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Roles of histone ubiquitylation in DNA damage signaling |
Sui-Sui DONG, Michael S. Y. HUEN() |
Genome Stability Research Laboratory, Department of Anatomy, Centre for Cancer Research, University of Hong Kong, Hong Kong, China |
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Abstract Histone ubiquitylation has emerged as an important chromatin modification associated with DNA damage signaling and repair pathways. These histone marks, laid down by E3 ubiquitin ligases that include RNF8 and RNF168, decorate chromatin domains surrounding DNA double-strand breaks (DSBs). Recent work implicated ubiquitylated histones in orchestrating cell cycle checkpoints, DNA repair and gene transcription. Here we summarize recent advances that contribute to our current knowledge of the highly dynamic nature of DSB-associated histone ubiquitylation, and discuss major challenges ahead in understanding the versatility of ubiquitin conjugation in maintaining genome stability.
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Keywords
DNA damage
histone ubiquitylation
ubiquitin ligase
RNF8
RNF168
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Corresponding Author(s):
HUEN Michael S. Y.,Email:huen.michael@hku.hk
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Issue Date: 01 October 2011
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1 |
Al-Hakim A, Escribano-Diaz C, Landry M C, O’Donnell L, Panier S, Szilard R K, Durocher D (2010). The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst) , 9(12): 1229–1240 doi: 10.1016/j.dnarep.2010.09.011 pmid:21056014
|
2 |
Bassing C H, Suh H, Ferguson D O, Chua K F, Manis J, Eckersdorff M, Gleason M, Bronson R, Lee C, Alt F W (2003). Histone H2AX: a dosage-dependent suppressor of oncogenic translocations and tumors. Cell , 114(3): 359–370 doi: 10.1016/S0092-8674(03)00566-X pmid:12914700
|
3 |
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(1): 80–86, 1-12 doi: 10.1038/ncb2008 pmid:20023648
|
4 |
Bennetzen M V, Larsen D H, Bunkenborg J, Bartek J, Lukas J, Andersen J S (2010). Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol Cell Proteomics , 9(6): 1314–1323 doi: 10.1074/mcp.M900616-MCP200 pmid:20164059
|
5 |
Bensimon A, Schmidt A, Ziv Y, Elkon R, Wang S Y, Chen D J, Aebersold R, Shiloh Y (2010). ATM-dependent and -independent dynamics of the nuclear phosphoproteome after DNA damage. Sci Signal , 3(151): rs3 doi: 10.1126/scisignal.2001034 pmid:21139141
|
6 |
Bhaskara V, Dupré A, Lengsfeld B, Hopkins B B, Chan A, Lee J H, Zhang X, Gautier J, Zakian V, Paull T T (2007). Rad50 adenylate kinase activity regulates DNA tethering by Mre11/Rad50 complexes. Mol Cell , 25(5): 647–661 doi: 10.1016/j.molcel.2007.01.028 pmid:17349953
|
7 |
Botuyan M V, Lee J, Ward I M, Kim J E, Thompson J R, 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(7): 1361–1373 doi: 10.1016/j.cell.2006.10.043 pmid:17190600
|
8 |
Burma S, Chen B P, Murphy M, Kurimasa A, Chen D J (2001). ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem , 276(45): 42462–42467 doi: 10.1074/jbc.C100466200 pmid:11571274
|
9 |
Celeste A, Difilippantonio S, Difilippantonio M J, Fernandez-Capetillo O, Pilch D R, Sedelnikova O A, Eckhaus M, Ried T, Bonner W M, Nussenzweig A (2003). H2AX haploinsufficiency modifies genomic stability and tumor susceptibility. Cell , 114(3): 371–383 doi: 10.1016/S0092-8674(03)00567-1 pmid:12914701
|
10 |
Chapman J R, Jackson S P (2008). Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage. EMBO Rep , 9(8): 795–801 doi: 10.1038/embor.2008.103 pmid:18583988
|
11 |
Chou D M, Adamson B, Dephoure N E, Tan X, Nottke A C, Hurov K E, Gygi S P, Colaiácovo M P, Elledge S J (2010a). 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(43): 18475–18480 doi: 10.1073/pnas.1012946107 pmid:20937877
|
12 |
Chou D M, Adamson B, Dephoure N E, Tan X, Nottke A C, Hurov K E, Gygi S P, Colaiácovo M P, Elledge S J (2010b). 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(43): 18475–18480 doi: 10.1073/pnas.1012946107 pmid:20937877
|
13 |
Ciccia A, Elledge S J (2010). The DNA damage response: making it safe to play with knives. Mol Cell , 40(2): 179–204 doi: 10.1016/j.molcel.2010.09.019 pmid:20965415
|
14 |
Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen D H, 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(3): 435–446 doi: 10.1016/j.cell.2008.12.041 pmid:19203579
|
15 |
Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller K M, Jackson S P (2009). Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature , 462(7275): 935–939 doi: 10.1038/nature08657 pmid:20016603
|
16 |
Gong Z, Cho Y W, Kim J E, Ge K, Chen J (2009). Accumulation of Pax2 transactivation domain interaction protein (PTIP) at sites of DNA breaks via RNF8-dependent pathway is required for cell survival after DNA damage. J Biol Chem , 284(11): 7284–7293 doi: 10.1074/jbc.M809158200 pmid:19124460
|
17 |
Hopfner K P, Karcher A, Craig L, Woo T T, Carney J P, Tainer J A (2001). Structural biochemistry and interaction architecture of the DNA double-strand break repair Mre11 nuclease and Rad50-ATPase. Cell , 105(4): 473–485 doi: 10.1016/S0092-8674(01)00335-X pmid:11371344
|
18 |
Huang J, Huen M S, Kim H, Leung C C, Glover J N, Yu X, Chen J (2009). RAD18 transmits DNA damage signalling to elicit homologous recombination repair. Nat Cell Biol , 11(5): 592–603 doi: 10.1038/ncb1865 pmid:19396164
|
19 |
Huen M S, Chen J (2010). Assembly of checkpoint and repair machineries at DNA damage sites. Trends Biochem Sci , 35(2): 101–108 doi: 10.1016/j.tibs.2009.09.001 pmid:19875294
|
20 |
Huen M S, Grant R, Manke I, Minn K, Yu X, Yaffe M B, Chen J (2007a). RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell , 131(5): 901–914 doi: 10.1016/j.cell.2007.09.041 pmid:18001825
|
21 |
Huen M S, Grant R, Manke I, Minn K, Yu X, Yaffe M B, Chen J (2007b). RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell , 131(5): 901–914 doi: 10.1016/j.cell.2007.09.041 pmid:18001825
|
22 |
Huen M S, Huang J, Yuan J, Yamamoto M, Akira S, Ashley C, Xiao W, Chen J (2008). Noncanonical E2 variant-independent function of UBC13 in promoting checkpoint protein assembly. Mol Cell Biol , 28(19): 6104–6112 doi: 10.1128/MCB.00987-08 pmid:18678647
|
23 |
Huyen Y, Zgheib O, Ditullio R A Jr, Gorgoulis V G, Zacharatos P, Petty T J, Sheston E A, Mellert H S, Stavridi E S, Halazonetis T D (2004). Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature , 432(7015): 406–411 doi: 10.1038/nature03114 pmid:15525939
|
24 |
Ikura T, Tashiro S, Kakino A, Shima H, Jacob N, Amunugama R, Yoder K, Izumi S, Kuraoka I, Tanaka K, Kimura H, Ikura M, Nishikubo S, Ito T, Muto A, Miyagawa K, Takeda S, Fishel R, Igarashi K, Kamiya K (2007). DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics. Mol Cell Biol , 27(20): 7028–7040 doi: 10.1128/MCB.00579-07 pmid:17709392
|
25 |
Ismail I H, Andrin C, McDonald D, Hendzel M J (2010). BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol , 191(1): 45–60 doi: 10.1083/jcb.201003034 pmid:20921134
|
26 |
Iwai K, Tokunaga F (2009). Linear polyubiquitination: a new regulator of NF-kappaB activation. EMBO Rep , 10(7): 706–713 doi: 10.1038/embor.2009.144 pmid:19543231
|
27 |
Jackson S P, Bartek J (2009). The DNA-damage response in human biology and disease. Nature , 461(7267): 1071–1078 doi: 10.1038/nature08467 pmid:19847258
|
28 |
Kim H, Chen J, Yu X (2007). Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science , 316(5828): 1202–1205 doi: 10.1126/science.1139621 pmid:17525342
|
29 |
Kolas N K, Chapman J R, Nakada S, Ylanko J, Chahwan R, Sweeney F D, Panier S, Mendez M, Wildenhain J, Thomson T M, Pelletier L, Jackson S P, Durocher D (2007). Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science , 318(5856): 1637–1640 doi: 10.1126/science.1150034 pmid:18006705
|
30 |
Komander D (2009). The emerging complexity of protein ubiquitination. Biochem Soc Trans , 37(Pt 5): 937–953 doi: 10.1042/BST0370937 pmid:19754430
|
31 |
Larsen D H, Poinsignon C, Gudjonsson T, Dinant C, Payne M R, Hari F J, Danielsen J M, Menard P, Sand J C, Stucki M, Lukas C, Bartek J, Andersen J S, Lukas J (2010). The chromatin-remodeling factor CHD4 coordinates signaling and repair after DNA damage. J Cell Biol , 190(5): 731–740 doi: 10.1083/jcb.200912135 pmid:20805324
|
32 |
Lilley C E, Chaurushiya M S, Boutell C, Landry S, Suh J, Panier S, Everett R D, Stewart G S, Durocher D, Weitzman M D (2010). A viral E3 ligase targets RNF8 and RNF168 to control histone ubiquitination and DNA damage responses. EMBO J , 29: 943–955
|
33 |
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(5): 887–900 doi: 10.1016/j.cell.2007.09.040 pmid:18001824
|
34 |
Manke I A, Lowery D M, Nguyen A, Yaffe M B (2003). BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science , 302(5645): 636–639 doi: 10.1126/science.1088877 pmid:14576432
|
35 |
Matsuoka S, Ballif B A, Smogorzewska A, McDonald E R 3rd, Hurov K E, Luo J, Bakalarski C E, Zhao Z, Solimini N, Lerenthal Y, Shiloh Y, Gygi S P, Elledge S J (2007). ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science , 316(5828): 1160–1166 doi: 10.1126/science.1140321 pmid:17525332
|
36 |
Melander F, Bekker-Jensen S, Falck J, Bartek J, Mailand N, Lukas J (2008). Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin. J Cell Biol , 181(2): 213–226 doi: 10.1083/jcb.200708210 pmid:18411307
|
37 |
Morris J R, Boutell C, Keppler M, Densham R, Weekes D, Alamshah A, Butler L, Galanty Y, Pangon L, Kiuchi T, Ng T, Solomon E (2009). The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature , 462(7275): 886–890 doi: 10.1038/nature08593 pmid:20016594
|
38 |
Morris J R, Solomon E (2004). BRCA1 : BARD1 induces the formation of conjugated ubiquitin structures, dependent on K6 of ubiquitin, in cells during DNA replication and repair. Hum Mol Genet , 13(8): 807–817 doi: 10.1093/hmg/ddh095 pmid:14976165
|
39 |
Mu J J, Wang Y, Luo H, Leng M, Zhang J, Yang T, Besusso D, Jung S Y, Qin J (2007). A proteomic analysis of ataxia telangiectasia-mutated (ATM)/ATM-Rad3-related (ATR) substrates identifies the ubiquitin-proteasome system as a regulator for DNA damage checkpoints. J Biol Chem , 282(24): 17330–17334 doi: 10.1074/jbc.C700079200 pmid:17478428
|
40 |
Munoz I M, Jowsey P A, Toth R, Rouse J (2007). Phospho-epitope binding by the BRCT domains of hPTIP controls multiple aspects of the cellular response to DNA damage. Nucleic Acids Res , 35(16): 5312–5322 doi: 10.1093/nar/gkm493 pmid:17690115
|
41 |
Murr R, Loizou J I, Yang Y G, Cuenin C, Li H, Wang Z Q, Herceg Z (2006). Histone acetylation by Trrap-Tip60 modulates loading of repair proteins and repair of DNA double-strand breaks. Nat Cell Biol , 8(1): 91–99 doi: 10.1038/ncb1343 pmid:16341205
|
42 |
Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang Y C, O’Donnell L, Kumakubo A, Munro M, Sicheri F, Gingras A C, Natsume T, Suda T, Durocher D (2010). Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature , 466(7309): 941–946 doi: 10.1038/nature09297 pmid:20725033
|
43 |
Panier S, Durocher D (2009). Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair (Amst) , 8(4): 436–443 doi: 10.1016/j.dnarep.2009.01.013 pmid:19230794
|
44 |
Paull T T, Rogakou E P, Yamazaki V, Kirchgessner C U, Gellert M, Bonner W M (2000). A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol , 10(15): 886–895 doi: 10.1016/S0960-9822(00)00610-2 pmid:10959836
|
45 |
Plans V, Scheper J, Soler M, Loukili N, Okano Y, Thomson T M (2006). The RING finger protein RNF8 recruits UBC13 for lysine 63-based self polyubiquitylation. J Cell Biochem , 97(3): 572–582 doi: 10.1002/jcb.20587 pmid:16215985
|
46 |
Polanowska J, Martin J S, Garcia-Muse T, Petalcorin M I, Boulton S J (2006). A conserved pathway to activate BRCA1-dependent ubiquitylation at DNA damage sites. EMBO J , 25(10): 2178–2188 doi: 10.1038/sj.emboj.7601102 pmid:16628214
|
47 |
Polo S E, Kaidi A, Baskcomb L, Galanty Y, Jackson S P (2010). Regulation of DNA-damage responses and cell-cycle progression by the chromatin remodelling factor CHD4. EMBO J , 29(18): 3130–3139 doi: 10.1038/emboj.2010.188 pmid:20693977
|
48 |
Rogakou E P, Pilch D R, Orr A H, Ivanova V S, Bonner W M (1998). DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem , 273(10): 5858–5868 doi: 10.1074/jbc.273.10.5858 pmid:9488723
|
49 |
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 doi: 10.1038/emboj.2009.160 pmid:19536136
|
50 |
Shanbhag N M, Rafalska-Metcalf I U, Balane-Bolivar C, Janicki S M, Greenberg R A (2010). ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell , 141(6): 970–981 doi: 10.1016/j.cell.2010.04.038 pmid:20550933
|
51 |
Shao G, Lilli D R, Patterson-Fortin J, Coleman K A, Morrissey D E, Greenberg R A (2009). The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci USA , 106(9): 3166–3171 doi: 10.1073/pnas.0807485106 pmid:19202061
|
52 |
Sims J J, Cohen R E (2009). Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80. Mol Cell , 33(6): 775–783 doi: 10.1016/j.molcel.2009.02.011 pmid:19328070
|
53 |
Smeenk G, Wiegant W W, Vrolijk H, Solari A P, Pastink A, van Attikum H (2010). The NuRD chromatin-remodeling complex regulates signaling and repair of DNA damage. J Cell Biol , 190(5): 741–749 doi: 10.1083/jcb.201001048 pmid:20805320
|
54 |
Smolka M B, Albuquerque C P, Chen S H, Zhou H (2007). Proteome-wide identification of in vivo targets of DNA damage checkpoint kinases. Proc Natl Acad Sci USA , 104(25): 10364–10369 doi: 10.1073/pnas.0701622104 pmid:17563356
|
55 |
Sobhian B, Shao G, Lilli D R, Culhane A C, Moreau L A, Xia B, Livingston D M, Greenberg R A (2007). RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science , 316(5828): 1198–1202 doi: 10.1126/science.1139516 pmid:17525341
|
56 |
Spycher C, Miller E S, Townsend K, Pavic L, Morrice N A, Janscak P, Stewart G S, Stucki M (2008). Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin. J Cell Biol , 181(2): 227–240 doi: 10.1083/jcb.200709008 pmid:18411308
|
57 |
Stewart G S, Panier S, Townsend K, Al-Hakim A K, Kolas N K, Miller E S, Nakada S, Ylanko J, Olivarius S, Mendez M, Oldreive C, Wildenhain J, Tagliaferro A, Pelletier L, Taubenheim N, Durandy A, Byrd P J, Stankovic T, Taylor A M, Durocher D (2009). The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell , 136(3): 420–434 doi: 10.1016/j.cell.2008.12.042 pmid:19203578
|
58 |
Stewart G S, Stankovic T, Byrd P J, Wechsler T, Miller E S, Huissoon A, Drayson M T, West S C, Elledge S J, Taylor A M (2007). RIDDLE immunodeficiency syndrome is linked to defects in 53BP1-mediated DNA damage signaling. Proc Natl Acad Sci USA , 104(43): 16910–16915 doi: 10.1073/pnas.0708408104 pmid:17940005
|
59 |
Stucki M, Clapperton J A, Mohammad D, Yaffe M B, Smerdon S J, Jackson S P (2005). MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell , 123(7): 1213–1226 doi: 10.1016/j.cell.2005.09.038 pmid:16377563
|
60 |
Ulrich H, Walden H (2010). Ubiquitin signalling in DNA replication and repair. Nat Rev Mol Cell Biol , 11: 479–489
|
61 |
Wang B, Elledge S J (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 doi: 10.1073/pnas.0710061104 pmid:18077395
|
62 |
Wang B, Matsuoka S, Ballif B A, Zhang D, Smogorzewska A, Gygi S P, Elledge S J (2007). Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science , 316(5828): 1194–1198 doi: 10.1126/science.1139476 pmid:17525340
|
63 |
Weake V M, Workman J L (2008). Histone ubiquitination: triggering gene activity. Mol Cell , 29(6): 653–663 doi: 10.1016/j.molcel.2008.02.014 pmid:18374642
|
64 |
Wu J, Prindle M J, Dressler G R, Yu X (2009). PTIP regulates 53BP1 and SMC1 at the DNA damage sites. J Biol Chem , 284(27): 18078–18084 doi: 10.1074/jbc.M109.002527 pmid:19414588
|
65 |
Wu L, Luo K, Lou Z, Chen J (2008). MDC1 regulates intra-S-phase checkpoint by targeting NBS1 to DNA double-strand breaks. Proc Natl Acad Sci USA , 105(32): 11200–11205 doi: 10.1073/pnas.0802885105 pmid:18678890
|
66 |
Xu Y, Sun Y, Jiang X, Ayrapetov M K, Moskwa P, Yang S, Weinstock D M, Price B D (2010). The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair. J Cell Biol , 191(1): 31–43 doi: 10.1083/jcb.201001160 pmid:20876283
|
67 |
Zhao G Y, Sonoda E, Barber L J, Oka H, Murakawa Y, Yamada K, Ikura T, Wang X, Kobayashi M, Yamamoto K, Boulton S J, Takeda S (2007). A critical role for the ubiquitin-conjugating enzyme Ubc13 in initiating homologous recombination. Mol Cell , 25(5): 663–675 doi: 10.1016/j.molcel.2007.01.029 pmid:17349954
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