RNF4 regulates DNA double-strand break repair in a cell cycle-dependent manner

References

• Rothkamm K, Kruger I, Thompson LH, Lobrich M. Pathways of DNA double-strand break repair during the mammalian cell cycle. Mol Cell Biol 2003; 23:5706-15; PMID:12897142; http://dx.doi.org/10.1128/MCB.23.16.5706-5715.2003
   PubMed Web of Science ®Google Scholar
• Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 2012; 47:497-510; PMID:22920291; http://dx.doi.org/10.1016/j.molcel.2012.07.029
   PubMed Web of Science ®Google Scholar
• Bekker-Jensen S, Mailand N. The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett 2011; 585:2914-9; PMID:21664912; http://dx.doi.org/10.1016/j.febslet.2011.05.056
   PubMed Web of Science ®Google Scholar
• Ciccia A, Elledge SJ. The DNA damage response: making it safe to play with knives. Mol Cell 2010; 40:179-204; PMID:20965415; http://dx.doi.org/10.1016/j.molcel.2010.09.019
   PubMed Web of Science ®Google Scholar
• Polo SE, Jackson SP. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 2011; 25:409-33; PMID:21363960; http://dx.doi.org/10.1101/gad.2021311
   PubMed Web of Science ®Google Scholar
• Perry JJ, Tainer JA, Boddy MN. A SIM-ultaneous role for SUMO and ubiquitin. Trends Biochem Sci 2008; 33:201-8; PMID:18403209; http://dx.doi.org/10.1016/j.tibs.2008.02.001
   PubMed Web of Science ®Google Scholar
• Vyas R, Kumar R, Clermont F, Helfricht A, Kalev P, Sotiropoulou P, Hendriks IA, Radaelli E, Hochepied T, Blanpain C, et al. RNF4 is required for DNA double-strand break repair in vivo. Cell Death and Differ 2013; 20:490-502; PMID:23197296; http://dx.doi.org/10.1038/cdd.2012.145
   PubMed Web of Science ®Google Scholar
• Poulsen SL, Hansen RK, Wagner SA, van Cuijk L, van Belle GJ, Streicher W, Wikstrom M, Choudhary C, Houtsmuller AB, Marteijn JA, et al. RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J Cell Biol 2013; 201:797-807; PMID:23751493; http://dx.doi.org/10.1083/jcb.201212075
   PubMed Web of Science ®Google Scholar
• Yin Y, Seifert A, Chua JS, Maure JF, Golebiowski F, Hay RT. SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev 2012; 26:1196-208; PMID:3371408; http://dx.doi.org/10.1101/gad.189274.112
   PubMed Web of Science ®Google Scholar
• Luo KT, Zhang HX, Wang LW, Yuan J, Lou ZK. Sumoylation of MDC1 is important for proper DNA damage response. EMBO J 2012; 31:3008-19; PMID:22635276; http://dx.doi.org/10.1038/emboj.2012.158
   PubMed Web of Science ®Google Scholar
• Guzzo CM, Berndsen CE, Zhu J, Gupta V, Datta A, Greenberg RA, Wolberger C, Matunis MJ. RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci Signal 2012; 5:ra88; PMID:23211528; http://dx.doi.org/10.1126/scisignal.2003485
   PubMed Web of Science ®Google Scholar
• Galanty Y, Belotserkovskaya R, Coates J, Jackson SP. RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev 2012; 26:1179-95; PMID:3371407; http://dx.doi.org/10.1101/gad.188284.112
   PubMed Web of Science ®Google Scholar
• Kuo C-Y, Li X, Kong X-Q, Luo C, Chang C-C, Chung Y, Shih H-M, Li KK, Ann DK. An arginine-rich motif of ring finger protein 4 (RNF4) oversees the recruitment and degradation of the phosphorylated and SUMOylated KAP1/TRIM28 during genotoxic stress. J Biol Chem 2014; 289(30):20757-72; PMID:24907272; http://dx.doi.org/10.1074/jbc.M114.555672
   PubMed Web of Science ®Google Scholar
• Gibbs-Seymour I, Oka Y, Rajendra E, Weinert Brian T, Passmore Lori A, Patel Ketan J, Olsen Jesper V, Choudhary C, Bekker-Jensen S, Mailand N. Ubiquitin-SUMO circuitry controls activated fanconi anemia ID complex dosage in response to DNA damage. Mol Cell 2015; 57:150-64; PMID:25557546; http://dx.doi.org/10.1016/j.molcel.2014.12.001
   PubMed Web of Science ®Google Scholar
• Xie J, Kim H, Moreau LA, Puhalla S, Garber J, Al Abo M, Takeda S, D'Andrea AD. RNF4-mediated polyubiquitination regulates the Fanconi anemia/BRCA pathway. J Clin Invest 2015; 125:1523-32; PMID:25751062; http://dx.doi.org/10.1172/JCI79325
   PubMed Web of Science ®Google Scholar
• Luo K, Deng M, Li Y, Wu C, Xu Z, Yuan J, Lou Z. CDK-mediated RNF4 phosphorylation regulates homologous recombination in S-phase. Nucleic Acids Res 2015; 43:5465-75; PMID:25948581; http://dx.doi.org/10.1093/nar/gkv434
   PubMed Web of Science ®Google Scholar
• Cheng C-T, Kuo C-Y, Ann DK. KAPtain in charge of multiple missions: Emerging roles of KAP1. World J Biol Chem 2014; 5:308-20; PMID:25225599; http://dx.doi.org/10.4331/wjbc.v5.i3.308
   PubMedGoogle Scholar
• White DE, Negorev D, Peng H, Ivanov AV, Maul GG, Rauscher FJ, 3rd. KAP1, a novel substrate for PIKK family members, colocalizes with numerous damage response factors at DNA lesions. Cancer Res 2006; 66:11594-9; PMID:17178852; http://dx.doi.org/10.1158/0008-5472.CAN-06-4138
   PubMed Web of Science ®Google Scholar
• Ziv Y, Bielopolski D, Galanty Y, Lukas C, Taya Y, Schultz DC, Lukas J, Bekker-Jensen S, Bartek J, Shiloh Y. Chromatin relaxation in response to DNA double-strand breaks is modulated by a novel ATM and KAP-1 dependent pathway. Nat Cell Biol 2006; 8:870-U142; PMID:16862143; http://dx.doi.org/10.1038/ncb1446
   PubMed Web of Science ®Google Scholar
• Goodarzi AA, Noon AT, Deckbar D, Ziv Y, Shiloh Y, Lobrich M, Jeggo PA. ATM signaling facilitates repair of DNA double-strand breaks associated with heterochromatin. Mol Cell 2008; 31:167-77; PMID:18657500; http://dx.doi.org/10.1016/j.molcel.2008.05.017
   PubMed Web of Science ®Google Scholar
• Noon AT, Shibata A, Rief N, Lobrich M, Stewart GS, Jeggo PA, Goodarzi AA. 53BP1-dependent robust localized KAP-1 phosphorylation is essential for heterochromatic DNA double-strand break repair. Nat Cell Biol 2010; 12:177-84; PMID:20081839; http://dx.doi.org/10.1038/ncb2017
   PubMed Web of Science ®Google Scholar
• Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, Goodarzi AA, Krempler A, Jeggo PA, Lobrich M. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J 2009; 28:3413-27; PMID:2752027; http://dx.doi.org/10.1038/emboj.2009.276
   PubMed Web of Science ®Google Scholar
• Shibata A, Conrad S, Birraux J, Geuting V, Barton O, Ismail A, Kakarougkas A, Meek K, Taucher-Scholz G, Lobrich M, et al. Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J 2011; 30:1079-92; PMID:3061033; http://dx.doi.org/10.1038/emboj.2011.27
   PubMed Web of Science ®Google Scholar
• Kakarougkas A, Ismail A, Klement K, Goodarzi AA, Conrad S, Freire R, Shibata A, Lobrich M, Jeggo PA. Opposing roles for 53BP1 during homologous recombination. Nucleic Acids Res 2013; 41:9719-31; PMID:23969417; http://dx.doi.org/10.1093/nar/gkt729
   PubMed Web of Science ®Google Scholar
• Goodarzi AA, Noon AT, Jeggo P. The impact of heterochromatin on DSB repair. Biochem Soc Trans 2009; 37:569-76; PMID:19442252; http://dx.doi.org/10.1042/BST0370569
   PubMed Web of Science ®Google Scholar
• Pagano M, Pepperkok R, Verde F, Ansorge W, Draetta G. Cyclin A is required at two points in the human cell cycle. EMBO J 1992; 11:961-71; PMID:1312467
   PubMed Web of Science ®Google Scholar
• Chou TF, Brown SJ, Minond D, Nordin BE, Li K, Jones AC, Chase P, Porubsky PR, Stoltz BM, Schoenen FJ, et al. Reversible inhibitor of p97, DBeQ, impairs both ubiquitin-dependent and autophagic protein clearance pathways. Proc Natl Acad Sci U S A 2011; 108:4834-9; PMID:21383145; http://dx.doi.org/10.1073/pnas.1015312108
   PubMed Web of Science ®Google Scholar
• Bennardo N, Cheng A, Huang N, Stark JM. Alternative-NHEJ is a mechanistically distinct pathway of mammalian chromosome break repair. PLoS Genet 2008; 4:e1000110; PMID:18584027; http://dx.doi.org/10.1371/journal.pgen.1000110
   PubMed Web of Science ®Google Scholar
• Huertas P. DNA resection in eukaryotes: deciding how to fix the break. Nat Struct Mol Biol 2010; 17:11-6; PMID:20051983; http://dx.doi.org/10.1038/nsmb.1710
   PubMed Web of Science ®Google Scholar
• Forment JV, Walker RV, Jackson SP. A high-throughput, flow cytometry-based method to quantify DNA-end resection in mammalian cells. Cytometry Part A 2012; 81A:922-8; PMID:22893507; http://dx.doi.org/10.1002/cyto.a.22155
   PubMed Web of Science ®Google Scholar
• Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. Human CtIP promotes DNA end resection. Nature 2007; 450:509-14; PMID:17965729; http://dx.doi.org/10.1038/nature06337
   PubMed Web of Science ®Google Scholar
• Forget AL, Kowalczykowski SC. Single-molecule imaging brings Rad51 nucleoprotein filaments into focus. Trends Cell Biol 2010; 20:269-76; PMID:2862779; http://dx.doi.org/10.1016/j.tcb.2010.02.004
   PubMed Web of Science ®Google Scholar
• Haaf T, Golub EI, Reddy G, Radding CM, Ward DC. Nuclear foci of mammalian Rad51 recombination protein in somatic cells after DNA damage and its localization in synaptonemal complexes. Proc Natl Acad Sci U S A 1995; 92:2298-302; PMID:7892263
   PubMed Web of Science ®Google Scholar
• Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 2000; 10:886-95; PMID:10959836; http://dx.doi.org/10.1016/S0960-9822(00)00610-2
   PubMed Web of Science ®Google Scholar
• Lin Y-H, Yuan J, Pei H, Liu T, Ann DK, Lou Z. KAP1 Deacetylation by SIRT1 Promotes Non-Homologous End-Joining Repair. PLoS ONE 2015; 10:e0123935; PMID:25905708; http://dx.doi.org/10.1371/journal.pone.0123935
   PubMedGoogle Scholar
• Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141:243-54; PMID:20362325; http://dx.doi.org/10.1016/j.cell.2010.03.012
   PubMed Web of Science ®Google Scholar
• Chapman JR, Barral P, Vannier JB, Borel V, Steger M, Tomas-Loba A, Sartori AA, Adams IR, Batista FD, Boulton SJ. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell 2013; 49:858-71; PMID:23333305; http://dx.doi.org/10.1016/j.molcel.2013.01.002
   PubMed Web of Science ®Google Scholar
• Escribano-Diaz C, Orthwein A, Fradet-Turcotte A, Xing M, Young JT, Tkac J, Cook MA, Rosebrock AP, Munro M, Canny MD, et al. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell 2013; 49:872-83; PMID:23333306; http://dx.doi.org/10.1016/j.molcel.2013.01.001
   PubMed Web of Science ®Google Scholar
• Ryan RF, Schultz DC, Ayyanathan K, Singh PB, Friedman JR, Fredericks WJ, Rauscher FJ, 3rd. KAP-1 corepressor protein interacts and colocalizes with heterochromatic and euchromatic HP1 proteins: a potential role for Kruppel-associated box-zinc finger proteins in heterochromatin-mediated gene silencing. Mol Cell Biol 1999; 19:4366-78; PMID:10330177; http://dx.doi.org/10.1128/MCB.19.6.4366
   PubMed Web of Science ®Google Scholar
• Baldeyron C, Soria G, Roche D, Cook AJ, Almouzni G. HP1alpha recruitment to DNA damage by p150CAF-1 promotes homologous recombination repair. J Cell Biol 2011; 193:81-95; PMID:3082177; http://dx.doi.org/10.1083/jcb.201101030
   PubMed Web of Science ®Google Scholar
• White D, Rafalska-Metcalf IU, Ivanov AV, Corsinotti A, Peng H, Lee SC, Trono D, Janicki SM, Rauscher FJ, 3rd. The ATM substrate KAP1 controls DNA repair in heterochromatin: regulation by HP1 proteins and serine 473/824 phosphorylation. Mol Cancer Res 2012; 10:401-14; PMID:22205726; http://dx.doi.org/10.1158/1541-7786.MCR-11-0134
   PubMed Web of Science ®Google Scholar
• Soria G, Almouzni G. Differential contribution of HP1 proteins to DNA end resection and homology-directed repair. Cell Cycle 2013; 12:422-9; PMID:23287531; http://dx.doi.org/10.4161/cc.23215
   PubMed Web of Science ®Google Scholar
• Lee YH, Kuo CY, Stark JM, Shih HM, Ann DK. HP1 promotes tumor suppressor BRCA1 functions during the DNA damage response. Nucleic Acids Res 2013; 41:5784-98; PMID:23589625; http://dx.doi.org/10.1093/nar/gkt231
   PubMed Web of Science ®Google Scholar
• Ragland RL, Patel S, Rivard RS, Smith K, Peters AA, Bielinsky AK, Brown EJ. RNF4 and PLK1 are required for replication fork collapse in ATR-deficient cells. Genes Dev 2013; 27:2259-73; PMID:24142876; http://dx.doi.org/10.1101/gad.223180.113
   PubMed Web of Science ®Google Scholar
• Davis EJ, Lachaud C, Appleton P, Macartney TJ, Näthke I, Rouse J. DVC1 (C1orf124) recruits the p97 protein segregase to sites of DNA damage. Nat Struct Mol Biol 2012; 19:1093-100; PMID:23042607; http://dx.doi.org/10.1038/nsmb.2394
   PubMed Web of Science ®Google Scholar
• Meerang M, Ritz D, Paliwal S, Garajova Z, Bosshard M, Mailand N, Janscak P, Hubscher U, Meyer H, Ramadan K. The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat Cell Biol 2011; 13:1376-82; PMID:22020440; http://dx.doi.org/10.1038/ncb2367
   PubMed Web of Science ®Google Scholar
• Mosbech A, Gibbs-Seymour I, Kagias K, Thorslund T, Beli P, Povlsen L, Nielsen SV, Smedegaard S, Sedgwick G, Lukas C, et al. DVC1 (C1orf124) is a DNA damage–targeting p97 adaptor that promotes ubiquitin-dependent responses to replication blocks. Nat Struct Mol Biol 2012; 19:1084-92; PMID:23042605; http://dx.doi.org/10.1038/nsmb.2395
   PubMed Web of Science ®Google Scholar
• Nie M, Aslanian A, Prudden J, Heideker J, Vashisht AA, Wohlschlegel JA, Yates JR, 3rd, Boddy MN. Dual recruitment of Cdc48 (p97)-Ufd1-Npl4 ubiquitin-selective segregase by small ubiquitin-like modifier protein (SUMO) and ubiquitin in SUMO-targeted ubiquitin ligase-mediated genome stability functions. J Biol Chem 2012; 287:29610-9; PMID:22730331; http://dx.doi.org/10.1074/jbc.M112.379768
   PubMed Web of Science ®Google Scholar
• Kalousi A, Hoffbeck A-S, Selemenakis Platonas N, Pinder J, Savage Kienan I, Khanna Kum K, Brino L, Dellaire G, Gorgoulis Vassilis G, Soutoglou E. The Nuclear Oncogene SET Controls DNA Repair by KAP1 and HP1 Retention to Chromatin. Cell Rep 2015; 11:149-63; PMID:25818296; http://dx.doi.org/10.1016/j.celrep.2015.03.005
   PubMed Web of Science ®Google Scholar
• Liu JP, Xu LL, Zhong JN, Liao J, Li J, Xu XZ. Protein phosphatase PP4 is involved in NHEJ-mediated repair of DNA double-strand breaks. Cell Cycle 2012; 11:2643-9; PMID:22732494; http://dx.doi.org/10.4161/cc.20957
   PubMed Web of Science ®Google Scholar
• Messerschmidt DM, de Vries W, Ito M, Solter D, Ferguson-Smith A, Knowles BB. Trim28 is required for epigenetic stability during mouse oocyte to embryo transition. Science 2012; 335:1499-502; PMID:22442485; http://dx.doi.org/10.1126/science.1216154
   PubMed Web of Science ®Google Scholar
• Santoni de Sio FR, Massacand J, Barde I, Offner S, Corsinotti A, Kapopoulou A, Bojkowska K, Dagklis A, Fernandez M, Ghia P, et al. KAP1 regulates gene networks controlling mouse B-lymphoid cell differentiation and function. Blood 2012; 119:4675-85; PMID:22452978; http://dx.doi.org/10.1182/blood-2011-12-401117
   PubMed Web of Science ®Google Scholar
• Santoni de Sio FR, Barde I, Offner S, Kapopoulou A, Corsinotti A, Bojkowska K, Genolet R, Thomas JH, Luescher IF, Pinschewer D, et al. KAP1 regulates gene networks controlling T-cell development and responsiveness. FASEB J 2012; 26:4561-75; PMID:22872677; http://dx.doi.org/10.1096/fj.12-206177
   PubMed Web of Science ®Google Scholar
• Hakli M, Karvonen U, Janne OA, Palvimo JJ. SUMO-1 promotes association of SNURF (RNF4) with PML nuclear bodies. Exp Cell Res 2005; 304:224-33; PMID:15707587; http://dx.doi.org/10.1016/j.yexcr.2004.10.029
   PubMed Web of Science ®Google Scholar
• Nguyen HV, Chen JL, Zhong J, Kim KJ, Crandall ED, Borok Z, Chen Y, Ann DK. SUMOylation attenuates sensitivity toward hypoxia- or desferroxamine-induced injury by modulating adaptive responses in salivary epithelial cells. Am J Pathol 2006; 168:1452-63; PMID:16651613; http://dx.doi.org/10.2353/ajpath.2006.050782
   PubMed Web of Science ®Google Scholar