Skip to main content
Genetics logoLink to Genetics
. 2002 Jan;160(1):49–62. doi: 10.1093/genetics/160.1.49

Differential suppression of DNA repair deficiencies of Yeast rad50, mre11 and xrs2 mutants by EXO1 and TLC1 (the RNA component of telomerase).

L Kevin Lewis 1, G Karthikeyan 1, James W Westmoreland 1, Michael A Resnick 1
PMCID: PMC1461956  PMID: 11805044

Abstract

Rad50, Mre11, and Xrs2 form a nuclease complex that functions in both nonhomologous end-joining (NHEJ) and recombinational repair of DNA double-strand breaks (DSBs). A search for highly expressed cDNAs that suppress the DNA repair deficiency of rad50 mutants yielded multiple isolates of two genes: EXO1 and TLC1. Overexpression of EXO1 or TLC1 increased the resistance of rad50, mre11, and xrs2 mutants to ionizing radiation and MMS, but did not increase resistance in strains defective in recombination (rad51, rad52, rad54, rad59) or NHEJ only (yku70, sir4). Increased Exo1 or TLC1 RNA did not alter checkpoint responses or restore NHEJ proficiency, but DNA repair defects of yku70 and rad27 (fen) mutants were differentially suppressed by the two genes. Overexpression of Exo1, but not mutant proteins containing substitutions in the conserved nuclease domain, increased recombination and suppressed HO and EcoRI endonuclease-induced killing of rad50 strains. exo1 rad50 mutants lacking both nuclease activities exhibited a high proportion of enlarged, G2-arrested cells and displayed a synergistic decrease in DSB-induced plasmid:chromosome recombination. These results support a model in which the nuclease activity of the Rad50/Mre11/Xrs2 complex is required for recombinational repair, but not NHEJ. We suggest that the 5'-3' exo activity of Exo1 is able to substitute for Rad50/Mre11/Xrs2 in rescission of specific classes of DSB end structures. Gene-specific suppression by TLC1, which encodes the RNA subunit of the yeast telomerase complex, demonstrates that components of telomerase can also impact on DSB repair pathways.

Full Text

The Full Text of this article is available as a PDF (324.8 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adams A. K., Holm C. Specific DNA replication mutations affect telomere length in Saccharomyces cerevisiae. Mol Cell Biol. 1996 Sep;16(9):4614–4620. doi: 10.1128/mcb.16.9.4614. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Aguilera A. Genetic evidence for different RAD52-dependent intrachromosomal recombination pathways in Saccharomyces cerevisiae. Curr Genet. 1995 Mar;27(4):298–305. doi: 10.1007/BF00352096. [DOI] [PubMed] [Google Scholar]
  3. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997 Sep 1;25(17):3389–3402. doi: 10.1093/nar/25.17.3389. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Aström S. U., Okamura S. M., Rine J. Yeast cell-type regulation of DNA repair. Nature. 1999 Jan 28;397(6717):310–310. doi: 10.1038/16833. [DOI] [PubMed] [Google Scholar]
  5. Bai Y., Symington L. S. A Rad52 homolog is required for RAD51-independent mitotic recombination in Saccharomyces cerevisiae. Genes Dev. 1996 Aug 15;10(16):2025–2037. doi: 10.1101/gad.10.16.2025. [DOI] [PubMed] [Google Scholar]
  6. Barnes G., Rio D. DNA double-strand-break sensitivity, DNA replication, and cell cycle arrest phenotypes of Ku-deficient Saccharomyces cerevisiae. Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):867–872. doi: 10.1073/pnas.94.3.867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Baumann P., West S. C. DNA end-joining catalyzed by human cell-free extracts. Proc Natl Acad Sci U S A. 1998 Nov 24;95(24):14066–14070. doi: 10.1073/pnas.95.24.14066. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. 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]
  9. Boulton S. J., Jackson S. P. Components of the Ku-dependent non-homologous end-joining pathway are involved in telomeric length maintenance and telomeric silencing. EMBO J. 1998 Mar 16;17(6):1819–1828. doi: 10.1093/emboj/17.6.1819. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Bressan D. A., Baxter B. K., Petrini J. H. The Mre11-Rad50-Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Nov;19(11):7681–7687. doi: 10.1128/mcb.19.11.7681. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Bressan D. A., Olivares H. A., Nelms B. E., Petrini J. H. Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics. 1998 Oct;150(2):591–600. doi: 10.1093/genetics/150.2.591. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Chamankhah M., Fontanie T., Xiao W. The Saccharomyces cerevisiae mre11(ts) allele confers a separation of DNA repair and telomere maintenance functions. Genetics. 2000 Jun;155(2):569–576. doi: 10.1093/genetics/155.2.569. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chapon C., Cech T. R., Zaug A. J. Polyadenylation of telomerase RNA in budding yeast. RNA. 1997 Nov;3(11):1337–1351. [PMC free article] [PubMed] [Google Scholar]
  14. Chen C., Kolodner R. D. Gross chromosomal rearrangements in Saccharomyces cerevisiae replication and recombination defective mutants. Nat Genet. 1999 Sep;23(1):81–85. doi: 10.1038/12687. [DOI] [PubMed] [Google Scholar]
  15. 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]
  16. Critchlow S. E., Jackson S. P. DNA end-joining: from yeast to man. Trends Biochem Sci. 1998 Oct;23(10):394–398. doi: 10.1016/s0968-0004(98)01284-5. [DOI] [PubMed] [Google Scholar]
  17. Elias-Arnanz M., Firmenich A. A., Berg P. Saccharomyces cerevisiae mutants defective in plasmid-chromosome recombination. Mol Gen Genet. 1996 Oct 16;252(5):530–538. doi: 10.1007/BF02172399. [DOI] [PubMed] [Google Scholar]
  18. Feldmann H., Winnacker E. L. A putative homologue of the human autoantigen Ku from Saccharomyces cerevisiae. J Biol Chem. 1993 Jun 15;268(17):12895–12900. [PubMed] [Google Scholar]
  19. Fiorentini P., Huang K. N., Tishkoff D. X., Kolodner R. D., Symington L. S. Exonuclease I of Saccharomyces cerevisiae functions in mitotic recombination in vivo and in vitro. Mol Cell Biol. 1997 May;17(5):2764–2773. doi: 10.1128/mcb.17.5.2764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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]
  21. Galy V., Olivo-Marin J. C., Scherthan H., Doye V., Rascalou N., Nehrbass U. Nuclear pore complexes in the organization of silent telomeric chromatin. Nature. 2000 Jan 6;403(6765):108–112. doi: 10.1038/47528. [DOI] [PubMed] [Google Scholar]
  22. Gary R., Park M. S., Nolan J. P., Cornelius H. L., Kozyreva O. G., Tran H. T., Lobachev K. S., Resnick M. A., Gordenin D. A. A novel role in DNA metabolism for the binding of Fen1/Rad27 to PCNA and implications for genetic risk. Mol Cell Biol. 1999 Aug;19(8):5373–5382. doi: 10.1128/mcb.19.8.5373. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gietz R. D., Schiestl R. H., Willems A. R., Woods R. A. Studies on the transformation of intact yeast cells by the LiAc/SS-DNA/PEG procedure. Yeast. 1995 Apr 15;11(4):355–360. doi: 10.1002/yea.320110408. [DOI] [PubMed] [Google Scholar]
  24. Goldstein A. L., McCusker J. H. Three new dominant drug resistance cassettes for gene disruption in Saccharomyces cerevisiae. Yeast. 1999 Oct;15(14):1541–1553. doi: 10.1002/(SICI)1097-0061(199910)15:14<1541::AID-YEA476>3.0.CO;2-K. [DOI] [PubMed] [Google Scholar]
  25. Gotta M., Laroche T., Formenton A., Maillet L., Scherthan H., Gasser S. M. The clustering of telomeres and colocalization with Rap1, Sir3, and Sir4 proteins in wild-type Saccharomyces cerevisiae. J Cell Biol. 1996 Sep;134(6):1349–1363. doi: 10.1083/jcb.134.6.1349. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Griffith J. D., Comeau L., Rosenfield S., Stansel R. M., Bianchi A., Moss H., de Lange T. Mammalian telomeres end in a large duplex loop. Cell. 1999 May 14;97(4):503–514. doi: 10.1016/s0092-8674(00)80760-6. [DOI] [PubMed] [Google Scholar]
  27. Hopfner K. P., Karcher A., Shin D. S., Craig L., Arthur L. M., Carney J. P., Tainer J. A. Structural biology of Rad50 ATPase: ATP-driven conformational control in DNA double-strand break repair and the ABC-ATPase superfamily. Cell. 2000 Jun 23;101(7):789–800. doi: 10.1016/s0092-8674(00)80890-9. [DOI] [PubMed] [Google Scholar]
  28. Hovland P., Flick J., Johnston M., Sclafani R. A. Galactose as a gratuitous inducer of GAL gene expression in yeasts growing on glucose. Gene. 1989 Nov 15;83(1):57–64. doi: 10.1016/0378-1119(89)90403-4. [DOI] [PubMed] [Google Scholar]
  29. Imai S., Armstrong C. M., Kaeberlein M., Guarente L. Transcriptional silencing and longevity protein Sir2 is an NAD-dependent histone deacetylase. Nature. 2000 Feb 17;403(6771):795–800. doi: 10.1038/35001622. [DOI] [PubMed] [Google Scholar]
  30. Ivanov E. L., Sugawara N., White C. I., Fabre F., Haber J. E. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol Cell Biol. 1994 May;14(5):3414–3425. doi: 10.1128/mcb.14.5.3414. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Kouprina N., Nikolaishvili N., Graves J., Koriabine M., Resnick M. A., Larionov V. Integrity of human YACs during propagation in recombination-deficient yeast strains. Genomics. 1999 Mar 15;56(3):262–273. doi: 10.1006/geno.1998.5727. [DOI] [PubMed] [Google Scholar]
  32. Kramer K. M., Haber J. E. New telomeres in yeast are initiated with a highly selected subset of TG1-3 repeats. Genes Dev. 1993 Dec;7(12A):2345–2356. doi: 10.1101/gad.7.12a.2345. [DOI] [PubMed] [Google Scholar]
  33. Landry J., Sutton A., Tafrov S. T., Heller R. C., Stebbins J., Pillus L., Sternglanz R. The silencing protein SIR2 and its homologs are NAD-dependent protein deacetylases. Proc Natl Acad Sci U S A. 2000 May 23;97(11):5807–5811. doi: 10.1073/pnas.110148297. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Larionov V., Kouprina N., Nikolaishvili N., Resnick M. A. Recombination during transformation as a source of chimeric mammalian artificial chromosomes in yeast (YACs). Nucleic Acids Res. 1994 Oct 11;22(20):4154–4162. doi: 10.1093/nar/22.20.4154. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Le S., Moore J. K., Haber J. E., Greider C. W. RAD50 and RAD51 define two pathways that collaborate to maintain telomeres in the absence of telomerase. Genetics. 1999 May;152(1):143–152. doi: 10.1093/genetics/152.1.143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Lee S. E., Moore J. K., Holmes A., Umezu K., Kolodner R. D., Haber J. E. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell. 1998 Aug 7;94(3):399–409. doi: 10.1016/s0092-8674(00)81482-8. [DOI] [PubMed] [Google Scholar]
  37. Lewis L. K., Kirchner J. M., Resnick M. A. Requirement for end-joining and checkpoint functions, but not RAD52-mediated recombination, after EcoRI endonuclease cleavage of Saccharomyces cerevisiae DNA. Mol Cell Biol. 1998 Apr;18(4):1891–1902. doi: 10.1128/mcb.18.4.1891. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Lewis L. K., Resnick M. A. Tying up loose ends: nonhomologous end-joining in Saccharomyces cerevisiae. Mutat Res. 2000 Jun 30;451(1-2):71–89. doi: 10.1016/s0027-5107(00)00041-5. [DOI] [PubMed] [Google Scholar]
  39. Lewis L. K., Westmoreland J. W., Resnick M. A. Repair of endonuclease-induced double-strand breaks in Saccharomyces cerevisiae: essential role for genes associated with nonhomologous end-joining. Genetics. 1999 Aug;152(4):1513–1529. doi: 10.1093/genetics/152.4.1513. [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Liang F., Han M., Romanienko P. J., Jasin M. Homology-directed repair is a major double-strand break repair pathway in mammalian cells. Proc Natl Acad Sci U S A. 1998 Apr 28;95(9):5172–5177. doi: 10.1073/pnas.95.9.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Liu H., Krizek J., Bretscher A. Construction of a GAL1-regulated yeast cDNA expression library and its application to the identification of genes whose overexpression causes lethality in yeast. Genetics. 1992 Nov;132(3):665–673. doi: 10.1093/genetics/132.3.665. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Lowell J. E., Pillus L. Telomere tales: chromatin, telomerase and telomere function in Saccharomyces cerevisiae. Cell Mol Life Sci. 1998 Jan;54(1):32–49. doi: 10.1007/s000180050123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. Lue N. F. Sequence-specific and conformation-dependent binding of yeast telomerase RNA to single-stranded telomeric DNA. Nucleic Acids Res. 1999 Jun 15;27(12):2560–2567. doi: 10.1093/nar/27.12.2560. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Lustig A. J. Mechanisms of silencing in Saccharomyces cerevisiae. Curr Opin Genet Dev. 1998 Apr;8(2):233–239. doi: 10.1016/s0959-437x(98)80146-9. [DOI] [PubMed] [Google Scholar]
  45. Martin S. G., Laroche T., Suka N., Grunstein M., Gasser S. M. Relocalization of telomeric Ku and SIR proteins in response to DNA strand breaks in yeast. Cell. 1999 May 28;97(5):621–633. doi: 10.1016/s0092-8674(00)80773-4. [DOI] [PubMed] [Google Scholar]
  46. Mills K. D., Sinclair D. A., Guarente L. MEC1-dependent redistribution of the Sir3 silencing protein from telomeres to DNA double-strand breaks. Cell. 1999 May 28;97(5):609–620. doi: 10.1016/s0092-8674(00)80772-2. [DOI] [PubMed] [Google Scholar]
  47. Moore J. K., Haber J. E. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol Cell Biol. 1996 May;16(5):2164–2173. doi: 10.1128/mcb.16.5.2164. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. 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]
  49. 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]
  50. Osman F., Subramani S. Double-strand break-induced recombination in eukaryotes. Prog Nucleic Acid Res Mol Biol. 1998;58:263–299. doi: 10.1016/s0079-6603(08)60039-2. [DOI] [PubMed] [Google Scholar]
  51. Palladino F., Laroche T., Gilson E., Axelrod A., Pillus L., Gasser S. M. SIR3 and SIR4 proteins are required for the positioning and integrity of yeast telomeres. Cell. 1993 Nov 5;75(3):543–555. doi: 10.1016/0092-8674(93)90388-7. [DOI] [PubMed] [Google Scholar]
  52. Pang D., Yoo S., Dynan W. S., Jung M., Dritschilo A. Ku proteins join DNA fragments as shown by atomic force microscopy. Cancer Res. 1997 Apr 15;57(8):1412–1415. [PubMed] [Google Scholar]
  53. Parenteau J., Wellinger R. J. Accumulation of single-stranded DNA and destabilization of telomeric repeats in yeast mutant strains carrying a deletion of RAD27. Mol Cell Biol. 1999 Jun;19(6):4143–4152. doi: 10.1128/mcb.19.6.4143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Park P. U., Defossez P. A., Guarente L. Effects of mutations in DNA repair genes on formation of ribosomal DNA circles and life span in Saccharomyces cerevisiae. Mol Cell Biol. 1999 May;19(5):3848–3856. doi: 10.1128/mcb.19.5.3848. [DOI] [PMC free article] [PubMed] [Google Scholar]
  55. Paull T. T., Gellert M. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 1999 May 15;13(10):1276–1288. doi: 10.1101/gad.13.10.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
  56. Petrini J. H. The mammalian Mre11-Rad50-nbs1 protein complex: integration of functions in the cellular DNA-damage response. Am J Hum Genet. 1999 May;64(5):1264–1269. doi: 10.1086/302391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Porter S. E., Greenwell P. W., Ritchie K. B., Petes T. D. The DNA-binding protein Hdf1p (a putative Ku homologue) is required for maintaining normal telomere length in Saccharomyces cerevisiae. Nucleic Acids Res. 1996 Feb 15;24(4):582–585. doi: 10.1093/nar/24.4.582. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Prescott J., Blackburn E. H. Telomerase RNA mutations in Saccharomyces cerevisiae alter telomerase action and reveal nonprocessivity in vivo and in vitro. Genes Dev. 1997 Feb 15;11(4):528–540. doi: 10.1101/gad.11.4.528. [DOI] [PubMed] [Google Scholar]
  59. 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]
  60. 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]
  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. Schulz V. P., Zakian V. A. The saccharomyces PIF1 DNA helicase inhibits telomere elongation and de novo telomere formation. Cell. 1994 Jan 14;76(1):145–155. doi: 10.1016/0092-8674(94)90179-1. [DOI] [PubMed] [Google Scholar]
  63. 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]
  64. 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]
  65. Singer M. S., Gottschling D. E. TLC1: template RNA component of Saccharomyces cerevisiae telomerase. Science. 1994 Oct 21;266(5184):404–409. doi: 10.1126/science.7545955. [DOI] [PubMed] [Google Scholar]
  66. Singer M. S., Kahana A., Wolf A. J., Meisinger L. L., Peterson S. E., Goggin C., Mahowald M., Gottschling D. E. Identification of high-copy disruptors of telomeric silencing in Saccharomyces cerevisiae. Genetics. 1998 Oct;150(2):613–632. doi: 10.1093/genetics/150.2.613. [DOI] [PMC free article] [PubMed] [Google Scholar]
  67. Sokolsky T., Alani E. EXO1 and MSH6 are high-copy suppressors of conditional mutations in the MSH2 mismatch repair gene of Saccharomyces cerevisiae. Genetics. 2000 Jun;155(2):589–599. doi: 10.1093/genetics/155.2.589. [DOI] [PMC free article] [PubMed] [Google Scholar]
  68. Stewart G. S., Maser R. S., Stankovic T., Bressan D. A., Kaplan M. I., Jaspers N. G., Raams A., Byrd P. J., Petrini J. H., Taylor A. M. The DNA double-strand break repair gene hMRE11 is mutated in individuals with an ataxia-telangiectasia-like disorder. Cell. 1999 Dec 10;99(6):577–587. doi: 10.1016/s0092-8674(00)81547-0. [DOI] [PubMed] [Google Scholar]
  69. Sugawara N., Ivanov E. L., Fishman-Lobell J., Ray B. L., Wu X., Haber J. E. DNA structure-dependent requirements for yeast RAD genes in gene conversion. Nature. 1995 Jan 5;373(6509):84–86. doi: 10.1038/373084a0. [DOI] [PubMed] [Google Scholar]
  70. 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]
  71. Takata M., Sasaki M. S., Sonoda E., Morrison C., Hashimoto M., Utsumi H., Yamaguchi-Iwai Y., Shinohara A., Takeda S. Homologous recombination and non-homologous end-joining pathways of DNA double-strand break repair have overlapping roles in the maintenance of chromosomal integrity in vertebrate cells. EMBO J. 1998 Sep 15;17(18):5497–5508. doi: 10.1093/emboj/17.18.5497. [DOI] [PMC free article] [PubMed] [Google Scholar]
  72. Tishkoff D. X., Boerger A. L., Bertrand P., Filosi N., Gaida G. M., Kane M. F., Kolodner R. D. Identification and characterization of Saccharomyces cerevisiae EXO1, a gene encoding an exonuclease that interacts with MSH2. Proc Natl Acad Sci U S A. 1997 Jul 8;94(14):7487–7492. doi: 10.1073/pnas.94.14.7487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  73. Tran H. T., Degtyareva N. P., Koloteva N. N., Sugino A., Masumoto H., Gordenin D. A., Resnick M. A. Replication slippage between distant short repeats in Saccharomyces cerevisiae depends on the direction of replication and the RAD50 and RAD52 genes. Mol Cell Biol. 1995 Oct;15(10):5607–5617. doi: 10.1128/mcb.15.10.5607. [DOI] [PMC free article] [PubMed] [Google Scholar]
  74. Tran H. T., Gordenin D. A., Resnick M. A. The 3'-->5' exonucleases of DNA polymerases delta and epsilon and the 5'-->3' exonuclease Exo1 have major roles in postreplication mutation avoidance in Saccharomyces cerevisiae. Mol Cell Biol. 1999 Mar;19(3):2000–2007. doi: 10.1128/mcb.19.3.2000. [DOI] [PMC free article] [PubMed] [Google Scholar]
  75. Tsubouchi H., Ogawa H. Exo1 roles for repair of DNA double-strand breaks and meiotic crossing over in Saccharomyces cerevisiae. Mol Biol Cell. 2000 Jul;11(7):2221–2233. doi: 10.1091/mbc.11.7.2221. [DOI] [PMC free article] [PubMed] [Google Scholar]
  76. Tsukamoto Y., Kato J., Ikeda H. Silencing factors participate in DNA repair and recombination in Saccharomyces cerevisiae. Nature. 1997 Aug 28;388(6645):900–903. doi: 10.1038/42288. [DOI] [PubMed] [Google Scholar]
  77. 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]
  78. Wach A., Brachat A., Pöhlmann R., Philippsen P. New heterologous modules for classical or PCR-based gene disruptions in Saccharomyces cerevisiae. Yeast. 1994 Dec;10(13):1793–1808. doi: 10.1002/yea.320101310. [DOI] [PubMed] [Google Scholar]
  79. Wu X., Wilson T. E., Lieber M. R. A role for FEN-1 in nonhomologous DNA end joining: the order of strand annealing and nucleolytic processing events. Proc Natl Acad Sci U S A. 1999 Feb 16;96(4):1303–1308. doi: 10.1073/pnas.96.4.1303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  80. Xiao W., Chow B. L., Rathgeber L. The repair of DNA methylation damage in Saccharomyces cerevisiae. Curr Genet. 1996 Dec;30(6):461–468. doi: 10.1007/s002940050157. [DOI] [PubMed] [Google Scholar]
  81. Zou H., Rothstein R. Holliday junctions accumulate in replication mutants via a RecA homolog-independent mechanism. Cell. 1997 Jul 11;90(1):87–96. doi: 10.1016/s0092-8674(00)80316-5. [DOI] [PubMed] [Google Scholar]

Articles from Genetics are provided here courtesy of Oxford University Press

RESOURCES