Chromosome Instability and Defective Recombinational Repair in Knockout Mutants of the Five Rad51 Paralogs

REFERENCES

• Albala, J. S., M. P. Thelen, C. Prange, W. Fan, M. Christensen, L. H. Thompson, and G. G. Lennon. 1997. Identification of a novel human RAD51 homolog, RAD51B. Genomics 46:476–479.
   PubMedGoogle Scholar
• Baumann, P., and S. C. West. 1998. Role of the human RAD51 protein in homologous recombination and double-stranded-break repair. Trends Biochem. Sci. 23:247–251.
   PubMed Web of Science ®Google Scholar
• Bennett, R. J., H. J. Dunderdale, and S. C. West. 1993. Resolution of Holliday junctions by RuvC resolvase: cleavage specificity and DNA distortion. Cell 74:1021–1031.
   PubMedGoogle Scholar
• Bezzubova, O. Y., A. Silbergleit, Y. Yamaguchi-Iwai, S. Takeda, and J. M. Buerstedde. 1997. Reduced X-ray resistance and homologous recombination frequencies in a RAD54-/- mutant of the chicken DT40 cell line. Cell 89:185–193.
   PubMedGoogle Scholar
• Bianco, P. R., R. B. Tracy, and S. C. Kowalczykowski. 1998. DNA strand exchange proteins: a biochemical and physical comparison. Front. Biosci. 3:D570–D603.
   PubMedGoogle Scholar
• Bishop, D. K.. 1994. RecA homologs Dmc1 and Rad51 interact to form multiple nuclear complexes prior to meiotic chromosome synapsis. Cell 79:1081–1092.
   PubMed Web of Science ®Google Scholar
• Bishop, D. K., U. Ear, A. Bhattacharyya, C. Calderone, M. Beckett, R. R. Weichselbaum, and A. Shinohara. 1998. Xrcc3 is required for assembly of Rad51 complexes in vivo. J. Biol. Chem. 273:21482–21488.
   PubMed Web of Science ®Google Scholar
• Braybrooke, J. P., K. G. Spink, J. Thacker, and I. D. Hickson. 2000. The RAD51 family member, RAD51L3, is a DNA-stimulated ATPase that forms a complex with XRCC2. J. Biol. Chem. 274:29100–29106.
   Google Scholar
• Brenneman, A. M., A. E. Weiss, J. A. Nickoloff, and D. J. Chen. 2000. XRCC3 is required for efficient repair of chromosome breaks by homologous recombination. Mutat. Res. 459:89–97.
   PubMed Web of Science ®Google Scholar
• Buerstedde, J. M., and S. Takeda. 1991. Increased ratio of targeted to random integration after transfection of chicken B cell lines. Cell 67:179–188.
   PubMed Web of Science ®Google Scholar
• Cartwright, R., A. M. Dunn, P. J. Simpson, C. E. Tambini, and J. Thacker. 1998. Isolation of novel human and mouse genes of the recA/RAD51 recombination-repair gene family. Nucleic Acids Res. 26:1653–1659.
   PubMedGoogle Scholar
• Cartwright, R., C. E. Tambini, P. J. Simpson, and J. Thacker. 1998. The XRCC2 DNA repair gene from human and mouse encodes a novel member of the recA/RAD51 family. Nucleic Acids Res. 26:3084–3089.
   PubMedGoogle Scholar
• Chen, J., D. P. Silver, D. Walpita, S. B. Cantor, A. F. Gazdar, G. Tomlinson, F. J. Couch, B. L. Weber, T. Ashley, D. M. Livingston, and R. Scully. 1998. Stable interaction between the products of the BRCA1 and BRCA2 tumor suppressor genes in mitotic and meiotic cells. Mol. Cell 2:317–328.
   PubMed Web of Science ®Google Scholar
• Chen, P. L., C. F. Chen, Y. Chen, J. Xiao, Z. D. Sharp, and W. H. Lee. 1998. The BRC repeats in BRCA2 are critical for RAD51 binding and resistance to methyl methanesulfonate treatment. Proc. Natl. Acad. Sci. USA 95:5287–5292.
   PubMed Web of Science ®Google Scholar
• Cheong, N., X. Wang, Y. Wang, and G. Iliakis. 1994. Loss of S-phase-dependent radioresistance in irs-1 cells exposed to X-rays. Mutat. Res. 314:77–85.
   PubMed Web of Science ®Google Scholar
• Clarke, A. A., N. J. Philpott, E. C. Gordon-Smith, and T. R. Rutherford. 1997. The sensitivity of Fanconi anaemia group C cells to apoptosis induced by mitomycin C is due to oxygen radical generation, not DNA crosslinking. Br. J. Haematol. 96:240–247.
   PubMed Web of Science ®Google Scholar
• Dosanjh, K. M., D. W. Collins, W. Fan, G. G. Lennon, J. S. Albala, Z. Shen, and D. Schild. 1998. Isolation and characterization of RAD51C, a new human member of the RAD51 family of related genes. Nucleic Acids Res. 26:1179–1184.
   PubMedGoogle Scholar
• Essers, J., R. W. Hendriks, S. M. A. Swagemakers, C. Troelstra, J. de Wit, D. Bootsma, J. H. J. Hoeijmakers, and R. Kanaar. 1997. Disruption of mouse RAD54 reduces ionizing radiation resistance and homologous recombination. Cell 89:195–204.
   PubMed Web of Science ®Google Scholar
• Gasior, S. L., A. K. Wong, Y. Kora, A. Shinohara, and D. K. Bishop. 1998. Rad52 associates with RPA and functions with rad55 and rad57 to assemble meiotic recombination complexes. Genes Dev. 12:2208–2221.
   PubMed Web of Science ®Google Scholar
• Haaf, T., E. Raderschall, G. Reddy, D. C. Ward, C. M. Radding, and E. I. Golub. 1999. Sequestration of mammalian Rad51-recombination protein into micronuclei. J. Cell Biol. 144:11–20.
   PubMed Web of Science ®Google Scholar
• Haber, J. E.. 1999. DNA recombination: the replication connection. Trends Biochem. Sci. 24:271–275.
   PubMed Web of Science ®Google Scholar
• Habu, T., T. Taki, A. West, Y. Nishimune, and T. Morita. 1996. 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. 24:470–477.
   PubMedGoogle Scholar
• Hartwell, L. H., P. Szankasi, C. J. Roberts, A. W. Murray, and S. H. Friend. 1997. Integrating genetic approaches into the discovery of anticancer drugs. Science 278:1064–1068.
   PubMed Web of Science ®Google Scholar
• Hays, S. L., A. A. Firmenich, and P. Berg. 1995. Complex formation in yeast double-strand break repair: participation of Rad51, Rad52, Rad55, and Rad57 proteins. Proc. Natl. Acad. Sci. USA 92:6925–6929.
   PubMedGoogle Scholar
• Huang, L. C., K. C. Clarkin, and G. M. Wahl. 1996. Sensitivity and selectivity of the DNA damage sensor responsible for activating p53-dependent G1 arrest. Proc. Natl. Acad. Sci. USA 93:4827–4832.
   PubMed Web of Science ®Google Scholar
• Ingraham, S. E., R. A. Lynch, S. Kathiresan, A. J. Buckler, and A. G. Menon. 1999. hREC2, a RAD51-like gene, is disrupted by t(12;14) (q15;q24.1) in a uterine leiomyoma. Cancer Genet. Cytogenet. 115:56–61.
   PubMed Web of Science ®Google Scholar
• Jasin, M. L.. 2000. LOH and mitotic recombination. DNA alterations in cancer: genetic and epigenetic changes.. M. Ehrlich. 191–209. Eaton Publishing, Natick, Mass
   Google Scholar
• Johnson, R. D., and M. Jasin. 2000. Sister chromatid gene conversion is a prominent double-strand break repair pathway in mammalian cells. EMBO J. 19:3398–3407.
   PubMed Web of Science ®Google Scholar
• Johnson, R. D., N. Liu, and M. Jasin. 1999. Mammalian XRCC2 promotes the repair of DNA double-strand breaks by homologous recombination. Nature 401:397–399.
   PubMed Web of Science ®Google Scholar
• Johnson, R. D., and L. S. Symington. 1995. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol. 15:4843–4850.
   PubMedGoogle Scholar
• Kadyk, L. C., and L. H. Hartwell. 1992. Sister chromatids are preferred over homologs as substrates for recombinational repair in Saccharomyces cerevisiae. Genetics 132:387–402.
   PubMed Web of Science ®Google Scholar
• Kanaar, R., J. H. Hoeijmakers, and D. C. van Gent. 1998. Molecular mechanisms of DNA double strand break repair. Trends Cell Biol. 8:483–489.
   PubMed Web of Science ®Google Scholar
• Kawabata, M., and K. Saeki. 1998. Sequence analysis and expression of a novel mouse homolog of Escherichia coli recA gene. Biochim. Biophys. Acta 1398:353–358.
   PubMedGoogle Scholar
• Kowalczykowski, S. C.. 2000. Initiation of genetic recombination and recombination-dependent replication. Trends Biochem. Sci. 25:156–165.
   PubMed Web of Science ®Google Scholar
• Liang, F., M. Han, P. J. Romanienko, and M. Jasin. 1998. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc. Natl. Acad. Sci. USA 95:5172–5177.
   PubMed Web of Science ®Google Scholar
• Lim, D.-S., and P. Hasty. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:7133–7143.
   PubMed Web of Science ®Google Scholar
• Liu, N., J. E. Lamerdin, R. S. Tebbs, D. Schild, J. D. Tucker, M. R. Shen, K. W. Brookman, M. J. Siciliano, C. A. Walter, W. Fan, L. S. Narayama, Z.-Q. Zhou, A. W. Adamson, K. J. Sorensen, D. J. Chen, N. J. Jones, and L. H. Thompson. 1998. XRCC2 and XRCC3, new human Rad51-family members, promote chromosome stability and protect against DNA crosslinks and other damages. Mol. Cell 1:783–793.
   PubMed Web of Science ®Google Scholar
• Liu, Y., M. Li, E. Y. Lee, and N. Maizels. 1999. Localization and dynamic relocalization of mammalian Rad52 during the cell cycle and in response to DNA damage. Curr. Biol. 9:975–978.
   PubMedGoogle Scholar
• Liu, Y., and N. Maizels. 2000. Coordinated response of mammalian Rad51 and rad52 to DNA damage. EMBO Rep. 1:85–90.
   PubMed Web of Science ®Google Scholar
• Mazin, A. V., E. Zaitseva, P. Sung, and S. C. Kowalczykowski. 2000. Tailed duplex DNA is the preferred substrate for Rad51 protein-mediated homologous pairing. EMBO J. 19:1148–1156.
   PubMed Web of Science ®Google Scholar
• McAllister, K. A., A. Haugen-Strano, S. Hagevik, H. A. Brownlee, N. K. Collins, P. A. Futreal, L. M. Bennett, and R. W. Wiseman. 1997. Characterization of the rat and mouse homologues of the BRCA2 breast cancer susceptibility gene. Cancer Res. 57:3121–3125.
   PubMedGoogle Scholar
• Meyn, M. S.. 1997. Chromosome instability syndromes: lessons for carcinogenesis. Curr. Top. Microbiol. Immunol. 221:71–148.
   PubMedGoogle Scholar
• Patel, K. J., V. P. Vu, H. Lee, A. Corcoran, F. C. Thistlethwaite, M. J. Evans, W. H. Colledge, L. S. Friedman, B. A. Ponder, and A. R. Venkitaraman. 1998. Involvement of Brca2 in DNA repair. Mol. Cell 1:347–357.
   PubMed Web of Science ®Google Scholar
• Pierce, A. J., R. D. Johnson, L. H. Thompson, and M. Jasin. 1999. XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev. 13:2633–2638.
   PubMed Web of Science ®Google Scholar
• Pinkel, D., L. H. Thompson, J. W. Gray, and M. Vanderlaan. 1985. Measurement of sister chromatid exchanges at very low bromodeoxyuridine substitution levels using a monoclonal antibody in Chinese hamster ovary cells. Cancer Res. 45:5795–5798.
   PubMed Web of Science ®Google Scholar
• Pittman, D. L., L. R. Weinberg, and J. C. Schimenti. 1998. Identification, characterization, and genetic mapping of Rad51d, a new mouse and human RAD51/RecA-related gene. Genomics 49:103–111.
   PubMedGoogle Scholar
• Raderschall, E., E. I. Golub, and T. Haaf. 1999. Nuclear foci of mammalian recombination proteins are located at single-stranded DNA regions formed after DNA damage. Proc. Natl. Acad. Sci. USA 96:1921–1926.
   PubMed Web of Science ®Google Scholar
• Rice, C. M., S. T. Smith, F. Bullrich, P. Havre, and E. B. Kmiec. 1997. Isolation of human and mouse genes based on homology to REC2, a recombinational repair gene from the fungus Ustilago maydis. Proc. Natl. Acad. Sci. USA 94:7417–7422.
   PubMedGoogle Scholar
• Rijkers, T., J. van den Ouweland, B. Morolli, A. G. Rolink, W. M. Baarends, P. P. H. Van Sloun, P. H. M. Lohman, and A. Pastink. 1998. Targeted inactivation of MmRAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18:6423–6429.
   PubMed Web of Science ®Google Scholar
• Schild, D., Y.-C. Lio, D. W. Collins, T. Tsomondo, and D. J. Chen. 2000. Evidence for simultaneous protein interactions between human Rad51 paralogs. J. Biol. Chem. 275:16443–16449.
   PubMed Web of Science ®Google Scholar
• Schoenmakers, E. F., C. Huysmans, and W. J. Van de Ven. 1999. Allelic knockout of novel splice variants of human recombination repair gene RAD51B in t(12;14) uterine leiomyomas. Cancer Res. 59:19–23.
   PubMed Web of Science ®Google Scholar
• Scully, R., J. Chen, R. L. Ochs, K. Keegan, M. Hoekstra, J. Feunteun, and D. M. Livingston. 1997. Dynamic changes of BRCA1 subnuclear location and phosphorylation state are initiated by DNA damage. Cell 90:425–435.
   PubMed Web of Science ®Google Scholar
• Shinohara, A., H. Ogawa, Y. Matsuda, N. Ushio, K. Ikeo, and T. Ogawa. 1993. Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nat. Genet. 4:239–243.
   PubMed Web of Science ®Google Scholar
• Shinohara, A., and T. Ogawa. 1995. Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci. 20:387–391.
   PubMed Web of Science ®Google Scholar
• Sonoda, E., M. S. Sasaki, J.-M. Buerstedde, O. Bezzubova, A. Shinohara, H. Ogawa, M. Takata, Y. Yamaguchi-Iwai, and S. Takeda. 1998. Rad51 deficient vertebrate cells accumulate chromosomal breaks prior to cell death. EMBO J. 17:598–608.
   PubMed Web of Science ®Google Scholar
• Sonoda, E., M. S. Sasaki, C. Morrison, Y. Yamaguchi-Iwai, M. Takata, and S. Takeda. 1999. Sister chromatid exchanges are mediated by homologous recombination in vertebrate cells. Mol. Cell. Biol. 19:5166–5169.
   PubMed Web of Science ®Google Scholar
• Sung, P.. 1997. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev. 11:1111–1121.
   PubMedGoogle Scholar
• Takao, N., H. Kato, R. Mori, C. Morrison, E. Sonada, X. Sun, H. Shimizu, K. Yoshioka, S. Takeda, and K. Yamamoto. 1999. Disruption of ATM in p53-null cells causes multiple functional abnormalities in cellular response to ionizing radiation. Oncogene 18:7002–7009.
   PubMedGoogle Scholar
• Takata, M., M. S. Sasaki, E. Sonoda, T. Fukushima, C. Morrison, J. S. Albala, S. M. Swagemakers, R. Kanaar, L. H. Thompson, and S. Takeda. 2000. The Rad51 paralog Rad51B promotes homologous recombinational repair. Mol. Cell. Biol. 20:6476–6482.
   PubMedGoogle Scholar
• Takata, M., M. S. Sasaki, E. Sonoda, C. Morrison, M. Hashimoto, H. Utsumi, Y. Yamaguchi-Iwai, A. Shinohara, and S. Takeda. 1998. Homologous recombination and nonhomologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 17:5497–5508.
   PubMed Web of Science ®Google Scholar
• Tashiro, S., N. Kotomura, A. Shinohara, K. Tanaka, K. Ueda, and N. Kamada. 1996. S phase specific formation of the human Rad51 protein nuclear foci in lymphocytes. Oncogene 12:2165–2170.
   PubMed Web of Science ®Google Scholar
• Tashiro, S., J. Walter, A. Shinohara, N. Kamada, and T. Cremer. 2000. Rad51 accumulation at sites of DNA damage and in postreplicative chromatin. J. Cell Biol. 150:283–291.
   PubMed Web of Science ®Google Scholar
• Tebbs, R. S., Y. Zhao, J. D. Tucker, J. B. Scheerer, M. J. Siciliano, M. Hwang, N. Liu, R. J. Legerski, and L. H. Thompson. 1995. Correction of chromosomal instability and sensitivity to diverse mutagens by a cloned cDNA of the XRCC3 DNA repair gene. Proc. Natl. Acad. Sci. USA 92:6354–6358.
   PubMed Web of Science ®Google Scholar
• Thacker, J.. 1999. A surfeit of RAD51-like genes?. Trends Genet. 15:166–168.
   PubMedGoogle Scholar
• Thompson, L. H., and D. Schild. 1999. The contribution of homologous recombination in preserving genome integrity in mammalian cells. Biochimie 81:87–105.
   PubMed Web of Science ®Google Scholar
• Thompson, L. H., and D. Schild. Homologous recombinational repair of DNA ensures mammalian chromosome stability. Mutat. Res., in press.
   Google Scholar
• Tsuzuki, T., Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, A. Matsushiro, Y. Yoshimura, and T. Morita. 1996. Targeted disruption of the Rad51 gene leads to lethality in embryonic mice. Proc. Natl. Acad. Sci. USA 93:6236–6240.
   PubMed Web of Science ®Google Scholar
• Tucker, J. D., N. J. Jones, N. A. Allen, J. L. Minkler, L. H. Thompson, and A. V. Carrano. 1991. Cytogenetic characterization of the ionizing radiation-sensitive Chinese hamster mutant irs1. Mutat. Res. 254:143–152.
   PubMedGoogle Scholar
• Wang, W., M. Seki, Y. Narita, E. Sonoda, S. Takeda, K. Yamada, T. Masuko, T. Katada, and T. Enomoto. 2000. Possible association of BLM in decreasing DNA double strand breaks during DNA replication. EMBO J. 19:3428–3435.
   PubMedGoogle Scholar
• Wooster, R., G. Bignell, J. Lancaster, S. Swift, S. Seal, J. Mangion, N. Collins, S. Gregory, C. Gumbs, and G. Micklem. 1995. Identification of the breast cancer susceptibility gene BRCA2. Nature 378:789–792.
   PubMed Web of Science ®Google Scholar
• Xiao, Y., and D. T. Weaver. 1997. Conditional gene targeted deletion by Cre recombinase demonstrates the requirement for the double-strand break repair Mre11 protein in murine embryonic stem cells. Nucleic Acids Res. 25:2985–2991.
   PubMed Web of Science ®Google Scholar
• Yamaguchi-Iwai, Y., E. Sonoda, J.-M. Buerstedde, O. Bezzubova, C. Morrison, M. Takata, A. Shinohara, and S. Takeda. 1998. Homologous recombination, but not DNA repair, is reduced in vertebrate cells deficient in RAD52. Mol. Cell. Biol. 18:6430–6435.
   PubMed Web of Science ®Google Scholar
• Yamaguchi-Iwai, Y., E. Sonoda, M. S. Sasaki, C. Morrison, T. Haraguchi, Y. Hiraoka, Y. M. Yamashita, T. Yagi, M. Takata, C. Price, N. Kakazu, and S. Takeda. 1999. Mre11 is essential for the maintenance of chromosomal DNA in vertebrate cells. EMBO J. 18:6619–6629.
   PubMedGoogle Scholar
• Yu, V. P., M. Koehler, C. Steinlein, M. Schmid, L. A. Hanakahi, A. J. van Gool, S. C. West, and A. R. Venkitaraman. 2000. Gross chromosomal rearrangements and genetic exchange between nonhomologous chromosomes following BRCA2 inactivation. Genes Dev. 14:1400–1406.
   PubMed Web of Science ®Google Scholar
• Yuan, S. S., S. Y. Lee, G. Chen, M. Song, G. E. Tomlinson, and E. Y. Lee. 1999. BRCA2 is required for ionizing radiation-induced assembly of Rad51 complex in vivo. Cancer Res. 59:3547–3551.
   PubMed Web of Science ®Google Scholar
• Zamble, D. B., and S. J. Lippard. 1995. Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem. Sci. 20:435–439.
   PubMed Web of Science ®Google Scholar