Ubiquitin-H2AX fusions render 53BP1 recruitment to DNA damage sites independent of RNF8 or RNF168

References

• Featherstone C, Jackson SP. DNA double-strand break repair. Curr Biol 1999; 9:R759-61; PMID:10531043; http://dx.doi.org/10.1016/S0960-9822(00)80005-6
   PubMed Web of Science ®Google Scholar
• Valerie K, Povirk LF. Regulation and mechanisms of mammalian double-strand break repair. Oncogene 2003; 22:5792-812; PMID:12947387; http://dx.doi.org/10.1038/sj.onc.1206679
   PubMed Web of Science ®Google Scholar
• Shiloh Y. ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 2003; 3:155-68; PMID:12612651; http://dx.doi.org/10.1038/nrc1011
   PubMed Web of Science ®Google Scholar
• Kastan MB, Bartek J. Cell-cycle checkpoints and cancer. Nature 2004; 432:316-23; PMID:15549093; http://dx.doi.org/10.1038/nature03097
   PubMed Web of Science ®Google Scholar
• Halazonetis TD, Gorgoulis VG, Bartek J. An oncogene-induced DNA damage model for cancer development. Science 2008; 319:1352-5; PMID:18323444; http://dx.doi.org/10.1126/science.1140735
   PubMed Web of Science ®Google Scholar
• DiTullio RA, Jr., Mochan TA, Venere M, Bartkova J, Sehested M, Bartek J, Halazonetis TD. 53BP1 functions in an ATM-dependent checkpoint pathway that is constitutively activated in human cancer. Nat Cell Biol 2002; 4:998-1002; PMID:12447382; http://dx.doi.org/10.1038/ncb892
   PubMed Web of Science ®Google Scholar
• Ward IM, Reina-San-Martin B, Olaru A, Minn K, Tamada K, Lau JS, Cascalho M, Chen L, Nussenzweig A, Livak F, et al. 53BP1 is required for class switch recombination. J Cell Biol 2004; 165:459-64; PMID:15159415; http://dx.doi.org/10.1083/jcb.200403021
   PubMed Web of Science ®Google Scholar
• Zgheib O, Huyen Y, DiTullio RA, Jr., Snyder A, Venere M, Stavridi ES, Halazonetis TD. ATM signaling and 53BP1. Radiother Oncol 2005; 76:119-22; PMID:16024119; http://dx.doi.org/10.1016/j.radonc.2005.06.026
   PubMed Web of Science ®Google Scholar
• Difilippantonio S, Gapud E, Wong N, Huang CY, Mahowald G, Chen HT, Kruhlak MJ, Callen E, Livak F, Nussenzweig MC, et al. 53BP1 facilitates long-range DNA end-joining during V(D)J recombination. Nature 2008; 456:529-33; PMID:18931658; http://dx.doi.org/10.1038/nature07476
   PubMed Web of Science ®Google Scholar
• Fitzgerald JE, Grenon M, Lowndes NF. 53BP1: function and mechanisms of focal recruitment. Biochem Soc Trans 2009; 37:897-904; PMID:19614615; http://dx.doi.org/10.1042/BST0370897
   PubMed Web of Science ®Google Scholar
• Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, et al. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 2010; 17:688-95; PMID:20453858; http://dx.doi.org/10.1038/nsmb.1831
   PubMed Web of Science ®Google 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
• Bunting SF, Callen E, Kozak ML, Kim JM, Wong N, Lopez-Contreras AJ, Ludwig T, Baer R, Faryabi RB, Malhowski A, et al. BRCA1 functions independently of homologous recombination in DNA interstrand crosslink repair. Mol Cell 2012; 46:125-35; PMID:22445484; http://dx.doi.org/10.1016/j.molcel.2012.02.015
   PubMed Web of Science ®Google Scholar
• Chapman JR, Sossick AJ, Boulton SJ, Jackson SP. BRCA1-associated exclusion of 53BP1 from DNA damage sites underlies temporal control of DNA repair. J Cell Sci 2012; PMID:22553214
   PubMed Web of Science ®Google Scholar
• Cescutti R, Negrini S, Kohzaki M, Halazonetis TD. TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint. EMBO J 2010; 29:3723-32; PMID:20871591; http://dx.doi.org/10.1038/emboj.2010.238
   PubMed Web of Science ®Google Scholar
• Iwabuchi K, Basu BP, Kysela B, Kurihara T, Shibata M, Guan D, Cao Y, Hamada T, Imamura K, Jeggo PA, et al. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J Biol Chem 2003; 278:36487-95; PMID:12824158; http://dx.doi.org/10.1074/jbc.M304066200
   PubMed Web of Science ®Google Scholar
• Ward IM, Minn K, Jorda KG, Chen J. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J Biol Chem 2003; 278:19579-82; PMID:12697768; http://dx.doi.org/10.1074/jbc.C300117200
   PubMed Web of Science ®Google Scholar
• Huyen Y, Zgheib O, Ditullio RA, Jr., Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004; 432:406-11; PMID:15525939; http://dx.doi.org/10.1038/nature03114
   PubMed Web of Science ®Google Scholar
• Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, Mer G. Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 2006; 127:1361-73; PMID:17190600
   PubMed Web of Science ®Google Scholar
• Schotta G, Sengupta R, Kubicek S, Malin S, Kauer M, Callen E, Celeste A, Pagani M, Opravil S, De La Rosa-Velazquez IA, et al. A chromatin-wide transition to H4K20 monomethylation impairs genome integrity and programmed DNA rearrangements in the mouse. Genes Dev 2008; 22:2048-61; PMID:18676810; http://dx.doi.org/10.1101/gad.476008
   PubMed Web of Science ®Google Scholar
• Hartlerode AJ, Guan Y, Rajendran A, Ura K, Schotta G, Xie A, Shah JV, Scully R. Impact of histone H4 lysine 20 methylation on 53BP1 responses to chromosomal double strand breaks. PloS One 2012; 7:e49211; PMID:23209566
   PubMed Web of Science ®Google Scholar
• Wakeman TP, Wang Q, Feng J, Wang XF. Bat3 facilitates H3K79 dimethylation by DOT1L and promotes DNA damage-induced 53BP1 foci at G1/G2 cell-cycle phases. EMBO J 2012; 31:2169-81; PMID:22373577; http://dx.doi.org/10.1038/emboj.2012.50
   PubMed Web of Science ®Google Scholar
• Stucki M, Jackson SP. Tudor domains track down DNA breaks. Nat Cell Biol 2004; 6:1150-2; PMID:15573092; http://dx.doi.org/10.1038/ncb1204-1150
   PubMed Web of Science ®Google Scholar
• Zgheib O, Pataky K, Brugger J, Halazonetis TD. An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks. Mol Cell Biol 2009; 29:1050-8; PMID:19064641; http://dx.doi.org/10.1128/MCB.01011-08
   PubMed Web of Science ®Google Scholar
• Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N, et al. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat Cell Biol 2002; 4:993-7; PMID:12447390; http://dx.doi.org/10.1038/ncb884
   PubMed Web of Science ®Google Scholar
• Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ. MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 2003; 421:961-6; PMID:12607005; http://dx.doi.org/10.1038/nature01446
   PubMed Web of Science ®Google Scholar
• Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007; 131:901-14; PMID:18001825; http://dx.doi.org/10.1016/j.cell.2007.09.041
   PubMed Web of Science ®Google Scholar
• Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM, et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 2007; 318:1637-40; PMID:18006705; http://dx.doi.org/10.1126/science.1150034
   PubMed Web of Science ®Google Scholar
• Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007; 131:887-900; PMID:18001824; http://dx.doi.org/10.1016/j.cell.2007.09.040
   PubMed Web of Science ®Google Scholar
• Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136:435-46; PMID:19203579; http://dx.doi.org/10.1016/j.cell.2008.12.041
   PubMed Web of Science ®Google Scholar
• Pinato S, Scandiuzzi C, Arnaudo N, Citterio E, Gaudino G, Penengo L. RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX. BMC Mol Biol 2009; 10:55; PMID:19500350; http://dx.doi.org/10.1186/1471-2199-10-55
   PubMed Web of Science ®Google Scholar
• Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, Nakada S, Ylanko J, Olivarius S, Mendez M, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136:420-34; PMID:19203578; http://dx.doi.org/10.1016/j.cell.2008.12.042
   PubMed Web of Science ®Google Scholar
• Moudry P, Lukas C, Macurek L, Hanzlikova H, Hodny Z, Lukas J, Bartek J. Ubiquitin-activating enzyme UBA1 is required for cellular response to DNA damage. Cell Cycle 2012 11:1573-82; PMID:22456334; http://dx.doi.org/10.4161/cc.19978
   PubMed Web of Science ®Google Scholar
• Helchowski CM, Skow LF, Roberts KH, Chute CL, Canman CE. A small ubiquitin binding domain inhibits ubiquitin-dependent protein recruitment to DNA repair foci. Cell Cycle 2013 12:3749-58; PMID:24107634; http://dx.doi.org/10.4161/cc.26640
   PubMed Web of Science ®Google Scholar
• Acs K, Luijsterburg MS, Ackermann L, Salomons FA, Hoppe T, Dantuma NP. The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat Struct Mol Biol 2011; 18:1345-50; PMID:22120668; http://dx.doi.org/10.1038/nsmb.2188
   PubMed Web of Science ®Google Scholar
• Mallette FA, Mattiroli F, Cui G, Young LC, Hendzel MJ, Mer G, Sixma TK, Richard S. RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J 2012; 31:1865-78; PMID:22373579; http://dx.doi.org/10.1038/emboj.2012.47
   PubMed Web of Science ®Google Scholar
• Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H, Landry MC, Kitevski-LeBlanc J, Noordermeer SM, Sicheri F, et al. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 2013; 499:50-4; PMID:23760478; http://dx.doi.org/10.1038/nature12318
   PubMed Web of Science ®Google Scholar
• Gatti M, Pinato S, Maspero E, Soffientini P, Polo S, Penengo L. A novel ubiquitin mark at the N-terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle 2012; 11:2538-44; PMID:22713238; http://dx.doi.org/10.4161/cc.20919
   PubMed Web of Science ®Google Scholar
• Mattiroli F, Vissers JH, van Dijk WJ, Ikpa P, Citterio E, Vermeulen W, Marteijn JA, Sixma TK. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 2012; 150:1182-95; PMID:22980979
   PubMed Web of Science ®Google Scholar
• Sharma N, Zhu Q, Wani G, He J, Wang QE, Wani AA. USP3 counteracts RNF168 via deubiquitinating H2A and γH2AX at lysine 13 and 15. Cell Cycle 2014; 13:106-14; PMID:24196443; http://dx.doi.org/10.4161/cc.26814
   PubMed Web of Science ®Google Scholar
• Dikic I, Wakatsuki S, Walters KJ. Ubiquitin-binding domains - from structures to functions. Nat Rev Mol Cell Biol 2009; 10:659-71; PMID:19773779; http://dx.doi.org/10.1038/nrm2767
   PubMed Web of Science ®Google Scholar
• Stewart GS, Stankovic T, Byrd PJ, Wechsler T, Miller ES, Huissoon A, Drayson MT, West SC, Elledge SJ, Taylor AM. RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc Natl Acad Sci U S A 2007; 104:16910-5; PMID:17940005; http://dx.doi.org/10.1073/pnas.0708408104
   PubMed Web of Science ®Google Scholar
• Dantuma NP, Groothuis TA, Salomons FA, Neefjes J. A dynamic ubiquitin equilibrium couples proteasomal activity to chromatin remodeling. J Cell Biol 2006; 173:19-26; PMID:16606690; http://dx.doi.org/10.1083/jcb.200510071
   PubMed Web of Science ®Google Scholar
• Stock JK, Giadrossi S, Casanova M, Brookes E, Vidal M, Koseki H, Brockdorff N, Fisher AG, Pombo A. Ring1-mediated ubiquitination of H2A restrains poised RNA polymerase II at bivalent genes in mouse ES cells. Nat Cell Biol 2007; 9:1428-35; PMID:18037880; http://dx.doi.org/10.1038/ncb1663
   PubMed Web of Science ®Google Scholar
• Zhu Q, Pao GM, Huynh AM, Suh H, Tonnu N, Nederlof PM, Gage FH, Verma IM. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011; 477:179-84; PMID:21901007; http://dx.doi.org/10.1038/nature10371
   PubMed Web of Science ®Google Scholar
• Callen E, Di Virgilio M, Kruhlak MJ, Nieto-Soler M, Wong N, Chen HT, Faryabi RB, Polato F, Santos M, Starnes LM, et al. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 2013; 153:1266-80; PMID:23727112; http://dx.doi.org/10.1016/j.cell.2013.05.023
   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
• Di Virgilio M, Callen E, Yamane A, Zhang W, Jankovic M, Gitlin AD, Feldhahn N, Resch W, Oliveira TY, Chait BT, et al. Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 2013; 339:711-5; PMID:23306439; http://dx.doi.org/10.1126/science.1230624
   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
• Zimmermann M, Lottersberger F, Buonomo SB, Sfeir A, de Lange T. 53BP1 regulates DSB repair using Rif1 to control 5' end resection. Science 2013; 339:700-4; PMID:23306437; http://dx.doi.org/10.1126/science.1231573
   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
   PubMed Web of Science ®Google Scholar
• Hu X, Paul A, Wang B. Rap80 protein recruitment to DNA double-strand breaks requires binding to both small ubiquitin-like modifier (SUMO) and ubiquitin conjugates. J Biol Chem 2012; 287:25510-9; PMID:22689573; http://dx.doi.org/10.1074/jbc.M112.374116
   PubMed Web of Science ®Google Scholar
• Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007; 316:1202-5; PMID:17525342; http://dx.doi.org/10.1126/science.1139621
   PubMed Web of Science ®Google Scholar
• Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, Livingston DM, Greenberg RA. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007; 316:1198-202; PMID:17525341; http://dx.doi.org/10.1126/science.1139516
   PubMed Web of Science ®Google Scholar
• Wang B, Elledge SJ. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci U S A 2007; 104:20759-63; PMID:18077395; http://dx.doi.org/10.1073/pnas.0710061104
   PubMed Web of Science ®Google Scholar
• Yan J, Kim YS, Yang XP, Li LP, Liao G, Xia F, Jetten AM. The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res 2007; 67:6647-56; PMID:17621610; http://dx.doi.org/10.1158/0008-5472.CAN-07-0924
   PubMed Web of Science ®Google Scholar
• Hsiao KY, Mizzen CA. Histone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair. J Mol Cell Biol 2013; 5:157-65; PMID:23329852; http://dx.doi.org/10.1093/jmcb/mjs066
   PubMed Web of Science ®Google Scholar
• Tang J, Cho NW, Cui G, Manion EM, Shanbhag NM, Botuyan MV, Mer G, Greenberg RA. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 2013; 20:317-25; PMID:23377543; http://dx.doi.org/10.1038/nsmb.2499
   PubMed Web of Science ®Google Scholar
• Panier S, Boulton SJ. Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 2014; 15:7-18; PMID:24326623; http://dx.doi.org/10.1038/nrm3719
   PubMed Web of Science ®Google Scholar
• Fierz B, Chatterjee C, McGinty RK, Bar-Dagan M, Raleigh DP, Muir TW. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat Chem Biol 2011; 7:113-9; PMID:21196936; http://dx.doi.org/10.1038/nchembio.501
   PubMed Web of Science ®Google Scholar
• Dhall A, Wei S, Fierz B, Woodcock CL, Lee TH, Chatterjee C. Sumoylated human histone H4 prevents chromatin compaction by inhibiting long-range internucleosomal interactions. J Biol Chem 2014; PMID:25294883
   PubMed Web of Science ®Google Scholar
• Watanabe S, Watanabe K, Akimov V, Bartkova J, Blagoev B, Lukas J, Bartek J. JMJD1C demethylates MDC1 to regulate the RNF8 and BRCA1-mediated chromatin response to DNA breaks. Nat Struct Mol Biol 2013; 20:1425-33; PMID:24240613; http://dx.doi.org/10.1038/nsmb.2702
   PubMed Web of Science ®Google Scholar
• Stucki M, Jackson SP. gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair 2006; 5:534-43; PMID:16531125; http://dx.doi.org/10.1016/j.dnarep.2006.01.012
   PubMed Web of Science ®Google Scholar
• Xu Y, Sun Y, Jiang X, Ayrapetov MK, Moskwa P, Yang S, Weinstock DM, Price BD. The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol 2010; 191:31-43; PMID:20876283; http://dx.doi.org/10.1083/jcb.201001160
   PubMed Web of Science ®Google Scholar
• Hammet A, Magill C, Heierhorst J, Jackson SP. Rad9 BRCT domain interaction with phosphorylated H2AX regulates the G1 checkpoint in budding yeast. EMBO Rep 2007; 8:851-7; PMID:17721446; http://dx.doi.org/10.1038/sj.embor.7401036
   PubMed Web of Science ®Google Scholar
• Sofueva S, Du LL, Limbo O, Williams JS, Russell P. BRCT domain interactions with phospho-histone H2A target Crb2 to chromatin at double-strand breaks and maintain the DNA damage checkpoint. Mol Cell Biol 2010; 30:4732-43; PMID:20679485; http://dx.doi.org/10.1128/MCB.00413-10
   PubMed Web of Science ®Google Scholar
• Schultz LB, Chehab NH, Malikzay A, Halazonetis TD. p53 binding protein 1 (53BP1) is an early participant in the cellular response to DNA double-strand breaks. J Cell Biol 2000; 151:1381-90; PMID:11134068; http://dx.doi.org/10.1083/jcb.151.7.1381
   PubMed Web of Science ®Google Scholar
• Wu J, Chen Y, Lu LY, Wu Y, Paulsen MT, Ljungman M, Ferguson DO, Yu X. Chfr and RNF8 synergistically regulate ATM activation. Nat Struct Mol Biol 2011; 18:761-8; PMID:21706008; http://dx.doi.org/10.1038/nsmb.2078
   PubMed Web of Science ®Google Scholar