Yeast Rmi1/Nce4 Controls Genome Stability as a Subunit of the Sgs1-Top3 Complex

REFERENCES

• 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
• Bellaoui, M., M. Chang, J. Ou, H. Xu, C. Boone, and G. W. Brown. 2003. Elg1 forms an alternative RFC complex important for DNA replication and genome integrity. EMBO J. 22:4304–4313.
   PubMed Web of Science ®Google Scholar
• Bennett, R. J., J. L. Keck, and J. C. Wang. 1999. Binding specificity determines polarity of DNA unwinding by the Sgs1 protein of S. cerevisiae. J. Mol. Biol. 289:235–248.
   PubMed Web of Science ®Google Scholar
• Bennett, R. J., M. F. Noirot-Gros, and J. C. Wang. 2000. Interaction between yeast Sgs1 helicase and DNA topoisomerase III. J. Biol. Chem. 275:26898–26905.
   PubMedGoogle Scholar
• Boddy, M. N., P. H. Gaillard, W. H. McDonald, P. Shanahan, J. R. Yates III, and P. Russell. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537–548.
   PubMed Web of Science ®Google Scholar
• Chakraverty, R. K., and I. D. Hickson. 1999. Defending genome integrity during DNA replication: a proposed role for RecQ family helicases. Bioessays 21:286–294.
   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
• Constantinou, A., M. Tarsounas, J. K. Karow, R. M. Brosh, V. A. Bohr, I. D. Hickson, and S. C. West. 2000. Werner's syndrome protein (WRN) migrates Holliday junctions and co-localizes with RPA upon replication arrest. EMBO Rep. 1:80–84.
   PubMed Web of Science ®Google Scholar
• Corpet, F. 1988. Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res. 16:10881–10890.
   PubMed Web of Science ®Google Scholar
• Davey, S., C. S. Han, S. A. Ramer, J. C. Klassen, A. Jacobson, A. Eisenberger, K. M. Hopkins, H. B. Lieberman, and G. A. Freyer. 1998. Fission yeast rad12+ regulates cell cycle checkpoint control and is homologous to the Bloom's syndrome disease gene. Mol. Cell Biol. 18:2721–2728.
   PubMed Web of Science ®Google Scholar
• DiGate, R. J., and K. J. Marians. 1988. Identification of a potent decatenating enzyme from Escherichia coli. J. Biol. Chem. 263:13366–13373.
   PubMed Web of Science ®Google Scholar
• Duno, M., B. Thomsen, O. Westergaard, L. Krejci, and C. Bendixen. 2000. Genetic analysis of the Saccharomyces cerevisiae Sgs1 helicase defines an essential function for the Sgs1-Top3 complex in the absence of SRS2 or TOP1. Mol. Gen. Genet. 264:89–97.
   PubMedGoogle 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
• Fricke, W. M., V. Kaliraman, and S. J. Brill. 2001. Mapping the DNA topoisomerase III binding domain of the Sgs1 DNA helicase. J. Biol. Chem. 276:8848–8855.
   PubMedGoogle Scholar
• Gangloff, S., B. de Massy, L. Arthur, R. Rothstein, and F. Fabre. 1999. The essential role of yeast topoisomerase III in meiosis depends on recombination. EMBO J. 18:1701–1711.
   PubMedGoogle 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
• Gangloff, S., C. Soustelle, and F. Fabre. 2000. Homologous recombination is responsible for cell death in the absence of the Sgs1 and Srs2 helicases. Nat. Genet. 25:192–194.
   PubMed Web of Science ®Google Scholar
• Goodwin, A., S. W. Wang, T. Toda, C. Norbury, and I. D. Hickson. 1999. Topoisomerase III is essential for accurate nuclear division in Schizosaccharomyces pombe. Nucleic Acids Res. 27:4050–4058.
   PubMedGoogle Scholar
• Guldener, U., S. Heck, T. Fielder, J. Beinhauer, and J. H. Hegemann. 1996. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 24:2519–2524.
   PubMed Web of Science ®Google Scholar
• Harmon, F. G., R. J. DiGate, and S. C. Kowalczykowski. 1999. RecQ helicase and topoisomerase III comprise a novel DNA strand passage function: a conserved mechanism for control of DNA recombination. Mol. Cell 3:611–620.
   PubMed Web of Science ®Google Scholar
• Hiasa, H., R. J. DiGate, and K. J. Marians. 1994. Decatenating activity of Escherichia coli DNA gyrase and topoisomerases I and III during oriC and pBR322 DNA replication in vitro. J. Biol. Chem. 269:2093–2099.
   PubMed Web of Science ®Google Scholar
• Hickson, I. D. 2003. RecQ helicases: caretakers of the genome. Nat. Rev. Cancer 3:169–178.
   PubMed Web of Science ®Google Scholar
• Ira, G., A. Malkova, G. Liberi, M. Foiani, and J. E. Haber. 2003. Srs2 and Sgs1-Top3 suppress crossovers during double-strand break repair in yeast. Cell 115:401–411.
   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
• Karow, J. K., A. Constantinou, J. L. Li, S. C. West, and I. D. Hickson. 2000. The Bloom's syndrome gene product promotes branch migration of Holliday junctions. Proc. Natl. Acad. Sci. USA 97:6504–6508.
   PubMed Web of Science ®Google Scholar
• Karow, J. K., R. H. Newman, P. S. Freemont, and I. D. Hickson. 1999. Oligomeric ring structure of the Bloom's syndrome helicase. Curr. Biol. 9:597–600.
   PubMed Web of Science ®Google Scholar
• Keil, R. L., and A. D. McWilliams. 1993. A gene with specific and global effects on recombination of sequences from tandemly repeated genes in Saccharomyces cerevisiae. Genetics 135:711–718.
   PubMedGoogle Scholar
• Kim, R. A., and J. C. Wang. 1992. Identification of the yeast TOP3 gene product as a single strand-specific DNA topoisomerase. J. Biol. Chem. 267:17178–17185.
   PubMed Web of Science ®Google Scholar
• Kim, Y. C., J. Lee, and H. S. Koo. 2000. Functional characterization of Caenorhabditis elegans DNA topoisomerase III alpha. Nucleic Acids Res. 28:2012–2017.
   PubMedGoogle Scholar
• Laursen, L. V., E. Ampatzidou, A. H. Andersen, and J. M. Murray. 2003. Role for the fission yeast RecQ helicase in DNA repair in G2. Mol. Cell. Biol. 23:3692–3705.
   PubMed Web of Science ®Google Scholar
• Maftahi, M., C. S. Han, L. D. Langston, J. C. Hope, N. Zigouras, and G. A. Freyer. 1999. The top3+ gene is essential in Schizosaccharomyces pombe and the lethality associated with its loss is caused by Rad12 helicase activity. Nucleic Acids Res. 27:4715–4724.
   PubMedGoogle Scholar
• Maftahi, M., J. C. Hope, L. Delgado-Cruzata, C. S. Han, and G. A. Freyer. 2002. The severe slow growth of Δsrs2 Δrqh1 in Schizosaccharomyces pombe is suppressed by loss of recombination and checkpoint genes. Nucleic Acids Res. 30:4781–4792.
   PubMedGoogle Scholar
• Miyajima, A., M. Seki, F. Onoda, M. Shiratori, N. Odagiri, K. Ohta, Y. Kikuchi, Y. Ohno, and T. Enomoto. 2000. Sgs1 helicase activity is required for mitotic but apparently not for meiotic functions. Mol. Cell. Biol. 20:6399–6409.
   PubMedGoogle Scholar
• Mohammad, M., R. D. York, J. Hommel, and G. M. Kapler. 2003. Characterization of a novel origin recognition complex-like complex: implications for DNA recognition, cell cycle control, and locus-specific gene amplification. Mol. Cell. Biol. 23:5005–5017.
   PubMedGoogle 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
• Murray, J. M., H. D. Lindsay, C. A. Munday, and A. M. Carr. 1997. Role of Schizosaccharomyces pombe RecQ homolog, recombination, and checkpoint genes in UV damage tolerance. Mol. Cell. Biol. 17:6868–6875.
   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
• Nurse, P., C. Levine, H. Hassing, and K. J. Marians. 2003. Topoisomerase III can serve as the cellular decatenase in Escherichia coli. J. Biol. Chem. 278:8653–8660.
   PubMedGoogle Scholar
• Oakley, T. J., A. Goodwin, R. K. Chakraverty, and I. D. Hickson. 2002. Inactivation of homologous recombination suppresses defects in topoisomerase III-deficient mutants. DNA Repair (Amsterdam) 1:463–482.
   PubMedGoogle Scholar
• Onoda, F., M. Seki, A. Miyajima, and T. Enomoto. 2001. Involvement of SGS1 in DNA damage-induced heteroallelic recombination that requires RAD52 in Saccharomyces cerevisiae. Mol. Gen. Genet. 264:702–708.
   PubMedGoogle Scholar
• Onodera, R., M. Seki, A. Ui, Y. Satoh, A. Miyajima, F. Onoda, and T. Enomoto. 2002. Functional and physical interaction between Sgs1 and Top3 and Sgs1-independent function of Top3 in DNA recombination repair. Genes Genet. Syst. 77:11–21.
   PubMedGoogle Scholar
• Ooi, S. L., D. D. Shoemaker, and J. D. Boeke. 2003. DNA helicase gene interaction network defined using synthetic lethality analyzed by microarray. Nat. Genet. 35:277–286.
   PubMed Web of Science ®Google Scholar
• Philipova, D., J. R. Mullen, H. S. Maniar, C. Gu, and S. J. Brill. 1996. A hierarchy of SSB protomers in replication protein A. Genes Dev. 10:2222–2233.
   PubMed Web of Science ®Google Scholar
• Rose, M. D., F. Winston, and P. Hieter. 1990. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
   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
• Shor, E., S. Gangloff, M. Wagner, J. Weinstein, G. Price, and R. Rothstein. 2002. Mutations in homologous recombination genes rescue top3 slow growth in Saccharomyces cerevisiae. Genetics 162:647–662.
   PubMedGoogle Scholar
• Sikorski, R. S., and P. Hieter. 1989. A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 12:19–27.
   Google Scholar
• Spell, R. M., and S. Jinks-Robertson. 2004. Determination of mitotic recombination rates by fluctuation analysis in Saccharomyces cerevisiae. Methods Mol. Biol. 262:3–12.
   PubMedGoogle Scholar
• Studier, F. W., A. H. Rosenberg, J. J. Dunn, and J. W. Dubendorff. 1990. Use of T7 RNA polymerase to direct expression of cloned genes. Methods Enzymol. 185:60–89.
   PubMed Web of Science ®Google Scholar
• Thomas, B. J., and R. Rothstein. 1989. Elevated recombination rates in transcriptionally active DNA. Cell 56:619–630.
   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
• Tong, A. H., G. Lesage, G. D. Bader, H. Ding, H. Xu, X. Xin, J. Young, G. F. Berriz, R. L. Brost, M. Chang, Y. Chen, X. Cheng, G. Chua, H. Friesen, D. S. Goldberg, J. Haynes, C. Humphries, G. He, S. Hussein, L. Ke, N. Krogan, Z. Li, J. N. Levinson, H. Lu, P. Menard, C. Munyana, A. B. Parsons, O. Ryan, R. Tonikian, T. Roberts, A. M. Sdicu, J. Shapiro, B. Sheikh, B. Suter, S. L. Wong, L. V. Zhang, H. Zhu, C. G. Burd, S. Munro, C. Sander, J. Rine, J. Greenblatt, M. Peter, A. Bretscher, G. Bell, F. P. Roth, G. W. Brown, B. Andrews, H. Bussey, and C. Boone. 2004. Global mapping of the yeast genetic interaction network. Science 303:808–813.
   PubMed Web of Science ®Google Scholar
• Ui, A., Y. Satoh, F. Onoda, A. Miyajima, M. Seki, and T. Enomoto. 2001. The N-terminal region of Sgs1, which interacts with Top3, is required for complementation of MMS sensitivity and suppression of hyper-recombination in sgs1 disruptants. Mol. Genet. Genomics 265:837–850.
   PubMedGoogle 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
• Wallis, J. W., G. Chrebet, G. Brodsky, M. Rolfe, and R. Rothstein. 1989. A hyper-recombination mutation in S. cerevisiae identifies a novel eukaryotic topoisomerase. Cell 58:409–419.
   PubMed Web of Science ®Google 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
• Watt, P. M., E. J. Louis, R. H. Borts, and I. D. Hickson. 1995. Sgs1: a eukaryotic homolog of E. coli RecQ that interacts with topoisomerase II in vivo and is required for faithful chromosome segregation. Cell 81:253–260.
   PubMed Web of Science ®Google Scholar
• Wu, L., S. L. Davies, P. S. North, H. Goulaouic, J. F. Riou, H. Turley, K. C. Gatter, and I. D. Hickson. 2000. The Bloom's syndrome gene product interacts with topoisomerase III. J. Biol. Chem. 275:9636–9644.
   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