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. 1995 Mar;15(3):1620–1631. doi: 10.1128/mcb.15.3.1620

A novel allele of Saccharomyces cerevisiae RFA1 that is deficient in recombination and repair and suppressible by RAD52.

A A Firmenich 1, M Elias-Arnanz 1, P Berg 1
PMCID: PMC230386  PMID: 7862153

Abstract

To understand the mechanisms involved in homologous recombination, we have performed a search for Saccharomyces cerevisiae mutants unable to carry out plasmid-to-chromosome gene conversion. For this purpose, we have developed a colony color assay in which recombination is induced by the controlled delivery of double-strand breaks (DSBs). Recombination occurs between a chromosomal mutant ade2 allele and a second plasmid-borne ade2 allele where DSBs are introduced via the site-specific HO endonuclease. Besides isolating a number of new alleles in known rad genes, we identified a novel allele of the RFA1 gene, rfa1-44, which encodes the large subunit of the heterotrimeric yeast single-stranded DNA-binding protein RPA. Characterization of rfa1-44 revealed that it is, like members of the RAD52 epistasis group, sensitive to X rays, high doses of UV, and HO-induced DSBs. In addition, rfa1-44 shows a reduced ability to undergo sporulation and HO-induced gene conversion. The mutation was mapped to a single-base substitution resulting in an aspartate at amino acid residue 77 instead of glycine. Moreover, all radiation sensitivities and repair defects of rfa1-44 are suppressed by RAD52 in a dose-dependent manner, and one RAD52 mutant allele, rad52-34, displays nonallelic noncomplementation when crossed with rfa1-44. Presented is a model accounting for this genetic interaction in which Rfa1, in a complex with Rad52, serves to assemble other proteins of the recombination-repair machinery at the site of DSBs and other kinds of DNA damage. We believe that our findings and those of J. Smith and R. Rothstein (Mol. Cell. Biol. 15:1632-1641, 1995) are the first in vivo demonstrations of the involvement of a eukaryotic single-stranded binding protein in recombination and repair processes.

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Selected References

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  1. Adachi Y., Laemmli U. K. Identification of nuclear pre-replication centers poised for DNA synthesis in Xenopus egg extracts: immunolocalization study of replication protein A. J Cell Biol. 1992 Oct;119(1):1–15. doi: 10.1083/jcb.119.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alani E., Padmore R., Kleckner N. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell. 1990 May 4;61(3):419–436. doi: 10.1016/0092-8674(90)90524-i. [DOI] [PubMed] [Google Scholar]
  3. Bates H., Bridges B. A., Woodgate R. Mutagenic DNA repair in Escherichia coli, XX. Overproduction of UmuD' protein results in suppression of the umuC36 mutation in excision defective bacteria. Mutat Res. 1991 Sep-Oct;250(1-2):199–204. doi: 10.1016/0027-5107(91)90176-o. [DOI] [PubMed] [Google Scholar]
  4. Becker D. M., Guarente L. High-efficiency transformation of yeast by electroporation. Methods Enzymol. 1991;194:182–187. doi: 10.1016/0076-6879(91)94015-5. [DOI] [PubMed] [Google Scholar]
  5. Bennett C. B., Lewis A. L., Baldwin K. K., Resnick M. A. Lethality induced by a single site-specific double-strand break in a dispensable yeast plasmid. Proc Natl Acad Sci U S A. 1993 Jun 15;90(12):5613–5617. doi: 10.1073/pnas.90.12.5613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Bootsma D., Hoeijmakers J. H. DNA repair. Engagement with transcription. Nature. 1993 May 13;363(6425):114–115. doi: 10.1038/363114a0. [DOI] [PubMed] [Google Scholar]
  7. Boundy-Mills K. L., Livingston D. M. A Saccharomyces cerevisiae RAD52 allele expressing a C-terminal truncation protein: activities and intragenic complementation of missense mutations. Genetics. 1993 Jan;133(1):39–49. doi: 10.1093/genetics/133.1.39. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brill S. J., DiNardo S., Voelkel-Meiman K., Sternglanz R. Need for DNA topoisomerase activity as a swivel for DNA replication for transcription of ribosomal RNA. 1987 Mar 26-Apr 1Nature. 326(6111):414–416. doi: 10.1038/326414a0. [DOI] [PubMed] [Google Scholar]
  9. Brill S. J., Stillman B. Replication factor-A from Saccharomyces cerevisiae is encoded by three essential genes coordinately expressed at S phase. Genes Dev. 1991 Sep;5(9):1589–1600. doi: 10.1101/gad.5.9.1589. [DOI] [PubMed] [Google Scholar]
  10. Brill S. J., Stillman B. Yeast replication factor-A functions in the unwinding of the SV40 origin of DNA replication. Nature. 1989 Nov 2;342(6245):92–95. doi: 10.1038/342092a0. [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. Clugston C. K., McLaughlin K., Kenny M. K., Brown R. Binding of human single-stranded DNA binding protein to DNA damaged by the anticancer drug cis-diamminedichloroplatinum (II). Cancer Res. 1992 Nov 15;52(22):6375–6379. [PubMed] [Google Scholar]
  13. Connolly B., White C. I., Haber J. E. Physical monitoring of mating type switching in Saccharomyces cerevisiae. Mol Cell Biol. 1988 Jun;8(6):2342–2349. doi: 10.1128/mcb.8.6.2342. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Coverley D., Kenny M. K., Lane D. P., Wood R. D. A role for the human single-stranded DNA binding protein HSSB/RPA in an early stage of nucleotide excision repair. Nucleic Acids Res. 1992 Aug 11;20(15):3873–3880. doi: 10.1093/nar/20.15.3873. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Coverley D., Kenny M. K., Munn M., Rupp W. D., Lane D. P., Wood R. D. Requirement for the replication protein SSB in human DNA excision repair. Nature. 1991 Feb 7;349(6309):538–541. doi: 10.1038/349538a0. [DOI] [PubMed] [Google Scholar]
  16. Cox M. M., Lehman I. R. Enzymes of general recombination. Annu Rev Biochem. 1987;56:229–262. doi: 10.1146/annurev.bi.56.070187.001305. [DOI] [PubMed] [Google Scholar]
  17. Dornreiter I., Erdile L. F., Gilbert I. U., von Winkler D., Kelly T. J., Fanning E. Interaction of DNA polymerase alpha-primase with cellular replication protein A and SV40 T antigen. EMBO J. 1992 Feb;11(2):769–776. doi: 10.1002/j.1460-2075.1992.tb05110.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Elledge S. J., Davis R. W. A family of versatile centromeric vectors designed for use in the sectoring-shuffle mutagenesis assay in Saccharomyces cerevisiae. Gene. 1988 Oct 30;70(2):303–312. doi: 10.1016/0378-1119(88)90202-8. [DOI] [PubMed] [Google Scholar]
  19. Elledge S. J., Mulligan J. T., Ramer S. W., Spottswood M., Davis R. W. Lambda YES: a multifunctional cDNA expression vector for the isolation of genes by complementation of yeast and Escherichia coli mutations. Proc Natl Acad Sci U S A. 1991 Mar 1;88(5):1731–1735. doi: 10.1073/pnas.88.5.1731. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Erdile L. F., Collins K. L., Russo A., Simancek P., Small D., Umbricht C., Virshup D., Cheng L., Randall S., Weinberg D. Initiation of SV40 DNA replication: mechanism and control. Cold Spring Harb Symp Quant Biol. 1991;56:303–313. doi: 10.1101/sqb.1991.056.01.037. [DOI] [PubMed] [Google Scholar]
  21. Erdile L. F., Heyer W. D., Kolodner R., Kelly T. J. Characterization of a cDNA encoding the 70-kDa single-stranded DNA-binding subunit of human replication protein A and the role of the protein in DNA replication. J Biol Chem. 1991 Jun 25;266(18):12090–12098. [PubMed] [Google Scholar]
  22. Feaver W. J., Svejstrup J. Q., Bardwell L., Bardwell A. J., Buratowski S., Gulyas K. D., Donahue T. F., Friedberg E. C., Kornberg R. D. Dual roles of a multiprotein complex from S. cerevisiae in transcription and DNA repair. Cell. 1993 Dec 31;75(7):1379–1387. doi: 10.1016/0092-8674(93)90624-y. [DOI] [PubMed] [Google Scholar]
  23. Firmenich A. A., Redding K. An efficient procedure for multiple transformations of yeast in parallel. Biotechniques. 1993 May;14(5):712-4, 716-8. [PubMed] [Google Scholar]
  24. Friedberg E. C. Deoxyribonucleic acid repair in the yeast Saccharomyces cerevisiae. Microbiol Rev. 1988 Mar;52(1):70–102. doi: 10.1128/mr.52.1.70-102.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. 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]
  26. Gietz R. D., Sugino A. New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene. 1988 Dec 30;74(2):527–534. doi: 10.1016/0378-1119(88)90185-0. [DOI] [PubMed] [Google Scholar]
  27. Guzder S. N., Qiu H., Sommers C. H., Sung P., Prakash L., Prakash S. DNA repair gene RAD3 of S. cerevisiae is essential for transcription by RNA polymerase II. Nature. 1994 Jan 6;367(6458):91–94. doi: 10.1038/367091a0. [DOI] [PubMed] [Google Scholar]
  28. Haber J. E., Borts R. H., Connolly B., Lichten M., Rudin N., White C. I. Physical monitoring of meiotic and mitotic recombination in yeast. Prog Nucleic Acid Res Mol Biol. 1988;35:209–259. [PubMed] [Google Scholar]
  29. Heyer W. D., Rao M. R., Erdile L. F., Kelly T. J., Kolodner R. D. An essential Saccharomyces cerevisiae single-stranded DNA binding protein is homologous to the large subunit of human RP-A. EMBO J. 1990 Jul;9(7):2321–2329. doi: 10.1002/j.1460-2075.1990.tb07404.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Hynes R. O. Integrins: a family of cell surface receptors. Cell. 1987 Feb 27;48(4):549–554. doi: 10.1016/0092-8674(87)90233-9. [DOI] [PubMed] [Google Scholar]
  31. Hynes R. O. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 1992 Apr 3;69(1):11–25. doi: 10.1016/0092-8674(92)90115-s. [DOI] [PubMed] [Google Scholar]
  32. Jacks T., Remington L., Williams B. O., Schmitt E. M., Halachmi S., Bronson R. T., Weinberg R. A. Tumor spectrum analysis in p53-mutant mice. Curr Biol. 1994 Jan 1;4(1):1–7. doi: 10.1016/s0960-9822(00)00002-6. [DOI] [PubMed] [Google Scholar]
  33. Jensen R. E., Herskowitz I. Directionality and regulation of cassette substitution in yeast. Cold Spring Harb Symp Quant Biol. 1984;49:97–104. doi: 10.1101/sqb.1984.049.01.013. [DOI] [PubMed] [Google Scholar]
  34. Jessberger R., Podust V., Hübscher U., Berg P. A mammalian protein complex that repairs double-strand breaks and deletions by recombination. J Biol Chem. 1993 Jul 15;268(20):15070–15079. [PubMed] [Google Scholar]
  35. Kenny M. K., Schlegel U., Furneaux H., Hurwitz J. The role of human single-stranded DNA binding protein and its individual subunits in simian virus 40 DNA replication. J Biol Chem. 1990 May 5;265(13):7693–7700. [PubMed] [Google Scholar]
  36. Kim C., Snyder R. O., Wold M. S. Binding properties of replication protein A from human and yeast cells. Mol Cell Biol. 1992 Jul;12(7):3050–3059. doi: 10.1128/mcb.12.7.3050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Kolodkin A. L., Klar A. J., Stahl F. W. Double-strand breaks can initiate meiotic recombination in S. cerevisiae. Cell. 1986 Aug 29;46(5):733–740. doi: 10.1016/0092-8674(86)90349-1. [DOI] [PubMed] [Google Scholar]
  38. Kornberg A. Control of initiation of the Escherichia coli chromosome. Cold Spring Harb Symp Quant Biol. 1991;56:275–278. doi: 10.1101/sqb.1991.056.01.033. [DOI] [PubMed] [Google Scholar]
  39. Kowalczykowski S. C. Biochemistry of genetic recombination: energetics and mechanism of DNA strand exchange. Annu Rev Biophys Biophys Chem. 1991;20:539–575. doi: 10.1146/annurev.bb.20.060191.002543. [DOI] [PubMed] [Google Scholar]
  40. Kowalczykowski S. C., Dixon D. A., Eggleston A. K., Lauder S. D., Rehrauer W. M. Biochemistry of homologous recombination in Escherichia coli. Microbiol Rev. 1994 Sep;58(3):401–465. doi: 10.1128/mr.58.3.401-465.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Kunz B. A., Haynes R. H. Phenomenology and genetic control of mitotic recombination in yeast. Annu Rev Genet. 1981;15:57–89. doi: 10.1146/annurev.ge.15.120181.000421. [DOI] [PubMed] [Google Scholar]
  42. Lawrence C. W. Classical mutagenesis techniques. Methods Enzymol. 1991;194:273–281. doi: 10.1016/0076-6879(91)94021-4. [DOI] [PubMed] [Google Scholar]
  43. Lee S. H., Hurwitz J. Mechanism of elongation of primed DNA by DNA polymerase delta, proliferating cell nuclear antigen, and activator 1. Proc Natl Acad Sci U S A. 1990 Aug;87(15):5672–5676. doi: 10.1073/pnas.87.15.5672. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Longhese M. P., Plevani P., Lucchini G. Replication factor A is required in vivo for DNA replication, repair, and recombination. Mol Cell Biol. 1994 Dec;14(12):7884–7890. doi: 10.1128/mcb.14.12.7884. [DOI] [PMC free article] [PubMed] [Google Scholar]
  45. Meyer R. R., Laine P. S. The single-stranded DNA-binding protein of Escherichia coli. Microbiol Rev. 1990 Dec;54(4):342–380. doi: 10.1128/mr.54.4.342-380.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  46. Milne G. T., Weaver D. T. Dominant negative alleles of RAD52 reveal a DNA repair/recombination complex including Rad51 and Rad52. Genes Dev. 1993 Sep;7(9):1755–1765. doi: 10.1101/gad.7.9.1755. [DOI] [PubMed] [Google Scholar]
  47. Modrich P. Mechanisms and biological effects of mismatch repair. Annu Rev Genet. 1991;25:229–253. doi: 10.1146/annurev.ge.25.120191.001305. [DOI] [PubMed] [Google Scholar]
  48. Mosig G. Bacteriophage T4 gene 32 participates in excision repair as well as recombinational repair of UV damages. Genetics. 1985 Jun;110(2):159–171. doi: 10.1093/genetics/110.2.159. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. Mosig G. The essential role of recombination in phage T4 growth. Annu Rev Genet. 1987;21:347–371. doi: 10.1146/annurev.ge.21.120187.002023. [DOI] [PubMed] [Google Scholar]
  50. Mémet S., Saurin W., Sentenac A. RNA polymerases B and C are more closely related to each other than to RNA polymerase A. J Biol Chem. 1988 Jul 25;263(21):10048–10051. [PubMed] [Google Scholar]
  51. Nakai S., Matsumoto S. Two types of radiation-sensitive mutant in yeast. Mutat Res. 1967 Mar-Apr;4(2):129–136. doi: 10.1016/0027-5107(67)90064-4. [DOI] [PubMed] [Google Scholar]
  52. Nash H. A. Bending and supercoiling of DNA at the attachment site of bacteriophage lambda. Trends Biochem Sci. 1990 Jun;15(6):222–227. doi: 10.1016/0968-0004(90)90034-9. [DOI] [PubMed] [Google Scholar]
  53. Nickoloff J. A., Chen E. Y., Heffron F. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc Natl Acad Sci U S A. 1986 Oct;83(20):7831–7835. doi: 10.1073/pnas.83.20.7831. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Nickoloff J. A., Singer J. D., Hoekstra M. F., Heffron F. Double-strand breaks stimulate alternative mechanisms of recombination repair. J Mol Biol. 1989 Jun 5;207(3):527–541. doi: 10.1016/0022-2836(89)90462-2. [DOI] [PubMed] [Google Scholar]
  55. 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]
  56. Padmore R., Cao L., Kleckner N. Temporal comparison of recombination and synaptonemal complex formation during meiosis in S. cerevisiae. Cell. 1991 Sep 20;66(6):1239–1256. doi: 10.1016/0092-8674(91)90046-2. [DOI] [PubMed] [Google Scholar]
  57. Pugh B. F., Tjian R. Diverse transcriptional functions of the multisubunit eukaryotic TFIID complex. J Biol Chem. 1992 Jan 15;267(2):679–682. [PubMed] [Google Scholar]
  58. Qiu H., Park E., Prakash L., Prakash S. The Saccharomyces cerevisiae DNA repair gene RAD25 is required for transcription by RNA polymerase II. Genes Dev. 1993 Nov;7(11):2161–2171. doi: 10.1101/gad.7.11.2161. [DOI] [PubMed] [Google Scholar]
  59. Resnick M. A. Genetic control of radiation sensitivity in Saccharomyces cerevisiae. Genetics. 1969 Jul;62(3):519–531. doi: 10.1093/genetics/62.3.519. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Resnick M. A., Martin P. The repair of double-strand breaks in the nuclear DNA of Saccharomyces cerevisiae and its genetic control. Mol Gen Genet. 1976 Jan 16;143(2):119–129. doi: 10.1007/BF00266917. [DOI] [PubMed] [Google Scholar]
  61. Resnick M. A. The repair of double-strand breaks in DNA; a model involving recombination. J Theor Biol. 1976 Jun;59(1):97–106. doi: 10.1016/s0022-5193(76)80025-2. [DOI] [PubMed] [Google Scholar]
  62. Roeder R. G. The complexities of eukaryotic transcription initiation: regulation of preinitiation complex assembly. Trends Biochem Sci. 1991 Nov;16(11):402–408. doi: 10.1016/0968-0004(91)90164-q. [DOI] [PubMed] [Google Scholar]
  63. Rothstein R. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 1991;194:281–301. doi: 10.1016/0076-6879(91)94022-5. [DOI] [PubMed] [Google Scholar]
  64. Rudin N., Haber J. E. Efficient repair of HO-induced chromosomal breaks in Saccharomyces cerevisiae by recombination between flanking homologous sequences. Mol Cell Biol. 1988 Sep;8(9):3918–3928. doi: 10.1128/mcb.8.9.3918. [DOI] [PMC free article] [PubMed] [Google Scholar]
  65. Schaeffer L., Roy R., Humbert S., Moncollin V., Vermeulen W., Hoeijmakers J. H., Chambon P., Egly J. M. DNA repair helicase: a component of BTF2 (TFIIH) basic transcription factor. Science. 1993 Apr 2;260(5104):58–63. doi: 10.1126/science.8465201. [DOI] [PubMed] [Google Scholar]
  66. Schiestl R. H., Gietz R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr Genet. 1989 Dec;16(5-6):339–346. doi: 10.1007/BF00340712. [DOI] [PubMed] [Google Scholar]
  67. Selby C. P., Sancar A. Structure and function of the (A)BC excinuclease of Escherichia coli. Mutat Res. 1990 Sep-Nov;236(2-3):203–211. doi: 10.1016/0921-8777(90)90005-p. [DOI] [PubMed] [Google Scholar]
  68. Sherman F. Getting started with yeast. Methods Enzymol. 1991;194:3–21. doi: 10.1016/0076-6879(91)94004-v. [DOI] [PubMed] [Google Scholar]
  69. Sherman F., Hicks J. Micromanipulation and dissection of asci. Methods Enzymol. 1991;194:21–37. doi: 10.1016/0076-6879(91)94005-w. [DOI] [PubMed] [Google Scholar]
  70. 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]
  71. Sikorski R. S., Hieter P. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics. 1989 May;122(1):19–27. doi: 10.1093/genetics/122.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Smith J., Rothstein R. A mutation in the gene encoding the Saccharomyces cerevisiae single-stranded DNA-binding protein Rfa1 stimulates a RAD52-independent pathway for direct-repeat recombination. Mol Cell Biol. 1995 Mar;15(3):1632–1641. doi: 10.1128/mcb.15.3.1632. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Stigger E., Dean F. B., Hurwitz J., Lee S. H. Reconstitution of functional human single-stranded DNA-binding protein from individual subunits expressed by recombinant baculoviruses. Proc Natl Acad Sci U S A. 1994 Jan 18;91(2):579–583. doi: 10.1073/pnas.91.2.579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Sugawara N., Haber J. E. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol Cell Biol. 1992 Feb;12(2):563–575. doi: 10.1128/mcb.12.2.563. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. 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]
  76. Sun H., Treco D., Szostak J. W. Extensive 3'-overhanging, single-stranded DNA associated with the meiosis-specific double-strand breaks at the ARG4 recombination initiation site. Cell. 1991 Mar 22;64(6):1155–1161. doi: 10.1016/0092-8674(91)90270-9. [DOI] [PubMed] [Google Scholar]
  77. Szostak J. W., Orr-Weaver T. L., Rothstein R. J., Stahl F. W. The double-strand-break repair model for recombination. Cell. 1983 May;33(1):25–35. doi: 10.1016/0092-8674(83)90331-8. [DOI] [PubMed] [Google Scholar]
  78. Tsurimoto T., Stillman B. Multiple replication factors augment DNA synthesis by the two eukaryotic DNA polymerases, alpha and delta. EMBO J. 1989 Dec 1;8(12):3883–3889. doi: 10.1002/j.1460-2075.1989.tb08567.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  79. Van Houten B., Snowden A. Mechanism of action of the Escherichia coli UvrABC nuclease: clues to the damage recognition problem. Bioessays. 1993 Jan;15(1):51–59. doi: 10.1002/bies.950150108. [DOI] [PubMed] [Google Scholar]
  80. Wang Z., Svejstrup J. Q., Feaver W. J., Wu X., Kornberg R. D., Friedberg E. C. Transcription factor b (TFIIH) is required during nucleotide-excision repair in yeast. Nature. 1994 Mar 3;368(6466):74–76. doi: 10.1038/368074a0. [DOI] [PubMed] [Google Scholar]
  81. Wold M. S., Weinberg D. H., Virshup D. M., Li J. J., Kelly T. J. Identification of cellular proteins required for simian virus 40 DNA replication. J Biol Chem. 1989 Feb 15;264(5):2801–2809. [PubMed] [Google Scholar]
  82. Zawel L., Reinberg D. Advances in RNA polymerase II transcription. Curr Opin Cell Biol. 1992 Jun;4(3):488–495. doi: 10.1016/0955-0674(92)90016-6. [DOI] [PubMed] [Google Scholar]

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