USP3 counteracts RNF168 via deubiquitinating H2A and γh2AX at lysine 13 and 15

Cell Cycle

Volumn 13, Issue 1, 2014, Pages 106-114

  Sharma, Nidhi ^a   Zhu, Qianzheng ^a   Wani, Gulzar ^a   He, Jingshan ^a   Wang, Qi En ^a   Wani, Altaf A ^a,b  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

H2AX; 53BP1; BRCA1; Deubiquitinating enzyme; DNA repair; Histone modification; RNF168; Ubiquitin ligase; USP3

Indexed keywords

BRCA1 PROTEIN; DUAL SPECIFICITY PHOSPHATASE 3; HISTONE H2A; HISTONE H2AX; LYSINE;

ARTICLE; DNA DAMAGE; FEMALE; GAMMA IRRADIATION; GENE OVEREXPRESSION; HISTONE UBIQUITINATION; HUMAN; HUMAN CELL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; ULTRAVIOLET RADIATION;

53BP1; BRCA1; DEUBIQUITINATING ENZYME; DNA REPAIR; HISTONE MODIFICATION; RNF168; UBIQUITIN LIGASE; USP3; ΓH2AX;

CELL LINE; DNA DAMAGE; DNA REPAIR; HISTONES; HUMANS; LYSINE; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; UBIQUITIN-PROTEIN LIGASES; UBIQUITIN-SPECIFIC PROTEASES; UBIQUITINATION;

EID: 84892562030     PISSN: 15384101     EISSN: 15514005     Source Type: Journal    
DOI: 10.4161/cc.26814     Document Type: Article

References (34)

1. Bekker-Jensen S, Lukas C, Kitagawa R, Melander F, Kastan MB, Bartek J, Lukas J. Spatial organization of the mammalian genome surveillance machinery in response to DNA strand breaks. J Cell Biol 2006; 173: 195-206; PMID:16618811; http://dx.doi.org/10.1083/jcb.200510130
2. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Löbrich M, Jeggo PA. ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 2004; 64: 2390-6; PMID:15059890; http://dx.doi.org/10. 1158/0008-5472.CAN-03-3207 (Pubitemid 38523891)
3. Burma S, Chen BP, Murphy M, Kurimasa A, Chen DJ. ATM phosphorylates histone H2AX in response to DNA double-strand breaks. J Biol Chem 2001; 276: 42462-7; PMID:11571274; http://dx.doi.org/10.1074/jbc.C100466200
4. Ward IM, Chen J. Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 2001; 276: 47759-62; PMID:11673449
5. Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature 2009; 461:1071-8; PMID:19847258; http://dx.doi.org/10.1038/ nature08467
6. Harper JW, Elledge SJ. The DNA damage response: ten years after. Mol Cell 2007; 28:739-45; PMID:18082599; http://dx.doi.org/10.1016/j.molcel.2007.11.015 (Pubitemid 350217064)
7. Celeste A, Fernandez-Capetillo O, Kruhlak MJ, Pilch DR, Staudt DW, Lee A, Bonner RF, Bonner WM, Nussenzweig A. Histone H2AX phosphorylation is dispensable for the initial recognition of DNA breaks. Nat Cell Biol 2003; 5: 675-9; PMID:12792649; http://dx.doi.org/10.1038/ncb1004 (Pubitemid 36818091)
8. Stucki M, Clapperton JA, Mohammad D, Yaffe MB, Smerdon SJ, Jackson SP. MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks. Cell 2005; 123: 1213-26; PMID:16377563; http://dx.doi.org/10.1016/j.cell.2005.09.038 (Pubitemid 41821780)
9. Lukas C, Falck J, Bartkova J, Bartek J, Lukas J. Distinct spatiotemporal dynamics of mammalian checkpoint regulators induced by DNA damage. Nat Cell Biol 2003; 5: 255-60; PMID:12598907; http://dx.doi.org/10.1038/ncb945 (Pubitemid 36322254)
10. Bergink S, Jentsch S. Principles of ubiquitin and SUMO modifications in DNA repair. Nature 2009; 458: 461-7; PMID:19325626; http://dx.doi.org/10.1038/ nature07963
11. Lukas J, Bartek J. DNA repair: New tales of an old tail. Nature 2009; 458: 581-3; PMID:19340068; http://dx.doi.org/10.1038/458581a
12. Messick TE, Greenberg RA. The ubiquitin landscape at DNA double-strand breaks. J Cell Biol 2009; 187: 319-26; PMID:19948475; http://dx.doi.org/10.1083/ jcb.200908074
13. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J, et al. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 2009; 136: 435-46; PMID:19203579; http://dx.doi.org/10.1016/j. cell.2008.12.041
14. Huen MS, Grant R, Manke I, Minn K, Yu X, Yaffe MB, Chen J. RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly. Cell 2007; 131: 901-14; PMID:18001825; http://dx.doi.org/10. 1016/j.cell.2007.09.041 (Pubitemid 350138083)
15. Mailand N, Bekker-Jensen S, Faustrup H, Melander F, Bartek J, Lukas C, Lukas J. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins. Cell 2007; 131:887-900; PMID:18001824; http://dx.doi.org/10.1016/j.cell.2007.09.040 (Pubitemid 350138084)
16. Mattiroli F, Vissers JH, van Dijk WJ, Ikpa P, Citterio E, Vermeulen W, Marteijn JA, Sixma TK. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell 2012; 150:1182-95; PMID:22980979; http://dx.doi.org/10. 1016/j.cell.2012.08.005
17. Bunting SF, Callén E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, et al. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 2010; 141:243-54; PMID:20362325; http://dx.doi.org/10.1016/j.cell.2010.03.012
18. Callen E, Di Virgilio M, Kruhlak MJ, Nieto-Soler M, Wong N, Chen HT, Faryabi RB, Polato F, Santos M, Starnes LM, et al. 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 2013; 153: 1266-80; PMID:23727112; http://dx.doi.org/10.1016/j.cell.2013.05.023
19. Cao L, Xu X, Bunting SF, Liu J, Wang RH, Cao LL, Wu JJ, Peng TN, Chen J, Nussenzweig A, et al. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol Cell 2009; 35: 534-41; PMID:19716796; http://dx.doi.org/10.1016/j.molcel.2009.06.037
20. Wang B, Elledge SJ. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci U S A 2007; 104:20759-63; PMID:18077395; http://dx.doi.org/10.1073/ pnas.0710061104
21. Sobhian B, Shao G, Lilli DR, Culhane AC, Moreau LA, Xia B, Livingston DM, Greenberg RA. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science 2007; 316:1198-202; PMID:17525341; http://dx.doi.org/10. 1126/science.1139516 (Pubitemid 46877483)
22. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, Nakada S, Ylanko J, Olivarius S, Mendez M, et al. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 2009; 136: 420-34; PMID:19203578; http://dx.doi.org/10.1016/j.cell.2008.12.042
23. Ginjala V, Nacerddine K, Kulkarni A, Oza J, Hill SJ, Yao M, Citterio E, van Lohuizen M, Ganesan S. BMI1 is recruited to DNA breaks and contributes to DNA damage-induced H2A ubiquitination and repair. Mol Cell Biol 2011; 31: 1972-82; PMID:21383063; http://dx.doi.org/10.1128/MCB.00981-10
24. Nacerddine K, Beaudry JB, Ginjala V, Westerman B, Mattiroli F, Song JY, van der Poel H, Ponz OB, Pritchard C, Cornelissen-Steijger P, et al. Aktmediated phosphorylation of Bmi1 modulates its oncogenic potential, E3 ligase activity, and DNA damage repair activity in mouse prostate cancer. J Clin Invest 2012; 122: 1920-32; PMID:22505453; http://dx.doi.org/10.1172/JCI57477
25. Wang H, Wang L, Erdjument-Bromage H, Vidal M, Tempst P, Jones RS, Zhang Y. Role of histone H2A ubiquitination in Polycomb silencing. Nature 2004; 431: 873-8; PMID:15386022; http://dx.doi.org/10.1038/nature02985 (Pubitemid 39434086)
26. Shanbhag NM, Rafalska-Metcalf IU, Balane-Bolivar C, Janicki SM, Greenberg RA. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell 2010; 141:970-81; PMID:20550933; http://dx.doi.org/ 10.1016/j.cell.2010.04.038
27. Nicassio F, Corrado N, Vissers JH, Areces LB, Bergink S, Marteijn JA, Geverts B, Houtsmuller AB, Vermeulen W, Di Fiore PP, et al. Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr Biol 2007; 17:1972-7; PMID:17980597; http://dx.doi.org/10.1016/j.cub.2007.10.034 (Pubitemid 350088491)
28. Mosbech A, Lukas C, Bekker-Jensen S, Mailand N. The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J Biol Chem 2013; 288: 16579-87; PMID:23615962; http://dx.doi.org/10.1074/jbc.M113.459917
29. Huyen Y, Zgheib O, Ditullio RA Jr., Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 2004; 432: 406-11; PMID:15525939; http://dx.doi.org/10.1038/nature03114 (Pubitemid 39551676)
30. Kim H, Chen J, Yu X. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 2007; 316: 1202-5; PMID:17525342; http://dx.doi.org/10.1126/science.1139621 (Pubitemid 46877484)
31. Pan MR, Peng G, Hung WC, Lin SY. Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 2011; 286: 28599-607; PMID:21676867; http://dx.doi.org/10.1074/jbc.M111.256297
32. Arab HH, Wani G, Ray A, Shah ZI, Zhu Q, Wani AA. Dissociation of CAK from core TFIIH reveals a functional link between XP-G/CS and the TFIIH disassembly state. PLoS One 2010; 5:e11007; PMID:20543986; http://dx.doi.org/10.1371/ journal.pone.0011007
33. Zhu Q, Wani G, Arab HH, El-Mahdy MA, Ray A, Wani AA. Chromatin restoration following nucleotide excision repair involves the incorporation of ubiquitinated H2A at damaged genomic sites. DNA Repair (Amst) 2009; 8: 262-73; PMID:19059499; http://dx.doi.org/10.1016/j.dnarep.2008.11.007
34. Zhu Q, Wani G, Sharma N, Wani A. Lack of CAK complex accumulation at DNA damage sites in XP-B and XP-B/CS fibroblasts reveals differential regulation of CAK anchoring to core TFIIH by XPB and XPD helicases during nucleotide excision repair. DNA Repair (Amst) 2012; 11: 942-50; PMID:23083890; http://dx.doi.org/10. 1016/j.dnarep.2012.09.003