Transpositions and translocations induced by site-specific double-strand breaks in budding yeast

DNA Repair

Volumn 5, Issue 9-10, 2006, Pages 998-1009

  Haber, James E ^a  

^a BRANDEIS UNIVERSITY   (United States)

Author keywords

Molecular mechanisms; Translocations; Transpositions

Indexed keywords

DNA FRAGMENT; DOUBLE STRANDED DNA; ENDONUCLEASE;

ARTICLE; CHROMATIN IMMUNOPRECIPITATION; CHROMOSOME ANALYSIS; CHROMOSOME DELETION; CHROMOSOME REARRANGEMENT; CHROMOSOME STRUCTURE; CHROMOSOME TRANSLOCATION; CROSSING OVER; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA TRANSPOSITION; DOWN REGULATION; EXCISION REPAIR; GENE CONVERSION; GENE REPLICATION; GENE SWITCHING; GENETIC RECOMBINATION; HOMOLOGOUS RECOMBINATION; MATING TYPE; MEIOSIS; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RECIPROCAL CHROMOSOME TRANSLOCATION; RETROPOSON; TRANSPOSON; YEAST;

CHROMOSOME BREAKAGE; CHROMOSOME DELETION; CHROMOSOMES, FUNGAL; DEOXYRIBONUCLEASES, TYPE II SITE-SPECIFIC; DNA REPAIR; DNA REPLICATION; DNA TRANSPOSABLE ELEMENTS; GENES, MATING TYPE, FUNGAL; MODELS, GENETIC; RAD51 RECOMBINASE; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SACCHAROMYCETALES; TRANSLOCATION, GENETIC;

SACCHAROMYCETALES;

EID: 33747877763     PISSN: 15687864     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.dnarep.2006.05.025     Document Type: Article

References (122)

1. Sonoda E., Sasaki M.S., Buerstedde J.M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., and Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17 (1998) 598-608
2. Keeney S. Mechanism and control of meiotic recombination initiation. Curr. Top. Dev. Biol. 52 (2001) 1-53
3. Weil C.F., and Kunze R. Transposition of maize Ac/Ds transposable elements in the yeast Saccharomyces cerevisiae. Nat. Genet. 26 (2000) 187-190
4. Yu J., Marshall K., Yamaguchi M., Haber J.E., and Weil C.F. Microhomology-dependent end joining and repair of transposon-induced DNA hairpins by host factors in Saccharomyces cerevisiae. Mol. Cell. Biol. 24 (2004) 1351-1364
5. Haber J.E. Switching of Saccharomyces cerevisiae mating-type genes. In: Craig R.C.N., Gellert M., and Lambowitz A. (Eds). Mobile DNA II (2002), ASM Press 927-952
6. Kostriken R., and Heffron F. The product of the HO gene is a nuclease: purification and characterization of the enzyme. Cold Spring Harb. Symp. Quant. Biol. 49 (1984) 89-96
7. White C.I., and Haber J.E. Intermediates of recombination during mating type switching in Saccharomyces cerevisiae. EMBO J. 9 (1990) 663-673
8. Vaze M., Pellicioli A., Lee S., Ira G., Liberi G., Arbel-Eden A., Foiani M., and Haber J. Recovery from checkpoint-mediated arrest after repair of a double-strand break requires srs2 helicase. Mol. Cell 10 (2002) 373
9. Moreau S., Ferguson J.R., and Symington L.S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining or telomere maintenance. Mol. Cell. Biol. 19 (1999) 556-566
10. Aylon Y., Liefshitz B., and Kupiec M. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J. 23 (2004) 4868-4875
11. Ira G., Pellicioli A., Balijja A., Wang X., Fiorani S., Carotenuto W., Liberi G., Bressan D., Wan L., Hollingsworth N.M., et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431 (2004) 1011-1017
12. van Attikum H., Fritsch O., Hohn B., and Gasser S.M. Recruitment of the INO80 Complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119 (2004) 777-788
13. Sugawara N., Wang X., and Haber J.E. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12 (2003) 209-219
14. Wang X., Ira G., Tercero J.A., Holmes A.M., Diffley J.F., and Haber J.E. Role of DNA replication proteins in double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 24 (2004) 6891-6899
15. Wolner B., van Komen S., Sung P., and Peterson C.L. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12 (2003) 221-232
16. Weiss K., and Simpson R.T. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating type locus HMLα. Mol. Cell. Biol. 18 (1998) 5392-5403
17. Chai B., Huang J., Cairns B.R., and Laurent B.C. Distinct roles for the RSC and Swi/Snf ATP-dependent chromatin remodelers in DNA double-strand break repair. Genes Dev. 19 (2005) 1656-1661
18. Shim E.Y., Ma J.L., Oum J.H., Yanez Y., and Lee S.E. The yeast chromatin remodeler RSC complex facilitates end joining repair of DNA double-strand breaks. Mol. Cell. Biol. 25 (2005) 3934-3944
19. Lisby M., and Rothstein R. DNA damage checkpoint and repair centers. Curr. Opin. Cell. Biol. 16 (2004) 328-334
20. Miyazaki T., Bressan D.A., Shinohara M., Haber J.E., and Shinohara A. In vivo assembly and disassembly of Rad51 and Rad52 complexes during double-strand break repair. EMBO J. 23 (2004) 939-949
21. Bressan D.A., Vazquez J., and Haber J.E. Mating type-dependent constraints on the mobility of the left arm of yeast chromosome III. J. Cell. Biol. 164 (2004) 361-371
22. Gloor G.B., Nassif N.A., Johnson-Schlitz D.M., Preston C.R., and Engels W.R. Targeted gene replacement in Drosophila via P element-induced gap repair. Science 253 (1991) 1110-1117
23. Colaiácovo M.P., Pâques F., and Haber J.E. Removal of one nonhomologous DNA end during gene conversion by a RAD1- and MSH2-independent pathway. Genetics 151 (1999) 1409-1423
24. Fishman-Lobell J., and Haber J.E. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258 (1992) 480-484
25. Jacquier A., and Dujon B. An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene. Cell 41 (1985) 383-394
26. Zinn A.R., and Butow R.A. Nonreciprocal exchange between alleles of the yeast mitochondrial 21S rRNA gene: kinetics and the involvement of a double-strand break. Cell 40 (1985) 887-895
27. Plessis A., Perrin A., Haber J.E., and Dujon B. Site-specific recombination determined by I-SceI, a mitochondrial group I intron-encoded endonuclease expressed in the yeast nucleus. Genetics 130 (1992) 451-460
28. Storici F., Durham C.L., Gordenin D.A., and Resnick M.A. Chromosomal site-specific double-strand breaks are efficiently targeted for repair by oligonucleotides in yeast. Proc. Natl. Acad. Sci. U.S.A. 100 (2003) 14994-14999
29. Wilson T.E. A genomics-based screen for yeast mutants with an altered recombination/end-joining repair ratio. Genetics 162 (2002) 677-688
30. Choulika A., Perrin A., Dujon B., and Nicolas J.F. Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol. Cell. Biol. 15 (1995) 1968-1973
31. Elliott B., Richardson C., Winderbaum J., Nickoloff J.A., and Jasin M. Gene conversion tracts from double-strand break repair in mammalian cells. Mol. Cell. Biol. 18 (1998) 93-101
32. Nickoloff J.A., and Brenneman M.A. Analysis of recombinational repair of DNA double-strand breaks in mammalian cells with I-SceI nuclease. Methods Mol. Biol. 262 (2004) 35-52
33. Pierce A.J., and Jasin M. Measuring recombination proficiency in mouse embryonic stem cells. Methods Mol. Biol. 291 (2005) 373-384
34. Nickoloff J.A., Singer J.D., Hoekstra M.F., and Heffron F. Double-strand breaks stimulate alternative mechanisms of recombination repair. J. Mol. Biol. 207 (1989) 527-541
35. Palmer S., Schildkraut E., Lazarin R., Nguyen J., and Nickoloff J.A. Gene conversion tracts in Saccharomyces cerevisiae can be extremely short and highly directional. Nucleic Acids Res. 31 (2003) 1164-1173
36. Sweetser D.B., Hough H., Whelden J.F., Arbuckle M., and Nickoloff J.A. Fine-resolution mapping of spontaneous and double-strand break-induced gene conversion tracts in Saccharomyces cerevisiae reveals reversible mitotic conversion polarity. Mol. Cell. Biol. 14 (1994) 3863-3875
37. Aylon Y., and Kupiec M. New insights into the mechanism of homologous recombination in yeast. Mutat. Res. 566 (2004) 231-248
38. Ben-Aroya S., Mieczkowski P.A., Petes T.D., and Kupiec M. The compact chromatin structure of a Ty repeated sequence suppresses recombination hotspot activity in Saccharomyces cerevisiae. Mol. Cell 15 (2004) 221-231
39. Inbar O., and Kupiec M. Recombination between divergent sequences leads to cell death in a mismatch-repair-independent manner. Curr. Genet. 38 (2000) 23-32
40. Inbar O., Liefshitz B., Bitan G., and Kupiec M. The relationship between homology length and crossing-over during the repair of a broken chromosome. J. Biol. Chem. 275 (2000) 30833-30838
41. Parket A., Inbar O., and Kupiec M. Recombination of Ty elements in yeast can be induced by a double-strand break. Genetics 140 (1995) 67-77
42. Ira G., Malkova A., Liberi G., Foiani M., and Haber J.E. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115 (2003) 401-411
43. Allers T., and Lichten M. Intermediates of yeast meiotic recombination contain heteroduplex DNA. Mol. Cell 8 (2001) 225-231
44. Schwacha A., and Kleckner N. Identification of double Holliday junctions as intermediates in meiotic recombination. Cell 83 (1995) 783-791
45. Szostak J.W., Orr W.T., Rothstein R.J., and Stahl F.W. The double-strand-break repair model for recombination. Cell 33 (1983) 25-35
46. Cromie G.A., and Leach D.R. Control of crossing over. Mol. Cell 6 (2000) 815-826
47. Langston L.D., and Symington L.S. Opposing roles for DNA structure-specific proteins Rad1, Msh2, Msh3, and Sgs1 in yeast gene targeting. EMBO J. 24 (2005) 2214-2223
48. Osman F., Dixon J., Doe C.L., and Whitby M.C. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Emel in meiosis. Mol. Cell 12 (2003) 761-774
49. Stahl F.W., Foss H.M., Young L.S., Borts R.H., Abdullah M.F., and Copenhaver G.P. Does crossover interference count in Saccharomyces cerevisiae?. Genetics 168 (2004) 35-48
50. Whitby M.C. Making crossovers during meiosis. Biochem. Soc. Trans. 33 (2005) 1451-1455
51. Constantinou A., Chen X.B., McGowan C.H., and West S.C. Holliday junction resolution in human cells: two junction endonucleases with distinct substrate specificities. EMBO J. 21 (2002) 5577-5585
52. Boddy M.N., Gaillard P.H., McDonald W.H., Shanahan P., Yates III J.R., and Russell P. Mus81-Emel are essential components of a Holliday junction resolvase. Cell 107 (2001) 537-548
53. de los Santos T., Hunter N., Lee C., Larkin B., Loidl J., and Hollingsworth N.M. The Mus81/Mms4 endonuclease acts independently of double-Holliday junction resolution to promote a distinct subset of crossovers during meiosis in budding yeast. Genetics 164 (2003) 81-94
54. Fabre F., Chan A., Heyer W.D., and Gangloff S. Alternate pathways involving Sgs1/Top3, Mus81/Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. U.S.A. 99 (2002) 16887-16892
55. Ii M., and Brill S.J. Roles of SGS1, MUS81, and RAD51 in the repair of lagging-strand replication defects in Saccharomyces cerevisiae. Curr. Genet. 48 (2005) 213-225
56. Kaliraman V., Mullen J.R., Fricke W.M., Bastin-Shanower S.A., and Brill S.J. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15 (2001) 2730-2740
57. Mullen J.R., Kaliraman V., Ibrahim S.S., and Brill S.J. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157 (2001) 103-118
58. Schmidt K.H., Derry K.L., and Kolodner R.D. Saccharomyces cerevisiae RRM3, a 5′ to 3′ DNA helicase, physically interacts with proliferating cell nuclear antigen. J. Biol. Chem. 277 (2002) 45331-45337
59. Torres J.Z., Schnakenberg S.L., and Zakian V.A. Saccharomyces cerevisiae Rrm3p DNA helicase promotes genome integrity by preventing replication fork stalling: viability of rrm3 cells requires the intra-S-phase checkpoint and fork restart activities. Mol. Cell. Biol. 24 (2004) 3198-3212
60. Ferguson D.O., and Holloman W.K. Recombinational repair of gaps in DNA is asymmetric in Ustilago maydis and can be explained by a migrating D-loop model. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 5419-5424
61. Pâques F., and Haber J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63 (1999) 349-404
62. Hu Y., Lu X., Barnes E., Yan M., Lou H., and Luo G. Recq15 and Blm RecQ DNA helicases have nonredundant roles in suppressing crossovers. Mol. Cell. Biol. 25 (2005) 3431-3442
63. Wu L., and Hickson I.D. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426 (2003) 870-874
64. Aboussekhra A., Chanet R., Adjiri A., and Fabre F. 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 (1992) 3224-3234
65. Friedl A.A., Liefshitz B., Steinlauf R., and Kupiec M. Deletion of the SRS2 gene suppresses elevated recombination and DNA damage sensitivity in rad5 and rad18 mutants of Saccharomyces cerevisiae. Mutat. Res. 486 (2001) 137-146
66. Krejci L., Van Komen S., Li Y., Villemain J., Reddy M.S., Klein H., Ellenberger T., and Sung P. DNA helicase Srs2 disrupts the Rad51 presynaptic filament. Nature 423 (2003) 305-309
67. Veaute X., Jeusset J., Soustelle C., Kowalczykowski S.C., Le Cam E., and Fabre F. The Srs2 helicase prevents recombination by disrupting Rad51 nucleoprotein filaments. Nature 423 (2003) 309-312
68. Prakash R., Krejci L., Van Komen S., Schurer K.A., Kramer W., and Sung P. Saccharomyces cerevisiae MPH1 gene, required for homologous recombination-mediated mutation avoidance, encodes a 3′ to 5′ DNA helicase. J. Biol. Chem. (2005)
69. Scheller J., Schurer A., Rudolph C., Hettwer S., and Kramer W. MPH1, a yeast gene encoding a DEAH protein, plays a role in protection of the genome from spontaneous and chemically induced damage. Genetics 155 (2000) 1069-1081
70. Schurer K.A., Rudolph C., Ulrich H.D., and Kramer W. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from homologous recombination, but not from postreplicative repair. Genetics 166 (2004) 1673-1686
71. Fishman-Lobell J., Rudin N., and Haber J.E. Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol. 12 (1992) 1292-1303
72. Plessis A., and Dujon B. Multiple tandem integrations of transforming DNA sequences in yeast chromosomes suggest a mechanism for integrative transformation by homologous recombination. Gene 134 (1993) 41-50
73. Gould S.J. The exaptive excellence of spandrels as a term and prototype. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 10750-10755
74. Wu X., Wu C., and Haber J.E. Rules of donor preference in Saccharomyces mating-type gene switching revealed by a competition assay involving two types of recombination. Genetics 147 (1997) 399-407
75. Shinohara A., Gasior S., Ogawa T., Kleckner N., and Bishop D.K. Saccharomyces cerevisiae recA homologues RAD51 and DMC1 have both distinct and overlapping roles in meiotic recombination. Genes Cells 2 (1997) 615-629
76. Putnam C.D., Pennaneach V., and Kolodner R.D. Saccharomyces cerevisiae as a model system to define the chromosomal instability phenotype. Mol. Cell. Biol. 25 (2005) 7226-7238
77. Davis A.P., and Symington L.S. The yeast recombinational repair protein Rad59 interacts with Rad52 and stimulates single-strand annealing. Genetics 159 (2001) 515-525
78. Sugawara N., Ira G., and Haber J.E. 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 (2000) 5300-5309
79. Umezu K., Sugawara N., Chen C., Haber J.E., and Kolodner R.D. Genetic analysis of yeast RPA1 reveals its multiple functions in DNA metabolism. Genetics 148 (1998) 989-1005
80. Pâques F., and Haber J.E. Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 17 (1997) 6765-6771
81. Sugawara N., Paques F., Colaiacovo M., and Haber J.E. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proc. Natl. Acad. Sci. U.S.A. 94 (1997) 9214-9219
82. Ozenberger B.A., and Roeder G.S. A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11 (1991) 1222-1231
83. Sugawara N., Goldfarb T., Studamire B., Alani E., and Haber J.E. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 9315-9320
84. Elliott B., Richardson C., and Jasin M. Chromosomal translocation mechanisms at intronic alu elements in mammalian cells. Mol. Cell 17 (2005) 885-894
85. Haber J.E., and Leung W.Y. Lack of chromosome territoriality in yeast: promiscuous rejoining of broken chromosome ends. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 13949-13954
86. Richardson C., and Jasin M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell. Biol. 20 (2000) 9068-9075
87. Richardson C., and Jasin M. Frequent chromosomal translocations induced by DNA double-strand breaks. Nature 405 (2000) 697-700
88. Dabert P., and Smith G.R. Gene replacement with linear DNA fragments in wild-type Escherichia coli: enhancement by Chi sites. Genetics 145 (1997) 877-889
89. Kogoma T. Stable DNA replication: interplay between DNA replication, homologous recombination, and transcription. Microbiol. Mol. Biol. Rev. 61 (1997) 212-238
90. Kuzminov A., and Stahl F.W. Double-strand end repair via the RecBC pathway in Escherichia coli primes DNA replication. Genes Dev. 13 (1999) 345-356
91. Mosig G. Recombination and recombination-dependent DNA replication in bacteriophage T4. Annu. Rev. Genet. 32 (1998) 379-413
92. Motamedi M.R., Szigety S.K., and Rosenberg S.M. Double-strand-break repair recombination in Escherichia coli: physical evidence for a DNA replication mechanism in vivo. Genes Dev. 13 (1999) 2889-2903
93. Skalka A. A Replicator's View of Recombination (and Repair) (1974), Plenum, New York
94. Haber J.E. DNA recombination: the replication connection. Trends Biochem. Sci. 24 (1999) 271-275
95. Kraus E., Leung W.Y., and Haber J.E. Break-induced replication: a review and an example in budding yeast. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 8255-8262
96. Malkova A., Ivanov E.L., and Haber J.E. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. U.S.A. 93 (1996) 7131-7136
97. Ira G., and Haber J.E. Characterization of RAD51-independent break-induced replication that acts preferentially with short homologous sequences. Mol. Cell. Biol. 22 (2002) 6384-6392
98. Davis A.P., and Symington L.S. RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24 (2004) 2344-2351
99. Morrow D.M., Connelly C., and Hieter P. "Break copy" duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147 (1997) 371-382
100. Malkova A., Signon L., Schaefer C.B., Naylor M., Theis J.F., Newlon C.S., and Haber J.E. RAD51-independent break-induced replication to repair a broken chromosome depends on a distant enhancer site. Genes Dev. 15 (2001) 1055-1160
101. Lemoine F.J., Degtyareva N.P., Lobachev K., and Petes T.D. Chromosomal translocations in yeast induced by low levels of DNA polymerase a model for chromosome fragile sites. Cell 120 (2005) 587-598
102. Signon L., Malkova A., Naylor M., and Haber J.E. Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21 (2001) 2048-2056
103. Krogh B.O., and Symington L.S. Recombination proteins in yeast. Annu. Rev. Genet. 38 (2004) 233-271
104. Malkova A., Naylor M., Yamaguchi M., Ira G., and Haber J.E. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25 (2005) 933-944
105. Le S., Moore J.K., Haber J.E., and Greider C. RAD50 and RAD51 define two different pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics 152 (1999) 143-152
106. Lundblad V., and Blackburn E.H. An alternative pathway for yeast telomere maintenance rescues est1-senescence. Cell 73 (1993) 347-360
107. Natarajan S., Groff-Vindman C., and McEachern M.J. Factors influencing the recombinational expansion and spread of telomeric tandem arrays in Kluyveromyces lactis. Eukaryot. Cell 2 (2003) 1115-1127
108. Teng S., Chang J., McCowan B., and Zakian V.A. Telomerase-independent lengthening of yeast telomeres occurs by an abrupt Rad50p-dependent, Rif-inhibited recombinational process. Mol. Cell 6 (2000) 947-952
109. McEachern M.J., and Haber J.E. Break-induced replication and recombinational telomere elongation in yeast. Annu. Rev. Biochem. 75 (2006) 111-135
110. Moore J.K., and Haber J.E. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16 (1996) 2164-2173
111. Valencia M., Bentele M., Vaze M.B., Herrmann G., Kraus E., Lee S.E., Schar P., and Haber J.E. NEJ1 controls non-homologous end joining in Saccharomyces cerevisiae. Nature 414 (2001) 666-669
112. Kramer K.M., Brock J.A., Bloom K., Moore J.K., and Haber J.E. Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol. 14 (1994) 1293-1301
113. Ma J.L., Kim E.M., Haber J.E., and Lee S.E. Yeast Mre11 and Rad1 proteins define a Ku-independent mechanism to repair double-strand breaks lacking overlapping end sequences. Mol. Cell. Biol. 23 (2003) 8820-8828
114. Yu X., and Gabriel A. Reciprocal translocations in Saccharomyces cerevisiae formed by nonhomologous end joining. Genetics 166 (2004) 741-751
115. Ramiro A.R., Jankovic M., Eisenreich T., Difilippantonio S., Chen-Kiang S., Muramatsu M., Honjo T., Nussenzweig A., and Nussenzweig M.C. AID is required for c-myc/IgH chromosome translocations in vivo. Cell 118 (2004) 431-438
116. Weinstock D.M., and Jasin M. Alternative pathways for the repair of RAG-induced DNA breaks. Mol. Cell. Biol. 26 (2006) 131-139
117. Moore J.K., and Haber J.E. Capture of retrotransposon DNA at the sites of chromosomal double-strand breaks. Nature 383 (1996) 644-646
118. Teng S.C., Kim B., and Gabriel A. Retrotransposon reverse-transcriptase-mediated repair of chromosomal breaks. Nature 383 (1996) 641-644
119. Ricchetti M., Fairhead C., and Dujon B. Mitochondrial DNA repairs double-strand breaks in yeast chromosomes. Nature 402 (1999) 96-100
120. Yu X., and Gabriel A. Patching broken chromosomes with extranuclear cellular DNA. Mol. Cell 4 (1999) 873-881
121. Nassif N., Penney J., Pal S., Engels W.R., and Gloor G.B. Efficient copying of nonhomologous sequences from ectopic sites via P-element-induced gap repair. Mol. Cell. Biol. 14 (1994) 1613-1625
122. Perrin A., Buckle M., and Dujon B. Asymmetrical recognition and activity of the I-SceI endonuclease on its site and on intron-exon junctions. EMBO J. 12 (1993) 2939-2947