Molecular Life Sciences

Living Edition
| Editors: Robert D. Wells, Judith S. Bond, Judith Klinman, Bettie Sue Siler Masters, Ellis Bell

Regulation of DSB Repair by Cell Cycle Signaling and the DNA Damage Response

Living reference work entry


Of the many types of DNA lesions, DNA double-strand breaks (DSBs) are considered the most harmful, because one unrepaired DSB is sufficient to trigger permanent growth arrest and cell death. In addition, DSBs are potent inducers of gross chromosomal rearrangements such as deletions, translocations, and amplifications. DSB signaling and repair through different pathways is crucial to preserve genomic integrity and maintain cellular homeostasis. Therefore, it is no wonder if the cell finely regulates DSB repair pathways in the different cell cycle phases and following activation of the DNA damage checkpoint. In this short entry we will illustrate some known aspects of the regulation of DSB repair in the mitotic cell cycle. In particular we will focus on the balance of the two main DSB repair pathways – NHEJ, nonhomologous end joining, and H(D)R, homologous (directed) recombination – as well as on the regulation of the resolution of joint molecules that arise during H(D)R.



Nucleoprotein Filament Mre11 Complex Strand Exchange Reaction Nucleolytic Processing Cell Cycle Regulatory Network 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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  1. Ahnesorg P, Jackson SP (2007) The non-homologous end-joining protein Nej1p is a target of the DNA damage checkpoint. DNA Repair (Amst) 6:190–201CrossRefGoogle Scholar
  2. Altmannova V, Eckert-Boulet N, Arneric M, Kolesar P, Chaloupkova R, Damborsky J, Sung P, Zhao X, Lisby M, Krejci L (2010) Rad52 SUMOylation affects the efficiency of the DNA repair. Nucleic Acids Res 38:4708–4721PubMedCentralPubMedCrossRefGoogle Scholar
  3. Ammazzalorso F, Pirzio LM, Bignami M, Franchitto A, Pichierri P (2010) ATR and ATM differently regulate WRN to prevent DSBs at stalled replication forks and promote replication fork recovery. EMBO J 29:3156–3169PubMedCentralPubMedCrossRefGoogle Scholar
  4. Anantha RW, Vassin VM, Borowiec JA (2007) Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J Biol Chem 282:35910–35923PubMedCrossRefGoogle Scholar
  5. Antunez de Mayolo A, Lisby M, Erdeniz N, Thybo T, Mortensen UH, Rothstein R (2006) Multiple start codons and phosphorylation result in discrete Rad52 protein species. Nucleic Acids Res 34:2587–2597PubMedCrossRefGoogle Scholar
  6. Aparicio T, Baer R, Gautier J (2014) DNA double-strand break repair pathway choice and cancer. DNA Repair (Amst) 19:169–175Google Scholar
  7. Bahassi EM, Ovesen JL, Riesenberg AL, Bernstein WZ, Hasty PE, Stambrook PJ (2008) The checkpoint kinases Chk1 and Chk2 regulate the functional associations between hBRCA2 and Rad51 in response to DNA damage. Oncogene 27:3977–3985PubMedCrossRefGoogle Scholar
  8. Balakrishnan L, Stewart J, Polaczek P, Campbell JL, Bambara RA (2010) Acetylation of Dna2 endonuclease/helicase and flap endonuclease 1 by p300 promotes DNA stability by creating long flap intermediates. J Biol Chem 285:4398–4404PubMedCentralPubMedCrossRefGoogle Scholar
  9. Baroni E, Viscardi V, Cartagena-Lirola H, Lucchini G, Longhese MP (2004) The functions of budding yeast Sae2 in the DNA damage response require Mec1- and Tel1-dependent phosphorylation. Mol Cell Biol 24:4151–4165PubMedCentralPubMedCrossRefGoogle Scholar
  10. Bayart E, Dutertre S, Jaulin C, Guo RB, Xi XG, Amor-Gueret M (2006) The Bloom syndrome helicase is a substrate of the mitotic Cdc2 kinase. Cell Cycle 5:1681–1686PubMedCrossRefGoogle Scholar
  11. Blanco MG, Matos J, West SC (2014) Dual control of yen1 nuclease activity and cellular localization by cdk and cdc14 prevents genome instability. Mol Cell 54:94–106PubMedCentralPubMedCrossRefGoogle Scholar
  12. Blander G, Zalle N, Daniely Y, Taplick J, Gray MD, Oren M (2002) DNA damage-induced translocation of the Werner helicase is regulated by acetylation. J Biol Chem 277:50934–50940PubMedCrossRefGoogle Scholar
  13. Branzei D, Sollier J, Liberi G, Zhao X, Maeda D, Seki M, Enomoto T, Ohta K, Foiani M (2006) Ubc9- and mms21-mediated sumoylation counteracts recombinogenic events at damaged replication forks. Cell 127:509–522PubMedCrossRefGoogle Scholar
  14. Bruderer R, Tatham MH, Plechanovova A, Matic I, Garg AK, Hay RT (2011) Purification and identification of endogenous polySUMO conjugates. EMBO Rep 12:142–148PubMedCentralPubMedCrossRefGoogle Scholar
  15. Callen E, Di Virgilio M, Kruhlak MJ, Nieto-Soler M, Wong N, Chen HT, Faryabi RB, Polato F, Santos M, Starnes LM et al (2013) 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 153:1266–1280PubMedCentralPubMedCrossRefGoogle Scholar
  16. Cartagena-Lirola H, Guerini I, Viscardi V, Lucchini G, Longhese MP (2006) Budding Yeast Sae2 is an In Vivo Target of the Mec1 and Tel1 Checkpoint Kinases During Meiosis. Cell Cycle 5:1549–1559PubMedCrossRefGoogle Scholar
  17. Chan DW, Ye R, Veillette CJ, Lees-Miller SP (1999) DNA-dependent protein kinase phosphorylation sites in Ku 70/80 heterodimer. Biochemistry 38:1819–1828PubMedCrossRefGoogle Scholar
  18. Chen X, Niu H, Chung WH, Zhu Z, Papusha A, Shim EY, Lee SE, Sung P, Ira G (2011) 11. Cell cycle regulation of DNA double-strand break end resection by Cdk1-dependent Dna2 phosphorylation. Nat Struct Mol Biol 18:1015–1019PubMedCentralPubMedCrossRefGoogle Scholar
  19. Chapman JR, Taylor MR, Boulton SJ (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497–510PubMedCrossRefGoogle Scholar
  20. Chen H, Lisby M, Symington LS (2013) RPA coordinates DNA end resection and prevents formation of DNA hairpins. Mol Cell 50:589–600PubMedCrossRefGoogle Scholar
  21. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, Olsen JV, Mann M (2009) Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 325:834–840PubMedCrossRefGoogle Scholar
  22. Conilleau S, Takizawa Y, Tachiwana H, Fleury F, Kurumizaka H, Takahashi M (2004) Location of tyrosine 315, a target for phosphorylation by cAbl tyrosine kinase, at the edge of the subunit-subunit interface of the human Rad51 filament. J Mol Biol 339:797–804PubMedCrossRefGoogle Scholar
  23. Cortez D, Wang Y, Qin J, Elledge SJ (1999) Requirement of ATM-dependent phosphorylation of brca1 in the DNA damage response to double-strand breaks. Science 286:1162–1166PubMedCrossRefGoogle Scholar
  24. D’Amours D, Jackson SP (2001) The yeast Xrs2 complex functions in S phase checkpoint regulation. Genes Dev 15:2238–2249PubMedCentralPubMedCrossRefGoogle Scholar
  25. Davies SL, North PS, Dart A, Lakin ND, Hickson ID (2004) Phosphorylation of the Bloom's syndrome helicase and its role in recovery from S-phase arrest. Mol Cell Biol 24:1279–1291PubMedCentralPubMedCrossRefGoogle Scholar
  26. Donnianni RA, Ferrari M, Lazzaro F, Clerici M, Tamilselvan Nachimuthu B, Plevani P, Muzi-Falconi M, Pellicioli A (2010) Elevated levels of the polo kinase Cdc5 override the Mec1/ATR checkpoint in budding yeast by acting at different steps of the signaling pathway. PLoS Genet 6:e1000763PubMedCentralPubMedCrossRefGoogle Scholar
  27. Dou H, Huang C, Singh M, Carpenter PB, Yeh ET (2010) Regulation of DNA repair through deSUMOylation and SUMOylation of replication protein A complex. Mol Cell 39:333–345PubMedCentralPubMedCrossRefGoogle Scholar
  28. Eissler CL, Mazon G, Powers BL, Savinov SN, Symington LS, Hall MC (2014) The cdk/cdc14 module controls activation of the yen1 holliday junction resolvase to promote genome stability. Mol Cell 54:80–93PubMedCrossRefGoogle Scholar
  29. El-Shemerly M, Hess D, Pyakurel AK, Moselhy S, Ferrari S (2008) ATR-dependent pathways control hEXO1 stability in response to stalled forks. Nucleic Acids Res 36:511–519PubMedCentralPubMedCrossRefGoogle Scholar
  30. Eladad S, Ye TZ, Hu P, Leversha M, Beresten S, Matunis MJ, Ellis NA (2005) Intra-nuclear trafficking of the BLM helicase to DNA damage-induced foci is regulated by SUMO modification. Hum Mol Genet 14:1351–1365PubMedCrossRefGoogle Scholar
  31. Esashi F, Christ N, Gannon J, Liu Y, Hunt T, Jasin M, West SC (2005) CDK-dependent phosphorylation of BRCA2 as a regulatory mechanism for recombinational repair. Nature 434:598–604PubMedCrossRefGoogle Scholar
  32. Ferrari M, Nachimuthu BT, Donnianni RA, Klein H, Pellicioli A (2013) Tid1/Rdh54 translocase is phosphorylated through a Mec1- and Rad53-dependent manner in the presence of DSB lesions in budding yeast. DNA Repair (Amst) 12:347–355CrossRefGoogle Scholar
  33. Gama V, Yoshida T, Gomez JA, Basile DP, Mayo LD, Haas AL, Matsuyama S (2006) Involvement of the ubiquitin pathway in decreasing Ku70 levels in response to drug-induced apoptosis. Exp Cell Res 312:488–499PubMedCrossRefGoogle Scholar
  34. Gatei M, Scott SP, Filippovitch I, Soronika N, Lavin MF, Weber B, Khanna KK (2000a) Role for ATM in DNA damage-induced phosphorylation of BRCA1. Cancer Res 60:3299–3304PubMedGoogle Scholar
  35. Gatei M, Young D, Cerosaletti KM, Desai-Mehta A, Spring K, Kozlov S, Lavin MF, Gatti RA, Concannon P, Khanna K (2000b) ATM-dependent phosphorylation of nibrin in response to radiation exposure. Nat Genet 25:115–119PubMedCrossRefGoogle Scholar
  36. Herzberg K, Bashkirov VI, Rolfsmeier M, Haghnazari E, McDonald WH, Anderson S, Bashkirova EV, Yates JR 3rd, Heyer WD (2006) Phosphorylation of Rad55 on serines 2, 8, and 14 is required for efficient homologous recombination in the recovery of stalled replication forks. Mol Cell Biol 26:8396–8409PubMedCentralPubMedCrossRefGoogle Scholar
  37. Heyer WD, Ehmsen KT, Liu J (2010) Regulation of homologous recombination in eukaryotes. Annu Rev Genet 44:113–139PubMedCentralPubMedCrossRefGoogle Scholar
  38. Huertas P, Jackson SP (2009) Human CtIP mediates cell cycle control of DNA end resection and double strand break repair. J Biol Chem 284:9558–9565PubMedCentralPubMedCrossRefGoogle Scholar
  39. Ira G, Pellicioli A, Balijja A, Wang X, Fiorani S, Carotenuto W, Liberi G, Bressan D, Wan L, Hollingsworth NM et al (2004) DNA end resection, homologous recombination and DNA damage checkpoint activation require CDK1. Nature 431:1011–1017PubMedCrossRefGoogle Scholar
  40. Kai M, Boddy MN, Russell P, Wang TS (2005) Replication checkpoint kinase Cds1 regulates Mus81 to preserve genome integrity during replication stress. Genes Dev 19:919–932PubMedCentralPubMedCrossRefGoogle Scholar
  41. Kaidi A, Weinert BT, Choudhary C, Jackson SP (2010) Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329:1348–1353PubMedCentralPubMedCrossRefGoogle Scholar
  42. Kawabe Y, Seki M, Seki T, Wang WS, Imamura O, Furuichi Y, Saitoh H, Enomoto T (2000) Covalent modification of the Werner's syndrome gene product with the ubiquitin-related protein, SUMO-1. J Biol Chem 275:20963–20966PubMedCrossRefGoogle Scholar
  43. Kim HS, Brill SJ (2003) MEC1-dependent phosphorylation of yeast RPA1 in vitro. DNA Repair (Amst) 2:1321–1335CrossRefGoogle Scholar
  44. Kitao H, Yuan ZM (2002) Regulation of ionizing radiation-induced Rad52 nuclear foci formation by c-Abl-mediated phosphorylation. J Biol Chem 277:48944–48948PubMedCrossRefGoogle Scholar
  45. Lazzaro F, Giannattasio M, Puddu F, Granata M, Pellicioli A, Plevani P, Muzi-Falconi M (2009) Checkpoint mechanisms at the intersection between DNA damage and repair. DNA Repair (Amst) 8:1055–1067CrossRefGoogle Scholar
  46. Lee JS, Collins KM, Brown AL, Lee CH, Chung JH (2000) hCds1-mediated phosphorylation of BRCA1 regulates the DNA damage response. Nature 404:201–204PubMedCrossRefGoogle Scholar
  47. Lee KJ, Jovanovic M, Udayakumar D, Bladen CL, Dynan WS (2004) Identification of DNA-PKcs phosphorylation sites in XRCC4 and effects of mutations at these sites on DNA end joining in a cell-free system. DNA Repair (Amst) 3:267–276CrossRefGoogle Scholar
  48. Lee DH, Acharya SS, Kwon M, Drane P, Guan Y, Adelmant G, Kalev P, Shah J, Pellman D, Marto JA et al (2014) Dephosphorylation enables the recruitment of 53BP1 to double-strand DNA breaks. Mol Cell 54:512–525PubMedCrossRefGoogle Scholar
  49. Li K, Wang R, Lozada E, Fan W, Orren DK, Luo J (2010) Acetylation of WRN protein regulates its stability by inhibiting ubiquitination. PLoS One 5:e10341PubMedCentralPubMedCrossRefGoogle Scholar
  50. Lim DS, Kim ST, Xu B, Maser RS, Lin J, Petrini JH, Kastan MB (2000) ATM phosphorylates p95/nbs1 in an S-phase checkpoint pathway. Nature 404:613–617PubMedCrossRefGoogle Scholar
  51. Lloyd J, Chapman JR, Clapperton JA, Haire LF, Hartsuiker E, Li J, Carr AM, Jackson SP, Smerdon SJ (2009) A supramodular FHA/BRCT-repeat architecture mediates Nbs1 adaptor function in response to DNA damage. Cell 139:100–111PubMedCentralPubMedCrossRefGoogle Scholar
  52. Ma Y, Pannicke U, Lu H, Niewolik D, Schwarz K, Lieber MR (2005) The DNA-dependent protein kinase catalytic subunit phosphorylation sites in human Artemis. J Biol Chem 280:33839–33846PubMedCrossRefGoogle Scholar
  53. Mimitou EP, Symington LS (2009) DNA end resection: many nucleases make light work. DNA Repair (Amst) 8:983–995CrossRefGoogle Scholar
  54. Morin I, Ngo HP, Greenall A, Zubko MK, Morrice N, Lydall D (2008) Checkpoint-dependent phosphorylation of Exo1 modulates the DNA damage response. EMBO J 27:2400–2410PubMedCentralPubMedCrossRefGoogle Scholar
  55. Muftuoglu M, Kusumoto R, Speina E, Beck G, Cheng WH, Bohr VA (2008) Acetylation regulates WRN catalytic activities and affects base excision DNA repair. PLoS One 3:e1918PubMedCentralPubMedCrossRefGoogle Scholar
  56. Muller-Tidow C, Ji P, Diederichs S, Potratz J, Baumer N, Kohler G, Cauvet T, Choudary C, van der Meer T, Chan WY et al (2004) The cyclin A1-CDK2 complex regulates DNA double-strand break repair. Mol Cell Biol 24:8917–8928PubMedCentralPubMedCrossRefGoogle Scholar
  57. Niu H, Wan L, Busygina V, Kwon Y, Allen JA, Li X, Kunz RC, Kubota K, Wang B, Sung P et al (2009) Regulation of meiotic recombination via Mek1-mediated Rad54 phosphorylation. Mol Cell 36:393–404PubMedCentralPubMedCrossRefGoogle Scholar
  58. Ohouo PY, Bastos de Oliveira FM, Almeida BS, Smolka MB (2010) DNA damage signaling recruits the Rtt107-Slx4 scaffolds via Dpb11 to mediate replication stress response. Mol Cell 39:300–306PubMedCrossRefGoogle Scholar
  59. Ohouo PY, Bastos de Oliveira FM, Liu Y, Ma CJ, Smolka MB (2013) DNA-repair scaffolds dampen checkpoint signalling by counteracting the adaptor Rad9. Nature 493:120–124PubMedCentralPubMedCrossRefGoogle Scholar
  60. Ouyang KJ, Woo LL, Zhu J, Huo D, Matunis MJ, Ellis NA (2009) SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol 7:e1000252PubMedCentralPubMedCrossRefGoogle Scholar
  61. Panier S, Boulton SJ (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15:7–18PubMedCrossRefGoogle Scholar
  62. Pellicioli A, Lee SE, Lucca C, Foiani M, Haber JE (2001) Regulation of Saccharomyces Rad53 checkpoint kinase during adaptation from DNA damage-induced G2/M arrest. Mol Cell 7:293–300PubMedCrossRefGoogle Scholar
  63. Postow L, Ghenoiu C, Woo EM, Krutchinsky AN, Chait BT, Funabiki H (2008) Ku80 removal from DNA through double strand break-induced ubiquitylation. J Cell Biol 182:467–479PubMedCentralPubMedCrossRefGoogle Scholar
  64. Riballo E, Kuhne M, Rief N, Doherty A, Smith GC, Recio MJ, Reis C, Dahm K, Fricke A, Krempler A et al (2004) A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to gamma-H2AX foci. Mol Cell 16:715–724PubMedCrossRefGoogle Scholar
  65. Robert T, Vanoli F, Chiolo I, Shubassi G, Bernstein KA, Rothstein R, Botrugno OA, Parazzoli D, Oldani A, Minucci S et al (2011) HDACs link the DNA damage response, processing of double-strand breaks and autophagy. Nature 471:74–79PubMedCentralPubMedCrossRefGoogle Scholar
  66. Sacher M, Pfander B, Hoege C, Jentsch S (2006) Control of Rad52 recombination activity by double-strand break-induced SUMO modification. Nat Cell Biol 8:1284–1290PubMedCrossRefGoogle Scholar
  67. Saponaro M, Callahan D, Zheng X, Krejci L, Haber JE, Klein HL, Liberi G (2010) Cdk1 targets Srs2 to complete synthesis-dependent strand annealing and to promote recombinational repair. PLoS Genet 6:e1000858PubMedCentralPubMedCrossRefGoogle Scholar
  68. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP (2007) Human CtIP promotes DNA end resection. Nature 450:509–514PubMedCentralPubMedCrossRefGoogle Scholar
  69. Schwartz EK, Heyer WD (2011) Processing of joint molecule intermediates by structure-selective endonucleases during homologous recombination in eukaryotes. Chromosoma 120:109–127PubMedCentralPubMedCrossRefGoogle Scholar
  70. Sorensen CS, Hansen LT, Dziegielewski J, Syljuasen RG, Lundin C, Bartek J, Helleday T (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7:195–201PubMedCrossRefGoogle Scholar
  71. Terasawa M, Ogawa T, Tsukamoto Y, Ogawa H (2008) Sae2p phosphorylation is crucial for cooperation with Mre11p for resection of DNA double-strand break ends during meiotic recombination in Saccharomyces cerevisiae. Genes Genet Syst 83:209–217PubMedCrossRefGoogle Scholar
  72. Tibbetts RS, Cortez D, Brumbaugh KM, Scully R, Livingston D, Elledge SJ, Abraham RT (2000) Functional interactions between BRCA1 and the checkpoint kinase ATR during genotoxic stress. Genes Dev 14:2989–3002PubMedCentralPubMedCrossRefGoogle Scholar
  73. Toh GW, Sugawara N, Dong J, Toth R, Lee SE, Haber JE, Rouse J (2010) Mec1/Tel1-dependent phosphorylation of Slx4 stimulates Rad1-Rad10-dependent cleavage of non-homologous DNA tails. DNA Repair (Amst) 9:718–726CrossRefGoogle Scholar
  74. Tougan T, Kasama T, Ohtaka A, Okuzaki D, Saito TT, Russell P, Nojima H (2010) The Mek1 phosphorylation cascade plays a role in meiotic recombination of Schizosaccharomyces pombe. Cell Cycle 9:4688–4702PubMedCentralPubMedCrossRefGoogle Scholar
  75. Ubersax JA, Woodbury EL, Quang PN, Paraz M, Blethrow JD, Shah K, Shokat KM, Morgan DO (2003) Targets of the cyclin-dependent kinase Cdk1. Nature 425:859–864PubMedCrossRefGoogle Scholar
  76. Wang YG, Nnakwe C, Lane WS, Modesti M, Frank KM (2004) Phosphorylation and regulation of DNA ligase IV stability by DNA-dependent protein kinase. J Biol Chem 279:37282–37290PubMedCrossRefGoogle Scholar
  77. Waters CA, Strande NT, Wyatt DW, Pryor JM, Ramsden DA (2014) Nonhomologous end joining: a good solution for bad ends. DNA Repair (Amst) 17:39–51CrossRefGoogle Scholar
  78. Williams RS, Dodson GE, Limbo O, Yamada Y, Williams JS, Guenther G, Classen S, Glover JN, Iwasaki H, Russell P et al (2009) Nbs1 flexibly tethers Ctp1 and Mre11-Rad50 to coordinate DNA double-strand break processing and repair. Cell 139:87–99PubMedCentralPubMedCrossRefGoogle Scholar
  79. Woods YL, Xirodimas DP, Prescott AR, Sparks A, Lane DP, Saville MK (2004) p14 Arf promotes small ubiquitin-like modifier conjugation of Werners helicase. J Biol Chem 279:50157–50166PubMedCrossRefGoogle Scholar
  80. Wu X, Ranganathan V, Weisman DS, Heine WF, Ciccone DN, O'Neill TB, Crick KE, Pierce KA, Lane WS, Rathbun G et al (2000) ATM phosphorylation of Nijmegen breakage syndrome protein is required in a DNA damage response. Nature 405:477–482PubMedCrossRefGoogle Scholar
  81. Yu X, Fu S, Lai M, Baer R, Chen J (2006) BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev 20:1721–1726PubMedCentralPubMedCrossRefGoogle Scholar
  82. Yu Y, Mahaney BL, Yano K, Ye R, Fang S, Douglas P, Chen DJ, Lees-Miller SP (2008) DNA-PK and ATM phosphorylation sites in XLF/Cernunnos are not required for repair of DNA double strand breaks. DNA Repair (Amst) 7:1680–1692CrossRefGoogle Scholar
  83. Yurchenko V, Xue Z, Gama V, Matsuyama S, Sadofsky MJ (2008) Ku70 is stabilized by increased cellular SUMO. Biochem Biophys Res Commun 366:263–268PubMedCentralPubMedCrossRefGoogle Scholar
  84. Yurchenko V, Xue Z, Sadofsky MJ (2006) SUMO modification of human XRCC4 regulates its localization and function in DNA double-strand break repair. Mol Cell Biol 26:1786–1794PubMedCentralPubMedCrossRefGoogle Scholar
  85. Zhao S, Weng YC, Yuan SS, Lin YT, Hsu HC, Lin SC, Gerbino E, Song MH, Zdzienicka MZ, Gatti RA et al (2000) Functional link between ataxia-telangiectasia and Nijmegen breakage syndrome gene products. Nature 405:473–477PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media New York 2014

Authors and Affiliations

  1. 1.Dipartimento di BioscienzeUniversità di MilanoMilanItaly