Phosphorylation of Slx4 by Mec1 and Tel1 Regulates the Single-Strand Annealing Mode of DNA Repair in Budding Yeast

REFERENCES

• Bardwell, L., A. J. Cooper, and E. C. Friedberg. 1992. Stable and specific association between the yeast recombination and DNA repair proteins RAD1 and RAD10 in vitro. Mol. Cell Biol. 12:3041–3049.
   PubMedGoogle Scholar
• Bastin-Shanower, S. A., W. M. Fricke, J. R. Mullen, and S. J. Brill. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23:3487–3496.
   PubMedGoogle Scholar
• Beranek, D. T. 1990. Distribution of methyl and ethyl adducts following alkylation with monofunctional alkylating agents. Mutat. Res. 231:11–30.
   PubMed Web of Science ®Google Scholar
• Brusky, J., Y. Zhu, and W. Xiao. 2000. UBC13, a DNA-damage-inducible gene, is a member of the error-free postreplication repair pathway in Saccharomyces cerevisiae. Curr. Genet. 37:168–174.
   PubMedGoogle Scholar
• Chang, M., M. Bellaoui, C. Boone, and G. W. Brown. 2002. A genome-wide screen for methyl methanesulfonate-sensitive mutants reveals genes required for S phase progression in the presence of DNA damage. Proc. Natl. Acad. Sci. USA 99:16934–16939.
   PubMed Web of Science ®Google Scholar
• Chin, J. K., V. I. Bashkirov, W. D. Heyer, and F. E. Romesberg. 2006. Esc4/Rtt107 and the control of recombination during replication. DNA Repair (Amsterdam) 5:618–628.
   PubMedGoogle Scholar
• Coulon, S., P. H. Gaillard, C. Chahwan, W. H. McDonald, J. R. Yates III, and P. Russell. 2004. Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15:71–80.
   PubMed Web of Science ®Google Scholar
• Desany, B. A., A. A. Alcasabas, J. B. Bachant, and S. J. Elledge. 1998. Recovery from DNA replicational stress is the essential function of the S-phase checkpoint pathway. Genes Dev. 12:2956–2970.
   PubMed Web of Science ®Google Scholar
• Duncker, B. P., K. Shimada, M. Tsai-Pflugfelder, P. Pasero, and S. M. Gasser. 2002. An N-terminal domain of Dbf4p mediates interaction with both origin recognition complex (ORC) and Rad53p and can deregulate late origin firing. Proc. Natl. Acad. Sci. USA 99:16087–16092.
   PubMed Web of Science ®Google Scholar
• Fabre, F., A. Chan, W. D. Heyer, and S. Gangloff. 2002. Alternate pathways involving Sgs1/Top3, Mus81/ Mms4, and Srs2 prevent formation of toxic recombination intermediates from single-stranded gaps created by DNA replication. Proc. Natl. Acad. Sci. USA 99:16887–16892.
   PubMed Web of Science ®Google 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
• Flott, S., and J. Rouse. 2005. Slx4 becomes phosphorylated after DNA damage in a Mec1/Tel1-dependent manner and is required for repair of DNA alkylation damage. Biochem. J. 391:325–333.
   PubMedGoogle Scholar
• Freudenreich, C. H., S. M. Kantrow, and V. A. Zakian. 1998. Expansion and length-dependent fragility of CTG repeats in yeast. Science 279:853–856.
   PubMed Web of Science ®Google Scholar
• Fricke, W. M., and S. J. Brill. 2003. Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev. 17:1768–1778.
   PubMed Web of Science ®Google Scholar
• Gangloff, S., J. P. McDonald, C. Bendixen, L. Arthur, and R. Rothstein. 1994. The yeast type I topoisomerase Top3 interacts with Sgs1, a DNA helicase homolog: a potential eukaryotic reverse gyrase. Mol. Cell. Biol. 14:8391–8398.
   PubMed Web of Science ®Google Scholar
• Goldfarb, T., and E. Alani. 2005. Distinct roles for the Saccharomyces cerevisiae mismatch repair proteins in heteroduplex rejection, mismatch repair and nonhomologous tail removal. Genetics 169:563–574.
   PubMed Web of Science ®Google Scholar
• Hanway, D., J. K. Chin, G. Xia, G. Oshiro, E. A. Winzeler, and F. E. Romesberg. 2002. Previously uncharacterized genes in the UV- and MMS-induced DNA damage response in yeast. Proc. Natl. Acad. Sci. USA 99:10605–10610.
   PubMed Web of Science ®Google Scholar
• Hennessy, K. M., A. Lee, E. Chen, and D. Botstein. 1991. A group of interacting yeast DNA replication genes. Genes Dev. 5:958–969.
   PubMedGoogle Scholar
• Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169–178.
   PubMed Web of Science ®Google Scholar
• Higgins, N. P., K. Kato, and B. Strauss. 1976. A model for replication repair in mammalian cells. J. Mol. Biol. 101:417–425.
   PubMed Web of Science ®Google Scholar
• Hoege, C., B. Pfander, G. L. Moldovan, G. Pyrowolakis, and S. Jentsch. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141.
   PubMed Web of Science ®Google Scholar
• Ito, T., T. Chiba, R. Ozawa, M. Yoshida, M. Hattori, and Y. Sakaki. 2001. A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98:4569–4574.
   PubMed Web of Science ®Google Scholar
• Kaliraman, V., J. R. Mullen, W. M. Fricke, S. A. Bastin-Shanower, and S. J. Brill. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2730–2740.
   PubMed Web of Science ®Google Scholar
• Kaye, J. A., J. A. Melo, S. K. Cheung, M. B. Vaze, J. E. Haber, and D. P. Toczyski. 2004. DNA breaks promote genomic instability by impeding proper chromosome segregation. Curr. Biol. 14:2096–2106.
   PubMedGoogle Scholar
• Khakhar, R. R., J. A. Cobb, L. Bjergbaek, I. D. Hickson, and S. M. Gasser. 2003. RecQ helicases: multiple roles in genome maintenance. Trends Cell Biol. 13:493–501.
   PubMed Web of Science ®Google Scholar
• Lawrence, C. W., and V. M. Maher. 2001. Mutagenesis in eukaryotes dependent on DNA polymerase zeta and Rev1p. Philos. Trans. R. Soc. London B 356:41–46.
   PubMed Web of Science ®Google Scholar
• Liberi, G., G. Maffioletti, C. Lucca, I. Chiolo, A. Baryshnikova, C. Cotta-Ramusino, M. Lopes, A. Pellicioli, J. E. Haber, and M. Foiani. 2005. Rad51-dependent DNA structures accumulate at damaged replication forks in sgs1 mutants defective in the yeast ortholog of BLM RecQ helicase. Genes Dev. 19:339–350.
   PubMed Web of Science ®Google Scholar
• Luke, B., G. Versini, M. Jaquenoud, I. W. Zaidi, T. Kurz, L. Pintard, P. Pasero, and M. Peter. 2006. The cullin Rtt101p promotes replication fork progression through damaged DNA and natural pause sites. Curr. Biol. 16:786–792.
   PubMedGoogle Scholar
• Michalet, X., R. Ekong, F. Fougerousse, S. Rousseaux, C. Schurra, N. Hornigold, M. van Slegtenhorst, J. Wolfe, S. Povey, J. S. Beckmann, and A. Bensimon. 1997. Dynamic molecular combing: stretching the whole human genome for high-resolution studies. Science 277:1518–1523.
   PubMed Web of Science ®Google Scholar
• Mullen, J. R., V. Kaliraman, and S. J. Brill. 2000. Bipartite structure of the SGS1 DNA helicase in Saccharomyces cerevisiae. Genetics 154:1101–1114.
   PubMedGoogle Scholar
• Mullen, J. R., V. Kaliraman, S. S. Ibrahim, and S. J. Brill. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103–118.
   PubMed Web of Science ®Google Scholar
• Myung, K., A. Datta, C. Chen, and R. D. Kolodner. 2001. SGS1, the Saccharomyces cerevisiae homologue of BLM and WRN, suppresses genome instability and homeologous recombination. Nat. Genet. 27:113–116.
   PubMed Web of Science ®Google Scholar
• Papouli, E., S. Chen, A. A. Davies, D. Huttner, L. Krejei, P. Sung, and H. D. Ulrich. 2005. Crosstalk between SUMO and ubiquitin on PCNA is mediated by recruitment of the helicase Srs2p. Mol. Cell 19:123–133.
   PubMed Web of Science ®Google Scholar
• Pasero, P., A. Bensimon, and E. Schwob. 2002. Single-molecule analysis reveals clustering and epigenetic regulation of replication origins at the yeast rDNA locus. Genes Dev. 16:2479–2484.
   PubMed Web of Science ®Google Scholar
• Prakash, L. 1981. Characterization of postreplication repair in Saccharomyces cerevisiae and effects of rad6, rad18, rev3 and rad52 mutations. Mol. Gen. Genet. 184:471–478.
   PubMedGoogle Scholar
• Prakash, S., R. E. Johnson, and L. Prakash. 2005. Eukaryotic translesion synthesis DNA polymerases: specificity of structure and function. Annu. Rev. Biochem. 74:317–353.
   PubMed Web of Science ®Google Scholar
• Roberts, T. M., M. S. Kobor, S. A. Bastin-Shanower, M. Ii, S. A. Horte, J. W. Gin, A. Emili, J. Rine, S. J. Brill, and G. W. Brown. 2006. Slx4 regulates DNA damage checkpoint-dependent phosphorylation of the BRCT domain protein Rtt107/Esc4. Mol. Biol. Cell 17:539–548.
   PubMed Web of Science ®Google Scholar
• Rouse, J. 2004. Esc4p, a new target of Mec1p (ATR), promotes resumption of DNA synthesis after DNA damage. EMBO J 23:1188–1197.
   PubMed Web of Science ®Google Scholar
• Rouse, J., and S. P. Jackson. 2000. LCD1: an essential gene involved in checkpoint control and regulation of the MEC1 signalling pathway in Saccharomyces cerevisiae. EMBO J. 19:5801–5812.
   PubMedGoogle Scholar
• Rupp, W. D., C. E. Wilde III, D. L. Reno, and P. Howard-Flanders. 1971. Exchanges between DNA strands in ultraviolet-irradiated Escherichia coli. J. Mol. Biol. 61:25–44.
   PubMed Web of Science ®Google Scholar
• Scholes, D. T., M. Banerjee, B. Bowen, and M. J. Curcio. 2001. Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159:1449–1465.
   PubMed Web of Science ®Google Scholar
• Schurer, K. A., C. Rudolph, H. D. Ulrich, and W. Kramer. 2004. Yeast MPH1 gene functions in an error-free DNA damage bypass pathway that requires genes from Homologous recombination, but not from postreplicative repair. Genetics 166:1673–1686.
   PubMed Web of Science ®Google Scholar
• Spell, R. M., and S. Jinks-Robertson. 2004. Examination of the roles of Sgs1 and Srs2 helicases in the enforcement of recombination fidelity in Saccharomyces cerevisiae. Genetics 168:1855–1865.
   PubMedGoogle Scholar
• Stelter, P., and H. D. Ulrich. 2003. Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425:188–191.
   PubMed Web of Science ®Google Scholar
• Sugawara, N., T. Goldfarb, B. Studamire, E. Alani, and J. E. Haber. 2004. Heteroduplex rejection during single-strand annealing requires Sgs1 helicase and mismatch repair proteins Msh2 and Msh6 but not Pms1. Proc. Natl. Acad. Sci. USA 101:9315–9320.
   PubMed Web of Science ®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 at GAL10, a transcriptionally regulated gene. Genetics 123:725–738.
   PubMed Web of Science ®Google Scholar
• Tong, A. H., M. Evangelista, A. B. Parsons, H. Xu, G. D. Bader, N. Page, M. Robinson, S. Raghibizadeh, C. W. Hogue, H. Bussey, B. Andrews, M. Tyers, and C. Boone. 2001. Systematic genetic analysis with ordered arrays of yeast deletion mutants. Science 294:2364–2368.
   PubMed Web of Science ®Google Scholar
• Tourriere, H., G. Versini, V. Cordon-Preciado, C. Alabert, and P. Pasero. 2005. Mre1 and Tof1 promote replication fork progression and recovery independently of Rad53. Mol. Cell. 19:699–706.
   PubMed Web of Science ®Google Scholar
• Traven, A., and J. Heierhorst. 2005. SQ/TQ cluster domains: concentrated ATM/ATR kinase phosphorylation site regions in DNA-damage-response proteins. Bioessays 27:397–407.
   PubMed Web of Science ®Google Scholar
• Ui, A., M. Seki, H. Ogiwara, R. Onodera, S. Fukushige, F. Onoda, and T. Enomoto. 2005. The ability of Sgs1 to interact with DNA topoisomerase III is essential for damage-induced recombination. DNA Repair (Amsterdam) 4:191–201.
   PubMedGoogle Scholar
• Ulrich, H. D. 2005. The RAD6 pathway: control of DNA damage bypass and mutagenesis by ubiquitin and SUMO. ChemBiochem 6:1735–1743.
   PubMedGoogle Scholar
• Watt, P. M., I. D. Hickson, R. H. Borts, and E. J. Louis. 1996. SGS1, a homologue of the Bloom's and Werner's syndrome genes, is required for maintenance of genome stability in Saccharomyces cerevisiae. Genetics 144:935–945.
   PubMed Web of Science ®Google Scholar
• Wu, L., and I. D. Hickson. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870–874.
   PubMed Web of Science ®Google Scholar
• Yamagata, K., J. Kato, A. Shimamoto, M. Goto, Y. Furuichi, and H. Ikeda. 1998. Bloom's and Werner's syndrome genes suppress hyperrecombination in yeast sgs1 mutant: implication for genomic instability in human diseases. Proc. Natl. Acad. Sci. USA 95:8733–8738.
   PubMed Web of Science ®Google Scholar
• Zappulla, D. C., A. S. Maharaj, J. J. Connelly, R. A. Jockusch, and R. Sternglanz. 2006. Rtt107/Esc4 binds silent chromatin and DNA repair proteins using different BRCT motifs. BMC Mol. Biol. 7:40.
   PubMed Web of Science ®Google Scholar
• Zhang, C., T. M. Roberts, J. Yang, R. Desai, and G. W. Brown. 2006. Suppression of genomic instability by SLX5 and SLX8 in Saccharomyces cerevisiae. DNA Repair (Amsterdam) 5:336–346.
   PubMed Web of Science ®Google Scholar
• Zhang, H., and C. W. Lawrence. 2005. The error-free component of the RAD6/RAD18 DNA damage tolerance pathway of budding yeast employs sister-strand recombination. Proc. Natl. Acad. Sci. USA 102:15954–15959.
   PubMed Web of Science ®Google Scholar