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. 2000 Feb;154(2):543–556. doi: 10.1093/genetics/154.2.543

The Saccharomyces cerevisiae DNA recombination and repair functions of the RAD52 epistasis group inhibit Ty1 transposition.

A J Rattray 1, B K Shafer 1, D J Garfinkel 1
PMCID: PMC1460957  PMID: 10655210

Abstract

RNA transcribed from the Saccharomyces cerevisiae retrotransposon Ty1 accumulates to a high level in mitotically growing haploid cells, yet transposition occurs at very low frequencies. The product of reverse transcription is a linear double-stranded DNA molecule that reenters the genome by either Ty1-integrase-mediated insertion or homologous recombination with one of the preexisting genomic Ty1 (or delta) elements. Here we examine the role of the cellular homologous recombination functions on Ty1 transposition. We find that transposition is elevated in cells mutated for genes in the RAD52 recombinational repair pathway, such as RAD50, RAD51, RAD52, RAD54, or RAD57, or in the DNA ligase I gene CDC9, but is not elevated in cells mutated in the DNA repair functions encoded by the RAD1, RAD2, or MSH2 genes. The increase in Ty1 transposition observed when genes in the RAD52 recombinational pathway are mutated is not associated with a significant increase in Ty1 RNA or proteins. However, unincorporated Ty1 cDNA levels are markedly elevated. These results suggest that members of the RAD52 recombinational repair pathway inhibit Ty1 post-translationally by influencing the fate of Ty1 cDNA.

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Selected References

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  1. Alani E., Reenan R. A., Kolodner R. D. Interaction between mismatch repair and genetic recombination in Saccharomyces cerevisiae. Genetics. 1994 May;137(1):19–39. doi: 10.1093/genetics/137.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alani E., Subbiah S., Kleckner N. The yeast RAD50 gene encodes a predicted 153-kD protein containing a purine nucleotide-binding domain and two large heptad-repeat regions. Genetics. 1989 May;122(1):47–57. doi: 10.1093/genetics/122.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Belcourt M. F., Farabaugh P. J. Ribosomal frameshifting in the yeast retrotransposon Ty: tRNAs induce slippage on a 7 nucleotide minimal site. Cell. 1990 Jul 27;62(2):339–352. doi: 10.1016/0092-8674(90)90371-K. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benson F. E., Baumann P., West S. C. Synergistic actions of Rad51 and Rad52 in recombination and DNA repair. Nature. 1998 Jan 22;391(6665):401–404. doi: 10.1038/34937. [DOI] [PubMed] [Google Scholar]
  5. Bertrand P., Tishkoff D. X., Filosi N., Dasgupta R., Kolodner R. D. Physical interaction between components of DNA mismatch repair and nucleotide excision repair. Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14278–14283. doi: 10.1073/pnas.95.24.14278. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bhatia P. K., Wang Z., Friedberg E. C. DNA repair and transcription. Curr Opin Genet Dev. 1996 Apr;6(2):146–150. doi: 10.1016/s0959-437x(96)80043-8. [DOI] [PubMed] [Google Scholar]
  7. Boeke J. D., Devine S. E. Yeast retrotransposons: finding a nice quiet neighborhood. Cell. 1998 Jun 26;93(7):1087–1089. doi: 10.1016/s0092-8674(00)81450-6. [DOI] [PubMed] [Google Scholar]
  8. Boeke J. D., Garfinkel D. J., Styles C. A., Fink G. R. Ty elements transpose through an RNA intermediate. Cell. 1985 Mar;40(3):491–500. doi: 10.1016/0092-8674(85)90197-7. [DOI] [PubMed] [Google Scholar]
  9. Boeke J. D., Styles C. A., Fink G. R. Saccharomyces cerevisiae SPT3 gene is required for transposition and transpositional recombination of chromosomal Ty elements. Mol Cell Biol. 1986 Nov;6(11):3575–3581. doi: 10.1128/mcb.6.11.3575. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bradshaw V. A., McEntee K. DNA damage activates transcription and transposition of yeast Ty retrotransposons. Mol Gen Genet. 1989 Sep;218(3):465–474. doi: 10.1007/BF00332411. [DOI] [PubMed] [Google Scholar]
  11. Cao L., Alani E., Kleckner N. A pathway for generation and processing of double-strand breaks during meiotic recombination in S. cerevisiae. Cell. 1990 Jun 15;61(6):1089–1101. doi: 10.1016/0092-8674(90)90072-m. [DOI] [PubMed] [Google Scholar]
  12. Chen W., Jinks-Robertson S. Mismatch repair proteins regulate heteroduplex formation during mitotic recombination in yeast. Mol Cell Biol. 1998 Nov;18(11):6525–6537. doi: 10.1128/mcb.18.11.6525. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Clever B., Interthal H., Schmuckli-Maurer J., King J., Sigrist M., Heyer W. D. Recombinational repair in yeast: functional interactions between Rad51 and Rad54 proteins. EMBO J. 1997 May 1;16(9):2535–2544. doi: 10.1093/emboj/16.9.2535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Conte D., Jr, Barber E., Banerjee M., Garfinkel D. J., Curcio M. J. Posttranslational regulation of Ty1 retrotransposition by mitogen-activated protein kinase Fus3. Mol Cell Biol. 1998 May;18(5):2502–2513. doi: 10.1128/mcb.18.5.2502. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Curcio M. J., Garfinkel D. J. New lines of host defense: inhibition of Ty1 retrotransposition by Fus3p and NER/TFIIH. Trends Genet. 1999 Feb;15(2):43–45. doi: 10.1016/s0168-9525(98)01643-6. [DOI] [PubMed] [Google Scholar]
  16. Curcio M. J., Hedge A. M., Boeke J. D., Garfinkel D. J. Ty RNA levels determine the spectrum of retrotransposition events that activate gene expression in Saccharomyces cerevisiae. Mol Gen Genet. 1990 Jan;220(2):213–221. doi: 10.1007/BF00260484. [DOI] [PubMed] [Google Scholar]
  17. Datta A., Adjiri A., New L., Crouse G. F., Jinks Robertson S. Mitotic crossovers between diverged sequences are regulated by mismatch repair proteins in Saccaromyces cerevisiae. Mol Cell Biol. 1996 Mar;16(3):1085–1093. doi: 10.1128/mcb.16.3.1085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Datta A., Hendrix M., Lipsitch M., Jinks-Robertson S. Dual roles for DNA sequence identity and the mismatch repair system in the regulation of mitotic crossing-over in yeast. Proc Natl Acad Sci U S A. 1997 Sep 2;94(18):9757–9762. doi: 10.1073/pnas.94.18.9757. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Davies A. A., Friedberg E. C., Tomkinson A. E., Wood R. D., West S. C. Role of the Rad1 and Rad10 proteins in nucleotide excision repair and recombination. J Biol Chem. 1995 Oct 20;270(42):24638–24641. doi: 10.1074/jbc.270.42.24638. [DOI] [PubMed] [Google Scholar]
  20. Derr L. K., Strathern J. N. A role for reverse transcripts in gene conversion. Nature. 1993 Jan 14;361(6408):170–173. doi: 10.1038/361170a0. [DOI] [PubMed] [Google Scholar]
  21. Eibel H., Gafner J., Stotz A., Philippsen P. Characterization of the yeast mobile element Ty1. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):609–617. doi: 10.1101/sqb.1981.045.01.079. [DOI] [PubMed] [Google Scholar]
  22. Eichinger D. J., Boeke J. D. The DNA intermediate in yeast Ty1 element transposition copurifies with virus-like particles: cell-free Ty1 transposition. Cell. 1988 Sep 23;54(7):955–966. doi: 10.1016/0092-8674(88)90110-9. [DOI] [PubMed] [Google Scholar]
  23. Elder R. T., Loh E. Y., Davis R. W. RNA from the yeast transposable element Ty1 has both ends in the direct repeats, a structure similar to retrovirus RNA. Proc Natl Acad Sci U S A. 1983 May;80(9):2432–2436. doi: 10.1073/pnas.80.9.2432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Emery H. S., Schild D., Kellogg D. E., Mortimer R. K. Sequence of RAD54, a Saccharomyces cerevisiae gene involved in recombination and repair. Gene. 1991 Jul 31;104(1):103–106. doi: 10.1016/0378-1119(91)90473-o. [DOI] [PubMed] [Google Scholar]
  25. Fink G., Farabaugh P., Roeder G., Chaleff D. Transposable elements (Ty) in yeast. Cold Spring Harb Symp Quant Biol. 1981;45(Pt 2):575–580. doi: 10.1101/sqb.1981.045.01.074. [DOI] [PubMed] [Google Scholar]
  26. Fishman-Lobell J., Haber J. E. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science. 1992 Oct 16;258(5081):480–484. doi: 10.1126/science.1411547. [DOI] [PubMed] [Google Scholar]
  27. Flavell A. J. Retroelements, reverse transcriptase and evolution. Comp Biochem Physiol B Biochem Mol Biol. 1995 Jan;110(1):3–15. doi: 10.1016/0305-0491(94)00122-b. [DOI] [PubMed] [Google Scholar]
  28. Furuse M., Nagase Y., Tsubouchi H., Murakami-Murofushi K., Shibata T., Ohta K. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 1998 Nov 2;17(21):6412–6425. doi: 10.1093/emboj/17.21.6412. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Game J. C. DNA double-strand breaks and the RAD50-RAD57 genes in Saccharomyces. Semin Cancer Biol. 1993 Apr;4(2):73–83. [PubMed] [Google Scholar]
  30. Game J. C., Johnston L. H., von Borstel R. C. Enhanced mitotic recombination in a ligase-defective mutant of the yeast Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4589–4592. doi: 10.1073/pnas.76.9.4589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Game J. C., Mortimer R. K. A genetic study of x-ray sensitive mutants in yeast. Mutat Res. 1974 Sep;24(3):281–292. doi: 10.1016/0027-5107(74)90176-6. [DOI] [PubMed] [Google Scholar]
  32. Garfinkel D. J., Boeke J. D., Fink G. R. Ty element transposition: reverse transcriptase and virus-like particles. Cell. 1985 Sep;42(2):507–517. doi: 10.1016/0092-8674(85)90108-4. [DOI] [PubMed] [Google Scholar]
  33. Garfinkel D. J. Genetic loose change: how retroelements and reverse transcriptase heal broken chromosomes. Trends Microbiol. 1997 May;5(5):173–175. doi: 10.1016/S0966-842X(97)01018-4. [DOI] [PubMed] [Google Scholar]
  34. Garfinkel D. J., Hedge A. M., Youngren S. D., Copeland T. D. Proteolytic processing of pol-TYB proteins from the yeast retrotransposon Ty1. J Virol. 1991 Sep;65(9):4573–4581. doi: 10.1128/jvi.65.9.4573-4581.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Goffeau A., Barrell B. G., Bussey H., Davis R. W., Dujon B., Feldmann H., Galibert F., Hoheisel J. D., Jacq C., Johnston M. Life with 6000 genes. Science. 1996 Oct 25;274(5287):546, 563-7. doi: 10.1126/science.274.5287.546. [DOI] [PubMed] [Google Scholar]
  36. Guzder S. N., Habraken Y., Sung P., Prakash L., Prakash S. Reconstitution of yeast nucleotide excision repair with purified Rad proteins, replication protein A, and transcription factor TFIIH. J Biol Chem. 1995 Jun 2;270(22):12973–12976. doi: 10.1074/jbc.270.22.12973. [DOI] [PubMed] [Google Scholar]
  37. Hoffman C. S., Winston F. A ten-minute DNA preparation from yeast efficiently releases autonomous plasmids for transformation of Escherichia coli. Gene. 1987;57(2-3):267–272. doi: 10.1016/0378-1119(87)90131-4. [DOI] [PubMed] [Google Scholar]
  38. Huang H., Hong J. Y., Burck C. L., Liebman S. W. Host genes that affect the target-site distribution of the yeast retrotransposon Ty1. Genetics. 1999 Apr;151(4):1393–1407. doi: 10.1093/genetics/151.4.1393. [DOI] [PMC free article] [PubMed] [Google Scholar]
  39. Ito H., Fukuda Y., Murata K., Kimura A. Transformation of intact yeast cells treated with alkali cations. J Bacteriol. 1983 Jan;153(1):163–168. doi: 10.1128/jb.153.1.163-168.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Ivanov E. L., Sugawara N., Fishman-Lobell J., Haber J. E. Genetic requirements for the single-strand annealing pathway of double-strand break repair in Saccharomyces cerevisiae. Genetics. 1996 Mar;142(3):693–704. doi: 10.1093/genetics/142.3.693. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Ji H., Moore D. P., Blomberg M. A., Braiterman L. T., Voytas D. F., Natsoulis G., Boeke J. D. Hotspots for unselected Ty1 transposition events on yeast chromosome III are near tRNA genes and LTR sequences. Cell. 1993 Jun 4;73(5):1007–1018. doi: 10.1016/0092-8674(93)90278-x. [DOI] [PubMed] [Google Scholar]
  42. Jiricny J. Replication errors: cha(lle)nging the genome. EMBO J. 1998 Nov 16;17(22):6427–6436. doi: 10.1093/emboj/17.22.6427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Johnson R. D., Symington L. S. Functional differences and interactions among the putative RecA homologs Rad51, Rad55, and Rad57. Mol Cell Biol. 1995 Sep;15(9):4843–4850. doi: 10.1128/mcb.15.9.4843. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Johzuka K., Ogawa H. Interaction of Mre11 and Rad50: two proteins required for DNA repair and meiosis-specific double-strand break formation in Saccharomyces cerevisiae. Genetics. 1995 Apr;139(4):1521–1532. doi: 10.1093/genetics/139.4.1521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Jordan I. K., McDonald J. F. Evidence for the role of recombination in the regulatory evolution of Saccharomyces cerevisiae Ty elements. J Mol Evol. 1998 Jul;47(1):14–20. doi: 10.1007/pl00006358. [DOI] [PubMed] [Google Scholar]
  46. Jordan I. K., McDonald J. F. Tempo and mode of Ty element evolution in Saccharomyces cerevisiae. Genetics. 1999 Apr;151(4):1341–1351. doi: 10.1093/genetics/151.4.1341. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Kim J. M., Vanguri S., Boeke J. D., Gabriel A., Voytas D. F. Transposable elements and genome organization: a comprehensive survey of retrotransposons revealed by the complete Saccharomyces cerevisiae genome sequence. Genome Res. 1998 May;8(5):464–478. doi: 10.1101/gr.8.5.464. [DOI] [PubMed] [Google Scholar]
  48. Kupiec M., Petes T. D. Meiotic recombination between repeated transposable elements in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jul;8(7):2942–2954. doi: 10.1128/mcb.8.7.2942. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Lee B. S., Lichtenstein C. P., Faiola B., Rinckel L. A., Wysock W., Curcio M. J., Garfinkel D. J. Posttranslational inhibition of Ty1 retrotransposition by nucleotide excision repair/transcription factor TFIIH subunits Ssl2p and Rad3p. Genetics. 1998 Apr;148(4):1743–1761. doi: 10.1093/genetics/148.4.1743. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Liebman S. W., Newnam G. A ubiquitin-conjugating enzyme, RAD6, affects the distribution of Ty1 retrotransposon integration positions. Genetics. 1993 Mar;133(3):499–508. doi: 10.1093/genetics/133.3.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Liefshitz B., Parket A., Maya R., Kupiec M. The role of DNA repair genes in recombination between repeated sequences in yeast. Genetics. 1995 Aug;140(4):1199–1211. doi: 10.1093/genetics/140.4.1199. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Liefshitz B., Steinlauf R., Friedl A., Eckardt-Schupp F., Kupiec M. Genetic interactions between mutants of the 'error-prone' repair group of Saccharomyces cerevisiae and their effect on recombination and mutagenesis. Mutat Res. 1998 Mar;407(2):135–145. doi: 10.1016/s0921-8777(97)00070-0. [DOI] [PubMed] [Google Scholar]
  53. Lovett S. T., Mortimer R. K. Characterization of null mutants of the RAD55 gene of Saccharomyces cerevisiae: effects of temperature, osmotic strength and mating type. Genetics. 1987 Aug;116(4):547–553. doi: 10.1093/genetics/116.4.547. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Malone R. E., Ward T., Lin S., Waring J. The RAD50 gene, a member of the double strand break repair epistasis group, is not required for spontaneous mitotic recombination in yeast. Curr Genet. 1990 Aug;18(2):111–116. doi: 10.1007/BF00312598. [DOI] [PubMed] [Google Scholar]
  55. McClanahan T., McEntee K. DNA damage and heat shock dually regulate genes in Saccharomyces cerevisiae. Mol Cell Biol. 1986 Jan;6(1):90–96. doi: 10.1128/mcb.6.1.90. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. McClanahan T., McEntee K. Specific transcripts are elevated in Saccharomyces cerevisiae in response to DNA damage. Mol Cell Biol. 1984 Nov;4(11):2356–2363. doi: 10.1128/mcb.4.11.2356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. McGill C. B., Shafer B. K., Derr L. K., Strathern J. N. Recombination initiated by double-strand breaks. Curr Genet. 1993;23(4):305–314. doi: 10.1007/BF00310891. [DOI] [PubMed] [Google Scholar]
  58. Modrich P., Lahue R. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu Rev Biochem. 1996;65:101–133. doi: 10.1146/annurev.bi.65.070196.000533. [DOI] [PubMed] [Google Scholar]
  59. Moore J. K., Haber J. E. Capture of retrotransposon DNA at the sites of chromosomal double-strand breaks. Nature. 1996 Oct 17;383(6601):644–646. doi: 10.1038/383644a0. [DOI] [PubMed] [Google Scholar]
  60. Moreau S., Ferguson J. R., Symington L. S. The nuclease activity of Mre11 is required for meiosis but not for mating type switching, end joining, or telomere maintenance. Mol Cell Biol. 1999 Jan;19(1):556–566. doi: 10.1128/mcb.19.1.556. [DOI] [PMC free article] [PubMed] [Google Scholar]
  61. Mortensen U. H., Bendixen C., Sunjevaric I., Rothstein R. DNA strand annealing is promoted by the yeast Rad52 protein. Proc Natl Acad Sci U S A. 1996 Oct 1;93(20):10729–10734. doi: 10.1073/pnas.93.20.10729. [DOI] [PMC free article] [PubMed] [Google Scholar]
  62. Nairz K., Klein F. mre11S--a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 1997 Sep 1;11(17):2272–2290. doi: 10.1101/gad.11.17.2272. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Nevo-Caspi Y., Kupiec M. Induction of Ty recombination in yeast by cDNA and transcription: role of the RAD1 and RAD52 genes. Genetics. 1996 Nov;144(3):947–955. doi: 10.1093/genetics/144.3.947. [DOI] [PMC free article] [PubMed] [Google Scholar]
  64. Nevo-Caspi Y., Kupiec M. Transcriptional induction of Ty recombination in yeast. Proc Natl Acad Sci U S A. 1994 Dec 20;91(26):12711–12715. doi: 10.1073/pnas.91.26.12711. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Nevo-Caspi Y., Kupiec M. cDNA-mediated Ty recombination can take place in the absence of plus-strand cDNA synthesis, but not in the absence of the integrase protein. Curr Genet. 1997 Jul;32(1):32–40. doi: 10.1007/s002940050245. [DOI] [PubMed] [Google Scholar]
  66. New J. H., Sugiyama T., Zaitseva E., Kowalczykowski S. C. Rad52 protein stimulates DNA strand exchange by Rad51 and replication protein A. Nature. 1998 Jan 22;391(6665):407–410. doi: 10.1038/34950. [DOI] [PubMed] [Google Scholar]
  67. Nugent C. I., Bosco G., Ross L. O., Evans S. K., Salinger A. P., Moore J. K., Haber J. E., Lundblad V. Telomere maintenance is dependent on activities required for end repair of double-strand breaks. Curr Biol. 1998 May 21;8(11):657–660. doi: 10.1016/s0960-9822(98)70253-2. [DOI] [PubMed] [Google Scholar]
  68. Ogawa T., Yu X., Shinohara A., Egelman E. H. Similarity of the yeast RAD51 filament to the bacterial RecA filament. Science. 1993 Mar 26;259(5103):1896–1899. doi: 10.1126/science.8456314. [DOI] [PubMed] [Google Scholar]
  69. Orphanides G., Lagrange T., Reinberg D. The general transcription factors of RNA polymerase II. Genes Dev. 1996 Nov 1;10(21):2657–2683. doi: 10.1101/gad.10.21.2657. [DOI] [PubMed] [Google Scholar]
  70. Orr-Weaver T. L., Szostak J. W., Rothstein R. J. Yeast transformation: a model system for the study of recombination. Proc Natl Acad Sci U S A. 1981 Oct;78(10):6354–6358. doi: 10.1073/pnas.78.10.6354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  71. Paquin C. E., Williamson V. M. Temperature effects on the rate of ty transposition. Science. 1984 Oct 5;226(4670):53–55. doi: 10.1126/science.226.4670.53. [DOI] [PubMed] [Google Scholar]
  72. Petukhova G., Stratton S., Sung P. Catalysis of homologous DNA pairing by yeast Rad51 and Rad54 proteins. Nature. 1998 May 7;393(6680):91–94. doi: 10.1038/30037. [DOI] [PubMed] [Google Scholar]
  73. Pâques F., Haber J. E. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol Mol Biol Rev. 1999 Jun;63(2):349–404. doi: 10.1128/mmbr.63.2.349-404.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Pâques F., Haber J. E. Two pathways for removal of nonhomologous DNA ends during double-strand break repair in Saccharomyces cerevisiae. Mol Cell Biol. 1997 Nov;17(11):6765–6771. doi: 10.1128/mcb.17.11.6765. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Rattray A. J., Symington L. S. Multiple pathways for homologous recombination in Saccharomyces cerevisiae. Genetics. 1995 Jan;139(1):45–56. doi: 10.1093/genetics/139.1.45. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Roeder G. S., Fink G. R. DNA rearrangements associated with a transposable element in yeast. Cell. 1980 Aug;21(1):239–249. doi: 10.1016/0092-8674(80)90131-2. [DOI] [PubMed] [Google Scholar]
  77. Rolfe M. UV-inducible transcripts in Saccharomyces cerevisiae. Curr Genet. 1985;9(7):533–538. doi: 10.1007/BF00381164. [DOI] [PubMed] [Google Scholar]
  78. Rothstein R. J. One-step gene disruption in yeast. Methods Enzymol. 1983;101:202–211. doi: 10.1016/0076-6879(83)01015-0. [DOI] [PubMed] [Google Scholar]
  79. Rudin N., Sugarman E., Haber J. E. Genetic and physical analysis of double-strand break repair and recombination in Saccharomyces cerevisiae. Genetics. 1989 Jul;122(3):519–534. doi: 10.1093/genetics/122.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Saparbaev M., Prakash L., Prakash S. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae. Genetics. 1996 Mar;142(3):727–736. doi: 10.1093/genetics/142.3.727. [DOI] [PMC free article] [PubMed] [Google Scholar]
  81. Schiestl R. H., Zhu J., Petes T. D. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol Cell Biol. 1994 Jul;14(7):4493–4500. doi: 10.1128/mcb.14.7.4493. [DOI] [PMC free article] [PubMed] [Google Scholar]
  82. Sharon G., Burkett T. J., Garfinkel D. J. Efficient homologous recombination of Ty1 element cDNA when integration is blocked. Mol Cell Biol. 1994 Oct;14(10):6540–6551. doi: 10.1128/mcb.14.10.6540. [DOI] [PMC free article] [PubMed] [Google Scholar]
  83. Sharples G. J., Leach D. R. Structural and functional similarities between the SbcCD proteins of Escherichia coli and the RAD50 and MRE11 (RAD32) recombination and repair proteins of yeast. Mol Microbiol. 1995 Sep;17(6):1215–1217. doi: 10.1111/j.1365-2958.1995.mmi_17061215_1.x. [DOI] [PubMed] [Google Scholar]
  84. Shinohara A., Ogawa H., Ogawa T. Rad51 protein involved in repair and recombination in S. cerevisiae is a RecA-like protein. Cell. 1992 May 1;69(3):457–470. doi: 10.1016/0092-8674(92)90447-k. [DOI] [PubMed] [Google Scholar]
  85. Shinohara A., Ogawa T. Stimulation by Rad52 of yeast Rad51-mediated recombination. Nature. 1998 Jan 22;391(6665):404–407. doi: 10.1038/34943. [DOI] [PubMed] [Google Scholar]
  86. Strathern J. N., Klar A. J., Hicks J. B., Abraham J. A., Ivy J. M., Nasmyth K. A., McGill C. Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus. Cell. 1982 Nov;31(1):183–192. doi: 10.1016/0092-8674(82)90418-4. [DOI] [PubMed] [Google Scholar]
  87. Sugawara N., Pâques F., Colaiácovo M., Haber J. E. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proc Natl Acad Sci U S A. 1997 Aug 19;94(17):9214–9219. doi: 10.1073/pnas.94.17.9214. [DOI] [PMC free article] [PubMed] [Google Scholar]
  88. Sugiyama T., New J. H., Kowalczykowski S. C. DNA annealing by RAD52 protein is stimulated by specific interaction with the complex of replication protein A and single-stranded DNA. Proc Natl Acad Sci U S A. 1998 May 26;95(11):6049–6054. doi: 10.1073/pnas.95.11.6049. [DOI] [PMC free article] [PubMed] [Google Scholar]
  89. Sun H., Treco D., Schultes N. P., Szostak J. W. Double-strand breaks at an initiation site for meiotic gene conversion. Nature. 1989 Mar 2;338(6210):87–90. doi: 10.1038/338087a0. [DOI] [PubMed] [Google Scholar]
  90. Sung P. Catalysis of ATP-dependent homologous DNA pairing and strand exchange by yeast RAD51 protein. Science. 1994 Aug 26;265(5176):1241–1243. doi: 10.1126/science.8066464. [DOI] [PubMed] [Google Scholar]
  91. Sung P., Robberson D. L. DNA strand exchange mediated by a RAD51-ssDNA nucleoprotein filament with polarity opposite to that of RecA. Cell. 1995 Aug 11;82(3):453–461. doi: 10.1016/0092-8674(95)90434-4. [DOI] [PubMed] [Google Scholar]
  92. 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 May 1;11(9):1111–1121. doi: 10.1101/gad.11.9.1111. [DOI] [PubMed] [Google Scholar]
  93. Svejstrup J. Q., Vichi P., Egly J. M. The multiple roles of transcription/repair factor TFIIH. Trends Biochem Sci. 1996 Sep;21(9):346–350. [PubMed] [Google Scholar]
  94. Svejstrup J. Q., Wang Z., Feaver W. J., Wu X., Bushnell D. A., Donahue T. F., Friedberg E. C., Kornberg R. D. Different forms of TFIIH for transcription and DNA repair: holo-TFIIH and a nucleotide excision repairosome. Cell. 1995 Jan 13;80(1):21–28. doi: 10.1016/0092-8674(95)90447-6. [DOI] [PubMed] [Google Scholar]
  95. Temin H. M. Reverse transcription in the eukaryotic genome: retroviruses, pararetroviruses, retrotransposons, and retrotranscripts. Mol Biol Evol. 1985 Nov;2(6):455–468. doi: 10.1093/oxfordjournals.molbev.a040365. [DOI] [PubMed] [Google Scholar]
  96. Teng S. C., Kim B., Gabriel A. Retrotransposon reverse-transcriptase-mediated repair of chromosomal breaks. Nature. 1996 Oct 17;383(6601):641–644. doi: 10.1038/383641a0. [DOI] [PubMed] [Google Scholar]
  97. Thomas B. J., Rothstein R. The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination at GAL10, a transcriptionally regulated gene. Genetics. 1989 Dec;123(4):725–738. doi: 10.1093/genetics/123.4.725. [DOI] [PMC free article] [PubMed] [Google Scholar]
  98. Tomkinson A. E., Bardwell A. J., Bardwell L., Tappe N. J., Friedberg E. C. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature. 1993 Apr 29;362(6423):860–862. doi: 10.1038/362860a0. [DOI] [PubMed] [Google Scholar]
  99. Usui T., Ohta T., Oshiumi H., Tomizawa J., Ogawa H., Ogawa T. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell. 1998 Nov 25;95(5):705–716. doi: 10.1016/s0092-8674(00)81640-2. [DOI] [PubMed] [Google Scholar]
  100. Weinstock K. G., Mastrangelo M. F., Burkett T. J., Garfinkel D. J., Strathern J. N. Multimeric arrays of the yeast retrotransposon Ty. Mol Cell Biol. 1990 Jun;10(6):2882–2892. doi: 10.1128/mcb.10.6.2882. [DOI] [PMC free article] [PubMed] [Google Scholar]
  101. Wilke C. M., Maimer E., Adams J. The population biology and evolutionary significance of Ty elements in Saccharomyces cerevisiae. Genetica. 1992;86(1-3):155–173. doi: 10.1007/BF00133718. [DOI] [PubMed] [Google Scholar]
  102. Winston F., Durbin K. J., Fink G. R. The SPT3 gene is required for normal transcription of Ty elements in S. cerevisiae. Cell. 1984 Dec;39(3 Pt 2):675–682. doi: 10.1016/0092-8674(84)90474-4. [DOI] [PubMed] [Google Scholar]

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