Homologous recombination plays a key role in the maintenance of genome integrity, especially during DNA replication and the repair of double-stranded DNA breaks (DSBs). Just a single un-repaired break can lead to aneuploidy, genetic aberrations or cell death. DSBs are caused by a vast number of both endogenous and exogenous agents including genotoxic chemicals or ionizing radiation, as well as through replication of a damaged template DNA or the replication fork collapse. It is essential for cell survival to recognise and process DSBs as well as other toxic intermediates and launch most appropriate repair mechanism. Many helicases have been implicated to play role in these processes, however their detail roles, specificities and co-operativity in the complex protein-protein interaction networks remain unclear. In this review we summarize the current knowledge about Saccharomyces cerevisiae helicase Srs2 and its effect on multiple DNA metabolic processes that generally affect genome stability. It would appear that Srs2 functions as an "Odd-Job Man" in these processes to make sure that the jobs proceed when and where they are needed.

Department of Biology Faculty of Medicine Masaryk University Brno CZ 625 00 Czech Republic

Erratum v

DNA Repair (Amst). 2012 Jun 1;11(6):594 PubMed

Zobrazit více v PubMed

Gorbalenya A.E., Koonin E.V., Donchenko A.P., Blinov V.M. A novel superfamily of nucleoside triphosphate-binding motif containing proteins which are probably involved in duplex unwinding in DNA and RNA replication and recombination. FEBS Lett. 1988;235:16–24. PubMed PMC

Hall M.C., Matson S.W. Helicase motifs: the engine that powers DNA unwinding. Mol. Microbiol. 1999;34:867–877. PubMed

Aboussekhra A., Chanet R., Zgaga Z., Cassier-Chauvat C., Heude M., Fabre F. RADH, a gene of Saccharomyces cerevisiae encoding a putative DNA helicase involved in DNA repair. Characteristics of radH mutants and sequence of the gene. Nucleic Acids Res. 1989;17:7211–7219. PubMed PMC

Chiolo I., Carotenuto W., Maffioletti G., Petrini J.H., Foiani M., Liberi G. Srs2 and Sgs1 DNA helicases associate with Mre11 in different subcomplexes following checkpoint activation and CDK1-mediated Srs2 phosphorylation. Mol. Cell. Biol. 2005;25:5738–5751. PubMed PMC

Rong L., Klein H.L. Purification and characterization of the SRS2 DNA helicase of the yeast Saccharomyces cerevisiae. J. Biol. Chem. 1993;268:1252–1259. PubMed

Van Komen S., Reddy M.S., Krejci L., Klein H., Sung P. ATPase and DNA helicase activities of the Saccharomyces cerevisiae anti-recombinase Srs2. J. Biol. Chem. 2003;278:44331–44337. PubMed

Krejci L., Macris M., Li Y., Van Komen S., Villemain J., Ellenberger T., Klein H., Sung P. Role of ATP hydrolysis in the anti-recombinase function of Saccharomyces cerevisiae Srs2 protein. J. Biol. Chem. 2004;279:23193–23199. PubMed

Dupaigne P., Le Breton C., Fabre F., Gangloff S., Le Cam E., Veaute X. The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: implications for crossover incidence during mitotic recombination. Mol. Cell. 2008;29:243–254. PubMed

Prakash R., Satory D., Dray E., Papusha A., Scheller J., Kramer W., Krejci L., Klein H., Haber J.E., Sung P., Ira G. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev. 2009;23:67–79. PubMed PMC

Antony E., Tomko E.J., Xiao Q., Krejci L., Lohman T.M., 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

Lohman T.M., Tomko E.J., Wu C.G. Non-hexameric DNA helicases and translocases: mechanisms and regulation. Nat. Rev. Mol. Cell Biol. 2008;9:391–401. 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 S.E., Lucca C., Foiani M., Haber J.E. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol. Cell. 2001;7:293–300. PubMed

Vaze M.B., Pellicioli A., Lee S.E., Ira G., Liberi G., Arbel-Eden A., Foiani M., Haber J.E. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires Srs2 helicase. Mol. Cell. 2002;10:373–385. PubMed

Zou L., Elledge S.J. Sensing DNA damage through ATRIP recognition of RPA–ssDNA complexes. Science. 2003;300:1542–1548. PubMed

Barber L.J., Youds J.L., Ward J.D., McIlwraith M.J., O’Neil N.J., Petalcorin M.I., Martin J.S., Collis S.J., Cantor S.B., Auclair M., Tissenbaum H., West S.C., Rose A.M., Boulton S.J. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell. 2008;135:261–271. PubMed PMC

Bussen W., Raynard S., Busygina V., Singh A.K., Sung P. Holliday junction processing activity of the BLM-Topo IIIalpha–BLAP75 complex. J. Biol. Chem. 2007;282:31484–31492. PubMed

Wu L., Bachrati C.Z., Ou J., Xu C., Yin J., Chang M., Wang W., Li L., Brown G.W., Hickson I.D. BLAP75/RMI1 promotes the BLM-dependent dissolution of homologous recombination intermediates. Proc. Natl. Acad. Sci. U.S.A. 2006;103:4068–4073. PubMed PMC

Wu L., Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature. 2003;426:870–874. PubMed

Aboussekhra A., Chanet R., Adjiri A., Fabre F. Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol. Cell. Biol. 1992;12:3224–3234. PubMed PMC

Chanet R., Heude M., Adjiri A., Maloisel L., Fabre F. Semidominant mutations in the yeast Rad51 protein and their relationships with the Srs2 helicase. Mol. Cell. Biol. 1996;16:4782–4789. PubMed PMC

Fabre F., Chan A., Heyer W.D., Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. U.S.A. 2002;99:16887–16892. PubMed PMC

Rong L., Palladino F., Aguilera A., Klein H.L. The hyper-gene conversion hpr5-1 mutation of Saccharomyces cerevisiae is an allele of the SRS2/RADH gene. Genetics. 1991;127:75–85. PubMed PMC

Klein H.L. 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

McVey M., Kaeberlein M., Tissenbaum H.A., Guarente L. The short life span of Saccharomyces cerevisiae sgs1 and srs2 mutants is a composite of normal aging processes and mitotic arrest due to defective recombination. Genetics. 2001;157:1531–1542. PubMed PMC

Schild D. Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics. 1995;140:115–127. PubMed PMC

Krejci L, Van Komen S., Li Y., Villemain J., Reddy M.S., 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 S.C., Le Cam E., Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature. 2003;423:309–312. 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

Colavito S., Macris-Kiss M., Seong C., Gleeson O., Greene E.C., Klein H.L., 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

Chen Z., Yang H., Pavletich N.P. Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures. Nature. 2008;453:489–494. PubMed

Conway A.B., Lynch T.W., Zhang Y., Fortin G.S., Fung C.W., Symington L.S., Rice P.A. Crystal structure of a Rad51 filament. Nat. Struct. Mol. Biol. 2004;11:791–796. PubMed

Qian X., He Y., Wu Y., Luo Y. Asp302 determines potassium dependence of a RadA recombinase from Methanococcus voltae. J. Mol. Biol. 2006;360:537–547. PubMed

Branzei D., Foiani M. The Rad53 signal transduction pathway: replication fork stabilization, DNA repair, and adaptation. Exp. Cell Res. 2006;312:2654–2659. PubMed

Branzei D., Foiani M. The checkpoint response to replication stress. DNA Repair (Amst.) 2009;8:1038–1046. PubMed

Liberi G., Chiolo I., Pellicioli A., Lopes M., Plevani P., Muzi-Falconi M., Foiani M. Srs2 DNA helicase is involved in checkpoint response and its regulation requires a functional Mec1-dependent pathway and Cdk1 activity. EMBO J. 2000;19:5027–5038. PubMed PMC

Ooi S.L., Shoemaker D.D., Boeke J.D. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 2003;35:277–286. PubMed

Pan X., Ye P., Yuan D.S., Wang X., Bader J.S., Boeke J.D. A DNA integrity network in the yeast Saccharomyces cerevisiae. Cell. 2006;124:1069–1081. PubMed

Schmidt K.H., Kolodner R.D. Requirement of Rrm3 helicase for repair of spontaneous DNA lesions in cells lacking Srs2 or Sgs1 helicase. Mol. Cell. Biol. 2004;24:3213–3226. PubMed PMC

Schmidt K.H., Kolodner R.D. Suppression of spontaneous genome rearrangements in yeast DNA helicase mutants. Proc. Natl. Acad. Sci. U.S.A. 2006;103:18196–18201. PubMed PMC

Ye P., Peyser B.D., Pan X., Boeke J.D., Spencer F.A., Bader J.S. Gene function prediction from congruent synthetic lethal interactions in yeast. Mol. Syst. Biol. 2005;1 2005 0026. PubMed PMC

Azvolinsky A., Dunaway S., Torres J.Z., Bessler J.B., Zakian V.A. The S. cerevisiae Rrm3p DNA helicase moves with the replication fork and affects replication of all yeast chromosomes. Genes Dev. 2006;20:3104–3116. PubMed PMC

Ivessa A.S., Zhou J.Q., Schulz V.P., Monson E.K., Zakian V.A. Saccharomyces Rrm3p, a 5′ to 3′ DNA helicase that promotes replication fork progression through telomeric and subtelomeric DNA. Genes Dev. 2002;16:1383–1396. PubMed PMC

Torres J.Z., Schnakenberg S.L., Zakian V.A. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 2004;24:3198–3212. PubMed PMC

Branzei D., Vanoli F., Foiani M. SUMOylation regulates Rad18-mediated template switch. Nature. 2008;456:915–920. PubMed

Schurer K.A., Rudolph C., Ulrich H.D., Kramer W. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from homologous recombination, but not from postreplicative repair. Genetics. 2004;166:1673–1686. PubMed PMC

Aguilera A., Klein H.L. Genetic control of intrachromosomal recombination in Saccharomyces cerevisiae. I. Isolation and genetic characterization of hyper-recombination mutations. Genetics. 1988;119:779–790. PubMed PMC

Lawrence C.W., Christensen R.B. Metabolic suppressors of trimethoprim and ultraviolet light sensitivities of Saccharomyces cerevisiae rad6 mutants. J. Bacteriol. 1979;139:866–876. PubMed PMC

Schiestl R.H., Zhu J., Petes T.D. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 1994;14:4493–4500. PubMed PMC

Papouli E., Chen S., Davies A.A., Huttner D., Krejci L., Sung P., Ulrich H.D. 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 G.L., Sacher M., Hoege C., Jentsch S. SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase. Nature. 2005;436:428–433. PubMed

Stelter P., Ulrich H.D. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature. 2003;425:188–191. PubMed

Milne G.T., Ho T., Weaver D.T. Modulation of Saccharomyces cerevisiae DNA double-strand break repair by SRS2 and RAD51. Genetics. 1995;139:1189–1199. PubMed PMC

Barbour L., Xiao W. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat. Res. 2003;532:137–155. PubMed

Sogo J.M., Lopes M., Foiani M. Fork reversal and ssDNA accumulation at stalled replication forks owing to checkpoint defects. Science. 2002;297:599–602. PubMed

Schiestl R.H., Prakash S., Prakash L. The SRS2 suppressor of rad6 mutations of Saccharomyces cerevisiae acts by channeling DNA lesions into the RAD52 DNA repair pathway. Genetics. 1990;124:817–831. PubMed PMC

Broomfield S., Xiao W. Suppression of genetic defects within the RAD6 pathway by srs2 is specific for error-free post-replication repair but not for damage-induced mutagenesis. Nucleic Acids Res. 2002;30:732–739. PubMed PMC

Smirnova M., Klein H.L. Role of the error-free damage bypass postreplication repair pathway in the maintenance of genomic stability. Mutat. Res. 2003;532:117–135. PubMed

Ulrich H.D. The srs2 suppressor of UV sensitivity acts specifically on the RAD5- and MMS2-dependent branch of the RAD6 pathway. Nucleic Acids Res. 2001;29:3487–3494. PubMed PMC

Burgess R.C., Lisby M., Altmannova V., Krejci L., Sung P., Rothstein R. Localization of recombination proteins and Srs2 reveals anti-recombinase function in vivo. J. Cell Biol. 2009;185:969–981. PubMed PMC

Krejci L., Damborsky J., Thomsen B., Duno M., Bendixen C. Molecular dissection of interactions between Rad51 and members of the recombination-repair group. Mol. Cell. Biol. 2001;21:966–976. PubMed PMC

Lucca C., Vanoli F., Cotta-Ramusino C., Pellicioli A., Liberi G., Haber J., Foiani M. Checkpoint-mediated control of replisome–fork association and signalling in response to replication pausing. Oncogene. 2004;23:1206–1213. PubMed

Zou L., Liu D., Elledge S.J. Replication protein A-mediated recruitment and activation of Rad17 complexes. Proc. Natl. Acad. Sci. U.S.A. 2003;100:13827–13832. PubMed PMC

Davies A.A., Huttner D., Daigaku Y., Chen S., Ulrich H.D. Activation of ubiquitin-dependent DNA damage bypass is mediated by replication protein A. Mol. Cell. 2008;29:625–636. PubMed PMC

New J.H., Sugiyama T., Zaitseva E., Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature. 1998;391:407–410. PubMed

Shinohara A., Ogawa T. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature. 1998;391:404–407. 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

Antunez de Mayolo A., Lisby M., Erdeniz N., Thybo T., Mortensen U.H., Rothstein R. Multiple start codons and phosphorylation result in discrete Rad52 protein species. Nucleic Acids Res. 2006;34:2587–2597. 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

Aylon Y., Liefshitz B., Bitan-Banin G., Kupiec M. Molecular dissection of mitotic recombination in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 2003;23:1403–1417. PubMed PMC

Ira G., Malkova A., Liberi G., Foiani M., Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell. 2003;115:401–411. PubMed PMC

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

Liberi G., Maffioletti G., Lucca C., Chiolo I., Baryshnikova A., Cotta-Ramusino C., Lopes M., Pellicioli A., Haber J.E., 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

Sugawara N., Ira G., Haber J.E. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol. 2000;20:5300–5309. PubMed PMC

Carter S.D., Vigasova D., Chen J., Chovanec M., Astrom S.U. Nej1 recruits the Srs2 helicase to DNA double-strand breaks and supports repair by a single-strand annealing-like mechanism. Proc. Natl. Acad. Sci. U.S.A. 2009;106:12037–12042. PubMed PMC

Wilson T.E. A genomics-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics. 2002;162:677–688. PubMed PMC

Ruiz J.F., Gomez-Gonzalez B., Aguilera A. Chromosomal translocations caused by either pol32-dependent or -independent triparental break-induced replication. Mol. Cell. Biol. 2009 PubMed PMC

Bhattacharyya S., Lahue R.S. Saccharomyces cerevisiae Srs2 DNA helicase selectively blocks expansions of trinucleotide repeats. Mol. Cell. Biol. 2004;24:7324–7330. PubMed PMC

Bhattacharyya S., Lahue R.S. Srs2 helicase of Saccharomyces cerevisiae selectively unwinds triplet repeat DNA. J. Biol. Chem. 2005;280:33311–33317. PubMed

Dhar A., Lahue R.S. Rapid unwinding of triplet repeat hairpins by Srs2 helicase of Saccharomyces cerevisiae. Nucleic Acids Res. 2008;36:3366–3373. PubMed PMC

Kerrest A., Anand R.P., Sundararajan R., Bermejo R., Liberi G., Dujon B., Freudenreich C.H., Richard G.F. SRS2 and SGS1 prevent chromosomal breaks and stabilize triplet repeats by restraining recombination. Nat. Struct. Mol. Biol. 2009;16:159–167. PubMed PMC

Shishkin A.A., Voineagu I., Matera R., Cherng N., Chernet B.T., Krasilnikova M.M., Narayanan V., Lobachev K.S., Mirkin S.M. Large-scale expansions of Friedreich's ataxia GAA repeats in yeast. Mol. Cell. 2009;35:82–92. PubMed PMC

Heude M., Chanet R., Fabre F. Regulation of the Saccharomyces cerevisiae Srs2 helicase during the mitotic cell cycle, meiosis and after irradiation. Mol. Gen. Genet. 1995;248:59–68. PubMed

Hannich J.T., Lewis A., Kroetz M.B., Li S.J., Heide H., Emili A., Hochstrasser M. Defining the SUMO-modified proteome by multiple approaches in Saccharomyces cerevisiae. J. Biol. Chem. 2005;280:4102–4110. PubMed

Hoege C., Pfander B., Moldovan G.L., Pyrowolakis G., Jentsch S. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature. 2002;419:135–141. PubMed

Korolev S., Hsieh J., Gauss G.H., Lohman T.M., Waksman G. Major domain swiveling revealed by the crystal structures of complexes of E. coli Rep helicase bound to single-stranded DNA and ADP. Cell. 1997;90:635–647. PubMed

Lee J.Y., Yang W. UvrD helicase unwinds DNA one base pair at a time by a two-part power stroke. Cell. 2006;127:1349–1360. PubMed PMC

Velankar S.S., Soultanas P., Dillingham M.S., Subramanya H.S., Wigley D.B. Crystal structures of complexes of PcrA DNA helicase with a DNA substrate indicate an inchworm mechanism. Cell. 1999;97:75–84. PubMed

Flores M.J., Bidnenko V., Michel B. The DNA repair helicase UvrD is essential for replication fork reversal in replication mutants. EMBO Rep. 2004;5:983–988. PubMed PMC

Veaute X., Delmas S., Selva M., Jeusset J., Le Cam E., Matic I., Fabre F., Petit M.A. UvrD helicase, unlike rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J. 2005;24:180–189. PubMed PMC

Maftahi M., Hope J.C., Delgado-Cruzata L., Han C.S., Freyer G.A. The severe slow growth of Deltasrs2 Deltarqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes. Nucleic Acids Res. 2002;30:4781–4792. PubMed PMC

Wang S.W., Goodwin A., Hickson I.D., Norbury C.J. Involvement of Schizosaccharomyces pombe Srs2 in cellular responses to DNA damage. Nucleic Acids Res. 2001;29:2963–2972. PubMed PMC

Doe C.L., Whitby M.C. The involvement of Srs2 in post-replication repair and homologous recombination in fission yeast. Nucleic Acids Res. 2004;32:1480–1491. PubMed PMC

Kohzaki M., Hatanaka A., Sonoda E., Yamazoe M., Kikuchi K., Vu Trung N., Szuts D., Sale J.E., Shinagawa H., Watanabe M., Takeda S. Cooperative roles of vertebrate Fbh1 and Blm DNA helicases in avoidance of crossovers during recombination initiated by replication fork collapse. Mol. Cell. Biol. 2007;27:2812–2820. PubMed PMC

Lorenz A., Osman F., Folkyte V., Sofueva S., Whitby M.C. Fbh1 limits Rad51-dependent recombination at blocked replication forks. Mol. Cell. Biol. 2009;29:4742–4756. PubMed PMC

Morishita T., Furukawa F., Sakaguchi C., Toda T., Carr A.M., 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 A.R., Whitby M.C. The F-box DNA helicase Fbh1 prevents Rhp51-dependent recombination without mediator proteins. Mol. Cell. Biol. 2005;25:8084–8096. PubMed PMC

Chiolo I., Saponaro M., Baryshnikova A., Kim J.H., Seo Y.S., 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

Richard G.F., Kerrest A., Lafontaine I., Dujon B. Comparative genomics of hemiascomycete yeasts: genes involved in DNA replication, repair, and recombination. Mol. Biol. Evol. 2005;22:1011–1023. PubMed

Hu Y., Raynard S., Sehorn M.G., Lu X., Bussen W., Zheng L., Stark J.M., Barnes E.L., Chi P., Janscak P., Jasin M., Vogel H., Sung P., Luo G. RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. Genes Dev. 2007;21:3073–3084. PubMed PMC

Bugreev D.V., Yu X., Egelman E.H., Mazin A.V. Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. Genes Dev. 2007;21:3085–3094. PubMed PMC

Robu M.E., Inman R.B., Cox M.M. RecA protein promotes the regression of stalled replication forks in vitro. Proc. Natl. Acad. Sci. U.S.A. 2001;98:8211–8218. PubMed PMC

Seigneur M., Ehrlich S.D., Michel B. RuvABC-dependent double-strand breaks in dnaBts mutants require recA. Mol. Microbiol. 2000;38:565–574. PubMed

The PCNA-associated protein PARI negatively regulates homologous recombination via the inhibition of DNA repair synthesis

Pro-recombination Role of Srs2 Protein Requires SUMO (Small Ubiquitin-like Modifier) but Is Independent of PCNA (Proliferating Cell Nuclear Antigen) Interaction

Srs2 promotes Mus81-Mms4-mediated resolution of recombination intermediates

Srs2 mediates PCNA-SUMO-dependent inhibition of DNA repair synthesis

Unwinding of synthetic replication and recombination substrates by Srs2

Dual roles of the SUMO-interacting motif in the regulation of Srs2 sumoylation

Homologous recombination and its regulation

Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities

Rad52 SUMOylation affects the efficiency of the DNA repair