From yeast to mammals: Recent advances in genetic control of homologous recombination

DNA Repair

Volumn 11, Issue 10, 2012, Pages 781-788

  Karpenshif, Yoav ^a   Bernstein, Kara A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer; Genetic instability; Homologous recombination; PARI; Rad51; Rad51 paralogues; Rad55 Rad57; RTEL; Shu complex; Srs2

Indexed keywords

HELICASE; NUCLEIC ACID BINDING PROTEIN; PROTEIN FBH1; PROTEIN RECQL5; PROTEIN SHU1; PROTEIN SHU2; PROTEIN SRS2; RAD51 PROTEIN; RAD55 PROTEIN; RAD57 PROTEIN; UNCLASSIFIED DRUG;

DNA REPAIR; DOUBLE STRANDED DNA BREAK; EUKARYOTIC CELL; GENE; GENETIC REGULATION; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; MITOTIC RECOMBINATION; NONHUMAN; PRIORITY JOURNAL; REGULATOR OF TELOMERE LENGTH 1 GENE; REVIEW; SACCHAROMYCES CEREVISIAE;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA HELICASES; HUMANS; MAMMALS; RAD51 RECOMBINASE; RECOMBINATIONAL DNA REPAIR; SACCHAROMYCES CEREVISIAE PROTEINS; YEASTS;

EUKARYOTA; MAMMALIA;

EID: 84867197361     PISSN: 15687864     EISSN: 15687856     Source Type: Journal    
DOI: 10.1016/j.dnarep.2012.07.001     Document Type: Review

References (75)

1. Vilenchik M.M., Knudson A.G. Endogenous DNA double-strand breaks: production, fidelity of repair, and induction of cancer. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:12871-12876.
2. Duker N.J. Chromosome breakage syndromes and cancer. Am. J. Med. Genet. 2002, 115:125-129.
3. Hiom K. Coping with DNA double strand breaks. DNA Repair (Amst) 2010, 9:1256-1263.
4. Holthausen J.T., Wyman C., Kanaar R. Regulation of DNA strand exchange in homologous recombination. DNA Repair 2010, 9:1264-1272.
5. Symington L.S., Gautier J. Double-strand break end resection and repair pathway choice. Annu. Rev. Genet. 2011, 45:247-271.
6. 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.
7. Holloman W.K. Unraveling the mechanism of BRCA2 in homologous recombination. Nat. Struct. Mol. Biol. 2011, 18:748-754.
8. Sugiyama T., Kowalczykowski S.C. Rad52 protein associates with replication protein A (RPA)-single-stranded DNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 2002, 277:31663-31672.
9. Chen P.L., Chen C.F., Chen Y., Xiao J., Sharp Z.D., Lee W.H. The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl. Acad. Sci. U.S.A. 1998, 95:5287-5292.
10. Heyer W.D. Biochemistry of eukaryotic homologous recombination. Top. Curr. Genet. 2007, 17:95-133.
11. Takata M., Sasaki M.S., Tachiiri S., Fukushima T., Sonoda E., Schild D., Thompson L.H., Takeda S. Chromosome Instability and Defective Recombinational Repair in Knockout Mutants of the Five Rad51 Paralogs. Mol. Cell. Biol. 2001, 21:2858-2866.
12. Heyer W.D., Ehmsen K.T., Liu J. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 2010, 44:113-139.
13. Kasparek T.R., Humphrey T.C. DNA double-strand break repair pathways, chromosomal rearrangements and cancer. Semin. Cell Dev. Biol. 2011, 22:886-897.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. 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.
20. Mankouri H.W., Chu W.K., Hickson I.D. A novel antirecombinase gains PARIty. Mol. Cell 2012, 45:6-7.
21. Hegde V., Klein H. Requirement for the SRS2 DNA helicase gene in non-homologous end joining in yeast. Nucleic Acids Res. 2000, 28:2779-2783.
22. 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.
23. Moldovan G.-L., Pfander B., Jentsch S. PCNA, the Maestro of the Replication Fork. Cell 2007, 129:665-679.
24. Moldovan G.L., Dejsuphong D., Petalcorin M.I., Hofmann K., Takeda S., Boulton S.J., D'Andrea A.D. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell 2012, 45:75-86.
25. 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.
26. 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.
27. Fugger K., Mistrik M., Danielsen J.R., 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.
28. 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.
29. 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.
30. Laulier C., Cheng A., Huang N., Stark J.M. Mammalian Fbh1 is important to restore normal mitotic progression following decatenation stress. DNA Repair 2010, 9:708-717.
31. 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.
32. 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.
33. Kanagaraj R., Saydam N., Garcia P.L., Zheng L., Janscak P. Human RECQ5β helicase promotes strand exchange on synthetic DNA structures resembling a stalled replication fork. Nucleic Acids Res. 2006, 34:5217-5231.
34. Schwendener S., Raynard S., Paliwal S., Cheng A., Kanagaraj R., Shevelev I., Stark J.M., Sung P., Janscak P. Physical Interaction of RECQ5 Helicase with RAD51 Facilitates Its Anti-recombinase Activity. J. Biol. Chem. 2010, 285:15739-15745.
35. Barber L.J., Youds J.L., Ward J.D., McIlwraith M.J., O'Neil N.J., Petalcorin M.I.R., 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.
36. Ding H., Schertzer M., Wu X., Gertsenstein M., Selig S., Kammori M., Pourvali R., Poon S., Vulto I., Chavez E., Tam P.P.L., Nagy A., Lansdorp P.M. Regulation of murine telomere length by Rtel: an essential gene encoding a helicase like protein. Cell 2004, 117:873-886.
37. Youds J.L., Mets D.G., McIlwraith M.J., Martin J.S., Ward J.D., Neil N.J.O., Rose A.M., West S.C., Meyer B.J., Boulton S.J. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 2010, 327:1254-1258.
38. Vannier J.B., Pavicic-Kaltenbrunner V., Petalcorin M.I., Ding H., Boulton S.J. RTEL1 dismantles T Loops and counteracts telomeric G4-DNA to maintain telomere integrity. Cell 2012, 149:795-806.
39. Uringa E.J., Lisaingo K., Pickett H.A., Brind'amour J., Rohde J.H., Zelensky A., Essers J., Lansdorp P.M. RTEL1 contributes to DNA replication, repair and telomere maintenance. Mol. Biol. Cell. 2012.
40. de Lange T. Shelterin: the protein complex that shapes and safeguards human telomeres. Genes Dev. 2005, 19:2100-2110.
41. Griffith J.D., Comeau L., Rosenfield S., Stansel R.M., Bianchi A., Moss H., de Lange T. Mammalian telomeres end in a large duplex loop. Cell 1999, 97:503-514.
42. Amiard S., Doudeau M., Pinte S., Poulet A., Lenain C., Faivre-Moskalenko C., Angelov D., Hug N., Vindigni A., Bouvet P., Paoletti J., Gilson E., Giraud-Panis M.-J. A topological mechanism for TRF2-enhanced strand invasion. Nat. Struct. Mol. Biol. 2007, 14:147-154.
43. Sfeir A., Kosiyatrakul S.T., Hockemeyer D., MacRae S.L., Karlseder J., Schildkraut C.L., de Lange T. Mammalian telomeres resemble fragile sites and require TRF1 for efficient replication. Cell 2009, 138:90-103.
44. Moldovan G.-L., Dejsuphong D., Petalcorin M.I.R., Hofmann K., Takeda S., Boulton S.J., D'Andrea A.D. Inhibition of homologous recombination by the PCNA-interacting protein PARI. Mol. Cell 2012, 45:75-86.
45. Benson F.E., Baumann P., West S.C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature 1998, 391:401-404.
46. Gasior S.L., Wong A.K., Kora Y., Shinohara A., Bishop D.K. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 1998, 12:2208-2221.
47. 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.
48. Symington L.S. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol. Mol. Biol. Rev. 2002, 66:630-670. table of contents.
49. 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.
50. Liu J., Renault L., Veaute X., Fabre F., Stahlberg H., Heyer W.D. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 2011, 479:245-248.
51. Martin V., Chahwan C., Gao H., Blais V., Wohlschlegel J., Yates J.R., McGowan C.H., Russell P. Sws1 is a conserved regulator of homologous recombination in eukaryotic cells. EMBO J. 2006, 25:2564-2574.
52. Bernstein K.A., Reid R.J., Sunjevaric I., Demuth K., Burgess R.C., 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.
53. 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.
54. Mankouri H.W., Ngo H.P., Hickson I.D. Shu proteins promote the formation of homologous recombination intermediates that are processed by Sgs1-Rmi1-Top3. Mol. Biol. Cell 2007, 18:4062-4073.
55. Ball L.G., Zhang K., Cobb J.A., Boone C., Xiao W. The yeast Shu complex couples error-free post-replication repair to homologous recombination. Mol. Microbiol. 2009, 73:89-102.
56. Ito T., Chiba T., Ozawa R., Yoshida M., Hattori M. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4569-4574.
57. Masson J.Y., Tarsounas M.C., Stasiak A.Z., Stasiak A., Shah R., McIlwraith M.J., Benson F.E., West S.C. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev. 2001, 15:3296-3307.
58. Garcia-Closas M., Egan K.M., Newcomb P.A., Brinton L.A., Titus-Ernstoff L., Chanock S., Welch R., Lissowska J., Peplonska B., Szeszenia-Dabrowska N., Zatonski W., Bardin-Mikolajczak A., Struewing J.P. Polymorphisms in DNA double-strand break repair genes and risk of breast cancer: two population-based studies in USA and Poland, and meta-analyses. Hum. Genet. 2006, 119:376-388.
59. Wooster R., Bignell G., Lancaster J., Swift S., Seal S., Mangion J., Collins N., Gregory S., Gumbs C., Micklem G. Identification of the breast cancer susceptibility gene BRCA2. Nature 1995, 378:789-792.
60. Chen H., Chen Y., Zhao Y., Fan W., Zhou K., Liu Y., Zhou L., Mao Y., Wei Q., Xu J., Lu D. Association of sequence variants on chromosomes 20, 11, and 5 (20q13.33, 11q23.3, and 5p15.33) with glioma susceptibility in a Chinese population. Am. J. Epidemiol. 2011, 173:915-922.
61. Wang S.S., Hartge P., Yeager M., Carreon T., Ruder A.M., Linet M., Inskip P.D., Black A., Hsing A.W., Alavanja M., Beane-Freeman L., Safaiean M., Chanock S.J., Rajaraman P. Joint associations between genetic variants and reproductive factors in glioma risk among women. Am. J. Epidemiol. 2011, 174:901-908.
62. Liu Y., Shete S., Etzel C.J., Scheurer M., Alexiou G., Armstrong G., Tsavachidis S., Liang F.W., Gilbert M., Aldape K., Armstrong T., Houlston R., Hosking F., Robertson L., Xiao Y., Wiencke J., Wrensch M., Andersson U., Melin B.S., Bondy M. Polymorphisms of LIG4, BTBD2, HMGA2, and RTEL1 genes involved in the double-strand break repair pathway predict glioblastoma survival. J. Clin. Oncol. 2010, 28:2467-2474.
63. Shete S., Hosking F.J., Robertson L.B., Dobbins S.E., Sanson M., Malmer B., Simon M., Marie Y., Boisselier B., Delattre J.Y., Hoang-Xuan K., El Hallani S., Idbaih A., Zelenika D., Andersson U., Henriksson R., Bergenheim A.T., Feychting M., Lonn S., Ahlbom A., Schramm J., Linnebank M., Hemminki K., Kumar R., Hepworth S.J., Price A., Armstrong G., Liu Y., Gu X., Yu R., Lau C., Schoemaker M., Muir K., Swerdlow A., Lathrop M., Bondy M., Houlston R.S. Genome-wide association study identifies five susceptibility loci for glioma. Nat. Genet. 2009, 41:899-904.
64. Wrensch M., Jenkins R.B., Chang J.S., Yeh R.F., Xiao Y., Decker P.A., Ballman K.V., Berger M., Buckner J.C., Chang S., Giannini C., Halder C., Kollmeyer T.M., Kosel M.L., LaChance D.H., McCoy L., O'Neill B.P., Patoka J., Pico A.R., Prados M., Quesenberry C., Rice T., Rynearson A.L., Smirnov I., Tihan T., Wiemels J., Yang P., Wiencke J.K. Variants in the CDKN2B and RTEL1 regions are associated with high-grade glioma susceptibility. Nat. Genet. 2009, 41:905-908.
65. Park D.J., Lesueur F., Nguyen-Dumont T., Pertesi M., Odefrey F., Hammet F., Neuhausen S.L., John E.M., Andrulis I.L., Terry M.B., Daly M., Buys S., Le Calvez-Kelm F., Lonie A., Pope B.J., Tsimiklis H., Voegele C., Hilbers F.M., Hoogerbrugge N., Barroso A., Osorio A., Giles G.G., Devilee P., Benitez J., Hopper J.L., Tavtigian S.V., Goldgar D.E., Southey M.C. Rare mutations in XRCC2 increase the risk of breast cancer. Am. J. Hum. Genet. 2012, 90:734-739.
66. Lin W.Y., Camp N.J., Cannon-Albright L.A., Allen-Brady K., Balasubramanian S., Reed M.W., Hopper J.L., Apicella C., Giles G.G., Southey M.C., Milne R.L., Arias-Perez J.I., Menendez-Rodriguez P., Benitez J., Grundmann M., Dubrowinskaja N., Park-Simon T.W., Dork T., Garcia-Closas M., Figueroa J., Sherman M., Lissowska J., Easton D.F., Dunning A.M., Rajaraman P., Sigurdson A.J., Doody M.M., Linet M.S., Pharoah P.D., Schmidt M.K., Cox A. A role for XRCC2 gene polymorphisms in breast cancer risk and survival. J. Med. Genet. 2011, 48:477-484.
67. Krupa R., Sliwinski T., Wisniewska-Jarosinska M., Chojnacki J., Wasylecka M., Dziki L., Morawiec J., Blasiak J. Polymorphisms in RAD51, XRCC2 and XRCC3 genes of the homologous recombination repair in colorectal cancer--a case control study. Mol. Biol. Rep. 2011, 38:2849-2854.
68. Yu K.D., Chen A.X., Qiu L.X., Fan L., Yang C., Shao Z.M. XRCC2 Arg188His polymorphism is not directly associated with breast cancer risk: evidence from 37,369 subjects. Breast Cancer Res. Treat. 2010, 123:219-225.
69. Silva S.N., Tomar M., Paulo C., Gomes B.C., Azevedo A.P., Teixeira V., Pina J.E., Rueff J., Gaspar J.F. Breast cancer risk and common single nucleotide polymorphisms in homologous recombination DNA repair pathway genes XRCC2, XRCC3, NBS1 and RAD51. Cancer Epidemiol. 2010, 34:85-92.
70. Curtin K., Lin W.Y., George R., Katory M., Shorto J., Cannon-Albright L.A., Smith G., Bishop D.T., Cox A., Camp N.J. Genetic variants in XRCC2: new insights into colorectal cancer tumorigenesis. Cancer Epidemiol. Biomarkers Prev. 2009, 18:2476-2484.
71. van der Heijden T., Modesti M., Hage S., Kanaar R., Wyman C., Dekker C. Homologous recombination in real time: DNA strand exchange by RecA. Mol. Cell 2008, 30:530-538.
72. Hilario J., Amitani I., Baskin R.J., Kowalczykowski S.C. Direct imaging of human Rad51 nucleoprotein dynamics on individual DNA molecules. Proc. Natl. Acad. Sci. U.S.A. 2009, 106:361-368.
73. Modesti M., Ristic D., van der Heijden T., Dekker C., van Mameren J., Peterman E.J., Wuite G.J., Kanaar R., Wyman C. Fluorescent human RAD51 reveals multiple nucleation sites and filament segments tightly associated along a single DNA molecule. Structure 2007, 15:599-609.
74. She Z., Gao Z.Q., Liu Y., Wang W.J., Liu G.F., Shtykova E.V., Xu J.H., Dong Y.H. Structural and SAXS analysis of the budding yeast SHU-complex proteins. FEBS Lett. 2012, 586:2306-2312.
75. Liu T., Wan L., Wu Y., Chen J., Huang J. hSWS1.SWSAP1 is an evolutionarily conserved complex required for efficient homologous recombination repair. J. Biol. Chem. 2011, 286:41758-41766.