Homologous recombination and its regulation

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.

[1]  Penny A. Johnson,et al.  XRCC3 and Rad51 modulate replication fork progression on damaged vertebrate chromosomes. , 2003, Molecular cell.

[2]  M. Jasin,et al.  Role for the Mammalian Swi5-Sfr1 Complex in DNA Strand Break Repair through Homologous Recombination , 2010, PLoS genetics.

[3]  Y. Tsutsui,et al.  The Swi5–Sfr1 complex stimulates Rhp51/Rad51 - and Dmc1-mediated DNA strand exchange in vitro , 2006, Nature Structural &Molecular Biology.

[4]  M. Colaiácovo,et al.  Distribution of meiotic recombination events: talking to your neighbors. , 2009, Current opinion in genetics & development.

[5]  E. Egelman,et al.  Similarity of the yeast RAD51 filament to the bacterial RecA filament. , 1993, Science.

[6]  S. West,et al.  The breast cancer tumor suppressor BRCA2 promotes the specific targeting of RAD51 to single-stranded DNA , 2010, Nature Structural &Molecular Biology.

[7]  Tom L. Blundell,et al.  Insights into DNA recombination from the structure of a RAD51–BRCA2 complex , 2002, Nature.

[8]  N. Pavletich,et al.  Mechanism of homologous recombination from the RecA–ssDNA/dsDNA structures , 2008, Nature.

[9]  P. Plevani,et al.  Overlapping mechanisms promote postsynaptic RAD-51 filament disassembly during meiotic double-strand break repair. , 2010, Molecular cell.

[10]  Wen-Hwa Lee,et al.  BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. , 2002, Science.

[11]  Jiri Bartek,et al.  The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair , 2005, Nature Cell Biology.

[12]  Franca Fraternali,et al.  Mutation of the RAD51C gene in a Fanconi anemia–like disorder , 2010, Nature Genetics.

[13]  T. Allers,et al.  Differential Timing and Control of Noncrossover and Crossover Recombination during Meiosis , 2001, Cell.

[14]  L. Symington,et al.  Recombination proteins in yeast. , 2004, Annual review of genetics.

[15]  M. J. Neale,et al.  Clarifying the mechanics of DNA strand exchange in meiotic recombination , 2006, Nature.

[16]  Rohit Prakash,et al.  Mechanism of the ATP-dependent DNA end-resection machinery from Saccharomyces cerevisiae , 2010, Nature.

[17]  R. Holliday,et al.  The homologous recombination system of Ustilago maydis. , 2008, Fungal genetics and biology : FG & B.

[18]  P. Sung,et al.  Superhelicity-driven homologous DNA pairing by yeast recombination factors Rad51 and Rad54. , 2000, Molecular cell.

[19]  Michael G. Sehorn,et al.  Bipartite stimulatory action of the Hop2-Mnd1 complex on the Rad51 recombinase. , 2007, Genes & development.

[20]  I. Hickson,et al.  Yeast as a model system to study RecQ helicase function. , 2010, DNA repair.

[21]  T. Lohman,et al.  Srs2 disassembles Rad51 filaments by a protein-protein interaction triggering ATP turnover and dissociation of Rad51 from DNA. , 2009, Molecular cell.

[22]  Rajan P. Kulkarni,et al.  DNA damage regulates the mobility of Brca2 within the nucleoplasm of living cells , 2010, Proceedings of the National Academy of Sciences.

[23]  Jeffrey N. Carey,et al.  Swi2/Snf2-related translocases prevent accumulation of toxic Rad51 complexes during mitotic growth. , 2010, Molecular cell.

[24]  Jason Liang,et al.  A Proteome-wide Analysis of Kinase-Substrate Network in the DNA Damage Response* , 2010, The Journal of Biological Chemistry.

[25]  R. Wysocki,et al.  The Swi2–Snf2-like protein Uls1 is involved in replication stress response , 2011, Nucleic acids research.

[26]  S. Kowalczykowski,et al.  DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[27]  A. Lau,et al.  Selective Inhibition of BRCA2-Deficient Mammary Tumor Cell Growth by AZD2281 and Cisplatin , 2008, Clinical Cancer Research.

[28]  P. Sung,et al.  Interaction with RPA Is Necessary for Rad52 Repair Center Formation and for Its Mediator Activity* , 2008, Journal of Biological Chemistry.

[29]  S. West,et al.  Visualization of recombination intermediates produced by RAD52‐mediated single‐strand annealing , 2001, EMBO reports.

[30]  M. Ikeguchi,et al.  Two different Swi5-containing protein complexes are involved in mating-type switching and recombination repair in fission yeast , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[31]  S. Jackson,et al.  Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks , 2009, Nature.

[32]  Ian D. Hickson,et al.  RecQ helicases: multifunctional genome caretakers , 2009, Nature Reviews Cancer.

[33]  Henning Stahlberg,et al.  Rad51 paralogs Rad55-Rad57 balance the anti-recombinase Srs2 in Rad51 filament formation , 2011, Nature.

[34]  S. Jentsch,et al.  Control of Rad52 recombination activity by double-strand break-induced SUMO modification , 2006, Nature Cell Biology.

[35]  Erik Hollnagel Att förstå olyckor : lätt att bli syndabock i "effektiv" organisation , 2010 .

[36]  L. Symington,et al.  The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing. , 2001, Genetics.

[37]  R. Rothstein,et al.  Multiple start codons and phosphorylation result in discrete Rad52 protein species , 2006, Nucleic acids research.

[38]  Hans Joenje,et al.  Biallelic Inactivation of BRCA2 in Fanconi Anemia , 2002, Science.

[39]  G. Luo,et al.  A Blm-Recql5 partnership in replication stress response. , 2011, Journal of molecular cell biology.

[40]  Michael G. Sehorn,et al.  Hed1 regulates Rad51-mediated recombination via a novel mechanism. , 2008, Genes & development.

[41]  F. Z. Watts,et al.  SUMO modification of Rad22, the Schizosaccharomyces pombe homologue of the recombination protein Rad52. , 2001, Nucleic acids research.

[42]  L. Symington,et al.  Rad51 gain-of-function mutants that exhibit high affinity DNA binding cause DNA damage sensitivity in the absence of Srs2 , 2008, Nucleic acids research.

[43]  A. Shinohara,et al.  Crossover interference in Saccharomyces cerevisiae requires a TID1/RDH54- and DMC1-dependent pathway. , 2003, Genetics.

[44]  M. Handel,et al.  Meiotic prophase arrest with failure of chromosome synapsis in mice deficient for Dmc1, a germline-specific RecA homolog. , 1998, Molecular cell.

[45]  Jeremy M. Stark,et al.  Rad51 overexpression promotes alternative double-strand break repair pathways and genome instability , 2004, Oncogene.

[46]  S. Smerdon,et al.  Plk1 and CK2 Act in Concert to Regulate Rad51 during DNA Double Strand Break Repair , 2012, Molecular cell.

[47]  Ina Ruck,et al.  USA , 1969, The Lancet.

[48]  J. Buerstedde,et al.  Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. , 1997, Genetics.

[49]  P. Sung,et al.  MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. , 2010, Molecular cell.

[50]  P. Hieter,et al.  Specific synthetic lethal killing of RAD54B-deficient human colorectal cancer cells by FEN1 silencing , 2009, Proceedings of the National Academy of Sciences.

[51]  C. Liao,et al.  RAD51C facilitates checkpoint signaling by promoting CHK2 phosphorylation , 2009, The Journal of cell biology.

[52]  Wolf-Dietrich Heyer,et al.  Rad54: the Swiss Army knife of homologous recombination? , 2006, Nucleic acids research.

[53]  T. Helleday,et al.  Hydroxyurea-Stalled Replication Forks Become Progressively Inactivated and Require Two Different RAD51-Mediated Pathways for Restart and Repair , 2010, Molecular cell.

[54]  Michael G. Sehorn,et al.  Human meiotic recombinase Dmc1 promotes ATP-dependent homologous DNA strand exchange , 2004, Nature.

[55]  S. Kowalczykowski,et al.  Two classes of BRC repeats in BRCA2 promote RAD51 nucleoprotein filament function by distinct mechanisms , 2011, Proceedings of the National Academy of Sciences.

[56]  Akira Shinohara,et al.  A Protein Complex Containing Mei5 and Sae3 Promotes the Assembly of the Meiosis-Specific RecA Homolog Dmc1 , 2004, Cell.

[57]  Eleni P. Mimitou,et al.  Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing , 2008, Nature.

[58]  Ken‐ichi Yamamoto,et al.  Detection of c‐Abl kinase‐promoted phosphorylation of Rad51 by specific antibodies reveals that Y54 phosphorylation is dependent on that of Y315 , 2009, FEBS letters.

[59]  N. Sternberg,et al.  Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process , 1984, Molecular and cellular biology.

[60]  P. Sung,et al.  Regulation of Rad51 Function by c-Abl in Response to DNA Damage* , 1998, The Journal of Biological Chemistry.

[61]  Stephen L. Gasior,et al.  Tid1/Rdh54 promotes colocalization of rad51 and dmc1 during meiotic recombination. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[62]  G. Gloor,et al.  Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair , 1994, Molecular and cellular biology.

[63]  D. Huo,et al.  SUMO Modification Regulates BLM and RAD51 Interaction at Damaged Replication Forks , 2009, PLoS biology.

[64]  F. Klein,et al.  Mnd1 Is Required for Meiotic Interhomolog Repair , 2004, Current Biology.

[65]  W. Xiao,et al.  The yeast Shu complex couples error‐free post‐replication repair to homologous recombination , 2009, Molecular microbiology.

[66]  C. Toniatti,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. , 2009, Journal of medicinal chemistry.

[67]  F. Couch,et al.  Control of BRCA2 cellular and clinical functions by a nuclear partner, PALB2. , 2006, Molecular cell.

[68]  S. West,et al.  RAD51C deficiency in mice results in early prophase I arrest in males and sister chromatid separation at metaphase II in females , 2007, The Journal of cell biology.

[69]  Jorge S. Reis-Filho,et al.  Resistance to therapy caused by intragenic deletion in BRCA2 , 2008, Nature.

[70]  H. Kitao,et al.  Regulation of Ionizing Radiation-induced Rad52 Nuclear Foci Formation by c-Abl-mediated Phosphorylation* , 2002, The Journal of Biological Chemistry.

[71]  T. Chou,et al.  Physics of RecA-mediated homologous recognition. , 2004, Biophysical journal.

[72]  T. Schüpbach,et al.  Drosophila brca2 Is Required for Mitotic and Meiotic DNA Repair and Efficient Activation of the Meiotic Recombination Checkpoint , 2008, PLoS genetics.

[73]  W. Chazin,et al.  Function of a Conserved Checkpoint Recruitment Domain in ATRIP Proteins , 2007, Molecular and Cellular Biology.

[74]  Neil Hunter,et al.  BLM Ortholog, Sgs1, Prevents Aberrant Crossing-over by Suppressing Formation of Multichromatid Joint Molecules , 2007, Cell.

[75]  P. Sung,et al.  Mechanism of homologous recombination: mediators and helicases take on regulatory functions , 2006, Nature Reviews Molecular Cell Biology.

[76]  S C West,et al.  BRCA2: a universal recombinase regulator , 2007, Oncogene.

[77]  Boris Pfander,et al.  SUMO-modified PCNA recruits Srs2 to prevent recombination during S phase , 2005, Nature.

[78]  Hideo Tsubouchi,et al.  The Budding Yeast Mei5 and Sae3 Proteins Act Together With Dmc1 During Meiotic Recombination , 2004, Genetics.

[79]  W. V. D. Van de Ven,et al.  Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. , 1999, Cancer research.

[80]  Tomohiko Sugiyama,et al.  The Recombination-deficient Mutant RPA (rfa1-t11) Is Displaced Slowly from Single-stranded DNA by Rad51 Protein* , 2003, Journal of Biological Chemistry.

[81]  J. Haber,et al.  Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Neil Hunter,et al.  RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. , 2008, Molecular cell.

[83]  J. T. Kadonaga,et al.  Strand pairing by Rad54 and Rad51 is enhanced by chromatin. , 2002, Genes & development.

[84]  F. Couch,et al.  Secondary mutations as a mechanism of cisplatin resistance in BRCA2-mutated cancers , 2008, Nature.

[85]  T. Toda,et al.  Role of the Schizosaccharomyces pombe F-Box DNA Helicase in Processing Recombination Intermediates , 2005, Molecular and Cellular Biology.

[86]  M. Foiani,et al.  The checkpoint response to replication stress. , 2009, DNA repair.

[87]  S. Kowalczykowski,et al.  DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2 , 2010, Nature.

[88]  Z. Cao,et al.  Dss1 Interaction with Brh2 as a Regulatory Mechanism for Recombinational Repair , 2007, Molecular and Cellular Biology.

[89]  David Klenerman,et al.  The BRC repeats of human BRCA2 differentially regulate RAD51 binding on single- versus double-stranded DNA to stimulate strand exchange , 2009, Proceedings of the National Academy of Sciences.

[90]  D. K. Bishop,et al.  Red-Hed regulation: recombinase Rad51, though capable of playing the leading role, may be relegated to supporting Dmc1 in budding yeast meiosis. , 2006, Genes & development.

[91]  G. Peng,et al.  BRIT1/MCPH1 Is Essential for Mitotic and Meiotic Recombination DNA Repair and Maintaining Genomic Stability in Mice , 2010, PLoS genetics.

[92]  G. Simchen,et al.  Sister chromatid‐based DNA repair is mediated by RAD54, not by DMC1 or TID1 , 1999, The EMBO journal.

[93]  Janice P. Evans,et al.  BRCA2 deficiency in mice leads to meiotic impairment and infertility , 2004, Development.

[94]  J. Griffin,et al.  BCR-ABL promotes the frequency of mutagenic single-strand annealing DNA repair. , 2009, Blood.

[95]  H. Olivares,et al.  Tid1/Rdh54 promotes dissociation of Dmc1 from nonrecombinogenic sites on meiotic chromatin. , 2006, Genes & development.

[96]  D. Ward,et al.  Mammalian ubiquitin-conjugating enzyme Ubc9 interacts with Rad51 recombination protein and localizes in synaptonemal complexes. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[97]  Jeremy M. Stark,et al.  Suppression of the DNA repair defects of BRCA2-deficient cells with heterologous protein fusions. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[98]  G. Roeder,et al.  The Meiosis-Specific Hop2 Protein of S. cerevisiae Ensures Synapsis between Homologous Chromosomes , 1998, Cell.

[99]  Stephen C. West,et al.  RTEL1 Maintains Genomic Stability by Suppressing Homologous Recombination , 2008, Cell.

[100]  A. Stasiak,et al.  Activation of Human Meiosis-specific Recombinase Dmc1 by Ca2+* , 2005, Journal of Biological Chemistry.

[101]  P. Sung Function of Yeast Rad52 Protein as a Mediator between Replication Protein A and the Rad51 Recombinase* , 1997, The Journal of Biological Chemistry.

[102]  A. Egashira,et al.  Double-Strand Break Repair-Independent Role for BRCA2 in Blocking Stalled Replication Fork Degradation by MRE11 , 2011, Cell.

[103]  Jiri Bartek,et al.  Human Fbh1 helicase contributes to genome maintenance via pro- and anti-recombinase activities , 2009, The Journal of cell biology.

[104]  Charles Boone,et al.  RMI1/NCE4, a suppressor of genome instability, encodes a member of the RecQ helicase/Topo III complex , 2005 .

[105]  I. Hickson,et al.  Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. , 2007, Molecular biology of the cell.

[106]  Michael G. Sehorn,et al.  RECQL5/Recql5 helicase regulates homologous recombination and suppresses tumor formation via disruption of Rad51 presynaptic filaments. , 2007, Genes & development.

[107]  J. Derisi,et al.  Mnd1p: An evolutionarily conserved protein required for meiotic recombination , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[108]  Xiaolan Zhao,et al.  A SUMO ligase is part of a nuclear multiprotein complex that affects DNA repair and chromosomal organization. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[109]  M. Doutriaux,et al.  Interaction between Arabidopsis Brca2 and Its Partners Rad51, Dmc1, and Dss11 , 2006, Plant Physiology.

[110]  P. Sung,et al.  Yeast Recombination Factor Rdh54 Functionally Interacts with the Rad51 Recombinase and Catalyzes Rad51 Removal from DNA* , 2006, Journal of Biological Chemistry.

[111]  Y. Furuichi,et al.  Covalent Modification of the Werner's Syndrome Gene Product with the Ubiquitin-related Protein, SUMO-1* , 2000, The Journal of Biological Chemistry.

[112]  S. West,et al.  Human Dmc1 protein binds DNA as an octameric ring. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[113]  Paul Liu,et al.  brca2 in zebrafish ovarian development, spermatogenesis, and tumorigenesis , 2010, Proceedings of the National Academy of Sciences.

[114]  M. Chovanec,et al.  DNA double-strand break repair by homologous recombination. , 2004, Mutation research.

[115]  M. Rice,et al.  Disruption of muREC2/RAD51L1 in Mice Results in Early Embryonic Lethality Which Can Be Partially Rescued in a p53−/− Background , 1999, Molecular and Cellular Biology.

[116]  W. Kaelin The Concept of Synthetic Lethality in the Context of Anticancer Therapy , 2005, Nature Reviews Cancer.

[117]  Carol Kolar,et al.  Human Replication Protein A−Rad52−Single-Stranded DNA Complex: Stoichiometry and Evidence for Strand Transfer Regulation by Phosphorylation† , 2009, Biochemistry.

[118]  Xiaolan Zhao,et al.  Extensive DNA damage-induced sumoylation contributes to replication and repair and acts in addition to the mec1 checkpoint. , 2012, Molecular cell.

[119]  S. West,et al.  Role of RAD51C and XRCC3 in Genetic Recombination and DNA Repair* , 2007, Journal of Biological Chemistry.

[120]  Jack W. Szostak,et al.  The double-strand-break repair model for recombination , 1983, Cell.

[121]  A. Look,et al.  CHK1 inhibition as a strategy for targeting fanconi anemia (FA) DNA repair pathway deficient tumors , 2009, Molecular Cancer.

[122]  M. Whitby,et al.  The F-Box DNA Helicase Fbh1 Prevents Rhp51-Dependent Recombination without Mediator Proteins , 2005, Molecular and Cellular Biology.

[123]  S. West,et al.  DNA repair synthesis facilitates RAD52-mediated second-end capture during DSB repair. , 2008, Molecular cell.

[124]  Gary S. Fortin,et al.  Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51–DNA complexes , 2002, The EMBO journal.

[125]  K. Nakao,et al.  Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[126]  Jiri Bartek,et al.  An Oncogene-Induced DNA Damage Model for Cancer Development , 2008, Science.

[127]  Thomas Helleday,et al.  Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADP-ribose) polymerase , 2005, Nature.

[128]  M. Adams,et al.  Drosophila BLM in Double-Strand Break Repair by Synthesis-Dependent Strand Annealing , 2003, Science.

[129]  S. Kowalczykowski,et al.  Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1–Top3 , 2010, Nature Structural &Molecular Biology.

[130]  H. Ogiwara,et al.  Rad52 sumoylation and its involvement in the efficient induction of homologous recombination. , 2008, DNA repair.

[131]  P. Sung,et al.  Rad54p Is a Chromatin Remodeling Enzyme Required for Heteroduplex DNA Joint Formation with Chromatin* , 2003, The Journal of Biological Chemistry.

[132]  P. Sung,et al.  Mechanism of eukaryotic homologous recombination. , 2008, Annual review of biochemistry.

[133]  Xiaolan Zhao,et al.  The Smc5/6 Complex and Esc2 Influence Multiple Replication-associated Recombination Processes in Saccharomyces cerevisiae , 2010, Molecular biology of the cell.

[134]  K. Ohta,et al.  Accumulation of sumoylated Rad52 in checkpoint mutants perturbed in DNA replication. , 2009, DNA repair.

[135]  C. Barlow,et al.  Loss of Rad52 partially rescues tumorigenesis and T-cell maturation in Atm-deficient mice , 2004, Oncogene.

[136]  J. Haber,et al.  Multiple Pathways of Recombination Induced by Double-Strand Breaks in Saccharomyces cerevisiae , 1999, Microbiology and Molecular Biology Reviews.

[137]  R. Camerini-Otero,et al.  Hop2-Mnd1 condenses DNA to stimulate the synapsis phase of DNA strand exchange. , 2010, Biophysical journal.

[138]  Jay M. Sage,et al.  Discovery of a Novel Function for Human Rad51 , 2010, The Journal of Biological Chemistry.

[139]  Junjie Chen,et al.  The Role of the Human SWI5-MEI5 Complex in Homologous Recombination Repair* , 2011, The Journal of Biological Chemistry.

[140]  W. Foulkes,et al.  BRCA1 and BRCA2: 1994 and beyond , 2004, Nature Reviews Cancer.

[141]  T. Pandita,et al.  hSSB1 and hSSB2 Form Similar Multiprotein Complexes That Participate in DNA Damage Response* , 2009, The Journal of Biological Chemistry.

[142]  Jeroen A. A. Demmers,et al.  RAD51AP1 is a structure-specific DNA binding protein that stimulates joint molecule formation during RAD51-mediated homologous recombination. , 2007, Molecular cell.

[143]  Catherine A. Wilson,et al.  Roles of brca2 (fancd1) in Oocyte Nuclear Architecture, Gametogenesis, Gonad Tumors, and Genome Stability in Zebrafish , 2011, PLoS genetics.

[144]  Erica S. Johnson,et al.  Ubiquitin-dependent Proteolytic Control of SUMO Conjugates* , 2007, Journal of Biological Chemistry.

[145]  P. Sung,et al.  Regulation of Rad51 Recombinase Presynaptic Filament Assembly via Interactions with the Rad52 Mediator and the Srs2 Anti-recombinase* , 2009, The Journal of Biological Chemistry.

[146]  A. Fersht,et al.  Mapping the physical and functional interactions between the tumor suppressors p53 and BRCA2 , 2010, Proceedings of the National Academy of Sciences.

[147]  R. Chanet,et al.  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 , 2004, Molecular and Cellular Biology.

[148]  P. Sung,et al.  Functional Interactions among Yeast Rad51 Recombinase, Rad52 Mediator, and Replication Protein A in DNA Strand Exchange* , 2000, The Journal of Biological Chemistry.

[149]  P. Sung Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. , 1997, Genes & development.

[150]  Gerald R. Smith,et al.  Swi5 Acts in Meiotic DNA Joint Molecule Formation in Schizosaccharomyces pombe , 2004, Genetics.

[151]  L. Symington,et al.  Copyright � 1995, American Society for Microbiology Functional Differences and Interactions among the Putative , 1995 .

[152]  N. Galjart,et al.  Differential Contributions of Mammalian Rad54 Paralogs to Recombination, DNA Damage Repair, and Meiosis , 2006, Molecular and Cellular Biology.

[153]  C. Eaves,et al.  BCR/ABL and other kinases from chronic myeloproliferative disorders stimulate single-strand annealing, an unfaithful DNA double-strand break repair. , 2008, Cancer research.

[154]  Shunichi Takeda,et al.  Single-stranded DNA-binding protein hSSB1 is critical for genomic stability , 2008, Nature.

[155]  W. Holloman,et al.  Unraveling the mechanism of BRCA2 in homologous recombination , 2011, Nature Structural &Molecular Biology.

[156]  W. Heyer,et al.  Regulation of homologous recombination in eukaryotes. , 2010, Annual review of genetics.

[157]  P. Dhar,et al.  Rad52 partially substitutes for the Rad51 paralog XRCC3 in maintaining chromosomal integrity in vertebrate cells , 2001, The EMBO journal.

[158]  F. Fabre,et al.  Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases , 2000, Nature Genetics.

[159]  W. Heyer,et al.  Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. , 2002, Molecular cell.

[160]  S. Gonzalo,et al.  The role of RPA2 phosphorylation in homologous recombination in response to replication arrest. , 2010, Carcinogenesis.

[161]  S. West,et al.  CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair , 2005, Nature.

[162]  J. Albala,et al.  The Rad51 Paralog Rad51B Promotes Homologous Recombinational Repair , 2000, Molecular and Cellular Biology.

[163]  Luca Pellegrini,et al.  Interaction with the BRCA2 C terminus protects RAD51–DNA filaments from disassembly by BRC repeats , 2007, Nature Structural &Molecular Biology.

[164]  S. Jackson,et al.  Regulation of Rad51 function by phosphorylation , 2011, EMBO reports.

[165]  J. Haber,et al.  Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. , 2009, Genes & development.

[166]  Ashok R. Venkitaraman,et al.  The BRC Repeats of BRCA2 Modulate the DNA-Binding Selectivity of RAD51 , 2009, Cell.

[167]  L. Haracska,et al.  Reconstitution of DNA repair synthesis in vitro and the role of polymerase and helicase activities , 2011, DNA repair.

[168]  J. Yates,et al.  Sws1 is a conserved regulator of homologous recombination in eukaryotic cells , 2006, The EMBO journal.

[169]  N. Mazloum,et al.  Dss1 regulates interaction of Brh2 with DNA. , 2009, Biochemistry.

[170]  R. Camerini-Otero,et al.  Hop2/Mnd1 acts on two critical steps in Dmc1-promoted homologous pairing. , 2007, Genes & development.

[171]  A. Stasiak,et al.  Purification and characterization of the human Rad51 protein, an analogue of E. coli RecA. , 1994, The EMBO journal.

[172]  A. Alexeev,et al.  Rad54 protein possesses chromatin-remodeling activity stimulated by the Rad51–ssDNA nucleoprotein filament , 2003, Nature Structural Biology.

[173]  P. Sung,et al.  Functional significance of the Rad51-Srs2 complex in Rad51 presynaptic filament disruption , 2009, Nucleic acids research.

[174]  J. Braybrooke,et al.  The RAD51 Family Member, RAD51L3, Is a DNA-stimulated ATPase That Forms a Complex with XRCC2* , 2000, The Journal of Biological Chemistry.

[175]  Robert M Brosh,et al.  FANCJ Uses Its Motor ATPase to Destabilize Protein-DNA Complexes, Unwind Triplexes, and Inhibit RAD51 Strand Exchange* , 2009, Journal of Biological Chemistry.

[176]  R. Rothstein,et al.  A Genetic Screen for top3 Suppressors in Saccharomyces cerevisiae Identifies SHU1, SHU2, PSY3 and CSM2 , 2005, Genetics.

[177]  J. Haber,et al.  In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. , 2003, Molecular cell.

[178]  Ying Li,et al.  DNA helicase Srs2 disrupts the Rad51 presynaptic filament , 2003, Nature.

[179]  K. Hofmann,et al.  Inhibition of homologous recombination by the PCNA-interacting protein PARI. , 2012, Molecular cell.

[180]  P. Hasty,et al.  A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53 , 1996, Molecular and cellular biology.

[181]  H. Saitoh,et al.  Perturbation of SUMOlation Enzyme Ubc9 by Distinct Domain within Nucleoporin RanBP2/Nup358* , 2002, The Journal of Biological Chemistry.

[182]  Ian D. Hickson,et al.  The Bloom's syndrome helicase suppresses crossing over during homologous recombination , 2003, Nature.

[183]  M. F. White,et al.  hSSB1 interacts directly with the MRN complex stimulating its recruitment to DNA double-strand breaks and its endo-nuclease activity , 2011, Nucleic acids research.

[184]  A. Shinohara,et al.  Stimulation by Rad52 of yeast Rad51- mediated recombination , 1998, Nature.

[185]  M. Ikeguchi,et al.  Fission yeast Swi5/Sfr1 and Rhp55/Rhp57 differentially regulate Rhp51‐dependent recombination outcomes , 2007, The EMBO journal.

[186]  S. Aaronson,et al.  BRCA2 Is Ubiquitinated In Vivo and Interacts with USP11, a Deubiquitinating Enzyme That Exhibits Prosurvival Function in the Cellular Response to DNA Damage , 2004, Molecular and Cellular Biology.

[187]  J. Thacker The RAD51 gene family, genetic instability and cancer. , 2005, Cancer letters.

[188]  P. Sung,et al.  Effects of Tumor-associated Mutations on Rad54 Functions* , 2004, Journal of Biological Chemistry.

[189]  F. Matsuda,et al.  Genetic investigation of four meiotic genes in women with premature ovarian failure. , 2008, European journal of endocrinology.

[190]  R. Rothstein,et al.  The Slx5-Slx8 Complex Affects Sumoylation of DNA Repair Proteins and Negatively Regulates Recombination , 2007, Molecular and Cellular Biology.

[191]  Robert J. D. Reid,et al.  The Smc5–Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus , 2007, Nature Cell Biology.

[192]  J. D'Orazio,et al.  DNA repair pathways and hereditary cancer susceptibility syndromes. , 2007, Frontiers in bioscience : a journal and virtual library.

[193]  S. West,et al.  Structure of the single-strand annealing domain of human RAD52 protein , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[194]  H. Klein,et al.  RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. , 1997, Genetics.

[195]  Yoshino Kubota,et al.  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 , 2010, Molecular and Cellular Biology.

[196]  D. Schild,et al.  Mutants of the Five Rad51 Paralogs Recombinational Repair in Knockout Chromosome Instability and Defective , 2022 .

[197]  David J. Chen,et al.  hSSB1 rapidly binds at the sites of DNA double-strand breaks and is required for the efficient recruitment of the MRN complex , 2010, Nucleic acids research.

[198]  M. Whitby The FANCM family of DNA helicases/translocases. , 2010, DNA repair.

[199]  R. Rothstein,et al.  Rad52 recruitment is DNA replication independent and regulated by Cdc28 and the Mec1 kinase , 2009, The EMBO journal.

[200]  Michael G. Sehorn,et al.  Functional interactions of meiotic recombination factors Rdh54 and Dmc1. , 2009, DNA repair.

[201]  Robert J. D. Reid,et al.  The Shu complex, which contains Rad51 paralogues, promotes DNA repair through inhibition of the Srs2 anti-recombinase , 2011, Molecular biology of the cell.

[202]  Ricky A. Sharma,et al.  Molecular and Cellular Pathobiology Cancer Research Poly ( ADP-Ribose ) Polymerase Is Hyperactivated in Homologous Recombination – Defective Cells , 2010 .

[203]  J. Yates,et al.  Phosphorylation of Rad55 on Serines 2, 8, and 14 Is Required for Efficient Homologous Recombination in the Recovery of Stalled Replication Forks , 2006, Molecular and Cellular Biology.

[204]  F. Fabre,et al.  The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments , 2003, Nature.

[205]  L. Symington,et al.  Role of the Saccharomyces cerevisiae Rad51 Paralogs in Sister Chromatid Recombination , 2008, Genetics.

[206]  W. Heyer,et al.  DNA Repair Protein Rad55 Is a Terminal Substrate of the DNA Damage Checkpoints , 2000, Molecular and Cellular Biology.

[207]  D. Schild,et al.  Overexpression of RAD51 suppresses recombination defects: a possible mechanism to reverse genomic instability , 2009, Nucleic Acids Research.

[208]  T. Lange,et al.  Homologous Recombination Generates T-Loop-Sized Deletions at Human Telomeres , 2004, Cell.

[209]  M. Whitby,et al.  Fbh1 Limits Rad51-Dependent Recombination at Blocked Replication Forks , 2009, Molecular and Cellular Biology.

[210]  Zhiyuan Shen,et al.  Distinct RAD51 associations with RAD52 and BCCIP in response to DNA damage and replication stress. , 2008, Cancer research.

[211]  M. Adams,et al.  Formation of deletions during double-strand break repair in Drosophila DmBlm mutants occurs after strand invasion. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[212]  R. Rothstein,et al.  A molecular genetic dissection of the evolutionarily conserved N terminus of yeast Rad52. , 2002, Genetics.

[213]  Melanie Keppler,et al.  The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress , 2009, Nature.

[214]  W. Heyer,et al.  Biochemistry of Meiotic Recombination: Formation, Processing, and Resolution of Recombination Intermediates. , 2008, Genome dynamics and stability.

[215]  P. Sung,et al.  Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. , 2003, Molecular cell.

[216]  N. Kleckner,et al.  DMC1: A meiosis-specific yeast homolog of E. coli recA required for recombination, synaptonemal complex formation, and cell cycle progression , 1992, Cell.

[217]  P. Sung,et al.  Functional Cross-talk among Rad51, Rad54, and Replication Protein A in Heteroduplex DNA Joint Formation* , 2002, The Journal of Biological Chemistry.

[218]  H. Kurumizaka,et al.  From meiosis to postmeiotic events: Uncovering the molecular roles of the meiosis‐specific recombinase Dmc1 , 2010, The FEBS journal.

[219]  O. Mazina,et al.  Rad54, the motor of homologous recombination. , 2010, DNA repair.

[220]  A. Shinohara,et al.  Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein , 1992, Cell.

[221]  Dieter Niederacher,et al.  Germline mutations in breast and ovarian cancer pedigrees establish RAD51C as a human cancer susceptibility gene , 2010, Nature Genetics.

[222]  S. Teng,et al.  Sumoylation of the BLM ortholog, Sgs1, promotes telomere–telomere recombination in budding yeast , 2009, Nucleic acids research.

[223]  M. Lopes,et al.  Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. , 2005, Genes & development.

[224]  Michael G. Sehorn,et al.  Molecular Anatomy of the Recombination Mediator Function of Saccharomyces cerevisiae Rad52* , 2008, Journal of Biological Chemistry.

[225]  H. Puchta,et al.  The role of DNA helicases and their interaction partners in genome stability and meiotic recombination in plants. , 2011, Journal of experimental botany.

[226]  Lajos Haracska,et al.  Role of yeast Rad5 and its human orthologs, HLTF and SHPRH in DNA damage tolerance. , 2010, DNA repair.

[227]  M. Whitby,et al.  The FANCM Ortholog Fml1 Promotes Recombination at Stalled Replication Forks and Limits Crossing Over during DNA Double-Strand Break Repair , 2008, Molecular cell.

[228]  P. Bray-Ward,et al.  A novel nucleic acid-binding protein that interacts with human rad51 recombinase. , 1997, Nucleic acids research.

[229]  Y. Li,et al.  Role of ATP Hydrolysis in the Antirecombinase Function of Saccharomyces cerevisiae Srs2 Protein* , 2004, Journal of Biological Chemistry.

[230]  P. Sung,et al.  Promotion of homologous recombination and genomic stability by RAD51AP1 via RAD51 recombinase enhancement. , 2007, Molecular cell.

[231]  P. Sung,et al.  Role of the Rad52 Amino-terminal DNA Binding Activity in DNA Strand Capture in Homologous Recombination* , 2009, The Journal of Biological Chemistry.

[232]  V. Bohr,et al.  Roles of Werner syndrome protein in protection of genome integrity. , 2010, DNA repair.

[233]  A. Nicolas,et al.  A genomewide screen in Saccharomyces cerevisiae for genes that suppress the accumulation of mutations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[234]  A. Sancar,et al.  Reconstitution of RPA-covered single-stranded DNA-activated ATR-Chk1 signaling , 2010, Proceedings of the National Academy of Sciences.

[235]  Y. Pommier,et al.  Phosphorylation of BLM, Dissociation from Topoisomerase IIIα, and Colocalization with γ-H2AX after Topoisomerase I-Induced Replication Damage , 2005, Molecular and Cellular Biology.

[236]  C. Mathew,et al.  Biallelic mutations in PALB2 cause Fanconi anemia subtype FA-N and predispose to childhood cancer , 2007, Nature Genetics.

[237]  R. Rothstein,et al.  Timing is everything: cell cycle control of Rad52 , 2010, Cell Division.

[238]  Yunfeng Pan,et al.  A PP4 phosphatase complex dephosphorylates RPA2 to facilitate DNA repair via homologous recombination , 2010, Nature Structural &Molecular Biology.

[239]  A. Gurtan,et al.  Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. , 2008, Blood.

[240]  Y. Drew,et al.  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 , 2010, Clinical Cancer Research.

[241]  Andrzej Stasiak,et al.  The Fanconi anemia protein FANCM can promote branch migration of Holliday junctions and replication forks. , 2008, Molecular cell.

[242]  S. Keeney,et al.  Molecular basis for enhancement of the meiotic DMC1 recombinase by RAD51 associated protein 1 (RAD51AP1) , 2011, Proceedings of the National Academy of Sciences.

[243]  M. Cox,et al.  The Rad51-dependent Pairing of Long DNA Substrates Is Stabilized by Replication Protein A* , 2002, The Journal of Biological Chemistry.

[244]  M. Grimaldi,et al.  The Anaphase-Promoting Complex/Cyclosome Controls Repair and Recombination by Ubiquitylating Rhp54 in Fission Yeast , 2008, Molecular and Cellular Biology.

[245]  H. Klein,et al.  The consequences of Rad51 overexpression for normal and tumor cells. , 2008, DNA repair.

[246]  W. Heyer,et al.  Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. , 2011, Biochimica et biophysica acta.

[247]  T. Helleday,et al.  Targeting homologous recombination repair defects in cancer. , 2010, Trends in pharmacological sciences.

[248]  M. Doutriaux,et al.  Brca2 is involved in meiosis in Arabidopsis thaliana as suggested by its interaction with Dmc1 , 2004, The EMBO journal.

[249]  Junjie Chen,et al.  SOSS complexes participate in the maintenance of genomic stability. , 2009, Molecular cell.

[250]  J. Thacker,et al.  Homologous recombination deficiency leads to profound genetic instability in cells derived from Xrcc2-knockout mice. , 2003, Cancer research.

[251]  Stephen J. Elledge,et al.  Sensing DNA Damage Through ATRIP Recognition of RPA-ssDNA Complexes , 2003, Science.

[252]  S. Yokoyama,et al.  The putative nuclear localization signal of the human RAD52 protein is a potential sumoylation site. , 2010, Journal of biochemistry.

[253]  R. Moyzis,et al.  UBL1, a human ubiquitin-like protein associating with human RAD51/RAD52 proteins. , 1996, Genomics.

[254]  Tim J. Craig,et al.  SGS1 is a multicopy suppressor of srs2: functional overlap between DNA helicases. , 2002, Nucleic acids research.

[255]  Michael G. Sehorn,et al.  Rad51 Recombinase and Recombination Mediators* , 2003, Journal of Biological Chemistry.

[256]  S. Brill,et al.  Mapping the DNA Topoisomerase III Binding Domain of the Sgs1 DNA Helicase* , 2001, The Journal of Biological Chemistry.

[257]  P. Lansdorp,et al.  RTEL1: an essential helicase for telomere maintenance and the regulation of homologous recombination , 2010, Nucleic acids research.

[258]  Junjie Chen,et al.  PALB2 Regulates Recombinational Repair through Chromatin Association and Oligomerization* , 2009, The Journal of Biological Chemistry.

[259]  Y. Matsuda,et al.  The mouse RecA-like gene Dmc1 is required for homologous chromosome synapsis during meiosis. , 1998, Molecular cell.

[260]  S C West,et al.  Identification and purification of two distinct complexes containing the five RAD51 paralogs. , 2001, Genes & development.

[261]  P. Sung,et al.  Enhancement of the RAD51 Recombinase Activity by the Tumor Suppressor PALB2 , 2010, Nature Structural &Molecular Biology.

[262]  S. Seal,et al.  PALB2, which encodes a BRCA2-interacting protein, is a breast cancer susceptibility gene , 2007, Nature Genetics.

[263]  P. Sung,et al.  Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. , 2011, DNA repair.

[264]  N. Kleckner,et al.  The Single-End Invasion An Asymmetric Intermediate at the Double-Strand Break to Double-Holliday Junction Transition of Meiotic Recombination , 2001, Cell.

[265]  M. Brenneman,et al.  Depletion of DSS1 protein disables homologous recombinational repair in human cells. , 2010, Mutation research.

[266]  J. Haber,et al.  Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. , 2001, Molecular cell.

[267]  T. Pandita,et al.  Rad52 inactivation is synthetically lethal with BRCA2 deficiency , 2010, Proceedings of the National Academy of Sciences.

[268]  T. Skorski,et al.  Targeting RAD51 phosphotyrosine-315 to prevent unfaithful recombination repair in BCR-ABL1 leukemia. , 2011, Blood.

[269]  T. Kodadek,et al.  Direct Association between the Yeast Rad51 and Rad54 Recombination Proteins* , 1996, The Journal of Biological Chemistry.

[270]  Steven S. Branda,et al.  The Sgs1 Helicase Regulates Chromosome Synapsis and Meiotic Crossing Over , 2003, Current Biology.

[271]  C. Bendixen,et al.  DNA strand annealing is promoted by the yeast Rad52 protein. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[272]  G. Roeder,et al.  Roles for two RecA homologs in promoting meiotic chromosome synapsis. , 1995, Genes & development.

[273]  J. Schimenti,et al.  Midgestation lethality in mice deficient for the RecA‐related gene, Rad51d/Rad51l3 , 2000, Genesis.

[274]  Stephen L. Gasior,et al.  Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. , 1998, Genes & development.

[275]  D. Schild,et al.  RAD51AP2, a novel vertebrate- and meiotic-specific protein, shares a conserved RAD51-interacting C-terminal domain with RAD51AP1/PIR51 , 2006, Nucleic acids research.

[276]  S. Kowalczykowski,et al.  Purified human BRCA2 stimulates RAD51-mediated recombination , 2010, Nature.

[277]  Michael G. Sehorn,et al.  A comparative analysis of Dmc1 and Rad51 nucleoprotein filaments , 2008, Nucleic acids research.

[278]  R. Syljuåsen,et al.  A genetic screen identifies BRCA2 and PALB2 as key regulators of G2 checkpoint maintenance , 2011, EMBO reports.

[279]  S. Gygi,et al.  Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. , 2009, Molecular cell.

[280]  Edward H Egelman,et al.  Stabilization of RAD51 nucleoprotein filaments by the C-terminal region of BRCA2 , 2007, Nature Structural &Molecular Biology.

[281]  J. Bartek,et al.  The DNA-damage response in human biology and disease , 2009, Nature.

[282]  S. Kowalczykowski,et al.  A Single-stranded DNA-binding Protein Is Needed for Efficient Presynaptic Complex Formation by the Saccharomyces cerevisiae Rad51 Protein* , 1997, Journal of Biological Chemistry.

[283]  Alan Ashworth,et al.  Structural basis for recruitment of BRCA2 by PALB2 , 2009, EMBO reports.

[284]  B. A. Ballif,et al.  ATM and ATR Substrate Analysis Reveals Extensive Protein Networks Responsive to DNA Damage , 2007, Science.

[285]  A. Jeyasekharan,et al.  The Carboxyl Terminus of Brca2 Links the Disassembly of Rad51 Complexes to Mitotic Entry , 2009, Current Biology.

[286]  E. Egelman,et al.  Novel pro- and anti-recombination activities of the Bloom's syndrome helicase. , 2007, Genes & development.

[287]  S. Yokoyama,et al.  Preferential binding to branched DNA strands and strand-annealing activity of the human Rad51B, Rad51C, Rad51D and Xrcc2 protein complex. , 2004, Nucleic acids research.

[288]  N. Kleckner,et al.  Interhomolog Bias during Meiotic Recombination: Meiotic Functions Promote a Highly Differentiated Interhomolog-Only Pathway , 1997, Cell.

[289]  R. Rothstein,et al.  Choreography of the DNA Damage Response Spatiotemporal Relationships among Checkpoint and Repair Proteins , 2004, Cell.

[290]  Akira Shinohara,et al.  Rad51‐deficient vertebrate cells accumulate chromosomal breaks prior to cell death , 1998, The EMBO journal.

[291]  E. Yeh,et al.  Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. , 2010, Molecular cell.

[292]  T. Kodadek,et al.  DMC1 functions in a Saccharomyces cerevisiae meiotic pathway that is largely independent of the RAD51 pathway. , 1997, Genetics.

[293]  M. Washburn,et al.  Mnd1/Hop2 Facilitates Dmc1-Dependent Interhomolog Crossover Formation in Meiosis of Budding Yeast , 2006, Molecular and Cellular Biology.

[294]  V. Pankratz,et al.  Microcephalin regulates BRCA2 and Rad51-associated DNA double-strand break repair. , 2009, Cancer research.

[295]  L. Krejci,et al.  Srs2: The “Odd-Job Man” in DNA repair , 2010, DNA repair.

[296]  J. Haber,et al.  Cdk1 Targets Srs2 to Complete Synthesis-Dependent Strand Annealing and to Promote Recombinational Repair , 2010, PLoS genetics.

[297]  S. West,et al.  Interactions between human BRCA2 protein and the meiosis‐specific recombinase DMC1 , 2007, The EMBO journal.

[298]  W. Holloman,et al.  Mutational analysis of Brh2 reveals requirements for compensating mediator functions , 2011, Molecular microbiology.

[299]  Efterpi Papouli,et al.  Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. , 2005, Molecular cell.

[300]  L. Symington,et al.  Suppression of the Double-Strand-Break-Repair Defect of the Saccharomyces cerevisiae rad57 Mutant , 2009, Genetics.

[301]  G. Roeder,et al.  Budding yeast Hed1 down-regulates the mitotic recombination machinery when meiotic recombination is impaired. , 2006, Genes & development.

[302]  P. Berg,et al.  Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[303]  Bing Xia,et al.  Cooperation of breast cancer proteins PALB2 and piccolo BRCA2 in stimulating homologous recombination , 2010, Nature Structural &Molecular Biology.

[304]  T. Ha,et al.  Tyrosine phosphorylation enhances RAD52-mediated annealing by modulating its DNA binding , 2011, The EMBO journal.

[305]  F. Ahmad,et al.  The N-terminal region of the Schizosaccharomyces pombe RecQ helicase, Rqh1p, physically interacts with Topoisomerase III and is required for Rqh1p function , 2005, Molecular Genetics and Genomics.

[306]  Anna Malkova,et al.  Srs2 and Sgs1–Top3 Suppress Crossovers during Double-Strand Break Repair in Yeast , 2003, Cell.

[307]  Jun Qin,et al.  MPS1-dependent mitotic BLM phosphorylation is important for chromosome stability. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[308]  W. Heyer,et al.  RAD54 controls access to the invading 3′-OH end after RAD51-mediated DNA strand invasion in homologous recombination in Saccharomyces cerevisiae , 2008, Nucleic acids research.

[309]  K. Ohta,et al.  Ubc9- and Mms21-Mediated Sumoylation Counteracts Recombinogenic Events at Damaged Replication Forks , 2006, Cell.

[310]  P. Sung,et al.  Interaction with Rad51 Is Indispensable for Recombination Mediator Function of Rad52* , 2002, The Journal of Biological Chemistry.

[311]  W. Heyer,et al.  Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins , 1997, The EMBO journal.

[312]  Y. Pommier,et al.  Phosphorylation of BLM, dissociation from topoisomerase IIIalpha, and colocalization with gamma-H2AX after topoisomerase I-induced replication damage. , 2005, Molecular and cellular biology.

[313]  R. Camerini-Otero,et al.  The resistance of DMC1 D-loops to dissociation may account for the DMC1 requirement in meiosis , 2010, Nature Structural &Molecular Biology.

[314]  S. Kowalczykowski,et al.  Rad52 promotes second-end DNA capture in double-stranded break repair to form complement-stabilized joint molecules , 2009, Proceedings of the National Academy of Sciences.

[315]  M. Leversha,et al.  Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. , 2005, Human molecular genetics.

[316]  Hiroki Inui,et al.  Mutations of a novel human RAD54 homologue, RAD54B, in primary cancer , 1999, Oncogene.

[317]  D. Branzei,et al.  Ubc9 is required for damage-tolerance and damage-induced interchromosomal homologous recombination in S. cerevisiae. , 2004, DNA repair.

[318]  A. Ashworth,et al.  Making the best of PARP inhibitors in ovarian cancer , 2010, Nature Reviews Clinical Oncology.

[319]  Michael G. Sehorn,et al.  The budding yeast Mei5-Sae3 complex interacts with Rad51 and preferentially binds a DNA fork structure. , 2011, DNA repair.

[320]  Alan Ashworth,et al.  Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy , 2005, Nature.

[321]  D. K. Bishop,et al.  The Mei5-Sae3 Protein Complex Mediates Dmc1 Activity in Saccharomyces cerevisiae* , 2009, Journal of Biological Chemistry.

[322]  P. Sung,et al.  ATP-dependent Chromatin Remodeling by the Saccharomyces cerevisiae Homologous Recombination Factor Rdh54* , 2008, Journal of Biological Chemistry.

[323]  A. Prescott,et al.  p14 Arf Promotes Small Ubiquitin-like Modifier Conjugation of Werners Helicase* , 2004, Journal of Biological Chemistry.

[324]  A. Baryshnikova,et al.  The Human F-Box DNA Helicase FBH1 Faces Saccharomyces cerevisiae Srs2 and Postreplication Repair Pathway Roles , 2007, Molecular and Cellular Biology.

[325]  G. Roeder,et al.  The importance of genetic recombination for fidelity of chromosome pairing in meiosis. , 2003, Developmental cell.