Recombinational repair in yeast: Functional interactions between Rad51 and Rad54 proteins

EMBO Journal

Volumn 16, Issue 9, 1997, Pages 2535-2544

  Clever, Beate ^a   Interthal, Heidrun ^a   Schmuckli Maurer, Jacqueline ^a   King, Jeff ^a   Sigrist, Markus ^a   Heyer, Wolf Dietrich ^a  

^a CH 3012   (Switzerland)

Author keywords

DNA repair; RAD51; RAD54; Recombination; S.cerevisiae

Indexed keywords

ADENOSINE TRIPHOSPHATASE; FUNGAL PROTEIN; MESYLIC ACID METHYL ESTER;

ARTICLE; CONTROLLED STUDY; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA STRAND BREAKAGE; EVOLUTION; GAMMA RADIATION; GENE DELETION; MATING TYPE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE;

BLOTTING, WESTERN; DNA DAMAGE; DNA REPAIR; DNA, FUNGAL; DNA-BINDING PROTEINS; FUNGAL PROTEINS; PROTEIN BINDING; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

ESCHERICHIA COLI; EUKARYOTA; SACCHAROMYCES CEREVISIAE;

EID: 0030910889     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.9.2535     Document Type: Article

References (75)

1. Aboussekhra, A.R., Chanet, R., Adjiri, A. and Fabre, F. (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.
2. Auble, D.T., Hansen, K.E., Mueller, C.G.F., Lane, W.S., Thorner, J. and Hahn, S. (1994) Mot1, a global repressor of RNA polymerase II transcription, inhibits TBP binding to DNA by an ATP-dependent mechanism. Genes Dev., 8, 1920-1934.
3. SEP1 arrest at pachytene during meiotic prophase. Chromosoma, 103, 129-141.
4. Bashkirov, V.I., Solinger, J.A. and Heyer, W.-D. (1995) Identification of functional domains in the Sep1 protein (= Kem1, Xrn1), which is required for transition through meiotic prophase in Saccharomyces cerevisiae. Chromosoma, 104, 215-222.
5. Basile, G., Aker, M. and Mortimer, R.K. (1992) Nucleotide sequence and transcriptional regulation of the yeast recombinational repair gene RAD51. Mol. Cell. Biol., 12, 3235-3246.
6. Bendixen, C., Sunjeyaric, I., Bauchwitz, R. and Rothstein, R. (1994) Identification of a mouse homologue of the Saccharomyces cerevisiae recombination and repair gene, RAD52. Genomics, 23, 300-303.
7. Bezzubova, O.Y., Schmidt, H., Ostermann, K., Heyer, W.-D. and Buerstedde, J.-M. (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.
8. Bishop, D.K., Park, D., Xu, L. and Kleckner, N. (1992) DMC1, a meiosis-specitic yeast homolog of E.coli recA required for recombination, synaptonemal complex formation, and cell cycle progression. Cell, 69, 439-456.
9. Broach, J.R., Strathern, J.N. and Hicks, J.B. (1979) Transformation in yeast: development of a hybrid cloning vector and isolation of the CAN1 gene. Gene, 8, 121-133.
10. Calderon, I.L., Contopoulou, C.R. and Mortimer, R.K. (1983) Isolation and characterization of yeast repair genes. II. Isolation of plasmids that complement the mutations rad50-1, rad51-1, rad54-3, and rad55-3. Curr. Genet., 7, 93-100.
11. Donovan, J.W., Milne, G.T. and Weaver, D.T. (1994) Homotypic and heterotypic protein associations control Rad51 function in double-strand break repair. Genes Dev., 8, 2552-2562.
12. Eisen, J.A., Sweder, K.S. and Hanawalt, P.C. (1995) Evolution of the SNF2 family of proteins: subfamilies with distinct sequences and functions. Nucleic Acids Res., 23, 2715-2723.
13. Emery, H.S., Schild, D., Kellogg, E. and Mortimer, R.K. (1991) Sequence of RAD54, a Saccharomyces cerevisiae gene involved in recombination and repair. Gene, 104, 103-106.
14. Fields, S. and Song, O.-K. (1989) A novel genetic system to detect protein-protein interactions. Nature, 340, 245-246.
15. Firmenich, A.A., Elias-Arnanz, M. and Berg, P. (1995) A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52. Mol. Cell. Biol., 15, 1620-1631.
16. Fishman-Lobell, J., Rudin, N. and Haber, J.E. (1992) Two alternative pathways of double-strand break repair that are kinetically separable and independently modulated. Mol. Cell. Biol., 12, 1292-1303.
17. Friedberg, E.C., Walker, G.C. and Siede, W. (1995) DNA Repair and Mutagenesis. American Society for Microbiology, Washington, DC.
18. Game, J.C. (1983) Radiation-sensitive mutants and repair in yeast. In Spencer, J.F.T., Spencer, D. and Smith, A.R.W. (eds), Yeast Genetics, Fundamental and Applied Aspects. Springer-Verlag, New York, pp. 109-137.
19. Game, J.C. (1993) DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin. Cancer Biol., 4, 73-83.
20. Gorbalenya, A.E. and Koonin, E.V. (1993) Helicases: amino acid sequence comparisons and structure-function relationships. Curr. Opin. Struct. Biol., 3, 419-429.
21. Guzder, S.N., Sung, P., Prakash, L. and Prakash, S. (1996) Nucleotide excision repair in yeast is mediated by sequential assembly of repair factors and not by a pre-assembled repairosome. J. Biol. Chem., 271, 8903-8910.
22. Gyuris, J., Golemis, E.A., Chertkov, H. and Brent, R. (1993) Cdi1, a human G1 and S phase protein phosphatase that associates with Cdk2. Cell, 75, 791-803.
23. Haber, J.E. (1992) Exploring the pathways of homologous recombination. Curr. Opin. Cell. Biol., 4, 401-412.
24. Harshman, K.D., Moye-Rowley, W.S. and Parker, C.S. (1988) Transcriptional activation by the SV40 AP-1 recognition element in yeast is mediated by a factor similar to AP-1 that is distinct from GCN4. Cell, 53, 321-330.
25. Haynes, R.H. and Kunz, B.A. (1981) DNA repair and mutagenesis in yeast. In Strathern, J.N., Jones, E.W. and Broach, J.R. (eds), The Molecular Biology of the Yeast Saccharomyces, Life Cycle and Inheritance. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 371-414.
26. Hays, S.L., Firmenich, A.A. and Berg, P. (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.
27. Heyer, W.-D. (1994) The search for the right partner: homologous pairing and DNA strand exchange proteins in eukaryotes. Experientia, 50, 223-233.
28. Hoeijmakers, J.H.J. (1993) Nucleotide excision repair II: from yeast to mammals. Trends Genet., 9, 211-217.
29. Holler, A., Bashkirov, V.I., Solinger, J.A., Reinhart, U. and Heyer, W.-D. (1995) Use of monoclonal antibodies in the functional characterization of the Saccharomyces cerevisiae Sep1 protein. Eur. J. Biochem., 231, 329-336.
30. Johnson, R.D. and Symington, L.S. (1995) Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol. Cell. Biol., 15, 4843-4850.
31. Kanaar, R. et al. (1996) Human and mouse homologs of the Saccharomyces cerevisiae RAD54 DNA repair gene: evidence for functional conservation. Curr. Biol., 6, 828-838.
32. Kaus, J.A. and Mortimer, R.K. (1991) Nucleotide sequence of the RAD57 gene of Saccharomyces cerevisiae. Gene, 105, 139-140.
33. Kleckner, N., Padmore, R. and Bishop, D.K. (1991) Meiotic chromosome metabolism: one view. Cold Spring Harbor Symp. Quant. Biol., 56, 729-743.
34. Kolodner, R. (1996) Biochemistry and genetics of eukaryotic mismatch repair. Genes Dev., 10, 1433-1442.
35. Kornberg, A. and Baker, T.A. (1992) DNA Replication. W.H. Freeman and Company, NY.
36. Kowalczykowski, S.C. and Eggleston, A.K. (1994) Homologous pairing and DNA strand exchange proteins. Annu. Rev. Biochem., 63, 991-1043.
37. Kowalczykowski, S.C., Dixon, D.A., Eggleston, A.K., Lauder, S.D. and Rehrauer, W.M. (1994) Biochemistry of homologous recombination in Escherichia coli. Microbiol. Rev., 58, 401-465.
38. Kramer, K.M., Brock, J.A., Bloom, K., Moore, J.K. and Haber, J.E. (1994) Two different types of double-strand breaks in Saccharomyces cerevisiae are repaired by similar RAD52-independent, nonhomologous recombination events. Mol. Cell. Biol., 14, 1293-1301.
39. Lea, D.E. and Coulson, C.A. (1949) The distribution of the numbers of mutants in bacterial populations. J. Genet., 49, 264-285.
40. Lovett, S.T. (1994) Sequence of the RAD55 gene of Saccharomyces cerevisiae: similarity of RAD55 to prokaryotic RecA and other RecA-like proteins. Gene, 142, 103-106.
41. Lovett, S. and Mortimer, R.K. (1987) Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength, and mating type. Genetics, 116, 547-553.
42. Milne, G.T. and Weaver, D.T. (1993) Dominant-negative alleles of RAD52 reveal a DNA repair/recombination complex including Rad51 and Rad52. Genes Dev., 7, 1755-1765.
43. Muris, D.F.R. et al. (1994) Cloning of human and mouse genes homologous to RAD52, a yeast gene involved in DNA repair and recombination. Mutat. Res., 315, 295-305.
44. +, a gene involved in the repair of radiation damage and replication fidelity. Cell Sci., 109, 73-81.
45. Ogawa, T., Yu, X., Shinohara, A. and Egelman, E.H. (1993) Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science, 259, 1896-1899.
46. Peterson, C.L. and Tamkun, J.W. (1995) The SWI-SNF complex: a chromatin remodeling machine? Trends Biochem. Sci., 20, 143-146.
47. Petes, T.D., Malone, R.E. and Symington, L.S. (1991) Recombination in yeast. In Broach, J.R., Pringle, J.R. and Jones, E.W. (eds), The Molecular and Cellular Biology of the Yeast Saccharomyces: Genome Dynamics, Protein Synthesis, and Energetics. Cold Spring Habor Laboratory Press, Cold Spring Harbor, NY, pp. 407-521.
48. Resnick, M.A. (1976) The repair of double-strand breaks in DNA: a model involving recombination. J. Theor. Biol., 59, 97-106.
49. Roeder, G.S. (1995) Sex and the single cell: meiosis in yeast. Proc. Natl Acad. Sci. USA, 92, 10450-10456.
50. Roth, D. and Wilson, J. (1988) Illegitimate recombination in mammalian cells. In Kucherlapati, R. and Smith, G.R. (eds), Genetic Recombination. American Society for Microbiology, Washington, DC, pp. 621-653.
51. Salinas, F. and Kodadek, T. (1995) Phage T4 homologous strand exchange: a DNA helicase, not the strand transferase, drives polar branch migration. Cell, 82, 111-119.
52. Sancar, A. and Hearst, J.E. (1993) Molecular matchmakers. Science, 259, 1415-1420.
53. Sandler, S.J., Satin, L.H., Samra, H.S. and Clark, A.J. (1996) recA-like genes from three archaean species with putative protein products similar to Rad51 and Dmc1 proteins of the yeast Saccharomyces cerevisiae. Nucleic Acids Res., 24, 2125-2132.
54. Santos-Rosa, H., Clever, B., Heyer, W.-D. and Aguilera, A. (1996) The yeast HRS1 gene encodes a polyglutamine-rich nuclear protein required for spontaneous and hpr1-induced deletion between direct repeats. Genetics, 142, 705-716.
55. Schiestl, R.S. and Gietz, R.D. (1989) High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet., 16, 339-346.
56. Schild, D. (1995) Suppression of a new allele of the yeast RAD52 gene by overexpression of RAD51, mutations in srs2 and ccr4, or mating-type heterozygosity. Genetics, 140, 115-127.
57. Sherman, F., Fink, G.R. and Hicks, J.B. (1982) Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
58. Shinohara, A., Ogawa, H. and Ogawa, T. (1992) Rad51 protein involved in repair and recombination in S.cerevisiae is a RecA-like protein. Cell, 69, 457-470.
59. Shinohara, A., Ogawa, H., Matsuda, Y., Ushio, N., Ikeo, K. and Ogawa, T. (1993) Cloning of human, mouse and fission yeast recombination genes homologous to RAD51 and recA. Nature Genet., 4, 239-243.
60. Shinohara, A. and Ogawa, T. (1995) Homologous recombination and the roles of double-strand breaks. Trends Biochem. Sci., 20, 387-391.
61. Story, R.M. and Steitz, T.A. (1992) Structure of the recA protein-ADP complex. Nature, 355, 374-376.
62. Story, R.M., Weber, I.T. and Steitz, T.A. (1992) The structure of the E.coli recA protein monomer and polymer. Nature, 355, 318-325.
63. Story, R.M., Bishop, D.K., Kleckner, N. and Steitz, T.A. (1993) Structural relationship of bacterial RecA proteins to recombination proteins from bacteriophage and yeast. Science, 259, 1892-1896.
64. Struhl, K. (1995) Yeast transcriptional regulatory mechanisms. Annu. Rev. Genet., 29, 651-674.
65. Subramanya, H.S., Bird, L.E., Brannigan, J.A. and Wigley, D.B. (1996) Crystal structure of a DExx box DNA helicase. Nature, 384, 379-383.
66. Sugawara, N., Ivanov, E.L., Fishman-Lobell, J., Ray, B.L. and Haber, J.E. (1995) DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature, 373, 84-86.
67. Sung, P. (1994) Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science, 265, 1241-1243.
68. Sung, P. and Robberson, D.L. (1995) DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell, 82, 453-461.
69. Svejstrup, J.Q., Wang, Z., Feaver, W.J., Wu, X., Bushnell, D.A., Donahue, T.F., Friedberg, E.C. and Kornberg, R.D. (1995) Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell, 80, 21-28.
70. Szostak, J.W., Orr-Weaver, T.L., Rothstein, R.J. and Stahl, F.W. (1983) The double-strand-break repair model for recombination. Cell, 3, 725-738.
71. Tabor, S. and Richardson, C.C. (1985) A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl Acad. Sci. USA, 82, 4767-4771.
72. Wach, A., Brachat, A., Pohlmann, R. and Philippsen, P. (1994) New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast, 10, 1793-1808.
73. Weaver, D.T. (1995) What to do at an end: DNA double-strand-break repair. Trends Genet., 11, 388-392.
74. West, S.C. (1992) Enzymes and molecular mechanisms of genetic recombination. Annu. Rev. Biochem., 61, 603-640.
75. Wood, R.D. (1996) DNA repair in eukaryotes. Annu. Rev. Biochem., 65, 135-167.