USP51 deubiquitylates H2AK13,15ub and regulates DNA damage response

Genes and Development

Volumn 30, Issue 8, 2016, Pages 946-959

  Wang, Zhiquan ^a   Zhang, Honglian ^a   Liu, Ji ^a   Cheruiyot, Abigael ^b   Lee, Jeong Heon ^a,c   Ordog, Tamas ^c   Lou, Zhenkun ^c   You, Zhongsheng ^b   Zhang, Zhiguo ^a,c  

^a MAYO GRADUATE SCHOOL   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c Mayo Clinic College of Medicine   (United States)

Author keywords

Deubiqutylating enzyme; DNA damage response; H2AK15ub; USP51

Indexed keywords

53BP1 PROTEIN; BRCA1 PROTEIN; DEUBIQUITINASE; DOUBLE STRANDED DNA; H2AK13,15UB PROTEIN; HISTONE H2A; HISTONE H2B; UNCLASSIFIED DRUG; USP51 PROTEIN; DNA; HISTONE; MDC1 PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN BINDING; TRANSACTIVATOR PROTEIN; USP51 PROTEIN, HUMAN;

ARTICLE; CHROMATIN; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; GENOMIC INSTABILITY; HELA CELL LINE; IN VITRO STUDY; IONIZING RADIATION; MOLECULAR DYNAMICS; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; U2OS CELL LINE; CELL SURVIVAL; GENETICS; HUMAN; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; TUMOR CELL LINE; UBIQUITINATION;

CELL LINE, TUMOR; CELL SURVIVAL; DNA; DNA DAMAGE; DNA REPAIR; HISTONES; HUMANS; NUCLEAR PROTEINS; PROTEIN BINDING; RADIATION, IONIZING; TRANS-ACTIVATORS; UBIQUITIN-SPECIFIC PROTEASES; UBIQUITINATION;

EID: 84963837773     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.271841.115     Document Type: Article

References (45)

1. 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.
2. Branzei D, Foiani M. 2008. Regulation of DNA repair throughout the cell cycle. Nat Rev Mol Cell Biol 9: 297-308.
3. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, et al. 2010. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254.
4. Chan KM, Fang D, Gan H, Hashizume R, Yu C, Schroeder M, Gupta N, Mueller S, James CD, Jenkins R, et al. 2013. The histone H3.3K27M mutation in pediatric glioma reprograms H3K27 methylation and gene expression. Genes Dev 27: 985-990.
5. Chen CC, Carson JJ, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler JK. 2008. Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell 134: 231-243.
6. Chen X, Paudyal SC, Chin RI, You Z. 2013. PCNApromotes processive DNA end resection by Exo1. Nucleic Acids Res 41: 9325-9338.
7. Ciccia A, Elledge SJ. 2010. The DNA damage response: making it safe to play with knives. Mol Cell 40: 179-204.
8. Doil C, Mailand N, Bekker-Jensen S, Menard P, Larsen DH, Pepperkok R, Ellenberg J, Panier S, Durocher D, Bartek J, et al. 2009. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell 136: 435-446.
9. Fradet-Turcotte A, Canny MD, Escribano-Diaz C, Orthwein A, Leung CC, Huang H, Landry MC, Kitevski-LeBlanc J, Noordermeer SM, Sicheri F, et al. 2013. 53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark. Nature 499: 50-54.
10. 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.
11. Ghosal G, Chen J. 2013. DNA damage tolerance: a doubleedged sword guarding the genome. Transl Cancer Res 2: 107-129.
12. Gudjonsson T, Altmeyer M, Savic V, Toledo L, Dinant C, Grofte M,Bartkova J, Poulsen M, Oka Y, Bekker-Jensen S, et al. 2012. TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150: 697-709.
13. Huen MS, Chen J. 2010. Assembly of checkpoint and repair machineries at DNA damage sites. Trends Biochem Sci 35: 101-108.
14. 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.
15. Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461: 1071-1078.
16. Jackson SP, Durocher D. 2013. Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell 49: 795-807.
17. Joo HY, Zhai L, Yang C, Nie S, Erdjument-Bromage H, Tempst P, Chang C, Wang H. 2007. Regulation of cell cycle progression and gene expression by H2A deubiquitination. Nature 449: 1068-1072.
18. Kolas NK, Chapman JR, Nakada S, Ylanko J, Chahwan R, Sweeney FD, Panier S, Mendez M, Wildenhain J, Thomson TM, et al. 2007. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase. Science 318: 1637-1640.
19. Lancini C, van den Berk PC, Vissers JH, Gargiulo G, Song JY, Hulsman D, Serresi M, Tanger E, Blom M, Vens C, et al. 2014. Tight regulation of ubiquitin-mediatedDNAdamage response by USP3 preserves the functional integrity of hematopoietic stem cells. J Exp Med 211: 1759-1777.
20. Li Q, Zhou H, Wurtele H, Davies B, Horazdovsky B, Verreault A,Zhang Z. 2008. Acetylation of histone H3 lysine 56 regulates replication-coupled nucleosome assembly. Cell 134: 244-255.
21. Liu C, Wang D, Wu J, Keller J, Ma T, Yu X. 2013. RNF168 forms a functional complex with RAD6 during the DNA damage response. J Cell Sci 126: 2042-2051.
22. 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.
23. 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.
24. Mao Z, Seluanov A, Jiang Y, Gorbunova V. 2007. TRF2 is required for repair of nontelomeric DNA double-strand breaks by homologous recombination. Proc Natl Acad Sci 104: 13068-13073.
25. Marechal A, Zou L. 2013. DNA damage sensing by the ATM and ATR kinases. Cold Spring Harb Perspect Biol 5: a012716.
26. 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.
27. Mosbech A, Lukas C, Bekker-Jensen S, Mailand N. 2013. The deubiquitylating enzyme USP44 counteracts the DNA doublestrand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J Biol Chem 288: 16579-16587.
28. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang YC, O'Donnell L, Kumakubo A, Munro M, Sicheri F, et al. 2010. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466: 941-946.
29. Nicassio F, Corrado N, Vissers JH, Areces LB, Bergink S, Marteijn JA, Geverts B, Houtsmuller AB, Vermeulen W, Di Fiore PP, et al. 2007. Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr Biol 17: 1972-1977.
30. Panier S, Boulton SJ. 2014. Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15: 7-18.
31. 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.
32. Patel AG, Sarkaria JN, Kaufmann SH. 2011. Nonhomologous end joining drives poly(ADP-ribose) polymerase (PARP) inhibitor lethality in homologous recombination-deficient cells. Proc Natl Acad Sci 108: 3406-3411.
33. Pei H, Zhang L, Luo K, Qin Y, Chesi M, Fei F, Bergsagel PL, Wang L,You Z, Lou Z. 2011. MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470: 124-128.
34. 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.
35. Rappold I, Iwabuchi K, Date T, Chen J. 2001. Tumor suppressor p53 binding protein 1 (53BP1) is involved in DNA damage-signaling pathways. J Cell Biol 153: 613-620.
36. Schwartz AL, Ciechanover A. 1999. The ubiquitin-proteasome pathway and pathogenesis of human diseases. Annu Rev Med 50: 57-74.
37. Seluanov A, Mittelman D, Pereira-Smith OM,Wilson JH, Gorbunova V. 2004. DNA end joining becomes less efficient and more error-prone during cellular senescence. Proc Natl Acad Sci 101: 7624-7629.
38. 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.
39. Shao G, Lilli DR, Patterson-Fortin J, Coleman KA, Morrissey DE, Greenberg RA. 2009. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci 106: 3166-3171.
40. Sharma N, Zhu Q,Wani G, He J, Wang QE,Wani AA. 2014. USP3 counteracts RNF168 via deubiquitinating H2A and γH2AX at lysine 13 and 15. Cell Cycle 13: 106-114.
41. Stewart GS, Panier S, Townsend K, Al-Hakim AK, Kolas NK, Miller ES, Nakada S, Ylanko J, Olivarius S, Mendez M, et al. 2009. The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage. Cell 136: 420-434.
42. Thorslund T, Ripplinger A, Hoffmann S, Wild T, Uckelmann M, Villumsen B, Narita T, Sixma TK, Choudhary C, Bekker-Jensen S,et al. 2015. Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage. Nature 527: 389-393.
43. 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 104: 20759-20763.
44. You Z, Shi LZ, Zhu Q, Wu P, Zhang YW, Basilio A, Tonnu N, Verma IM, Berns MW, Hunter T. 2009. CtIP links DNA double-strand break sensing to resection. Mol Cell 36: 954-969.
45. Zhang Z, Yang H, Wang H. 2014. The histone H2A deubiquitinase USP16 interacts with HERC2 and fine-tunes cellular response to DNA damage. J Biol Chem 289: 32883-32894.