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Review Article

Multiple cellular mechanisms prevent chromosomal rearrangements involving repetitive DNA

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Pages 297-313 | Received 19 Jan 2012, Accepted 09 Mar 2012, Published online: 12 Apr 2012

References

  • Acharya S, Foster PL, Brooks P, Fishel R. 2003. The coordinated functions of the E. coli MutS and MutL proteins in mismatch repair. Mol Cell 12:233–246.
  • Abeysinghe SS, Chuzhanova N, Krawczak M, Ball EV, Cooper DN. 2003. Translocation and gross deletion breakpoints in human inherited disease and cancer I: Nucleotide composition and recombination-associated motifs. Hum Mutat 22:229–244.
  • Argueso JL, Westmoreland J, Mieczkowski PA, Gawel M, Petes TD, Resnick MA. 2008. Double-strand breaks associated with repetitive DNA can reshape the genome. Proc Natl Acad Sci USA 105:11845–11850.
  • Ashton TM, Mankouri HW, Heidenblut A, McHugh PJ, Hickson ID. 2011. Pathways for Holliday junction processing during homologous recombination in Saccharomyces cerevisiae. Mol Cell Biol 31:1921–1933.
  • Aylon Y, Liefshitz B, Kupiec M. 2004. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J 23:4868–4875.
  • Bailey JA, Yavor AM, Massa HF, Trask BJ, Eichler EE. 2001. Segmental duplications: organization and impact within the current human genome project assembly. Genome Res 11:1005–1017.
  • Bailey JA, Liu G, Eichler EE. 2003. An Alu transposition model for the origin and expansion of human segmental duplications. Am J Hum Genet 73:823–834.
  • Bailis AM, Arthur L, Rothstein R. 1992. Genome rearrangement in top3 mutants of Saccharomyces cerevisiae requires a functional RAD1 excision repair gene. Mol Cell Biol 12:4988–4993.
  • Barber LJ, Youds JL, Ward JD, McIlwraith MJ, O’Neil NJ, Petalcorin MI, Martin JS, Collis SJ, Cantor SB, Auclair M, Tissenbaum H, West SC, Rose AM, Boulton SJ. 2008. RTEL1 maintains genomic stability by suppressing homologous recombination. Cell 135:261–271.
  • Ben-Aroya S, Mieczkowski PA, Petes TD, Kupiec M. 2004. The compact chromatin structure of a Ty repeated sequence suppresses recombination hotspot activity in Saccharomyces cerevisiae. Mol Cell 15:221–231.
  • Bennett RJ, Keck JL, Wang JC. 1999. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J Mol Biol 289:235–248.
  • Bennett RJ, Sharp JA, Wang JC. 1998. Purification and characterization of the Sgs1 DNA helicase activity of Saccharomyces cerevisiae. J Biol Chem 273:9644–9650.
  • Bugreev DV, Mazina OM, Mazin AV. 2006. Rad54 protein promotes branch migration of Holliday junctions. Nature 442:590–593.
  • Burgess SM, Kleckner N, Weiner BM. 1999. Somatic pairing of homologs in budding yeast: existence and modulation. Genes Dev 13:1627–1641.
  • Burgess SM, Kleckner N. 1999. Collisions between yeast chromosomal loci in vivo are governed by three layers of organization. Genes Dev 13:1871–1883.
  • Ceballos SJ, Heyer WD. 2011. Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim Biophys Acta 1809:509–523.
  • Cejka P, Kowalczykowski SC. 2010. The full-length Saccharomyces cerevisiae Sgs1 protein is a vigorous DNA helicase that preferentially unwinds holliday junctions. J Biol Chem 285:8290–8301.
  • Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. 2010. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat Struct Mol Biol 17:1377–1382.
  • Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A. 2003. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 5:675–679.
  • Chai B, Huang J, Cairns BR, Laurent BC. 2005. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev 19:1656–1661.
  • Chan JE, Kolodner RD. 2011. A genetic and structural study of genome rearrangements mediated by high copy repeat Ty1 elements. PLoS Genet 7:e1002089.
  • Chen F, Nastasi A, Shen Z, Brenneman M, Crissman H, Chen DJ. 1997. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes Rad51 and Rad52. Mutat Res 384:205–211.
  • Chen JM, Cooper DN, Férec C, Kehrer-Sawatzki H, Patrinos GP. 2010. Genomic rearrangements in inherited disease and cancer. Semin Cancer Biol 20:222–233.
  • Chen W, Jinks-Robertson S. 1998. Mismatch repair proteins regulate heteroduplex formation during mitotic recombination in yeast. Mol Cell Biol 18:6525–6537.
  • Chen X, Niu H, Chung WH, Zhu Z, Papusha A, Shim EY, Lee SE, Sung P, Ira G. 2011. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 18:1015–1019.
  • Chen Y, Peng C, Li D, Li S. 2010. Molecular and cellular bases of chronic myeloid leukemia. Protein Cell 1:124–132.
  • Chiolo I, Minoda A, Colmenares SU, Polyzos A, Costes SV, Karpen GH. 2011. Double-strand breaks in heterochromatin move outside of a dynamic HP1a domain to complete recombinational repair. Cell 144:732–744.
  • Chuzhanova N, Chen JM, Bacolla A, Patrinos GP, Férec C, Wells RD, Cooper DN. 2009. Gene conversion causing human inherited disease: evidence for involvement of non-B-DNA-forming sequences and recombination-promoting motifs in DNA breakage and repair. Hum Mutat 30:1189–1198.
  • Claij N, te Riele H. 1999. Microsatellite instability in human cancer: a prognostic marker for chemotherapy? Exp Cell Res 246:1–10.
  • Cleary JD, Pearson CE. 2005. Replication fork dynamics and dynamic mutations: the fork-shift model of repeat instability. Trends Genet 21:272–280.
  • Cook GW, Konkel MK, Major JD 3rd, Walker JA, Han K, Batzer MA. 2011. Alu pair exclusions in the human genome. Mob DNA 2:10.
  • Costes SV, Chiolo I, Pluth JM, Barcellos-Hoff MH, Jakob B. 2010. Spatiotemporal characterization of ionizing radiation induced DNA damage foci and their relation to chromatin organization. Mutat Res 704:78–87.
  • Datta A, Adjiri A, New L, Crouse GF, Jinks Robertson S. 1996. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae. Mol Cell Biol 16:1085–1093.
  • Datta A, Hendrix M, Lipsitch M, Jinks-Robertson S. 1997. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc Natl Acad Sci USA 94:9757–9762.
  • Davis AP, Symington LS. 2001. The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing. Genetics 159:515–525.
  • Dayani Y, Simchen G, Lichten M. 2011. Meiotic recombination intermediates are resolved with minimal crossover formation during return-to-growth, an analogue of the mitotic cell cycle. PLoS Genet 7:e1002083.
  • Doherty KM, Sharma S, Uzdilla LA, Wilson TM, Cui S, Vindigni A, Brosh RM Jr. 2005. RECQ1 helicase interacts with human mismatch repair factors that regulate genetic recombination. J Biol Chem 280:28085–28094.
  • Duan Z, Andronescu M, Schutz K, McIlwain S, Kim YJ, Lee C, Shendure J, Fields S, Blau CA, Noble WS. 2010. A three-dimensional model of the yeast genome. Nature 465:363–367.
  • Elliott B, Richardson C, Jasin M. 2005. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol Cell 17:885–894.
  • El-Osta A, Wolffe AP. 2000. DNA methylation and histone deacetylation in the control of gene expression: basic biochemistry to human development and disease. Gene Expr 9:63–75.
  • Esposito MS. 1978. Evidence that spontaneous mitotic recombination occurs at the two-strand stage. Proc Natl Acad Sci USA 75:4436–4440.
  • Fishman-Lobell J, Rudin N, Haber JE. 1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol Cell Biol 12:1292–1303.
  • Fournier A, McLeer-Florin A, Lefebvre C, Duley S, Barki L, Ribeyron J, Alboukadel K, Hamaidia S, Granjon A, Gressin R, Lajmanovich A, Bonnefoix T, Chauvelier S, Debernardi A, Rousseaux S, de Fraipont F, Figeac M, Kerckaert JP, De Vos J, Usson Y, Delaval K, Grichine A, Vourc’h C, Khochbin S, Feil R, Leroux D, Callanan MB. 2010. 1q12 chromosome translocations form aberrant heterochromatic foci associated with changes in nuclear architecture and gene expression in B cell lymphoma. EMBO Mol Med 2:159–171.
  • Fraga MF, Esteller M. 2005. Towards the human cancer epigenome: a first draft of histone modifications. Cell Cycle 4:1377–1381.
  • Goldfarb T, Alani E. 2005. Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 169:563–574.
  • Gravel S, Chapman JR, Magill C, Jackson SP. 2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev 22:2767–2772.
  • Grimme JM, Honda M, Wright R, Okuno Y, Rothenberg E, Mazin AV, Ha T, Spies M. 2010. Human Rad52 binds and wraps single-stranded DNA and mediates annealing via two hRad52-ssDNA complexes. Nucleic Acids Res 38:2917–2930.
  • Gu Z, Rifkin SA, White KP, Li WH. 2004. Duplicate genes increase gene expression diversity within and between species. Nat Genet 36:577–579.
  • Guirouilh-Barbat J, Huck S, Bertrand P, Pirzio L, Desmaze C, Sabatier L, Lopez BS. 2004. Impact of the KU80 pathway on NHEJ-induced genome rearrangements in mammalian cells. Mol Cell 14:611–623.
  • Gupta RC, Folta-Stogniew E, Radding CM. 1999. Human Rad51 protein can form homologous joints in the absence of net strand exchange. J Biol Chem 274:1248–1256.
  • Hannan AJ. 2010. TRPing up the genome: Tandem repeat polymorphisms as dynamic sources of genetic variability in health and disease. Discov Med 10:314–321.
  • Hastings PJ, Lupski JR, Rosenberg SM, Ira G. 2009. Mechanisms of change in gene copy number. Nat Rev Genet 10:551–564.
  • Heck JA, Gresham D, Botstein D, Alani E. 2006. Accumulation of recessive lethal mutations in Saccharomyces cerevisiae mlh1 mismatch repair mutants is not associated with gross chromosomal rearrangements. Genetics 174:519–523.
  • Heyer WD, Li X, Rolfsmeier M, Zhang XP. 2006. Rad54: the Swiss Army knife of homologous recombination? Nucleic Acids Res 34:4115–4125.
  • Hickson ID, Mankouri HW. 2011. Processing of homologous recombination repair intermediates by the Sgs1-Top3-Rmi1 and Mus81-Mms4 complexes. Cell Cycle 10:3078–3085.
  • Holmes VF, Benjamin KR, Crisona NJ, Cozzarelli NR. 2001. Bypass of heterology during strand transfer by Saccharomyces cerevisiae Rad51 protein. Nucleic Acids Res 29:5052–5057.
  • Hombauer H, Srivatsan A, Putnam CD, Kolodner RD. 2011. Mismatch repair, but not heteroduplex rejection, is temporally coupled to DNA replication. Science 334:1713–1716.
  • Holthausen JT, Wyman C, Kanaar R. 2010. Regulation of DNA strand exchange in homologous recombination. DNA Repair (Amst) 9:1264–1272.
  • Huertas P, Cortés-Ledesma F, Sartori AA, Aguilera A, Jackson SP. 2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455:689–692.
  • Huertas P, Jackson SP. 2009. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284:9558–9565.
  • Huyen Y, Zgheib O, Ditullio RA Jr, Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406–411.
  • International Human Genome Sequencing Consortium. 2001. Initial sequencing and analysis of the human genome. Nature 409:860–921.
  • Ira G, Malkova A, Liberi G, Foiani M, Haber JE. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–411.
  • Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, Haber JE, Foiani M. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011–1017.
  • Jain S, Sugawara N, Lydeard J, Vaze M, Tanguy Le Gac N, Haber JE. 2009. A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev 23:291–303.
  • Jazayeri A, Falck J, Lukas C, Bartek J, Smith GC, Lukas J, Jackson SP. 2006. ATM- and cell cycle-dependent regulation of ATR in response to DNA double-strand breaks. Nat Cell Biol 8:37–45.
  • Jeffreys AJ, Holloway JK, Kauppi L, May CA, Neumann R, Slingsby MT, Webb AJ. 2004. Meiotic recombination hot spots and human DNA diversity. Philos Trans R Soc Lond, B, Biol Sci 359:141–152.
  • Jinks-Robertson S, Petes TD. 1985. High-frequency meiotic gene conversion between repeated genes on nonhomologous chromosomes in yeast. Proc Natl Acad Sci USA 82:3350–3354.
  • Jinks-Robertson S, Petes TD. 1986. Chromosomal translocations generated by high-frequency meiotic recombination between repeated yeast genes. Genetics 114:731–752.
  • Jiricny J. 2006. The multifaceted mismatch-repair system. Nat Rev Mol Cell Biol 7:335–346.
  • Kadyk LC, Hartwell LH. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402.
  • Kiianitsa K, Solinger JA, Heyer WD. 2006. Terminal association of Rad54 protein with the Rad51-dsDNA filament. Proc Natl Acad Sci USA 103:9767–9772.
  • Kobayashi T. 2011. Regulation of ribosomal RNA gene copy number and its role in modulating genome integrity and evolutionary adaptability in yeast. Cell Mol Life Sci 68:1395–1403.
  • Kolodner RD, Putnam CD, Myung K. 2002. Maintenance of genome stability in Saccharomyces cerevisiae. Science 297:552–557.
  • Kolodner RD, Marsischky GT. 1999. Eukaryotic DNA mismatch repair. Curr Opin Genet Dev 9:89–96.
  • Kosugi S, Hasebe M, Tomita M, Yanagawa H. 2009. Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 106:10171–10176.
  • Kovtun IV, McMurray CT. 2008. Features of trinucleotide repeat instability in vivo. Cell Res 18:198–213.
  • Kraus E, Leung WY, Haber JE. 2001. Break-induced replication: a review and an example in budding yeast. Proc Natl Acad Sci USA 98:8255–8262.
  • Krejci L, Van Komen S, Li Y, Villemain J, Reddy MS, Klein H, Ellenberger T, Sung P. 2003. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423:305–309.
  • Krogh BO, Symington LS. 2004. Recombination proteins in yeast. Annu Rev Genet 38:233–271.
  • Kunkel TA, Erie DA. 2005. DNA mismatch repair. Annu Rev Biochem 74:681–710.
  • Kurahashi H, Inagaki H, Kato T, Hosoba E, Kogo H, Ohye T, Tsutsumi M, Bolor H, Tong M, Emanuel BS. 2009. Impaired DNA replication prompts deletions within palindromic sequences, but does not induce translocations in human cells. Hum Mol Genet 18:3397–3406.
  • Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR 3rd, Abmayr SM, Washburn MP, Workman JL. 2004. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 306:2084–2087.
  • Lao JP, Oh SD, Shinohara M, Shinohara A, Hunter N. 2008. Rad52 promotes postinvasion steps of meiotic double-strand-break repair. Mol Cell 29:517–524.
  • Lazzaro F, Sapountzi V, Granata M, Pellicioli A, Vaze M, Haber JE, Plevani P, Lydall D, Muzi-Falconi M. 2008. Histone methyltransferase Dot1 and Rad9 inhibit single-stranded DNA accumulation at DSBs and uncapped telomeres. EMBO J 27:1502–1512.
  • Lee SE, Myung K. 2009. Faithful after break-up: suppression of chromosomal translocations. Cell Mol Life Sci 66:3149–3160.
  • Léger-Silvestre I, Trumtel S, Noaillac-Depeyre J, Gas N. 1999. Functional compartmentalization of the nucleus in the budding yeast Saccharomyces cerevisiae. Chromosoma 108:103–113.
  • Lettier G, Feng Q, de Mayolo AA, Erdeniz N, Reid RJ, Lisby M, Mortensen UH, Rothstein R. 2006. The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet 2:e194.
  • Li GM. 2008. Mechanisms and functions of DNA mismatch repair. Cell Res 18:85–98.
  • Li X, Heyer WD. 2009. RAD54 controls access to the invading 3′-OH end after RAD51-mediated DNA strand invasion in homologous recombination in Saccharomyces cerevisiae. Nucleic Acids Res 37:638–646.
  • Liang B, Qiu J, Ratnakumar K, Laurent BC. 2007. RSC functions as an early double-strand-break sensor in the cell’s response to DNA damage. Curr Biol 17:1432–1437.
  • Liang F, Han M, Romanienko PJ, Jasin M. 1998. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci USA 95:5172–5177.
  • Lichten M, Borts RH, Haber JE. 1987. Meiotic gene conversion and crossing over between dispersed homologous sequences occurs frequently in Saccharomyces cerevisiae. Genetics 115:233–246.
  • Liefshitz B, Parket A, Maya R, Kupiec M. 1995. The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics 140:1199–1211.
  • Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD. 2011. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245–248.
  • Llorente B, Smith CE, Symington LS. 2008. Break-induced replication: what is it and what is it for? Cell Cycle 7:859–864.
  • Lo YC, Paffett KS, Amit O, Clikeman JA, Sterk R, Brenneman MA, Nickoloff JA. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol Cell Biol 26:4086–4094.
  • Lobachev KS, Gordenin DA, Resnick MA. 2002. The Mre11 complex is required for repair of hairpin-capped double-strand breaks and prevention of chromosome rearrangements. Cell 108:183–193.
  • Lupski JR, Stankiewicz P. 2005. Genomic disorders: molecular mechanisms for rearrangements and conveyed phenotypes. PLoS Genet 1:e49.
  • Mankouri HW, Ashton TM, Hickson ID. 2011. Holliday junction-containing DNA structures persist in cells lacking Sgs1 or Top3 following exposure to DNA damage. Proc Natl Acad Sci USA 108:4944–4949.
  • Mao Z, Bozzella M, Seluanov A, Gorbunova V. 2008. Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair 7:1765–1771.
  • Marques-Bonet T, Eichler EE. 2009. The evolution of human segmental duplications and the core duplicon hypothesis. Cold Spring Harb Symp Quant Biol 74:355–362.
  • Matos J, Blanco MG, Maslen S, Skehel JM, West SC. 2011. Regulatory control of the resolution of DNA recombination intermediates during meiosis and mitosis. Cell 147:158–172.
  • McEachern MJ, Haber JE. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem 75:111–135.
  • McVean G. 2010. What drives recombination hotspots to repeat DNA in humans? Philos Trans R Soc Lond, B, Biol Sci 365:1213–1218.
  • Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–774.
  • Mimitou EP, Symington LS. 2009a. DNA end resection: many nucleases make light work. DNA Repair (Amst) 8:983–995.
  • Mimitou EP, Symington LS. 2009b. Nucleases and helicases take center stage in homologous recombination. Trends Biochem Sci 34:264–272.
  • Mimitou EP, Symington LS. 2011. DNA end resection–unraveling the tail. DNA Repair (Amst) 10:344–348.
  • Miné J, Disseau L, Takahashi M, Cappello G, Dutreix M, Viovy JL. 2007. Real-time measurements of the nucleation, growth and dissociation of single Rad51-DNA nucleoprotein filaments. Nucleic Acids Res 35:7171–7187.
  • Mirny LA. 2011. The fractal globule as a model of chromatin architecture in the cell. Chromosome Res 19:37–51.
  • Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X. 2004. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767–775.
  • Myers S, Bottolo L, Freeman C, McVean G, Donnelly P. 2005. A fine-scale map of recombination rates and hotspots across the human genome. Science 310:321–324.
  • Myers S, Freeman C, Auton A, Donnelly P, McVean G. 2008. A common sequence motif associated with recombination hot spots and genome instability in humans. Nat Genet 40:1124–1129.
  • Myers S, Spencer CC, Auton A, Bottolo L, Freeman C, Donnelly P, McVean G. 2006. The distribution and causes of meiotic recombination in the human genome. Biochem Soc Trans 34:526–530.
  • Namsaraev EA, Berg P. 2000. Rad51 uses one mechanism to drive DNA strand exchange in both directions. J Biol Chem 275:3970–3976.
  • Narayanan V, Mieczkowski PA, Kim HM, Petes TD, Lobachev KS. 2006. The pattern of gene amplification is determined by the chromosomal location of hairpin-capped breaks. Cell 125:1283–1296.
  • Németh A, Längst G. 2011. Genome organization in and around the nucleolus. Trends Genet 27:149–156.
  • Nicholson A, Hendrix M, Jinks-Robertson S, Crouse GF. 2000. Regulation of mitotic homeologous recombination in yeast. Functions of mismatch repair and nucleotide excision repair genes. Genetics 154:133–146.
  • Nimonkar AV, Kowalczykowski SC. 2009. Second-end DNA capture in double-strand break repair: how to catch a DNA by its tail. Cell Cycle 8:1816–1817.
  • Ogiwara H, Ui A, Otsuka A, Satoh H, Yokomi I, Nakajima S, Yasui A, Yokota J, Kohno T. 2011. Histone acetylation by CBP and p300 at double-strand break sites facilitates SWI/SNF chromatin remodeling and the recruitment of non-homologous end joining factors. Oncogene 30:2135–2146.
  • Ohno S, Wolf U, Atkin NB. 1968. Evolution from fish to mammals by gene duplication. Hereditas 59:169–187.
  • Osley MA, Shen X. 2006. Altering nucleosomes during DNA double-strand break repair in yeast. Trends Genet 22:671–677.
  • Oum JH, Seong C, Kwon Y, Ji JH, Sid A, Ramakrishnan S, Ira G, Malkova A, Sung P, Lee SE, Shim EY. 2011. RSC facilitates Rad59-dependent homologous recombination between sister chromatids by promoting cohesin loading at DNA double-strand breaks. Mol Cell Biol 31:3924–3937.
  • Paek AL, Kaochar S, Jones H, Elezaby A, Shanks L, Weinert T. 2009. Fusion of nearby inverted repeats by a replication-based mechanism leads to formation of dicentric and acentric chromosomes that cause genome instability in budding yeast. Genes Dev 23:2861–2875.
  • Pâques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63:349–404.
  • Park EJ, Hur SK, Kwon J. 2010. Human INO80 chromatin-remodelling complex contributes to DNA double-strand break repair via the expression of Rad54B and XRCC3 genes. Biochem J 431:179–187.
  • Park PU, Defossez PA, Guarente L. 1999. Effects of mutations in DNA repair genes on formation of ribosomal DNA circles and life span in Saccharomyces cerevisiae. Mol Cell Biol 19:3848–3856.
  • Peng JC, Karpen GH. 2008. Epigenetic regulation of heterochromatic DNA stability. Curr Opin Genet Dev 18:204–211.
  • Pentao L, Wise CA, Chinault AC, Patel PI, Lupski JR. 1992. Charcot-Marie-Tooth type 1A duplication appears to arise from recombination at repeat sequences flanking the 1.5 Mb monomer unit. Nat Genet 2:292–300.
  • Petes TD. 1980. Unequal meiotic recombination within tandem arrays of yeast ribosomal DNA genes. Cell 19:765–774.
  • Plank JL, Wu J, Hsieh TS. 2006. Topoisomerase IIIalpha and Bloom’s helicase can resolve a mobile double Holliday junction substrate through convergent branch migration. Proc Natl Acad Sci USA 103:11118–11123.
  • Prakash R, Satory D, Dray E, Papusha A, Scheller J, Kramer W, Krejci L, Klein H, Haber JE, Sung P, Ira G. 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23:67–79.
  • Puget N, Gad S, Perrin-Vidoz L, Sinilnikova OM, Stoppa-Lyonnet D, Lenoir GM, Mazoyer S. 2002. Distinct BRCA1 rearrangements involving the BRCA1 pseudogene suggest the existence of a recombination hot spot. Am J Hum Genet 70:858–865.
  • Putnam CD, Hayes TK, Kolodner RD. 2009. Specific pathways prevent duplication-mediated genome rearrangements. Nature 460:984–989.
  • Ragone S, Maman JD, Furnham N, Pellegrini L. 2008. Structural basis for inhibition of homologous recombination by the RecX protein. EMBO J 27:2259–2269.
  • Raynard S, Bussen W, Sung P. 2006. A double Holliday junction dissolvasome comprising BLM, topoisomerase IIIalpha, and BLAP75. J Biol Chem 281:13861–13864.
  • Richard GF, Pâques F. 2000. Mini- and microsatellite expansions: the recombination connection. EMBO Rep 1:122–126.
  • Roeder GS. 1997. Meiotic chromosomes: it takes two to tango. Genes Dev 11:2600–2621.
  • Rogakou EP, Boon C, Redon C, Bonner WM. 1999. Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146:905–916.
  • Rosselli W, Stasiak A. 1991. The ATPase activity of RecA is needed to push the DNA strand exchange through heterologous regions. EMBO J 10:4391–4396.
  • Rossi MJ, Mazin AV. 2008. Rad51 protein stimulates the branch migration activity of Rad54 protein. J Biol Chem 283:24698–24706.
  • Rothenberg E, Grimme JM, Spies M, Ha T. 2008. Human Rad52-mediated homology search and annealing occurs by continuous interactions between overlapping nucleoprotein complexes. Proc Natl Acad Sci USA 105:20274–20279.
  • Samoshkin A, Dulev S, Loukinov D, Rosenfeld JA, Strunnikov AV. 2012. Condensin dysfunction in human cells induces nonrandom chromosomal breaks in anaphase, with distinct patterns for both unique and repeated genomic regions. Chromosoma 121:191–199.
  • Saydam N, Kanagaraj R, Dietschy T, Garcia PL, Peña-Diaz J, Shevelev I, Stagljar I, Janscak P. 2007. Physical and functional interactions between Werner syndrome helicase and mismatch-repair initiation factors. Nucleic Acids Res 35:5706–5716.
  • Schmidt KH, Viebranz E, Doerfler L, Lester C, Rubenstein A. 2010. Formation of complex and unstable chromosomal translocations in yeast. PLoS ONE 5:e12007.
  • Selva EM, New L, Crouse GF, Lahue RS. 1995. Mismatch correction acts as a barrier to homeologous recombination in Saccharomyces cerevisiae. Genetics 139:1175–1188.
  • Shaw CJ, Lupski JR. 2004. Implications of human genome architecture for rearrangement-based disorders: the genomic basis of disease. Hum Mol Genet 13 Spec No 1:R57–R64.
  • Shen P, Huang HV. 1986. Homologous recombination in Escherichia coli: dependence on substrate length and homology. Genetics 112:441–457.
  • Shen X, Mizuguchi G, Hamiche A, Wu C. 2000. A chromatin remodelling complex involved in transcription and DNA processing. Nature 406:541–544.
  • Shim EY, Hong SJ, Oum JH, Yanez Y, Zhang Y, Lee SE. 2007. RSC mobilizes nucleosomes to improve accessibility of repair machinery to the damaged chromatin. Mol Cell Biol 27:1602–1613.
  • Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM, Petrini JH, Haber JE, Lichten M. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr Biol 14:1703–1711.
  • Slotkin RK, Martienssen R. 2007. Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285.
  • Sluiter MD, van Rensburg EJ. 2011. Large genomic rearrangements of the BRCA1 and BRCA2 genes: review of the literature and report of a novel BRCA1 mutation. Breast Cancer Res Treat 125:325–349.
  • Snijders AM, Fridlyand J, Mans DA, Segraves R, Jain AN, Pinkel D, Albertson DG. 2003. Shaping of tumor and drug-resistant genomes by instability and selection. Oncogene 22:4370–4379.
  • Stankiewicz P, Lupski JR. 2006. The genomic basis of disease, mechanisms and assays for genomic disorders. Genome Dyn 1:1–16.
  • Stankiewicz P, Lupski JR. 2002. Genome architecture, rearrangements and genomic disorders. Trends Genet 18:74–82.
  • Strand M, Prolla TA, Liskay RM, Petes TD. 1993. Destabilization of tracts of simple repetitive DNA in yeast by mutations affecting DNA mismatch repair. Nature 365:274–276.
  • Stratton MR, Campbell PJ, Futreal PA. 2009. The cancer genome. Nature 458:719–724.
  • Stephens PJ, Greenman CD, Fu B, Yang F, Bignell GR, Mudie LJ, Pleasance ED, Lau KW, Beare D, Stebbings LA, McLaren S, Lin ML, McBride DJ, Varela I, Nik-Zainal S, Leroy C, Jia M, Menzies A, Butler AP, Teague JW, Quail MA, Burton J, Swerdlow H, Carter NP, Morsberger LA, Iacobuzio-Donahue C, Follows GA, Green AR, Flanagan AM, Stratton MR, Futreal PA, Campbell PJ. 2011. Massive genomic rearrangement acquired in a single catastrophic event during cancer development. Cell 144:27–40.
  • Strunnikov AV. 2010. One-hit wonders of genomic instability. Cell Div 5:15.
  • Sugawara N, Goldfarb T, Studamire B, Alani E, Haber JE. 2004. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc Natl Acad Sci USA 101:9315–9320.
  • Sugiyama T, Zaitseva EM, Kowalczykowski SC. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J Biol Chem 272:7940–7945.
  • Sugiyama T, Kowalczykowski SC. 2002. 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 277:31663–31672.
  • Sugiyama T, Kantake N. 2009. Dynamic regulatory interactions of rad51, rad52, and replication protein-a in recombination intermediates. J Mol Biol 390:45–55.
  • Sung P. 1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science 265:1241–1243.
  • Sung P. 1997. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J Biol Chem 272:28194–28197.
  • Sung P, Krejci L, Van Komen S, Sehorn MG. 2003. Rad51 recombinase and recombination mediators. J Biol Chem 278:42729–42732.
  • Surtees JA, Argueso JL, Alani E. 2004. Mismatch repair proteins: key regulators of genetic recombination. Cytogenet Genome Res 107:146–159.
  • Svendsen JM, Harper JW. 2010. GEN1/Yen1 and the SLX4 complex: Solutions to the problem of Holliday junction resolution. Genes Dev 24:521–536.
  • Symington LS. 2002. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66:630–70, table of contents.
  • Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet 45:247–271.
  • Szostak JW, Orr-Weaver TL, Rothstein RJ, Stahl FW. 1983. The double-strand-break repair model for recombination. Cell 33:25–35.
  • Szostak JW, Wu R. 1980. Unequal crossing over in the ribosomal DNA of Saccharomyces cerevisiae. Nature 284:426–430.
  • Tanizawa H, Noma KI. 2011. Unravelling global genome organization by 3C-seq. Semin Cell Dev Biol (In Press).
  • Timusk ER, Ferguson MM, Moghadam HK, Norman JD, Wilson CC, Danzmann RG. 2011. Genome evolution in the fish family salmonidae: generation of a brook charr genetic map and comparisons among charrs (Arctic charr and brook charr) with rainbow trout. BMC Genet 12:68.
  • Torres-Rosell J, Sunjevaric I, De Piccoli G, Sacher M, Eckert-Boulet N, Reid R, Jentsch S, Rothstein R, Aragón L, Lisby M. 2007. The Smc5-Smc6 complex and SUMO modification of Rad52 regulates recombinational repair at the ribosomal gene locus. Nat Cell Biol 9:923–931.
  • Tripathi P, Pal D, Muniyappa K. 2007. Saccharomyces cerevisiae Hop1 protein zinc finger motif binds to the Holliday junction and distorts the DNA structure: implications for holliday junction migration. Biochemistry 46:12530–12542.
  • Tsubouchi H, Ogawa H. 2000. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell 11:2221–2233.
  • Tsukuda T, Lo YC, Krishna S, Sterk R, Osley MA, Nickoloff JA. 2009. INO80-dependent chromatin remodeling regulates early and late stages of mitotic homologous recombination. DNA Repair (Amst) 8:360–369.
  • van Attikum H, Fritsch O, Gasser SM. 2007. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26:4113–4125.
  • van Attikum H, Fritsch O, Hohn B, Gasser SM. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777–788.
  • van Attikum H, Gasser SM. 2005. ATP-dependent chromatin remodeling and DNA double-strand break repair. Cell Cycle 4:1011–1014.
  • van der Heijden T, Modesti M, Hage S, Kanaar R, Wyman C, Dekker C. 2008. Homologous recombination in real time: DNA strand exchange by RecA. Mol Cell 30:530–538.
  • Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F. 2003. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423:309–312.
  • Velculescu VE. 2008. Defining the blueprint of the cancer genome. Carcinogenesis 29:1087–1091.
  • Waldman AS. 2008. Ensuring the fidelity of recombination in mammalian chromosomes. Bioessays 30:1163–1171.
  • Wanat JJ, Kim KP, Koszul R, Zanders S, Weiner B, Kleckner N, Alani E. 2008. Csm4, in collaboration with Ndj1, mediates telomere-led chromosome dynamics and recombination during yeast meiosis. PLoS Genet 4:e1000188.
  • Ward TR, Hoang ML, Prusty R, Lau CK, Keil RL, Fangman WL, Brewer BJ. 2000. Ribosomal DNA replication fork barrier and HOT1 recombination hot spot: shared sequences but independent activities. Mol Cell Biol 20:4948–4957.
  • Watt PM, Hickson ID, Borts RH, Louis EJ. 1996. SGS1, a homologue of the Bloom’s and Werner’s syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144:935–945.
  • Weiner BM, Kleckner N. 1994. Chromosome pairing via multiple interstitial interactions before and during meiosis in yeast. Cell 77:977–991.
  • Wolfe KH, Shields DC. 1997. Molecular evidence for an ancient duplication of the entire yeast genome. Nature 387:708–713.
  • Wu Y, Kantake N, Sugiyama T, Kowalczykowski SC. 2008. Rad51 protein controls Rad52-mediated DNA annealing. J Biol Chem 283:14883–14892.
  • Yang Q, Zhang R, Wang XW, Linke SP, Sengupta S, Hickson ID, Pedrazzi G, Perrera C, Stagljar I, Littman SJ, Modrich P, Harris CC. 2004. The mismatch DNA repair heterodimer, hMSH2/6, regulates BLM helicase. Oncogene 23:3749–3756.
  • Zhang PG, Huang SZ, Pin AL, Adams KL. 2010. Extensive divergence in alternative splicing patterns after gene and genome duplication during the evolutionary history of Arabidopsis. Mol Biol Evol 27:1686–1697.
  • Zheng XF, Prakash R, Saro D, Longerich S, Niu H, Sung P. 2011. Processing of DNA structures via DNA unwinding and branch migration by the S. cerevisiae Mph1 protein. DNA Repair (Amst) 10:1034–1043.
  • Zhou Y, Mishra B. 2005. Quantifying the mechanisms for segmental duplications in mammalian genomes by statistical analysis and modeling. Proc Natl Acad Sci USA 102:4051–4056.
  • Zhou Y, Wubneh H, Schwarz C, Landweber LF. 2011. A chimeric chromosome in the ciliate oxytricha resulting from duplication. J Mol Evol 73:70–73.
  • Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–994.
  • Zierhut C, Diffley JF. 2008. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J 27:1875–1885.

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