Spatiotemporal regulation of posttranslational modifications in the DNA damage response

EMBO Journal

Volumn 35, Issue 1, 2016, Pages 6-23

  Dantuma, Nico P ^a   Van Attikum, Haico ^b  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

chromatin; DNA repair; Poly(ADP ribosyl)ation; SUMO; ubiquitin

Indexed keywords

ATM PROTEIN; ATR PROTEIN; COP9 SIGNALOSOME; CULLIN; DNA; DOUBLE STRANDED DNA; HISTONE ACETYLTRANSFERASE; HISTONE H1; HISTONE H2A; HISTONE H2AX; HISTONE H3; HISTONE H4; HISTONE METHYLTRANSFERASE; NEDD8 PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE 1; POLY(ADENOSINE DIPHOSPHATE RIBOSE); POLYCOMB GROUP PROTEIN; POLYUBIQUITIN; PROTEIN KINASE C; PROTEIN RNF168; RNA POLYMERASE II; SUMO 2 PROTEIN; SUMO TARGETED UBIQUITIN LIGASE; TRANSCRIPTION ELONGATION FACTOR; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG; HISTONE; NONHISTONE PROTEIN;

ADENOSINE DIPHOSPHATE RIBOSYLATION; DNA DAMAGE; DNA DAMAGE RESPONSE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; EXCISION REPAIR; GENOME; HOMOLOGOUS RECOMBINATION; HUMAN; NEDDYLATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ACETYLATION; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; REVIEW; SUMOYLATION; UBIQUITINATION; ANIMAL; DNA REPAIR; GENE EXPRESSION REGULATION; METABOLISM; SPATIOTEMPORAL ANALYSIS;

ANIMALS; CHROMOSOMAL PROTEINS, NON-HISTONE; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION; HISTONES; HUMANS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SPATIO-TEMPORAL ANALYSIS;

EID: 84955326867     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.15252/embj.201592595     Document Type: Review

References (169)

1. Acs K, Luijsterburg MS, Ackermann L, Salomons FA, Hoppe T, Dantuma NP, (2011) The AAA-ATPase VCP/p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks. Nat Struct Mol Biol 18: 1345-1350
2. Ahel D, Horejsi Z, Wiechens N, Polo SE, Garcia-Wilson E, Ahel I, Flynn H, Skehel M, West SC, Jackson SP, Owen-Hughes T, Boulton SJ, (2009) Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1. Science 325: 1240-1243
3. Ali AA, Timinszky G, Arribas-Bosacoma R, Kozlowski M, Hassa PO, Hassler M, Ladurner AG, Pearl LH, Oliver AW, (2012) The zinc-finger domains of PARP1 cooperate to recognize DNA strand breaks. Nat Struct Mol Biol 19: 685-692
4. Altmeyer M, Neelsen KJ, Teloni F, Pozdnyakova I, Pellegrino S, Grofte M, Rask MB, Streicher W, Jungmichel S, Nielsen ML, Lukas J, (2015) Liquid demixing of intrinsically disordered proteins is seeded by poly(ADP-ribose). Nat Commun 6: 8088
5. 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: 128-135
6. Ayrapetov MK, Gursoy-Yuzugullu O, Xu C, Xu Y, Price BD, (2014) DNA double-strand breaks promote methylation of histone H3 on lysine 9 and transient formation of repressive chromatin. Proc Natl Acad Sci USA 111: 9169-9174
7. Beck C, Robert I, Reina-San-Martin B, Schreiber V, Dantzer F, (2014) Poly(ADP-ribose) polymerases in double-strand break repair: focus on PARP1, PARP2 and PARP3. Exp Cell Res 329: 18-25
8. Bekker-Jensen S, Rendtlew Danielsen J, Fugger K, Gromova I, Nerstedt A, Lukas C, Bartek J, Lukas J, Mailand N, (2010) HERC2 coordinates ubiquitin-dependent assembly of DNA repair factors on damaged chromosomes. Nat Cell Biol 12: 80-86
9. Bekker-Jensen S, Mailand N, (2011) The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks. FEBS Lett 585: 2914-2919
10. Bergink S, Salomons FA, Hoogstraten D, Groothuis TA, de Waard H, Wu J, Yuan L, Citterio E, Houtsmuller AB, Neefjes J, Hoeijmakers JH, Vermeulen W, Dantuma NP, (2006) DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev 20: 1343-1352
11. Botuyan MV, Lee J, Ward IM, Kim JE, Thompson JR, Chen J, Mer G, (2006) Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell 127: 1361-1373
12. Brinkmann K, Schell M, Hoppe T, Kashkar H, (2015) Regulation of the DNA damage response by ubiquitin conjugation. Front Genet 6: 98
13. Brown JS, Lukashchuk N, Sczaniecka-Clift M, Britton S, le Sage C, Calsou P, Beli P, Galanty Y, Jackson SP, (2015) Neddylation Promotes Ubiquitylation and Release of Ku from DNA-Damage Sites. Cell Rep 11: 704-714
14. Caldecott KW, (2014) DNA single-strand break repair. Exp Cell Res 329: 2-8
15. Chapman JR, Taylor MR, Boulton SJ, (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497-510
16. Chen J, Feng W, Jiang J, Deng Y, Huen MS, (2012) Ring finger protein RNF169 antagonizes the ubiquitin-dependent signaling cascade at sites of DNA damage. J Biol Chem 287: 27715-27722
17. Chen WT, Alpert A, Leiter C, Gong F, Jackson SP, Miller KM, (2013) Systematic identification of functional residues in mammalian histone H2AX. Mol Cell Biol 33: 111-126
18. Chou DM, Adamson B, Dephoure NE, Tan X, Nottke AC, Hurov KE, Gygi SP, Colaiacovo MP, Elledge SJ, (2010) A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage. Proc Natl Acad Sci USA 107: 18475-18480
19. van Cuijk L, van Belle GJ, Turkyilmaz Y, Poulsen SL, Janssens RC, Theil AF, Sabatella M, Lans H, Mailand N, Houtsmuller AB, Vermeulen W, Marteijn JA, (2015) SUMO and ubiquitin-dependent XPC exchange drives nucleotide excision repair. Nat Commun 6: 7499
20. van Cuijk L, Vermeulen W, Marteijn JA, (2014) Ubiquitin at work: the ubiquitous regulation of the damage recognition step of NER. Exp Cell Res 329: 101-109
21. Dantuma NP, Hoppe T, (2012) Growing sphere of influence: Cdc48/p97 orchestrates ubiquitin-dependent extraction from chromatin. Trends Cell Biol 22: 483-491
22. Dantuma NP, Acs K, Luijsterburg MS, (2014) Should I stay or should I go: VCP/p97-mediated chromatin extraction in the DNA damage response. Exp Cell Res 329: 9-17
23. DaRosa PA, Wang Z, Jiang X, Pruneda JN, Cong F, Klevit RE, Xu W, (2015) Allosteric activation of the RNF146 ubiquitin ligase by a poly(ADP-ribosyl)ation signal. Nature 517: 223-226
24. Dijk M, Typas D, Mullenders L, Pines A, (2014) Insight in the multilevel regulation of NER. Exp Cell Res 329: 116-123
25. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J, Lukas J, Lukas C, (2009) RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136: 435-446
26. 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: 78-89
27. Feng L, Chen J, (2012) The E3 ligase RNF8 regulates KU80 removal and NHEJ repair. Nat Struct Mol Biol 19: 201-206
28. Fischle W, Wang Y, Jacobs SA, Kim Y, Allis CD, Khorasanizadeh S, (2003) Molecular basis for the discrimination of repressive methyl-lysine marks in histone H3 by Polycomb and HP1 chromodomains. Genes Dev 17: 1870-1881
29. Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H, Landry MC, Kitevski-LeBlanc J, Noordermeer SM, Sicheri F, Durocher D, (2013) 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499: 50-54
30. Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP, (2009) Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462: 935-939
31. Galanty Y, Belotserkovskaya R, Coates J, Jackson SP, (2012) RNF4, a SUMO-targeted ubiquitin E3 ligase, promotes DNA double-strand break repair. Genes Dev 26: 1179-1195
32. Gatti M, Pinato S, Maspero E, Soffientini P, Polo S, Penengo L, (2012) A novel ubiquitin mark at the N-terminal tail of histone H2As targeted by RNF168 ubiquitin ligase. Cell Cycle 11: 2538-2544
33. Gatti M, Pinato S, Maiolica A, Rocchio F, Prato MG, Aebersold R, Penengo L, (2015) RNF168 promotes noncanonical K27 ubiquitination to signal DNA damage. Cell Rep 10: 226-238
34. Ginjala V, Nacerddine K, Kulkarni A, Oza J, Hill SJ, Yao M, Citterio E, van Lohuizen M, Ganesan S, (2011) BMI1 is recruited to DNA breaks and contributes to DNA damage-induced H2A ubiquitination and repair. Mol Cell Biol 31: 1972-1982
35. Giunta S, Belotserkovskaya R, Jackson SP, (2010) DNA damage signaling in response to double-strand breaks during mitosis. J Cell Biol 190: 197-207
36. Gonzalez-Prieto R, Cuijpers SA, Luijsterburg MS, van Attikum H, Vertegaal AC, (2015) SUMOylation and PARylation cooperate to recruit and stabilize SLX4 at DNA damage sites. EMBO Rep 16: 512-519
37. Gottschalk AJ, Timinszky G, Kong SE, Jin J, Cai Y, Swanson SK, Washburn MP, Florens L, Ladurner AG, Conaway JW, Conaway RC, (2009) Poly(ADP-ribosyl)ation directs recruitment and activation of an ATP-dependent chromatin remodeler. Proc Natl Acad Sci USA 106: 13770-13774
38. Groisman R, Polanowska J, Kuraoka I, Sawada J, Saijo M, Drapkin R, Kisselev AF, 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: 357-367
39. Groocock LM, Nie M, Prudden J, Moiani D, Wang T, Cheltsov A, Rambo RP, Arvai AS, Hitomi C, Tainer JA, Luger K, Perry JJ, Lazzerini-Denchi E, Boddy MN, (2014) RNF4 interacts with both SUMO and nucleosomes to promote the DNA damage response. EMBO Rep 15: 601-608
40. Gudjonsson T, Altmeyer M, Savic V, Toledo L, Dinant C, Grofte M, Bartkova J, Poulsen M, Oka Y, Bekker-Jensen S, Mailand N, Neumann B, Heriche JK, Shearer R, Saunders D, Bartek J, Lukas J, Lukas C, (2012) TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150: 697-709
41. Guervilly J, Takedachi A, Naim V, Scaglione S, Chawhan C, Lovera Y, Despras E, Kuraoka I, Kannouche P, Rosselli F, Gaillard PL, (2015) The SLX4 Complex Is a SUMO E3 Ligase that Impacts on Replication Stress Outcome and Genome Stability. Mol Cell 57: 123-137
42. 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: ra88
43. Hakme A, Wong HK, Dantzer F, Schreiber V, (2008) The expanding field of poly(ADP-ribosyl)ation reactions. 'Protein Modifications: beyond the Usual Suspects' Review Series. EMBO Rep 9: 1094-1100
44. Hay RT, (2005) SUMO: a history of modification. Mol Cell 18: 1-12
45. Hendriks IA, Treffers LW, Verlaan-de Vries M, Olsen JV, Vertegaal AC, (2015) SUMO-2 Orchestrates Chromatin Modifiers in Response to DNA Damage. Cell Rep 10: 1778-1791
46. Hershko A, Ciechanover A, (1998) The ubiquitin system. Annu Rev Biochem 67: 425-479
47. 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: 135-141
48. Hsiao KY, Mizzen CA, (2013) Histone H4 deacetylation facilitates 53BP1 DNA damage signaling and double-strand break repair. J Mol Cell Biol 5: 157-165
49. Hu Y, Scully R, Sobhian B, Xie A, Shestakova E, Livingston DM, (2011) RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev 25: 685-700
50. Huang J, Huen MS, Kim H, Leung CC, Glover JN, Yu X, Chen J, (2009) RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat Cell Biol 11: 592-603
51. Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J, (2007) RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 131: 901-914
52. Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, Trouche D, Legube G, (2010) High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. EMBO J 29: 1446-1457
53. Ismail IH, Gagne JP, Caron MC, McDonald D, Xu Z, Masson JY, Poirier GG, Hendzel MJ, (2012) CBX4-mediated SUMO modification regulates BMI1 recruitment at sites of DNA damage. Nucleic Acids Res 40: 5497-5510
54. Ito K, Adachi S, Iwakami R, Yasuda H, Muto Y, Seki N, Okano Y, (2001) N-Terminally extended human ubiquitin-conjugating enzymes (E2s) mediate the ubiquitination of RING-finger proteins, ARA54 and RNF8. Eur J Biochem 268: 2725-2732
55. Jackson SP, Bartek J, (2009) The DNA-damage response in human biology and disease. Nature 461: 1071-1078
56. Jansen JG, Tsaalbi-Shtylik A, de Wind N, (2015) Roles of mutagenic translesion synthesis in mammalian genome stability, health and disease. DNA Repair (Amst) 29: 56-64
57. Jentsch S, Pyrowolakis G, (2000) Ubiquitin and its kin: how close are the family ties? Trends Cell Biol 10: 335-342
58. Jentsch S, Psakhye I, (2013) Control of nuclear activities by substrate-selective and protein-group SUMOylation. Annu Rev Genet 47: 167-186
59. Jungmichel S, Rosenthal F, Altmeyer M, Lukas J, Hottiger MO, Nielsen ML, (2013) Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses. Mol Cell 52: 272-285
60. Kaidi A, Jackson SP, (2013) KAT5 tyrosine phosphorylation couples chromatin sensing to ATM signalling. Nature 498: 70-74
61. Kakarougkas A, Ismail A, Chambers AL, Riballo E, Herbert AD, Kunzel J, Lobrich M, Jeggo PA, Downs JA, (2014) Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin. Mol Cell 55: 723-732
62. Kalb R, Mallery DL, Larkin C, Huang JT, Hiom K, (2014) BRCA1 is a histone-H2A-specific ubiquitin ligase. Cell Rep 8: 999-1005
63. Kang HC, Lee YI, Shin JH, Andrabi SA, Chi Z, Gagne JP, Lee Y, Ko HS, Lee BD, Poirier GG, Dawson VL, Dawson TM, (2011) Iduna is a poly(ADP-ribose) (PAR)-dependent E3 ubiquitin ligase that regulates DNA damage. Proc Natl Acad Sci USA 108: 14103-14108
64. Kapetanaki MG, Guerrero-Santoro J, Bisi DC, Hsieh CL, Rapic-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 USA 103: 2588-2593
65. Kashima L, Idogawa M, Mita H, Shitashige M, Yamada T, Ogi K, Suzuki H, Toyota M, Ariga H, Sasaki Y, Tokino T, (2012) CHFR protein regulates mitotic checkpoint by targeting PARP-1 protein for ubiquitination and degradation. J Biol Chem 287: 12975-12984
66. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM, Pelletier L, Jackson SP, Durocher D, (2007) Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318: 1637-1640
67. Komander D, Rape M, (2012) The ubiquitin code. Annu Rev Biochem 81: 203-229
68. Kraus WL, (2008) Transcriptional control by PARP-1: chromatin modulation, enhancer-binding, coregulation, and insulation. Curr Opin Cell Biol 20: 294-302
69. Kravtsova-Ivantsiv Y, Ciechanover A, (2012) Non-canonical ubiquitin-based signals for proteasomal degradation. J Cell Sci 125: 539-548
70. Lachaud C, Castor D, Hain K, Munoz I, Wilson J, MacArtney TJ, Schindler D, Rouse J, (2014) Distinct functional roles for the two SLX4 ubiquitin-binding UBZ domains mutated in Fanconi anemia. J Cell Sci 127: 2811-2817
71. Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, Peres L, Zhou J, Zhu J, Raught B, de The H, (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10: 547-555
72. Langelier MF, Planck JL, Roy S, Pascal JM, (2011) Crystal structures of poly(ADP-ribose) polymerase-1 (PARP-1) zinc fingers bound to DNA: structural and functional insights into DNA-dependent PARP-1 activity. J Biol Chem 286: 10690-10701
73. Langelier MF, Pascal JM, (2013) PARP-1 mechanism for coupling DNA damage detection to poly(ADP-ribose) synthesis. Curr Opin Struct Biol 23: 134-143
74. Larsen DH, Poinsignon C, Gudjonsson T, Dinant C, Payne MR, Hari FJ, Danielsen JM, Menard P, Sand JC, Stucki M, Lukas C, Bartek J, Andersen JS, Lukas J, (2010) The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol 190: 731-740
75. Lee DH, Acharya SS, Kwon M, Drane P, Guan Y, Adelmant G, Kalev P, Shah J, Pellman D, Marto JA, Chowdhury D, (2014) Dephosphorylation enables the recruitment of 53BP1 to double-strand DNA breaks. Mol Cell 54: 512-525
76. Leung AK, (2014) Poly(ADP-ribose): an organizer of cellular architecture. J Cell Biol 205: 613-619
77. Leung JW, Agarwal P, Canny MD, Gong F, Robison AD, Finkelstein IJ, Durocher D, Miller KM, (2014) Nucleosome acidic patch promotes RNF168- and RING1B/BMI1-dependent H2AX and H2A ubiquitination and DNA damage signaling. PLoS Genet 10: e1004178
78. Li M, Lu LY, Yang CY, Wang S, Yu X, (2013) The FHA and BRCT domains recognize ADP-ribosylation during DNA damage response. Genes Dev 27: 1752-1768
79. Li M, Yu X, (2013) Function of BRCA1 in the DNA damage response is mediated by ADP-ribosylation. Cancer Cell 23: 693-704
80. Liu C, Wu J, Paudyal SC, You Z, Yu X, (2013) CHFR is important for the first wave of ubiquitination at DNA damage sites. Nucleic Acids Res 41: 1698-1710
81. Lok GT, Sy SM, Dong SS, Ching YP, Tsao SW, Thomson TM, Huen MS, (2012) Differential regulation of RNF8-mediated Lys48- and Lys63-based polyubiquitylation. Nucleic Acids Res 40: 196-205
82. Lord CJ, Ashworth A, (2012) The DNA damage response and cancer therapy. Nature 481: 287-294
83. Lottersberger F, Bothmer A, Robbiani DF, Nussenzweig MC, de Lange T, (2013) Role of 53BP1 oligomerization in regulating double-strand break repair. Proc Natl Acad Sci USA 110: 2146-2151
84. Luijsterburg MS, Goedhart J, Moser J, Kool H, Geverts B, Houtsmuller AB, Mullenders LH, Vermeulen W, van Driel R, (2007) Dynamic in vivo interaction of DDB2 E3 ubiquitin ligase with UV-damaged DNA is independent of damage-recognition protein XPC. J Cell Sci 120: 2706-2716
85. Luijsterburg MS, Acs K, Ackermann L, Wiegant WW, Bekker-Jensen S, Larsen DH, Khanna KK, van Attikum H, Mailand N, Dantuma NP, (2012a) A new non-catalytic role for ubiquitin ligase RNF8 in unfolding higher-order chromatin structure. EMBO J 31: 2511-2527
86. Luijsterburg MS, Lindh M, Acs K, Vrouwe MG, Pines A, van Attikum H, Mullenders LH, Dantuma NP, (2012b) DDB2 promotes chromatin decondensation at UV-induced DNA damage. J Cell Biol 197: 267-281
87. Lukas J, Lukas C, Bartek J, (2011) More than just a focus: the chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13: 1161-1169
88. Luo K, Zhang H, Wang L, Yuan J, Lou Z, (2012) Sumoylation of MDC1 is important for proper DNA damage response. EMBO J 31: 3008-3019
89. Lydeard JR, Schulman BA, Harper JW, (2013) Building and remodelling Cullin-RING E3 ubiquitin ligases. EMBO Rep 14: 1050-1061
90. Ma T, Chen Y, Zhang F, Yang CY, Wang S, Yu X, (2013) RNF111-dependent neddylation activates DNA damage-induced ubiquitination. Mol Cell 49: 897-907
91. Mahajan A, Yuan C, Lee H, Chen ES, Wu PY, Tsai MD, (2008) Structure and function of the phosphothreonine-specific FHA domain. Sci Signal 1: re12.
92. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J, (2007) RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 131: 887-900
93. Mallette FA, Mattiroli F, Cui G, Young LC, Hendzel MJ, Mer G, Sixma TK, Richard S, (2012) RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites. EMBO J 31: 1865-1878
94. Marteijn JA, Bekker-Jensen S, Mailand N, Lans H, Schwertman P, Gourdin AM, Dantuma NP, Lukas J, Vermeulen W, (2009) Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response. J Cell Biol 186: 835-847
95. Mattiroli F, Vissers JH, 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: 1182-1195
96. Marteijn JA, Lans H, Vermeulen W, Hoeijmakers JH, (2014) Understanding nucleotide excision repair and its roles in cancer and ageing. Nat Rev Mol Cell Biol 15: 465-481
97. Mattiroli F, Uckelmann M, Sahtoe DD, van Dijk WJ, Sixma TK, (2014) The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nat Commun 5: 3291
98. McGinty RK, Henrici RC, Tan S, (2014) Crystal structure of the PRC1 ubiquitylation module bound to the nucleosome. Nature 514: 591-596
99. Meerang M, Ritz D, Paliwal S, Garajova Z, Bosshard M, Mailand N, Janscak P, Hubscher U, Meyer H, Ramadan K, (2011) The ubiquitin-selective segregase VCP/p97 orchestrates the response to DNA double-strand breaks. Nat Cell Biol 13: 1376-1382
100. Min J, Zhang Y, Xu RM, (2003) Structural basis for specific binding of Polycomb chromodomain to histone H3 methylated at Lys 27. Genes Dev 17: 1823-1828
101. Moyal L, Lerenthal Y, Gana-Weisz M, Mass G, So S, Wang SY, Eppink B, Chung YM, Shalev G, Shema E, Shkedy D, Smorodinsky NI, van Vliet N, Kuster B, Mann M, Ciechanover A, Dahm-Daphi J, Kanaar R, Hu MC, Chen DJ, et al, (2011) Requirement of ATM-dependent monoubiquitylation of histone H2B for timely repair of DNA double-strand breaks. Mol Cell 41: 529-542
102. 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: 116-127
103. Muratani M, Tansey WP, (2003) How the ubiquitin-proteasome system controls transcription. Nat Rev Mol Cell Biol 4: 192-201
104. Nakamura K, Kato A, Kobayashi J, Yanagihara H, Sakamoto S, Oliveira DV, Shimada M, Tauchi H, Suzuki H, Tashiro S, Zou L, Komatsu K, (2011) Regulation of homologous recombination by RNF20-dependent H2B ubiquitination. Mol Cell 41: 515-528
105. Oberoi J, Richards MW, Crumpler S, Brown N, Blagg J, Bayliss R, (2010) Structural basis of poly(ADP-ribose) recognition by the multizinc binding domain of checkpoint with forkhead-associated and RING Domains (CHFR). J Biol Chem 285: 39348-39358
106. Oestergaard VH, Pentzold C, Pedersen RT, Iosif S, Alpi A, Bekker-Jensen S, Mailand N, Lisby M, (2012) RNF8 and RNF168 but not HERC2 are required for DNA damage-induced ubiquitylation in chicken DT40 cells. DNA Repair (Amst) 11: 892-905
107. Orthwein A, Fradet-Turcotte A, Noordermeer SM, Canny MD, Brun CM, Strecker J, Escribano-Diaz C, Durocher D, (2014) Mitosis inhibits DNA double-strand break repair to guard against telomere fusions. Science 344: 189-193
108. Ouyang J, Garner E, Hallet A, Nguyen HD, Rickman KA, Gill G, Smogorzewska A, Zou L, (2015) Noncovalent Interactions with SUMO and Ubiquitin Orchestrate Distinct Functions of the SLX4 Complex in Genome Maintenance. Mol Cell 57: 108-122
109. Panier S, Ichijima Y, Fradet-Turcotte A, Leung CC, Kaustov L, Arrowsmith CH, Durocher D, (2012) Tandem protein interaction modules organize the ubiquitin-dependent response to DNA double-strand breaks. Mol Cell 47: 383-395
110. Panier S, Boulton SJ, (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15: 7-18
111. Parsons JL, Dianov GL, (2013) Co-ordination of base excision repair and genome stability. DNA Repair (Amst) 12: 326-333
112. Petroski MD, Deshaies RJ, (2005) Function and regulation of cullin-RING ubiquitin ligases. Nat Rev Mol Cell Biol 6: 9-20
113. Petroski MD, Zhou X, Dong G, Daniel-Issakani S, Payan DG, Huang J, (2007) Substrate modification with lysine 63-linked ubiquitin chains through the UBC13-UEV1A ubiquitin-conjugating enzyme. J Biol Chem 282: 29936-29945
114. Pickart CM, (2000) Ubiquitin in chains. Trends Biochem Sci 25: 544-548
115. Pickart CM, (2001) Mechanisms underlying ubiquitination. Annu Rev Biochem 70: 503-533
116. 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: 235-249
117. Pines A, Mullenders LH, van Attikum H, Luijsterburg MS, (2013) Touching base with PARPs: moonlighting in the repair of UV lesions and double-strand breaks. Trends Biochem Sci 38: 321-330
118. Polanowska J, Martin JS, Garcia-Muse T, Petalcorin MI, Boulton SJ, (2006) A conserved pathway to activate BRCA1-dependent ubiquitylation at DNA damage sites. EMBO J 25: 2178-2188
119. Polo SE, Kaidi A, Baskcomb L, Galanty Y, Jackson SP, (2010) Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J 29: 3130-3139
120. Polo SE, Jackson SP, (2011) Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev 25: 409-433
121. 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: 467-479
122. Postow L, (2011) Destroying the ring: freeing DNA from Ku with ubiquitin. FEBS Lett 585: 2876-2882
123. Postow L, Funabiki H, (2013) An SCF complex containing Fbxl12 mediates DNA damage-induced Ku80 ubiquitylation. Cell Cycle 12: 587-595
124. Poulsen M, Lukas C, Lukas J, Bekker-Jensen S, Mailand N, (2012) Human RNF169 is a negative regulator of the ubiquitin-dependent response to DNA double-strand breaks. J Cell Biol 197: 189-199
125. Poulsen SL, Hansen RK, Wagner SA, van Cuijk L, van Belle GJ, Streicher W, Wikstrom M, Choudhary C, Houtsmuller AB, Marteijn JA, Bekker-Jensen S, Mailand N, (2013) RNF111/Arkadia is a SUMO-targeted ubiquitin ligase that facilitates the DNA damage response. J Cell Biol 201: 797-807
126. Prudden J, Pebernard S, Raffa G, Slavin DA, Perry JJ, Tainer JA, McGowan CH, Boddy MN, (2007) SUMO-targeted ubiquitin ligases in genome stability. EMBO J 26: 4089-4101
127. Psakhye I, Jentsch S, (2012) Protein group modification and synergy in the SUMO pathway as exemplified in DNA repair. Cell 151: 807-820
128. 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
129. Ramadan K, (2012) p97/VCP- and Lys48-linked polyubiquitination form a new signaling pathway in DNA damage response. Cell Cycle 11: 1062-1069
130. Ravid T, Hochstrasser M, (2008) Diversity of degradation signals in the ubiquitin-proteasome system. Nat Rev Mol Cell Biol 9: 679-690
131. Reid LJ, Shakya R, Modi AP, Lokshin M, Cheng JT, 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 USA 105: 20876-20881
132. Rendtlew Danielsen J, Povlsen LK, Villumsen BH, Streicher W, Nilsson J, Wikstrom M, Bekker-Jensen S, Mailand N, (2012) DNA damage-inducible SUMOylation of HERC2 promotes RNF8 binding via a novel SUMO-binding Zinc finger. J Cell Biol 197: 179-187
133. Robu M, Shah RG, Petitclerc N, Brind'Amour J, Kandan-Kulangara F, Shah GM, (2013) Role of poly(ADP-ribose) polymerase-1 in the removal of UV-induced DNA lesions by nucleotide excision repair. Proc Natl Acad Sci USA 110: 1658-1663.
134. Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM, (2001) Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc Natl Acad Sci USA 98: 5134-5139
135. Sarangi P, Zhao X, (2015) SUMO-mediated regulation of DNA damage repair and responses. Trends Biochem Sci 40: 233-242
136. 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: 2461-2468
137. Scrima A, Konickova R, Czyzewski BK, Kawasaki Y, Jeffrey PD, Groisman R, Nakatani Y, Iwai S, Pavletich NP, Thoma NH, (2008) Structural basis of UV DNA-damage recognition by the DDB1-DDB2 complex. Cell 135: 1213-1223
138. Scrima A, Fischer ES, Lingaraju GM, Bohm K, Cavadini S, Thoma NH, (2011) Detecting UV-lesions in the genome: the modular CRL4 ubiquitin ligase does it best!. FEBS Lett 585: 2818-2825
139. Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM, Greenberg RA, (2010) ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 141: 970-981
140. Shiloh Y, (2003) ATM and related protein kinases: safeguarding genome integrity. Nat Rev Cancer 3: 155-168
141. Sims JJ, Cohen RE, (2009) Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol Cell 33: 775-783
142. Smeenk G, Wiegant WW, Vrolijk H, Solari AP, Pastink A, van Attikum H, (2010) The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol 190: 741-749
143. Smeenk G, van Attikum H, (2013) The chromatin response to DNA breaks: leaving a mark on genome integrity. Annu Rev Biochem 82: 55-80
144. Smeenk G, Wiegant WW, Marteijn JA, Luijsterburg MS, Sroczynski N, Costelloe T, Romeijn RJ, Pastink A, Mailand N, Vermeulen W, van Attikum H, (2013) Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5/SNF2H to RNF168-dependent DNA damage signaling. J Cell Sci 126: 889-903
145. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, Livingston DM, Greenberg RA, (2007) RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 316: 1198-1202
146. Stelter P, Ulrich HD, (2003) Control of spontaneous and damage-induced mutagenesis by SUMO and ubiquitin conjugation. Nature 425: 188-191
147. Stewart GS, Wang B, Bignell CR, Taylor AM, Elledge SJ, (2003) MDC1 is a mediator of the mammalian DNA damage checkpoint. Nature 421: 961-966
148. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, Nakada S, Ylanko J, Olivarius S, Mendez M, Oldreive C, Wildenhain J, Tagliaferro A, Pelletier L, Taubenheim N, Durandy A, Byrd PJ, Stankovic T, Taylor AM, Durocher D, (2009) The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136: 420-434
149. Stracker TH, Theunissen JW, Morales M, Petrini JH, (2004) The Mre11 complex and the metabolism of chromosome breaks: the importance of communicating and holding things together. DNA Repair (Amst) 3: 845-854
150. Stucki M, Jackson SP, (2006) gammaH2AX and MDC1: anchoring the DNA-damage-response machinery to broken chromosomes. DNA Repair (Amst) 5: 534-543
151. 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: 387-400
152. Sun H, Leverson JD, Hunter T, (2007) Conserved function of RNF4 family proteins in eukaryotes: targeting a ubiquitin ligase to SUMOylated proteins. EMBO J 26: 4102-4112
153. Sun Y, Jiang X, Xu Y, Ayrapetov MK, Moreau LA, Whetstine JR, Price BD, (2009) Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol 11: 1376-1382
154. 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: 63-77
155. Tang J, Cho NW, Cui G, Manion EM, Shanbhag NM, Botuyan MV, Mer G, Greenberg RA, (2013) Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20: 317-325
156. Tatham MH, Geoffroy MC, Shen L, Plechanovova A, Hattersley N, Jaffray EG, Palvimo JJ, Hay RT, (2008) RNF4 is a poly-SUMO-specific E3 ubiquitin ligase required for arsenic-induced PML degradation. Nat Cell Biol 10: 538-546
157. Thorslund T, Ripplinger A, Hoffmann S, Wild T, Uckelmann M, Villumsen B, Narita T, Sixma TK, Choudhary C, Bekker-Jensen S, Mailand N, (2015) Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527: 389-393
158. Ui A, Nagaura Y, Yasui A, (2015) Transcriptional elongation factor ENL phosphorylated by ATM recruits polycomb and switches off transcription for DSB repair. Mol Cell 58: 468-482
159. Ulrich HD, Jentsch S, (2000) Two RING finger proteins mediate cooperation between ubiquitin-conjugating enzymes in DNA repair. EMBO J 19: 3388-3397
160. Wang H, Zhai L, Xu J, Joo HY, 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: 383-394
161. Wang Z, Michaud GA, Cheng Z, Zhang Y, Hinds TR, Fan E, Cong F, Xu W, (2012) Recognition of the iso-ADP-ribose moiety in poly(ADP-ribose) by WWE domains suggests a general mechanism for poly(ADP-ribosyl)ation-dependent ubiquitination. Genes Dev 26: 235-240
162. Weake VM, Workman JL, (2008) Histone ubiquitination: triggering gene activity. Mol Cell 29: 653-663
163. Windheim M, Peggie M, Cohen P, (2008) Two different classes of E2 ubiquitin-conjugating enzymes are required for the mono-ubiquitination of proteins and elongation by polyubiquitin chains with a specific topology. Biochem J 409: 723-729
164. Wu J, Chen Y, Lu LY, Wu Y, Paulsen MT, Ljungman M, Ferguson DO, Yu X, (2011) Chfr and RNF8 synergistically regulate ATM activation. Nat Struct Mol Biol 18: 761-768
165. Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W, (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2: 851-861
166. Yamamoto KN, Kobayashi S, Tsuda M, Kurumizaka H, Takata M, Kono K, Jiricny J, Takeda S, Hirota K, (2011) Involvement of SLX4 in interstrand cross-link repair is regulated by the Fanconi anemia pathway. Proc Natl Acad Sci USA 108: 6492-6496
167. Yin Y, Seifert A, Chua JS, Maure JF, Golebiowski F, Hay RT, (2012) SUMO-targeted ubiquitin E3 ligase RNF4 is required for the response of human cells to DNA damage. Genes Dev 26: 1196-1208
168. Zhao GY, Sonoda E, Barber LJ, Oka H, Murakawa Y, Yamada K, Ikura T, Wang X, Kobayashi M, Yamamoto K, Boulton SJ, Takeda S, (2007) A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol Cell 25: 663-675
169. Zhao S, Ulrich HD, (2010) Distinct consequences of posttranslational modification by linear versus K63-linked polyubiquitin chains. Proc Natl Acad Sci USA 107: 7704-7709