The Drosophila melanogaster RAD54 Homolog, DmRAD54, Is Involved in the Repair of Radiation Damage and Recombination

REFERENCES

• Aboussekhra, A., R. Chanet, A. Adjiri, and F. Fabre. 1992. 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. 12:3224–3234.
   PubMedGoogle Scholar
• Akaboshi, E., Y. Inoue, and H. Ryo. 1994. Cloning of the cDNA and genomic DNA that correspond to the recA-like gene of Drosophila melanogaster. Jpn. J. Genet. 69:663–670.
   PubMedGoogle Scholar
• 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
• Basile, G., M. Aker, and R. K. Mortimer. 1992. Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol. Cell. Biol. 12:3235–3246.
   PubMed Web of Science ®Google Scholar
• Beall, E. L., and D. C. Rio. 1996. Drosophila IRBP/Ku p70 corresponds to the mutagen-sensitive mus309 gene and is involved in P-element excision in vivo. Genes Dev. 10:921–933.
   PubMed Web of Science ®Google Scholar
• Becker, H. J. 1976. Mitotic recombination, p. 1019–1087. In M. Ashburner and E. Novitski (ed.), The genetics and biology of Drosophila, vol. 1c. Academic Press, Ltd., London, United Kingdom.
   Google Scholar
• Bendixen, C., I. Sunjevaric, R. Bauchwitz, and R. Rothstein. 1994. Identification of a mouse homologue of the Saccharomyces cerevisiae recombination and repair gene, RAD52. Genomics 23:300–303.
   PubMedGoogle Scholar
• Bezzubova, O., H. Schmidt, K. Ostermann, W.-D. Heyer, and J.-M. Buerstedde. 1993. Identification of a chicken RAD52 homologue suggests conservation of the RAD52 recombination pathway throughout the evolution of higher eukaryotes. Nucleic Acids Res. 21:5945–5949.
   PubMedGoogle Scholar
• Bezzubova, O., A. Shinohara, R. G. Mueller, H. Ogawa, and J.-M. Buerstedde. 1993. A chicken RAD51 homologue is expressed at high levels in lymphoid and reproductive organs. Nucleic Acids Res. 21:1577–1580.
   PubMed Web of Science ®Google Scholar
• Boulton, S. J., and S. P. Jackson. 1996. Saccharomyces cerevisiae Ku70 potentiates illegitimate DNA double-strand break repair and serves as a barrier to error-prone DNA repair pathways. EMBO J. 15:5093–5103.
   PubMed Web of Science ®Google Scholar
• Cavener, D. R. 1987. Comparison of the consensus sequences flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res. 4:1353–1361.
   Google Scholar
• Chepurnaya, O. V., S. A. Kozhin, V. T. Peshekhonov, and V. G. Korolev. 1995. RAD58(XRS4)—a new gene in the RAD52 epistasis group. Curr. Genet. 28:274–279.
   PubMedGoogle Scholar
• Contopoulou, C. R., V. E. Cook, and R. K. Mortimer. 1987. Analysis of DNA double strand breakage and repair using orthogonal field alternation gel electrophoresis. Yeast 3:71–76.
   PubMed Web of Science ®Google Scholar
• Dolganov, G. M., R. S. Maser, A. Novikov, L. Tosto, S. Chong, D. A. Bressan, and H. J. Petrini. 1996. Human Rad50 is physically associated with human Mre11: identification of a conserved multiprotein complex implicated in recombinational DNA repair. Mol. Cell. Biol. 16:4832–4841.
   PubMed Web of Science ®Google Scholar
• Eckardt-Schupp, E. Personal communication.
   Google Scholar
• Eisen, J. A., K. S. Sweder, and P. C. Hanawalt. 1995. Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res. 23:2715–2723.
   PubMed Web of Science ®Google Scholar
• Engels, W. R., C. R. Preston, P. Thompson, and W. B. Eggleston. 1986. In situ hybridization to Drosophila salivary chromosomes with biotinylated DNA probes and alkaline phosphatase. Focus 8:6–8.
   Google Scholar
• Flygare, J., F. Benson, and D. Hellgren. 1996. Expression of the human RAD51 gene during the cell cycle in primary human peripheral blood lymphocytes. Biochim. Biophys. Acta 1312:231–236.
   PubMedGoogle Scholar
• Friedberg, E. C., G. C. Walker, and W. Siede. 1995. DNA repair and mutagenesis. ASM Press, Washington, D.C.
   Google Scholar
• Game, J. C. 1993. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin. Cancer Biol. 4:73–83.
   PubMed Web of Science ®Google Scholar
• Godwin, A. R., R. J. Bollag, D.-M. Christie, and R. M. Liskay. 1994. Spontaneous and restriction enzyme-induced chromosomal recombination in mammalian cells. Proc. Natl. Acad. Sci. USA 91:12554–12558.
   PubMed Web of Science ®Google Scholar
• Gorbalenya, A. E., and E. V. Koonin. 1993. Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol. 3:419–429.
   Web of Science ®Google Scholar
• Haynes, R. H., and B. A. Kunz. 1981. DNA repair and mutagenesis in yeast, p. 371–414. In J. Strathern, E. W. Jones and J. R. Broach (ed.), The molecular biology of the yeast Saccharomyces cerevisiae: life cycle and inheritance. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Jacoby, D. B., and P. C. Wensink. 1994. Yolk protein factor 1 is a Drosophila homolog of Ku, the DNA-binding subunit of a DNA-dependent protein kinase from humans. J. Biol. Chem. 269:11484–11491.
   PubMedGoogle Scholar
• Jang, Y. K., Y. H. Jin, E. M. Kim, F. Fabre, S. H. Hong, and S. D. Park. 1994. Cloning and sequence analysis of rhp51+, a Schizosaccharomyces pombe homolog of the Saccharomyces cerevisiae RAD51 gene. Gene 142:207–211.
   PubMedGoogle Scholar
• Jeggo, P. A., G. E. Taccioli, and S. P. Jackson. 1995. Menage a trois: double strand break repair, V(D)J recombination and DNA-PK. Bioessays 17:949–957.
   PubMed Web of Science ®Google Scholar
• Jeong-Yu, S., and D. Carroll. 1992. Test of the double-strand break repair model of recombination in Xenopus laevis oocytes. Mol. Cell. Biol. 12:112–119.
   PubMed Web of Science ®Google Scholar
• Kanaar, R., C. Troelstra, S. M. A. Swagemakers, J. Essers, B. Smit, J.-H. Franssen, A. Pastink, O. Bezzubova, J.-M. Buerstedde, B. Clever, W.-D. Heyer, and J. H. J. Hoeijmakers. 1996. Characterization of human and mouse homologs of the Saccharomyces cerevisiae double-strand DNA break repair gene RAD54. Curr. Biol. 6:828–838.
   PubMedGoogle Scholar
• Lehman, C. W., J. K. Trautman, and D. Carroll. 1994. Illegitimate recombination in Xenopus: characterization of end-joined junctions. Nucleic Acids Res. 22:434–442.
   PubMedGoogle Scholar
• Lim, D.-S., and P. Hasty. 1996. A mutation in mouse rad51 results in an early embryonic lethal that is suppresses by a mutation in p53. Mol. Cell. Biol. 16:7133–7143.
   PubMed Web of Science ®Google Scholar
• Lin, F.-L. M., K. Sperle, and N. Sternberg. 1990. Repair of double-stranded DNA breaks by homologous DNA fragments during transfer of DNA into mouse L cells. Mol. Cell. Biol. 10:113–119.
   PubMed Web of Science ®Google Scholar
• Lindsley, D. L., and G. G. Zimm. 1992. The genome of Drosophila melanogaster. Academic Press, Inc., San Diego, Calif.
   Google Scholar
• Lukacsovich, T., D. Yang, and A. S. Waldman. 1994. Repair of a specific double-strand break generated within a mammalian chromosome by yeast endonuclease I-SceI. Nucleic Acids Res. 22:5649–5657.
   PubMed Web of Science ®Google Scholar
• McKee, B. D., X.-J. Ren, and C.-S. Hong. 1996. A recA-like gene in Drosophila melanogaster that is expressed at high levels in female but not male meiotic tissues. Chromosoma 104:479–488.
   PubMedGoogle Scholar
• Milne, G. T., S. Jin, K. B. Shannon, and D. T. Weaver. 1996. Mutations in two ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol. Cell. Biol. 16:4189–4198.
   PubMedGoogle Scholar
• Morita, T., Y. Yoshimura, A. Yamamoto, K. Murata, M. Mori, H. Yamamoto, and A. Matsushiro. 1993. A mouse homolog of the Escherichia coli recA and Saccharomyces cerevisiae RAD51 genes. Proc. Natl. Acad. Sci. USA 90:6577–6580.
   PubMed Web of Science ®Google Scholar
• Mortensen, U. H., C. Bendixen, I. Sunjevaric, and R. Rothstein. 1996. DNA strand annealing is promoted by the yeast Rad52 protein. Proc. Natl. Acad. Sci. USA 93:10729–10734.
   PubMed Web of Science ®Google Scholar
• Mozer, B., R. Marlor, S. Parkhurst, and V. Corces. 1985. Characterization and developmental expression of a Drosophila ras oncogene. Mol. Cell. Biol. 5:885–889.
   PubMedGoogle Scholar
• Muris, D. F. R., O. Bezzubova, J.-M. Buerstedde, K. Vreeken, A. S. Balajee, C. J. Osgood, C. Troelstra, J. H. J. Hoeijmakers, K. Ostermann, H. Schmidt, A. T. Natarajan, J. C. J. Eeken, P. H. M. Lohman, and A. Pastink. 1994. Cloning of human and mouse genes homologous to RAD52, a yeast gene involved in DNA repair and recombination. Mutat. Res. 315:295–305.
   PubMedGoogle Scholar
• Muris, D. F. R., K. Vreeken, A. M. Carr, B. C. Broughton, A. R. Lehmann, P. H. M. Lohman, and A. Pastink. 1993. Cloning the RAD51 homologue of Schizosaccharomyces pombe. Nucleic Acids Res. 12:4586–4591.
   Google Scholar
• Muris, D. F. R., K. Vreeken, A. M. Carr, J. M. Murray, C. Smit, P. H. M. Lohman, and A. Pastink. 1996. Isolation of the Schizosaccharomyces pombe RAD54 homologue, rhp54+, a gene involved in the repair of radiation damage and replication fidelity. J. Cell Sci. 109:73–81.
   PubMedGoogle Scholar
• Ostermann, K., A. Lorentz, and H. Schmidt. 1993. 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. 21:5940–5944.
   PubMedGoogle Scholar
• Pastink, A., E. Heemskerk, M. J. M. Nivard, C. J. van Vliet, and E. W. Vogel. 1991. Mutational specificity of ethyl methanesulfonate in excision-repair proficient and deficient strains of Drosophila melanogaster. Mol. Gen. Genet. 229:213–218.
   PubMedGoogle Scholar
• Petes, T. D., R. E. Malone, and L. S. Symington. 1991. Recombination in yeast, p. 407–521. In J. Broach, J. Pringle, and E. Jones (ed.), The molecular and cellular biology of the yeast Saccharomyces: genome dynamics, protein synthesis, and energetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Petrini, J. H. J., M. E. Walsh, C. DiMare, X.-N. Chen, J. R. Korenberg, and D. T. Weaver. 1995. Isolation and characterization of the human MRE11 homologue. Genomics 29:80–86.
   PubMedGoogle Scholar
• Price, A. 1993. The repair of ionising radiation-induced damage to DNA. Cancer Biol. 4:61–71.
   PubMed Web of Science ®Google Scholar
• Roth, D. B., T. Lindahl, and M. Gellert. 1995. How to make ends meet. Curr. Biol. 5:496–499.
   PubMedGoogle Scholar
• Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Sander, M., K. Owenhaupt, W. S. Lane, and A. Rich. 1991. Cloning and characterization of Rrp1, the gene encoding Drosophila strand transferase: carboxy-terminal homology to DNA repair endo/exonucleases. Nucleic Acids Res. 19:4523–4529.
   PubMed Web of Science ®Google Scholar
• Sanger, F., S. Nicklen, and A. R. Coulson. 1977. DNA sequencing with chain-termination inhibitors. Proc. Natl. Acad. Sci. USA 74:5463–5467.
   PubMed Web of Science ®Google Scholar
• Shen, Z., K. Denison, R. Lobb, J. M. Gatewood, and D. J. Chen. 1995. The human and mouse homologs of the yeast RAD52 gene: cDNA cloning, sequence analysis, assignment to human chromosome 12p12.2-p13, and mRNA expression in mouse tissues. Genomics 25:199–206.
   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., H. Ogawa, and T. Ogawa. 1992. RAD51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell 69:457–470.
   PubMed Web of Science ®Google Scholar
• Siede, W., A. A. Friedl, I. Dianova, F. Eckardt-Schupp, and E. C. Friedberg. 1996. The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 142:91–102.
   PubMed Web of Science ®Google Scholar
• Sung, P., and D. L. Robberson. 1995. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell 82:453–461.
   PubMed Web of Science ®Google Scholar
• Szakmary, A. Personal communication.
   Google Scholar
• Taki, T., T. Ohnishi, A. Yamamote, S. Hiraga, N. Arita, S. Izumoto, T. Hayakawa, and T. Morita. 1996. Antisense inhibition of the RAD51 enhances radiosensitivity. Biochem. Biophys. Res. Commun. 223:434–438.
   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
• Tavassoli, M., M. Shayeghi, A. Nasim, and F. Z. Watts. 1995. Cloning and characterisation of the Schizosaccharomyces pombe rad32 gene: a gene required for repair of double-strand breaks and recombination. Nucleic Acids Res. 23:383–388.
   PubMedGoogle Scholar
• Troelstra, C., A. van Gool, J. de Wit, W. Vermeulen, D. Bootsma, and J. H. J. Hoeijmakers. 1992. ERCC6, a member of a subfamily of putative helicases, is involved in Cockayne’s syndrome and preferential repair of active genes. Cell 71:939–953.
   PubMed Web of Science ®Google Scholar
• Tsuzuki, T., Y. Fujii, K. Sakumi, Y. Tominaga, K. Nakao, M. Sekiguchi, A. Matusuhiro, 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
• Vogel, E. W. 1992. Tests for recombinagens in somatic cells of Drosophila. Mutat. Res. 284:159–175.
   PubMed Web of Science ®Google Scholar
• Weaver, D. T. 1995. What to do at an end: DNA double-strand-break repair. Trends Genet. 11:388–392.
   PubMedGoogle Scholar
• Yamamoto, A., T. Taki, H. Yagi, T. Habu, K. Yoshida, Y. Yoshimura, K. Yamamoto, A. Matsushiro, Y. Nishimune, and T. Morita. 1996. Cell cycledependent expression of the mouse Rad51 gene in proliferating cells. Mol. Gen. Genet. 251:1–12.
   PubMedGoogle Scholar
• Zdzienicka, M. Z. 1995. Mammalian mutants defective in the response to ionizing radiation-induced DNA damage. Mutat. Res. 336:203–213.
   PubMedGoogle Scholar