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Article

Distinct Roles of Mus81, Yen1, Slx1-Slx4, and Rad1 Nucleases in the Repair of Replication-Born Double-Strand Breaks by Sister Chromatid Exchange

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Pages 1592-1603 | Received 23 Jan 2012, Accepted 14 Feb 2012, Published online: 20 Mar 2023

REFERENCES

  • Aguilera A, Gomez-Gonzalez B. 2008. Genome instability: a mechanistic view of its causes and consequences. Nat. Rev. Genet. 9:204–217.
  • Alberti S, Gitler AD, Lindquist S. 2007. A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24:913–919.
  • Andersen SL, et al. 2009. Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol. Cell 35:128–135.
  • Bastin-Shanower SA, Fricke WM, Mullen JR, Brill SJ. 2003. The mechanism of Mus81-Mms4 cleavage site selection distinguishes it from the homologous endonuclease Rad1-Rad10. Mol. Cell. Biol. 23:3487–3496.
  • Blanco MG, Matos J, Rass U, Ip SC, West SC. 2010. Functional overlap between the structure-specific nucleases Yen1 and Mus81-Mms4 for DNA-damage repair in S. cerevisiae. DNA Repair (Amst.). 9:394–402.
  • Boddy MN, et al. 2001. Mus81-Eme1 are essential components of a Holliday junction resolvase. Cell 107:537–548.
  • Cejka P, Plank JL, Bachrati CZ, Hickson ID, Kowalczykowski SC. 2010. Rmi1 stimulates decatenation of double Holliday junctions during dissolution by Sgs1-Top3. Nat. Struct. Mol. Biol. 17:1377–1382.
  • Chakraverty RK, et al. 2001. Topoisomerase III acts upstream of Rad53p in the S-phase DNA damage checkpoint. Mol. Cell. Biol. 21:7150–7162.
  • Ciccia A, McDonald N, West SC. 2008. Structural and functional relationships of the XPF/MUS81 family of proteins. Annu. Rev. Biochem. 77:259–287.
  • Cortes-Ledesma F, Aguilera A. 2006. Double-strand breaks arising by replication through a nick are repaired by cohesin-dependent sister-chromatid exchange. EMBO Rep. 7:919–926.
  • Cortes-Ledesma F, Tous C, Aguilera A. 2007. Different genetic requirements for repair of replication-born double-strand breaks by sister-chromatid recombination and break-induced replication. Nucleic Acids Res. 35:6560–6570.
  • Coulon S, et al. 2004. Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol. Biol. Cell 15:71–80.
  • De Piccoli G, et al. 2006. Smc5-Smc6 mediate DNA double-strand-break repair by promoting sister-chromatid recombination. Nat. Cell Biol. 8:1032–1034.
  • Doe CL, Ahn JS, Dixon J, Whitby MC. 2002. Mus81-Eme1 and Rqh1 involvement in processing stalled and collapsed replication forks. J. Biol. Chem. 277:32753–32759.
  • Ehmsen KT, Heyer WD. 2008. Saccharomyces cerevisiae Mus81-Mms4 is a catalytic, DNA structure-selective endonuclease. Nucleic Acids Res. 36:2182–2195.
  • Ehmsen KT, Heyer WD. 2009. A junction branch point adjacent to a DNA backbone nick directs substrate cleavage by Saccharomyces cerevisiae Mus81-Mms4. Nucleic Acids Res. 37:2026–2036.
  • Fabre F, Chan A, Heyer WD, Gangloff S. 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. U. S. A. 99:16887–16892.
  • Fekairi S, et al. 2009. Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138:78–89.
  • Flott S, et al. 2007. Phosphorylation of Slx4 by Mec1 and Tel1 regulates the single-strand annealing mode of DNA repair in budding yeast. Mol. Cell. Biol. 27:6433–6445.
  • Fricke WM, Bastin-Shanower SA, Brill SJ. 2005. Substrate specificity of the Saccharomyces cerevisiae Mus81-Mms4 endonuclease. DNA Repair (Amst.). 4:243–251.
  • Fricke WM, Brill SJ. 2003. Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev. 17:1768–1778.
  • Gangloff S, McDonald JP, Bendixen C, Arthur L, Rothstein R. 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.
  • Gaskell LJ, Osman F, Gilbert RJ, Whitby MC. 2007. Mus81 cleavage of Holliday junctions: a failsafe for processing meiotic recombination intermediates? EMBO J. 26:1891–1901.
  • Gonzalez-Barrera S, Cortes-Ledesma F, Wellinger RE, Aguilera A. 2003. Equal sister chromatid exchange is a major mechanism of double-strand break repair in yeast. Mol. Cell 11:1661–1671.
  • Gonzalez-Barrera S, Garcia-Rubio M, Aguilera A. 2002. Transcription and double-strand breaks induce similar mitotic recombination events in Saccharomyces cerevisiae. Genetics 162:603–614.
  • Habraken Y, Sung P, Prakash L, Prakash S. 1994. Holliday junction cleavage by yeast Rad1 protein. Nature 371:531–534.
  • Hanada K, et al. 2007. The structure-specific endonuclease Mus81 contributes to replication restart by generating double-strand DNA breaks. Nat. Struct. Mol. Biol. 14:1096–1104.
  • Heyer WD, Ehmsen KT, Liu J. 2010. Regulation of homologous recombination in eukaryotes. Annu. Rev. Genet. 44:113–139.
  • Ho CK, Mazon G, Lam AF, Symington LS. 2010. Mus81 and Yen1 promote reciprocal exchange during mitotic recombination to maintain genome integrity in budding yeast. Mol. Cell 40:988–1000.
  • Interthal H, Heyer WD. 2000. MUS81 encodes a novel helix-hairpin-helix protein involved in the response to UV- and methylation-induced DNA damage in Saccharomyces cerevisiae. Mol. Gen. Genet. 263:812–827.
  • Ip SC, et al. 2008. Identification of Holliday junction resolvases from humans and yeast. Nature 456:357–361.
  • Jessop L, Lichten M. 2008. Mus81/Mms4 endonuclease and Sgs1 helicase collaborate to ensure proper recombination intermediate metabolism during meiosis. Mol. Cell 31:313–323.
  • Kaliraman V, Mullen JR, Fricke WM, Bastin-Shanower SA, Brill SJ. 2001. Functional overlap between Sgs1-Top3 and the Mms4-Mus81 endonuclease. Genes Dev. 15:2730–2740.
  • Lorenz A, West SC, Whitby MC. 2010. The human Holliday junction resolvase GEN1 rescues the meiotic phenotype of a Schizosaccharomyces pombe mus81 mutant. Nucleic Acids Res. 38:1866–1873.
  • Martini E, Diaz RL, Hunter N, Keeney S. 2006. Crossover homeostasis in yeast meiosis. Cell 126:285–295.
  • Mullen JR, Kaliraman V, Ibrahim SS, Brill SJ. 2001. Requirement for three novel protein complexes in the absence of the Sgs1 DNA helicase in Saccharomyces cerevisiae. Genetics 157:103–118.
  • Munoz IM, et al. 2009. Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol. Cell 35:116–127.
  • Oh SD, Lao JP, Taylor AF, Smith GR, Hunter N. 2008. RecQ helicase, Sgs1, and XPF family endonuclease, Mus81-Mms4, resolve aberrant joint molecules during meiotic recombination. Mol. Cell 31:324–336.
  • Osman F, Dixon J, Doe CL, Whitby MC. 2003. Generating crossovers by resolution of nicked Holliday junctions: a role for Mus81-Eme1 in meiosis. Mol. Cell 12:761–774.
  • Paques F, Haber JE. 1999. Multiple pathways of recombination induced by double-strand breaks in Saccharomyces cerevisiae. Microbiol. Mol. Biol. Rev. 63:349–404.
  • Pardo B, Gomez-Gonzalez B, Aguilera A. 2009. DNA repair in mammalian cells. DNA double-strand break repair: how to fix a broken relationship. Cell. Mol. Life Sci. 66:1039–1056.
  • Rass U, et al. 2010. Mechanism of Holliday junction resolution by the human GEN1 protein. Genes Dev. 24:1559–1569.
  • Roseaulin L, et al. 2008. Mus81 is essential for sister chromatid recombination at broken replication forks. EMBO J. 27:1378–1387.
  • Saito TT, Youds JL, Boulton SJ, Colaiacovo MP. 2009. Caenorhabditis elegans HIM-18/SLX-4 interacts with SLX-1 and XPF-1 and maintains genomic integrity in the germline by processing recombination intermediates. PLoS Genet. 5:e1000735.
  • Schwartz EK, Heyer WD. 2011. Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120:423–424.
  • Sekelsky JJ, McKim KS, Chin GM, Hawley RS. 1995. The Drosophila meiotic recombination gene mei-9 encodes a homologue of the yeast excision repair protein Rad1. Genetics 141:619–627.
  • Smith GR, Boddy MN, Shanahan P, Russell P. 2003. Fission yeast Mus81.Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion. Genetics 165:2289–2293.
  • Svendsen JM, et al. 2009. Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138:63–77.
  • Tay YD, Wu L. 2010. Overlapping roles for Yen1 and Mus81 in cellular Holliday junction processing. J. Biol. Chem. 285:11427–11432.
  • Taylor ER, McGowan CH. 2008. Cleavage mechanism of human Mus81-Eme1 acting on Holliday junction structures. Proc. Natl. Acad. Sci. U. S. A. 105:3757–3762.
  • Watt PM, Louis EJ, Borts RH, Hickson ID. 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.
  • Wechsler T, Newman S, West SC. 2011. Aberrant chromosome morphology in human cells defective for Holliday junction resolution. Nature 471:642–646.
  • West SC. 2003. Molecular views of recombination proteins and their control. Nat. Rev. Mol. Cell Biol. 4:435–445.
  • Wu L, Hickson ID. 2003. The Bloom's syndrome helicase suppresses crossing over during homologous recombination. Nature 426:870–874.
  • Yildiz O, Majumder S, Kramer B, Sekelsky JJ. 2002. Drosophila MUS312 interacts with the nucleotide excision repair endonuclease MEI-9 to generate meiotic crossovers. Mol. Cell 10:1503–1509.

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