document Type: Article

References (62)

1. E. Antony, E.J. Tomko, Q. Xiao, L. Krejci, T.M. Lohman, and T. Ellenberger Srs2 disassembles Rad51 filaments by a protein-protein interaction triggering ATP turnover and dissociation of Rad51 from DNA Mol. Cell 35 2009 105 115
2. S.J. Boulton, A. Gartner, J. Reboul, P. Vaglio, N. Dyson, D.E. Hill, and M. Vidal Combined functional genomic maps of the C. elegans DNA damage response Science 295 2002 127 131
3. R.C. Burgess, M. Lisby, V. Altmannova, L. Krejci, P. Sung, and R. Rothstein Localization of recombination proteins and Srs2 reveals anti-recombinase function in vivo J. Cell Biol. 185 2009 969 981
4. J.R. Chapman, M.R.G. Taylor, and S.J. Boulton Playing the end game: DNA double-strand break repair pathway choice Mol. Cell 47 2012 497 510
5. Z. Chen, H. Yang, and N.P. Pavletich Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures Nature 453 2008 489 494
6. J. Chun, E.S. Buechelmaier, and S.N. Powell Rad51 paralog complexes BCDX2 and CX3 act at different stages in the BRCA1-BRCA2-dependent homologous recombination pathway Mol. Cell. Biol. 33 2013 387 395
7. C. Danilowicz, A. Peacock-Villada, J. Vlassakis, A. Facon, E. Feinstein, N. Kleckner, and M. Prentiss The differential extension in dsDNA bound to Rad51 filaments may play important roles in homology recognition and strand exchange Nucleic Acids Res. 42 2014 526 533
8. A.L. Forget, and S.C. Kowalczykowski Single-molecule imaging of DNA pairing by RecA reveals a three-dimensional homology search Nature 482 2012 423 427
9. G.S. Fortin, and L.S. Symington Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes EMBO J. 21 2002 3160 3170
10. C.A. French, J.-Y. Masson, C.S. Griffin, P. O'Regan, S.C. West, and J. Thacker Role of mammalian RAD51L2 (RAD51C) in recombination and genetic stability J. Biol. Chem. 277 2002 19322 19330
11. C.A. French, C.E. Tambini, and J. Thacker Identification of functional domains in the RAD51L2 (RAD51C) protein and its requirement for gene conversion J. Biol. Chem. 278 2003 45445 45450
12. S.L. Gasior, A.K. Wong, Y. Kora, A. Shinohara, and D.K. Bishop Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes Genes Dev. 12 1998 2208 2221
13. B.C. Godthelp, W.W. Wiegant, A. van Duijn-Goedhart, O.D. Schärer, P.P.W. van Buul, R. Kanaar, and M.Z. Zdzienicka Mammalian Rad51C contributes to DNA cross-link resistance, sister chromatid cohesion and genomic stability Nucleic Acids Res. 30 2002 2172 2182
14. L. Golmard, V. Caux-Moncoutier, G. Davy, E. Al Ageeli, B. Poirot, C. Tirapo, D. Michaux, C. Barbaroux, C.D. d'Enghien, A. Nicolas, and et al. Germline mutation in the RAD51B gene confers predisposition to breast cancer BMC Cancer 13 2013 484
15. D.K. Gonda, and C.M. Radding By searching processively RecA protein pairs DNA molecules that share a limited stretch of homology Cell 34 1983 647 654
16. D.K. Gonda, and C.M. Radding The mechanism of the search for homology promoted by recA protein. Facilitated diffusion within nucleoprotein networks J. Biol. Chem. 261 1986 13087 13096
17. A.M. Gruver, K.A. Miller, C. Rajesh, P.G. Smiraldo, S. Kaliyaperumal, R. Balder, K.M. Stiles, J.S. Albala, and D.L. Pittman The ATPase motif in RAD51D is required for resistance to DNA interstrand crosslinking agents and interaction with RAD51C Mutagenesis 20 2005 433 440
18. S.L. Hays, A.A. Firmenich, and P. Berg Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins Proc. Natl. Acad. Sci. USA 92 1995 6925 6929
19. S.M. Honigberg, B.J. Rao, and C.M. Radding Ability of RecA protein to promote a search for rare sequences in duplex DNA Proc. Natl. Acad. Sci. USA 83 1986 9586 9590
20. N.G. Howlett, T. Taniguchi, S. Olson, B. Cox, Q. Waisfisz, C. De Die-Smulders, N. Persky, M. Grompe, H. Joenje, G. Pals, and et al. Biallelic inactivation of BRCA2 in Fanconi anemia Science 297 2002 606 609
21. R.B. Jensen, A. Carreira, and S.C. Kowalczykowski Purified human BRCA2 stimulates RAD51-mediated recombination Nature 467 2010 678 683
22. R.B. Jensen, A. Ozes, T. Kim, A. Estep, and S.C. Kowalczykowski BRCA2 is epistatic to the RAD51 paralogs in response to DNA damage DNA Repair (Amst.) 12 2013 306 311
23. A.D. Jeyasekharan, Y. Liu, H. Hattori, V. Pisupati, A.B. Jonsdottir, E. Rajendra, M. Lee, E. Sundaramoorthy, S. Schlachter, C.F. Kaminski, and et al. A cancer-associated BRCA2 mutation reveals masked nuclear export signals controlling localization Nat. Struct. Mol. Biol. 20 2013 1191 1198
24. R.D. Johnson, N. Liu, and M. Jasin Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination Nature 401 1999 397 399
25. L. Krejci, S. Van Komen, Y. Li, J. Villemain, M.S. Reddy, H. Klein, T. Ellenberger, and P. Sung DNA helicase Srs2 disrupts the Rad51 presynaptic filament Nature 423 2003 305 309
26. J.M. Lancaster, R. Wooster, J. Mangion, C.M. Phelan, C. Cochran, C. Gumbs, S. Seal, R. Barfoot, N. Collins, G. Bignell, and et al. BRCA2 mutations in primary breast and ovarian cancers Nat. Genet. 13 1996 238 240
27. Z. Lin, H. Kong, M. Nei, and H. Ma Origins and evolution of the recA/RAD51 gene family: evidence for ancient gene duplication and endosymbiotic gene transfer Proc. Natl. Acad. Sci. USA 103 2006 10328 10333
28. J. Liu, T. Doty, B. Gibson, and W.-D. Heyer Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA Nat. Struct. Mol. Biol. 17 2010 1260 1262
29. J. Liu, L. Renault, X. Veaute, F. Fabre, H. Stahlberg, and W.-D. Heyer Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation Nature 479 2011 245 248
30. T. Liu, L. Wan, Y. Wu, J. Chen, and J. Huang hSWS1·SWSAP1 is an evolutionarily conserved complex required for efficient homologous recombination repair J. Biol. Chem. 286 2011 41758 41766
31. C. Loveday, C. Turnbull, E. Ramsay, D. Hughes, E. Ruark, J.R. Frankum, G. Bowden, B. Kalmyrzaev, M. Warren-Perry, K. Snape Breast Cancer Susceptibility Collaboration (UK) Germline mutations in RAD51D confer susceptibility to ovarian cancer Nat. Genet. 43 2011 879 882
32. J.S. Martin, N. Winkelmann, M.I.R. Petalcorin, M.J. McIlwraith, and S.J. Boulton RAD-51-dependent and -independent roles of a Caenorhabditis elegans BRCA2-related protein during DNA double-strand break repair Mol. Cell. Biol. 25 2005 3127 3139
33. V. Martín, C. Chahwan, H. Gao, V. Blais, J. Wohlschlegel, J.R. Yates 3rd, C.H. McGowan, and P. Russell Sws1 is a conserved regulator of homologous recombination in eukaryotic cells EMBO J. 25 2006 2564 2574
34. J.Y. Masson, M.C. Tarsounas, A.Z. Stasiak, A. Stasiak, R. Shah, M.J. McIlwraith, F.E. Benson, and S.C. West Identification and purification of two distinct complexes containing the five RAD51 paralogs Genes Dev. 15 2001 3296 3307
35. A. Meindl, H. Hellebrand, C. Wiek, V. Erven, B. Wappenschmidt, D. Niederacher, M. Freund, P. Lichtner, L. Hartmann, H. Schaal, and et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene Nat. Genet. 42 2010 410 414
36. M.I.R. Petalcorin, J. Sandall, D.B. Wigley, and S.J. Boulton CeBRC-2 stimulates D-loop formation by RAD-51 and promotes DNA single-strand annealing J. Mol. Biol. 361 2006 231 242
37. M.I.R. Petalcorin, V.E. Galkin, X. Yu, E.H. Egelman, and S.J. Boulton Stabilization of RAD-51-DNA filaments via an interaction domain in Caenorhabditis elegans BRCA2 Proc. Natl. Acad. Sci. USA 104 2007 8299 8304
38. A.J. Pierce, R.D. Johnson, L.H. Thompson, and M. Jasin XRCC3 promotes homology-directed repair of DNA damage in mammalian cells Genes Dev. 13 1999 2633 2638
39. Z. Qi, S. Redding, J.Y. Lee, B. Gibb, Y. Kwon, H. Niu, W.A. Gaines, P. Sung, and E.C. Greene DNA sequence alignment by microhomology sampling during homologous recombination Cell 160 2015 856 869
40. N. Rahman, S. Seal, D. Thompson, P. Kelly, A. Renwick, A. Elliott, S. Reid, K. Spanova, R. Barfoot, T. Chagtai Breast Cancer Susceptibility Collaboration (UK) PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene Nat. Genet. 39 2007 165 167
41. A.J. Rattray, and L.S. Symington Multiple pathways for homologous recombination in Saccharomyces cerevisiae Genetics 139 1995 45 56
42. S. Reid, D. Schindler, H. Hanenberg, K. Barker, S. Hanks, R. Kalb, K. Neveling, P. Kelly, S. Seal, M. Freund, and et al. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer Nat. Genet. 39 2007 162 164
43. J. San Filippo, P. Sung, and H. Klein Mechanism of eukaryotic homologous recombination Annu. Rev. Biochem. 77 2008 229 257
44. H. Sasanuma, M.S. Tawaramoto, J.P. Lao, H. Hosaka, E. Sanda, M. Suzuki, E. Yamashita, N. Hunter, M. Shinohara, A. Nakagawa, and A. Shinohara A new protein complex promoting the assembly of Rad51 filaments Nat. Commun. 4 2013 1676
45. E. Shor, J. Weinstein, and R. Rothstein A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3 and CSM2: four genes involved in error-free DNA repair Genetics 169 2005 1275 1289
46. S. Sigurdsson, S. Van Komen, W. Bussen, D. Schild, J.S. Albala, and P. Sung Mediator function of the human Rad51B-Rad51C complex in Rad51/RPA-catalyzed DNA strand exchange Genes Dev. 15 2001 3308 3318
47. J.A. Solinger, K. Kiianitsa, and W.D. Heyer Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments Mol. Cell 10 2002 1175 1188
48. P. Sung Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase Genes Dev. 11 1997 1111 1121
49. M. Takata, M.S. Sasaki, E. Sonoda, T. Fukushima, C. Morrison, J.S. Albala, S.M. Swagemakers, R. Kanaar, L.H. Thompson, and S. Takeda The Rad51 paralog Rad51B promotes homologous recombinational repair Mol. Cell. Biol. 20 2000 6476 6482
50. M. Takata, M.S. Sasaki, S. Tachiiri, T. Fukushima, E. Sonoda, D. Schild, L.H. Thompson, and S. Takeda Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs Mol. Cell. Biol. 21 2001 2858 2866
51. Y. Tao, X. Li, Y. Liu, J. Ruan, S. Qi, L. Niu, and M. Teng Structural analysis of Shu proteins reveals a DNA binding role essential for resisting damage J. Biol. Chem. 287 2012 20231 20239
52. T. Thorslund, M.J. McIlwraith, S.A. Compton, S. Lekomtsev, M. Petronczki, J.D. Griffith, and S.C. West The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA Nat. Struct. Mol. Biol. 17 2010 1263 1265
53. S.S. Tsang, S.A. Chow, and C.M. Radding Networks of DNA and RecA protein are intermediates in homologous pairing Biochemistry 24 1985 3226 3232
54. F. Vaz, H. Hanenberg, B. Schuster, K. Barker, C. Wiek, V. Erven, K. Neveling, D. Endt, I. Kesterton, F. Autore, and et al. Mutation of the RAD51C gene in a Fanconi anemia-like disorder Nat. Genet. 42 2010 406 409
55. J.D. Ward, L.J. Barber, M.I. Petalcorin, J. Yanowitz, and S.J. Boulton Replication blocking lesions present a unique substrate for homologous recombination EMBO J. 26 2007 3384 3396
56. J.D. Ward, D.M. Muzzini, M.I.R. Petalcorin, E. Martinez-Perez, J.S. Martin, P. Plevani, G. Cassata, F. Marini, and S.J. Boulton Overlapping mechanisms promote postsynaptic RAD-51 filament disassembly during meiotic double-strand break repair Mol. Cell 37 2010 259 272
57. C. Wiese, J.M. Hinz, R.S. Tebbs, P.B. Nham, S.S. Urbin, D.W. Collins, L.H. Thompson, and D. Schild Disparate requirements for the Walker A and B ATPase motifs of human RAD51D in homologous recombination Nucleic Acids Res. 34 2006 2833 2843
58. R. Wooster, G. Bignell, J. Lancaster, S. Swift, S. Seal, J. Mangion, N. Collins, S. Gregory, C. Gumbs, and G. Micklem Identification of the breast cancer susceptibility gene BRCA2 Nature 378 1995 789 792
59. B. Xia, J.C. Dorsman, N. Ameziane, Y. de Vries, M.A. Rooimans, Q. Sheng, G. Pals, A. Errami, E. Gluckman, J. Llera, and et al. Fanconi anemia is associated with a defect in the BRCA2 partner PALB2 Nat. Genet. 39 2007 159 161
60. N.A. Yamada, J.M. Hinz, V.L. Kopf, K.D. Segalle, and L.H. Thompson XRCC3 ATPase activity is required for normal XRCC3-Rad51C complex dynamics and homologous recombination J. Biol. Chem. 279 2004 23250 23254
61. Y. Yonetani, H. Hochegger, E. Sonoda, S. Shinya, H. Yoshikawa, S. Takeda, and M. Yamazoe Differential and collaborative actions of Rad51 paralog proteins in cellular response to DNA damage Nucleic Acids Res. 33 2005 4544 4552
62. E.N. Zaitsev, and S.C. Kowalczykowski The simultaneous binding of two double-stranded DNA molecules by Escherichia coli RecA protein J. Mol. Biol. 287 1999 21 31