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The Crossroads of Ubiquitination and DNA Repair: A Structural Perspective

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DNA Replication, Recombination, and Repair

Abstract

The timely repair of DNA damage is crucial to the maintenance of genome integrity. The DNA damage response relies on the cross talk between a large number of protein complexes and is subject to regulation by posttranslational modifications. Ubiquitination has emerged as an integral part of several DNA repair and damage-signaling responses. This posttranslational modification not only targets proteins for degradation by the proteasome but also has important regulatory roles. Here, we review our current understanding of selected DNA repair pathways influenced by ubiquitination, with a special focus on protein structure and architecture.

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References

  • Aboussekhra A, Biggerstaff M, Shivji MK, Vilpo JA, Moncollin V, Podust VN, Protić M, Hübscher U, Egly JM, Wood RD (1995) Mammalian DNA nucleotide excision repair reconstituted with purified protein components. Cell 80(6):859–868

    Article  PubMed  CAS  Google Scholar 

  • Alpi AF, Pace PE, Babu MM, Patel KJ (2008) Mechanistic insight into site-restricted monoubiquitination of FANCD2 by Ube2t, FANCL, and FANCI. Mol Cell 32(6):767–777

    Article  PubMed  CAS  Google Scholar 

  • Anamika A, Markin CJ, Rout MK, Spyracopoulos L (2014) Molecular basis for impaired DNA damage response function associated with the RAP80 E81 defect. J Biol Chem 289(18):12852–12862

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Andersen SL, Bergstralh DT, Kohl KP, LaRocque JR, Moore CB, Sekelsky J (2009) Drosophila MUS312 and the vertebrate ortholog BTBD12 interact with DNA structure-specific endonucleases in DNA repair and recombination. Mol Cell 35(1):128–135

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Angers S, Li T, Yi X, MacCoss MJ, Moon RT, Zheng N (2006) Molecular architecture and assembly of the DDB1-CUL4A ubiquitin ligase machinery. Nature 443(7111):590–593

    PubMed  CAS  Google Scholar 

  • Anindya R, Mari PO, Kristensen U, Kool H, Giglia-Mari G, Mullenders LH, Fousteri M, Vermeulen W, Egly JM, Svejstrup JQ (2010) A ubiquitin-binding domain in Cockayne syndrome B required for transcription-coupled nucleotide excision repair. Mol Cell 38(5):637–648

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Auerbach AD, Wolman SR (1976) Susceptibility of Fanconi’s anaemia fibroblasts to chromosome damage by carcinogens. Nature 261(5560):494–496

    Article  PubMed  CAS  Google Scholar 

  • Auerbach AD, Wolman SR (1978) Carcinogen-induced chromosome breakage in Fanconi’s anaemia heterozygous cells. Nature 271(5640):69–71

    Article  PubMed  CAS  Google Scholar 

  • Auerbach AD, Sagi M, Adler B (1985) Fanconi anemia: prenatal diagnosis in 30 fetuses at risk. Pediatrics 76(5):794–800

    PubMed  CAS  Google Scholar 

  • Batty D, Rapic’-Otrin V, Levine A, Wood R (2000) Stable binding of human XPC complex to irradiated DNA confers strong discrimination for damaged sites. J Mol Biol 300(2):275–290

    Article  PubMed  CAS  Google Scholar 

  • Bennett EJ, Rush J, Gygi SP, Harper JW (2010) Dynamics of cullin-RING ubiquitin ligase network revealed by systematic quantitative proteomics. Cell 143(6):951–965

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Castillo A, Paul A, Sun B, Huang TH, Wang Y, Yazinski SA, Tyler J, Li L, You MJ, Zou L, Yao J, Wang B (2014) The BRCA1-interacting protein Abraxas is required for genomic stability and tumor suppression. Cell Rep 8(3):807–817

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Chen X, Zhang Y, Douglas L, Zhou P (2001) UV-damaged DNA-binding proteins are targets of CUL-4A-mediated ubiquitination and degradation. J Biol Chem 276(51):48175–48182

    PubMed  CAS  Google Scholar 

  • Ciccia A, Ling C, Coulthard R, Yan Z, Xue Y, Meetei AR, el Laghmani H, Joenje H, McDonald N, de Winter JP, Wang W, West SC (2007) Identification of FAAP24, a Fanconi anemia core complex protein that interacts with FANCM. Mol Cell 25(3):331–343

    Article  PubMed  CAS  Google Scholar 

  • Citterio E, Van Den Boom V, Schnitzler G, Kanaar R, Bonte E, Kingston RE, Hoeijmakers JH, Vermeulen W (2000) ATP-dependent chromatin remodeling by the Cockayne syndrome B DNA repair-transcription-coupling factor. Mol Cell Biol 20(20):7643–7653

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cleaver JE, Lam ET, Revet I (2009) Disorders of nucleotide excision repair: the genetic and molecular basis of heterogeneity. Nat Rev Genet 10(11):756–768

    Article  PubMed  CAS  Google Scholar 

  • Cohn MA, Kowal P, Yang K, Haas W, Huang TT, Gygi SP, D’Andrea AD (2007) A UAF1-containing multisubunit protein complex regulates the Fanconi anemia pathway. Mol Cell 28(5):786–797

    Article  PubMed  CAS  Google Scholar 

  • Cole AR, Lewis LP, Walden H (2010) The structure of the catalytic subunit FANCL of the Fanconi anemia core complex. Nat Struct Mol Biol 17(3):294–298

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Coleman KA, Greenberg RA (2011) The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J Biol Chem 286(15):13669–13680

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cooper EM, Cutcliffe C, Kristiansen TZ, Pandey A, Pickart CM, Cohen RE (2009) K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J 28(6):621–631

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Cope GA, Suh GS, Aravind L, Schwarz SE, Zipursky SL, Koonin EV, Deshaies RJ (2002) Role of predicted metalloprotease motif of Jab1/Csn5 in cleavage of Nedd8 from Cul1. Science 298(5593):608–611

    Article  PubMed  CAS  Google Scholar 

  • Coulon S, Gaillard PH, Chahwan C, McDonald WH, Yates JR 3rd, Russell P (2004) Slx1-Slx4 are subunits of a structure-specific endonuclease that maintains ribosomal DNA in fission yeast. Mol Biol Cell 15(1):71–80

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Coulthard R, Deans AJ, Swuec P, Bowles M, Costa A, West SC, McDonald NQ (2013) Architecture and DNA recognition elements of the Fanconi anemia FANCM-FAAP24 complex. Structure 21(9):1648–1658

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • De Bont R, van Larebeke N (2004) Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 19(3):169–185

    Article  PubMed  Google Scholar 

  • Deans AJ, West SC (2009) FANCM connects the genome instability disorders Bloom’s syndrome and Fanconi anemia. Mol Cell 36(6):943–953

    Article  PubMed  CAS  Google Scholar 

  • Deans AJ, West SC (2011) DNA interstrand crosslink repair and cancer. Nat Rev Cancer 11(7):467–480

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dery U, Masson JY (2007) Twists and turns in the function of DNA damage signaling and repair proteins by post-translational modifications. DNA Repair (Amst) 6(5):561–577

    Article  CAS  Google Scholar 

  • Dever SM, Golding SE, Rosenberg E, Adams BR, Idowu MO, Quillin JM, Valerie N, Xu B, Povirk LF, Valerie K (2011) Mutations in the BRCT binding site of BRCA1 result in hyper-recombination. Aging 3(5):515–532

    PubMed Central  PubMed  CAS  Google Scholar 

  • Dever SM, White ER, Hartman MCT, Valerie K (2012) BRCA1-directed, enhanced and aberrant homologous recombination: mechanism and potential treatment strategies. Cell Cycle 11(4):687–694

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Dualan R, Brody T, Keeney S, Nichols A, Admon A, Linn S (1995) Chromosomal localization and cDNA cloning of the genes (DDB1 and DDB2) for the p127 and p48 subunits of a human damage-specific DNA binding protein. Genomics 29(1):62–69

    Article  PubMed  CAS  Google Scholar 

  • Echalier A, Pan Y, Birol M, Tavernier N, Pintard L, Hoh F, Ebel C, Galophe N, Claret FX, Dumas C (2013) Insights into the regulation of the human COP9 signalosome catalytic subunit, CSN5/Jab1. Proc Natl Acad Sci U S A 110(4):1273–1278

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • El-Mahdy M, Zhu Q, Wang Q, Wani G, Praetorius-Ibba M, Wani A (2006) Cullin 4A-mediated proteolysis of DDB2 protein at DNA damage sites regulates in vivo lesion recognition by XPC. J Biol Chem 281(19):13404–13411

    Article  PubMed  CAS  Google Scholar 

  • Enchev RI, Scott DC, da Fonseca PC, Schreiber A, Monda JK, Schulman BA, Peter M, Morris EP (2012) Structural basis for a reciprocal regulation between SCF and CSN. Cell Rep 2(3):616–627

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fei J, Chen J (2012) KIAA1530 protein is recruited by Cockayne syndrome complementation group protein A (CSA) to participate in transcription-coupled repair (TCR). J Biol Chem 287(42):35118–35126

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fekairi S, Scaglione S, Chahwan C, Taylor ER, Tissier A, Coulon S, Dong MQ, Ruse C, Yates JR 3rd, Russell P, Fuchs RP, McGowan CH, Gaillard PH (2009) Human SLX4 is a Holliday junction resolvase subunit that binds multiple DNA repair/recombination endonucleases. Cell 138(1):78–89

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Feng L, Wang J, Chen J (2010) The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J Biol Chem 285(40):30982–30988

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Fischer ES, Scrima A, Bohm K, Matsumoto S, Lingaraju GM, Faty M, Yasuda T, Cavadini S, Wakasugi M, Hanaoka F, Iwai S, Gut H, Sugasawa K, Thoma NH (2011) The molecular basis of CRL4DDB2/CSA ubiquitin ligase architecture, targeting, and activation. Cell 147(5):1024–1039

    Article  PubMed  CAS  Google Scholar 

  • Fitch M, Nakajima S, Yasui A, Ford J (2003) In vivo recruitment of XPC to UV-induced cyclobutane pyrimidine dimers by the DDB2 gene product. J Biol Chem 278(47):46906–46910

    Article  PubMed  CAS  Google Scholar 

  • Fricke WM, Brill SJ (2003) Slx1-Slx4 is a second structure-specific endonuclease functionally redundant with Sgs1-Top3. Genes Dev 17(14):1768–1778

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Friedberg EC, Walker GC, Siede RD, Wood RD, Schultz RA, Ellenberger T (2006) DNA repair and mutagenesis, 2nd edn. ASM Press, Washington, DC

    Google Scholar 

  • Furukawa M, Zhang Y, McCarville J, Ohta T, Xiong Y (2000) The CUL1 C-terminal sequence and ROC1 are required for efficient nuclear accumulation, NEDD8 modification, and ubiquitin ligase activity of CUL1. Mol Cell Biol 20(21):8185–8197

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Ghodke H, Wang H, Hsieh CL, Woldemeskel S, Watkins SC, Rapic-Otrin V, Van Houten B (2014) Single-molecule analysis reveals human UV-damaged DNA-binding protein (UV-DDB) dimerizes on DNA via multiple kinetic intermediates. Proc Natl Acad Sci U S A 111(18):E1862–E1871

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Gillet LC, Scharer OD (2006) Molecular mechanisms of mammalian global genome nucleotide excision repair. Chem Rev 106(2):253–276

    Article  PubMed  CAS  Google Scholar 

  • Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev A, Tanaka K, Nakatani Y (2003) The ubiquitin ligase activity in the DDB2 and CSA complexes is differentially regulated by the COP9 signalosome in response to DNA damage. Cell 113(3):357–367

    Article  PubMed  CAS  Google Scholar 

  • Groisman R, Kuraoka I, Chevallier O, Gaye N, Magnaldo T, Tanaka K, Kisselev AF, Harel-Bellan A, Nakatani Y (2006) CSA-dependent degradation of CSB by the ubiquitin-proteasome pathway establishes a link between complementation factors of the Cockayne syndrome. Genes Dev 20(11):1429–1434

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guerrero-Santoro J, Kapetanaki M, Hsieh C, Gorbachinsky I, Levine A, Rapic-Otrin V (2008) The cullin 4B-based UV-damaged DNA-binding protein ligase binds to UV-damaged chromatin and ubiquitinates histone H2A. Cancer Res 68(13):5014–5022

    Article  PubMed  CAS  Google Scholar 

  • Guettler S, LaRose J, Petsalaki E, Gish G, Scotter A, Pawson T, Rottapel R, Sicheri F (2011) Structural basis and sequence rules for substrate recognition by tankyrase explain the basis for Cherubism disease. Cell 147(6):1340–1354

    Article  PubMed  CAS  Google Scholar 

  • Gurtan AM, D’Andrea AD (2006) Dedicated to the core: understanding the Fanconi anemia complex. DNA Repair (Amst) 5(9–10):1119–1125

    Article  CAS  Google Scholar 

  • Guzzo CM, Matunis MJ (2013) Expanding SUMO and ubiquitin-mediated signaling through hybrid SUMO-ubiquitin chains and their receptors. Cell Cycle 12(7):1015–1017

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Guzzo CM, Berndsen CE, Zhu J, Gupta V, Datta A, Greenberg RA, Wolberger C, Matunis MJ (2012) RNF4-dependent hybrid SUMO-ubiquitin chains are signals for RAP80 and thereby mediate the recruitment of BRCA1 to sites of DNA damage. Sci Signal 5(253):88–88

    Google Scholar 

  • Hannah J, Zhou P (2009) Regulation of DNA damage response pathways by the cullin-RING ubiquitin ligases. DNA Repair (Amst) 8(4):536–543

    Google Scholar 

  • Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28(5):739–745

    Article  PubMed  CAS  Google Scholar 

  • He Y, McCall C, Hu J, Zeng Y, Xiong Y (2006) DDB1 functions as a linker to recruit receptor WD40 proteins to CUL4-ROC1 ubiquitin ligases. Genes Dev 20(21):2949–2954

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Henning KA, Li L, Iyer N, McDaniel LD, Reagan MS, Legerski R, Schultz RA, Stefanini M, Lehmann AR, Mayne LV, Friedberg EC (1995) The Cockayne syndrome group A gene encodes a WD repeat protein that interacts with CSB protein and a subunit of RNA polymerase II TFIIH. Cell 82(4):555–564

    Article  PubMed  CAS  Google Scholar 

  • Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425–479

    Article  PubMed  CAS  Google Scholar 

  • Higa L, Wu M, Ye T, Kobayashi R, Sun H, Zhang H (2006) CUL4-DDB1 ubiquitin ligase interacts with multiple WD40-repeat proteins and regulates histone methylation. Nat Cell Biol 8(11):1277–1283

    Article  PubMed  CAS  Google Scholar 

  • Hoadley KA, Xue Y, Ling C, Takata M, Wang W, Keck JL (2012) Defining the molecular interface that connects the Fanconi anemia protein FANCM to the Bloom syndrome dissolvasome. Proc Natl Acad Sci U S A 109(12):4437–4442

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hodskinson MR, Silhan J, Crossan GP, Garaycoechea JI, Mukherjee S, Johnson CM, Scharer OD, Patel KJ (2014) Mouse SLX4 is a tumor suppressor that stimulates the activity of the nuclease XPF-ERCC1 in DNA crosslink repair. Mol Cell 54(3):472–484

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hodson C, Cole AR, Lewis LP, Miles JA, Purkiss A, Walden H (2011) Structural analysis of human FANCL, the E3 ligase in the Fanconi anemia pathway. J Biol Chem 286(37):32628–32637

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hodson C, Purkiss A, Miles JA, Walden H (2014) Structure of the human FANCL RING-Ube2T complex reveals determinants of cognate E3-E2 selection. Structure 22(2):337–344

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S (2002) RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419(6903):135–141

    Article  PubMed  CAS  Google Scholar 

  • Hoeijmakers JH (2009) DNA damage, aging, and cancer. N Engl J Med 361(15):1475–1485

    Article  PubMed  CAS  Google Scholar 

  • Hofmann K (2009) Ubiquitin-binding domains and their role in the DNA damage response. DNA Repair (Amst) 8(4):544–556

    Article  CAS  Google Scholar 

  • Hotton SK, Callis J (2008) Regulation of cullin RING ligases. Annu Rev Plant Biol 59:467–489

    Article  PubMed  CAS  Google Scholar 

  • Hu X, Kim JA, Castillo A, Huang M, Liu J, Wang B (2011a) NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J Biol Chem 286(13):11734–11745

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Hu Y, Scully R, Sobhian B, Xie A, Shestakova E, Livingston DM (2011b) RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev 25(7):685–700

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Huang Y, Leung JW, Lowery M, Matsushita N, Wang Y, Shen X, Huong D, Takata M, Chen J, Li L (2014) Modularized functions of the Fanconi anemia core complex. Cell Rep 7(6):1849–1857

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81:291–322

    Article  PubMed  CAS  Google Scholar 

  • Jackson S, Xiong Y (2009) CRL4s: the CUL4-RING E3 ubiquitin ligases. Trends Biochem Sci 34(11):562–570

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Jin J, Arias E, Chen J, Harper J, Walter J (2006) A family of diverse Cul4-Ddb1-interacting proteins includes Cdt2, which is required for S phase destruction of the replication factor Cdt1. Mol Cell 23(5):709–721

    Article  PubMed  CAS  Google Scholar 

  • Jin J, Li X, Gygi SP, Harper JW (2007) Dual E1 activation systems for ubiquitin differentially regulate E2 enzyme charging. Nature 447(7148):1135–1138

    Article  PubMed  CAS  Google Scholar 

  • Joo W, Xu G, Persky NS, Smogorzewska A, Rudge DG, Buzovetsky O, Elledge SJ, Pavletich NP (2011) Structure of the FANCI-FANCD2 complex: insights into the Fanconi anemia DNA repair pathway. Science 333(6040):312–316

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kalb R, Mallery DL, Larkin C, Huang JT, Hiom K (2014) BRCA1 is a histone-H2A-specific ubiquitin ligase. Cell Rep 8(4):999–1005

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kamiuchi S, Saijo M, Citterio E, de Jager M, Hoeijmakers JH, Tanaka K (2002) Translocation of Cockayne syndrome group A protein to the nuclear matrix: possible relevance to transcription-coupled DNA repair. Proc Natl Acad Sci U S A 99(1):201–206

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapić-Otrin V, Levine AS (2006) The DDB1-CUL4ADDB2 ubiquitin ligase is deficient in xeroderma pigmentosum group E and targets histone H2A at UV-damaged DNA sites. Proc Natl Acad Sci U S A 103(8):2588–2593

    Article  PubMed  CAS  Google Scholar 

  • Kee Y, D’Andrea AD (2012) Molecular pathogenesis and clinical management of Fanconi anemia. J Clin Invest 122(11):3799–3806

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159–180

    Article  PubMed  CAS  Google Scholar 

  • Kim H, D’Andrea AD (2012) Regulation of DNA cross-link repair by the Fanconi anemia/BRCA pathway. Genes Dev 26(13):1393–1408

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim JM, Kee Y, Gurtan A, D’Andrea AD (2008) Cell cycle-dependent chromatin loading of the Fanconi anemia core complex by FANCM/FAAP24. Blood 111(10):5215–5222

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Kim H, Yang K, Dejsuphong D, D’Andrea AD (2012) Regulation of Rev1 by the Fanconi anemia core complex. Nat Struct Mol Biol 19(2):164–170

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Klein Douwel D, Boonen RA, Long DT, Szypowska AA, Raschle M, Walter JC, Knipscheer P (2014) XPF-ERCC1 acts in unhooking DNA interstrand crosslinks in cooperation with FANCD2 and FANCP/SLX4. Mol Cell 54(3):460–471

    Article  PubMed  CAS  Google Scholar 

  • Komander D, Rape M (2012) The ubiquitin code. Annu Rev Biochem 81(1):203–229

    Article  PubMed  CAS  Google Scholar 

  • Kratz K, Schopf B, Kaden S, Sendoel A, Eberhard R, Lademann C, Cannavo E, Sartori AA, Hengartner MO, Jiricny J (2010) Deficiency of FANCD2-associated nuclease KIAA1018/FAN1 sensitizes cells to interstrand crosslinking agents. Cell 142(1):77–88

    Article  PubMed  CAS  Google Scholar 

  • Kulathu Y, Komander D (2012) Atypical ubiquitylation – the unexplored world of polyubiquitin beyond Lys48 and Lys63 linkages. Nat Rev Mol Cell Biol 13(8):508–523

    Article  PubMed  CAS  Google Scholar 

  • Lan L, Nakajima S, Kapetanaki MG, Hsieh CL, Fagerburg M, Thickman K, Rodriguez-Collazo P, Leuba SH, Levine AS, Rapic-Otrin V (2012) Monoubiquitinated histone H2A destabilizes photolesion-containing nucleosomes with concomitant release of UV-damaged DNA-binding protein E3 ligase. J Biol Chem 287(15):12036–12049

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lee J, Zhou P (2007) DCAFs, the missing link of the CUL4-DDB1 ubiquitin ligase. Mol Cell 26(6):775–780

    Article  PubMed  CAS  Google Scholar 

  • Leongamornlert D, Mahmud N, Tymrakiewicz M, Saunders E, Dadaev T, Castro E, Goh C, Govindasami K, Guy M, Brien LO, Sawyer E, Hall A, Wilkinson R, Easton D, Collaborators TU, Goldgar D, Eeles R, Kote-Jarai Z (2012) Germline BRCA1 mutations increase prostate cancer risk. British J Cancer 106(10):1697–1701

    Article  CAS  Google Scholar 

  • Leung JW, Wang Y, Fong KW, Huen MS, Li L, Chen J (2012) Fanconi anemia (FA) binding protein FAAP20 stabilizes FA complementation group A (FANCA) and participates in interstrand cross-link repair. Proc Natl Acad Sci U S A 109(12):4491–4496

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Li T, Chen X, Garbutt KC, Zhou P, Zheng N (2006) Structure of DDB1 in complex with a paramyxovirus V protein: viral hijack of a propeller cluster in ubiquitin ligase. Cell 124(1):105–117

    Article  PubMed  CAS  Google Scholar 

  • Liede A (2004) Cancer risks for male carriers of germline mutations in BRCA1 or BRCA2: a review of the literature. J Clin Oncol 22(4):735–742

    Article  PubMed  CAS  Google Scholar 

  • Lindahl T, Wood RD (1999) Quality control by DNA repair. Science 286(5446):1897–1905

    Article  PubMed  CAS  Google Scholar 

  • Lingaraju GM, Bunker RD, Cavadini S, Hess D, Hassiepen U, Renatus M, Fischer ES, Thoma NH (2014) Crystal structure of the human COP9 signalosome. Nature 512(7513):161–165

    Article  PubMed  CAS  Google Scholar 

  • Liu T, Ghosal G, Yuan J, Chen J, Huang J (2010) FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329(5992):693–696

    Article  PubMed  CAS  Google Scholar 

  • Longerich S, San Filippo J, Liu D, Sung P (2009) FANCI binds branched DNA and is monoubiquitinated by UBE2T-FANCL. J Biol Chem 284(35):23182–23186

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Lyapina S, Cope G, Shevchenko A, Serino G, Tsuge T, Zhou C, Wolf DA, Wei N, Shevchenko A, Deshaies RJ (2001) Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science 292(5520):1382–1385

    Article  PubMed  CAS  Google Scholar 

  • MacKay C, Declais AC, Lundin C, Agostinho A, Deans AJ, MacArtney TJ, Hofmann K, Gartner A, West SC, Helleday T, Lilley DM, Rouse J (2010) Identification of KIAA1018/FAN1, a DNA repair nuclease recruited to DNA damage by monoubiquitinated FANCD2. Cell 142(1):65–76

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mattiroli F, Vissers JHA, van Dijk WJ, Ikpa P, Citterio E, Vermeulen W, Marteijn JA, Sixma TK (2012) RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 150(6):1182–1195

    Article  PubMed  CAS  Google Scholar 

  • Meetei AR, de Winter JP, Medhurst AL, Wallisch M, Waisfisz Q, van de Vrugt HJ, Oostra AB, Yan Z, Ling C, Bishop CE, Hoatlin ME, Joenje H, Wang W (2003) A novel ubiquitin ligase is deficient in Fanconi anemia. Nat Genet 35(2):165–170

    Article  PubMed  CAS  Google Scholar 

  • Min J, Pavletich N (2007) Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature 449(7162):570–575

    Article  PubMed  CAS  Google Scholar 

  • Mirchandani KD, McCaffrey RM, D’Andrea AD (2008) The Fanconi anemia core complex is required for efficient point mutagenesis and Rev1 foci assembly. DNA Repair (Amst) 7(6):902–911

    Article  CAS  Google Scholar 

  • Miskinyte S, Butler MG, Hervé D, Sarret C, Nicolino M, Petralia JD, Bergametti F, Arnould M, Pham VN, Gore AV, Spengos K, Gazal S, Woimant F, Steinberg GK, Weinstein BM, Tournier-Lasserve E (2011) Loss of BRCC3 deubiquitinating enzyme leads to abnormal angiogenesis and is associated with syndromic moyamoya. Am J Hum Genet 88(6):718–728

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Mok MTS, Henderson BR (2012) The in vivo dynamic organization of BRCA1-A complex proteins at DNA damage-induced nuclear foci. Traffic 13(6):800–814

    Article  PubMed  CAS  Google Scholar 

  • Morimoto M, Nishida T, Honda R, Yasuda H (2000) Modification of cullin-1 by ubiquitin-like protein Nedd8 enhances the activity of SCF(skp2) toward p27(kip1). Biochem Biophys Res Commun 270(3):1093–1096

    Article  PubMed  CAS  Google Scholar 

  • Moser J, Volker M, Kool H, Alekseev S, Vrieling H, Yasui A, van Zeeland A, Mullenders L (2005) The UV-damaged DNA binding protein mediates efficient targeting of the nucleotide excision repair complex to UV-induced photo lesions. DNA Repair (Amst) 4(5):571–582

    Article  CAS  Google Scholar 

  • Mundt KE, Porte J, Murray JM, Brikos C, Christensen PU, Caspari T, Hagan IM, Millar JB, Simanis V, Hofmann K, Carr AM (1999) The COP9/signalosome complex is conserved in fission yeast and has a role in S phase. Curr Biol 9(23):1427–1430

    Article  PubMed  CAS  Google Scholar 

  • Mundt KE, Liu C, Carr AM (2002) Deletion mutants in COP9/signalosome subunits in fission yeast Schizosaccharomyces pombe display distinct phenotypes. Mol Biol Cell 13(2):493–502

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Munoz IM, Hain K, Declais AC, Gardiner M, Toh GW, Sanchez-Pulido L, Heuckmann JM, Toth R, Macartney T, Eppink B, Kanaar R, Ponting CP, Lilley DM, Rouse J (2009) Coordination of structure-specific nucleases by human SLX4/BTBD12 is required for DNA repair. Mol Cell 35(1):116–127

    Article  PubMed  CAS  Google Scholar 

  • Nag A, Bondar T, Shiv S, Raychaudhuri P (2001) The xeroderma pigmentosum group E gene product DDB2 is a specific target of cullin 4A in mammalian cells. Mol Cell Biol 21(20):6738–6747

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Nakazawa Y, Sasaki K, Mitsutake N, Matsuse M, Shimada M, Nardo T, Takahashi Y, Ohyama K, Ito K, Mishima H, Nomura M, Kinoshita A, Ono S, Takenaka K, Masuyama R, Kudo T, Slor H, Utani A, Tateishi S, Yamashita S, Stefanini M, Lehmann AR, Yoshiura K, Ogi T (2012) Mutations in UVSSA cause UV-sensitive syndrome and impair RNA polymerase IIo processing in transcription-coupled nucleotide-excision repair. Nat Genet 44(5):586–592

    Article  PubMed  CAS  Google Scholar 

  • Niedzwiedz W, Mosedale G, Johnson M, Ong CY, Pace P, Patel KJ (2004) The Fanconi anaemia gene FANCC promotes homologous recombination and error-prone DNA repair. Mol Cell 15(4):607–620

    Article  PubMed  CAS  Google Scholar 

  • Nijman SM, Huang TT, Dirac AM, Brummelkamp TR, Kerkhoven RM, D’Andrea AD, Bernards R (2005) The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell 17(3):331–339

    Article  PubMed  CAS  Google Scholar 

  • Nikkila J, Coleman KA, Morrissey D, Pylkas K, Erkko H, Messick TE, Karppinen S-M, Amelina A, Winqvist R, Greenberg RA (2009) Familial breast cancer screening reveals an alteration in the RAP80 UIM domain that impairs DNA damage response function. Oncogene 28(16):1843–1852

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Palle K, Vaziri C (2011) Rad18 E3 ubiquitin ligase activity mediates Fanconi anemia pathway activation and cell survival following DNA Topoisomerase 1 inhibition. Cell Cycle 10(10):1625–1638

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pathare GR, Nagy I, Sledz P, Anderson DJ, Zhou HJ, Pardon E, Steyaert J, Forster F, Bracher A, Baumeister W (2014) Crystal structure of the proteasomal deubiquitylation module Rpn8-Rpn11. Proc Natl Acad Sci U S A 111(8):2984–2989

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Patterson-Fortin J, Shao G, Bretscher H, Messick TE, Greenberg RA (2010) Differential regulation of JAMM domain deubiquitinating enzyme activity within the RAP80 complex. J Biol Chem 285(40):30971–30981

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pick E, Golan A, Zimbler JZ, Guo L, Sharaby Y, Tsuge T, Hofmann K, Wei N (2012) The minimal deneddylase core of the COP9 signalosome excludes the Csn6 MPN− domain. PLoS One 7(8), e43980

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Pines A, Vrouwe MG, Marteijn JA, Typas D, Luijsterburg MS, Cansoy M, Hensbergen P, Deelder A, de Groot A, Matsumoto S, Sugasawa K, Thoma N, Vermeulen W, Vrieling H, Mullenders L (2012) PARP1 promotes nucleotide excision repair through DDB2 stabilization and recruitment of ALC1. J Cell Biol 199(2):235–249

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Podust VN, Brownell JE, Gladysheva TB, Luo RS, Wang C, Coggins MB, Pierce JW, Lightcap ES, Chau V (2000) A Nedd8 conjugation pathway is essential for proteolytic targeting of p27Kip1 by ubiquitination. Proc Natl Acad Sci U S A 97(9):4579–4584

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Puumalainen MR, Lessel D, Ruthemann P, Kaczmarek N, Bachmann K, Ramadan K, Naegeli H (2014) Chromatin retention of DNA damage sensors DDB2 and XPC through loss of p97 segregase causes genotoxicity. Nat Commun 5:3695

    Article  PubMed Central  PubMed  Google Scholar 

  • Py BF, Kim M-S, Vakifahmetoglu-Norberg H, Yuan J (2013) Deubiquitination of NLRP3 by BRCC3 critically regulates inflammasome activity. Mol Cell 49(2):331–338

    Article  PubMed  CAS  Google Scholar 

  • Rajendra E, Oestergaard VH, Langevin F, Wang M, Dornan GL, Patel KJ, Passmore LA (2014) The genetic and biochemical basis of FANCD2 monoubiquitination. Mol Cell 54(5):858–869

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Raschle M, Knipscheer P, Enoiu M, Angelov T, Sun J, Griffith JD, Ellenberger TE, Scharer OD, Walter JC (2008) Mechanism of replication-coupled DNA interstrand crosslink repair. Cell 134(6):969–980

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Read MA, Brownell JE, Gladysheva TB, Hottelet M, Parent LA, Coggins MB, Pierce JW, Podust VN, Luo RS, Chau V, Palombella VJ (2000) Nedd8 modification of cul-1 activates SCF(beta(TrCP))-dependent ubiquitination of IkappaBalpha. Mol Cell Biol 20(7):2326–2333

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Reid LJ, Shakya R, Modi AP, Lokshin M, Cheng J-T, Jasin M, Baer R, Ludwig T (2008) E3 ligase activity of BRCA1 is not essential for mammalian cell viability or homology-directed repair of double-strand DNA breaks. Proc Natl Acad Sci U S A 105(52):20876–20881

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Reyes-Turcu FE, Ventii KH, Wilkinson KD (2009) Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu Rev Biochem 78:363–397

    Article  PubMed  CAS  Google Scholar 

  • Sarikas A, Hartmann T, Pan ZQ (2011) The cullin protein family. Genome Biol 12(4):220

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sato Y, Yoshikawa A, Yamagata A, Mimura H, Yamashita M, Ookata K, Nureki O, Iwai K, Komada M, Fukai S (2008) Structural basis for specific cleavage of Lys 63-linked polyubiquitin chains. Nature 455(7211):358–362

    Article  PubMed  CAS  Google Scholar 

  • Sato Y, Yoshikawa A, Mimura H, Yamashita M, Yamagata A, Fukai S (2009) Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80. EMBO J 28(16):2461–2468

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Scheffner M, Nuber U, Huibregtse JM (1995) Protein ubiquitination involving an E1-E2-E3 enzyme ubiquitin thioester cascade. Nature 373(6509):81–83

    Article  PubMed  CAS  Google Scholar 

  • Schwechheimer C, Serino G, Callis J, Crosby WL, Lyapina S, Deshaies RJ, Gray WM, Estelle M, Deng XW (2001) Interactions of the COP9 signalosome with the E3 ubiquitin ligase SCFTIRI in mediating auxin response. Science 292(5520):1379–1382

    Article  PubMed  CAS  Google Scholar 

  • Schwertman P, Lagarou A, Dekkers DH, Raams A, van der Hoek AC, Laffeber C, Hoeijmakers JH, Demmers JA, Fousteri M, Vermeulen W, Marteijn JA (2012) UV-sensitive syndrome protein UVSSA recruits USP7 to regulate transcription-coupled repair. Nat Genet 44(5):598–602

    Article  PubMed  CAS  Google Scholar 

  • Scrima A, Konícková R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP, Thomä NH (2008) Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135(7):1213–1223

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shao G, Lilli DR, Patterson-Fortin J, Coleman KA, Morrissey DE, Greenberg RA (2009a) The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci U S A 106(9):3166–3171

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Shao G, Patterson-Fortin J, Messick TE, Feng D, Shanbhag N, Wang Y, Greenberg RA (2009b) MERIT40 controls BRCA1-Rap80 complex integrity and recruitment to DNA double-strand breaks. Genes Dev 23(6):740–754

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sharon M, Mao H, Boeri Erba E, Stephens E, Zheng N, Robinson CV (2009) Symmetrical modularity of the COP9 signalosome complex suggests its multifunctionality. Structure 17(1):31–40

    Article  PubMed  CAS  Google Scholar 

  • Shiyanov P, Nag A, Raychaudhuri P (1999) Cullin 4A associates with the UV-damaged DNA-binding protein DDB. J Biol Chem 274(50):35309–35312

    Article  PubMed  CAS  Google Scholar 

  • Sims JJ, Cohen RE (2009) Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of Rap80. Mol Cell 33(6):775–783

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Singh TR, Saro D, Ali AM, Zheng XF, Du CH, Killen MW, Sachpatzidis A, Wahengbam K, Pierce AJ, Xiong Y, Sung P, Meetei AR (2010) MHF1-MHF2, a histone-fold-containing protein complex, participates in the Fanconi anemia pathway via FANCM. Mol Cell 37(6):879–886

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Smogorzewska A, Desetty R, Saito TT, Schlabach M, Lach FP, Sowa ME, Clark AB, Kunkel TA, Harper JW, Colaiacovo MP, Elledge SJ (2010) A genetic screen identifies FAN1, a Fanconi anemia-associated nuclease necessary for DNA interstrand crosslink repair. Mol Cell 39(1):36–47

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Solyom S, Aressy B, Pylkas K, Patterson-Fortin J, Hartikainen JM, Kallioniemi A, Kauppila S, Nikkila J, Kosma VM, Mannermaa A, Greenberg RA, Winqvist R (2012) Breast cancer-associated Abraxas mutation disrupts nuclear localization and DNA damage response functions. Sci Transl Med 4(122):122–123

    Article  CAS  Google Scholar 

  • Sugasawa K, Hanaoka F (2007) Sensing of DNA damage by XPC/Rad4: one protein for many lesions. Nat Struct Mol Biol 14(10):887–888

    Article  PubMed  CAS  Google Scholar 

  • Sugasawa K, Ng JM, Masutani C, Iwai S, van der Spek PJ, Eker AP, Hanaoka F, Bootsma D, Hoeijmakers JH (1998) Xeroderma pigmentosum group C protein complex is the initiator of global genome nucleotide excision repair. Mol Cell 2(2):223–232

    Article  PubMed  CAS  Google Scholar 

  • Sugasawa K, Okamoto T, Shimizu Y, Masutani C, Iwai S, Hanaoka F (2001) A multistep damage recognition mechanism for global genomic nucleotide excision repair. Genes Dev 15(5):507–521

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G, Mori T, Iwai S, Tanaka K, Tanaka K, Hanaoka F (2005) UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121(3):387–400

    Article  PubMed  CAS  Google Scholar 

  • Svejstrup JQ (2002) Mechanisms of transcription-coupled DNA repair. Nat Rev Mol Cell Biol 3(1):21–29

    Article  PubMed  CAS  Google Scholar 

  • Svendsen JM, Smogorzewska A, Sowa ME, O’Connell BC, Gygi SP, Elledge SJ, Harper JW (2009) Mammalian BTBD12/SLX4 assembles a Holliday junction resolvase and is required for DNA repair. Cell 138(1):63–77

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Takao M, Abramic M, Moos M, Otrin V, Wootton J, McLenigan M, Levine A, Protic M (1993) A 127 kDa component of a UV-damaged DNA-binding complex, which is defective in some xeroderma pigmentosum group E patients, is homologous to a slime mold protein. Nucleic Acids Res 21(17):4111–4118

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Tremblay CS, Huang FF, Habi O, Huard CC, Godin C, Levesque G, Carreau M (2008) HES1 is a novel interactor of the Fanconi anemia core complex. Blood 112(5):2062–2070

    Article  PubMed  CAS  Google Scholar 

  • van Gool AJ, Citterio E, Rademakers S, van Os R, Vermeulen W, Constantinou A, Egly JM, Bootsma D, Hoeijmakers JH (1997) The Cockayne syndrome B protein, involved in transcription-coupled DNA repair, resides in an RNA polymerase II-containing complex. EMBO J 16(19):5955–5965

    Article  PubMed Central  PubMed  Google Scholar 

  • Vikrant KR, Yadav LR, Nakhwa P, Waghmare SK, Goyal P, Varma AK (2013a) Structural and functional implication of RAP80 ΔGlu81 mutation. PLoS One 8(9), e72707

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Vikrant NP, Badgujar DC, Kumar R, Rathore KKS, Varma AK (2013b) Structural and functional characterization of the MERIT40 to understand its role in DNA repair. J Biomol Struct Dyn 1–16

    Google Scholar 

  • Wang B, Elledge SJ (2007) 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 104(52):20759–20763

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wang H, Zhai L, Xu J, Joo H, Jackson S, Erdjument-Bromage H, Tempst P, Xiong Y, Zhang Y (2006) Histone H3 and H4 ubiquitylation by the CUL4-DDB-ROC1 ubiquitin ligase facilitates cellular response to DNA damage. Mol Cell 22(3):383–394

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Matsuoka S, Ballif BA, Zhang D, Smogorzewska A, Gygi SP, Elledge SJ (2007) Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science 316(5828):1194–1198

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Wei N, Serino G, Deng XW (2008) The COP9 signalosome: more than a protease. Trends Biochem Sci 33(12):592–600

    Article  PubMed  CAS  Google Scholar 

  • Williams SA, Longerich S, Sung P, Vaziri C, Kupfer GM (2011) The E3 ubiquitin ligase RAD18 regulates ubiquitylation and chromatin loading of FANCD2 and FANCI. Blood 117(19):5078–5087

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Worden EJ, Padovani C, Martin A (2014) Structure of the Rpn11–Rpn8 dimer reveals mechanisms of substrate deubiquitination during proteasomal degradation. Nat Struct Mol Biol 21(3):220–227

    Article  PubMed  CAS  Google Scholar 

  • Wu K, Chen A, Pan ZQ (2000) Conjugation of Nedd8 to CUL1 enhances the ability of the ROC1-CUL1 complex to promote ubiquitin polymerization. J Biol Chem 275(41):32317–32324

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Liu C, Chen J, Yu X (2012) RAP80 protein is important for genomic stability and is required for stabilizing BRCA1-A complex at DNA damage sites in vivo. J Biol Chem 287(27):22919–22926

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yan Z, Delannoy M, Ling C, Daee D, Osman F, Muniandy PA, Shen X, Oostra AB, Du H, Steltenpool J, Lin T, Schuster B, Decaillet C, Stasiak A, Stasiak AZ, Stone S, Hoatlin ME, Schindler D, Woodcock CL, Joenje H, Sen R, de Winter JP, Li L, Seidman MM, Whitby MC, Myung K, Constantinou A, Wang W (2010) A histone-fold complex and FANCM form a conserved DNA-remodeling complex to maintain genome stability. Mol Cell 37(6):865–878

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yang H, Zhang T, Tao Y, Wang F, Tong L, Ding J (2013) Structural insights into the functions of the FANCM-FAAP24 complex in DNA repair. Nucleic Acids Res 41(22):10573–10583

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yasuda T, Sugasawa K, Shimizu Y, Iwai S, Shiomi T, Hanaoka F (2005) Nucleosomal structure of undamaged DNA regions suppresses the non-specific DNA binding of the XPC complex. DNA Repair (Amst) 4(3):389–395

    Article  CAS  Google Scholar 

  • Yeh JI, Levine AS, Du S, Chinte U, Ghodke H, Wang H, Shi H, Hsieh CL, Conway JF, Van Houten B, Rapic-Otrin V (2012) Damaged DNA induced UV-damaged DNA-binding protein (UV-DDB) dimerization and its roles in chromatinized DNA repair. Proc Natl Acad Sci U S A 109(41):E2737–E2746

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Yin Z, Menendez D, Resnick MA, French JE, Janardhan KS, Jetten AM (2012) RAP80 is critical in maintaining genomic stability and suppressing tumor development. Cancer Res 72(19):5080–5090

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang J, Walter JC (2014) Mechanism and regulation of incisions during DNA interstrand cross-link repair. DNA Repair (Amst) 19:135–142

    Article  CAS  Google Scholar 

  • Zhang L, Lubin A, Chen H, Sun Z, Gong F (2012a) The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability. Cell Cycle 11(23):4378–4384

    Article  PubMed Central  PubMed  CAS  Google Scholar 

  • Zhang X, Horibata K, Saijo M, Ishigami C, Ukai A, Kanno S, Tahara H, Neilan EG, Honma M, Nohmi T, Yasui A, Tanaka K (2012b) Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat Genet 44(5):593–597

    Article  PubMed  CAS  Google Scholar 

  • Zheng H, Gupta V, Patterson-Fortin J, Bhattacharya S, Katlinski K, Wu J, Varghese B, Carbone CJ, Aressy B, Fuchs SY, Greenberg RA (2013) A BRISC-SHMT complex deubiquitinates IFNAR1 and regulates interferon responses. Cell Rep 5(1):180–193

    Article  PubMed  CAS  Google Scholar 

  • Zimmerman ES, Schulman BA, Zheng N (2010) Structural assembly of cullin-RING ubiquitin ligase complexes. Curr Opin Struct Biol 20(6):714–721

    Article  PubMed Central  PubMed  CAS  Google Scholar 

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Lingaraju, G.M. et al. (2016). The Crossroads of Ubiquitination and DNA Repair: A Structural Perspective. In: Hanaoka, F., Sugasawa, K. (eds) DNA Replication, Recombination, and Repair. Springer, Tokyo. https://doi.org/10.1007/978-4-431-55873-6_9

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