Multiple Pathways Promote Short-Sequence Recombination in Saccharomyces cerevisiae

REFERENCES

• Ahn, B. Y., K. J. Dornfeld, T. J. Fagrelius, and D. M. Livingston. 1988. Effect of limited homology on gene conversion in a Saccharomyces cerevisiae plasmid recombination system. Mol. Cell. Biol. 8: 2442–2448.
   PubMedGoogle Scholar
• Alani, E., L. Cao, and N. Kleckner. 1987. A method for gene disruption that allows repeated use of URA3 selection in the construction of multiply disrupted yeast strains. Genetics 116: 541–545.
   PubMedGoogle Scholar
• Alani, E., R. Padmore, and N. Kleckner. 1990. Analysis of wild-type and rad50 mutants of yeast suggests an intimate relationship between meiotic chromosome synapsis and recombination. Cell 61: 419–436.
   PubMed Web of Science ®Google Scholar
• Alani, E., S. Subbiah, and N. Kleckner. 1989. The yeast RAD50 gene encodes a predicted 153-kD protein containing a purine nucleotide-binding domain and two large heptad-repeat regions. Genetics 122: 47–57.
   PubMedGoogle Scholar
• Bailis, A. M., and S. Maines. 1996. Nucleotide excision repair gene function in short-sequence recombination. J. Bacteriol. 178: 2136–2140.
   PubMedGoogle Scholar
• Bailis, A. M., S. Maines, and M. C. Negritto. 1995. The essential helicase gene RAD3 suppresses short-sequence recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 15: 3998–4008.
   PubMedGoogle Scholar
• Bardwell, A. J., L. Bardwell, A. E. Tomkinson, and E. C. Friedberg. 1994. Specific cleavage of model recombination and repair intermediates by the yeast Rad1-Rad10 DNA endonuclease. Science 265: 2082–2085.
   PubMed Web of Science ®Google Scholar
• Bowers, J., P. T. Tran, R. M. Liskay, and E. Alani. 2000. Analysis of yeast MSH2-MSH6 suggests that the initiation of mismatch repair can be separated into discrete steps. J. Mol. Biol. 302: 327–338.
   PubMedGoogle Scholar
• Bressan, D. A., B. K. Baxter, and J. H. J. Petrini. 1999. The Mre11-Rad50 Xrs2 protein complex facilitates homologous recombination-based double-strand break repair in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 7681–7687.
   PubMedGoogle Scholar
• Bressan, D. A., H. A. Olivares, B. E. Nelms, and J. H. J. Petrini. 1998. Alteration of N-terminal phosphoesterase signature motifs inactivates Saccharomyces cerevisiae Mre11. Genetics 150: 591–600.
   PubMed Web of Science ®Google Scholar
• Britten, R. J., and D. E. Kohne. 1968. Repeated sequences in DNA: hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms. Science 161: 529–540.
   PubMed Web of Science ®Google Scholar
• Burke, D., D. Dawson, and T. Stearns (ed.). 2000. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   Google Scholar
• Chen, L., K. Trujillo, W. Ramos, P. Sung, and A. E. Tomkinson. 2001. Promotion of Dnl4-catalyzed DNA end-joining by the Rad50/Mre11/Xrs2 and Hdf1 and Hdf2 complexes. Cell 8: 1105–1115.
   Google Scholar
• D'Amours, D., and S. P. Jackson. 2001. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev. 15: 2238–2249.
   PubMedGoogle Scholar
• Deininger, P. L., and M. A. Batzer. 1999. Alu repeats and human disease. Mol. Genet. Metab. 67: 183–193.
   PubMed Web of Science ®Google Scholar
• Evans, E., N. Sugawara, J. E. Haber, and E. Alani. 2000. The Saccharomyces cerevisiae Msh2 mismatch repair protein localizes to recombination intermediates in vivo. Mol. Cell 5: 789–799.
   PubMedGoogle Scholar
• Fishman-Lobell, J., and J. E. Haber. 1992. Removal of nonhomologous DNA ends in double-strand break recombination: the role of the yeast ultraviolet repair gene RAD1. Science 258: 480–484.
   PubMedGoogle Scholar
• Frank, G., J. Qiu, M. Y. Somsouk, Y. Weng, L. Somsouk, J. P. Nolan, and B. Shen. 1998. Partial functional deficiency of E160D flap endonuclease-1 mutant in vitro and in vivo is due to defective cleavage of DNA substrates. J. Biol. Chem. 273: 33064–33072.
   PubMed Web of Science ®Google Scholar
• Furuse, M., Y. Nagase, M. Lopes, C. Lucca, M. Ferrari, G. Liberi, M. Muzi Falconi, and P. Plevani. 2000. Distinct roles of two separable in vitro activities of yeast Mre11 in mitotic and meiotic recombination. EMBO J. 17: 6412–6425.
   Google Scholar
• Haber, J. E. 1998. The many interfaces of Mre11. Cell 95: 583–586.
   PubMed Web of Science ®Google Scholar
• Hartsuiker, E., E. Vaessen, A. M. Carr, and J. Kohli. 2001. Fission yeast Rad50 stimulates sister chromatid recombination and links cohesion with repair. EMBO J. 20: 6660–6671.
   PubMedGoogle Scholar
• Haynes, R. H., and B. A. Kunz. 1981. DNA repair and mutagenesis in yeast, p. 371–414. In J. N. Strathern, E. W. Jones, and J.R. Broach (ed.), The molecular biology of the yeast Saccharomyces: life cycle and inheritance. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
   Google Scholar
• Holmes, A., and J. E. Haber. 1999. Double-strand break repair requires both leading and lagging strand DNA polymerases. Cell 96: 415–424.
   PubMed Web of Science ®Google Scholar
• Ivanov, E. L., V. G. Korolev, and F. Fabre. 1992. XRS2, a DNA repair gene of Saccharomyces cerevisiae, is needed for meiotic recombination. Genetics 132: 651–664.
   PubMed Web of Science ®Google Scholar
• Ivanov, E. L., N. Sugawara, C. I. White, F. Fabre, and J. E. Haber. 1994. Mutations in XRS2 and RAD50 delay but do not prevent mating-type switching in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 3414–3425.
   PubMedGoogle Scholar
• Jinks-Robertson, S., M. Michelitch, and S. Ramcharan. 1993. Substrate length requirements for efficient mitotic recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 13: 3937–3950.
   PubMedGoogle Scholar
• Johnson, R. E., G. K. Kovvali, L. Prakash, and S. Prakash. 1998. Requirement of the yeast Rth1 5′ to 3′ exonuclease for the stability of simple repetitive DNA. Science 269: 238–239.
   Google Scholar
• Kadyk, L. C., and L. H. Hartwell. 1993. Replication-dependent sister chromatid recombination in rad1 mutants of Saccharomyces cerevisiae. Genetics 133: 469–487.
   PubMedGoogle Scholar
• Kirkpatrick, D. T., and T. D. Petes. 1997. Repair of DNA loops involves DNA-mismatch and nucleotide-excision repair proteins. Nature 387: 929–931.
   PubMedGoogle Scholar
• Klein, H. 1989. Different types of recombination events are controlled by the RAD1 and RAD52 genes of Saccharomyces cerevisiae. Genetics 120: 367–377.
   Google Scholar
• Kramer, K. M., J. A. Brock, K. Bloom, J. K. Moore, and J. E. Haber. 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.
   PubMedGoogle Scholar
• Lee, B.-S., L. Bi, D. J. Garfinkel, and A. M. Bailis. 2000. Nucleotide excision repair/TFIIH helicases Rad3 and Ssl2 inhibit short-sequence recombination and Ty1 retrotransposition by similar mechanisms. Mol. Cell. Biol. 20: 2436–2445.
   PubMedGoogle Scholar
• Lee, S. E., J. K. Moore, A. Holmes, K. Umezu, R. D. Kolodner, and J. E. Haber. 1998. Saccharomyces Ku70, Mre11/Rad50, and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94: 399–409.
   PubMed Web of Science ®Google Scholar
• Lieber, M. 1997. The FEN-1 family of structure-specific nucleases in eukaryotic DNA replication, recombination and repair. Bioessays 19: 233–240.
   PubMedGoogle Scholar
• Maines, S., M. C. Negritto, X. Wu, G. M. Manthey, and A. M. Bailis. 1998. Novel mutations in the RAD3 and SSL1 genes perturb genome stability by stimulating recombination between short repeats in Saccharomyces cerevisiae. Genetics 150: 963–976.
   PubMedGoogle Scholar
• Manivasakam, P., S. C. Weber, J. McElver, and R. H. Schiestl. 1995. Micro-homology mediated PCR targeting in Saccharomyces cerevisiae. Nucleic Acids Res. 23: 2799–2800.
   PubMedGoogle Scholar
• Marsischky, G. T., S. Lee, J. Griffith, and R. D. Kolodner. 1999. Saccharomyces cerevisiae MSH2/6 complex interacts with Holliday junctions and facilitates their cleavage by phage resolution enzymes. J. Biol. Chem. 274: 7200–7206.
   PubMed Web of Science ®Google 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
• Moore, J. K., and J. E. Haber. 1996. Cell cycle and genetic requirements of two pathways of nonhomologous end-joining repair of double-strand breaks in Saccharomyces cerevisiae. Mol. Cell. Biol. 16: 2164–2173.
   PubMed Web of Science ®Google Scholar
• Moreau, S., J. R. Ferguson, and L. S. Symington. 1999. The nuclease activity of Mre11 is required for meiosis but not mating type switching, end joining, or telomere maintenance. Mol. Cell. Biol. 19: 556–566.
   PubMed Web of Science ®Google Scholar
• Morrison, A., A. L. Johnson, L. H. Johnston, and A. Sugino. 1993. Pathway correcting DNA replication errors in Saccharomyces cerevisiae. EMBO J. 12: 1467–1473.
   PubMed Web of Science ®Google Scholar
• Morrow, D. M., C. Connelly, and P. Hieter. 1997. “Break-copy” duplication: a model for chromosome fragment formation in Saccharomyces cerevisiae. Genetics 147: 371–382.
   PubMed Web of Science ®Google Scholar
• Nairz, K., and F. Klein. 1997. Mre11-S, a yeast mutation that blocks double-strand-break processing and permits nonhomologous synapsis in meiosis. Genes Dev. 11: 2272–2290.
   PubMed Web of Science ®Google Scholar
• Negritto, M. T., J. Qiu, D. O. Ratay, B. Shen, and A. M. Bailis. 2001. Novel function of Rad27 (FEN-1) in short-sequence recombination. Mol. Cell. Biol. 21: 2349–2358.
   PubMedGoogle Scholar
• Negritto, M. T., X. Wu, T. Kuo, S. Chu, and A. M. Bailis. 1997. Influence of DNA sequence identity on efficiency of targeted gene replacement. Mol. Cell. Biol. 17:278–286.
   PubMedGoogle Scholar
• Nickoloff, J. A., E. Y. Chen, and F. Heffron. 1986. A 24-base-pair DNA sequence from the MAT locus stimulates intergenic recombination in yeast. Proc. Natl. Acad. Sci. USA 83: 7831–7835.
   PubMedGoogle Scholar
• Paques, F., and J. E. Haber. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63: 349–404.
   PubMed Web of Science ®Google Scholar
• Paull, T. T., and M. Gellert. 1999. Nbs1 potentiates ATP-driven DNA unwinding and endonuclease cleavage by the Mre11/Rad50 complex. Genes Dev. 13: 1276–1288.
   PubMed Web of Science ®Google Scholar
• Petrini, J. H. J. 2000. The Mre11 complex and ATM: collaborating to navigate S phase. Curr. Opin. Cell Biol. 12: 293–296.
   PubMedGoogle Scholar
• Orr-Weaver, T. L., J. W. Szostak, and R. J. Rothstein. 1981. Yeast transformation: a model system for the study of recombination. Proc. Natl. Acad. Sci. USA 78: 6354–6358.
   PubMed Web of Science ®Google Scholar
• Reagan, M. S., C. Pittenger, W. Siede, and E. C. Friedberg. 1995. Characterization of a mutant strain of Saccharomyces cerevisiae with a deletion of the RAD27 gene, a structural homolog of the RAD2 nucleotide excision repair gene. J. Bacteriol. 177: 364–371.
   PubMedGoogle Scholar
• Reenan, R. A. G., and R. D. Kolodner. 1992. Isolation and characterization of two Saccharomyces cerevisiae genes encoding homologs of the bacterial HexA and MutS mismatch repair proteins. Genetics 132: 963–973.
   PubMedGoogle Scholar
• Reynolds, R. J., and E. C. Friedberg. 1981. Molecular mechanisms of pyrimidine dimer excision in Saccharomyces cerevisiae: incision of ultraviolet irradiated deoxyribonucleic acid in vivo. J. Bacteriol. 146: 692–704.
   PubMed Web of Science ®Google Scholar
• Ronne, H., and R. Rothstein. 1988. Mitotic sectored colonies: evidence of heteroduplex DNA formation during direct repeat recombination. Proc. Natl. Acad. Sci. USA 85: 2696–2700.
   PubMed Web of Science ®Google Scholar
• Rothstein, R. 1991. Targeting, disruption, replacement, and allele rescue: integrative DNA transformation in yeast. Methods Enzymol. 194: 281–301.
   PubMedGoogle Scholar
• Rothstein, R., C. Helms, and N. Rosenberg. 1987. Concerted deletions and inversions are caused by mitotic recombination between delta sequences in Saccharomyces cerevisiae. Mol. Cell. Biol. 7: 1198–1207.
   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
• Saparbaev, M., L. Prakash, and S. Prakash. 1996. Requirement of mismatch repair genes MSH2 and MSH3 in the RAD1-RAD10 pathway of mitotic recombination in Saccharomyces cerevisiae. Genetics 142: 727–736.
   PubMed Web of Science ®Google Scholar
• Schiestl, R. H., and T. D. Petes. 1991. Integration of DNA fragments by illegitimate recombination in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88: 7585–7589.
   PubMedGoogle Scholar
• Schiestl, R. H., and S. Prakash. 1988. RAD1, an excision repair gene of Saccharomyces cerevisiae, is also involved in recombination. Mol. Cell. Biol. 8: 3619–3625.
   PubMed Web of Science ®Google Scholar
• Schiestl, R. H., and S. Prakash. 1990. RAD10, an excision repair gene of Saccharomyces cerevisiae, is involved in the RAD1 pathway of mitotic recombination. Mol. Cell. Biol. 10: 2485–2491.
   PubMedGoogle Scholar
• Schiestl, R. H., J. Zhu, and T. D. Petes. 1994. Effect of mutations in genes affecting homologous recombination on restriction enzyme-mediated and illegitimate recombination in Saccharomyces cerevisiae. Mol. Cell. Biol. 14: 4493–4500.
   PubMedGoogle Scholar
• Schild, D., B. Konforti, C. Perez, W. Gish, and R. K. Mortimer. 1983. Isolation and characterization of yeast DNA repair genes. I. Cloning of the RAD52 gene. Curr. Genet. 7: 85–92.
   PubMed Web of Science ®Google Scholar
• Sommers, C. H., E. J. Miller, B. Dujon, S. Prakash, and L. Prakash. 1995. Conditional lethality of null mutations in RTH1 that encodes the yeast counterpart of a mammalian 5′ to 3′ exonuclease required for lagging strand synthesis in reconstituted systems. J. Biol. Chem. 270: 4193–4196.
   PubMedGoogle Scholar
• Sugawara, N., and J. E. Haber. 1992. Characterization of double-strand break-induced recombination: homology requirements and single-stranded DNA formation. Mol. Cell. Biol. 12: 563–575.
   PubMedGoogle Scholar
• Sugawara, N., F. Paques, M. Colaiacovo, and J. E. Haber. 1997. Role of Saccharomyces cerevisiae Msh2 and Msh3 repair proteins in double-strand break-induced recombination. Proc. Natl. Acad. Sci. USA 94: 9214–9219.
   PubMed Web of Science ®Google Scholar
• Sung, P., P. Reynolds, L. Prakash, and S. Prakash. 1993. Purification and characterization of the Saccharomyces cerevisiae Rad1/Rad10 endonuclease. J. Biol. Chem. 26: 23691–23699.
   Google Scholar
• Symington, L. S., L. E. Kang, and S. Moreau. 2000. Alteration of gene conversion tract length and associated crossing over during plasmid gap repair in a nuclease-deficient strain of Saccharomyces cerevisiae. Nucleic Acids Res. 28: 4649–4656.
   PubMedGoogle Scholar
• Szankasi, P., C. Gysler, U. Zehntner, U. Leupold, J. Kohli, and P. Munz. 1986. Mitotic recombination between dispersed but related tRNA genes of S. pombe generates a reciprocal translocation. Mol. Gen. Genet. 202: 394–402.
   Google Scholar
• Thomas, B. J., and R. Rothstein. 1989. The genetic control of direct-repeat recombination in Saccharomyces: the effect of rad52 and rad1 on mitotic recombination of a GAL10 transcriptionally regulated gene. Genetics 123: 725–738.
   PubMed Web of Science ®Google Scholar
• Tomkinson, A. E., A. J. Bardwell, L. Bardwell, N. J. Tappe, and E. C. Friedberg. 1993. Yeast DNA repair and recombination proteins Rad1 and Rad10 constitute a single-stranded-DNA endonuclease. Nature 362: 860–862.
   PubMedGoogle Scholar
• Trujillo, K. M., and P. Sung. 2001. DNA structure-specific nuclease activities in the Saccharomyces cerevisiae Rad50-Mre11 complex. J. Biol. Chem. 276: 35458–35464.
   PubMed Web of Science ®Google Scholar
• Tsubouchi, H., and H. Ogawa. 1998. A novel mre11 mutation impairs processing of double-strand breaks of DNA during both mitosis and meiosis. Mol. Cell. Biol. 18: 260–268.
   PubMedGoogle Scholar
• Tsukamoto, Y., J. Kato, and H. Ikeda. 1996. Hdf1, a yeast Ku-protein homologue, is involved in illegitimate recombination, but not in homologous recombination. Nucleic Acids Res. 24: 2067–2072.
   PubMedGoogle Scholar
• Usui, T., T. Ohta, H. Oshiumi, J. Tomizawa, H. Ogawa, and T. Ogawa. 1998. Complex formation and functional versatility of Mre11 of budding yeast in recombination. Cell 95: 705–716.
   PubMed Web of Science ®Google Scholar
• Wilcox, D. R., and L. Prakash. 1981. Incision and postincision step of pyrimidine dimer removal in excision-defective mutants of Saccharomyces cerevisiae. J. Bacteriol. 148: 618–623.
   PubMed Web of Science ®Google Scholar
• Wilson, T. E., U. Grawunder, and M. R. Lieber. 1997. Yeast DNA ligase IV mediates non-homologous DNA end joining. Nature 388: 495–498.
   PubMed Web of Science ®Google Scholar