Homologous recombination and its regulation
Jazyk angličtina Země Anglie, Velká Británie Médium print-electronic
Typ dokumentu časopisecké články, Research Support, N.I.H., Extramural, práce podpořená grantem, přehledy
Grantová podpora
R01 GM080670
NIGMS NIH HHS - United States
GM080670
NIGMS NIH HHS - United States
PubMed
22467216
PubMed Central
PMC3401455
DOI
10.1093/nar/gks270
PII: gks270
Knihovny.cz E-zdroje
- MeSH
- homologní rekombinace * MeSH
- lidé MeSH
- meióza MeSH
- nádory diagnóza terapie MeSH
- nemoc genetika MeSH
- posttranslační úpravy proteinů MeSH
- rekombinasa Rad51 metabolismus MeSH
- replikační protein A metabolismus MeSH
- zvířata MeSH
- Check Tag
- lidé MeSH
- zvířata MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- přehledy MeSH
- Research Support, N.I.H., Extramural MeSH
- Názvy látek
- rekombinasa Rad51 MeSH
- replikační protein A MeSH
Homologous recombination (HR) is critical both for repairing DNA lesions in mitosis and for chromosomal pairing and exchange during meiosis. However, some forms of HR can also lead to undesirable DNA rearrangements. Multiple regulatory mechanisms have evolved to ensure that HR takes place at the right time, place and manner. Several of these impinge on the control of Rad51 nucleofilaments that play a central role in HR. Some factors promote the formation of these structures while others lead to their disassembly or the use of alternative repair pathways. In this article, we review these mechanisms in both mitotic and meiotic environments and in different eukaryotic taxa, with an emphasis on yeast and mammal systems. Since mutations in several proteins that regulate Rad51 nucleofilaments are associated with cancer and cancer-prone syndromes, we discuss how understanding their functions can lead to the development of better tools for cancer diagnosis and therapy.
Zobrazit více v PubMed
Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461:1071–1078. PubMed PMC
Paques F, Haber JE. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 1999;63:349–404. PubMed PMC
Sung P, Krejci L, Van Komen S, Sehorn MG. Rad51 recombinase and recombination mediators. J. Biol. Chem. 2003;278:42729–42732. PubMed
Ogawa T, Yu X, Shinohara A, Egelman EH. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 1993;259:1896–1899. PubMed
Chen Z, Yang H, Pavletich NP. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature. 2008;453:489–484. PubMed
Klapstein K, Chou T, Bruinsma R. Physics of RecA-mediated homologous recognition. Biophys. J. 2004;87:1466–1477. PubMed PMC
Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. The double-strand-break repair model for recombination. Cell. 1983;33:25–35. PubMed
Krogh BO, Symington LS. Recombination proteins in yeast. Annu. Rev. Genet. 2004;38:233–271. PubMed
Nassif N, Penney J, Pal S, Engels WR, Gloor GB. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 1994;14:1613–1625. PubMed PMC
Allers T, Lichten M. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell. 2001;106:47–57. PubMed
Hunter N, Kleckner N. The single-end invasion: an asymmetric intermediate at the double-strand break to double-holliday junction transition of meiotic recombination. Cell. 2001;106:59–70. PubMed
Malkova A, Ivanov EL, Haber JE. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl Acad. Sci. USA. 1996;93:7131–7136. PubMed PMC
Lin FL, Sperle K, Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol. Cell. Biol. 1984;4:1020–1034. PubMed PMC
Heyer WD, Ehmsen KT, Liu J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010;44:113–139. PubMed PMC
San Filippo J, Sung P, Klein H. Mechanism of eukaryotic homologous recombination. Annu. Rev. Biochem. 2008;77:229–257. PubMed
Sung P, Klein H. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat. Rev. Mol. Cell Biol. 2006;7:739–750. PubMed
Sugiyama T, Zaitseva EM, Kowalczykowski SC. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 1997;272:7940–7945. PubMed
Sung P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 1997;272:28194–28197. PubMed
Gasior SL, Wong AK, Kora Y, Shinohara A, Bishop DK. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 1998;12:2208–2221. PubMed PMC
Lisby M, Barlow JH, Burgess RC, Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell. 2004;118:699–713. PubMed
Sugawara N, Wang X, Haber JE. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell. 2003;12:209–219. PubMed
Wolner B, van Komen S, Sung P, Peterson CL. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell. 2003;12:221–232. PubMed
Kantake N, Sugiyama T, Kolodner RD, Kowalczykowski SC. The recombination-deficient mutant RPA (rfa1-t11) is displaced slowly from single-stranded DNA by Rad51 protein. J. Biol. Chem. 2003;278:23410–23417. PubMed
Eggler AL, Inman RB, Cox MM. The Rad51-dependent pairing of long DNA substrates is stabilized by replication protein A. J. Biol. Chem. 2002;277:39280–39288. PubMed
Van Komen S, Petukhova G, Sigurdsson S, Sung P. Functional cross-talk among Rad51, Rad54, and replication protein A in heteroduplex DNA joint formation. J. Biol. Chem. 2002;277:43578–43587. PubMed
Cejka P, Cannavo E, Polaczek P, Masuda-Sasa T, Pokharel S, Campbell JL, Kowalczykowski SC. DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature. 2010;467:112–116. PubMed PMC
Niu H, Chung WH, Zhu Z, Kwon Y, Zhao W, Chi P, Prakash R, Seong C, Liu D, Lu L, et al. Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae. Nature. 2010;467:108–111. PubMed PMC
Ball HL, Ehrhardt MR, Mordes DA, Glick GG, Chazin WJ, Cortez D. Function of a conserved checkpoint recruitment domain in ATRIP proteins. Mol. Cell. Biol. 2007;27:3367–3377. PubMed PMC
Choi JH, Lindsey-Boltz LA, Kemp M, Mason AC, Wold MS, Sancar A. Reconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling. Proc. Natl Acad. Sci. USA. 2010;107:13660–13665. PubMed PMC
Zou L, Elledge SJ. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science. 2003;300:1542–1548. PubMed
Seong C, Sehorn MG, Plate I, Shi I, Song B, Chi P, Mortensen U, Sung P, Krejci L. Molecular anatomy of the recombination mediator function of Saccharomyces cerevisiae Rad52. J. Biol. Chem. 2008;283:12166–12174. PubMed PMC
Shinohara A, Ogawa H, Ogawa T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992;69:457–470. PubMed
Krejci L, Song B, Bussen W, Rothstein R, Mortensen UH, Sung P. Interaction with Rad51 is indispensable for recombination mediator function of Rad52. J. Biol. Chem. 2002;277:40132–40141. PubMed
Shinohara A, Ogawa T. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature. 1998;391:404–407. PubMed
Song B, Sung P. Functional interactions among yeast Rad51 recombinase, Rad52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem. 2000;275:15895–15904. PubMed
Sugiyama T, New JH, Kowalczykowski SC. 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. 1998;95:6049–6054. PubMed PMC
Plate I, Hallwyl SC, Shi I, Krejci L, Müller C, Albertsen L, Sung P, Mortensen UH. Interaction with RPA is necessary for Rad52 repair center formation and for its mediator activity. J. Biol. Chem. 2008;283:29077–29085. PubMed PMC
Davis AP, Symington LS. The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing. Genetics. 2001;159:515–525. PubMed PMC
Mortensen UH, Bendixen C, Sunjevaric I, Rothstein R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl Acad. Sci. USA. 1996;93:10729–10734. PubMed PMC
McIlwraith MJ, West SC. DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. Mol. Cell. 2008;29:510–516. PubMed
Nimonkar AV, Sica RA, Kowalczykowski SC. Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules. Proc. Natl Acad. Sci. USA. 2009;106:3077–3082. PubMed PMC
Mortensen UH, Erdeniz N, Feng Q, Rothstein R. A molecular genetic dissection of the evolutionarily conserved N terminus of yeast Rad52. Genetics. 2002;161:549–562. PubMed PMC
Shi I, Hallwyl SC, Seong C, Mortensen U, Rothstein R, Sung P. Role of the Rad52 amino-terminal DNA binding activity in DNA strand capture in homologous recombination. J. Biol. Chem. 2009;284:33275–33284. PubMed PMC
Hays SL, Firmenich AA, Berg P. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl Acad. Sci. USA. 1995;92:6925–6929. PubMed PMC
Johnson RD, Symington LS. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 1995;15:4843–4850. PubMed PMC
Sung P. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 1997;11:1111–1121. PubMed
Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature. 2011;479:245–248. PubMed PMC
Fortin GS, Symington LS. 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. 2002;21:3160–3170. PubMed PMC
Fung CW, Mozlin AM, Symington LS. Suppression of the double-strand-break-repair defect of the Saccharomyces cerevisiae rad57 mutant. Genetics. 2009;181:1195–1206. PubMed PMC
Malik PS, Symington LS. Rad51 gain-of-function mutants that exhibit high affinity DNA binding cause DNA damage sensitivity in the absence of Srs2. Nucleic Acids Res. 2008;36:6504–6510. PubMed PMC
Mozlin AM, Fung CW, Symington LS. Role of the Saccharomyces cerevisiae Rad51 paralogs in sister chromatid recombination. Genetics. 2008;178:113–126. PubMed PMC
Braybrooke JP, Spink KG, Thacker J, Hickson ID. The RAD51 family member, RAD51L3, is a DNA-stimulated ATPase that forms a complex with XRCC2. J. Biol. Chem. 2000;275:29100–29106. PubMed
Martín V, Chahwan C, Gao H, Blais V, Wohlschlegel J, Yates JR, McGowan CH, Russell P. Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J. 2006;25:2564–2574. PubMed PMC
Mankouri HW, Ngo HP, Hickson ID. Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol. Biol. Cell. 2007;18:4062–4073. PubMed PMC
Shor E, Weinstein J, Rothstein R. A genetic screen for top3 suppressors in Saccharomyces cerevisiae identifies SHU1, SHU2, PSY3 and CSM2: four genes involved in error-free DNA repair. Genetics. 2005;169:1275–1289. PubMed PMC
Ball LG, Zhang K, Cobb JA, Boone C, Xiao W. The yeast Shu complex couples error-free post-replication repair to homologous recombination. Mol. Microbiol. 2009;73:89–102. PubMed
Choi K, Szakal B, Chen YH, Branzei D, Zhao X. The Smc5/6 complex and Esc2 influence multiple replication-associated recombination processes in Saccharomyces cerevisiae. Mol. Biol. Cell. 2010;21:2306–2314. PubMed PMC
Huang ME, Rio AG, Nicolas A, Kolodner RD. A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations. Proc. Natl Acad. Sci. USA. 2003;100:11529–11534. PubMed PMC
Bernstein KA, Reid RJ, Sunjevaric I, Demuth K, Burgess RC, Rothstein R. The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase. Mol. Biol. Cell. 2011;22:1599–1607. PubMed PMC
Mazin AV, Mazina OM, Bugreev DV, Rossi MJ. Rad54, the motor of homologous recombination. DNA Repair) 2010;9:286–302. PubMed PMC
Alexeev A, Mazin A, Kowalczykowski SC. Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51-ssDNA nucleoprotein filament. Nat. Struct. Biol. 2003;10:182–186. PubMed
Alexiadis V, Kadonaga JT. Strand pairing by Rad54 and Rad51 is enhanced by chromatin. Genes Dev. 2002;16:2767–2771. PubMed PMC
Jaskelioff M, Van Komen S, Krebs JE, Sung P, Peterson CL. Rad54p is a chromatin remodeling enzyme required for heteroduplex DNA joint formation with chromatin. J. Biol. Chem. 2003;278:9212–9218. PubMed
Kwon Y, Seong C, Chi P, Greene EC, Klein H, Sung P. ATP-dependent chromatin remodeling by the Saccharomyces cerevisiae homologous recombination factor Rdh54. J. Biol. Chem. 2008;283:10445–10452. PubMed PMC
Chi P, Kwon Y, Seong C, Epshtein A, Lam I, Sung P, Klein HL. Yeast recombination factor Rdh54 functionally interacts with the Rad51 recombinase and catalyzes Rad51 removal from DNA. J. Biol. Chem. 2006;281:26268–26279. PubMed
Heyer WD, Li X, Rolfsmeier M, Zhang XP. Rad54: the Swiss Army knife of homologous recombination? Nucleic Acids Res. 2006;34:4115–4125. PubMed PMC
Li X, Heyer WD. RAD54 controls access to the invading 3′-OH end after RAD51-mediated DNA strand invasion in homologous recombination in Saccharomyces cerevisiae. Nucleic Acids Res. 2009;37:638–646. PubMed PMC
Solinger JA, Kiianitsa K, Heyer WD. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell. 2002;10:1175–1188. PubMed
Shah PP, Zheng X, Epshtein A, Carey JN, Bishop DK, Klein HL. Swi2/Snf2-related translocases prevent accumulation of toxic Rad51 complexes during mitotic growth. Mol. Cell. 2010;39:862–872. PubMed PMC
Cal-Bakowska M, Litwin I, Bocer T, Wysocki R, Dziadkowiec D. The Swi2-Snf2-like protein Uls1 is involved in replication stress response. Nucleic Acids Res. 2011;39:8765–8777. PubMed PMC
Uzunova K, Göttsche K, Miteva M, Weisshaar SR, Glanemann C, Schnellhardt M, Niessen M, Scheel H, Hofmann K, Johnson ES, et al. Ubiquitin-dependent proteolytic control of SUMO conjugates. J. Biol. Chem. 2007;282:34167–34175. PubMed
Branzei D, Foiani M. The checkpoint response to replication stress. DNA Repair. 2009;8:1038–1046. PubMed
Gangloff S, Soustelle C, Fabre F. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 2000;25:192–194. PubMed
Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell. 2001;7:293–300. PubMed
Marini V, Krejci L. Srs2: the “Odd-Job Man” in DNA repair. DNA Repair. 2010;9:268–275. PubMed PMC
Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS, Klein H, Ellenberger T, Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature. 2003;423:305–309. PubMed
Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature. 2003;423:309–312. PubMed
Colavito S, Macris-Kiss M, Seong C, Gleeson O, Greene EC, Klein HL, Krejci L, Sung P. Functional significance of the Rad51-Srs2 complex in Rad51 presynaptic filament disruption. Nucleic Acids Res. 2009;37:6754–6764. PubMed PMC
Krejci L, Macris M, Li Y, Van Komen S, Villemain J, Ellenberger T, Klein H, Sung P. Role of ATP hydrolysis in the antirecombinase function of Saccharomyces cerevisiae Srs2 protein. J. Biol. Chem. 2004;279:23193–23199. PubMed
Seong C, Colavito S, Kwon Y, Sung P, Krejci L. Regulation of Rad51 recombinase presynaptic filament assembly via interactions with the Rad52 mediator and the Srs2 anti-recombinase. J. Biol. Chem. 2009;284:24363–24371. PubMed PMC
Antony E, Tomko EJ, Xiao Q, Krejci L, Lohman TM, Ellenberger T. Srs2 disassembles Rad51 filaments by a protein-protein interaction triggering ATP turnover and dissociation of Rad51 from DNA. Mol. Cell. 2009;35:105–115. PubMed PMC
Bugreev DV, Yu X, Egelman EH, Mazin AV. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 2007;21:3085–3094. PubMed PMC
Hu Y, Raynard S, Sehorn MG, Lu X, Bussen W, Zheng L, Stark JM, Barnes EL, Chi P, Janscak P, et al. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 2007;21:3073–3084. PubMed PMC
Sommers JA, Rawtani N, Gupta R, Bugreev DV, Mazin AV, Cantor SB, Brosh RM. FANCJ uses its motor ATPase to destabilize protein-DNA complexes, unwind triplexes, and inhibit RAD51 strand exchange. J. Biol. Chem. 2009;284:7505–7517. PubMed PMC
Chiolo I, Saponaro M, Baryshnikova A, Kim JH, Seo YS, Liberi G. The human F-Box DNA helicase FBH1 faces Saccharomyces cerevisiae Srs2 and postreplication repair pathway roles. Mol. Cell. Biol. 2007;27:7439–7450. PubMed PMC
Fugger K, Mistrik M, Danielsen JR, Dinant C, Falck J, Bartek J, Lukas J, Mailand N. Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities. J. Cell. Biol. 2009;186:655–663. PubMed PMC
Lorenz A, Osman F, Folkyte V, Sofueva S, Whitby MC. Fbh1 limits Rad51-dependent recombination at blocked replication forks. Mol. Cell. Biol. 2009;29:4742–4756. PubMed PMC
Moldovan GL, Dejsuphong D, Petalcorin MI, Hofmann K, Takeda S, Boulton SJ, D'Andrea AD. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell. 2011;45:75–86. PubMed PMC
Morishita T, Furukawa F, Sakaguchi C, Toda T, Carr AM, Iwasaki H, Shinagawa H. Role of the Schizosaccharomyces pombe F-Box DNA helicase in processing recombination intermediates. Mol. Cell. Biol. 2005;25:8074–8083. PubMed PMC
Osman F, Dixon J, Barr AR, Whitby MC. The F-Box DNA helicase Fbh1 prevents Rhp51-dependent recombination without mediator proteins. Mol. Cell. Biol. 2005;25:8084–8096. PubMed PMC
Gari K, Decaillet C, Stasiak AZ, Stasiak A, Constantinou A. The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. Mol. Cell. 2008;29:141–148. PubMed
Prakash R, Satory D, Dray E, Papusha A, Scheller J, Kramer W, Krejci L, Klein H, Haber JE, Sung P, et al. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev. 2009;23:67–79. PubMed PMC
Sun W, Nandi S, Osman F, Ahn JS, Jakovleska J, Lorenz A, Whitby MC. The FANCM ortholog Fml1 promotes recombination at stalled replication forks and limits crossing over during DNA double-strand break repair. Mol. Cell. 2008;32:118–128. PubMed PMC
Zheng XF, Prakash R, Saro D, Longerich S, Niu H, Sung P. Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. DNA Repair. 2011;10:1034–1043. PubMed PMC
Sebesta M, Burkovics P, Haracska L, Krejci L. Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities. DNA Repair. 2011;10:567–576. PubMed PMC
Singh TR, Saro D, Ali AM, Zheng XF, Du CH, Killen MW, Sachpatzidis A, Wahengbam K, Pierce AJ, Xiong Y, et al. MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol. Cell. 2010;37:879–886. PubMed PMC
Wang RC, Smogorzewska A, de Lange T. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell. 2004;119:355–368. PubMed
Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O'Neil NJ, Petalcorin MI, Martin JS, Collis SJ, Cantor SB, Auclair M, et al. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell. 2008;135:261–271. PubMed PMC
Uringa EJ, Youds JL, Lisaingo K, Lansdorp PM, Boulton SJ. RTEL1: an essential helicase for telomere maintenance and the regulation of homologous recombination. Nucleic Acids Res. 2011;39:1647–1655. PubMed PMC
Ahmad F, Stewart E. The N-terminal region of the Schizosaccharomyces pombe RecQ helicase, Rqh1p, physically interacts with Topoisomerase III and is required for Rqh1p function. Mol. Genet. Genomics. 2005;273:102–114. PubMed
Chang M, Bellaoui M, Zhang C, Desai R, Morozov P, Delgado-Cruzata L, Rothstein R, Freyer GA, Boone C, Brown GW. RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex. EMBO J. 2005;24:2024–2033. PubMed PMC
Ira G, Malkova A, Liberi G, Foiani M, Haber JE. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell. 2003;115:401–411. PubMed PMC
Mankouri HW, Craig TJ, Morgan A. SGS1 is a multicopy suppressor of srs2: functional overlap between DNA helicases. Nucleic Acids Res. 2002;30:1103–1113. PubMed PMC
Oh SD, Lao JP, Hwang PY, Taylor AF, Smith GR, Hunter N. BLM ortholog, Sgs1, prevents aberrant crossing-over by suppressing formation of multichromatid joint molecules. Cell. 2007;130:259–272. PubMed PMC
Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N. RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell. 2008;31:324–336. PubMed PMC
Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. 2010;17:1377–1382. PubMed PMC
Wu L, Hickson ID. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature. 2003;426:870–874. PubMed
Adams MD, McVey M, Sekelsky JJ. Drosophila BLM in double-strand break repair by synthesis-dependent strand annealing. Science. 2003;299:265–267. PubMed
McVey M, Larocque JR, Adams MD, Sekelsky JJ. Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. Proc. Natl Acad. Sci. USA. 2004;101:15694–15699. PubMed PMC
Liberi G, Maffioletti G, Lucca C, Chiolo I, Baryshnikova A, Cotta-Ramusino C, Lopes M, Pellicioli A, Haber JE, Foiani M. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 2005;19:339–350. PubMed PMC
Rockmill B, Fung JC, Branda SS, Roeder GS. The Sgs1 helicase regulates chromosome synapsis and meiotic crossing over. Curr. Biol. 2003;13:1954–1962. PubMed
Mimitou EP, Symington LS. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature. 2008;455:770–774. PubMed PMC
Ashton TM, Hickson ID. Yeast as a model system to study RecQ helicase function. DNA Repair. 2010;9:303–314. PubMed
Ward JD, Muzzini DM, Petalcorin MI, Martinez-Perez E, Martin JS, Plevani P, Cassata G, Marini F, Boulton SJ. Overlapping mechanisms promote postsynaptic RAD-51 filament disassembly during meiotic double-strand break repair. Mol. Cell. 2010;37:259–272. PubMed
Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, Enomoto T, Ohta K, Foiani M. Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell. 2006;127:509–522. PubMed
Maeda D, Seki M, Onoda F, Branzei D, Kawabe Y, Enomoto T. Ubc9 is required for damage-tolerance and damage-induced interchromosomal homologous recombination in S. cerevisiae. DNA Repair. 2004;3:335–341. PubMed
Soustelle C, Vernis L, Fréon K, Reynaud-Angelin A, Chanet R, Fabre F, Heude M. A new Saccharomyces cerevisiae strain with a mutant Smt3-deconjugating Ulp1 protein is affected in DNA replication and requires Srs2 and homologous recombination for its viability. Mol. Cell. Biol. 2004;24:5130–5143. PubMed PMC
Zhao X, Blobel G. A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. Proc. Natl Acad. Sci. USA. 2005;102:4777–4782. PubMed PMC
Burgess RC, Rahman S, Lisby M, Rothstein R, Zhao X. The Slx5-Slx8 complex affects sumoylation of DNA repair proteins and negatively regulates recombination. Mol. Cell. Biol. 2007;27:6153–6162. PubMed PMC
Dou H, Huang C, Singh M, Carpenter PB, Yeh ET. Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol. Cell. 2010;39:333–345. PubMed PMC
Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature. 2009;462:935–939. PubMed PMC
Morris JR, Boutell C, Keppler M, Densham R, Weekes D, Alamshah A, Butler L, Galanty Y, Pangon L, Kiuchi T, et al. The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature. 2009;462:886–890. PubMed
Shi W, Feng Z, Zhang J, Gonzalez-Suarez I, Vanderwaal RP, Wu X, Powell SN, Roti Roti JL, Gonzalo S. The role of RPA2 phosphorylation in homologous recombination in response to replication arrest. Carcinogenesis. 2010;31:994–1002. PubMed PMC
Deng X, Prakash A, Dhar K, Baia GS, Kolar C, Oakley GG, Borgstahl GE. Human replication protein A-Rad52-single-stranded DNA complex: stoichiometry and evidence for strand transfer regulation by phosphorylation. Biochemistry. 2009;48:6633–6643. PubMed PMC
Barlow JH, Rothstein R. Rad52 recruitment is DNA replication independent and regulated by Cdc28 and the Mec1 kinase. EMBO J. 2009;28:1121–1130. PubMed PMC
Barlow JH, Rothstein R. Timing is everything: cell cycle control of Rad52. Cell Div. 2010;5:7. PubMed PMC
Lee DH, Pan Y, Kanner S, Sung P, Borowiec JA, Chowdhury D. A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination. Nat. Struct. Mol. Biol. 2010;17:365–372. PubMed PMC
Kovalenko OV, Plug AW, Haaf T, Gonda DK, Ashley T, Ward DC, Radding CM, Golub EI. Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. Proc. Natl Acad. Sci. USA. 1996;93:2958–2963. PubMed PMC
Shen Z, Pardington-Purtymun PE, Comeaux JC, Moyzis RK, Chen DJ. UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. Genomics. 1996;36:271–279. PubMed
Saitoh H, Pizzi MD, Wang J. Perturbation of SUMOlation enzyme Ubc9 by distinct domain within nucleoporin RanBP2/Nup358. J. Biol. Chem. 2002;277:4755–4763. PubMed
Slupianek A, Dasgupta Y, Ren SY, Gurdek E, Donlin M, Nieborowska-Skorska M, Fleury F, Skorski T. Targeting RAD51 phosphotyrosine-315 to prevent unfaithful recombination repair in BCR-ABL1 leukemia. Blood. 2011;118:1062–1068. PubMed PMC
Yuan ZM, Huang Y, Ishiko T, Nakada S, Utsugisawa T, Kharbanda S, Wang R, Sung P, Shinohara A, Weichselbaum R, et al. Regulation of Rad51 function by c-Abl in response to DNA damage. J. Biol. Chem. 1998;273:3799–3802. PubMed
Flott S, Kwon Y, Pigli YZ, Rice PA, Sung P, Jackson SP. Regulation of Rad51 function by phosphorylation. EMBO Rep. 2011;12:833–839. PubMed PMC
Yata K, Lloyd J, Maslen S, Bleuyard JY, Skehel M, Smerdon SJ, Esashi F. Plk1 and CK2 Act in Concert to Regulate Rad51 during DNA Double Strand Break Repair. Mol. Cell. 2012;45:371–383. PubMed PMC
Bashkirov VI, King JS, Bashkirova EV, Schmuckli-Maurer J, Heyer WD. DNA repair protein Rad55 is a terminal substrate of the DNA damage checkpoints. Mol. Cell. Biol. 2000;20:4393–4404. PubMed PMC
Herzberg K, Bashkirov VI, Rolfsmeier M, Haghnazari E, McDonald WH, Anderson S, Bashkirova EV, Yates JR, Heyer WD. Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol. Cell. Biol. 2006;26:8396–8409. PubMed PMC
Ho JC, Warr NJ, Shimizu H, Watts FZ. SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52. Nucleic Acids Res. 2001;29:4179–4186. PubMed PMC
Sacher M, Pfander B, Hoege C, Jentsch S. Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat. Cell. Biol. 2006;8:1284–1290. PubMed
Ohuchi T, Seki M, Branzei D, Maeda D, Ui A, Ogiwara H, Tada S, Enomoto T. Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. DNA Repair. 2008;7:879–889. PubMed
Ohuchi T, Seki M, Kugou K, Tada S, Ohta K, Enomoto T. Accumulation of sumoylated Rad52 in checkpoint mutants perturbed in DNA replication. DNA Repair. 2009;8:690–696. PubMed
Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, Chaloupkova R, Damborsky J, Sung P, Zhao X, Lisby M, Krejci L. Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res. 2010;38:4708–4721. PubMed PMC
Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, Jentsch S, Rothstein R, Aragón L, Lisby M. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat. Cell. Biol. 2007;9:923–931. PubMed
Saito K, Kagawa W, Suzuki T, Suzuki H, Yokoyama S, Saitoh H, Tashiro S, Dohmae N, Kurumizaka H. The putative nuclear localization signal of the human RAD52 protein is a potential sumoylation site. J. Biochem. 2010;147:833–842. PubMed
Antúnez de Mayolo A, Lisby M, Erdeniz N, Thybo T, Mortensen UH, Rothstein R. Multiple start codons and phosphorylation result in discrete Rad52 protein species. Nucleic Acids Res. 2006;34:2587–2597. PubMed PMC
Kitao H, Yuan ZM. Regulation of ionizing radiation-induced Rad52 nuclear foci formation by c-Abl-mediated phosphorylation. J. Biol. Chem. 2002;277:48944–48948. PubMed
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. PubMed PMC
Saponaro M, Callahan D, Zheng X, Krejci L, Haber JE, Klein HL, Liberi G. Cdk1 targets Srs2 to complete synthesis-dependent strand annealing and to promote recombinational repair. PLoS Genet. 2010;6:e1000858. PubMed PMC
Hishida T, Hirade Y, Haruta N, Kubota Y, Iwasaki H. Srs2 plays a critical role in reversible G2 arrest upon chronic and low doses of UV irradiation via two distinct homologous recombination-dependent mechanisms in postreplication repair-deficient cells. Mol. Cell. Biol. 2010;30:4840–4850. PubMed PMC
Papouli E, Chen S, Davies AA, Huttner D, Krejci L, Sung P, Ulrich HD. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell. 2005;19:123–133. PubMed
Pfander B, Moldovan GL, Sacher M, Hoege C, Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature. 2005;436:428–433. PubMed
Eladad S, Ye TZ, Hu P, Leversha M, Beresten S, Matunis MJ, Ellis NA. Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum. Mol. Genet. 2005;14:1351–1365. PubMed
Lu CY, Tsai CH, Brill SJ, Teng SC. Sumoylation of the BLM ortholog, Sgs1, promotes telomere-telomere recombination in budding yeast. Nucleic Acids Res. 2010;38:488–498. PubMed PMC
Ouyang KJ, Woo LL, Zhu J, Huo D, Matunis MJ, Ellis NA. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol. 2009;7:e1000252. PubMed PMC
Kawabe Y, Seki M, Seki T, Wang WS, Imamura O, Furuichi Y, Saitoh H, Enomoto T. Covalent modification of the Werner's syndrome gene product with the ubiquitin-related protein, SUMO-1. J. Biol. Chem. 2000;275:20963–20966. PubMed
Woods YL, Xirodimas DP, Prescott AR, Sparks A, Lane DP, Saville MK. p14 Arf promotes small ubiquitin-like modifier conjugation of Werners helicase. J. Biol. Chem. 2004;279:50157–50166. PubMed
Trickey M, Grimaldi M, Yamano H. The anaphase-promoting complex/cyclosome controls repair and recombination by ubiquitylating Rhp54 in fission yeast. Mol. Cell. Biol. 2008;28:3905–3916. PubMed PMC
Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, Kunz RC, Kubota K, Wang B, Sung P, et al. Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol. Cell. 2009;36:393–404. PubMed PMC
Chen SH, Albuquerque CP, Liang J, Suhandynata RT, Zhou H. A proteome-wide analysis of kinase-substrate network in the DNA damage response. J. Biol. Chem. 2010;285:12803–12812. PubMed PMC
Cremona CA, Sarangi P, Yang Y, Hang LE, Rahman S, Zhao X. Extensive DNA Damage-Induced Sumoylation Contributes to Replication and Repair and Acts in Addition to the Mec1 Checkpoint. Mol. Cell. 2012;45:422–432. PubMed PMC
Chu WK, Hickson ID. RecQ helicases: multifunctional genome caretakers. Nat. Rev. Cancer. 2009;9:644–654. PubMed
Knoll A, Puchta H. The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. J. Exp. Bot. 2011;62:1565–1579. PubMed
Lu X, Lou H, Luo G. A Blm-Recql5 partnership in replication stress response. J. Mol. Cell. Biol. 2011;3:31–38. PubMed
Rossi ML, Ghosh AK, Bohr VA. Roles of Werner syndrome protein in protection of genome integrity. DNA Repair. 2010;9:331–344. PubMed PMC
Unk I, Hajdú I, Blastyák A, Haracska L. Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. DNA Repair. 2010;9:257–267. PubMed
Whitby MC. The FANCM family of DNA helicases/translocases. DNA Repair. 2010;9:224–236. PubMed
Dudás A, Chovanec M. DNA double-strand break repair by homologous recombination. Mutat Res. 2004;566:131–167. PubMed
Lim DS, Hasty P. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 1996;16:7133–7143. PubMed PMC
Sonoda E, Sasaki MS, Buerstedde JM, Bezzubova O, Shinohara A, Ogawa H, Takata M, Yamaguchi-Iwai Y, Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 1998;17:598–608. PubMed PMC
Tsuzuki T, Fujii Y, Sakumi K, Tominaga Y, Nakao K, Sekiguchi M, Matsushiro A, Yoshimura Y, Morita T. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl Acad. Sci. USA. 1996;93:6236–6240. PubMed PMC
Sage JM, Gildemeister OS, Knight KL. Discovery of a novel function for human Rad51: maintenance of the mitochondrial genome. J. Biol. Chem. 2010;285:18984–18990. PubMed PMC
Richard DJ, Bolderson E, Cubeddu L, Wadsworth RI, Savage K, Sharma GG, Nicolette ML, Tsvetanov S, McIlwraith MJ, Pandita RK, et al. Single-stranded DNA-binding protein hSSB1 is critical for genomic stability. Nature. 2008;453:677–681. PubMed
Huang J, Gong Z, Ghosal G, Chen J. SOSS complexes participate in the maintenance of genomic stability. Mol. Cell. 2009;35:384–393. PubMed PMC
Li Y, Bolderson E, Kumar R, Muniandy PA, Xue Y, Richard DJ, Seidman M, Pandita TK, Khanna KK, Wang W. HSSB1 and hSSB2 form similar multiprotein complexes that participate in DNA damage response. J. Biol. Chem. 2009;284:23525–23531. PubMed PMC
Richard DJ, Cubeddu L, Urquhart AJ, Bain A, Bolderson E, Menon D, White MF, Khanna KK. hSSB1 interacts directly with the MRN complex stimulating its recruitment to DNA double-strand breaks and its endo-nuclease activity. Nucleic Acids Res. 2011;39:3643–3651. PubMed PMC
Richard DJ, Savage K, Bolderson E, Cubeddu L, So S, Ghita M, Chen DJ, White MF, Richard K, Prise KM, et al. hSSB1 rapidly binds at the sites of DNA double-strand breaks and is required for the efficient recruitment of the MRN complex. Nucleic Acids Res. 2011;39:1692–1702. PubMed PMC
Thorslund T, West SC. BRCA2: a universal recombinase regulator. Oncogene. 2007;26:7720–7730. PubMed
Yang H, Jeffrey PD, Miller J, Kinnucan E, Sun Y, Thoma NH, Zheng N, Chen PL, Lee WH, Pavletich NP. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science. 2002;297:1837–1848. PubMed
Saeki H, Siaud N, Christ N, Wiegant WW, van Buul PP, Han M, Zdzienicka MZ, Stark JM, Jasin M. Suppression of the DNA repair defects of BRCA2-deficient cells with heterologous protein fusions. Proc. Natl Acad. Sci. USA. 2006;103:8768–8773. PubMed PMC
Holloman WK. Unraveling the mechanism of BRCA2 in homologous recombination. Nat. Struct. Mol. Biol. 2011;18:748–754. PubMed PMC
Holloman WK, Schirawski J, Holliday R. The homologous recombination system of Ustilago maydis. Fungal Genet. Biol. 2008;45(Suppl. 1):S31–39. PubMed PMC
Jensen RB, Carreira A, Kowalczykowski SC. Purified human BRCA2 stimulates RAD51-mediated recombination. Nature. 2010;467:678–683. PubMed PMC
Liu J, Doty T, Gibson B, Heyer WD. Human BRCA2 protein promotes RAD51 filament formation on RPA-covered single-stranded DNA. Nat. Struct. Mol. Biol. 2010;17:1260–1262. PubMed PMC
Thorslund T, McIlwraith MJ, Compton SA, Lekomtsev S, Petronczki M, Griffith JD, West SC. The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA. Nat. Struct. Mol. Biol. 2010;17:1263–1265. PubMed PMC
Carreira A, Hilario J, Amitani I, Baskin RJ, Shivji MK, Venkitaraman AR, Kowalczykowski SC. The BRC repeats of BRCA2 modulate the DNA-binding selectivity of RAD51. Cell. 2009;136:1032–1043. PubMed PMC
Carreira A, Kowalczykowski SC. Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms. Proc. Natl Acad. Sci. USA. 2011;108:10448–10453. PubMed PMC
Pellegrini L, Yu DS, Lo T, Anand S, Lee M, Blundell TL, Venkitaraman AR. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature. 2002;420:287–293. PubMed
Shivji MK, Mukund SR, Rajendra E, Chen S, Short JM, Savill J, Klenerman D, Venkitaraman AR. The BRC repeats of human BRCA2 differentially regulate RAD51 binding on single- versus double-stranded DNA to stimulate strand exchange. Proc. Natl Acad. Sci. USA. 2009;106:13254–13259. PubMed PMC
Davies OR, Pellegrini L. Interaction with the BRCA2 C terminus protects RAD51-DNA filaments from disassembly by BRC repeats. Nat. Struct. Mol. Biol. 2007;14:475–483. PubMed PMC
Esashi F, Galkin VE, Yu X, Egelman EH, West SC. Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2. Nat. Struct. Mol. Biol. 2007;14:468–474. PubMed
Ayoub N, Rajendra E, Su X, Jeyasekharan AD, Mahen R, Venkitaraman AR. The carboxyl terminus of Brca2 links the disassembly of Rad51 complexes to mitotic entry. Curr. Biol. 2009;19:1075–1085. PubMed PMC
Schlacher K, Christ N, Siaud N, Egashira A, Wu H, Jasin M. Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell. 2011;145:529–542. PubMed PMC
Jeyasekharan AD, Ayoub N, Mahen R, Ries J, Esposito A, Rajendra E, Hattori H, Kulkarni RP, Venkitaraman AR. DNA damage regulates the mobility of Brca2 within the nucleoplasm of living cells. Proc. Natl Acad. Sci. USA. 2010;107:21937–21942. PubMed PMC
Zhou Q, Kojic M, Cao Z, Lisby M, Mazloum NA, Holloman WK. Dss1 interaction with Brh2 as a regulatory mechanism for recombinational repair. Mol. Cell. Biol. 2007;27:2512–2526. PubMed PMC
Zhou Q, Mazloum N, Mao N, Kojic M, Holloman WK. Dss1 regulates interaction of Brh2 with DNA. Biochemistry. 2009;48:11929–11938. PubMed PMC
Faza MB, Kemmler S, Panse VG. Sem1: A versatile “molecular glue”? Nucleus. 2010;1:12–17. PubMed PMC
Kristensen CN, Bystol KM, Li B, Serrano L, Brenneman MA. Depletion of DSS1 protein disables homologous recombinational repair in human cells. Mutat. Res. 2010;694:60–64. PubMed
Xia B, Sheng Q, Nakanishi K, Ohashi A, Wu J, Christ N, Liu X, Jasin M, Couch FJ, Livingston DM. Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. Mol. Cell. 2006;22:719–729. PubMed
Rahman N, Seal S, Thompson D, Kelly P, Renwick A, Elliott A, Reid S, Spanova K, Barfoot R, Chagtai T, et al. PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene. Nat. Genet. 2007;39:165–167. PubMed PMC
Oliver AW, Swift S, Lord CJ, Ashworth A, Pearl LH. Structural basis for recruitment of BRCA2 by PALB2. EMBO Rep. 2009;10:990–996. PubMed PMC
Sy SM, Huen MS, Zhu Y, Chen J. PALB2 regulates recombinational repair through chromatin association and oligomerization. J. Biol. Chem. 2009;284:18302–18310. PubMed PMC
Buisson R, Dion-Cote AM, Coulombe Y, Launay H, Cai H, Stasiak AZ, Stasiak A, Xia B, Masson JY. Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination. Nat. Struct. Mol. Biol. 2010;17:1247–1254. PubMed PMC
Dray E, Etchin J, Wiese C, Saro D, Williams GJ, Hammel M, Yu X, Galkin VE, Liu D, Tsai MS, et al. Enhancement of RAD51 recombinase activity by the tumor suppressor PALB2. Nat. Struct. Mol. Biol. 2010;17:1255–1259. PubMed PMC
Menzel T, Nahse-Kumpf V, Kousholt AN, Klein DK, Lund-Andersen C, Lees M, Johansen JV, Syljuasen RG, Sorensen CS. A genetic screen identifies BRCA2 and PALB2 as key regulators of G2 checkpoint maintenance. EMBO Rep. 2011;12:705–712. PubMed PMC
Rajagopalan S, Andreeva A, Rutherford TJ, Fersht AR. Mapping the physical and functional interactions between the tumor suppressors p53 and BRCA2. Proc. Natl. Acad. Sci. USA. 2010;107:8587–8592. PubMed PMC
Wu X, Mondal G, Wang X, Wu J, Yang L, Pankratz VS, Rowley M, Couch FJ. Microcephalin regulates BRCA2 and Rad51-associated DNA double-strand break repair. Cancer Res. 2009;69:5531–5536. PubMed PMC
Liang Y, Gao H, Lin SY, Peng G, Huang X, Zhang P, Goss JA, Brunicardi FC, Multani AS, Chang S, et al. BRIT1/MCPH1 is essential for mitotic and meiotic recombination DNA repair and maintaining genomic stability in mice. PLoS Genet. 2010;6:e1000826. PubMed PMC
Fujimori A, Tachiiri S, Sonoda E, Thompson LH, Dhar PK, Hiraoka M, Takeda S, Zhang Y, Reth M, Takata M. Rad52 partially substitutes for the Rad51 paralog XRCC3 in maintaining chromosomal integrity in vertebrate cells. EMBO J. 2001;20:5513–5520. PubMed PMC
Feng Z, Scott SP, Bussen W, Sharma GG, Guo G, Pandita TK, Powell SN. Rad52 inactivation is synthetically lethal with BRCA2 deficiency. Proc. Natl Acad. Sci. USA. 2011;108:686–691. PubMed PMC
Singleton MR, Wentzell LM, Liu Y, West SC, Wigley DB. Structure of the single-strand annealing domain of human RAD52 protein. Proc. Natl. Acad. Sci. USA. 2002;99:13492–13497. PubMed PMC
Van Dyck E, Stasiak AZ, Stasiak A, West SC. Visualization of recombination intermediates produced by RAD52-mediated single-strand annealing. EMBO Rep. 2001;2:905–909. PubMed PMC
Kojic M, Zhou Q, Fan J, Holloman WK. Mutational analysis of Brh2 reveals requirements for compensating mediator functions. Mol. Microbiol. 2011;79:180–191. PubMed PMC
Wray J, Liu J, Nickoloff JA, Shen Z. Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. Cancer Res. 2008;68:2699–2707. PubMed PMC
Treuner K, Helton R, Barlow C. Loss of Rad52 partially rescues tumorigenesis and T-cell maturation in Atm-deficient mice. Oncogene. 2004;23:4655–4661. PubMed
Takata M, Sasaki MS, Sonoda E, Fukushima T, Morrison C, Albala JS, Swagemakers SM, Kanaar R, Thompson LH, Takeda S. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol. Cell. Biol. 2000;20:6476–6482. PubMed PMC
Takata M, Sasaki MS, Tachiiri S, Fukushima T, Sonoda E, Schild D, Thompson LH, Takeda S. Chromosome instability and defective recombinational repair in knockout mutants of the five Rad51 paralogs. Mol. Cell. Biol. 2001;21:2858–2866. PubMed PMC
Thacker J. The RAD51 gene family, genetic instability and cancer. Cancer Lett. 2005;219:125–135. PubMed
Masson JY, Tarsounas MC, Stasiak AZ, Stasiak A, Shah R, McIlwraith MJ, Benson FE, West SC. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 2001;15:3296–3307. PubMed PMC
Badie S, Liao C, Thanasoula M, Barber P, Hill MA, Tarsounas M. RAD51C facilitates checkpoint signaling by promoting CHK2 phosphorylation. J. Cell. Biol. 2009;185:587–600. PubMed PMC
Henry-Mowatt J, Jackson D, Masson JY, Johnson PA, Clements PM, Benson FE, Thompson LH, Takeda S, West SC, Caldecott KW. XRCC3 and Rad51 modulate replication fork progression on damaged vertebrate chromosomes. Mol. Cell. 2003;11:1109–1117. PubMed
Petermann E, Orta ML, Issaeva N, Schultz N, Helleday T. Hydroxyurea-stalled replication forks become progressively inactivated and require two different RAD51-mediated pathways for restart and repair. Mol. Cell. 2010;37:492–502. PubMed PMC
Yokoyama H, Sarai N, Kagawa W, Enomoto R, Shibata T, Kurumizaka H, Yokoyama S. Preferential binding to branched DNA strands and strand-annealing activity of the human Rad51B, Rad51C, Rad51D and Xrcc2 protein complex. Nucleic Acids Res. 2004;32:2556–2565. PubMed PMC
Kuznetsov S, Pellegrini M, Shuda K, Fernandez-Capetillo O, Liu Y, Martin BK, Burkett S, Southon E, Pati D, Tessarollo L, et al. RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females. J. Cell. Biol. 2007;176:581–592. PubMed PMC
Liu Y, Tarsounas M, O'regan P, West SC. Role of RAD51C and XRCC3 in genetic recombination and DNA repair. J. Biol. Chem. 2007;282:1973–1979. PubMed
Schild D, Wiese C. Overexpression of RAD51 suppresses recombination defects: a possible mechanism to reverse genomic instability. Nucleic Acids Res. 2010;38:1061–1070. PubMed PMC
Deans B, Griffin CS, O'Regan P, Jasin M, Thacker J. Homologous recombination deficiency leads to profound genetic instability in cells derived from Xrcc2-knockout mice. Cancer Res. 2003;63:8181–8187. PubMed
Pittman DL, Schimenti JC. Midgestation lethality in mice deficient for the RecA-related gene, Rad51d/Rad51l3. Genesis. 2000;26:167–173. PubMed
Shu Z, Smith S, Wang L, Rice MC, Kmiec EB. Disruption of muREC2/RAD51L1 in mice results in early embryonic lethality which can Be partially rescued in a p53(-/-) background. Mol. Cell. Biol. 1999;19:8686–8693. PubMed PMC
Kovalenko OV, Golub EI, Bray-Ward P, Ward DC, Radding CM. A novel nucleic acid-binding protein that interacts with human rad51 recombinase. Nucleic Acids Res. 1997;25:4946–4953. PubMed PMC
Modesti M, Budzowska M, Baldeyron C, Demmers JA, Ghirlando R, Kanaar R. RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. Mol. Cell. 2007;28:468–481. PubMed
Wiese C, Dray E, Groesser T, San Filippo J, Shi I, Collins DW, Tsai MS, Williams GJ, Rydberg B, Sung P, et al. Promotion of homologous recombination and genomic stability by RAD51AP1 via RAD51 recombinase enhancement. Mol. Cell. 2007;28:482–490. PubMed PMC
Ceballos SJ, Heyer WD. Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim. Biophys. Acta. 2011;1809:509–523. PubMed PMC
Wesoly J, Agarwal S, Sigurdsson S, Bussen W, Van Komen S, Qin J, van Steeg H, van Benthem J, Wassenaar E, Baarends WM, et al. Differential contributions of mammalian Rad54 paralogs to recombination, DNA damage repair, and meiosis. Mol. Cell. Biol. 2006;26:976–989. PubMed PMC
Neale MJ, Keeney S. Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature. 2006;442:153–158. PubMed PMC
Hunter N. Molecular Genetics of Recombination, Topics in Current Genetics. Heidelberg: Springer-Verlag Berlin; 2007. Meiotic recombination; pp. 381–441.
Bishop DK, Park D, Xu L, Kleckner N. DMC1: a meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell. 1992;69:439–456. PubMed
Rockmill B, Sym M, Scherthan H, Roeder GS. Roles for two RecA homologs in promoting meiotic chromosome synapsis. Genes Dev. 1995;9:2684–2695. PubMed
Schwacha A, Kleckner N. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell. 1997;90:1123–1135. PubMed
Pittman DL, Cobb J, Schimenti KJ, Wilson LA, Cooper DM, Brignull E, Handel MA, Schimenti JC. Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. Mol. Cell. 1998;1:697–705. PubMed
Yoshida K, Kondoh G, Matsuda Y, Habu T, Nishimune Y, Morita T. The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. Mol. Cell. 1998;1:707–718. PubMed
Benson FE, Stasiak A, West SC. Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. EMBO J. 1994;13:5764–5771. PubMed PMC
Passy SI, Yu X, Li Z, Radding CM, Masson JY, West SC, Egelman EH. Human Dmc1 protein binds DNA as an octameric ring. Proc. Natl Acad. Sci. USA. 1999;96:10684–10688. PubMed PMC
Sehorn MG, Sigurdsson S, Bussen W, Unger VM, Sung P. Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange. Nature. 2004;429:433–437. PubMed
Sheridan SD, Yu X, Roth R, Heuser JE, Sehorn MG, Sung P, Egelman EH, Bishop DK. A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments. Nucleic Acids Res. 2008;36:4057–4066. PubMed PMC
Bugreev DV, Golub EI, Stasiak AZ, Stasiak A, Mazin AV. Activation of human meiosis-specific recombinase Dmc1 by Ca2+ J. Biol. Chem. 2005;280:26886–26895. PubMed
Sheridan S, Bishop DK. Red-Hed regulation: recombinase Rad51, though capable of playing the leading role, may be relegated to supporting Dmc1 in budding yeast meiosis. Genes Dev. 2006;20:1685–1691. PubMed
Shinohara M, Gasior SL, Bishop DK, Shinohara A. Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. Proc. Natl Acad. Sci. USA. 2000;97:10814–10819. PubMed PMC
Bugreev DV, Pezza RJ, Mazina OM, Voloshin ON, Camerini-Otero RD, Mazin AV. The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis. Nat. Struct. Mol. Biol. 2011;18:56–60. PubMed PMC
Kagawa W, Kurumizaka H. From meiosis to postmeiotic events: uncovering the molecular roles of the meiosis-specific recombinase Dmc1. FEBS J. 2010;277:590–598. PubMed
Ehmsen KT, Heyer WD. Biochemistry of Meiotic Recombination: Formation, Processing, and Resolution of Recombination Intermediates. Genome. Dyn. Stab. 2008;3:91. PubMed PMC
Hayase A, Takagi M, Miyazaki T, Oshiumi H, Shinohara M, Shinohara A. A protein complex containing Mei5 and Sae3 promotes the assembly of the meiosis-specific RecA homolog Dmc1. Cell. 2004;119:927–940. PubMed
Ferrari SR, Grubb J, Bishop DK. The Mei5-Sae3 protein complex mediates Dmc1 activity in Saccharomyces cerevisiae. J. Biol. Chem. 2009;284:11766–11770. PubMed PMC
Say AF, Ledford LL, Sharma D, Singh AK, Leung WK, Sehorn HA, Tsubouchi H, Sung P, Sehorn MG. The budding yeast Mei5-Sae3 complex interacts with Rad51 and preferentially binds a DNA fork structure. DNA Repair. 2011;10:586–594. PubMed PMC
Schwacha A, Kleckner N. Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway. Cell. 1997;90:1123–1135. PubMed
Tsubouchi H, Roeder GS. The budding yeast mei5 and sae3 proteins act together with dmc1 during meiotic recombination. Genetics. 2004;168:1219–1230. PubMed PMC
Akamatsu Y, Dziadkowiec D, Ikeguchi M, Shinagawa H, Iwasaki H. Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast. Proc. Natl Acad. Sci. USA. 2003;100:15770–15775. PubMed PMC
Akamatsu Y, Tsutsui Y, Morishita T, Siddique MS, Kurokawa Y, Ikeguchi M, Yamao F, Arcangioli B, Iwasaki H. Fission yeast Swi5/Sfr1 and Rhp55/Rhp57 differentially regulate Rhp51-dependent recombination outcomes. EMBO J. 2007;26:1352–1362. PubMed PMC
Ellermeier C, Schmidt H, Smith GR. Swi5 acts in meiotic DNA joint molecule formation in Schizosaccharomyces pombe. Genetics. 2004;168:1891–1898. PubMed PMC
Haruta N, Kurokawa Y, Murayama Y, Akamatsu Y, Unzai S, Tsutsui Y, Iwasaki H. The Swi5-Sfr1 complex stimulates Rhp51/Rad51- and Dmc1-mediated DNA strand exchange in vitro. Nat. Struct. Mol. Biol. 2006;13:823–830. PubMed
Akamatsu Y, Jasin M. Role for the mammalian Swi5-Sfr1 complex in DNA strand break repair through homologous recombination. PLoS Genet. 2010;6:e1001160. PubMed PMC
Yuan J, Chen J. The role of the human SWI5-MEI5 complex in homologous recombination repair. J. Biol. Chem. 2011;286:9888–9893. PubMed PMC
Leu JY, Chua PR, Roeder GS. The meiosis-specific Hop2 protein of S. cerevisiae ensures synapsis between homologous chromosomes. Cell. 1998;94:375–386. PubMed
Chi P, San Filippo J, Sehorn MG, Petukhova GV, Sung P. Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. Genes Dev. 2007;21:1747–1757. PubMed PMC
Pezza RJ, Voloshin ON, Vanevski F, Camerini-Otero RD. Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. Genes Dev. 2007;21:1758–1766. PubMed PMC
Henry JM, Camahort R, Rice DA, Florens L, Swanson SK, Washburn MP, Gerton JL. Mnd1/Hop2 facilitates Dmc1-dependent interhomolog crossover formation in meiosis of budding yeast. Mol. Cell. Biol. 2006;26:2913–2923. PubMed PMC
Zierhut C, Berlinger M, Rupp C, Shinohara A, Klein F. Mnd1 is required for meiotic interhomolog repair. Curr. Biol. 2004;14:752–762. PubMed
Gerton JL, DeRisi JL. Mnd1p: an evolutionarily conserved protein required for meiotic recombination. Proc. Natl Acad. Sci. USA. 2002;99:6895–6900. PubMed PMC
Pezza RJ, Camerini-Otero RD, Bianco PR. Hop2-Mnd1 condenses DNA to stimulate the synapsis phase of DNA strand exchange. Biophys. J. 2010;99:3763–3772. PubMed PMC
Van Komen S, Petukhova G, Sigurdsson S, Stratton S, Sung P. Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. Mol. Cell. 2000;6:563–572. PubMed
Klein HL. RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics. 1997;147:1533–1543. PubMed PMC
Shinohara M, Shita-Yamaguchi E, Buerstedde JM, Shinagawa H, Ogawa H, Shinohara A. Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics. 1997;147:1545–1556. PubMed PMC
Dresser ME, Ewing DJ, Conrad MN, Dominguez AM, Barstead R, Jiang H, Kodadek T. DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. Genetics. 1997;147:533–544. PubMed PMC
Clever B, Interthal H, Schmuckli-Maurer J, King J, Sigrist M, Heyer WD. Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J. 1997;16:2535–2544. PubMed PMC
Jiang H, Xie Y, Houston P, Stemke-Hale K, Mortensen UH, Rothstein R, Kodadek T. Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem. 1996;271:33181–33186. PubMed
Holzen TM, Shah PP, Olivares HA, Bishop DK. Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites on meiotic chromatin. Genes Dev. 2006;20:2593–2604. PubMed PMC
Chi P, Kwon Y, Moses DN, Seong C, Sehorn MG, Singh AK, Tsubouchi H, Greene EC, Klein HL, Sung P. Functional interactions of meiotic recombination factors Rdh54 and Dmc1. DNA Repair. 2009;8:279–284. PubMed PMC
Arbel A, Zenvirth D, Simchen G. Sister chromatid-based DNA repair is mediated by RAD54, not by DMC1 or TID1. EMBO J. 1999;18:2648–2658. PubMed PMC
Tsubouchi H, Roeder GS. Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. Genes Dev. 2006;20:1766–1775. PubMed PMC
Busygina V, Sehorn MG, Shi IY, Tsubouchi H, Roeder GS, Sung P. Hed1 regulates Rad51-mediated recombination via a novel mechanism. Genes Dev. 2008;22:786–795. PubMed PMC
Shinohara M, Sakai K, Shinohara A, Bishop DK. Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. Genetics. 2003;163:1273–1286. PubMed PMC
Tsubouchi H, Roeder GS. The importance of genetic recombination for fidelity of chromosome pairing in meiosis. Dev. Cell. 2003;5:915–925. PubMed
Dray E, Dunlop MH, Kauppi L, San Filippo J, Wiese C, Tsai MS, Begovic S, Schild D, Jasin M, Keeney S, et al. Molecular basis for enhancement of the meiotic DMC1 recombinase by RAD51 associated protein 1 (RAD51AP1) Proc. Natl Acad. Sci. USA. 2011;108:3560–3565. PubMed PMC
Kovalenko OV, Wiese C, Schild D. RAD51AP2, a novel vertebrate- and meiotic-specific protein, shares a conserved RAD51-interacting C-terminal domain with RAD51AP1/PIR51. Nucleic Acids Res. 2006;34:5081–5092. PubMed PMC
Dray E, Siaud N, Dubois E, Doutriaux MP. Interaction between Arabidopsis Brca2 and its partners Rad51, Dmc1, and Dss1. Plant Physiol. 2006;140:1059–1069. PubMed PMC
Thorslund T, Esashi F, West SC. Interactions between human BRCA2 protein and the meiosis-specific recombinase DMC1. EMBO J. 2007;26:2915–2922. PubMed PMC
Rodríguez-Marí A, Wilson C, Titus TA, Cañestro C, BreMiller RA, Yan YL, Nanda I, Johnston A, Kanki JP, Gray EM, et al. Roles of brca2 (fancd1) in oocyte nuclear architecture, gametogenesis, gonad tumors, and genome stability in zebrafish. PLoS Genet. 2011;7:e1001357. PubMed PMC
Siaud N, Dray E, Gy I, Gérard E, Takvorian N, Doutriaux MP. Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1. EMBO J. 2004;23:1392–1401. PubMed PMC
Klovstad M, Abdu U, Schüpbach T. Drosophila brca2 is required for mitotic and meiotic DNA repair and efficient activation of the meiotic recombination checkpoint. PLoS Genet. 2008;4:e31. PubMed PMC
Sharan SK, Pyle A, Coppola V, Babus J, Swaminathan S, Benedict J, Swing D, Martin BK, Tessarollo L, Evans JP, et al. BRCA2 deficiency in mice leads to meiotic impairment and infertility. Development. 2004;131:131–142. PubMed
Shive HR, West RR, Embree LJ, Azuma M, Sood R, Liu P, Hickstein DD. brca2 in zebrafish ovarian development, spermatogenesis, and tumorigenesis. Proc. Natl Acad. Sci. USA. 2010;107:19350–19355. PubMed PMC
Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science. 2008;319:1352–1355. PubMed
Spry M, Scott T, Pierce H, D'Orazio JA. DNA repair pathways and hereditary cancer susceptibility syndromes. Front. Biosci. 2007;12:4191–4207. PubMed
Narod SA, Foulkes WD. BRCA1 and BRCA2: 1994 and beyond. Nat. Rev. Cancer. 2004;4:665–676. PubMed
Howlett NG, Taniguchi T, Olson S, Cox B, Waisfisz Q, De Die-Smulders C, Persky N, Grompe M, Joenje H, Pals G, et al. Biallelic inactivation of BRCA2 in Fanconi anemia. Science. 2002;297:606–609. PubMed
Jones P, Altamura S, Boueres J, Ferrigno F, Fonsi M, Giomini C, Lamartina S, Monteagudo E, Ontoria JM, Orsale MV, et al. Discovery of 2-{4-[(3S)-piperidin-3-yl]phenyl}-2H-indazole-7-carboxamide (MK-4827): a novel oral poly(ADP-ribose)polymerase (PARP) inhibitor efficacious in BRCA-1 and -2 mutant tumors. J. Med. Chem. 2009;52:7170–7185. PubMed
Meindl A, Hellebrand H, Wiek C, Erven V, Wappenschmidt B, Niederacher D, Freund M, Lichtner P, Hartmann L, Schaal H, et al. Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene. Nat. Genet. 2010;42:410–414. PubMed
Reid S, Schindler D, Hanenberg H, Barker K, Hanks S, Kalb R, Neveling K, Kelly P, Seal S, Freund M, et al. Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer. Nat. Genet. 2007;39:162–164. PubMed
Vaz F, Hanenberg H, Schuster B, Barker K, Wiek C, Erven V, Neveling K, Endt D, Kesterton I, Autore F, et al. Mutation of the RAD51C gene in a Fanconi anemia-like disorder. Nat. Genet. 2010;42:406–409. PubMed
Hiramoto T, Nakanishi T, Sumiyoshi T, Fukuda T, Matsuura S, Tauchi H, Komatsu K, Shibasaki Y, Inui H, Watatani M, et al. Mutations of a novel human RAD54 homologue, RAD54B, in primary cancer. Oncogene. 1999;18:3422–3426. PubMed
Schoenmakers EF, Huysmans C, Van de Ven WJ. Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. Cancer Res. 1999;59:19–23. PubMed
Smirnova M, Van Komen S, Sung P, Klein HL. Effects of tumor-associated mutations on Rad54 functions. J. Biol. Chem. 2004;279:24081–24088. PubMed
Martinez-Perez E, Colaiacovo MP. Distribution of meiotic recombination events: talking to your neighbors. Curr. Opin. Genet. Dev. 2009;19:105–112. PubMed PMC
Richardson C, Stark JM, Ommundsen M, Jasin M. Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability. Oncogene. 2004;23:546–553. PubMed
Klein HL. The consequences of Rad51 overexpression for normal and tumor cells. DNA Repair. 2008;7:686–693. PubMed PMC
Cramer K, Nieborowska-Skorska M, Koptyra M, Slupianek A, Penserga ET, Eaves CJ, Aulitzky W, Skorski T. BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. Cancer Res. 2008;68:6884–6888. PubMed PMC
Fernandes MS, Reddy MM, Gonneville JR, DeRoo SC, Podar K, Griffin JD, Weinstock DM, Sattler M. BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair. Blood. 2009;114:1813–1819. PubMed PMC
Mandon-Pepin B, Touraine P, Kuttenn F, Derbois C, Rouxel A, Matsuda F, Nicolas A, Cotinot C, Fellous M. Genetic investigation of four meiotic genes in women with premature ovarian failure. Eur.J. Endocrinol./EFES. 2008;158:107–115. PubMed
Farmer H, McCabe N, Lord CJ, Tutt AN, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, et al. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature. 2005;434:917–921. PubMed
Kaelin WG. The concept of synthetic lethality in the context of anticancer therapy. Nat. Rev. Cancer. 2005;5:689–698. PubMed
Chen CC, Kennedy RD, Sidi S, Look AT, D'Andrea A. CHK1 inhibition as a strategy for targeting Fanconi Anemia (FA) DNA repair pathway deficient tumors. Mol. Cancer. 2009;8:24. PubMed PMC
McManus KJ, Barrett IJ, Nouhi Y, Hieter P. Specific synthetic lethal killing of RAD54B-deficient human colorectal cancer cells by FEN1 silencing. Proc. Natl Acad. Sci. USA. 2009;106:3276–3281. PubMed PMC
Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase. Nature. 2005;434:913–917. PubMed
Mukhopadhyay A, Elattar A, Cerbinskaite A, Wilkinson SJ, Drew Y, Kyle S, Los G, Hostomsky Z, Edmondson RJ, Curtin NJ. Development of a functional assay for homologous recombination status in primary cultures of epithelial ovarian tumor and correlation with sensitivity to poly(ADP-ribose) polymerase inhibitors. Clin. Cancer Res. 2010;16:2344–2351. PubMed
Gottipati P, Vischioni B, Schultz N, Solomons J, Bryant HE, Djureinovic T, Issaeva N, Sleeth K, Sharma RA, Helleday T. Poly(ADP-ribose) polymerase is hyperactivated in homologous recombination-defective cells. Cancer Res. 2010;70:5389–5398. PubMed
Banerjee S, Kaye SB, Ashworth A. Making the best of PARP inhibitors in ovarian cancer. Nat. Rev. Clin. Oncol. 2010;7:508–519. PubMed
Evers B, Drost R, Schut E, de Bruin M, van der Burg E, Derksen PW, Holstege H, Liu X, van Drunen E, Beverloo HB, et al. Selective inhibition of BRCA2-deficient mammary tumor cell growth by AZD2281 and cisplatin. Clin. Cancer. Res. 2008;14:3916–3925. PubMed
Evers B, Helleday T, Jonkers J. Targeting homologous recombination repair defects in cancer. Trends Pharmacol. Sci. 2010;31:372–380. PubMed
Edwards SL, Brough R, Lord CJ, Natrajan R, Vatcheva R, Levine DA, Boyd J, Reis-Filho JS, Ashworth A. Resistance to therapy caused by intragenic deletion in BRCA2. Nature. 2008;451:1111–1115. PubMed
Sakai W, Swisher EM, Karlan BY, Agarwal MK, Higgins J, Friedman C, Villegas E, Jacquemont C, Farrugia DJ, Couch FJ, et al. Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers. Nature. 2008;451:1116–1120. PubMed PMC
Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J, Helleday T. The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat. Cell Biol. 2005;7:195–201. PubMed
Popova M, Shimizu H, Yamamoto K, Lebechec M, Takahashi M, Fleury F. Detection of c-Abl kinase-promoted phosphorylation of Rad51 by specific antibodies reveals that Y54 phosphorylation is dependent on that of Y315. FEBS Lett. 2009;583:1867–1872. PubMed
Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC. CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature. 2005;434:598–604. PubMed
Schoenfeld AR, Apgar S, Dolios G, Wang R, Aaronson SA. BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol. Cell. Biol. 2004;24:7444–7455. PubMed PMC
Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, III, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science. 2007;316:1160–1166. PubMed
Kim JM, Kee Y, Gurtan A, D'Andrea AD. Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood. 2008;111:5215–5222. PubMed PMC
Fricke WM, Kaliraman V, Brill SJ. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J. Biol. Chem. 2001;276:8848–8855. PubMed PMC
Rao VA, Fan AM, Meng L, Doe CF, North PS, Hickson ID, Pommier Y. Phosphorylation of BLM, dissociation from topoisomerase IIIalpha, and colocalization with gamma-H2AX after topoisomerase I-induced replication damage. Mol. Cell. Biol. 2005;25:8925–8937. PubMed PMC
Leng M, Chan DW, Luo H, Zhu C, Qin J, Wang Y. MPS1-dependent mitotic BLM phosphorylation is important for chromosome stability. Proc. Natl Acad. Sci. USA. 2006;103:11485–11490. PubMed PMC
Concurrent D-loop cleavage by Mus81 and Yen1 yields half-crossover precursors
Mapping and Analysis of Swi5 and Sfr1 Phosphorylation Sites
RECQ5: A Mysterious Helicase at the Interface of DNA Replication and Transcription
Esc2 promotes Mus81 complex-activity via its SUMO-like and DNA binding domains
A Polar and Nucleotide-Dependent Mechanism of Action for RAD51 Paralogs in RAD51 Filament Remodeling
SUMOylation of Rad52-Rad59 synergistically change the outcome of mitotic recombination
Srs2 promotes Mus81-Mms4-mediated resolution of recombination intermediates
Strand invasion by HLTF as a mechanism for template switch in fork rescue
Role of PCNA and TLS polymerases in D-loop extension during homologous recombination in humans
Srs2 mediates PCNA-SUMO-dependent inhibition of DNA repair synthesis
Dual roles of the SUMO-interacting motif in the regulation of Srs2 sumoylation