Rad51-Independent Interchromosomal Double-Strand Break Repair by Gene Conversion Requires Rad52 but Not Rad55, Rad57, or Dmc1

REFERENCES

• Bai, Y., and L. S. Symington. 1996. A RAD52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 10:2025–2037.
   PubMedGoogle Scholar
• Bartsch, S., L. E. Kang, and L. S. Symington. 2000. Rad51 is required for the repair of plasmid double-stranded DNA gaps from either plasmid or chromosomal templates. Mol. Cell. Biol. 20:1194–1205.
   PubMed Web of Science ®Google Scholar
• Brenneman, M. A., B. M. Wagener, C. A. Miller, C. Allen, and J. A. Nickoloff. 2002. XRCC3 controls the fidelity of homologous recombination: roles for XRCC3 in late stages of recombination. Mol. Cell 10:387–395.
   PubMed Web of Science ®Google Scholar
• Bugreev, D. V., O. M. Mazina, and A. V. Mazin. 2006. Rad54 protein promotes branch migration of Holliday junctions. Nature 442:590–593.
   PubMed Web of Science ®Google Scholar
• Clikeman, J. A., G. J. Khalsa, S. L. Barton, and J. A. Nickoloff. 2001. Homologous recombinational repair of double-strand breaks in yeast is enhanced by MAT heterozygosity through yKu-dependent and -independent mechanisms. Genetics 157:579–589.
   PubMedGoogle Scholar
• Davis, A. P., and L. S. Symington. 2004. RAD51-dependent break-induced replication in yeast. Mol. Cell. Biol. 24:2344–2351.
   PubMed Web of Science ®Google Scholar
• Fortin, G. S., and L. S. Symington. 2002. Mutations in yeast Rad51 that partially bypass the requirement for Rad55 and Rad57 in DNA repair by increasing the stability of Rad51-DNA complexes. EMBO J. 21:3160–3170.
   PubMedGoogle Scholar
• Haber, J. E., and M. Hearn. 1985. rad52-1-independent mitotic gene conversion in Saccharomyces cerevisiae frequently results in chromosome loss. Genetics 111:7–22.
   PubMedGoogle Scholar
• Hall, S. D., and R. D. Kolodner. 1994. Homologous pairing and strand exchange promoted by the Escherichia coli RecT protein. Proc. Natl. Acad. Sci. USA 91:3205–3209.
   PubMedGoogle Scholar
• Ivanov, E. L., N. Sugawara, J. Fishman-Lobell, and J. E. Haber. 1996. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics 142:693–704.
   PubMed Web of Science ®Google Scholar
• Iyer, L. M., E. V. Koonin, and L. Aravind. 2002. Classification and evolutionary history of the single-strand annealing proteins, RecT, Redbeta, ERF and RAD52. BMC Genomics 3:8.
   PubMed Web of Science ®Google Scholar
• Jinks-Robertson, S., M. Michelitch, and S. Ramcharan. 1993. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 13:3937–3950.
   PubMedGoogle Scholar
• Johnson, R. D., and L. S. Symington. 1995. Functional differences and interactions among the putative RecA homologues Rad51, Rad55, and Rad57. Mol. Cell. Biol. 15:4843–4850.
   PubMedGoogle Scholar
• Kang, L. E., and L. S. Symington. 2000. Aberrant double-strand break repair in rad51 mutants of Saccharomyces cerevisiae. Mol. Cell. Biol. 20:9162–9172.
   PubMedGoogle Scholar
• Kim, P. M., K. S. Paffett, J. A. Solinger, W.-D. Heyer, and J. A. Nickoloff. 2002. Spontaneous and double-strand break-induced recombination, and gene conversion tract lengths, are differentially affected by overexpression of wild-type or ATPase-defective yeast Rad54. Nucleic Acids Res. 30:2727–2735.
   PubMedGoogle Scholar
• Krishna, S., B. M. Wagener, H. P. Liu, Y.-C. Lo, R. Sterk, J. H. J. Petrini, and J. A. Nickoloff. 2007. Mre11 and Ku regulation of double-strand break repair by gene conversion and break-induced replication. DNA Repair 6:797–808.
   PubMedGoogle Scholar
• Krogh, B. O., and L. S. Symington. 2004. Recombination proteins in yeast. Annu. Rev. Genet. 38:233–271.
   PubMed Web of Science ®Google Scholar
• Lettier, G., Q. Feng, A. A. de Mayolo, N. Erdeniz, R. J. Reid, M. Lisby, U. H. Mortensen, and R. Rothstein. 2006. The role of DNA double-strand breaks in spontaneous homologous recombination in S. cerevisiae. PLoS Genet. 2:1773–1786.
   Google Scholar
• Lisby, M., J. H. Barlow, R. C. Burgess, and R. Rothstein. 2004. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 118:699–713.
   PubMed Web of Science ®Google Scholar
• Lisby, M., R. Rothstein, and U. H. Mortensen. 2001. Rad52 forms DNA repair and recombination centers during S phase. Proc. Natl. Acad. Sci. USA 98:8276–8282.
   PubMed Web of Science ®Google Scholar
• Lo, Y.-C., R. B. Kurtz, and J. A. Nickoloff. 2005. Analysis of chromosome/allele loss in genetically unstable yeast by quantitative real-time PCR. BioTechniques 38:685–690.
   PubMedGoogle Scholar
• Lo, Y.-C., K. S. Paffett, O. Amit, J. A. Clikeman, R. Sterk, M. A. Brenneman, and J. A. Nickoloff. 2006. Sgs1 regulates gene conversion tract lengths and crossovers independently of its helicase activity. Mol. Cell. Biol. 26:4086–4094.
   PubMed Web of Science ®Google Scholar
• Lovett, S. T., and R. K. Mortimer. 1987. Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics 116:547–553.
   PubMedGoogle Scholar
• Lydeard, J. R., S. Jain, M. Yamaguchi, and J. E. Haber. 2007. Break-induced replication and telomerase-independent telomere maintenance require Pol32. Nature 448:820–823.
   PubMed Web of Science ®Google Scholar
• Malkova, A., E. L. Ivanov, and J. E. Haber. 1996. Double-strand break repair in the absence of RAD51 in yeast: a possible role for break-induced DNA replication. Proc. Natl. Acad. Sci. USA 93:7131–7136.
   PubMed Web of Science ®Google Scholar
• Malkova, A., M. L. Naylor, M. Yamaguchi, G. Ira, and J. E. Haber. 2005. RAD51-dependent break-induced replication differs in kinetics and checkpoint responses from RAD51-mediated gene conversion. Mol. Cell. Biol. 25:933–944.
   PubMed Web of Science ®Google Scholar
• McDonald, J. P., and R. Rothstein. 1994. Unrepaired heteroduplex DNA in Saccharomyces cerevisiae is decreased in RAD1 RAD52-independent recombination. Genetics 137:393–405.
   PubMedGoogle Scholar
• Mills, K. D., D. O. Ferguson, and F. W. Alt. 2003. The role of DNA breaks in genomic instability and tumorigenesis. Immunol. Rev. 194:77–95.
   PubMed Web of Science ®Google Scholar
• Moore, J. K., and J. E. Haber. 1996. Cell-cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:2164–2173.
   PubMed Web of Science ®Google Scholar
• Morimatsu, K., and S. C. Kowalczykowski. 2003. RecFOR proteins load RecA protein onto gapped DNA to accelerate DNA strand exchange: a universal step of recombinational repair. Mol. Cell 11:1337–1347.
   PubMed Web of Science ®Google Scholar
• Nagaraju, G., S. Odate, A. Xie, and R. Scully. 2006. Differential regulation of short- and long-tract gene conversion between sister chromatids by Rad51C. Mol. Cell. Biol. 26:8075–8086.
   PubMed Web of Science ®Google Scholar
• Neale, M. J., and S. Keeney. 2006. Clarifying the mechanics of DNA strand exchange in meiotic recombination. Nature 442:153–158.
   PubMed Web of Science ®Google Scholar
• Nickoloff, J. A. 2002. Recombination: mechanisms and roles in tumorigenesis, p. 49-59. In J. R. Bertino (ed.), Encyclopedia of Cancer, Second Edition, vol. 4. Elsevier Science (USA), San Diego.
   Google Scholar
• Nickoloff, J. A., J. D. Singer, M. F. Hoekstra, and F. Heffron. 1989. Double-strand breaks stimulate alternative mechanisms of recombination repair. J. Mol. Biol. 207:527–541.
   PubMedGoogle Scholar
• Nickoloff, J. A., D. B. Sweetser, J. A. Clikeman, G. J. Khalsa, and S. L. Wheeler. 1999. Multiple heterologies increase mitotic double-strand break-induced allelic gene conversion tract lengths in yeast. Genetics 153:665–679.
   PubMedGoogle Scholar
• Noirot, P., and R. D. Kolodner. 1998. DNA strand invasion promoted by Escherichia coli RecT protein. J. Biol. Chem. 273:12274–12280.
   PubMedGoogle Scholar
• Paffett, K. S., J. A. Clikeman, S. Palmer, and J. A. Nickoloff. 2005. Overexpression of Rad51 inhibits double-strand break-induced homologous recombination but does not affect gene conversion tract lengths. DNA Repair 4:687–698.
   PubMedGoogle Scholar
• Paques, F., and J. E. Haber. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349–404.
   PubMed Web of Science ®Google Scholar
• Petes, T. D., R. E. Malone, and L. S. Symington. 1991. Recombination in yeast, p. 407-521. In J. R. Broach, J. R. Pringle, and E. W. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis, and energetics, vol. I. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
   Google Scholar
• Petukhova, G., S. Stratton, and P. Sung. 1998. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature 393:91–94.
   PubMedGoogle Scholar
• Rattray, A. J., and L. S. Symington. 1995. Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics 139:45–56.
   PubMedGoogle Scholar
• Rattray, A. J., and L. S. Symington. 1994. Use of a chromosomal inverted repeat to demonstrate that the RAD51 and RAD52 genes of Saccharomyces cerevisiae have different roles in mitotic recombination. Genetics 138:587–595.
   PubMedGoogle Scholar
• Rijkers, T., J. Vandenouweland, B. Morolli, A. G. Rolink, W. M. Baarends, P. P. H. Vansloun, P. H. M. Lohman, and A. Pastink. 1998. Targeted inactivation of mouse RAD52 reduces homologous recombination but not resistance to ionizing radiation. Mol. Cell. Biol. 18:6423–6429.
   PubMed Web of Science ®Google Scholar
• Saleh-Gohari, N., H. E. Bryant, N. Schultz, K. M. Parker, T. N. Cassel, and T. Helleday. 2005. Spontaneous homologous recombination is induced by collapsed replication forks that are caused by endogenous DNA single-strand breaks. Mol. Cell. Biol. 25:7158–7169.
   PubMed Web of Science ®Google Scholar
• Shen, Z., and J. A. Nickoloff. 2007. Mammalian homologous recombination repair and cancer intervention, p. 119-156. In Q. Wei, L. Li, and D. J. Chen (ed.), DNA repair, genetic instability, and cancer. World Scientific Publishing Co., Singapore.
   Google Scholar
• Signon, L., A. Malkova, M. L. Naylor, H. Klein, and J. E. Haber. 2001. Genetic requirements for RAD51- and RAD54-independent break-induced replication repair of a chromosomal double-strand break. Mol. Cell. Biol. 21:2048–2056.
   PubMed Web of Science ®Google Scholar
• Solinger, J. A., and W. D. Heyer. 2001. Rad54 protein stimulates the postsynaptic phase of Rad51 protein-mediated DNA strand exchange. Proc. Natl. Acad. Sci. USA 98:8447–8453.
   PubMed Web of Science ®Google Scholar
• Solinger, J. A., K. Kiianitsa, and W. D. Heyer. 2002. Rad54, a Swi2/Snf2-like recombinational repair protein, disassembles Rad51:dsDNA filaments. Mol. Cell 10:1175–1188.
   PubMed Web of Science ®Google Scholar
• Storici, F., J. R. Snipe, G. K. Chan, D. A. Gordenin, and M. A. Resnick. 2006. Conservative repair of a chromosomal double-strand break by single-strand DNA through two steps of annealing. Mol. Cell. Biol. 26:7645–7657.
   PubMed Web of Science ®Google Scholar
• Sugawara, N., E. L. Ivanov, J. Fishman-Lobell, B. L. Ray, X. Wu, and J. E. Haber. 1995. DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature 373:84–86.
   PubMed Web of Science ®Google Scholar
• Sugawara, N., X. Wang, and J. E. Haber. 2003. In vivo roles of Rad52, Rad54, and Rad55 proteins in Rad51-mediated recombination. Mol. Cell 12:209–219.
   PubMedGoogle Scholar
• Sung, P. 1997. Function of yeast Rad52 protein as a mediator between replication protein-A and the Rad51 recombinase. J. Biol. Chem. 272:28194–28197.
   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
• Sung, P., L. Krejci, S. Van Komen, and M. G. Sehorn. 2003. Rad51 recombinase and recombination mediators. J. Biol. Chem. 278:42729–42732.
   PubMed Web of Science ®Google Scholar
• Symington, L. S., L. E. Kang, and S. Moreau. 2000. Alteration of gene conversion tract length and associated crossing over during plasmid gap repair in nuclease-deficient strains of Saccharomyces cerevisiae. Nucleic Acids Res. 28:4649–4656.
   PubMedGoogle Scholar
• van Veelen, L. R., J. Essers, M. W. van de Rakt, H. Odijk, A. Pastink, M. Z. Zdzienicka, C. C. Paulusma, and R. Kanaar. 2005. Ionizing radiation-induced foci formation of mammalian Rad51 and Rad54 depends on the Rad51 paralogs, but not on Rad52. Mutat. Res. 574:34–49.
   PubMed Web of Science ®Google Scholar
• Weiss, K., and R. T. Simpson. 1998. High-resolution structural analysis of chromatin at specific loci: Saccharomyces cerevisiae silent mating-type locus HMLα. Mol. Cell. Biol. 18:5392–5403.
   PubMedGoogle Scholar
• Weng, Y.-S., and J. A. Nickoloff. 1998. Evidence for independent mismatch repair processing on opposite sides of a double-strand break in Saccharomyces cerevisiae. Genetics 148:59–70.
   PubMedGoogle Scholar
• West, S. C. 2003. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4:435–445.
   PubMed Web of Science ®Google Scholar
• Wolner, B., S. van Komen, P. Sung, and C. L. Peterson. 2003. Recruitment of the recombinational repair machinery to a DNA double-strand break in yeast. Mol. Cell 12:221–232.
   PubMedGoogle Scholar
• Yang, H., P. D. Jeffrey, J. Miller, E. Kinnucan, Y. Sun, N. H. Thoma, N. Zheng, P. L. Chen, W. H. Lee, and N. P. Pavletich. 2002. BRCA2 function in DNA binding and recombination from a BRCA2-DSS1-ssDNA structure. Science 297:1837–1848.
   PubMed Web of Science ®Google Scholar
• Zou, H., and R. Rothstein. 1997. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell 90:87–96.
   PubMedGoogle Scholar