Cdk1-dependent regulation of the Mre11 complex couples DNA repair pathways to cell cycle progression

References

• Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 2012; 47:497 - 510; http://dx.doi.org/10.1016/j.molcel.2012.07.029; PMID: 22920291
   PubMed Web of Science ®Google Scholar
• Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, Haber JE. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 1998; 94:399 - 409; http://dx.doi.org/10.1016/S0092-8674(00)81482-8; PMID: 9708741
   PubMed Web of Science ®Google Scholar
• Takata M, Sasaki MS, 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; 17:5497 - 508; http://dx.doi.org/10.1093/emboj/17.18.5497; PMID: 9736627
   PubMed Web of Science ®Google Scholar
• Zhang Y, Hefferin ML, Chen L, Shim EY, Tseng HM, Kwon Y, Sung P, Lee SE, Tomkinson AE. Role of Dnl4-Lif1 in nonhomologous end-joining repair complex assembly and suppression of homologous recombination. Nat Struct Mol Biol 2007; 14:639 - 46; http://dx.doi.org/10.1038/nsmb1261; PMID: 17589524
   PubMed Web of Science ®Google Scholar
• Pardo B, Gómez-González B, Aguilera A. DNA repair in mammalian cells: DNA double-strand break repair: how to fix a broken relationship. Cell Mol Life Sci 2009; 66:1039 - 56; http://dx.doi.org/10.1007/s00018-009-8740-3; PMID: 19153654
   PubMed Web of Science ®Google Scholar
• Langerak P, Russell P. Regulatory networks integrating cell cycle control with DNA damage checkpoints and double-strand break repair. Philos Trans R Soc Lond B Biol Sci 2011; 366:3562 - 71; http://dx.doi.org/10.1098/rstb.2011.0070; PMID: 22084383
   PubMed Web of Science ®Google Scholar
• Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM, et al. DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 2004; 431:1011 - 7; http://dx.doi.org/10.1038/nature02964; PMID: 15496928
   PubMed Web of Science ®Google Scholar
• Aylon Y, Liefshitz B, Kupiec M. The CDK regulates repair of double-strand breaks by homologous recombination during the cell cycle. EMBO J 2004; 23:4868 - 75; http://dx.doi.org/10.1038/sj.emboj.7600469; PMID: 15549137
   PubMed Web of Science ®Google Scholar
• Huertas P, Cortés-Ledesma F, Sartori AA, Aguilera A, Jackson SP. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 2008; 455:689 - 92; http://dx.doi.org/10.1038/nature07215; PMID: 18716619
   PubMed Web of Science ®Google Scholar
• Huertas P, Jackson SP. Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 2009; 284:9558 - 65; http://dx.doi.org/10.1074/jbc.M808906200; PMID: 19202191
   PubMed Web of Science ®Google Scholar
• Limbo O, Chahwan C, Yamada Y, de Bruin RA, Wittenberg C, Russell P. Ctp1 is a cell-cycle-regulated protein that functions with Mre11 complex to control double-strand break repair by homologous recombination. Mol Cell 2007; 28:134 - 46; http://dx.doi.org/10.1016/j.molcel.2007.09.009; PMID: 17936710
   PubMed Web of Science ®Google Scholar
• Yu X, Baer R. Nuclear localization and cell cycle-specific expression of CtIP, a protein that associates with the BRCA1 tumor suppressor. J Biol Chem 2000; 275:18541 - 9; http://dx.doi.org/10.1074/jbc.M909494199; PMID: 10764811
   PubMed Web of Science ®Google Scholar
• Chen X, Niu H, Chung WH, Zhu Z, Papusha A, Shim EY, Lee SE, Sung P, Ira G. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 2011; 18:1015 - 9; http://dx.doi.org/10.1038/nsmb.2105; PMID: 21841787
   PubMed Web of Science ®Google Scholar
• Holt LJ, Tuch BB, Villén J, Johnson AD, Gygi SP, Morgan DO. Global analysis of Cdk1 substrate phosphorylation sites provides insights into evolution. Science 2009; 325:1682 - 6; http://dx.doi.org/10.1126/science.1172867; PMID: 19779198
   PubMed Web of Science ®Google Scholar
• Clerici M, Mantiero D, Guerini I, Lucchini G, Longhese MP. The Yku70-Yku80 complex contributes to regulate double-strand break processing and checkpoint activation during the cell cycle. EMBO Rep 2008; 9:810 - 8; http://dx.doi.org/10.1038/embor.2008.121; PMID: 18600234
   PubMed Web of Science ®Google Scholar
• Foster SS, Balestrini A, Petrini JH. Functional interplay of the Mre11 nuclease and Ku in the response to replication-associated DNA damage. Mol Cell Biol 2011; 31:4379 - 89; http://dx.doi.org/10.1128/MCB.05854-11; PMID: 21876003
   PubMed Web of Science ®Google Scholar
• Mimitou EP, Symington LS. Ku prevents Exo1 and Sgs1-dependent resection of DNA ends in the absence of a functional MRX complex or Sae2. EMBO J 2010; 29:3358 - 69; http://dx.doi.org/10.1038/emboj.2010.193; PMID: 20729809
   PubMed Web of Science ®Google Scholar
• D’Amours D, Jackson SP. The Mre11 complex: at the crossroads of dna repair and checkpoint signalling. Nat Rev Mol Cell Biol 2002; 3:317 - 27; http://dx.doi.org/10.1038/nrm805; PMID: 11988766
   PubMed Web of Science ®Google Scholar
• Stracker TH, Petrini JH. The MRE11 complex: starting from the ends. Nat Rev Mol Cell Biol 2011; 12:90 - 103; http://dx.doi.org/10.1038/nrm3047; PMID: 21252998
   PubMed Web of Science ®Google Scholar
• Nicolette ML, Lee K, Guo Z, Rani M, Chow JM, Lee SE, Paull TT. Mre11-Rad50-Xrs2 and Sae2 promote 5′ strand resection of DNA double-strand breaks. Nat Struct Mol Biol 2010; 17:1478 - 85; http://dx.doi.org/10.1038/nsmb.1957; PMID: 21102445
   PubMed Web of Science ®Google Scholar
• Falck J, Forment JV, Coates J, Mistrik M, Lukas J, Bartek J, Jackson SP. CDK targeting of NBS1 promotes DNA-end resection, replication restart and homologous recombination. EMBO Rep 2012; 13:561 - 8; http://dx.doi.org/10.1038/embor.2012.58; PMID: 22565321
   PubMed Web of Science ®Google Scholar
• Wohlbold L, Merrick KA, De S, Amat R, Kim JH, Larochelle S, Allen JJ, Zhang C, Shokat KM, Petrini JH, et al. Chemical genetics reveals a specific requirement for Cdk2 activity in the DNA damage response and identifies Nbs1 as a Cdk2 substrate in human cells. PLoS Genet 2012; 8:e1002935; http://dx.doi.org/10.1371/journal.pgen.1002935; PMID: 22927831
   PubMedGoogle Scholar
• D’Amours D, Jackson SP. The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev 2001; 15:2238 - 49; http://dx.doi.org/10.1101/gad.208701; PMID: 11544181
   PubMed Web of Science ®Google Scholar
• Grenon M, Gilbert C, Lowndes NF. Checkpoint activation in response to double-strand breaks requires the Mre11/Rad50/Xrs2 complex. Nat Cell Biol 2001; 3:844 - 7; http://dx.doi.org/10.1038/ncb0901-844; PMID: 11533665
   PubMed Web of Science ®Google Scholar
• Usui T, Ogawa H, Petrini JH. A DNA damage response pathway controlled by Tel1 and the Mre11 complex. Mol Cell 2001; 7:1255 - 66; http://dx.doi.org/10.1016/S1097-2765(01)00270-2; PMID: 11430828
   PubMed Web of Science ®Google Scholar
• Albuquerque CP, Smolka MB, Payne SH, Bafna V, Eng J, Zhou H. A multidimensional chromatography technology for in-depth phosphoproteome analysis. Mol Cell Proteomics 2008; 7:1389 - 96; http://dx.doi.org/10.1074/mcp.M700468-MCP200; PMID: 18407956
   PubMed Web of Science ®Google Scholar
• Smolka MB, Albuquerque CP, Chen SH, Zhou H. Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci U S A 2007; 104:10364 - 9; http://dx.doi.org/10.1073/pnas.0701622104; PMID: 17563356
   PubMed Web of Science ®Google Scholar
• Li X, Gerber SA, Rudner AD, Beausoleil SA, Haas W, Villén J, Elias JE, Gygi SP. Large-scale phosphorylation analysis of alpha-factor-arrested Saccharomyces cerevisiae. J Proteome Res 2007; 6:1190 - 7; http://dx.doi.org/10.1021/pr060559j; PMID: 17330950
   PubMed Web of Science ®Google Scholar
• Amon A, Irniger S, Nasmyth K. Closing the cell cycle circle in yeast: G2 cyclin proteolysis initiated at mitosis persists until the activation of G1 cyclins in the next cycle. Cell 1994; 77:1037 - 50; http://dx.doi.org/10.1016/0092-8674(94)90443-X; PMID: 8020094
   PubMed Web of Science ®Google Scholar
• Grandin N, Charbonneau M. Mitotic cyclins regulate telomeric recombination in telomerase-deficient yeast cells. Mol Cell Biol 2003; 23:9162 - 77; http://dx.doi.org/10.1128/MCB.23.24.9162-9177.2003; PMID: 14645528
   PubMed Web of Science ®Google Scholar
• Enserink JM, Hombauer H, Huang ME, Kolodner RD. Cdc28/Cdk1 positively and negatively affects genome stability in S. cerevisiae. J Cell Biol 2009; 185:423 - 37; http://dx.doi.org/10.1083/jcb.200811083; PMID: 19398760
   PubMed Web of Science ®Google Scholar
• Kinoshita E, Kinoshita-Kikuta E, Takiyama K, Koike T. Phosphate-binding tag, a new tool to visualize phosphorylated proteins. Mol Cell Proteomics 2006; 5:749 - 57; http://dx.doi.org/10.1074/mcp.T500024-MCP200; PMID: 16340016
   PubMed Web of Science ®Google Scholar
• Garcia B, Stollar EJ, Davidson AR. The importance of conserved features of yeast actin-binding protein 1 (Abp1p): the conditional nature of essentiality. Genetics 2012; 191:1199 - 211; http://dx.doi.org/10.1534/genetics.112.141739; PMID: 22661326
   PubMed Web of Science ®Google Scholar
• Weinert TA, Hartwell LH. The RAD9 gene controls the cell cycle response to DNA damage in Saccharomyces cerevisiae. Science 1988; 241:317 - 22; http://dx.doi.org/10.1126/science.3291120; PMID: 3291120
   PubMed Web of Science ®Google Scholar
• Surana U, Robitsch H, Price C, Schuster T, Fitch I, Futcher AB, Nasmyth K. The role of CDC28 and cyclins during mitosis in the budding yeast S. cerevisiae. Cell 1991; 65:145 - 61; http://dx.doi.org/10.1016/0092-8674(91)90416-V; PMID: 1849457
   PubMed Web of Science ®Google Scholar
• Pellicioli A, Lucca C, Liberi G, Marini F, Lopes M, Plevani P, Romano A, Di Fiore PP, Foiani M. Activation of Rad53 kinase in response to DNA damage and its effect in modulating phosphorylation of the lagging strand DNA polymerase. EMBO J 1999; 18:6561 - 72; http://dx.doi.org/10.1093/emboj/18.22.6561; PMID: 10562568
   PubMed Web of Science ®Google Scholar
• Mallory JC, Bashkirov VI, Trujillo KM, Solinger JA, Dominska M, Sung P, Heyer WD, Petes TD. Amino acid changes in Xrs2p, Dun1p, and Rfa2p that remove the preferred targets of the ATM family of protein kinases do not affect DNA repair or telomere length in Saccharomyces cerevisiae. DNA Repair (Amst) 2003; 2:1041 - 64; http://dx.doi.org/10.1016/S1568-7864(03)00115-0; PMID: 12967660
   PubMed Web of Science ®Google Scholar
• Abraham RT. Cell cycle checkpoint signaling through the ATM and ATR kinases. Genes Dev 2001; 15:2177 - 96; http://dx.doi.org/10.1101/gad.914401; PMID: 11544175
   PubMed Web of Science ®Google Scholar
• Cortez D, Wang Y, Qin J, Elledge SJ. Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 1999; 286:1162 - 6; http://dx.doi.org/10.1126/science.286.5442.1162; PMID: 10550055
   PubMed Web of Science ®Google Scholar
• O’Neill T, Dwyer AJ, Ziv Y, Chan DW, Lees-Miller SP, Abraham RH, Lai JH, Hill D, Shiloh Y, Cantley LC, et al. Utilization of oriented peptide libraries to identify substrate motifs selected by ATM. J Biol Chem 2000; 275:22719 - 27; http://dx.doi.org/10.1074/jbc.M001002200; PMID: 10801797
   PubMed Web of Science ®Google Scholar
• Kozlov SV, Graham ME, Peng C, Chen P, Robinson PJ, Lavin MF. Involvement of novel autophosphorylation sites in ATM activation. EMBO J 2006; 25:3504 - 14; http://dx.doi.org/10.1038/sj.emboj.7601231; PMID: 16858402
   PubMed Web of Science ®Google Scholar
• Yu Y, Mahaney BL, Yano K, Ye R, Fang S, Douglas P, Chen DJ, Lees-Miller SP. DNA-PK and ATM phosphorylation sites in XLF/Cernunnos are not required for repair of DNA double strand breaks. DNA Repair (Amst) 2008; 7:1680 - 92; http://dx.doi.org/10.1016/j.dnarep.2008.06.015; PMID: 18644470
   PubMed Web of Science ®Google Scholar
• Shim EY, Chung WH, Nicolette ML, Zhang Y, Davis M, Zhu Z, Paull TT, Ira G, Lee SE. Saccharomyces cerevisiae Mre11/Rad50/Xrs2 and Ku proteins regulate association of Exo1 and Dna2 with DNA breaks. EMBO J 2010; 29:3370 - 80; http://dx.doi.org/10.1038/emboj.2010.219; PMID: 20834227
   PubMed Web of Science ®Google Scholar
• Wohlbold L, Fisher RP. Behind the wheel and under the hood: functions of cyclin-dependent kinases in response to DNA damage. DNA Repair (Amst) 2009; 8:1018 - 24; http://dx.doi.org/10.1016/j.dnarep.2009.04.009; PMID: 19464967
   PubMed Web of Science ®Google Scholar
• Boulton SJ, Jackson SP. Identification of a Saccharomyces cerevisiae Ku80 homologue: roles in DNA double strand break rejoining and in telomeric maintenance. Nucleic Acids Res 1996; 24:4639 - 48; http://dx.doi.org/10.1093/nar/24.23.4639; PMID: 8972848
   PubMed Web of Science ®Google Scholar
• Siede W, Friedl AA, Dianova I, Eckardt-Schupp F, Friedberg EC. The Saccharomyces cerevisiae Ku autoantigen homologue affects radiosensitivity only in the absence of homologous recombination. Genetics 1996; 142:91 - 102; PMID: 8770587
   PubMed Web of Science ®Google Scholar
• Milne GT, Jin S, Shannon KB, Weaver DT. Mutations in two Ku homologs define a DNA end-joining repair pathway in Saccharomyces cerevisiae. Mol Cell Biol 1996; 16:4189 - 98; PMID: 8754818
   PubMed Web of Science ®Google Scholar
• Berkovich E, Monnat RJ Jr., Kastan MB. Assessment of protein dynamics and DNA repair following generation of DNA double-strand breaks at defined genomic sites. Nat Protoc 2008; 3:915 - 22; http://dx.doi.org/10.1038/nprot.2008.54; PMID: 18451799
   PubMed Web of Science ®Google Scholar
• Frank-Vaillant M, Marcand S. Transient stability of DNA ends allows nonhomologous end joining to precede homologous recombination. Mol Cell 2002; 10:1189 - 99; http://dx.doi.org/10.1016/S1097-2765(02)00705-0; PMID: 12453425
   PubMed Web of Science ®Google Scholar
• Fukushima T, Takata M, Morrison C, Araki R, Fujimori A, Abe M, Tatsumi K, Jasin M, Dhar PK, Sonoda E, et al. Genetic analysis of the DNA-dependent protein kinase reveals an inhibitory role of Ku in late S-G2 phase DNA double-strand break repair. J Biol Chem 2001; 276:44413 - 8; http://dx.doi.org/10.1074/jbc.M106295200; PMID: 11577093
   PubMed Web of Science ®Google Scholar
• Pierce AJ, Hu P, Han M, Ellis N, Jasin M. Ku DNA end-binding protein modulates homologous repair of double-strand breaks in mammalian cells. Genes Dev 2001; 15:3237 - 42; http://dx.doi.org/10.1101/gad.946401; PMID: 11751629
   PubMed Web of Science ®Google Scholar
• Karathanasis E, Wilson TE. Enhancement of Saccharomyces cerevisiae end-joining efficiency by cell growth stage but not by impairment of recombination. Genetics 2002; 161:1015 - 27; PMID: 12136007
   PubMed Web of Science ®Google Scholar
• Zhang Y, Shim EY, Davis M, Lee SE. Regulation of repair choice: Cdk1 suppresses recruitment of end joining factors at DNA breaks. DNA Repair (Amst) 2009; 8:1235 - 41; http://dx.doi.org/10.1016/j.dnarep.2009.07.007; PMID: 19699692
   PubMed Web of Science ®Google Scholar
• Lisby M, Barlow JH, Burgess RC, Rothstein R. Choreography of the DNA damage response: spatiotemporal relationships among checkpoint and repair proteins. Cell 2004; 118:699 - 713; http://dx.doi.org/10.1016/j.cell.2004.08.015; PMID: 15369670
   PubMed Web of Science ®Google Scholar
• Buis J, Stoneham T, Spehalski E, Ferguson DO. Mre11 regulates CtIP-dependent double-strand break repair by interaction with CDK2. Nat Struct Mol Biol 2012; 19:246 - 52; http://dx.doi.org/10.1038/nsmb.2212; PMID: 22231403
   PubMed Web of Science ®Google Scholar
• Brinkworth RI, Breinl RA, Kobe B. Structural basis and prediction of substrate specificity in protein serine/threonine kinases. Proc Natl Acad Sci U S A 2003; 100:74 - 9; http://dx.doi.org/10.1073/pnas.0134224100; PMID: 12502784
   PubMed Web of Science ®Google Scholar
• Rass E, Grabarz A, Plo I, Gautier J, Bertrand P, Lopez BS. Role of Mre11 in chromosomal nonhomologous end joining in mammalian cells. Nat Struct Mol Biol 2009; 16:819 - 24; http://dx.doi.org/10.1038/nsmb.1641; PMID: 19633668
   PubMed Web of Science ®Google Scholar
• Deriano L, Stracker TH, Baker A, Petrini JH, Roth DB. Roles for NBS1 in alternative nonhomologous end-joining of V(D)J recombination intermediates. Mol Cell 2009; 34:13 - 25; http://dx.doi.org/10.1016/j.molcel.2009.03.009; PMID: 19362533
   PubMed Web of Science ®Google Scholar
• Taylor EM, Cecillon SM, Bonis A, Chapman JR, Povirk LF, Lindsay HD. The Mre11/Rad50/Nbs1 complex functions in resection-based DNA end joining in Xenopus laevis. Nucleic Acids Res 2010; 38:441 - 54; http://dx.doi.org/10.1093/nar/gkp905; PMID: 19892829
   PubMed Web of Science ®Google Scholar
• St-Pierre J, Douziech M, Bazile F, Pascariu M, Bonneil E, Sauvé V, Ratsima H, D’Amours D. Polo kinase regulates mitotic chromosome condensation by hyperactivation of condensin DNA supercoiling activity. Mol Cell 2009; 34:416 - 26; http://dx.doi.org/10.1016/j.molcel.2009.04.013; PMID: 19481522
   PubMed Web of Science ®Google Scholar
• Roy MA, Siddiqui N, D’Amours D. Dynamic and selective DNA-binding activity of Smc5, a core component of the Smc5-Smc6 complex. Cell Cycle 2011; 10:690 - 700; http://dx.doi.org/10.4161/cc.10.4.14860; PMID: 21293191
   PubMed Web of Science ®Google Scholar
• Ratsima H, Ladouceur AM, Pascariu M, Sauvé V, Salloum Z, Maddox PS, D’Amours D. Independent modulation of the kinase and polo-box activities of Cdc5 protein unravels unique roles in the maintenance of genome stability. Proc Natl Acad Sci U S A 2011; 108:E914 - 23; http://dx.doi.org/10.1073/pnas.1106448108; PMID: 21987786
   PubMedGoogle Scholar
• Foiani M, Marini F, Gamba D, Lucchini G, Plevani P. The B subunit of the DNA polymerase alpha-primase complex in Saccharomyces cerevisiae executes an essential function at the initial stage of DNA replication. Mol Cell Biol 1994; 14:923 - 33; PMID: 8289832
   PubMed Web of Science ®Google Scholar
• Field J, Nikawa J, Broek D, MacDonald B, Rodgers L, Wilson IA, Lerner RA, Wigler M. Purification of a RAS-responsive adenylyl cyclase complex from Saccharomyces cerevisiae by use of an epitope addition method. Mol Cell Biol 1988; 8:2159 - 65; PMID: 2455217
   PubMed Web of Science ®Google Scholar
• Dosztányi Z, Csizmok V, Tompa P, Simon I. IUPred: web server for the prediction of intrinsically unstructured regions of proteins based on estimated energy content. Bioinformatics 2005; 21:3433 - 4; http://dx.doi.org/10.1093/bioinformatics/bti541; PMID: 15955779
   PubMed Web of Science ®Google Scholar