Repair and consequences of double-strand breaks in DNA

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 428, Issue 1-2, 1999, Pages 141-156

  Pastink, Albert ^a   Lohman, Paul H M ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

DNA; Double strand breaks; Ku; Non homologous end joining; RAD52 group; recombination; Scid

Indexed keywords

DOUBLE STRANDED DNA; RECOMBINANT PROTEIN;

CONFERENCE PAPER; DNA DAMAGE; DNA REPAIR; DNA STRAND BREAKAGE; DNA SYNTHESIS; EXCISION REPAIR; GENE MUTATION; HUMAN; MEIOSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE;

ANIMALS; DNA DAMAGE; DNA REPAIR; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; FUNGAL PROTEINS; HUMANS; RAD52 DNA REPAIR AND RECOMBINATION PROTEIN; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SCHIZOSACCHAROMYCES;

SACCHAROMYCES CEREVISIAE;

EID: 0032775314     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1383-5742(99)00042-3     Document Type: Conference Paper

References (152)

1. Lin F.L., Sperle K., Sternberg N. Repair of double-stranded DNA breaks by homologous DNA fragments during transfer of DNA into mouse L cells. Mol. Cell. Biol. 10:1990;113-119.
2. Lin F.L., Sperle K., Sternberg N. Model for homologous recombination during transfer of DNA into mouse L cells: role for DNA ends in the recombination process. Mol. Cell. Biol. 4:1984;1020-1034.
3. Maryon E., Carroll D. Characterization of recombination intermediates from DNA injected into Xenopus laevis oocytes: evidence for a nonconservative mechanism of homologous recombination. Mol. Cell. Biol. 11:1991;3278-3287.
4. Jeong-Yu S.J., Carroll D. Test of the double-strand-break repair model of recombination in Xenopus laevis oocytes. Mol. Cell. Biol. 12:1992;112-119.
5. Haber J.E. In vivo biochemistry: physical monitoring of recombination induced by site-specific endonucleases. Bioessays. 17:1995;609-620.
6. Ivanov E.L., Haber J.E. RAD1 and RAD10, but not other excision repair genes, are required for double-strand break-induced recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 15:1995;2245-2251.
7. Bardwell A.J., Bardwell L., Tomkinson A.E., Friedberg E.C. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science. 265:1994;2082-2085.
8. Sung P., Reynolds P., Prakash L., Prakash S. Purification and characterization of the Saccharomyces cerevisiae RAD1/RAD10 endonuclease. J. Biol. Chem. 268:1993;26391-26399.
9. Sugawara N., Haber J.E. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12:1992;563-575.
10. Ivanov E.L., Sugawara N., Fishman-Lobell J., Haber J.E. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics. 142:1996;693-704.
11. Ozenberger B.A., Roeder G.S. A unique pathway of double-strand break repair operates in tandemly repeated genes. Mol. Cell. Biol. 11:1991;1222-1231.
12. Saparbaev M., Prakash L., Prakash S. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae. Genetics. 142:1996;727-736.
13. Sugawara N., Paques F., Colaiacovo M., 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.
14. Paques F., 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.
15. Sargent R.G., Rolig R.L., Kilburn A.E., Adair G.M., Wilson J.H., Nairn R.S. Recombination-dependent deletion formation in mammalian cells deficient in the nucleotide excision repair gene ERCC1. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13122-13127.
16. Boyd J.B., Golino M.D., Setlow R.B. The mei-9 alpha mutant of Drosophila melanogaster increases mutagen sensitivity and decreases excision repair. Genetics. 84:1976;527-544.
17. Schmidt H., Kapitza-Fecke P., Stephen E.R., Gutz H. Some of the swi genes of Schizosaccharomyces pombe also have a function in the repair of radiation damage. Curr. Genet. 16:1989;89-94.
18. Zdzienicka M.Z. Mammalian X-ray sensitive mutants: a tool for the elucidation of the cellular response to ionizing radiation. Cancer Surveys. 28:1996;281-293.
19. Li Z., Otevrel T., Gao Y., Cheng H.L., Seed B., Stamato T.D., Taccioli G.E., Alt F.W. The XRCC4 gene encodes a novel protein involved in DNA double-strand break repair and V(D)J recombination. Cell. 83:1995;1079-1089.
20. Grawunder U., Wilm M., Wu X., Kulesza P., Wilson T.E., Mann M., Lieber M. Activity of DNA ligase IV stimulated by complex formation with XRCC4 protein in mammmalian cells. Nature. 388:1997;492-495.
21. Critchlow S.E., Bowater R.P., Jackson S.P. Mammalian DNA double-strand break repair protein XRCC4 interacts with DNA ligase IV. Curr. Biol. 7:1997;588-598.
22. Chu G. Double strand break repair. J. Biol. Chem. 272:1997;24097-24100.
23. Jin S., Inoue S., Weaver D.T. Functions of the DNA dependent protein kinase. Cancer Surveys. 29:1997;221-261.
24. Critchlow S.E., Jackson S.P. DNA end-joining: from yeast to man. TIBS. 23:1998;394-398.
25. Tsukamoto Y., Ikeda H. Double-strand break repair mediated by DNA end-joining. Genes Cells. 3:1998;135-144.
26. Ramsden D.A., Gellert M. Ku protein stimulates DNA end joining by mammalian DNA ligases: a direct role for Ku in repair of DNA double-strand breaks. EMBO J. 17:1998;609-614.
27. Jeggo P.A. DNA-PK: at the cross-roads of biochemistry and genetics. Mutat. Res. 384:1997;1-14.
28. Lees-Miller S.P. The DNA-dependent protein kinase, DNA-PK: 10 years and no ends in sight. Biochem. Cell Biol. 74:1996;503-512.
29. Woo R.A., McLure K.G., Lees-Miller S.P., Rancourt D.E., Lee P.W. DNA-dependent protein kinase acts upstream of p53 in response to DNA damage. Nature. 394:1998;700-704.
30. Siede W., Friedl A.A., Dianova I., Eckardt-Schupp F., Friedberg E.C. The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics. 142:1996;91-102.
31. Milne G.T., Jin S., Shannon K.B., Weaver D.T. Mutations in two ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:1996;4189-4198.
32. Boulton S.J., Jackson S.P. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res. 24:1996;4639-4648.
33. Boulton S.J., Jackson S.P. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15:1996;5093-5103.
34. Herrmann G., Lindahl T., Schar P. Saccharomyces cerevisiae LIF1: a function involved in DNA double-strand break repair related to mammalian XRCC4. EMBO J. 17:1998;4188-4198.
35. Tsukamoto Y., Kato J., Ikeda H. Effects of mutations of RAD50, RAD51, RAD52, and related genes on illegitimate recombination in Saccharomyces cerevisiae. Genetics. 142:1996;383-391.
36. Tsukamoto Y., Kato J., Ikeda H. Budding yeast Rad50, Mre11, Xrs2, and Hdf1, but not Rad52, are involved in the formation of deletions on a dicentric plasmid. Mol. Gen. Genet. 255:1997;543-547.
37. Tsukamoto Y., Kato J., Ikeda H. Silencing factors participate in DNA repair and recombination in Saccharomyces cerevisiae. Nature. 388:1997;900-903.
38. Boulton S.J., Jackson S.P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 17:1998;1819-1828.
39. Porter S.E., Greenwell P.W., Ritchie K.B., Petes T.D. The DNA-binding protein Hdf1p (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 24:1996;582-585.
40. Gravel S., Larrivee M., Labrecque P., Wellinger R.J. Yeast Ku as a regulator of chromosomal DNA end structure. Science. 280:1998;741-744.
41. Nugent C.I., Bosco G., Ross L.O., Evans S.K., Salinger A.P., Moore J.K., Haber J.E., Lundblad V. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr. Biol. 8:1998;657-660.
42. Laroche T., Martin S.G., Gotta M., Gorham H.C., Pryde F.E., Louis E.J., Gasser S.M. Mutation of yeast Ku genes disrupts the subnuclear organization of telomeres. Curr. Biol. 8:1998;653-656.
43. Zhu C., Bogue M.A., Lim D.S., Hasty P., Roth D.B. Ku86-deficient mice exhibit severe combined immunodeficiency and defective processing of V(D)J recombination intermediates. Cell. 86:1996;379-389.
44. Nussenzweig A., Chen C., da Costa Soares V., Sanchez M., Sokol K., Nussenzweig M.C., Li G.C. Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature. 382:1996;551-555.
45. Nussenzweig A., Sokol K., Burgman P., Li L., Li G.C. Hypersensitivity of Ku80-deficient cell lines and mice to DNA damage: the effects of ionizing radiation on growth, survival, and development. Proc. Natl. Acad. Sci. U.S.A. 94:1997;13588-13593.
46. Ouyang H., Nussenzweig A., Kurimasa A., Soares V.C., Li X., Cordon-Cardo C., Li W., Cheong N., Nussenzweig M., Iliakis G., Chen D.J., Li G.C. Ku70 is required for DNA repair but not for T cell antigen receptor gene recombination in vivo. J. Exp. Med. 186:1997;921-929.
47. Gu Y., Jin S., Gao Y., Weaver D.T., Alt F.W. Ku70-deficient embryonic stem cells have increased ionizing radiosensitivity, defective DNA end-binding activity, and inability to support V(D)J recombination. Proc. Natl. Acad. Sci. U.S.A. 94:1997;8076-8081.
48. Gu Y., Seidl K.J., Rathbun G.A., Zhu C., Manis J.P., van der Stoep N., Davidson L., Cheng H.L., Sekiguchi J.M., Frank K., Stanhope-Baker P., Schlissel M.S., Roth D.B., Alt F.W. Growth retardation and leaky SCID phenotype of Ku70-deficient mice. Immunity. 7:1997;653-665.
49. Blunt T., Gell D., Fox M., Taccioli G.E., Lehmann A.R., Jackson S.P., Jeggo P.A. Identification of a nonsense mutation in the carboxyl-terminal region of DNA-dependent protein kinase catalytic subunit in the scid mouse. Proc. Natl. Acad. Sci. U.S.A. 93:1996;10285-10290.
50. Araki R., Fujimori A., Hamatani K., Mita K., Saito T., Mori M., Fukumura R., Morimyo M., Muto M., Itoh M., Tatsumi K., Abe M. Nonsense mutation at Tyr-4046 in the DNA-dependent protein kinase catalytic subunit of severe combined immune deficiency mice. Proc. Natl. Acad. Sci. U.S.A. 94:1997;2438-2443.
51. Pergola F., Zdzienicka M.Z., Lieber M.R. V(D)J recombination in mammalian cell mutants defective in DNA double-strand break repair. Mol. Cell. Biol. 13:1993;3464-3471.
52. Kulesza P., Lieber M.R. DNA-PK is essential only for coding joint formation in V(D)J recombination. Nucleic Acids Res. 26:1998;3944-3948.
53. Gao Y., Chaudhuri J., Zhu C., Davidson L., Weaver D., Alt F.W. A targeted DNA-PKcs-Null mutation reveals DNA-PK-Independent functions for KU in V(D)J recombination. Immunity. 9:1998;367-376.
54. Taccioli G.E., Amatucci A.G., Beamish H.J., Gell D., Xiang X.H., Torres Arzayus M.I., Priestley A., Jackson S.P., Rothstein A.M., Jeggo P.A., Herrera V.L.M. Targeted disruption of the catalytic subunit of the DNA-PK gene in mice confers severe combined immunodeficiency and radiosensitivity. Immunity. 9:1998;355-366.
55. Fukumura R., Araki R., Fujimori A., Mori M., Saito T., Watanabe F., Sarashi M., Itsukaichi H., Eguchi-Kasai K., Sato K., Tatsumi K., Abe M. Murine cell line SX9 bearing a mutation in the dna-pkcs gene exhibits aberrant V(D)J recombination not only in the coding joint but also in the signal joint. J. Biol. Chem. 273:1998;13058-13064.
56. Wiler R., Leber R., Moore B.B., VanDyk L.F., Perryman L.E., Meek K. Equine severe combined immunodeficiency: a defect in V(D)J recombination and DNA-dependent protein kinase activity. Proc. Natl. Acad. Sci. U.S.A. 92:1995;11485-11489.
57. Errami A., He D.M., Friedl A.A., Overkamp W.J.I., Morolli B., Hendrickson E.A., Eckardt-Schupp F., Oshimura M., Lohman P.H.M., Jackson S.P., Zdzienicka M.Z. XR-C1, a new CHO cell mutant which is defective in DNA-PKcs, is impaired in both V(D)J coding and signal joint formation. Nucleic Acids Res. 26:1998;3146-3153.
58. Jhappan C., Morse III H.C., Fleischmann R.D., Gottesman M.M., Merlino G. DNA-PKcs: a T-cell tumour suppressor encoded at the mouse scid locus. Nat. Genet. 17:1997;483-486.
59. Li G.C., Ouyang H., Li X., Nagasawa H., Little J.B., Chen D.J., Ling C.C., Fuks Z., Cordon-Cardo C. Ku70: a candidate tumor suppressor gene for murine T cell lymphoma. Mol. Cell. 2:1998;1-8.
60. Shinohara M., Shita-Yamaguchi E., Buerstedde J.-M., Shinagawa H., Ogawa H., Shinohara A. Characterization of the roles of the Saccharomyces cerevisiae RAD54 gene and a homologue of RAD54, RDH54/TID1, in mitosis and meiosis. Genetics. 147:1997;1545-1556.
61. Klein H.L. RDH54, a RAD54 homologue in Saccharomyces cerevisiae, is required for mitotic diploid-specific recombination and repair and for meiosis. Genetics. 147:1997;1533-1543.
62. Game J.C. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin. Cancer Biol. 4:1993;73-83.
63. E.C. Friedberg, G.C. Walker, W. Siede, DNA Repair and Mutagenesis, ASM Press, Washington, DC, 1995.
64. J.A. Nickoloff, M.F. Hoekstra, Double-Strand Break and Recombinational Repair in Saccharomyces cerevisiae, In: J.A. Nickoloff and M.F. Hoekstra (Eds.), DNA Damage and Repair, Vol. I: DNA Repair in Prokaryotes and Lower Eukaryotes, Humana Press, Totowa, NJ, 1998, pp. 335-362.
65. Contopoulou C.R., Cook V.E., Mortimer R.K. Analysis of DNA double strand breakage and repair using orthogonal field alternation gel electrophoresis. Yeast. 3:1987;71-76.
66. Ogawa T., Yu X., Shinohara A., Egelman E.H. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 259:1993;1896-1899.
67. Story R.M., Bishop D.K., Kleckner N., Steitz T.A. Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage T4 and yeast. Science. 259:1993;1892-1896.
68. Sung P. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science. 265:1994;1241-1243.
69. Sung P., Robberson D.L. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell. 82:1995;453-461.
70. Sugiyama T., Zaitseva E.M., Kowalczykowski S.C. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J. Biol. Chem. 272:1997;7940-7945.
71. Namsaraev E., Berg P. Characterization of strand exchange activity of yeast Rad51 protein. Mol. Cell. Biol. 17:1997;5359-5368.
72. Sung P. Function of yeast Rad52 protein as a mediator between replication protein A and the Rad51 recombinase. J. Biol. Chem. 272:1997;28194-28197.
73. Sung P. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11:1997;1111-1121.
74. Sugiyama T., New J.H., Kowalczykowski S.C. DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc. Natl. Acad. Sci. U.S.A. 95:1998;6049-6054.
75. New J.H., Sugiyama T., Zaitseva E., Kowalczykowski S.C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature. 391:1998;407-410.
76. Shinohara A., Ogawa T. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature. 391:1998;404-407.
77. Petukhova G., Stratton S., Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature. 393:1998;91-94.
78. Gupta R.C., Golub E.I., Wold M.S., Radding C.M. Polarity of DNA strand exchange promoted by recombination proteins of the RecA family. Proc. Natl. Acad. Sci. U.S.A. 95:1998;9843-9848.
79. Namsaraev A., Berg P. Branch migration during Rad51-promoted strand exchange proceeds in either direction. Proc. Natl. Acad. U.S.A. 95:1998;10477-10481.
80. Shinohara A., Ogawa H., Ogawa T. RAD51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 69:1992;457-470.
81. Johnson R.D., Symington L.S. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 15:1995;4843-4850.
82. Hays S.L., Firmenich A.A., Berg P. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. U.S.A. 92:1995;6925-6929.
83. Jiang H., Xie Y., Houston P., Stemke-Hale K., Mortensen U.H., Rothstein R., Kodadek T. Direct association between the yeast Rad51 and Rad54 recombination proteins. J. Biol. Chem. 271:1996;33181-33186.
84. Clever B., Interthal H., Schmuckli-Maurer J., King J., Sigrist M., Heyer W.-D. Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J. 16:1997;2535-2544.
85. Firmenich A.A., Elias-Arnanz M., Berg P. A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Mol. Cell. Biol. 15:1995;1620-1631.
86. Smith J., Rothstein R. A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfa1 stimulates a RAD52-independent pathway for direct-repeat recombination. Mol. Cell. Biol. 15:1995;1632-1641.
87. Bai Y., Symington L.S. A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 10:1996;2025-2037.
88. Johzuka K., Ogawa H. Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics. 139:1995;1521-1532.
89. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 61:1990;419-436.
90. Nairz K., Klein F. mre11S-a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11:1997;2272-2290.
91. Connelly J.C., Kirkham L.A., Leach D.R. The SbcCD nuclease of Escherichia coli is a structural maintenance of chromosomes (SMC) family protein that cleaves hairpin DNA. Proc. Natl. Acad. Sci. U.S.A. 95:1998;7969-7974.
92. Usui T., Ohta T., Oshiumi H., Tomizawa J.-I., Ogawa H., Ogawa T. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell. 95:1998;705-716.
93. Petrini J.H., Bressan D.A., Yao M.S. The RAD52 epistasis group in mammalian double strand break repair. Semin. Immunol. 9:1997;181-188.
94. Baumann P., Benson F.E., West S.C. Human Rad51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell. 87:1996;757-766.
95. Baumann P., West S.C. The human rad51 protein: polarity of strand transfer and stimulation by hRP-A. EMBO J. 16:1997;5198-5206.
96. Benson F.E., Baumann P., West S.C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature. 391:1998;401-404.
97. Shen Z., Cloud K.G., Chen D.J., Park M.S. Specific interactions between the human RAD51 and RAD52 proteins. J. Biol. Chem. 271:1996;148-152.
98. Golub E.I., Kovalenko O.V., Gupta R.C., Ward D.C., Radding C.M. Interaction of human recombination proteins Rad51 and Rad54. Nucleic Acids Res. 25:1997;4106-4110.
99. Carney J.P., Maser R.S., Olivares H., Davis E.M., Le Beau M., Yates III J.R., Hays L., Morgan W.F., Petrini J.H. The hMre11/hRad50 protein complex and Nijmegen breakage syndrome: linkage of double-strand break repair to the cellular DNA damage response. Cell. 93:1998;477-486.
100. Varon R., Vissinga C., Platzer M., Cerosaletti K.M., Chrzanowska K.H., Saar K., Beckmann G., Seemanova E., Cooper P.R., Nowak N.J., Stumm M., Weemaes C.M.R., Gatti R.A., Wilson R.K., Digweed M., Rosenthal A., Sperling K., Concannon P., Reis A. Nibrin, a novel DNA double-strand break repair protein, is mutated in Nijmegen breakage syndrome. Cell. 93:1998;467-476.
101. Sato S., Seki N., Hotta Y., Tabata S. Expression profiles of a human gene identified as a structural homologue of meiosis-specific recA-like genes. DNA Res. 2:1995;183-186.
102. Habu T., Taki T., West A., Nishimune Y., Morita T. The mouse and human homologs of DMC1, the yeast meiosis-specific homologous recombination gene, have a common unique form of exon-skipped transcript in meiosis. Nucleic Acids Res. 24:1996;470-477.
103. Albala J.S., Thelen M.P., Prange C., Fan W., Christensen M., Thompson L.H., Lennon G.G. Identification of a novel human RAD51 homolog, RAD51B. Genomics. 46:1997;476-479.
104. Rice M.C., Smith S.T., Bullrich F., Havre P., Kmiec E.B. Isolation of human and mouse genes based on homology to REC2, a recombinational repair gene from the fungus Ustilago maydis. Proc. Natl. Acad. Sci. U.S.A. 94:1997;7417-7422.
105. Liu N., Lamerdin J.E., Tebbs R.S., Schild D., Tucker J.D., Shen M.R., Brookman K.W., Siciliano M.J., Walter C.A., Fan W., Narayana L.S., Zhou Z.Q., Adamson A.W., Sorensen K.J., Chen D.J., Jones N.J., Thompson L.H. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA cross-links and other damages. Mol. Cell. 1:1998;783-793.
106. Dosanjh M.K., Collins D.W., Fan W., Lennon G.G., Albala J.S., Shen Z., Schild D. Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes. Nucleic Acids Res. 26:1998;1179-1184.
107. Cartwright R., Tambini C.E., Simpson P.J., Thacker J. The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucleic Acids Res. 26:1998;3084-3089.
108. Pittman D.L., Weinberg L.R., Schimenti J.C. Identification, characterization, and genetic mapping of Rad51d, a new mouse and human RAD51/RecA-related gene. Genomics. 49:1998;103-111.
109. Muris D.F., Vreeken K., Carr A.M., Broughton B.C., Lehman A.R., Lohman P.H.M., Pastink A. Cloning the Rad51 homologue of Schizosaccharomyces pombe. Nucleic Acids Res. 21:1993;4586-4591.
110. Shinohara A., Ogawa H., Matsuda Y., Ushio N., Ikeo K., Ogawa T. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat. Genet. 4:1993;239-243.
111. Ostermann K., Lorentz A., Schmidt H. The fission yeast rad22 gene, having a function in mating-type switching and repair of DNA damages, encodes a protein homolog to Rad52 of Saccharomyces cerevisiae. Nucleic Acids Res. 21:1993;5940-5944.
112. Jang Y.K., Jin Y.H., Kim E.M., Fabre F., Hong S.H., Park S.D. Cloning and sequence analysis of rhp51+, a Schizosaccharomyces pombe homolog of the Saccharomyces cerevisiae RAD51 gene. Gene. 142:1994;207-211.
113. Tavassoli M., Shayeghi M., Nasim A., Watts F.Z. Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double-strand breaks and recombination. Nucleic Acids Res. 23:1995;383-388.
114. +, a gene involved in the repair of radiation damage and replication fidelity. J. Cell. Sci. 109:1996;73-81.
115. + genes. Curr. Genet. 31:1997;248-254.
116. Waga S., Bauer G., Stillman B. Reconstitution of complete SV40 DNA replication with purified replication factors. J. Biol. Chem. 269:1994;10923-10934.
117. Haaf T., Golub E.I., Reddy G., Radding C.M., Ward D.C. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc. Natl. Acad. Sci. U.S.A. 92:1995;2298-2302.
118. Maser R.S., Monsen K.J., Nelms B.E., Petrini J.H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell. Biol. 17:1997;6087-6096.
119. Park M.S. Expression of human RAD52 confers resistance to ionizing radiation in mammalian cells. J. Biol. Chem. 270:1995;15467-15470.
120. Johnson B.L., Thyagarajan B., Krueger L., Hirsch B., Campbell C. Elevated levels of recombinational DNA repair in human somatic cells expressing the Saccharomyces cerevisiae RAD52 gene. Mutat. Res. 363:1996;179-189.
121. Xia S.J., Shammas M.A., Reis R.J. Elevated recombination in immortal human cells is mediated by HsRAD51 recombinase. Mol. Cell. Biol. 17:1997;7151-7158.
122. Rijkers T., van den Ouweland J., Morolli B., Rolink A.G., Baarends W.M., van Sloun P.P.H., Lohman P.H.M., Pastink A. Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18:1998;6423-6429.
123. Yamaguchi-Iwai Y., Sonoda E., Buerstedde J.-M., Bezzubova O., Morrison C., Takata M., Shinohara A., Takeda S. Homologous recombination, but DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18:1998;6430-6435.
124. Tsuzuki T., Fujii Y., Sakumi K., Tominaga Y., Nakao K., Sekiguchi M., Matsushiro A., Yoshimura Y., Morita T. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. U.S.A. 93:1996;6236-6240.
125. Lim D.S., Hasty P. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:1996;7133-7143.
126. Sonoda E., Sasaki M.S., Buerstedde J.-M., Bezzubova O., Shinohara A., Ogawa H., Takata M., Yamaguchi-Iwai Y., Takeda S. Rad51-deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:1998;598-608.
127. Yamamoto A., Taki T., Yagi H., Habu T., Yoshida K., Yoshimura Y., Yamamoto K., Matsushiro A., Nishimune Y., Morita T. Cell cycle-dependent expression of the mouse Rad51 gene in proliferating cells. Mol. Gen. Genet. 251:1996;1-12.
128. Tashiro S., Kotomura N., Shinohara A., Tanaka K., Ueda K., Kamada N. S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene. 12:1996;2165-2170.
129. -/- mutant of the chicken DT40 cell line. Cell. 89:1997;185-193.
130. Essers J., Hendriks R.W., Swagemakers S.M., Troelstra C., de Wit J., Bootsma D., Hoeijmakers J.H., Kanaar R. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell. 89:1997;195-204.
131. Kooistra R., Vreeken K., Zonneveld J.B., de Jong A., Eeken J.C., Osgood C.J., Buerstedde J.-M., Lohman P.H.M., Pastink A. The Drosophila melanogaster RAD54 homolog, DmRAD54, is involved in the repair of radiation damage and recombination. Mol. Cell. Biol. 17:1997;6097-6104.
132. Ghabrial A., Ray R.P., Schupbach T. okra and spindle-B encode components of the RAD52 DNA repair pathway and affect meiosis and patterning in Drosophila oogenesis. Genes Dev. 12:1998;2711-2723.
133. Takata M., Sasaki M.S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:1998;5497-5508.
134. Beall E.L., Rio D.C. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev. 11:1997;2137-2151.
135. Lankenau D.H. Genetics of genetics in Drosophila: P elements serving the study of homologous recombination, gene conversion and targeting. Chromosoma. 103:1995;659-668.
136. Bennett C.B., Lewis A.L., Baldwin K.K., Resnick M.A. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid. Proc. Natl. Acad. Sci. U.S.A. 90:1993;5613-5617.
137. Lee S.E., Moore J.K., Holmes A., Umezu K., Kolodner R.D., Haber J.E. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell. 94:1998;399-409.
138. Petes T.D., Hill C.W. Recombination between repeated genes in microorganisms. Annu. Rev. Genet. 22:1988;147-168.
139. Lichten M., Haber J.E. Position effects in ectopic and allelic mitotic recombination in Saccharomyces cerevisiae. Genetics. 123:1989;261-268.
140. Haber J.E., Leung W.Y., Borts R.H., Lichten M. The frequency of meiotic recombination in yeast is independent of the number and position of homologous donor sequences: implications for chromosome pairing. Proc. Natl. Acad. Sci. U.S.A. 88:1991;1120-1124.
141. Godwin A.R., Bollag R.J., Christie D.M., Liskay R.M. Spontaneous and restriction enzyme-induced chromosomal recombination in mammalian cells. Proc. Natl. Acad. Sci. U.S.A. 91:1994;12554-12558.
142. Shulman M.J., Collins C., Connor A., Read L.R., Baker M.D. Interchromosomal recombination is suppressed in mammalian somatic cells. EMBO J. 14:1995;4102-4107.
143. de Wind N., Dekker M., Berns A., Radman M., te Riele H. Inactivation of the mouse Msh2 gene results in mismatch repair deficiency, methylation tolerance, hyperrecombination, and predisposition to cancer. Cell. 82:1995;321-330.
144. Chen C., Umezu K., Kolodner R.D. Chromosomal rearrangements occur in S. cerevisiae rfa1 mutator mutants due to mutagenic lesions processed by double-strand-break repair. Mol. Cell. 2:1998;9-22.
145. Taccioli G.E., Rathbun G., Oltz E., Stamato T., Jeggo P.A., Alt F.W. Impairment of V(D)J recombination in double-strand break repair mutants. Science. 260:1993;207-210.
146. Darroudi F., Natarajan A.T. Cytological characterization of Chinese hamster ovary X-ray-sensitive mutant cells xrs 5 and xrs 6: I. Induction of chromosomal aberrations by X-irradiation and its modulation with 3-aminobenzamide and caffeine. Mutat. Res. 177:1987;133-148.
147. Darroudi F., Natarajan A.T. Cytological characterization of Chinese hamster ovary X-ray-sensitive mutant cells, xrs 5 and xrs 6: II. Induction of sister-chromatid exchanges and chromosomal aberrations by X-rays and UV-irradiation and their modulation by inhibitors of poly(ADP-ribose) synthetase and alpha-polymerase. Mutat. Res. 177:1987;149-160.
148. Scully R., Chen J., Plug A., Xiao Y., Weaver D., Feunteun J., Ashley T., Livingston D.M. Association of BRCA1 with Rad51 in mitotic and meiotic cells. Cell. 88:1997;265-275.
149. Chen J., Silver D.P., Walpita D., Cantor S.B., Gazdar A.F., Tomlinson G., Couch F.J., Weber B.L., Ashley T., Livingston D.M., Scully R. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell. 2:1998;317-328.
150. Buchhop S., Gibson M.K., Wang X.W., Wagner P., Sturzbecher H.W., Harris C.C. Interaction of p53 with the human Rad51 protein. Nucleic Acids Res. 25:1997;3868-3874.
151. Akaboshi E., Inoue Y., Ryo H. Cloning of the cDNA and genomic DNA that correspond to the recA-like gene of Drosophila melanogaster. Japanese J. Genet. 69:1994;663-670.
152. McKee B.D., Ren X.-J., Hong C.-S. A recA-like gene in Drosophila melanogaster that is expressed at high levels in female but not male meiotic tissues. Chromosoma. 104:1996;479-488.