Noncanonical views of homology-directed DNA repair

Genes and Development

Volumn 30, Issue 10, 2016, Pages 1138-1154

  Verma, Priyanka ^a   Greenberg, Roger A ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ALT; Break induced replication; DNA repair; Homologous recombination; Telomere

Indexed keywords

RAD51 PROTEIN; SINGLE STRANDED DNA;

DNA END JOINING REPAIR; DNA SYNTHESIS; EUKARYOTE; GENE CONVERSION; GENE REARRANGEMENT; GENETIC VARIABILITY; GENOMICS; NONHUMAN; PRIORITY JOURNAL; PROKARYOTE; REVIEW; TELOMERE HOMEOSTASIS; ANIMAL; DNA REPLICATION; DNA TEMPLATE; DOUBLE STRANDED DNA BREAK; GENETICS; HUMAN; METABOLISM; NEOPLASM; NUCLEIC ACID HYBRIDIZATION; RECOMBINATION REPAIR; SEQUENCE HOMOLOGY; TELOMERE;

ANIMALS; DNA BREAKS, DOUBLE-STRANDED; DNA REPLICATION; DNA, SINGLE-STRANDED; HUMANS; NEOPLASMS; NUCLEIC ACID HYBRIDIZATION; RAD51 RECOMBINASE; RECOMBINATIONAL DNA REPAIR; SEQUENCE HOMOLOGY, NUCLEIC ACID; TELOMERE; TEMPLATES, GENETIC;

EID: 84969760939     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.280545.116     Document Type: Review

References (220)

1. Adair GM, Rolig RL, Moore-Faver D, Zabelshansky M, Wilson JH, Nairn RS. 2000. Role of ERCC1 in removal of long non-homologous tails during targeted homologous recombination. EMBO J 19: 5552-5561.
2. Adams MD, McVey M, Sekelsky JJ. 2003. DrosophilaBLMin double- strand break repair by synthesis-dependent strand annealing. Science 299: 265-267.
3. Adelman CA, Boulton SJ. 2010. Metabolism of postsynaptic recombination intermediates. FEBS Lett 584: 3709-3716.
4. Agmon N, Pur S, Liefshitz B, Kupiec M. 2009. Analysis of repair mechanism choice during homologous recombination. Nucleic Acids Res 37: 5081-5092.
5. Allers T, Lichten M. 2009. Differential timing and control of noncrossover and crossover recombination during meiosis. Cell 106: 47-57.
6. Anand RP, Lovett ST, Haber JE. 2013. Break-induced DNA replication. Cold Spring Harb Perspect Biol 5: a010397.
7. Aniukwu J, Glickman MS, Shuman S. 2008. The pathways and outcomes of mycobacterial NHEJ depend on the structure of the broken DNA ends. Genes Dev 22: 512-527.
8. Asai T, Sommer S, Bailone A, Kogoma T. 1993. Homologous recombination- dependent initiation of DNA replication from DNA damage-inducible origins in Escherichia coli. EMBO J 12: 3287-3295.
9. Audebert M, Salles B, Calsou P. 2004. Involvement of poly(ADPribose) polymerase-1 and XRCC1/DNA ligase III in an alternative route for DNA double-strand breaks rejoining. J Biol Chem 279: 55117-55126.
10. Ayora S, Carrasco B, Cardenas PP, Cesar CE, Canas C, Yadav T, Marchisone C, Alonso JC. 2011. Double-strand break repair in bacteria: a view from Bacillus subtilis. FEMS Microbiol Rev 35: 1055-1081.
11. Bai Y, Symington LS. 1996. A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev 10: 2025-2037.
12. Beck CR, Carvalho CMB, Banser L, Gambin T, Stubbolo D, Yuan B, Sperle K, McCahan SM, Henneke M, Seeman P, et al. 2015. Complex genomic rearrangements at the PLP1 locus include triplication and quadruplication. PLoS Genet 11: e1005050.
13. Belmaaza A, Chartrand P. 1994. One-sided invasion events in homologous recombination at double-strand breaks. Mutat Res 314: 199-208.
14. Bennardo N, Cheng A, Huang N, Stark JM. 2008. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 4: e1000110.
15. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Sivachenko AY, Sboner A, Esgueva R, Pflueger D, Sougnez C, et al. 2011. The genomic complexity of primary human prostate cancer. Nature 470: 214-220.
16. Bosco G, Haber JE. 1998. Chromosome break-induced DNA replication leads to nonreciprocal translocations and telomere capture. Genetics 150: 1037-1047.
17. Boulton SJ, Jackson SP. 1996. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J 15: 5093-5103.
18. Bowater R, Doherty AJ. 2006. Making ends meet: repairing breaks in bacterial DNA by non-homologous end-joining. PLoS Genet 2: e8.
19. Brenneman MA, Wagener BM, Miller CA, Allen C, Nickoloff JA. 2002. XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol Cell 10: 387-395.
20. Bryan TM, Englezou A, Gupta J, Bacchetti S, Reddel RR. 1995. Telomere elongation in immortal human cells without detectable telomerase activity. EMBO J 14: 4240-4248.
21. Bryant HE, Schultz N, Thomas HD, Parker KM, Flower D, Lopez E, Kyle S, Meuth M, Curtin NJ, Helleday T. 2005. Specific killing of BRCA2-deficient tumours with inhibitors of poly(ADPribose) polymerase. Nature 434: 913-917.
22. Bryk M, Belisle M, Mueller JE, Belfort M. 1995. Selection of a remote cleavage site by I-tevI, the td intron-encoded endonuclease. J Mol Biol 247: 197-210.
23. Bunting SF, Nussenzweig A. 2013. End-joining, translocations and cancer. Nat Rev Cancer 13: 443-454.
24. Bzymek M, Lovett ST. 2001. Evidence for two mechanisms of palindrome- stimulated deletion in Escherichia coli: single-strand annealing and replication slipped mispairing. Genetics 158: 527-540.
25. Cannavo E, Cejka P. 2014. Sae2 promotes dsDNA endonuclease activity within Mre11-Rad50-Xrs2 to resect DNA breaks. Nature 514: 122-125.
26. Carvalho CMB, Lupski JR. 2016. Mechanisms underlying structural variant formation in genomic disorders. Nat Rev Genet 17: 224-238.
27. Carvalho CM, Zhang F, Lupski JR. 2011. Structural variation of the human genome: mechanisms, assays, and role in male infertility. Syst Biol Reprod Med 57: 3-16.
28. Carvalho CMB, Pehlivan D, Ramocki MB, Fang P, Alleva B, Franco LM, Belmont JW, Hastings PJ, Lupski JR. 2013. Replicative mechanisms for CNV formation are error prone. Nat Genet 45: 1319-1326.
29. Carvalho CMB, Pfundt R, King DA, Lindsay SJ, Zuccherato LW, Macville MVE, Liu P, Johnson D, Stankiewicz P, Brown CW, et al. 2015. Absence of heterozygosity due to template switching during replicative rearrangements. Am J Hum Genet 96: 555-564.
30. Ceccaldi R, Liu JC, Amunugama R, Hajdu I, Primack B, Petalcorin MIR, O’Connor KW, Konstantinopoulos PA, Elledge SJ, Boulton SJ, et al. 2015. Homologous-recombination-deficient tumours are dependent on Poltheta-mediated repair. Nature 518: 258-262.
31. Ceccaldi R, Rondinelli B, D’Andrea AD. 2016. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol 26: 52-64.
32. Cesare AJ, Griffith JD. 2004. Telomeric DNA in ALT cells is characterized by free telomeric circles and heterogeneous t-loops. Mol Cell Biol 24: 9948-9957.
33. Cesare AJ, Reddel RR. 2010. Alternative lengthening of telomeres: models, mechanisms and implications. Nat Rev Genet 11: 319-330.
34. Cesare AJ, Kaul Z, Cohen SB, Napier CE, Pickett HA, Neumann AA, Reddel RR. 2009. Spontaneous occurrence of telomeric DNA damage response in the absence of chromosome fusions. Nat Struct Mol Biol 16: 1244-1251.
35. Chan SH, Yu AM, McVey M. 2010. Dual roles for DNA polymerase theta in alternative end-joining repair of double-strand breaks in Drosophila. PLoS Genet 6: e1001005.
36. Chandramouly G, Kwok A, Huang B, Willis NA, Xie A, Scully R. 2013. BRCA1 and CtIP suppress long-tract gene conversion between sister chromatids. Nat Commun 4: 2404.
37. Chapman JR, Taylor MRG, Boulton SJ. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497-510.
38. Chayot R, Montagne B, Mazel D, Ricchetti M. 2010. An end-joining repair mechanism in Escherichia coli. Proc Natl Acad Sci 107: 2141-2146.
39. Chen C, Umezu K, Kolodner RD. 1998. Chromosomal rearrangements occur in S. cerevisiae rfa1 mutator mutants due to mutagenic lesions processed by double-strand-break repair. Mol Cell 2: 9-22.
40. Chen Q, Ijpma A, Greider CW. 2001. Two survivor pathways that allow growth in the absence of telomerase are generated by distinct telomere recombination events. Mol Cell Biol 21: 1819-1827.
41. Cho NW, Dilley RL, Lampson MA, Greenberg RA. 2014. Interchromosomal homology searches drive directional ALT telomere movement and synapsis. Cell 159: 108-121.
42. Chung W-H, Zhu Z, Papusha A, Malkova A, Ira G. 2010. Defective resection at DNA double-strand breaks leads to de novo telomere formation and enhances gene targeting. PLoS Genet 6: e1000948.
43. Compton SA, Choi J-H, Cesare AJ, Özgür S, Griffith JD. 2007. Xrcc3 and Nbs1 are required for the production of extrachromosomal telomeric circles in human alternative lengthening of telomere cells. Cancer Res 67: 1513-1519.
44. Conomos D, Stutz MD, Hills M, Neumann AA, Bryan TM, Reddel RR, Pickett HA. 2012. Variant repeats are interspersed throughout the telomeres and recruit nuclear receptors in ALT cells. J Cell Biol 199: 893-906.
45. Corneo B, Wendland RL, Deriano L, Cui X, Klein IA, Wong S-Y, Arnal S, Holub AJ, Weller GR, Pancake BA, et al. 2007. Rag mutations reveal robust alternative end joining. Nature 449: 483-486.
46. Costantino L, Sotiriou SK, Rantala JK, Magin S, Mladenov E, Helleday T, Haber JE, Iliakis G, Kallioniemi OP, Halazonetis TD. 2014. Break-induced replication repair of damaged forks induces genomic duplications in human cells. Science 343: 88-91.
47. Cox KE, Marechal A, Flynn RL. 2016. SMARCAL1 resolves replication stress at ALT telomeres. Cell Rep 14: 1032-1040.
48. Daigaku Y, Keszthelyi A, Müller CA, Miyabe I, Brooks T, Retkute R, Hubank M, Nieduszynski CA, Carr AM. 2015.Aglobal profile of replicative polymerase usage. Nat Struct Mol Biol 22: 192-198.
49. Davis AP, Symington LS. 2004. RAD51-dependent break-induced replication in yeast. Mol Cell Biol 24: 2344-2351.
50. Decottignies A. 2007. Microhomology-mediated end joining in fission yeast is repressed by pku70 and relies on genes involved in homologous recombination. Genetics 176: 1403-1415.
51. de Koning APJ, Gu W, Castoe TA, Batzer MA, Pollock DD. 2011. Repetitive elements may comprise over two-thirds of the human genome. PLoS Genet 7: e1002384.
52. Deng SK, Gibb B, de Almeida MJ, Greene EC, Symington LS. 2014. RPA antagonizes microhomology-mediated repair of DNA double-strand breaks. Nat Struct Mol Biol 21: 405-412.
53. Dewar JM, Lydall D. 2010. Pif1- and Exo1-dependent nucleases coordinate checkpoint activation following telomere uncapping. EMBO J 29: 4020-4034.
54. Difilippantonio MJ, Petersen S, Chen HT, Johnson R, Jasin M, Kanaar R, Ried T, Nussenzweig A. 2002. Evidence for replicative repair of DNA double-strand breaks leading to oncogenic translocation and gene amplification. J Exp Med 196: 469-480.
55. Dilley RL, Greenberg RA. 2015. ALTernative telomere maintenance and cancer. Trends Cancer 1: 145-156.
56. Dinkelmann M, Spehalski E, Stoneham T, Buis J, Wu Y, Sekiguchi JM, Ferguson DO. 2009. Multiple functions of MRN in end-joining pathways during isotype class switching. Nat Struct Mol Biol 16: 808-813.
57. Donnianni RA, Symington LS. 2013. Break-induced replication occurs by conservative DNA synthesis. Proc Natl Acad Sci 110: 13475-13480.
58. Drosopoulos WC, Kosiyatrakul ST, Schildkraut CL. 2015. BLM helicase facilitates telomere replication during leading strand synthesis of telomeres. J Cell Biol 210: 191-208.
59. Dudley DD, Chaudhuri J, Bassing CH, Alt FW. 2005. Mechanism and control of V(D)J recombination versus class switch recombination: similarities and differences. Adv Immunol 86: 43-112.
60. Dunham MA, Neumann AA, Fasching CL, Reddel RR. 2000. Telomere maintenance by recombination in human cells. Nat Genet 26: 447-450.
61. Dupaigne P, Le Breton C, Fabre F, Gangloff S, Le Cam E, Veaute X. 2008. The Srs2 helicase activity is stimulated by Rad51 filaments on dsDNA: implications for crossover incidence during mitotic recombination. Mol Cell 29: 243-254.
62. Elliott B, Richardson C, Jasin M. 2005. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol Cell 17: 885-894.
63. Esposito MS. 1978. Evidence that spontaneous mitotic recombination occurs at the two-strand stage. Proc Natl Acad Sci 75: 4436-4440.
64. Farmer H, McCabe N, Lord CJ, Tutt ANJ, Johnson DA, Richardson TB, Santarosa M, Dillon KJ, Hickson I, Knights C, et al. 2005. Targeting the DNA repair defect in BRCA mutant cells as a therapeutic strategy. Nature 434: 917-921.
65. Fasching CL, Cejka P, Kowalczykowski SC, Heyer W-D. 2015. Top3-Rmi1 dissolve Rad51-mediated D loops by a topoisomerase-based mechanism. Mol Cell 57: 595-606.
66. Ferguson DO, Holloman WK. 1996. Recombinational repair of gaps inDNAis asymmetric in Ustilago maydis and can be explained by a migrating D-loop model. Proc Natl Acad Sci 93: 5419-5424.
67. Finn KJ, Li JJ. 2013. Single-stranded annealing induced by re-initiation of replication origins provides a novel and efficient mechanism for generating copy number expansion via non-allelic homologous recombination. PLoS Genet 9: e1003192.
68. Fishman-Lobell J, Haber J. 1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258: 480-484.
69. 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.
70. Flynn RL, Cox KE, Jeitany M, Wakimoto H, Bryll AR, Ganem NJ, Bersani F, Pineda JR, Suva ML, Benes CH, et al. 2015. Alternative lengthening of telomeres renders cancer cells hypersensitive to ATR inhibitors. Science 347: 273-277.
71. Fukui K, Nakagawa N, Kitamura Y, Nishida Y, Masui R, Kuramitsu S. 2008. Crystal structure of MutS2 endonuclease domain and the mechanism of homologous recombination suppression. J Biol Chem 283: 33417-33427.
72. Gabbai CB, Marians KJ. 2010. Recruitment to stalled replication forks of the PriA DNA helicase and replisome-loading activities is essential for survival. DNA Repair (Amst) 9: 202-209.
73. Garcia V, Phelps SEL, Gray S, Neale MJ. 2011. Bidirectional resection of DNA double-strand breaks by Mre11 and Exo1. Nature 479: 241-244.
74. Gari K, Décaillet C, Stasiak AZ, Stasiak A, Constantinou A. 2008. The Fanconi anemia protein FANCMcan promote branch migration of Holliday junctions and replication forks. Mol Cell 29: 141-148.
75. Ghezraoui H, Piganeau M, Renouf B, Renaud J-B, Sallmyr A, Ruis B, Oh S, Tomkinson AE, Hendrickson EA, Giovannangeli C, et al. 2014. Chromosomal translocations in human cells are generated by canonical nonhomologous end-joining. Mol Cell 55: 829-842.
76. Gilbertson LA, Stahl FW. 1996. A test of the double-strand break repair model for meiotic recombination in Saccharomyces Cerevisiae. Genetics 144: 27-41.
77. Griffith JD, Comeau L, Rosenfield S, Stansel RM, Bianchi A, Moss H, de Lange T. 1999. Mammalian telomeres end in a large duplex loop. Cell 97: 503-514.
78. Gupta R, Barkan D, Redelman-Sidi G, Shuman S, Glickman MS. 2011. Mycobacteria exploit three genetically distinct DNA double-strand break repair pathways. Mol Microbiol 79: 316-330.
79. Gupta R, Shuman S, Glickman MS. 2015. RecF and RecR play critical roles in the homologous recombination and singlestrand annealing pathways of mycobacteria. J Bacteriol 197: 3121-3132.
80. Handa N, Morimatsu K, Lovett ST, Kowalczykowski SC. 2009. Reconstitution of initial steps of dsDNA break repair by the RecF pathway of E. coli. Genes Dev 23: 1234-1245.
81. Hastings PJ, Ira G, Lupski JR. 2009a. A microhomology-mediated break-induced replication model for the origin of human copy number variation. ed. I. Matic. PLoS Genet 5: e1000327.
82. Hastings PJ, Lupski JR, Rosenberg SM, Ira G. 2009b. Mechanisms of change in gene copy number. Nat Rev Genet 10: 551-564.
83. Henson JD, Reddel RR. 2010. Assaying and investigating alternative lengthening of telomeres activity in human cells and cancers. FEBS Lett 584: 3800-3811.
84. Henson JD, Cao Y, Huschtscha LI, Chang AC, Au AYM, Pickett HA, Reddel RR. 2009. DNA C-circles are specific and quantifiable markers of alternative-lengthening-of-telomeres activity. Nat Biotech 27: 1181-1185.
85. Heyer W-D, Ehmsen KT, Liu J. 2010. Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44: 113-139.
86. Hicks WM, Kim M, Haber JE. 2010. Increased mutagenesis and unique mutation signature associated with mitotic gene conversion. Science 329: 82-85.
87. Hogg M, Sauer-Eriksson AE, Johansson E. 2012. Promiscuous DNA synthesis by human DNA polymerase theta. Nucleic Acids Res 40: 2611-2622.
88. Horowitz H, Haber JE. 1985. Identification of autonomously replicating circular subtelomeric Y' elements in Saccharomyces cerevisiae. Mol Cell Biol 5: 2369-2380.
89. Hu Y, Tang H-B, Liu N-N, Tong X-J, Dang W, Duan Y-M, Fu X-H, Zhang Y, Peng J, Meng F-L, et al. 2013. Telomerase-null survivor screening identifies novel telomere recombination regulators. PLoS Genet 9: e1003208.
90. Huang P, Pryde FE, Lester D, Maddison RL, Borts RH, Hickson ID, Louis EJ. 2001. SGS1 is required for telomere elongation in the absence of telomerase. Curr Biol 11: 125-129.
91. Ira G, Haber JE. 2002. Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol Cell Biol 22: 6384-6392.
92. 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.
93. Ithurbide S, Bentchikou E, Coste G, Bost B, Servant P, Sommer S. 2015. Single strand annealing plays a major role in RecA-independent recombination between repeated sequences in the radioresistant Deinococcus radiodurans bacterium. PLoS Genet 11: e1005636.
94. Ivanov EL, Haber JE. 1995. RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol Cell Biol 15: 2245-2251.
95. Ivanov EL, Sugawara N, Fishman-Lobell J, Haber JE. 1996. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 142: 693-704.
96. 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.
97. Jiang Q, Greenberg R. 2015. Deciphering the BRCA1 tumor suppressor network. J Biol Chem 290: 17724-17732.
98. Jiang W-Q, Zhong Z-H, Henson JD, Neumann AA, Chang AC-M, Reddel RR. 2005. Suppression of alternative lengthening of telomeres by Sp100-mediated sequestration of the MRE11/RAD50/NBS1 complex. Mol Cell Biol 25: 2708-2721.
99. Johnson FB, Marciniak RA, McVey M, Stewart SA, Hahn WC, Guarente L. 2001. The Saccharomyces cerevisiae WRN homolog Sgs1p participates in telomere maintenance in cells lacking telomerase. EMBO J 20: 905-913.
100. Judd SR, Petes TD. 1988. Physical lengths of meiotic and mitotic gene conversion tracts in Saccharomyces cerevisiae. Genetics 118: 401-410.
101. Kantake N, Madiraju MVVM, Sugiyama T, Kowalczykowski SC. 2002. Escherichia coli RecO protein anneals ssDNA complexed with its cognate ssDNA-binding protein: a common step in genetic recombination. Proc Natl Acad Sci 99: 15327-15332.
102. Keeney S, Neale MJ. 2006. Initiation of meiotic recombination by formation of DNA double-strand breaks: mechanism and regulation. Biochem Soc Trans 34: 523-525.
103. Kent T, Chandramouly G, McDevitt SM, Ozdemir AY, Pomerantz RT. 2015. Mechanism of microhomology-mediated end-joining promoted by human DNA polymerase theta. Nat Struct Mol Biol 22: 230-237.
104. Kidd JM, Cooper GM, Donahue WF, Hayden HS, Sampas N, Graves T, Hansen N, Teague B, Alkan C, Antonacci F, et al. 2008. Mapping and sequencing of structural variation from eight human genomes. Nature 453: 56-64.
105. Kolomietz E, Meyn MS, Pandita A, Squire JA. 2002. The role of Alu repeat clusters as mediators of recurrent chromosomal aberrations in tumors. Genes Chromosomes Cancer 35: 97-112.
106. 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.
107. Krogh BO, Symington LS. 2004. Recombination proteins in yeast. Annu Rev Genet 38: 233-271.
108. Lambert S, Mizuno K, Blaisonneau J, Martineau S, Chanet R, Fréon K, Murray JM, Carr AM, Baldacci G. 2010. Homologous recombination restarts blocked replication forks at the expense of genome rearrangements by template exchange. Mol Cell 39: 346-359.
109. Langston LD, O’Donnell M. 2008. DNA polymerase δ is highly processive with proliferating cell nuclear antigen and undergoes collision release upon completing DNA. J Biol Chem 283: 29522-29531.
110. 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.
111. Le S, Moore JK, Haber JE, Greider CW. 1999. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152: 143-152.
112. Lee EH, Kornberg A. 1991. Replication deficiencies in priA mutants of Escherichia coli lacking the primosomal replication n′ protein. Proc Natl Acad Sci 88: 3029-3032.
113. Lee JA, Carvalho CMB, Lupski JR. 2007. A DNA replication mechanism for generating nonrecurrent rearrangements associated with genomic disorders. Cell 131: 1235-1247.
114. Lee-Theilen M, Matthews AJ, Kelly D, Zheng S, Chaudhuri J. 2010. CtIP promotes microhomology-mediated alternative end joining during class-switch recombination. Nat Struct Mol Biol 18: 75-79.
115. Li F, Dong J, Eichmiller R, Holland C, Minca E, Prakash R, Sung P, Yong Shim E, Surtees JA, Eun Lee S. 2013. Role of Saw1 in Rad1/Rad10 complex assembly at recombination intermediates in budding yeast. EMBO J 32: 461-472.
116. Lieber MR. 2010. The mechanism of double-strand DNA break repair by the nonhomologous DNA end joining pathway. Annu Rev Biochem 79: 181-211.
117. Lin FL, Sperle K, Sternberg N. 1984. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol Cell Biol 4: 1020-1034.
118. Lin C-Y, Chang H-H, Wu K-J, Tseng S-F, Lin C-C, Lin C-P, Teng SC. 2005. Extrachromosomal telomeric circles contribute to Rad52-, Rad50-, and polymerase δ-mediated telomere-telomere recombination in Saccharomyces cerevisiae. Eukaryot Cell 4: 327-336.
119. Liu J, Renault L, Veaute X, Fabre F, Stahlberg H, Heyer W-D. 2011a. Rad51 paralogues Rad55-Rad57 balance the antirecombinase Srs2 in Rad51 filament formation. Nature 479: 245-248.
120. Liu P, Erez A, Sreenath Nagamani SC, Dhar SU, Kołodziejska KE, Dharmadhikari AV, Cooper ML, Wiszniewska J, Zhang F, Withers MA, et al. 2011b. Chromosome catastrophes involve replication mechanisms generating complex genomic rearrangements. Cell 146: 889-903.
121. Liu P, Carvalho CMB, Hastings PJ, Lupski JR. 2012. Mechanisms for recurrent and complex human genomic rearrangements. Curr Opin Genet Dev 22: 211-220.
122. Lundblad V, Blackburn EH. 1993. An alternative pathway for yeast telomere maintenance rescues est1− senescence. Cell 73: 347-360.
123. Lydeard JR, Jain S, Yamaguchi M, Haber JE. 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448: 820-823.
124. Lydeard JR, Lipkin-Moore Z, Sheu Y-J, Stillman B, Burgers PM, Haber JE. 2010. Break-induced replication requires all essential DNA replication factors except those specific for pre-RC assembly. Genes Dev 24: 1133-1144.
125. Ma J-L, Kim EM, Haber JE, Lee SE. 2003. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double- strand breaks lacking overlapping end sequences. Mol Cell Biol 23: 8820-8828.
126. Malkova A, Ivanov EL, Haber JE. 1996. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc Natl Acad Sci 93: 7131-7136.
127. Malkova A, Naylor ML, Yamaguchi M, Ira G, Haber JE. 2005. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol Cell Biol 25: 933-944.
128. Marians KJ. 2000. PriA-directed replication fork restart in Escherichia coli. Trends Biochem Sci 25: 185-189.
129. Marrero VA, Symington LS. 2010. ExtensiveDNAend processing by Exo1 and Sgs1 inhibits break-induced replication. PLoS Genet 6: e1001007.
130. Marzec P, Armenise C, Perot G, Roumelioti F-M, Basyuk E, Gagos S, Chibon F, Dejardin J. 2015. Nuclear-receptor-mediated telomere insertion leads to genome instability in ALT cancers. Cell 160: 913-927.
131. Mateos-Gomez PA, Gong F, Nair N, Miller KM, Lazzerini-Denchi E, Sfeir A. 2015. Mammalian polymerase theta promotes alternative NHEJ and suppresses recombination. Nature 518: 254-257.
132. Mayle R, Campbell IM, Beck CR, Yu Y, Wilson M, Shaw CA, Bjergbaek L, Lupski JR, Ira G. 2015. DNA REPAIR. Mus81 and converging forks limit the mutagenicity of replication fork breakage. Science 349: 742-747.
133. Mazon G, Lam AF, Ho CK, Kupiec M, Symington LS. 2012. The Rad1-Rad10 nuclease promotes chromosome translocations between dispersed repeats. Nat Struct Mol Biol 19: 964-971.
134. McDermott DH, Gao J-L, Liu Q, Siwicki M, Martens C, Jacobs P, Velez D, Yim E, Bryke CR, Hsu N, et al. 2015. Chromothriptic cure of WHIM syndrome. Cell 160: 686-699.
135. McEachern MJ, Haber JE. 2006. Break-induced replication and recombinational telomere elongation in yeast. Annu Rev Biochem 75: 111-135.
136. McVey M, Lee SE. 2008. MMEJ repair of double-strand breaks (director’s cut): deleted sequences and alternative endings. Trends Genet 24: 529-538.
137. Meyer D, Fu BXH, Heyer W-D. 2015. DNA polymerases δ and λ cooperate in repairing double-strand breaks by microhomology- mediated end-joining in Saccharomyces cerevisiae. Proc Natl Acad Sci 112: E6907-E6916.
138. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455: 770-774.
139. Mitchel K, Zhang H, Welz-Voegele C, Jinks-Robertson S. 2010. Molecular structures of crossover and noncrossover intermediates during gap repair in yeast: implications for recombination. Mol Cell 38: 211-222.
140. Mizuno K, Miyabe I, Schalbetter SA, Carr AM, Murray JM. 2012. Recombination-restarted replication makes inverted chromosome fusions at inverted repeats. Nature 493: 246-249.
141. Morrow DM, Connelly C, Hieter P. 1997. ‘Break copy’ duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147: 371-382.
142. Muntoni A, Reddel RR. 2005. The first molecular details of ALT in human tumor cells. Hum Mol Genet 14: R191-R196.
143. Muntoni A, Neumann AA, Hills M, Reddel RR. 2009. Telomere elongation involves intra-molecular DNA replication in cells utilizing alternative lengthening of telomeres. Hum Mol Genet 18: 1017-1027.
144. Murnane JP, Sabatier L, Marder BA, Morgan WF. 1994. Telomere dynamics in an immortal human cell line. EMBO J 13: 4953-4962.
145. Nabetani A, Ishikawa F. 2009. Unusual telomeric DNAs in human telomerase-negative immortalized cells. Mol Cell Biol 29: 703-713.
146. Nagaraju G, Hartlerode A, Kwok A, Chandramouly G, Scully R. 2009. XRCC2andXRCC3 regulate the balance between shortand long-tract gene conversions between sister chromatids. Mol Cell Biol 29: 4283-4294.
147. Nassif N, Penney J, Pal S, Engels WR, Gloor GB. 1994. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol Cell Biol 14: 1613-1625.
148. Natarajan S, McEachern MJ. 2002. Recombinational telomere elongation promoted by DNA circles. Mol Cell Biol 22: 4512-4521.
149. Newman JA, Cooper CDO, Aitkenhead H, Gileadi O. 2015. Structure of the helicase domain ofDNApolymerase theta reveals a possible role in the microhomology-mediated end-joining pathway. Structure 23: 2319-2330.
150. Nurse P, Zavitz KH, Marians KJ. 1991. Inactivation of the Escherichia coli priA DNA replication protein induces the SOS response. J Bacteriol 173: 6686-6693.
151. O’Sullivan RJ, Arnoult N, Lackner DH, Oganesian L, Haggblom C, Corpet A, Almouzni G, Karlseder J. 2014. Rapid induction of alternative lengthening of telomeres by depletion of the histone chaperone ASF1. Nat Struct Mol Biol 21: 167-174.
152. Ozenberger BA, Roeder GS. 1991. A unique pathway of doublestrand break repair operates in tandemly repeated genes. Mol Cell Biol 11: 1222-1231.
153. Paliwal S, Kanagaraj R, Sturzenegger A, Burdova K, Janscak P. 2014. Human RECQ5 helicase promotes repair of DNA double- strand breaks by synthesis-dependent strand annealing. Nucleic Acids Res 42: 2380-2390.
154. Pâques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 63: 349-404.
155. Pâques F, Leung W-Y, Haber JE. 1998. Expansions and contractions in a tandem repeat induced by double-strand break repair. Mol Cell Biol 18: 2045-2054.
156. Payen C, Koszul R, Dujon B, Fischer G. 2008. Segmental duplications arise from Pol32-dependent repair of broken forks through two alternative replication-based mechanisms. PLoS Genet 4: e1000175.
157. Porter SE, White MA, Petes TD. 1993. Genetic evidence that the meiotic recombination hotspot at the His4 locus of Saccharomyces cerevisiae does not represent a site for a symmetrically processed double-strand break. Genetics 134: 5-19.
158. Potts PR, Yu H. 2007. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomerebinding proteins. Nat Struct Mol Biol 14: 581-590.
159. Prakash R, Satory D, Dray E, Papusha A, Scheller J, Kramer W, Krejci L, Klein H, Haber JE, Sung P, et al. 2009. YeastMph1helicase dissociates Rad51-made D-loops: implications for crossover control in mitotic recombination. Genes Dev 23: 67-79.
160. Prakash R, Zhang Y, Feng W, Jasin M. 2015. Homologous recombination and human health: the roles of BRCA1, BRCA2, and associated proteins. Cold Spring Harb Perspect Biol 7: a016600.
161. Rass E, Grabarz A, Plo I, Gautier J, Bertrand P, Lopez BS. 2009. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat Struct Mol Biol 16: 819-824.
162. Resnick MA. 1976. The repair of double-strand breaks in DNA: a model involving recombination. J Theor Biol 59: 97-106.
163. Richardson C, Moynahan ME, Jasin M. 1998. Double-strand break repair by interchromosomal recombination: suppression of chromosomal translocations. Genes Dev 12: 3831-3842.
164. Rocha EPC, Cornet E, Michel B. 2005. Comparative and evolutionary analysis of the bacterial homologous recombination systems. PLoS Genet 1: e15.
165. Rodgers K, McVey M. 2015. Error-prone repair of DNA doublestrand breaks. J Cell Physiol 231: 15-24.
166. Saini N, Ramakrishnan S, Elango R, Ayyar S, Zhang Y, Deem A, Ira G, Haber JE, Lobachev KS, Malkova A. 2013. Migrating bubble during break-induced replication drives conservative DNA synthesis. Nature 502: 389-392.
167. Sakofsky CJ, Ayyar S, Deem AK, Chung W-H, Ira G, Malkova A. 2015. Translesion polymerases drive microhomology-mediated break-induced replication leading to complex chromosomal rearrangements. Mol Cell 60: 860-872.
168. Saparbaev M, Prakash L, Prakash S. 1996. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae. Genetics 142: 727-736.
169. Sasaki M, Lange J, Keeney S. 2010. Genome destabilization by homologous recombination in the germ line. Nat Rev Mol Cell Biol 11: 182-195.
170. Schmidt KH, Wu J, Kolodner RD. 2006. Control of translocations between highly diverged genes by Sgs1, the Saccharomyces cerevisiae homolog of the Bloom’s syndrome protein. Mol Cell Biol 26: 5406-5420.
171. Sfeir A, de Lange T. 2012. Removal of shelterin reveals the telomere end-protection problem. Science 336: 593-597.
172. Sfeir A, Symington LS. 2015. Microhomology-mediated end joining: a back-up survival mechanism or dedicated pathway? Trends Biochem Sci 40: 701-714.
173. Shay JW, Bacchetti S. 1997. A survey of telomerase activity in human cancer. Eur J Cancer 33: 787-791.
174. Signon L, Malkova A, Naylor ML, Klein H, Haber JE. 2001. Genetic requirements for RAD51- and RAD54-independent breakinduced replication repair of a chromosomal double-strand break. Mol Cell Biol 21: 2048-2056.
175. Simsek D, Jasin M. 2010. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol 17: 410-416.
176. Simsek D, Brunet E, Wong SY-W, Katyal S, Gao Y, McKinnon PJ, Lou J, Zhang L, Li J, Rebar EJ, et al. 2011. DNA ligase III promotes alternative nonhomologous end-joining during chromosomal translocation formation. PLoS Genet 7: e1002080.
177. Slack A, Thornton PC, Magner DB, Rosenberg SM, Hastings PJ. 2006. On the mechanism of gene amplification induced under stress in Escherichia coli. PLoS Genet 2: e48.
178. Smith CE, Llorente B, Symington LS. 2007. Template switching during break-induced replication. Nature 447: 102-105.
179. Štafa A, Miklenić M, Žunar B, Lisnić B, Symington LS, Svetec I-K. 2014. Sgs1 and Exo1 suppress targeted chromosome duplication during ends-in and ends-out gene targeting. DNA Repair (Amst) 22: 12-23.
180. Stark JM, Pierce AJ, Oh J, Pastink A, Jasin M. 2004. Genetic steps of mammalian homologous repair with distinct mutagenic consequences. Mol Cell Biol 24: 9305-9316.
181. Strathern JN, Klar AJ, Hicks JB, Abraham JA, Ivy JM, Nasmyth KA, McGill C. 1982. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell 31: 183-192.
182. Sugawara N, Pâques F, Colaiácovo M, Haber JE. 1997. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double- strand break-induced recombination. Proc Natl Acad Sci 94: 9214-9219.
183. Sugawara N, Ira G, Haber JE. 2000.DNAlength dependence of the single-strand annealing pathway and the role of Saccharomyces cerevisiae RAD59 in double-strand break repair. Mol Cell Biol 20: 5300-5309.
184. 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.
185. Sung P, Klein H. 2006. Mechanism of homologous recombination: mediators and helicases take on regulatory functions. Nat Rev Mol Cell Biol 7: 739-750.
186. Sweigert SE, Carroll D. 1990. Repair and recombination of X-irradiated plasmids in Xenopus laevis oocytes. Mol Cell Biol 10: 5849-5856.
187. Symington LS. 2002. Role of RAD52 epistasis group genes in homologous recombination and double-strand break repair. Microbiol Mol Biol Rev 66: 630-670.
188. Symington LS, Gautier J. 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet 45: 247-271.
189. Symington LS, Rothstein R, Lisby M. 2014. Mechanisms and regulation of mitotic recombination in Saccharomyces cerevisiae. Genetics 198: 795-835.
190. Teng SC, Zakian VA. 1999. Telomere-telomere recombination is an efficient bypass pathway for telomere maintenance in Saccharomyces cerevisiae. Mol Cell Biol 19: 8083-8093.
191. Teng SC, Chang J, McCowan B, Zakian VA. 2000. Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol Cell 6: 947-952.
192. Tokutake Y, Matsumoto T, Watanabe T, Maeda S, Tahara H, Sakamoto S, Niida H, Sugimoto M, Ide T, Furuichi Y. 1998. Extra-chromosomal telomere repeat DNA in telomerase-negative immortalized cell lines. Biochem Biophys ResCommun 247: 765-772.
193. Truong LN, Li Y, Shi LZ, Hwang PY-H, He J, Wang H, Razavian N, Berns MW, Wu X. 2013. Microhomology-mediated end joining and homologous recombination share the initial end resection step to repairDNAdouble-strand breaks in mammalian cells. Proc Natl Acad Sci 110: 7720-7725.
194. Tsukamoto Y, Taggart AK, Zakian VA. 2001. The role of the Mre11-Rad50-Xrs2 complex in telomerase-mediated lengthening of Saccharomyces cerevisiae telomeres. Curr Biol 11: 1328-1335.
195. Tsukamoto M, Yamashita K, Miyazaki T, Shinohara M, Shinohara A. 2003. The N-terminal DNA-binding domain of Rad52 promotes RAD51-independent recombination in Saccharomyces cerevisiae. Genetics 165: 1703-1715.
196. Veaute X, Jeusset J, Soustelle C, Kowalczykowski SC, Le Cam E, Fabre F. 2003.TheSrs2 helicase prevents recombinationby disrupting Rad51 nucleoprotein filaments. Nature 423: 309-312.
197. Veaute X, Delmas S, Selva M, Jeusset J, LeCam E, Matic I, Fabre F, Petit M-A. 2005. UvrD helicase, unlike Rep helicase, dismantles RecA nucleoprotein filaments in Escherichia coli. EMBO J 24: 180-189.
198. Villarreal DD, Lee K, Deem A, Shim EY, Malkova A, Lee SE. 2012. Microhomology directs diverse DNA break repair pathways and chromosomal translocations. PLoS Genet 8: e1003026.
199. Voelkel-Meiman K, Roeder GS. 1990. A chromosome containing HOT1 preferentially receives information during mitotic interchromosomal gene conversion. Genetics 124: 561-572.
200. Walmsley RW, Chan CSM, Tye B-K, Petes TD. 1984. Unusual DNA sequences associated with the ends of yeast chromosomes. Nature 310: 157-160.
201. Wang RC, Smogorzewska A, de Lange T. 2004. Homologous recombination generates T-loop-sized deletions at human telomeres. Cell 119: 355-368.
202. Wang H, Rosidi B, Perrault R, Wang M, Zhang L, Windhofer F, Iliakis G. 2005. DNA ligase III as a candidate component of backup pathways of nonhomologous end joining. Cancer Res 65: 4020-4030.
203. Weinstock DM, Richardson CA, Elliott B, Jasin M. 2006. Modeling oncogenic translocations: distinct roles for double-strand break repair pathways in translocation formation in mammalian cells. DNA Repair (Amst) 5: 1065-1074.
204. Willis NA, Chandramouly G, Huang B, Kwok A, Follonier C, Deng C, Scully R. 2014. BRCA1 controls homologous recombination at Tus/Ter-stalled mammalian replication forks. Nature 510: 556-559.
205. Willis NA, Rass E, Scully R. 2015. Deciphering the code of the cancer genome: mechanisms of chromosome rearrangement. Trends Cancer 1: 217-230.
206. Wilson MA, Kwon Y, Xu Y, Chung W-H, Chi P, Niu H, Mayle R, Chen X, Malkova A, Sung P, et al. 2013. Pif1 helicase and Polδ promote recombination-coupled DNA synthesis via bubble migration. Nature 502: 393-396.
207. Wu L, Hickson ID. 2003. The Bloom’s syndrome helicase suppresses crossing over during homologous recombination. Nature 426: 870-874.
208. Wu Y, Kantake N, Sugiyama T, Kowalczykowski SC. 2008. Rad51 protein controls Rad52-mediated DNA Annealing. J Biol Chem 283: 14883-14892.
209. Xie A, Kwok A, Scully R. 2009. Role of mammalian Mre11 in classical and alternative nonhomologous end joining. Nat Struct Mol Biol 16: 814-818.
210. Xu L, Marians KJ. 2003. PriA mediates DNA replication pathway choice at recombination intermediates. Mol Cell 11: 817-826.
211. Yan CT, Boboila C, Souza EK, Franco S, Hickernell TR, Murphy M, Gumaste S, Geyer M, Zarrin AA, Manis JP, et al. 2007. IgH class switching and translocations use a robust non-classical end-joining pathway. Nature 449: 478-482.
212. Youds JL, Mets DG, McIlwraith MJ, Martin JS, Ward JD, ONeil NJ, Rose AM, West SC, Meyer BJ, Boulton SJ. 2010. RTEL-1 enforces meiotic crossover interference and homeostasis. Science 327: 1254-1258.
213. Yousefzadeh MJ, Wyatt DW, Takata K-I, Mu Y, Hensley SC, Tomida J, Bylund GO, Doublie S, Johansson E, Ramsden DA, et al. 2014. Mechanism of suppression of chromosomal instability by DNA polymerase POLQ. PLoS Genet 10: e1004654.
214. Yu AM, McVey M. 2010. Synthesis-dependent microhomologymediated end joining accounts for multiple types of repair junctions. Nucleic Acids Res 38: 5706-5717.
215. Zahn KE, Averill AM, Aller P, Wood RD, Doublie S. 2015. Human DNApolymerase theta grasps the primer terminus to mediate DNA repair. Nat Struct Mol Biol 22: 304-311.
216. Zahradka K, Slade D, Bailone A, Sommer S, Averbeck D, Petranovic M, Lindner AB, Radman M. 2006. Reassembly of shattered chromosomes in Deinococcus radiodurans. Nature 443: 569-573.
217. Zhang Y, Jasin M. 2011. An essential role for CtIP in chromosomal translocation formation through an alternative end-joining pathway. Nat Struct Mol Biol 18: 80-84.
218. Zhang C-Z, Spektor A, Cornils H, Francis JM, Jackson EK, Liu S, Meyerson M, Pellman D. 2015. Chromothripsis from DNA damage in micronuclei. Nature 522: 179-184.
219. Zhu C, Mills KD, Ferguson DO, Lee C, Manis J, Fleming J, Gao Y, Morton CC, Alt FW. 2002. Unrepaired DNA breaks in p53-deficient cells lead to oncogenic gene amplification subsequent to translocations. Cell 109: 811-821.
220. Zhu Z, Chung W-H, 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.