Homologous recombination, non-homologous end-joining and cell cycle: Genome's angels

Current Genomics

Volumn 5, Issue 1, 2004, Pages 49-58

  Delacote F ^a   Guirouilh Barbat, J ^a   Lambert, S ^a   Lopez, B S ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

Double strand breaks; Homologous recombination; Ionizing radiation; Mammalian cells; NHEJ; Non homologous recombination

Indexed keywords

BRCA1 PROTEIN; DNA; DOUBLE STRANDED DNA;

ANIMAL CELL; CELL CYCLE; CELL DAMAGE; CELL DIFFERENTIATION; DNA BINDING; DNA RECOMBINATION; DNA REPAIR; DNA REPLICATION; DNA STRAND BREAKAGE; DNA SYNTHESIS INHIBITION; EMBRYO DEVELOPMENT; GENOME ANALYSIS; GENOTOXICITY; HOMOLOGOUS RECOMBINATION; IONIZING RADIATION; MAMMAL CELL; MEIOSIS; MOLECULAR MECHANICS; MOUSE; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION;

ANIMALIA; MAMMALIA;

EID: 0347755355     PISSN: 13892029     EISSN: None     Source Type: Journal    
DOI: 10.2174/1389202043490041     Document Type: Review

References (126)

1. Roeder, G.S. Chromosome synapsis and genetic recombination: their roles in meiotic chromosome segregation. Trends. Genet, 1990, 6: 385-389.
2. Kleckner, N., Meiosis: how could it work? Proc. Natl. Acad. Sci. USA, 1996, 93: 8167-8174.
3. Cohen, P.E. and Pollard, J.W. Regulation of meiotic recombination and prophase I progression in mammals. Bioessays, 2001, 23: 996-1009.
4. Jeggo, P.A., Taccioli, G.E. and Jackson, S.P. Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays, 1995, 17: 949-957.
5. Smith, G.C. and Jackson, S.P. The DNA-dependent protein kinase. Genes Dev., 1999, 13: 916-934.
6. Van Dyck, E., Stasiak, A.Z., Stasiak, A. and West, S.C. Binding of double-strand breaks in DNA by human RAD52 protein. Nature, 1999, 398: 728-731.
7. Khanna, K.K. and Jackson, S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet., 2001, 27: 247-254.
8. Daboussi, F., Dumay, A., Delacote, F. and Lopez, B. DNA double-strand break repair signalling: The case of RAD51 post-translational regulation. Cell Signal, 2002, 14: 969-975.
9. Cary, R.B., Peterson, S.R., Wang, J., Bear, D.G., Bradbury, E.M., and Chen, D.J. DNA looping by Ku and the DNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA, 1997, 94: 4267-4272.
10. Feldmann, E., Schmiemann, V., Goedecke, W., Reichenberger, S., and Pfeiffer, P. DNA double-strand break repair in cell-free extracts from Ku80-deficient cells: implications for Ku serving as an alignment factor in non-homologous DNA end joining. Nucleic Acids Res., 2000, 28: 2585-2596.
11. Liang, F. and Jasin, M. Ku80-deficient cells exhibit excess degradation of extrachromosomal DNA. J. Biol. Chem., 1996, 271: 14405-14411.
12. Baumann, P. and West, S.C. DNA end-joining catalyzed by human cell-free extracts. Proc. Natl. Acad. Sci. USA, 1998, 95: 14066-14070.
13. Kurimasa, A., Kumano, S., Boubnov, N.V., Story, M.D., Tung, C.S., Peterson, S.R. and Chen, D.J. Requirement for the kinase activity of human DNA-dependent protein kinase catalytic subunit in DNA strand break rejoining. Mol. Cell Biol., 1999, 19: 3877-3884.
14. Chan, D.W., Ye, R., Veillette, C.J. and Lees-Miller, S.P. DNA-dependent protein kinase phosphorylation sites in Ku 70/80 heterodimer. Biochemistry, 1999, 38: 1819-1828.
15. Leber, R., Wise, T.W., Mizuta, R. and Meek, K. The XRCC4 gene product is a target for and interacts with the DNA- dependent protein kinase. J. Biol. Chem., 1998, 273: 1794-1801.
16. Chan, D.W. and Lees-Miller, S.P. The DNA-dependent protein kinase is inactivated by autophosphorylation of the catalytic subunit. J. Biol. Chem., 1996, 271: 8936-8941.
17. Nick McElhinny, S.A., Snowden, C.M., McCarville, J. and Ramsden, D.A. Ku recruits the XRCC4-ligase IV complex to DNA ends. Mol. Cell Biol., 2000, 20: 2996-3003.
18. Bryans, M., Valenzano, M.C. and T.D. Stamato, Absence of DNA ligase IV protein in XR-1 cells: evidence for stabilization by XRCC4. Mutat. Res., 1999, 433: 53-58.
19. Lee, K.J., Huang, J., Takeda, Y. and Dynan, W.S. DNA ligase IV and XRCC4 form a stable mixed tetramer that functions synergistically with other repair factors in a cell-free end-joining system. J. Biol. Chem., 2000, 275: 34787-34796.
20. Sibanda, B.L., Critchlow, S.E., Begun, J., Pei, X.Y., Jackson, S.P., Blundell, T.L. and Pellegrini, L. Crystal structure of an Xrcc4-DNA ligase IV complex. Nat. Struct. Biol., 2001, 8: 1015-1019.
21. Grawunder, U., Zimmer, D., Kulesza, P. and Lieber, M.R. Requirement for an interaction of XRCC4 with DNA ligase IV for wild- type V(D)J recombination and DNA double-strand break repair in vivo. J. Biol. Chem., 1998, 273: 24708-24714.
22. Liang, F., Han, M., Romanienko, P.J. and Jasin, M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA, 1998, 95: p. 5172-5177.
23. Lin, Y. and Waldman, A.S. Capture of DNA sequences at double-strand breaks in mammalian chromosomes. Genetics, 2001, 158: 1665-1674.
24. Featherstone, C. and Jackson, S.P. DNA double-strand break repair. Curr. Biol., 1999, 9: R759-761.
25. Paques, F. and Haber, J.E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev., 1999, 63: 349-404.
26. Liebhaber, S.A., Goossens, M. and Kan, Y.W. Homology and concerted evolution at the alpha 1 and alpha 2 loci of human alpha-globin. Nature, 1981, 290: 26-29.
27. Arnheim, N. Concerted evolution of multigene families. In Evolution of Genes and proteins Ed. Koehn, R. K. and Nei. M. Sinauer Associates, Sunderland, MA. 1983, 38-61.
28. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J. and Stahl, F.W. The double-strand-break repair model for recombination. Cell, 1983, 33: 25-35.
29. Carney, J.P., Maser, R.S., Olivares, H., Davis, E.M., Le Beau, M., Yates, 3rd J.R., Hays, L., Morgan, W.F. and 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, 1998, 93: 477-486.
30. Sung, P. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast R-AD51 protein. Science, 1994, 265: 1241-1243.
31. Baumann, P., Benson, F.E. and West, S.C. Human RAD51 protein promotes ATP-dependent homologous pairing and strand transfer reactions in vitro. Cell, 1996, 87: 757-766.
32. Sung, P. Function of yeast RAD52 protein as a mediator between replication protein A and the RAD51 recombinase. J. Biol. Chem., 1997, 272: 28194-28197.
33. New, J.H., Sugiyama, T., Zaitseva, E. and Kowalczykowski, S.C. RAD52 protein stimulates DNA strand exchange by RAD51 and replication protein A. Nature, 1998, 391: 407-410.
34. Shinohara, A. and Ogawa, T. Stimulation by FAD52 of yeast RAD51-mediated recombination. Nature, 1998, 391: 404-407.
35. Benson, F.E., Baumann, P. and West, S.C. Synergistic actions of RAD51 and RAD52 in recombination and DNA repair. Nature, 1998, 391: 401-404.
36. Song, B. and Sung, P. Functional interactions among yeast RAD51 recombinase, RAD52 mediator, and replication protein A in DNA strand exchange. J. Biol. Chem., 2000, 275: 15895-15904.
37. New, J.H. and Kowalczykowski, S.C. RAD52 protein has a second stimulatory role in DNA strand exchange that complements replication protein-A function. J. Biol. Chem., 2002, 277: 26171-26176.
38. Sugiyama, T. and Kowalczykowski, S.C. 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., 2002, 277: 31663-31672.
39. 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., 1992, 12: 3224-3234.
40. Shinohara, A., Ogawa, H. and Ogawa, T. RAD51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell, 1992, 69: 457-470.
41. Morita, T., Yoshimura, Y., Yamamoto, A., Murata, K., Mori, M., Yamamoto, H. and Matsushiro, A. A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae. RAD51 Genes Proc. Natl. Acad. Sci. USA, 1993, 90: 6577-6580.
42. Shinohara, A., Ogawa, H., Matsuda, Y., Ushio, N., Ikeo, K. and Ogawa, T. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat. Genet., 1993, 4: 239-243.
43. Ivanov, E.L., Sugawara, N., Fishman-Lobell, J. and Haber, J.E. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics, 1996, 142: 693-704.
44. 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. USA, 1996, 93: 7131-7136.
45. Lambert, S. and Lopez, B.S. Characterization of mammalian RAD51 double strand break repair using non lethal dominant negative forms. EMBO J., 2000, 19: 3090-3099.
46. Lovett, S.T. Sequence of the RAD55 gene of Saccharomyces cerevisiae: similarity of RAD55 to prokaryotic RecA and other RecA-like proteins. Gene, 1994, 142: 103-106.
47. Kans, J.A. and Mortimer, R.K. Nucleotide sequence of the RAD57 gene of Saccharomyces cerevisiae. Gene, 1991, 105: 139-140.
48. 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., 1997, 11: 1111-1121.
49. Johnson, R.D., Liu, N. and Jasin, M. Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination. Nature, 1999, 401: 397-399.
50. Pierce, A.J., Johnson, R.D., Thompson, L.H. and Jasin, M. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev., 1999, 13: 2633-2638.
51. Takata, M., Sasaki, M.S., Sonoda, E., Fukushima, T., Morrison, C., Albala, J.S., Swagemakers, S.M., Kanaar, R., Thompson, L.H. and Takeda, S. The RAD51 paralog RAD51B promotes homologous recombinational repair. Mol. Cell Biol., 2000, 20: 6476-6482.
52. Takata, M., Sasaki, M.S., Tachiiri, S., Fukushima, T., Sonoda, E., Schild, D., Thompson, L.H. and Takeda, S. Chromosome instability and defective recombinational repair in knockout mutants of the five RAD51 paralogs. Mol. Cell Biol., 2001, 21: 2858-2866.
53. Liu, N., Schild, D., Thelen, M.P. and Thompson, L.H. Involvement of RAD51C in two distinct protein complexes of RAD51 paralogs in human cells. Nucleic Acids Res., 2002, 30: 1009-1015.
54. Miller, K.A., Yoshikawa, D.M., McConnell, I.R., Clark, R., Schild, D. and Albala, J.S. RAD51C interacts with RAD51B and is central to a larger protein complex in. vivo exclusive of RAD51. J. Biol. Chem., 2002, 277: 8406-8411.
55. Masson, J.Y., Tarsounas, M.C., Stasiak, A.Z., Stasiak, A., Shah, R., McIlwraith, M.J., Benson, F.E. and West, S.C. Identification and purification of two distinct complexes containing the five RAD51 paralogs. Genes Dev., 2001, 15: 3296-3307.
56. Lio, Y.C., Mazin, A.V., Kowalczykowski, S.C. and Chen, D.J. Complex formation by the human RAD51B and RAD51C DNA repair proteins and their activities in vitro. J. Biol. Chem., 2003, 278: 2469-2478.
57. Sigurdsson, S., Van Komen, S., Bussen, W., Schild, D., Albala, J.S. and Sung, P. Mediator function of the human RAD51B-Rad51C complex in RAD51/RPA-catalyzed DNA strand exchange. Genes Dev., 2001, 15: 3308-3318.
58. Kurumizaka, H., Ikawa, S., Nakada, M., Eda, K., Kagawa, W., Takata, M., Takeda, S., Yokoyama, S. and Shibata, T. Homologous-pairing activity of the human DNA-repair proteins Xrcc3.Rad51C. Proc. Natl. Acad. Sci. USA, 2001, 98: 5538-5543.
59. Kurumizaka, H., Ikawa, S., Nakada, M., Enomoto, R., Kagawa, W., Kinebuchi, T., Yamazoe, M., Yokoyama, S. and Shibata, T. Homologous pairing and ring and filament structure formation activities of the human Xrcc2*Rad51D complex. J. Biol. Chem., 2002, 277: 14315-14320.
60. Sturzbecher, H.W., Donzelmann, B., Henning, W., Knippschild, U., and Buchhop, S. p53 is linked directly to homologous recombination processes via RAD51/RecA protein interaction. EMBO J., 1996, 15: 1992-2002.
61. Buchhop, S., Gibson, M.K., Wang, X.W., Wagner, P., Sturzbecher, H.W. and Harris, C.C. Interaction of p53 with the human RAD51 protein. Nucleic Acids Res., 1997, 25: 3868-3874.
62. Mizuta, R., LaSalle, J.M., Cheng, H.L., Shinohara, A., Ogawa, H., Copeland, N., Jenkins, N.A., Lalande, M. and Alt, F.W. RAB22 and RAB163/mouse BRCA2: proteins that specifically interact with the RAD51 protein. Proc. Natl. Acad. Sci. USA, 1997, 94: 6927-6932.
63. Scully, R., Chen, J., Plug, A., Xiao, Y., Weaver, D., Feunteun, J., Ashley, T. and Livingston, D.M. Association of BRCA1 with RAD51 in mitotic and meiotic cells. Cell, 1997, 88: 265-275.
64. Marmorstein, L.Y., Ouchi, T. and Aaronson, S,A. The BRCA2 gene product functionally interacts with p53 and RAD51. Proc. Natl. Acad. Sci. USA, 1998, 95: 13869-13874.
65. Sengupta, S., Linke, S.P., Pedeux, R., Yang, Q., Farnsworth, J., Garfield, S.H., Valerie, K., Shay, J.W., Ellis, N.A., Wasylyk, B. and Harris, C.C. BLM helicase-dependent transport of p53 to sites of stalled DNA replication forks modulates homologous recombination. EMBO J., 2003, 22: 1210-1222.
66. Moynahan, M.E., Chiu, J.W., Koller, B.H. and Jasin, M. BRCA1 controls homology-directed DNA repair. Mol. Cell, 1999, 4: 511-518.
67. Moynahan, M.E., Pierce, A.J. and Jasin, M. BRCA2 is required for homology-directed repair of chromosomal breaks. Mol. Cell, 2001, 7: 263-272.
68. Davies, A.A., Masson, J.Y., McIlwraith, M.J., Stasiak, A.Z., Stasiak, A., Venkitaraman, A.R. and West, S.C. Role of BRCA2 in control of the RAD51 recombination and DNA repair protein. Mol. Cell, 2001, 7: 273-282.
69. Yang, H., Jeffrey, P.D., Miller, J., Kinnucan, E., Sun, Y., Thoma, N.H., Zheng, N., Chen, P.L., Lee, W.H. and Pavletich, N.P. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science, 2002, 297: 1837-1848.
70. Saintigny, Y., Rouillard, D., Chaput, B., Soussi, T. and Lopez, B.S. Mutant p53 proteins stimulate spontaneous and radiation-induced intrachromosomal homologous recombination independently of the alteration of the transactivation activity and of the G1 checkpoint, Oncogene, 1999, 18: 3553-3563.
71. Dudenhoffer, C., Kurth, M., Janus, F., Deppert, W. and Wiesmuller, L. Dissociation of the recombination control and the sequence-specific transactivation function of P53. Oncogene, 1999, 18: 5773-5784.
72. Willers, H., McCarthy, E.E., Wu, B., Wunsch, H., Tang, W., Taghian, D.G., Xia, F. and Powell, S.N. Dissociation of p53-mediated suppression of homologous recombination from G1/S cell cycle checkpoint control. Oncogene, 2000, 19: 632-639.
73. Baldeyron, C., Jacquemin, E., Smith, J., Jacquemont, C., De Oliveira, I., Gad, S., Feunteun, J., Stoppa-Lyonnet, D. and Papadopoulo, D. A single mutated BRCA1 allele leads to impaired fidelity of double strand break end-joining. Oncogene, 2002, 21: 1401-1410.
74. Zhong, Q., Boyer, T.G., Chen, P.L. and Lee, W.H. Deficient nonhomologous end-joining activity in cell-free extracts from BRCA1-null fibroblasts. Cancer Res., 2002, 62: 3966-3970.
75. Zhong, Q., Chen, C.F., Chen, P.L. and Lee, W.H. BRCA1. facilitates microhomology-mediated end joining of DNA double strand breaks. J. Biol. Chem., 2002, 277: 28641-28647.
76. Bertwistle, D. and Ashworth, A. The pathology of familial breast cancer: How do the functions of BRCA1 and BRCA2 relate to breast tumour pathology? Breast. Cancer Res., 1999, 1: 41-47.
77. Scully, R. and Livingston, D.M. In search of the tumour-suppressor functions of BRCA1 and BRCA2. Nature, 2000, 408: 429-432.
78. Welcsh, P.L., Owens, K.N. and King, M.C. Insights into the functions of BRCA1 and BRCA2. Trends Genet., 2000, 16: 69-74.
79. Le Page, F., Randrianarison, V., Marot, D., Cabannes, J., Perricaudet, M., Feunteun, J. and Sarasin, A. BRCA1 and BRCA2 are necessary for the transcription-coupled repair of the oxidative 8-oxoguanine lesion in human cells. Cancer Res., 2000, 60: 5548-5552.
80. Ganesan, S., Silver, D.P., Greenberg, R.A., Avni, D., Drapkin, R., Miron, A., Mok, S.C., Randrianarison, V., Brodie, S., Salstrom, J., Rasmussen, T.P., Klimke, A., Marrese, C., Marahrens, Y., Deng, C.X., Feunteun, J. and Livingston, D.M. BRCA1 supports XIST RNA concentration on the inactive X chromosome. Cell, 2002, 111: 393-405.
81. Venkitaraman, A.R. Cancer Susceptibility and the Functions of BRCA1 and BRCA2, Cell, 2002,108: p. 171-182.
82. 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., 1996, 16: 2164-2173.
83. Tauchi, H., Kobayashi, J., Morishima, K., van Gent, D.C., Shiraishi, T., Verkaik, N.S., vanHeems, D., Ito, E., Nakamura, A., Sonoda, E., Takata, M., Takeda, S., Matsuura, S. and Komatsu, K. Nbs1 is essential for DNA repair by homologous recombination in higher vertebrate cells. Nature, 2002, 420: 93-98.
84. Huang, J. and Dynan, W.S. Reconstitution of the mammalian DNA double-strand break end-joining reaction reveals a requirement for an Mre11/Rad50/NBS1-containing fraction. Nucleic Acids Res., 2002, 30: 667-674.
85. Maser, R.S., Monsen, K.J., Nelms, B.E. and Petrini, J.H. hMre11 and hRad50 nuclear foci are induced during the normal cellular response to DNA double-strand breaks. Mol. Cell Biol., 1997, 17: 6087-6096.
86. Stewart, G.S., Maser, R.S., Stankovic, T., Bressan, D.A., Kaplan, M.I., Jaspers, N.G., Raams, A., Byrd, P.J., Petrini, J.H. and Taylor, A.M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell, 1999, 99: 577-587.
87. Goldberg, M., Stucki, M., Falck, J., D'Amours, D., Rahman, D., Pappin, D., Bartek, J. and Jackson, S.P. MDC1 is required for the intra-S-phase DNA damage checkpoint. Nature, 2003, 421: 952-956.
88. Khanna, K.K., Lavin, M.F., Jackson, S.P. and Mulhern, T.D. ATM, a central controller of cellular responses to DNA damage. Cell Death Differ., 2001, 8: 1052-1065.
89. Vispé, S., Cazaux, C., Lesca, C. and Defais, M. Overexpression of RAD51 protein stimulates homologous recombination and increases resistance of mammalian cells to ionizing radiation. Nucleic Acids Res., 1998, 26: 2859-2864.
90. Huang, Y., Nakada, S., Ishiko, T., Utsugisawa, T., Datta, R., Kharbanda, S., Yoshida, K., Talanian, R.V., Weichselbaum, R., Kufe, D. and Yuan, Z.M. Role for caspase-mediated cleavage of RAD51 in induction of apoptosis by DNA damage. Mol. Cell Biol., 1999, 19: 2986-2997.
91. Arnaudeau, C., Helleday, T. and Jenssen, D. The RAD51 protein supports homologous recombination by an exchange mechanism in mammalian cells. J. Mol. Biol., 1999, 289: 1231-1238.
92. Pierce, A.J., Hu, P., Han, M., Ellis, N. and Jasin, M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev., 2001, 15: 3237-3242.
93. Allen, C., Kurimasa, A., Brenneman, M.A., Chen, D.J. and Nickoloff, J.A. DNA-dependent protein kinase suppresses double-strand break-induced and spontaneous homologous recombination. Proc. Natl. Acad. Sci. USA, 2002, 99: 3758-3563.
94. Delacote, F., Han, M., Stamato, T.D., Jasin, M. and Lopez, B.S. An xrcc4 defect or Wortmannin stimulates homologous recombination specifically induced by double-strand breaks in mammalian cells. Nucleic Acids Res., 2002, 30: 3454-3463.
95. Haaf, T., Golub, E.I., Reddy, G., Radding, C.M. and 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. USA, 1995, 92: 2298-2302.
96. Rijkers, T., Van Den Ouweland, J., Morolli, B., Rolink, A.G., Baarends, W.M., Van Sloun. P.P., Lohman, P.H. and Pastink, A. Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell Biol., 1998, 18: 6423-6429.
97. Yamaguchi-Iwai, Y., Sonoda, E., Buerstedde, J.M., Bezzubova, O., Morrison, C., Takata, M., Shinohara, A. and Takeda, S. Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell Biol., 1998, 18: 6430-6435.
98. Saintigny, Y., Delacote, F., Vares, G., Petitot, F., Lambert, S., Averbeck, D. and Lopez, B.S. Characterization of homologous recombination induced by replication inhibition in mammalian cells. EMBO J., 2001, 20: 3861-3870.
99. Frank-Vaillant, M. and Marcand, S. Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol. Cell, 2002, 10: 1189-1199.
100. Siede, W., Friedl, A.A., Dianova, I., Eckardt-Schupp, F. and Friedberg, E.C. The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics, 1996, 142: 91-102.
101. Boulton, S.J. and Jackson, S.P. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res., 1996, 24: 4639-4648.
102. Boulton, S.J. and 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., 1996, 15: 5093-5103.
103. Jeggo, P.A. Identification of genes involved in repair of DNA double-strand breaks in mammalian cells. Radiat. Res., 1998, 150: S80-91.
104. Takata, M., Sasaki, M.S., Sonoda, E., Morrison, C., Hashimoto, M., Utsumi, H., Yamaguchi-Iwai, Y., Shinohara, A. and 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. EMB0 J., 1998, 17: 5497-5508.
105. Buerstedde, J.M. and Takeda, S. Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell, 1991, 67: 179-188.
106. Essers, J., van Steeg, H., de Wit, J., Swagemakers, S.M., Vermeij, M., Hoeijmakers, J.H. and Kanaar, R. Homologous and non-homologous recombination differentially affect DNA damage repair in mice. EMBO J., 2000, 19: 1703-1710.
107. Biedermann, K.A., Sun, J.R., Giaccia, A.J., Tosto, L.M. and Brown, J.M. scid mutation in mice confers hypersensitivity to ionizing radiation and a deficiency in DNA double-strand break repair. Proc. Natl. Acad. Sci. USA, 1991, 88: 1394-1397.
108. Gao, Y., Chaudhuri, J., Zhu, L., Davidson, C., Weaver, D.T. and Alt, F.W. A. targeted. DNA-PKcs-null mutation reveals DNA-PK-independent functions for KU in V(D)J recombination. Immunity, 1998, 9: 367-376.
109. Gu, Y., Jin, S., Gao, Y., Weaver, D.T. and 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. USA, 1997, 94: 8076-8081.
110. Nussenzweig, A., Sokol, K., Burgman, P., Li, L. and 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. USA. 1997, 94: 13588-13593.
111. Lee, S.E., Mitchell, R.A., Cheng, A. and Hendrickson, E.A. Evidence for DNA-PK-dependent and -independent DNA double-strand break repair pathways in mammalian cells as a function of the cell cycle. Mol. Cell Biol., 1997, 17: 1425-1433.
112. Fabre, F., Boulet, A. and Roman, H. Gene conversion at different points in the mitotic cycle of Saccharomyces cerevisiae. Mol. Gen. Genet., 1984, 195: 139-143.
113. Kadyk, L.C. and Hartwell, L.H. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics, 1992, 132: 387-402.
114. Johnson, R.D. and Jasin, M. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J., 2000, 19: 3398-3407.
115. Lambert, S. and Lopez, B.S. Role of RAD51 in sister-chromatid exchanges in mammalian cells. Oncogene, 2001, 20: 6627-6631.
116. Dronkert, M.L., Beverloo, H.B., Johnson, R.D., Hoeijmakers, J.H., Jasin, M. and Kanaar, R. Mouse RAD54 affects DNA double-strand break repair and sister chromatid exchange. Mol. Cell Biol., 2000, 20: 3147-3156.
117. Flygare, J., Benson, F. and Hellgren, D. Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes. Biochim. Biophys. Acta, 1996, 1312: 231-236.
118. Yamamoto, A., Taki, T., Yagi, H., Habu, T., Yoshida, K., Yoshimura, Y., Yamamoto, K., Matsushiro, A., Nishimune, Y. and Morita, T. Cell cycle-dependent expression of the mouse RAD51 gene in proliferating cells. Mol. Gen. Genet., 1996, 251: 1-12.
119. Chen, F., Nastasi, A., Shen, Z., Brenneman, M., Crissman, H. and Chen, D.J. Cell cycle-dependent protein expression of mammalian homologs of yeast DNA double-strand break repair genes RAD51 and RAD52. Mutat. Res., 1997, 384: 205-211.
120. Richardson, C. and Jasin, M. Coupled homologous and nonhomologous repair of a double-strand break preserves genomic integrity in mammalian cells. Mol. Cell Biol., 2000, 20: 9068-9075.
121. Hollstein, M., Sidransky, D., Vogelstein, B. and Harris, C.C. p53, mutations. in. human. cancers. Science, 1991, 253: 49-53.
122. Levine, A.J., Momand, J., and Finlay, C.A. The p53 tumour suppressor gene. Nature, 1991, 351: 453-456.
123. Hainaut, P. The tumor suppressor protein p53: a receptor to genotoxic stress that controls cell growth and survival. Curr. Opin. Oncol, 1995, 7: 76-82.
124. Saintigny, Y., Rouillard, D., Chaput, B., Soussi, T. and Lopez, B.S. Mutant p53 proteins stimulate spontaneous and radiation-induced intrachromosomal homologous recombination independently of the alteration of the transactivation activity and of the G1 checkpoint., Oncogene, 1999, 18: 3553-3563.
125. Difilippantonio, M.J., Zhu, I., Chen, H.T., Meffre, E., Nussenzweig, M.C., Max, E.E, Ried, T. and Nussenzweig, A. DNA repair protein Ku80 suppresses chromosomal aberrations and malignant transformation. Nature, 2000, 404: 510-514.
126. Frank, K.M., Sharpless, N.E., Gao, Y., Sekiguchi, J.M., Ferguson, D.O., Zhu, C., Manis, J.P., Horner, J., DePinho, R.A. and Alt, F.W. DNA ligase IV deficiency in mice leads to defective neurogenesis and embryonic lethality via the p53 pathway. Mol. Cell, 2000, 5, p. 993-1002.