1932

Abstract

Double-strand breaks (DSBs) pose a severe challenge to genome integrity; consequently, cells have developed efficient mechanisms to repair DSBs through several pathways of homologous recombination and other nonhomologous end-joining processes. Much of our understanding of these pathways has come from the analysis of site-specific DSBs created by the HO endonuclease in the budding yeast . I was fortunate to get in on the ground floor of analyzing the fate of synchronously induced DSBs through the study of what I coined “in vivo biochemistry.” I have had the remarkable good fortune to profit from the development of new techniques that have permitted an ever more detailed dissection of these repair mechanisms, which are described here.

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2016-11-23
2024-10-10
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Literature Cited

  1. Aboussekhra A, Chanet R, Adjiri A, Fabre F. 1.  1992. Semidominant suppressors of Srs2 helicase mutations of Saccharomyces cerevisiae map in the RAD51 gene, whose sequence predicts a protein with similarities to procaryotic RecA proteins. Mol. Cell. Biol 12:3224–34 [Google Scholar]
  2. Agmon N, Liefshitz B, Zimmer C, Fabre E, Kupiec M. 2.  2013. Effect of nuclear architecture on the efficiency of double-strand break repair. Nat. Cell Biol. 15:694–99 [Google Scholar]
  3. Anand RP, Lovett SL, Haber JE. 3.  2013. Break-induced DNA replication. DNA Replication SD Bell, M Méchali, ML DePamphilis 43–60 Cold Spring Harbor, NY: Cold Spring Harb. Press [Google Scholar]
  4. Anand RP, Tsaponina O, Greenwell PW, Lee CS, Du W. 4.  et al. 2014. Chromosome rearrangements via template switching between diverged repeated sequences. Genes Dev. 28:2394–406 [Google Scholar]
  5. Aylon Y, Liefshitz B, Kupiec M. 5.  2004. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23:4868–75 [Google Scholar]
  6. Aymard F, Bugler B, Schmidt CK, Guillou E, Caron P. 6.  et al. 2014. Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks. Nat. Struct. Mol. Biol. 21:366–74 [Google Scholar]
  7. Ceballos SJ, Heyer WD. 7.  2011. Functions of the Snf2/Swi2 family Rad54 motor protein in homologous recombination. Biochim. Biophys. Acta 1809:509–23 [Google Scholar]
  8. Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. 8.  2010. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. 17:1377–82 [Google Scholar]
  9. Chen H, Lisby M, Symington LS. 9.  2013. RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol. Cell 50:589–600 [Google Scholar]
  10. Chen X, Niu H, Chung WH, Zhu Z, Papusha A. 10.  et al. 2011. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat. Struct. Mol. Biol. 18:1015–19 [Google Scholar]
  11. Chen Z, Yang H, Pavletich NP. 11.  2008. Mechanism of homologous recombination from the RecA-ssDNA/dsDNA structures. Nature 453:489–94 [Google Scholar]
  12. Clerici M, Mantiero D, Lucchini G, Longhese MP. 12.  2006. The Saccharomyces cerevisiae Sae2 protein negatively regulates DNA damage checkpoint signalling. EMBO Rep. 7:212–18 [Google Scholar]
  13. Clerici M, Trovesi C, Galbiati A, Lucchini G, Longhese MP. 13.  2014. Mec1/ATR regulates the generation of single-stranded DNA that attenuates Tel1/ATM signaling at DNA ends. EMBO J. 33:198–216 [Google Scholar]
  14. Cloud V, Chan YL, Grubb J, Budke B, Bishop DK. 14.  2012. Rad51 is an accessory factor for Dmc1-mediated joint molecule formation during meiosis. Science 337:1222–25 [Google Scholar]
  15. Colaiacovo MP, Paques F, Haber JE. 15.  1999. Removal of one nonhomologous DNA end during gene conversion by a RAD1- and MSH2-independent pathway. Genetics 151:1409–23 [Google Scholar]
  16. Colleaux L, d'Auriol L, Betermier M, Cottarel G, Jacquier A. 16.  et al. 1986. Universal code equivalent of a yeast mitochondrial intron reading frame is expressed into E. coli as a specific double strand endonuclease. Cell 44:521–33 [Google Scholar]
  17. Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E. 17.  et al. 2014. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 343:88–91 [Google Scholar]
  18. Davis AP, Symington LS. 18.  2004. RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24:2344–51 [Google Scholar]
  19. Deem A, Keszthelyi A, Blackgrove T, Vayl A, Coffey B. 19.  et al. 2011. Break-induced replication is highly inaccurate. PLOS Biol. 9:e1000594 [Google Scholar]
  20. Diede SJ, Gottschling DE. 20.  2001. Exonuclease activity is required for sequence addition and Cdc13p loading at a de novo telomere. Curr. Biol. 11:1336–40 [Google Scholar]
  21. Dion V, Kalck V, Horigome C, Tobin BD, Gasser SM. 21.  2012. Increased mobility of double-strand breaks requires Mec1, Rad9 and the homologous recombination machinery. Nat. Cell Biol. 14:502–9 [Google Scholar]
  22. Dotiwala F, Eapen VV, Harrison JC, Arbel-Eden A, Ranade V. 22.  et al. 2013. DNA damage checkpoint triggers autophagy to regulate the initiation of anaphase. PNAS 110:E41–49 [Google Scholar]
  23. Dotiwala F, Harrison JC, Jain S, Sugawara N, Haber JE. 23.  2010. Mad2 prolongs DNA damage checkpoint arrest caused by a double-strand break via a centromere-dependent mechanism. Curr. Biol. 20:328–32 [Google Scholar]
  24. Eapen VV, Sugawara N, Tsabar M, Wu WH, Haber JE. 24.  2012. The Saccharomyces cerevisiae chromatin remodeler Fun30 regulates DNA end resection and checkpoint deactivation. Mol. Cell. Biol. 32:4727–40 [Google Scholar]
  25. Eapen VV, Waterman DP, Benard A, Schiffman N, Sayas E. 25.  et al. A novel pathway of targeted autophagy is induced by DNA damage in budding yeast..
  26. Fishman-Lobell J, Haber JE. 26.  1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258:480–84 [Google Scholar]
  27. Fishman-Lobell J, Rudin N, Haber JE. 27.  1992. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12:1292–303 [Google Scholar]
  28. Frank-Vaillant M, Marcand S. 28.  2001. NHEJ regulation by mating type is exercised through a novel protein, Lif2p, essential to the ligase IV pathway. Genes Dev. 15:3005–12 [Google Scholar]
  29. Game JC, Mortimer RK. 29.  1974. A genetic study of X-ray sensitive mutants in yeast. Mutat. Res. 24:281–92 [Google Scholar]
  30. Gravel S, Chapman JR, Magill C, Jackson SP. 30.  2008. DNA helicases Sgs1 and BLM promote DNA double-strand break resection. Genes Dev. 22:2767–72 [Google Scholar]
  31. Guillemain G, Ma E, Mauger S, Miron S, Thai R. 31.  et al. 2007. Mechanisms of checkpoint kinase Rad53 inactivation after a double-strand break in Saccharomyces cerevisiae. Mol. Cell. Biol. 27:3378–89 [Google Scholar]
  32. Haber JE. 32.  2006. Chromosome breakage and repair. Genetics 173:1181–85 [Google Scholar]
  33. Haber JE. 33.  2012. Mating-type genes and MAT switching in Saccharomyces cerevisiae. Genetics 191:33–64 [Google Scholar]
  34. Haber JE, Garvik B. 34.  1977. A new gene affecting the efficiency of mating-type interconversions in homothallic strains of Saccharomyces cerevisiae. Genetics 87:33–50 [Google Scholar]
  35. Haber JE, Ray BL, Kolb JM, White CI. 35.  1993. Rapid kinetics of mismatch repair of heteroduplex DNA that is formed during recombination in yeast. PNAS 90:3363–67 [Google Scholar]
  36. Harrison JC, Haber JE. 36.  2006. Surviving the breakup: the DNA damage checkpoint. Annu. Rev. Genet. 40:209–35 [Google Scholar]
  37. Hentges P, Ahnesorg P, Pitcher RS, Bruce CK, Kysela B. 37.  et al. 2006. Evolutionary and functional conservation of the DNA non-homologous end-joining protein, XLF/Cernunnos. J. Biol. Chem. 281:37517–26 [Google Scholar]
  38. Herskowitz I. 38.  1989. A regulatory hierarchy for cell specialization in yeast. Nature 342:749–57 [Google Scholar]
  39. Heyer WD. 39.  2007. Biochemistry of eukaryotic homologous recombination. Molecular Genetics of Recombination A Aguilera, R Rothstein 95–133 Top. Curr. Genet. Ser. 17 Berlin: Springer-Verlag [Google Scholar]
  40. Hicks WM, Kim M, Haber JE. 40.  2010. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329:82–85 [Google Scholar]
  41. Hicks WM, Yamaguchi M, Haber JE. 41.  2011. Inaugural article: real-time analysis of double-strand DNA break repair by homologous recombination. PNAS 108:3108–15 [Google Scholar]
  42. Holbeck SL, Strathern JN. 42.  1997. A role for REV3 in mutagenesis during double-strand break repair in Saccharomyces cerevisiae. Genetics 147:1017–24 [Google Scholar]
  43. Holliday R. 43.  1964. A mechanism for gene conversion in fungi. Genet. Res. 5:282–304 [Google Scholar]
  44. Holmes AM, Haber JE. 44.  1999. Double-strand break repair in yeast requires both leading and lagging strand DNA polymerases. Cell 96:415–24 [Google Scholar]
  45. Horigome C, Oma Y, Konishi T, Schmid R, Marcomini I. 45.  et al. 2014. SWR1 and INO80 chromatin remodelers contribute to DNA double-strand break perinuclear anchorage site choice. Mol. Cell 55:626–39 [Google Scholar]
  46. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP. 46.  2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455:689–92 [Google Scholar]
  47. Huertas P, Jackson SP. 47.  2009. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J. Biol. Chem. 284:9558–65 [Google Scholar]
  48. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L. 48.  et al. 2010. High-resolution profiling of γH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29:1446–57 [Google Scholar]
  49. Ira G, Haber JE. 49.  2002. Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol. Cell. Biol. 22:6384–92 [Google Scholar]
  50. Ira G, Malkova A, Liberi G, Foiani M, Haber JE. 50.  2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–11 [Google Scholar]
  51. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S. 51.  et al. 2004. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011–17 [Google Scholar]
  52. Ivanov EL, Sugawara N, White CI, Fabre F, Haber JE. 52.  1994. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:3414–25 [Google Scholar]
  53. Jacquier A, Dujon B. 53.  1985. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41:383–94 [Google Scholar]
  54. Jain S, Sugawara N, Haber JE. 54.  2016. Role of double-strand break end-tethering during gene conversion in Saccharomyces cerevisiae. PLOS Genet. 12:e1005976 [Google Scholar]
  55. Jain S, Sugawara N, Lydeard J, Vaze M, Tanguy le Gac N, Haber JE. 55.  2009. A recombination execution checkpoint regulates the choice of homologous recombination pathway during DNA double-strand break repair. Genes Dev. 23:291–303 [Google Scholar]
  56. Jain S, Sugawara N, Mehta A, Ryu T, Haber JE. 56.  2016. Sgs1 and Mph1 enforce the recombination execution checkpoint during DNA double-strand break repair in Saccharomyces cerevisiae. Genetics. 203:667–75 [Google Scholar]
  57. Jasin M, Haber JE. 57.  2016. The democratization of gene editing: Insights from site-specific cleavage and double-strand break repair. DNA Rep. 44:6–16 [Google Scholar]
  58. Jasin M, Rothstein R. 58.  2013. Repair of strand breaks by homologous recombination. Cold Spring Harb. Perspect. Biol. 5:a012740 [Google Scholar]
  59. Jensen RE, Herskowitz I. 59.  1984. Directionality and regulation of cassette substitution in yeast. Cold Spring Harb. Symp. Quant. Biol. 49:97–104 [Google Scholar]
  60. Katz SS, Gimble FS, Storici F. 60.  2014. To nick or not to nick: comparison of I-SceI single- and double-strand break-induced recombination in yeast and human cells. PLOS ONE 9:e88840 [Google Scholar]
  61. Kaye JA, Melo JA, Cheung SK, Vaze MB, Haber JE, Toczyski DP. 61.  2004. DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr. Biol. 14:2096–106 [Google Scholar]
  62. Kegel A, Sjostrand JO, Astrom SU. 62.  2001. Nej1p, a cell type–specific regulator of nonhomologous end joining in yeast. Curr. Biol. 11:1611–17 [Google Scholar]
  63. Kim JA, Haber JE. 63.  2009. Chromatin assembly factors Asf1 and CAF-1 have overlapping roles in deactivating the DNA damage checkpoint when DNA repair is complete. PNAS 106:1151–56 [Google Scholar]
  64. Kim JA, Kruhlak M, Dotiwala F, Nussenzweig A, Haber JE. 64.  2007. Heterochromatin is refractory to γ-H2AX modification in yeast and mammals. J. Cell Biol. 178:209–18 [Google Scholar]
  65. Kostriken R, Strathern JN, Klar AJ, Hicks JB, Heffron F. 65.  1983. A site-specific endonuclease essential for mating-type switching in Saccharomyces cerevisiae. Cell 35:167–74 [Google Scholar]
  66. Kramer KM, Brock JA, Bloom K, Moore JK, Haber JE. 66.  1994. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol. 14:1293–301 [Google Scholar]
  67. Lee CS, Haber JE. 67.  2015. Mating-type gene switching in Saccharomyces cerevisiae. Microbiol. Spectr. 3:MDNA3–0013-2014 [Google Scholar]
  68. Lee CS, Lee K, Legube G, Haber JE. 68.  2014. Dynamics of yeast histone H2A and H2B phosphorylation in response to a double-strand break. Nat. Struct. Mol. Biol. 21:103–9 [Google Scholar]
  69. Lee JY, Terakawa T, Qi Z, Steinfeld JB, Redding S. 69.  et al. 2015. DNA recombination: base triplet stepping by the Rad51/RecA family of recombinases. Science 349:977–81 [Google Scholar]
  70. Lee CS, Wang RW, Chang HH, Capurso D, Segal MR, Haber JE. 70.  2016. Chromosome position determines the success of double-strand break repair. PNAS 113:E146–54 [Google Scholar]
  71. Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, Haber JE. 71.  1998. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399–409 [Google Scholar]
  72. Lee SE, Pellicioli A, Malkova A, Foiani M, Haber JE. 72.  2001. The Saccharomyces recombination protein Tid1p is required for adaptation from G2/M arrest induced by a double-strand break. Curr. Biol. 11:1053–57 [Google Scholar]
  73. Lee SE, Pellicioli A, Vaze MB, Sugawara N, Malkova A. 73.  et al. 2003. Yeast rad52 and rad51 recombination proteins define a second pathway of DNA damage assessment in response to a single double-strand break. Mol. Cell. Biol. 23:8913–23 [Google Scholar]
  74. Leroy C, Lee SE, Vaze MB, Ochsenbein F, Guerois R. 74.  et al. 2003. PP2C phosphatases Ptc2 and Ptc3 are required for DNA checkpoint inactivation after a double-strand break. Mol. Cell 11:827–35 [Google Scholar]
  75. Li F, Dong J, Pan X, Oum JH, Boeke JD, Lee SE. 75.  2008. Microarray-based genetic screen defines SAW1, a gene required for Rad1/Rad10-dependent processing of recombination intermediates. Mol. Cell 30:325–35 [Google Scholar]
  76. Li J, Coic E, Lee K, Lee CS, Kim JA. 76.  et al. 2012. Regulation of budding yeast mating-type switching donor preference by the FHA domain of Fkh1. PLOS Genet. 8:e1002630 [Google Scholar]
  77. Liras P, McCusker J, Mascioli S, Haber JE. 77.  1978. Characterization of a mutation in yeast causing nonrandom chromosome loss during mitosis. Genetics 88:651–71 [Google Scholar]
  78. Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer WD. 78.  2011. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479:245–48 [Google Scholar]
  79. Lobachev K, Vitriol E, Stemple J, Resnick MA, Bloom K. 79.  2004. Chromosome fragmentation after induction of a double-strand break is an active process prevented by the RMX repair complex. Curr. Biol. 14:2107–12 [Google Scholar]
  80. Lovett ST, Mortimer RK. 80.  1987. Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics 116:547–53 [Google Scholar]
  81. Lydeard JR, Jain S, Yamaguchi M, Haber JE. 81.  2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448:820–23 [Google Scholar]
  82. Lydeard JR, Lipkin-Moore Z, Jain S, Eapen VV, Haber JE. 82.  2010. Sgs1 and Exo1 redundantly inhibit break-induced replication and de novo telomere addition at broken chromosome ends. PLOS Genet. 6:e1000973 [Google Scholar]
  83. Lydeard JR, Lipkin-Moore Z, Sheu YJ, Stillman B, Burgers PM, Haber JE. 83.  2010. Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev. 24:1133–44 [Google Scholar]
  84. Lyndaker AM, Goldfarb T, Alani E. 84.  2008. Mutants defective in Rad1-Rad10-Slx4 exhibit a unique pattern of viability during mating-type switching in Saccharomyces cerevisiae. Genetics 179:1807–21 [Google Scholar]
  85. Ma JL, Kim EM, Haber JE, Lee SE. 85.  2003. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23:8820–28 [Google Scholar]
  86. Malik PS, Symington LS. 86.  2008. Rad51 gain-of-function mutants that exhibit high affinity DNA binding cause DNA damage sensitivity in the absence of Srs2. Nucleic Acids Res. 36:6504–10 [Google Scholar]
  87. Malkova A, Klein F, Leung WY, Haber JE. 87.  2000. HO endonuclease-induced recombination in yeast meiosis resembles Spo11-induced events. PNAS 97:14500–5 [Google Scholar]
  88. Malkova A, Naylor M, Yamaguchi M, Ira G, Haber JE. 88.  2005. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25:933–44 [Google Scholar]
  89. Malkova A, Signon L, Schaefer CB, Naylor ML, Theis JF. 89.  et al. 2001. RAD51-independent break-induced replication to repair a broken chromosome depends on a distant enhancer site. Genes Dev. 15:1055–60 [Google Scholar]
  90. Maloisel L, Fabre F, Gangloff S. 90.  2008. DNA polymerase-δ is preferentially recruited during homologous recombination to promote heteroduplex DNA extension. Mol. Cell. Biol. 28:1373–82 [Google Scholar]
  91. Mayle R, Campbell IM, Beck CR, Yu Y, Wilson M. 91.  et al. 2015. Mus81 and converging forks limit the mutagenicity of replication fork breakage. Science 349:742–47 [Google Scholar]
  92. McClintock B. 92.  1956. Controlling elements and the gene. Cold Spring Harbor Symp. Quant. Biol. 21:197–216 [Google Scholar]
  93. McEntee K, Weinstock GM, Lehman IR. 93.  1979. Initiation of general recombination catalyzed in vitro by the recA protein of Escherichia coli. PNAS 76:2615–19 [Google Scholar]
  94. McVey M, Lee SE. 94.  2008. MMEJ repair of double-strand breaks (director's cut): deleted sequences and alternative endings. Trends Genet. 24:529–38 [Google Scholar]
  95. Meselson MM, Radding CM. 95.  1975. A general model for genetic recombination. PNAS 72:358–61 [Google Scholar]
  96. Mimitou EP, Symington LS. 96.  2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770–74 [Google Scholar]
  97. Mimitou EP, Symington LS. 97.  2010. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J. 29:3358–69 [Google Scholar]
  98. Mine-Hattab J, Rothstein R. 98.  2012. Increased chromosome mobility facilitates homology search during recombination. Nat. Cell Biol. 14:510–17 [Google Scholar]
  99. Moore JK, Haber JE. 99.  1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164–73 [Google Scholar]
  100. Nasmyth K. 100.  1983. Molecular analysis of a cell lineage. Nature 302:670–76 [Google Scholar]
  101. Ogawa T, Wabiko H, Tsurimoto T, Horii T, Masukata H, Ogawa H. 101.  1979. Characteristics of purified recA protein and the regulation of its synthesis in vivo. Cold Spring Harb. Symp. Quant. Biol. 43:Pt 2909–15 [Google Scholar]
  102. Ooi SL, Boeke JD. 102.  2001. A DNA microarray-based genetic screen for nonhomologous end-joining mutants in Saccharomyces cerevisiae. Science 294:2552–56 [Google Scholar]
  103. Oshima Y, Takano I. 103.  1971. Mating types in Saccharomyces: their convertibility and homothallism. Genetics 67:327–35 [Google Scholar]
  104. Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE. 104.  2001. Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage–induced G2/M arrest. Mol. Cell 7:293–300 [Google Scholar]
  105. Plessis A, Perrin A, Haber JE, Dujon B. 105.  1992. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics 130:451–60 [Google Scholar]
  106. Prakash R, Satory D, Dray E, Papusha A, Scheller J. 106.  et al. 2009. Yeast Mph1 helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev. 23:67–79 [Google Scholar]
  107. Ray BL, White CI, Haber JE. 107.  1991. Heteroduplex formation and mismatch repair of the “stuck” mutation during mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:5372–80 [Google Scholar]
  108. Renkawitz J, Lademann CA, Jentsch S. 108.  2013. γH2AX spreading linked to homology search. Cell Cycle 12:2526–27 [Google Scholar]
  109. Renkawitz J, Lademann CA, Kalocsay M, Jentsch S. 109.  2013. Monitoring homology search during DNA double-strand break repair in vivo. Mol. Cell 50:261–72 [Google Scholar]
  110. Resnick MA. 110.  1976. The repair of double-strand breaks in DNA: a model involving recombination. J. Theor. Biol. 59:97–106 [Google Scholar]
  111. Rouet P, Smih F, Jasin M. 111.  1994. Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. Mol. Cell. Biol. 14:8096–106 [Google Scholar]
  112. Rudin N, Sugarman E, Haber JE. 112.  1989. Genetic and physical analysis of double-strand break repair and recombination in Saccharomyces cerevisiae. Genetics 122:519–34 [Google Scholar]
  113. Ruff P, Koh KD, Keskin H, Pai RB, Storici F. 113.  2014. Aptamer-guided gene targeting in yeast and human cells. Nucleic Acids Res. 42:e61 [Google Scholar]
  114. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y. 114.  et al. 2013. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502:389–92 [Google Scholar]
  115. Sakofsky CJ, Ayyar S, Deem AK, Chung WH, Ira G, Malkova A. 115.  2015. Translesion polymerases drive microhomology-mediated break-induced replication leading to complex chromosomal rearrangements. Mol. Cell 60:860–72 [Google Scholar]
  116. Sanchez Y, Desany BA, Jones WJ, Liu Q, Wang B, Elledge SJ. 116.  1996. Regulation of RAD53 by the ATM-like kinases MEC1 and TEL1 in yeast cell cycle checkpoint pathways. Science 271:357–60 [Google Scholar]
  117. Sandell LL, Zakian VA. 117.  1993. Loss of a yeast telomere: arrest, recovery, and chromosome loss. Cell 75:729–39 [Google Scholar]
  118. Shen Y, Nandi P, Taylor MB, Stuckey S, Bhadsavle HP. 118.  et al. 2011. RNA-driven genetic changes in bacteria and in human cells. Mutat. Res. 717:91–98 [Google Scholar]
  119. Shibata T, DasGupta C, Cunningham RP, Radding CM. 119.  1979. Purified Escherichia coli recA protein catalyzes homologous pairing of superhelical DNA and single-stranded fragments. PNAS 76:1638–42 [Google Scholar]
  120. Shroff R, Arbel-Eden A, Pilch D, Ira G, Bonner WM. 120.  et al. 2004. Distribution and dynamics of chromatin modification induced by a defined DNA double-strand break. Curr. Biol. 14:1703–11 [Google Scholar]
  121. Signon L, Malkova A, Naylor ML, Klein H, Haber JE. 121.  2001. Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21:2048–56 [Google Scholar]
  122. Sinha S, Villarreal D, Shim EY, Lee SE. 122.  2016. Risky business: microhomology-mediated end joining. Mutat. Res. 788:17–24 [Google Scholar]
  123. Smith CE, Llorente B, Symington LS. 123.  2007. Template switching during break-induced replication. Nature 447:102–5 [Google Scholar]
  124. Storici F, Snipe JR, Chan GK, Gordenin DA, Resnick MA. 124.  2006. Conservative repair of a chromosomal double-strand break by single-strand DNA through two steps of annealing. Mol. Cell. Biol. 26:7645–57 [Google Scholar]
  125. Strathern JN, Klar AJ, Hicks JB, Abraham JA, Ivy JM. 125.  et al. 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31:183–92 [Google Scholar]
  126. Strecker J, Gupta GD, Zhang W, Bashkurov M, Landry MC. 126.  et al. 2016. DNA damage signalling targets the kinetochore to promote chromatin mobility. Nat. Cell Biol. 18:281–90 [Google Scholar]
  127. Sugawara N, Goldfarb T, Studamire B, Alani E, Haber JE. 127.  2004. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. PNAS 101:9315–20 [Google Scholar]
  128. Sugawara N, Haber JE. 128.  2012. Monitoring DNA recombination initiated by HO endonuclease. Methods Mol. Biol. 920:349–70 [Google Scholar]
  129. Sugawara N, Ira G, Haber JE. 129.  2000. DNA length dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol. Cell. Biol. 20:5300–9 [Google Scholar]
  130. Sugawara N, Paques F, Colaiacovo M, Haber JE. 130.  1997. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. PNAS 94:9214–19 [Google Scholar]
  131. Sugawara N, Wang X, Haber JE. 131.  2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209–19 [Google Scholar]
  132. Sugiyama T, Kowalczykowski SC. 132.  2002. Rad52 protein associates with RPA-ssDNA to accelerate Rad51-mediated displacement of RPA and presynaptic complex formation. J. Biol. Chem. 19:19 [Google Scholar]
  133. Sun K, Coic E, Zhou Z, Durrens P, Haber JE. 133.  2002. Saccharomyces forkhead protein Fkh1 regulates donor preference during mating-type switching through the recombination enhancer. Genes Dev. 16:2085–96 [Google Scholar]
  134. Sung P. 134.  1994. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast Rad51 protein. Science 265:1241–43 [Google Scholar]
  135. Szostak JW, Orr WT, Rothstein RJ, Stahl FW. 135.  1983. The double-strand-break repair model for recombination. Cell 33:25–35 [Google Scholar]
  136. Takano I, Oshima Y. 136.  1970. Mutational nature of an allele-specific conversion of the mating type by the homothallic gene HOα in Saccharomyces. Genetics 65:421–27 [Google Scholar]
  137. Toczyski DP, Galgoczy DJ, Hartwell LH. 137.  1997. CDC5 and CKII control adaptation to the yeast DNA damage checkpoint. Cell 90:1097–106 [Google Scholar]
  138. Toh GW, Sugawara N, Dong J, Toth R, Lee SE. 138.  et al. 2010. Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1-Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair 9:718–26 [Google Scholar]
  139. Tomkinson AE, Bardwell AJ, Bardwell L, Tappe NJ, Friedberg EC. 139.  1993. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature 362:860–62 [Google Scholar]
  140. Tsaponina O, Haber JE. 140.  2014. Frequent interchromosomal template switches during gene conversion in S. cerevisiae. Mol. Cell 55:615–25 [Google Scholar]
  141. Valencia M, Bentele M, Vaze MB, Herrmann G, Kraus E. 141.  et al. 2001. NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414:666–69 [Google Scholar]
  142. Vaze M, Pellicioli A, Lee S, Ira G, Liberi G. 142.  et al. 2002. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell 10:373 [Google Scholar]
  143. Vidanes GM, Sweeney FD, Galicia S, Cheung S, Doyle JP. 143.  et al. 2010. CDC5 inhibits the hyperphosphorylation of the checkpoint kinase Rad53, leading to checkpoint adaptation. PLOS Biol. 8:e1000286 [Google Scholar]
  144. Vrielynck N, Chambon A, Vezon D, Pereira L, Chelysheva L. 144.  et al. 2016. A DNA topoisomerase VI-like complex initiates meiotic recombination. Science 351:939–43 [Google Scholar]
  145. Wang X, Haber JE. 145.  2004. Role of Saccharomyces single-stranded DNA-binding protein RPA in the strand invasion step of double-strand break repair. PLOS Biol. 2:104–11 [Google Scholar]
  146. Wang X, Ira G, Tercero JA, Holmes AM, Diffley JF, Haber JE. 146.  2004. Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 24:6891–99 [Google Scholar]
  147. Weiffenbach B, Rogers DT, Haber JE, Zoller M, Russell DW, Smith M. 147.  1983. Deletions and single base pair changes in the yeast mating type locus that prevent homothallic mating type conversions. PNAS 80:3401–5 [Google Scholar]
  148. Weng YS, Nickoloff JA. 148.  1998. Evidence for independent mismatch repair processing on opposite sides of a double-strand break in Saccharomyces cerevisiae. Genetics 148:59–70 [Google Scholar]
  149. Weng YS, Whelden J, Gunn L, Nickoloff JA. 149.  1996. Double-strand break-induced mitotic gene conversion: examination of tract polarity and products of multiple recombinational repair events. Curr. Genet. 29:335–43 [Google Scholar]
  150. White CI, Haber JE. 150.  1990. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9:663–73 [Google Scholar]
  151. White RL, Fox MS. 151.  1975. Heterozygosity in unreplicated bacteriophage λ recombinants. Genetics 81:33–50 [Google Scholar]
  152. Willetts NS, Clark AJ, Low B. 152.  1969. Genetic location of certain mutations conferring recombination deficiency in Escherichia coli. J. Bacteriol. 97:244–49 [Google Scholar]
  153. Wilson MA, Kwon Y, Xu Y, Chung WH, Chi P. 153.  et al. 2013. Pif1 helicase and Polδ promote recombination-coupled DNA synthesis via bubble migration. Nature 502:393–96 [Google Scholar]
  154. Wilson TE. 154.  2002. A genomics-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics 162:677–88 [Google Scholar]
  155. Wolner B, van Komen S, Sung P, Peterson CL. 155.  2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12:221–32 [Google Scholar]
  156. Wu L, Hickson ID. 156.  2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870–74 [Google Scholar]
  157. Wu X, Haber JE. 157.  1996. A 700 bp cis-acting region controls mating-type dependent recombination along the entire left arm of yeast chromosome III. Cell 87:277–85 [Google Scholar]
  158. Yang D, Boyer B, Prévost C, Danilowicz C, Prentiss M. 158.  2015. Integrating multi-scale data on homologous recombination into a new recognition mechanism based on simulations of the RecA-ssDNA/dsDNA structure. Nucleic Acids Res. 43:2110251–63 [Google Scholar]
  159. Yeeles JT, Poli J, Marians KJ, Pasero P. 159.  2013. Rescuing stalled or damaged replication forks. Cold Spring Harb. Perspect. Biol. 5:a012815 [Google Scholar]
  160. Zhou Y, Caron P, Legube G, Paull TT. 160.  2014. Quantitation of DNA double-strand break resection intermediates in human cells. Nucleic Acids Res. 42:e19 [Google Scholar]
  161. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 161.  2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981–94 [Google Scholar]
  162. Zierhut C, Diffley JF. 162.  2008. Break dosage, cell cycle stage and DNA replication influence DNA double strand break response. EMBO J. 27:1875–85 [Google Scholar]
  163. Zinn AR, Butow RA. 163.  1984. Kinetics and intermediates of yeast mitochondrial DNA recombination. Cold Spring Harb. Symp. Quant. Biol. 49:115–21 [Google Scholar]
  164. Zou L, Elledge SJ. 164.  2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–48 [Google Scholar]
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