Role of deubiquitinating enzymes in DNA repair

Molecular and Cellular Biology

Volumn 36, Issue 4, 2016, Pages 524-544

  Kee, Younghoon ^a   Huang, Tony T ^b  

^a UNIVERSITY OF SOUTH FLORIDA   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 ASSOCIATED PROTEIN 1; DEUBIQUITINASE; DNA; DNA DIRECTED DNA POLYMERASE BETA; FANCI PROTEIN; FANCONI ANEMIA GROUP D2 PROTEIN; OTU FAMILY DEUBIQUITINATING ENZYME 1; PAD ONE HOMOLOG 1; UBIQUITIN SPECIFIC PROTEASE 34; UBIQUITIN SPECIFIC PROTEASE 4; UBIQUITIN SPECIFIC PROTEASE 47; UBIQUITIN SPECIFIC PROTEASE 7; UNCLASSIFIED DRUG; UBIQUITIN;

ARTICLE; DNA ADDUCT; DNA ALKYLATION; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; DNA REPLICATION; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVE SITE; EXCISION REPAIR; GENE OVEREXPRESSION; GENETIC SCREENING; GENOME; HUMAN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ANIMAL; METABOLISM; UBIQUITINATION;

ANIMALS; DNA DAMAGE; DNA REPAIR; DNA REPLICATION; HUMANS; SIGNAL TRANSDUCTION; UBIQUITIN; UBIQUITIN-SPECIFIC PROTEASES; UBIQUITINATION;

EID: 84957899372     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00847-15     Document Type: Article

References (243)

1. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK, Bernards R. 2005. A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773-786. http://dx.doi.org/10.1016/j.cell.2005.11.007.
2. Sowa ME, Bennett EJ, Gygi SP, Harper JW. 2009. Defining the human deubiquitinating enzyme interaction landscape. Cell 138:389-403. http://dx.doi.org/10.1016/j.cell.2009.04.042.
3. Ye Y, Blaser G, Horrocks MH, Ruedas-Rama MJ, Ibrahim S, Zhukov AA, Orte A, Klenerman D, Jackson SE, Komander D. 2012. Ubiquitin chain conformation regulates recognition and activity of interacting proteins. Nature 492:266-270. http://dx.doi.org/10.1038/nature11722.
4. Faesen AC, Luna-Vargas MP, Geurink PP, Clerici M, Merkx R, van Dijk WJ, Hameed DS, El Oualid F, Ovaa H, Sixma TK. 2011. The differential modulation of USP activity by internal regulatory domains, interactors and eight ubiquitin chain types. Chem Biol 18:1550-1561. http://dx.doi.org/10.1016/j.chembiol.2011.10.017.
5. Mevissen TE, Hospenthal MK, Geurink PP, Elliott PR, Akutsu M, Arnaudo N, Ekkebus R, Kulathu Y, Wauer T, El Oualid F, Freund SM, Ovaa H, Komander D. 2013. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell 154:169-184. http://dx.doi.org/10.1016/j.cell.2013.05.046.
6. Komander D, Rape M. 2012. The ubiquitin code. Annu Rev Biochem 81:203-229. http://dx.doi.org/10.1146/annurev-biochem-060310-170328.
7. Komander D. 2010. Mechanism, specificity and structure of the deubiquitinases. Subcell Biochem 54:69-87. http://dx.doi.org/10.1007/978-1-4419-6676-6_6.
8. Huang TT, D'Andrea AD. 2006. Regulation of DNA repair by ubiquitylation. Nat Rev Mol Cell Biol 7:323-334. http://dx.doi.org/10.1038/nrm1908.
9. Chapman JR, Taylor MR, Boulton SJ. 2012. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47:497-510. http://dx.doi.org/10.1016/j.molcel.2012.07.029.
10. Ciccia A, Elledge SJ. 2010. The DNA damage response: making it safe to play with knives. Mol Cell 40:179-204. http://dx.doi.org/10.1016/j.molcel.2010.09.019.
11. Paull TT, Rogakou EP, Yamazaki V, Kirchgessner CU, Gellert M, Bonner WM. 2000. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr Biol 10:886-895. http://dx.doi.org/10.1016/S0960-9822(00)00610-2.
12. 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. http://dx.doi.org/10.1038/nature01446.
13. 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 104:20759-20763. http://dx.doi.org/10.1073/pnas.0710061104.
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. http://dx.doi.org/10.1016/j.cell.2007.09.041.
15. 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. http://dx.doi.org/10.1016/j.cell.2007.09.040.
16. 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. http://dx.doi.org/10.1016/j.cell.2008.12.041.
17. 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. http://dx.doi.org/10.1016/j.cell.2008.12.042.
18. 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. http://dx.doi.org/10.1126/science.1150034.
19. 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. http://dx.doi.org/10.1038/nature15401.
20. Penengo L, Mapelli M, Murachelli AG, Confalonieri S, Magri L, Musacchio A, Di Fiore PP, Polo S, Schneider TR. 2006. Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin. Cell 124:1183-1195. http://dx.doi.org/10.1016/j.cell.2006.02.020.
21. Panier S, Durocher D. 2009. Regulatory ubiquitylation in response to DNA double-strand breaks. DNA Repair (Amst) 8:436-443. http://dx.doi.org/10.1016/j.dnarep.2009.01.013.
22. 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. http://dx.doi.org/10.1016/j.molcel.2012.05.045.
23. 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. http://dx.doi.org/10.1038/emboj.2012.47.
24. 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. http://dx.doi.org/10.1016/j.cell.2012.08.005.
25. 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. http://dx.doi.org/10.1371/journal.pgen.1004178.
26. Raschle M, Smeenk G, Hansen RK, Temu T, Oka Y, Hein MY, Nagaraj N, Long DT, Walter JC, Hofmann K, Storchova Z, Cox J, Bekker-Jensen S, Mailand N, Mann M. 2015. DNA repair. Proteomics reveals dynamic assembly of repair complexes during bypass of DNA crosslinks. Science 348:1253671. http://dx.doi.org/10.1126/science.1253671.
27. Hofmann RM, Pickart CM. 1999. Noncanonical MMS2-encoded ubiquitin-conjugating enzyme functions in assembly of novel polyubiquitin chains for DNA repair. Cell 96:645-653. http://dx.doi.org/10.1016/S0092-8674(00)80575-9.
28. 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. http://dx.doi.org/10.1016/j.molcel.2007.01.029.
29. 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. http://dx.doi.org/10.1016/j.celrep.2014.12.021.
30. 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. http://dx.doi.org/10.1126/science.1139516.
31. 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 316:1194-1198. http://dx.doi.org/10.1126/science.1139476.
32. Kim H, Chen J, Yu X. 2007. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science 316:1202-1205. http://dx.doi.org/10.1126/science.1139621.
33. Yan J, Kim YS, Yang XP, Li LP, Liao G, Xia F, Jetten AM. 2007. The ubiquitin-interacting motif containing protein RAP80 interacts with BRCA1 and functions in DNA damage repair response. Cancer Res 67:6647-6656. http://dx.doi.org/10.1158/0008-5472.CAN-07-0924.
34. 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 287:22919-22926. http://dx.doi.org/10.1074/jbc.M112.351007.
35. Sy SM, Huen MS, Chen J. 2009. PALB2 is an integral component of the BRCA complex required for homologous recombination repair. Proc Natl Acad Sci U S A 106:7155-7160. http://dx.doi.org/10.1073/pnas.0811159106.
36. Zhang F, Fan Q, Ren K, Andreassen PR. 2009. PALB2 functionally connects the breast cancer susceptibility proteins BRCA1 and BRCA2. Mol Cancer Res 7:1110-1118. http://dx.doi.org/10.1158/1541-7786.MCR-09-0123.
37. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, Xu X, Deng CX, Finkel T, Nussenzweig M, Stark JM, Nussenzweig A. 2010. 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141:243-254. http://dx.doi.org/10.1016/j.cell.2010.03.012.
38. 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. http://dx.doi.org/10.1101/gad.2011011.
39. Coleman KA, Greenberg RA. 2011. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J Biol Chem 286:13669-13680. http://dx.doi.org/10.1074/jbc.M110.213728.
40. Huyen Y, Zgheib O, Ditullio RA, Jr, Gorgoulis VG, Zacharatos P, Petty TJ, Sheston EA, Mellert HS, Stavridi ES, Halazonetis TD. 2004. Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks. Nature 432:406-411. http://dx.doi.org/10.1038/nature03114.
41. 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. http://dx.doi.org/10.1038/nature12318.
42. Cao L, Xu X, Bunting SF, Liu J, Wang RH, Cao LL, Wu JJ, Peng TN, Chen J, Nussenzweig A, Deng CX, Finkel T. 2009. A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol Cell 35:534-541. http://dx.doi.org/10.1016/j.molcel.2009.06.037.
43. Bothmer A, Robbiani DF, Di Virgilio M, Bunting SF, Klein IA, Feldhahn N, Barlow J, Chen HT, Bosque D, Callen E, Nussenzweig A, Nussenzweig MC. 2011. Regulation of DNA end joining, resection, and immunoglobulin class switch recombination by 53BP1. Mol Cell 42:319-329. http://dx.doi.org/10.1016/j.molcel.2011.03.019.
44. Zimmermann M, de Lange T. 2014. 53BP1: pro choice in DNA repair. Trends Cell Biol 24:108-117. http://dx.doi.org/10.1016/j.tcb.2013.09.003.
45. Zimmermann M, Lottersberger F, Buonomo SB, Sfeir A, de Lange T. 2013. 53BP1 regulates DSB repair using Rif1 to control 5' end resection. Science 339:700-704. http://dx.doi.org/10.1126/science.1231573.
46. Di Virgilio M, Callen E, Yamane A, Zhang W, Jankovic M, Gitlin AD, Feldhahn N, Resch W, Oliveira TY, Chait BT, Nussenzweig A, Casellas R, Robbiani DF, Nussenzweig MC. 2013. Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 339:711-715. http://dx.doi.org/10.1126/science.1230624.
47. Chapman JR, Barral P, Vannier JB, Borel V, Steger M, Tomas-Loba A, Sartori AA, Adams IR, Batista FD, Boulton SJ. 2013. RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell 49:858-871. http://dx.doi.org/10.1016/j.molcel.2013.01.002.
48. Escribano-Diaz C, Orthwein A, Fradet-Turcotte A, Xing M, Young JT, Tkac J, Cook MA, Rosebrock AP, Munro M, Canny MD, Xu D, Durocher D. 2013. A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell 49:872-883. http://dx.doi.org/10.1016/j.molcel.2013.01.001.
49. Feng L, Fong KW, Wang J, Wang W, Chen J. 2013. RIF1 counteracts BRCA1-mediated end resection during DNA repair. J Biol Chem 288:11135-11143. http://dx.doi.org/10.1074/jbc.M113.457440.
50. Xu G, Chapman JR, Brandsma I, Yuan J, Mistrik M, Bouwman P, Bartkova J, Gogola E, Warmerdam D, Barazas M, Jaspers JE, Watanabe K, Pieterse M, Kersbergen A, Sol W, Celie PH, Schouten PC, van den Broek B, Salman A, Nieuwland M, de Rink I, de Ronde J, Jalink K, Boulton SJ, Chen J, van Gent DC, Bartek J, Jonkers J, Borst P, Rottenberg S. 2015. REV7 counteracts DNA double-strand break resection and affects PARP inhibition. Nature 521:541-544. http://dx.doi.org/10.1038/nature14328.
51. Boersma V, Moatti N, Segura-Bayona S, Peuscher MH, van der Torre J, Wevers BA, Orthwein A, Durocher D, Jacobs JJ. 2015. MAD2L2 controls DNA repair at telomeres and DNA breaks by inhibiting 5' end resection. Nature 521:537-540. http://dx.doi.org/10.1038/nature14216.
52. Wang J, Aroumougame A, Lobrich M, Li Y, Chen D, Chen J, Gong Z. 2014. PTIP associates with Artemis to dictate DNA repair pathway choice. Genes Dev 28:2693-2698. http://dx.doi.org/10.1101/gad.252478.114.
53. Zong D, Callen E, Pegoraro G, Lukas C, Lukas J, Nussenzweig A. 2015. Ectopic expression of RNF168 and 53BP1 increases mutagenic but not physiological non-homologous end joining. Nucleic Acids Res 43:4950-4961. http://dx.doi.org/10.1093/nar/gkv336.
54. 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 28:621-631. http://dx.doi.org/10.1038/emboj.2009.27.
55. Liu Z, Wu J, Yu X. 2007. CCDC98 targets BRCA1 to DNA damage sites. Nat Struct Mol Biol 14:716-720. http://dx.doi.org/10.1038/nsmb1279.
56. Kim H, Huang J, Chen J. 2007. CCDC98 is a BRCA1-BRCT domainbinding protein involved in the DNA damage response. Nat Struct Mol Biol 14:710-715. http://dx.doi.org/10.1038/nsmb1277.
57. Wang B, Hurov K, Hofmann K, Elledge SJ. 2009. NBA1, a new player in the Brca1 A complex, is required for DNA damage resistance and checkpoint control. Genes Dev 23:729-739. http://dx.doi.org/10.1101/gad.1770309.
58. 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 285:30982-30988. http://dx.doi.org/10.1074/jbc.M110.135392.
59. Hu X, Kim JA, Castillo A, Huang M, Liu J, Wang B. 2011. NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J Biol Chem 286:11734-11745. http://dx.doi.org/10.1074/jbc.M110.200857.
60. Dong Y, Hakimi MA, Chen X, Kumaraswamy E, Cooch NS, Godwin AK, Shiekhattar R. 2003. Regulation of BRCC, a holoenzyme complex containing BRCA1 and BRCA2, by a signalosome-like subunit and its role in DNA repair. Mol Cell 12:1087-1099. http://dx.doi.org/10.1016/S1097-2765(03)00424-6.
61. 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 5:180-193. http://dx.doi.org/10.1016/j.celrep.2013.08.025.
62. 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 U S A 106:3166-3171. http://dx.doi.org/10.1073/pnas.0807485106.
63. Okamoto K, Bartocci C, Ouzounov I, Diedrich JK, Yates JR, III, Denchi EL. 2013. A two-step mechanism for TRF2-mediated chromosome-end protection. Nature 494:502-505. http://dx.doi.org/10.1038/nature11873.
64. Verma R, Aravind L, Oania R, McDonald WH, Yates JR, III, Koonin EV, Deshaies RJ. 2002. Role of Rpn11 metalloprotease in deubiquitination and degradation by the 26S proteasome. Science 298:611-615. http://dx.doi.org/10.1126/science.1075898.
65. Yao T, Cohen RE. 2002. A cryptic protease couples deubiquitination and degradation by the proteasome. Nature 419:403-407. http://dx.doi.org/10.1038/nature01071.
66. Butler LR, Densham RM, Jia J, Garvin AJ, Stone HR, Shah V, Weekes D, Festy F, Beesley J, Morris JR. 2012. The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J 31:3918-3934. http://dx.doi.org/10.1038/emboj.2012.232.
67. Kakarougkas A, Ismail A, Katsuki Y, Freire R, Shibata A, Jeggo PA. 2013. Co-operation of BRCA1 and POH1 relieves the barriers posed by 53BP1 and RAP80 to resection. Nucleic Acids Res 41:10298-10311. http://dx.doi.org/10.1093/nar/gkt802.
68. 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 21:220-227. http://dx.doi.org/10.1038/nsmb.2771.
69. Krogan NJ, Lam MH, Fillingham J, Keogh MC, Gebbia M, Li J, Datta N, Cagney G, Buratowski S, Emili A, Greenblatt JF. 2004. Proteasome involvement in the repair of DNA double-strand breaks. Mol Cell 16:1027-1034. http://dx.doi.org/10.1016/j.molcel.2004.11.033.
70. Schwarz T, Sohn C, Kaiser B, Jensen ED, Mansky KC. 2010. The 19S proteasomal lid subunit POH1 enhances the transcriptional activation by Mitf in osteoclasts. J Cell Biochem 109:967-974. http://dx.doi.org/10.1002/jcb.22475.
71. Wauer T, Komander D. 2014. The JAMM in the proteasome. Nat Struct Mol Biol 21:346-348. http://dx.doi.org/10.1038/nsmb.2800.
72. Amerik AY, Swaminathan S, Krantz BA, Wilkinson KD, Hochstrasser M. 1997. In vivo disassembly of free polyubiquitin chains by yeast Ubp14 modulates rates of protein degradation by the proteasome. EMBO J 16:4826-4838. http://dx.doi.org/10.1093/emboj/16.16.4826.
73. Nakajima S, Lan L, Wei L, Hsieh CL, Rapic-Otrin V, Yasui A, Levine AS. 2014. Ubiquitin-specific protease 5 is required for the efficient repair of DNA double-strand breaks. PLoS One 9:e84899. http://dx.doi.org/10.1371/journal.pone.0084899.
74. Reyes-Turcu FE, Horton JR, Mullally JE, Heroux A, Cheng X, Wilkinson KD. 2006. The ubiquitin binding domain ZnF UBP recognizes the C-terminal diglycine motif of unanchored ubiquitin. Cell 124:1197-1208. http://dx.doi.org/10.1016/j.cell.2006.02.038.
75. Nishi R, Wijnhoven P, le Sage C, Tjeertes J, Galanty Y, Forment JV, Clague MJ, Urbe S, Jackson SP. 2014. Systematic characterization of deubiquitylating enzymes for roles in maintaining genome integrity. Nat Cell Biol 16:1016-1026. http://dx.doi.org/10.1038/ncb3028.
76. Kato K, Nakajima K, Ui A, Muto-Terao Y, Ogiwara H, Nakada S. 2014. Fine-tuning of DNA damage-dependent ubiquitination by OTUB2 supports the DNA repair pathway choice. Mol Cell 53:617-630. http://dx.doi.org/10.1016/j.molcel.2014.01.030.
77. Altun M, Walter TS, Kramer HB, Herr P, Iphofer A, Bostrom J, David Y, Komsany A, Ternette N, Navon A, Stuart DI, Ren J, Kessler BM. 2015. The human otubain2-ubiquitin structure provides insights into the cleavage specificity of poly-ubiquitin-linkages. PLoS One 10: e0115344. http://dx.doi.org/10.1371/journal.pone.0115344.
78. Henry KW, Wyce A, Lo WS, Duggan LJ, Emre NC, Kao CF, Pillus L, Shilatifard A, Osley MA, Berger SL. 2003. Transcriptional activation via sequential histone H2B ubiquitylation and deubiquitylation, mediated by SAGA-associated Ubp8. Genes Dev 17:2648-2663. http://dx.doi.org/10.1101/gad.1144003.
79. Sloper-Mould KE, Eyre HJ, Wang XW, Sutherland GR, Baker RT. 1999. Characterization and chromosomal localization of USP3, a novel human ubiquitin-specific protease. J Biol Chem 274:26878-26884. http://dx.doi.org/10.1074/jbc.274.38.26878.
80. Nicassio F, Corrado N, Vissers JH, Areces LB, Bergink S, Marteijn JA, Geverts B, Houtsmuller AB, Vermeulen W, Di Fiore PP, Citterio E. 2007. Human USP3 is a chromatin modifier required for S phase progression and genome stability. Curr Biol 17:1972-1977. http://dx.doi.org/10.1016/j.cub.2007.10.034.
81. Sharma N, Zhu Q, Wani G, He J, Wang QE, Wani AA. 2014. USP3 counteracts RNF168 via deubiquitinating H2A and gamma H2AX at lysine 13 and 15. Cell Cycle 13:106-114. http://dx.doi.org/10.4161/cc.26814.
82. Mosbech A, Lukas C, Bekker-Jensen S, Mailand N. 2013. The deubiquitylating enzyme USP44 counteracts the DNA double-strand break response mediated by the RNF8 and RNF168 ubiquitin ligases. J Biol Chem 288:16579-16587. http://dx.doi.org/10.1074/jbc.M113.459917.
83. Lancini C, van den Berk PC, Vissers JH, Gargiulo G, Song JY, Hulsman D, Serresi M, Tanger E, Blom M, Vens C, van Lohuizen M, Jacobs H, Citterio E. 2014. Tight regulation of ubiquitin-mediated DNA damage response by USP3 preserves the functional integrity of hematopoietic stem cells. J Exp Med 211:1759-1777. http://dx.doi.org/10.1084/jem.20131436.
84. Delgado-Diaz MR, Martin Y, Berg A, Freire R, Smits VA. 2014. Dub3 controls DNA damage signalling by direct deubiquitination of H2AX. Mol Oncol 8:884-893. http://dx.doi.org/10.1016/j.molonc.2014.03.003.
85. Fuchs G, Shema E, Vesterman R, Kotler E, Wolchinsky Z, Wilder S, Golomb L, Pribluda A, Zhang F, Haj-Yahya M, Feldmesser E, Brik A, Yu X, Hanna J, Aberdam D, Domany E, Oren M. 2012. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation. Mol Cell 46:662-673. http://dx.doi.org/10.1016/j.molcel.2012.05.023.
86. Stegmeier F, Rape M, Draviam VM, Nalepa G, Sowa ME, Ang XL, McDonald ER, III, Li MZ, Hannon GJ, Sorger PK, Kirschner MW, Harper JW, Elledge SJ. 2007. Anaphase initiation is regulated by antagonistic ubiquitination and deubiquitination activities. Nature 446:876-881. http://dx.doi.org/10.1038/nature05694.
87. Zhang Y, Foreman O, Wigle DA, Kosari F, Vasmatzis G, Salisbury JL, van Deursen J, Galardy PJ. 2012. USP44 regulates centrosome positioning to prevent aneuploidy and suppress tumorigenesis. J Clin Invest 122:4362-4374. http://dx.doi.org/10.1172/JCI63084.
88. Zhang Y, van Deursen J, Galardy PJ. 2011. Overexpression of ubiquitin specific protease 44 (USP44) induces chromosomal instability and is frequently observed in human T-cell leukemia. PLoS One 6:e23389. http://dx.doi.org/10.1371/journal.pone.0023389.
89. Holland AJ, Cleveland DW. 2012. The deubiquitinase USP44 is a tumor suppressor that protects against chromosome missegregation. J Clin Invest 122:4325-4328. http://dx.doi.org/10.1172/JCI66420.
90. Typas D, Luijsterburg MS, Wiegant WW, Diakatou M, Helfricht A, Thijssen PE, van de Broek B, Mullenders LH, van Attikum H. 2015. The de-ubiquitylating enzymes USP26 and USP37 regulate homologous recombination by counteracting RAP80. Nucleic Acids Res 43:6919-6933. http://dx.doi.org/10.1093/nar/gkv613.
91. Yu M, Liu K, Mao Z, Luo J, Gu W, Zhao W. 27 October 2015. USP11 is a negative regulator to gamman H2AX ubiquitylation by RNF8/RNF168. J Biol Chem http://dx.doi.org/10.1074/jbc.M114.624478.
92. Schoenfeld AR, Apgar S, Dolios G, Wang R, Aaronson SA. 2004. BRCA2 is ubiquitinated in vivo and interacts with USP11, a deubiquitinating enzyme that exhibits prosurvival function in the cellular response to DNA damage. Mol Cell Biol 24:7444-7455. http://dx.doi.org/10.1128/MCB.24.17.7444-7455.2004.
93. Wiltshire TD, Lovejoy CA, Wang T, Xia F, O'Connor MJ, Cortez D. 2010. Sensitivity to poly(ADP-ribose) polymerase (PARP) inhibition identifies ubiquitin-specific peptidase 11 (USP11) as a regulator of DNA double-strand break repair. J Biol Chem 285:14565-14571. http://dx.doi.org/10.1074/jbc.M110.104745.
94. Hendriks IA, Schimmel J, Eifler K, Olsen JV, Vertegaal AC. 2015. Ubiquitin-specific protease 11 (USP11) deubiquitinates hybrid small ubiquitin-like modifier (SUMO)-ubiquitin chains to counteract RING finger protein 4 (RNF4). J Biol Chem 290:15526-15537. http://dx.doi.org/10.1074/jbc.M114.618132.
95. Vyas R, Kumar R, Clermont F, Helfricht A, Kalev P, Sotiropoulou P, Hendriks IA, Radaelli E, Hochepied T, Blanpain C, Sablina A, van Attikum H, Olsen JV, Jochemsen AG, Vertegaal AC, Marine JC. 2013. RNF4 is required for DNA double-strand break repair in vivo. Cell Death Differ 20:490-502. http://dx.doi.org/10.1038/cdd.2012.145.
96. 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. http://dx.doi.org/10.1126/scisignal.2003485.
97. 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. http://dx.doi.org/10.1038/emboj.2012.158.
98. 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. http://dx.doi.org/10.1101/gad.188284.112.
99. 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. http://dx.doi.org/10.1101/gad.189274.112.
100. Nakada S, Tai I, Panier S, Al-Hakim A, Iemura S, Juang YC, O'Donnell L, Kumakubo A, Munro M, Sicheri F, Gingras AC, Natsume T, Suda T, Durocher D. 2010. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature 466:941-946. http://dx.doi.org/10.1038/nature09297.
101. Juang YC, Landry MC, Sanches M, Vittal V, Leung CC, Ceccarelli DF, Mateo AR, Pruneda JN, Mao DY, Szilard RK, Orlicky S, Munro M, Brzovic PS, Klevit RE, Sicheri F, Durocher D. 2012. OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol Cell 45:384-397. http://dx.doi.org/10.1016/j.molcel.2012.01.011.
102. Wiener R, DiBello AT, Lombardi PM, Guzzo CM, Zhang X, Matunis MJ, Wolberger C. 2013. E2 ubiquitin-conjugating enzymes regulate the deubiquitinating activity of OTUB1. Nat Struct Mol Biol 20:1033-1039. http://dx.doi.org/10.1038/nsmb.2655.
103. Zhu Q, Sharma N, He J, Wani G, Wani AA. 2015. USP7 deubiquitinase promotes ubiquitin-dependent DNA damage signaling by stabilizing RNF168. Cell Cycle 14:1413-1425. http://dx.doi.org/10.1080/15384101.2015.1007785.
104. Sy SM, Jiang J, O WS, Deng Y, Huen MS. 2013. The ubiquitin specific protease USP34 promotes ubiquitin signaling at DNA double-strand breaks. Nucleic Acids Res 41:8572-8580. http://dx.doi.org/10.1093/nar/gkt622.
105. 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. http://dx.doi.org/10.1016/j.cell.2012.06.039.
106. Kee Y, Lyon N, Huibregtse JM. 2005. The Rsp5 ubiquitin ligase is coupled to and antagonized by the Ubp2 deubiquitinating enzyme. EMBO J 24:2414-2424. http://dx.doi.org/10.1038/sj.emboj.7600710.
107. Kee Y, Munoz W, Lyon N, Huibregtse JM. 2006. The deubiquitinating enzyme Ubp2 modulates Rsp5-dependent Lys63-linked polyubiquitin conjugates in Saccharomyces cerevisiae. J Biol Chem 281:36724-36731. http://dx.doi.org/10.1074/jbc.M608756200.
108. Lam MH, Emili A. 2013. Ubp2 regulates Rsp5 ubiquitination activity in vivo and in vitro. PLoS One 8:e75372. http://dx.doi.org/10.1371/journal.pone.0075372.
109. Dar A, Shibata E, Dutta A. 2013. Deubiquitination of Tip60 by USP7 determines the activity of the p53-dependent apoptotic pathway. Mol Cell Biol 33:3309-3320. http://dx.doi.org/10.1128/MCB.00358-13.
110. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. 2005. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci U S A 102:13182-13187. http://dx.doi.org/10.1073/pnas.0504211102.
111. Di Croce L, Helin K. 2013. Transcriptional regulation by Polycomb group proteins. Nat Struct Mol Biol 20:1147-1155. http://dx.doi.org/10.1038/nsmb.2669.
112. 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. http://dx.doi.org/10.1128/MCB.00981-10.
113. Ismail IH, Andrin C, McDonald D, Hendzel MJ. 2010. BMI1-mediated histone ubiquitylation promotes DNA double-strand break repair. J Cell Biol 191:45-60. http://dx.doi.org/10.1083/jcb.201003034.
114. Pan MR, Peng G, Hung WC, Lin SY. 2011. Monoubiquitination of H2AX protein regulates DNA damage response signaling. J Biol Chem 286:28599-28607. http://dx.doi.org/10.1074/jbc.M111.256297.
115. Jensen DE, Proctor M, Marquis ST, Gardner HP, Ha SI, Chodosh LA, Ishov AM, Tommerup N, Vissing H, Sekido Y, Minna J, Borodovsky A, Schultz DC, Wilkinson KD, Maul GG, Barlev N, Berger SL, Prendergast GC, Rauscher FJ, III. 1998. BAP1: a novel ubiquitin hydrolase which binds to the BRCA1 RING finger and enhances BRCA1-mediated cell growth suppression. Oncogene 16:1097-1112. http://dx.doi.org/10.1038/sj.onc.1201861.
116. Ventii KH, Devi NS, Friedrich KL, Chernova TA, Tighiouart M, Van Meir EG, Wilkinson KD. 2008. BRCA1-associated protein-1 is a tumor suppressor that requires deubiquitinating activity and nuclear localization. Cancer Res 68:6953-6962. http://dx.doi.org/10.1158/0008-5472.CAN-08-0365.
117. Ismail IH, Davidson R, Gagne JP, Xu ZZ, Poirier GG, Hendzel MJ. 2014. Germline mutations in BAP1 impair its function in DNA double-strand break repair. Cancer Res 74:4282-4294. http://dx.doi.org/10.1158/0008-5472.CAN-13-3109.
118. Yu H, Pak H, Hammond-Martel I, Ghram M, Rodrigue A, Daou S, Barbour H, Corbeil L, Hebert J, Drobetsky E, Masson JY, Di Noia JM, Affar EB. 2014. Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair. Proc Natl Acad Sci U S A 111:285-290. http://dx.doi.org/10.1073/pnas.1309085110.
119. Scheuermann JC, de Ayala Alonso AG, Oktaba K, Ly-Hartig N, McGinty RK, Fraterman S, Wilm M, Muir TW, Muller J. 2010. Histone H2A deubiquitinase activity of the Polycomb repressive complex PR-DUB. Nature 465:243-247. http://dx.doi.org/10.1038/nature08966.
120. 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. http://dx.doi.org/10.1038/nature06256.
121. Deng SK, Gibb B, de Almeida MJ, Greene EC, Symington LS. 2014. RPA antagonizes microhomology-mediated repair of DNA double-strand breaks. Nat Struct Mol Biol 21:405-412. http://dx.doi.org/10.1038/nsmb.2786.
122. Deng SK, Yin Y, Petes TD, Symington LS. 2015. Mre11-Sae2 and RPA collaborate to prevent palindromic gene amplification. Mol Cell 60:500-508. http://dx.doi.org/10.1016/j.molcel.2015.09.027.
123. Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542-1548. http://dx.doi.org/10.1126/science.1083430.
124. Longhese MP, Neecke H, Paciotti V, Lucchini G, Plevani P. 1996. The 70 kDa subunit of replication protein A is required for the G1/S and intra-S DNA damage checkpoints in budding yeast. Nucleic Acids Res 24:3533-3537. http://dx.doi.org/10.1093/nar/24.18.3533.
125. Lee SE, Moore JK, Holmes A, Umezu K, Kolodner RD, Haber JE. 1998. Saccharomyces Ku70, mre11/rad50 and RPA proteins regulate adaptation to G2/M arrest after DNA damage. Cell 94:399-409. http://dx.doi.org/10.1016/S0092-8674(00)81482-8.
126. Sugiyama T, Zaitseva EM, Kowalczykowski SC. 1997. A single-stranded DNA-binding protein is needed for efficient presynaptic complex formation by the Saccharomyces cerevisiae Rad51 protein. J Biol Chem 272:7940-7945. http://dx.doi.org/10.1074/jbc.272.12.7940.
127. Sung P. 1997. Yeast Rad55 and Rad57 proteins form a heterodimer that functions with replication protein A to promote DNA strand exchange by Rad51 recombinase. Genes Dev 11:1111-1121. http://dx.doi.org/10.1101/gad.11.9.1111.
128. Takeda S, Nakamura K, Taniguchi Y, Paull TT. 2007. Ctp1/CtIP and the MRN complex collaborate in the initial steps of homologous recombination. Mol Cell 28:351-352. http://dx.doi.org/10.1016/j.molcel.2007.10.016.
129. Lengsfeld BM, Rattray AJ, Bhaskara V, Ghirlando R, Paull TT. 2007. Sae2 is an endonuclease that processes hairpin DNA cooperatively with the Mre11/Rad50/Xrs2 complex. Mol Cell 28:638-651. http://dx.doi.org/10.1016/j.molcel.2007.11.001.
130. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP. 2007. Human CtIP promotes DNA end resection. Nature 450:509-514. http://dx.doi.org/10.1038/nature06337.
131. Mimitou EP, Symington LS. 2009. DNA end resection: many nucleases make light work. DNA Repair (Amst) 8:983-995. http://dx.doi.org/10.1016/j.dnarep.2009.04.017.
132. Lee KY, Im JS, Shibata E, Park J, Handa N, Kowalczykowski SC, Dutta A. 2015. MCM8-9 complex promotes resection of double-strand break ends by MRE11-RAD50-NBS1 complex. Nat Commun 6:7744. http://dx.doi.org/10.1038/ncomms8744.
133. Mimitou EP, Symington LS. 2008. Sae2, Exo1 and Sgs1 collaborate in DNA double-strand break processing. Nature 455:770-774. http://dx.doi.org/10.1038/nature07312.
134. Zhu Z, Chung WH, Shim EY, Lee SE, Ira G. 2008. Sgs1 helicase and two nucleases Dna2 and Exo1 resect DNA double-strand break ends. Cell 134:981-994. http://dx.doi.org/10.1016/j.cell.2008.08.037.
135. Nimonkar AV, Ozsoy AZ, Genschel J, Modrich P, Kowalczykowski SC. 2008. Human exonuclease 1 and BLM helicase interact to resect DNA and initiate DNA repair. Proc Natl Acad Sci U S A 105:16906-16911. http://dx.doi.org/10.1073/pnas.0809380105.
136. Chen PL, Liu F, Cai S, Lin X, Li A, Chen Y, Gu B, Lee EY, Lee WH. 2005. Inactivation of CtIP leads to early embryonic lethality mediated by G1 restraint and to tumorigenesis by haploid insufficiency. Mol Cell Biol 25:3535-3542. http://dx.doi.org/10.1128/MCB.25.9.3535-3542.2005.
137. Polato F, Callen E, Wong N, Faryabi R, Bunting S, Chen HT, Kozak M, Kruhlak MJ, Reczek CR, Lee WH, Ludwig T, Baer R, Feigenbaum L, Jackson S, Nussenzweig A. 2014. CtIP-mediated resection is essential for viability and can operate independently of BRCA1. J Exp Med 211:1027-1036. http://dx.doi.org/10.1084/jem.20131939.
138. Makharashvili N, Tubbs AT, Yang SH, Wang H, Barton O, Zhou Y, Deshpande RA, Lee JH, Lobrich M, Sleckman BP, Wu X, Paull TT. 2014. Catalytic and noncatalytic roles of the CtIP endonuclease in double-strand break end resection. Mol Cell 54:1022-1033. http://dx.doi.org/10.1016/j.molcel.2014.04.011.
139. Barton O, Naumann SC, Diemer-Biehs R, Kunzel J, Steinlage M, Conrad S, Makharashvili N, Wang J, Feng L, Lopez BS, Paull TT, Chen J, Jeggo PA, Lobrich M. 2014. Polo-like kinase 3 regulates CtIP during DNA double-strand break repair in G1. J Cell Biol 206:877-894. http://dx.doi.org/10.1083/jcb.201401146.
140. Peterson SE, Li Y, Wu-Baer F, Chait BT, Baer R, Yan H, Gottesman ME, Gautier J. 2013. Activation of DSB processing requires phosphorylation of CtIP by ATR. Mol Cell 49:657-667. http://dx.doi.org/10.1016/j.molcel.2012.11.020.
141. Huertas P, Cortes-Ledesma F, Sartori AA, Aguilera A, Jackson SP. 2008. CDK targets Sae2 to control DNA-end resection and homologous recombination. Nature 455:689-692. http://dx.doi.org/10.1038/nature07215.
142. Kaidi A, Weinert BT, Choudhary C, Jackson SP. 2010. Human SIRT6 promotes DNA end resection through CtIP deacetylation. Science 329:1348-1353. http://dx.doi.org/10.1126/science.1192049.
143. Rajendran P, Kidane AI, Yu TW, Dashwood WM, Bisson WH, Lohr CV, Ho E, Williams DE, Dashwood RH. 2013. HDAC turnover, CtIP acetylation and dysregulated DNA damage signaling in colon cancer cells treated with sulforaphane and related dietary isothiocyanates. Epigenetics 8:612-623. http://dx.doi.org/10.4161/epi.24710.
144. Yu X, Fu S, Lai M, Baer R, Chen J. 2006. BRCA1 ubiquitinates its phosphorylation-dependent binding partner CtIP. Genes Dev 20:1721-1726. http://dx.doi.org/10.1101/gad.1431006.
145. Steger M, Murina O, Huhn D, Ferretti LP, Walser R, Hanggi K, Lafranchi L, Neugebauer C, Paliwal S, Janscak P, Gerrits B, Del Sal G, Zerbe O, Sartori AA. 2013. Prolyl isomerase PIN1 regulates DNA double-strand break repair by counteracting DNA end resection. Mol Cell 50:333-343. http://dx.doi.org/10.1016/j.molcel.2013.03.023.
146. Schmidt CK, Galanty Y, Sczaniecka-Clift M, Coates J, Jhujh S, Demir M, Cornwell M, Beli P, Jackson SP. 2015. Systematic E2 screening reveals a UBE2D-RNF138-CtIP axis promoting DNA repair. Nat Cell Biol 17:1458-1470. http://dx.doi.org/10.1038/ncb3260.
147. Lafranchi L, de Boer HR, de Vries EG, Ong SE, Sartori AA, van Vugt MA. 2014. APC/C(Cdh1) controls CtIP stability during the cell cycle and in response to DNA damage. EMBO J 33:2860-2879. http://dx.doi.org/10.15252/embj.201489017.
148. Liu H, Zhang H, Wang X, Tian Q, Hu Z, Peng C, Jiang P, Wang T, Guo W, Chen Y, Li X, Zhang P, Pei H. 2015. The deubiquitylating enzyme USP4 cooperates with CtIP in DNA double-strand break end resection. Cell Rep 13:93-107. http://dx.doi.org/10.1016/j.celrep.2015.08.056.
149. Wijnhoven P, Konietzny R, Blackford AN, Travers J, Kessler BM, Nishi R, Jackson SP. 2015. USP4 auto-deubiquitylation promotes homologous recombination. Mol Cell 60:362-373. http://dx.doi.org/10.1016/j.molcel.2015.09.019.
150. Vlasschaert C, Xia X, Coulombe J, Gray DA. 2015. Evolution of the highly networked deubiquitinating enzymes USP4, USP15, and USP11. BMC Evol Biol 15:230. http://dx.doi.org/10.1186/s12862-015-0511-1.
151. Song EJ, Werner SL, Neubauer J, Stegmeier F, Aspden J, Rio D, Harper JW, Elledge SJ, Kirschner MW, Rape M. 2010. The Prp19 complex and the Usp4Sart3 deubiquitinating enzyme control reversible ubiquitination at the spliceosome. Genes Dev 24:1434-1447. http://dx.doi.org/10.1101/gad.1925010.
152. Yao T, Song L, Jin J, Cai Y, Takahashi H, Swanson SK, Washburn MP, Florens L, Conaway RC, Cohen RE, Conaway JW. 2008. Distinct modes of regulation of the Uch37 deubiquitinating enzyme in the proteasome and in the Ino80 chromatin-remodeling complex. Mol Cell 31:909-917. http://dx.doi.org/10.1016/j.molcel.2008.08.027.
153. Gospodinov A, Vaissiere T, Krastev DB, Legube G, Anachkova B, Herceg Z. 2011. Mammalian Ino80 mediates double-strand break repair through its role in DNA end strand resection. Mol Cell Biol 31:4735-4745. http://dx.doi.org/10.1128/MCB.06182-11.
154. van Attikum H, Fritsch O, Gasser SM. 2007. Distinct roles for SWR1 and INO80 chromatin remodeling complexes at chromosomal double-strand breaks. EMBO J 26:4113-4125. http://dx.doi.org/10.1038/sj.emboj.7601835.
155. Kee Y, D'Andrea AD. 2010. Expanded roles of the Fanconi anemia pathway in preserving genomic stability. Genes Dev 24:1680-1694. http://dx.doi.org/10.1101/gad.1955310.
156. Garcia-Higuera I, Taniguchi T, Ganesan S, Meyn MS, Timmers C, Hejna J, Grompe M, D'Andrea AD. 2001. Interaction of the Fanconi anemia proteins and BRCA1 in a common pathway. Mol Cell 7:249-262. http://dx.doi.org/10.1016/S1097-2765(01)00173-3.
157. Smogorzewska A, Matsuoka S, Vinciguerra P, McDonald ER, III, Hurov KE, Luo J, Ballif BA, Gygi SP, Hofmann K, D'Andrea AD, Elledge SJ. 2007. Identification of the FANCI protein, a monoubiquitinated FANCD2 paralog required for DNA repair. Cell 129:289-301. http://dx.doi.org/10.1016/j.cell.2007.03.009.
158. Sims AE, Spiteri E, Sims RJ, III, Arita AG, Lach FP, Landers T, Wurm M, Freund M, Neveling K, Hanenberg H, Auerbach AD, Huang TT. 2007. FANCI is a second monoubiquitinated member of the Fanconi anemia pathway. Nat Struct Mol Biol 14:564-567. http://dx.doi.org/10.1038/nsmb1252.
159. 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 142:65-76. http://dx.doi.org/10.1016/j.cell.2010.06.021.
160. 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 142:77-88. http://dx.doi.org/10.1016/j.cell.2010.06.022.
161. Liu T, Ghosal G, Yuan J, Chen J, Huang J. 2010. FAN1 acts with FANCI-FANCD2 to promote DNA interstrand cross-link repair. Science 329:693-696. http://dx.doi.org/10.1126/science.1192656.
162. 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 39:36-47. http://dx.doi.org/10.1016/j.molcel.2010.06.023.
163. 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 54:460-471. http://dx.doi.org/10.1016/j.molcel.2014.03.015.
164. 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 54:472-484. http://dx.doi.org/10.1016/j.molcel.2014.03.014.
165. Fu D, Dudimah FD, Zhang J, Pickering A, Paneerselvam J, Palrasu M, Wang H, Fei P. 2013. Recruitment of DNA polymerase eta by FANCD2 in the early response to DNA damage. Cell Cycle 12:803-809. http://dx.doi.org/10.4161/cc.23755.
166. Murina O, von Aesch C, Karakus U, Ferretti LP, Bolck HA, Hanggi K, Sartori AA. 2014. FANCD2 and CtIP cooperate to repair DNA interstrand crosslinks. Cell Rep 7:1030-1038. http://dx.doi.org/10.1016/j.celrep.2014.03.069.
167. Unno J, Itaya A, Taoka M, Sato K, Tomida J, Sakai W, Sugasawa K, Ishiai M, Ikura T, Isobe T, Kurumizaka H, Takata M. 2014. FANCD2 binds CtIP and regulates DNA-end resection during DNA interstrand crosslink repair. Cell Rep 7:1039-1047. http://dx.doi.org/10.1016/j.celrep.2014.04.005.
168. Yeo JE, Lee EH, Hendrickson EA, Sobeck A. 2014. CtIP mediates replication fork recovery in a FANCD2-regulated manner. Hum Mol Genet 23:3695-3705. http://dx.doi.org/10.1093/hmg/ddu078.
169. Chen YH, Jones MJ, Yin Y, Crist SB, Colnaghi L, Sims RJ, III, Rothenberg E, Jallepalli PV, Huang TT. 2015. ATR-mediated phosphorylation of FANCI regulates dormant origin firing in response to replication stress. Mol Cell 58:323-338. http://dx.doi.org/10.1016/j.molcel.2015.02.031.
170. Chaudhury I, Sareen A, Raghunandan M, Sobeck A. 2013. FANCD2 regulates BLM complex functions independently of FANCI to promote replication fork recovery. Nucleic Acids Res 41:6444-6459. http://dx.doi.org/10.1093/nar/gkt348.
171. 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 17:331-339. http://dx.doi.org/10.1016/j.molcel.2005.01.008.
172. Kim JM, Parmar K, Huang M, Weinstock DM, Ruit CA, Kutok JL, D'Andrea AD. 2009. Inactivation of murine Usp1 results in genomic instability and a Fanconi anemia phenotype. Dev Cell 16:314-320. http://dx.doi.org/10.1016/j.devcel.2009.01.001.
173. Oestergaard VH, Langevin F, Kuiken HJ, Pace P, Niedzwiedz W, Simpson LJ, Ohzeki M, Takata M, Sale JE, Patel KJ. 2007. Deubiquitination of FANCD2 is required for DNA crosslink repair. Mol Cell 28:798-809. http://dx.doi.org/10.1016/j.molcel.2007.09.020.
174. Cotto-Rios XM, Jones MJ, Busino L, Pagano M, Huang TT. 2011. APC/CCdh1-dependent proteolysis of USP1 regulates the response to UV-mediated DNA damage. J Cell Biol 194:177-186. http://dx.doi.org/10.1083/jcb.201101062.
175. Cohn MA, Kee Y, Haas W, Gygi SP, D'Andrea AD. 2009. UAF1 is a subunit of multiple deubiquitinating enzyme complexes. J Biol Chem 284:5343-5351. http://dx.doi.org/10.1074/jbc.M808430200.
176. Park E, Kim JM, Primack B, Weinstock DM, Moreau LA, Parmar K, D'Andrea AD. 2013. Inactivation of Uaf1 causes defective homologous recombination and early embryonic lethality in mice. Mol Cell Biol 33:4360-4370. http://dx.doi.org/10.1128/MCB.00870-13.
177. 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 28:786-797. http://dx.doi.org/10.1016/j.molcel.2007.09.031.
178. Yang K, Moldovan GL, Vinciguerra P, Murai J, Takeda S, D'Andrea AD. 2011. Regulation of the Fanconi anemia pathway by a SUMO-like delivery network. Genes Dev 25:1847-1858. http://dx.doi.org/10.1101/gad.17020911.
179. Lee KY, Yang K, Cohn MA, Sikdar N, D'Andrea AD, Myung K. 2010. Human ELG1 regulates the level of ubiquitinated proliferating cell nuclear antigen (PCNA) through its interactions with PCNA and USP1. J Biol Chem 285:10362-10369. http://dx.doi.org/10.1074/jbc.M109.092544.
180. Sale JE, Lehmann AR, Woodgate R. 2012. Y-family DNA polymerases and their role in tolerance of cellular DNA damage. Nat Rev Mol Cell Biol 13:141-152. http://dx.doi.org/10.1038/nrm3289.
181. Zhuang Z, Johnson RE, Haracska L, Prakash L, Prakash S, Benkovic SJ. 2008. Regulation of polymerase exchange between Poleta and Poldelta by monoubiquitination of PCNA and the movement of DNA polymerase holoenzyme. Proc Natl Acad Sci U S A 105:5361-5366. http://dx.doi.org/10.1073/pnas.0801310105.
182. Jones MJ, Colnaghi L, Huang TT. 2012. Dysregulation of DNA polymerase kappa recruitment to replication forks results in genomic instability. EMBO J 31:908-918. http://dx.doi.org/10.1038/emboj.2011.457.
183. Huang TT, Nijman SM, Mirchandani KD, Galardy PJ, Cohn MA, Haas W, Gygi SP, Ploegh HL, Bernards R, D'Andrea AD. 2006. Regulation of monoubiquitinated PCNA by DUB autocleavage. Nat Cell Biol 8:339-347.
184. Piatkov KI, Colnaghi L, Bekes M, Varshavsky A, Huang TT. 2012. The auto-generated fragment of the Usp1 deubiquitylase is a physiological substrate of the N-end rule pathway. Mol Cell 48:926-933. http://dx.doi.org/10.1016/j.molcel.2012.10.012.
185. Williams SA, Maecker HL, French DM, Liu J, Gregg A, Silverstein LB, Cao TC, Carano RA, Dixit VM. 2011. USP1 deubiquitinates ID proteins to preserve a mesenchymal stem cell program in osteosarcoma. Cell 146:918-930. http://dx.doi.org/10.1016/j.cell.2011.07.040.
186. Zlatanou A, Sabbioneda S, Miller ES, Greenwalt A, Aggathanggelou A, Maurice MM, Lehmann AR, Stankovic T, Reverdy C, Colland F, Vaziri C, Stewart GS. 11 May 2015. USP7 is essential for maintaining Rad18 stability and DNA damage tolerance. Oncogene http://dx.doi.org/10.1038/onc.2015.149.
187. Qian J, Pentz K, Zhu Q, Wang Q, He J, Srivastava AK, Wani AA. 2015. USP7 modulates UV-induced PCNA monoubiquitination by regulating DNA polymerase eta stability. Oncogene 34:4791-4796. http://dx.doi.org/10.1038/onc.2014.394.
188. Poole LB, Hall A, Nelson KJ. 2011. Overview of peroxiredoxins in oxidant defense and redox regulation. Curr Protoc Toxicol Chapter 7:Unit 7.9. http://dx.doi.org/10.1002/0471140856.tx0709s49.
189. Tonks NK. 2006. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 7:833-846. http://dx.doi.org/10.1038/nrm2039.
190. Tonks NK. 2005. Redox redux: revisiting PTPs and the control of cell signaling. Cell 121:667-670. http://dx.doi.org/10.1016/j.cell.2005.05.016.
191. Salmeen A, Barford D. 2008. Methods for preparing crystals of reversibly oxidized proteins: crystallization of protein tyrosine phosphatase 1B as an example. Methods Mol Biol 476:101-116.
192. den Hertog J, Groen A, van der Wijk T. 2005. Redox regulation of protein-tyrosine phosphatases. Arch Biochem Biophys 434:11-15. http://dx.doi.org/10.1016/j.abb.2004.05.024.
193. Cotto-Rios XM, Bekes M, Chapman J, Ueberheide B, Huang TT. 2012. Deubiquitinases as a signaling target of oxidative stress. Cell Rep 2:1475-1484. http://dx.doi.org/10.1016/j.celrep.2012.11.011.
194. Lee JG, Baek K, Soetandyo N, Ye Y. 2013. Reversible inactivation of deubiquitinases by reactive oxygen species in vitro and in cells. Nat Commun 4:1568. http://dx.doi.org/10.1038/ncomms2532.
195. Kulathu Y, Garcia FJ, Mevissen TE, Busch M, Arnaudo N, Carroll KS, Barford D, Komander D. 2013. Regulation of A20 and other OTU deubiquitinases by reversible oxidation. Nat Commun 4:1569. http://dx.doi.org/10.1038/ncomms2567.
196. Zlatanou A, Despras E, Braz-Petta T, Boubakour-Azzouz I, Pouvelle C, Stewart GS, Nakajima S, Yasui A, Ishchenko AA, Kannouche PL. 2011. The hMsh2-hMsh6 complex acts in concert with monoubiquitinated PCNA and Pol eta in response to oxidative DNA damage in human cells. Mol Cell 43:649-662. http://dx.doi.org/10.1016/j.molcel.2011.06.023.
197. Lee HS, Lee SA, Hur SK, Seo JW, Kwon J. 2014. Stabilization and targeting of INO80 to replication forks by BAP1 during normal DNA synthesis. Nat Commun 5:5128. http://dx.doi.org/10.1038/ncomms6128.
198. Morrison AJ, Highland J, Krogan NJ, Arbel-Eden A, Greenblatt JF, Haber JE, Shen X. 2004. INO80 and gamma-H2AX interaction links ATP-dependent chromatin remodeling to DNA damage repair. Cell 119:767-775. http://dx.doi.org/10.1016/j.cell.2004.11.037.
199. van Attikum H, Fritsch O, Hohn B, Gasser SM. 2004. Recruitment of the INO80 complex by H2A phosphorylation links ATP-dependent chromatin remodeling with DNA double-strand break repair. Cell 119:777-788. http://dx.doi.org/10.1016/j.cell.2004.11.033.
200. Fousteri M, Mullenders LH. 2008. Transcription-coupled nucleotide excision repair in mammalian cells: molecular mechanisms and biological effects. Cell Res 18:73-84. http://dx.doi.org/10.1038/cr.2008.6.
201. Hanawalt PC, Spivak G. 2008. Transcription-coupled DNA repair: two decades of progress and surprises. Nat Rev Mol Cell Biol 9:958-970. http://dx.doi.org/10.1038/nrm2549.
202. Saijo M. 2013. The role of Cockayne syndrome group A (CSA) protein in transcription-coupled nucleotide excision repair. Mech Ageing Dev 134:196-201. http://dx.doi.org/10.1016/j.mad.2013.03.008.
203. 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 20:1429-1434. http://dx.doi.org/10.1101/gad.378206.
204. 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 44:598-602. http://dx.doi.org/10.1038/ng.2230.
205. Zhang X, Horibata K, Saijo M, Ishigami C, Ukai A, Kanno S, Tahara H, Neilan EG, Honma M, Nohmi T, Yasui A, Tanaka K. 2012. Mutations in UVSSA cause UV-sensitive syndrome and destabilize ERCC6 in transcription-coupled DNA repair. Nat Genet 44:593-597. http://dx.doi.org/10.1038/ng.2228.
206. 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 nucleotideexcision repair. Nat Genet 44:586-592. http://dx.doi.org/10.1038/ng.2229.
207. Schwertman P, Vermeulen W, Marteijn JA. 2013. UVSSA and USP7, a new couple in transcription-coupled DNA repair. Chromosoma 122:275-284. http://dx.doi.org/10.1007/s00412-013-0420-2.
208. Sugasawa K, Okuda Y, Saijo M, Nishi R, Matsuda N, Chu G, Mori T, Iwai S, Tanaka K, Hanaoka F. 2005. UV-induced ubiquitylation of XPC protein mediated by UV-DDB-ubiquitin ligase complex. Cell 121:387-400. http://dx.doi.org/10.1016/j.cell.2005.02.035.
209. 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. http://dx.doi.org/10.1083/jcb.201212075.
210. 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. http://dx.doi.org/10.1038/ncomms8499.
211. He J, Zhu Q, Wani G, Sharma N, Han C, Qian J, Pentz K, Wang QE, Wani AA. 2014. Ubiquitin-specific protease 7 regulates nucleotide excision repair through deubiquitinating XPC protein and preventing XPC protein from undergoing ultraviolet light-induced and VCP/p97 protein-regulated proteolysis. J Biol Chem 289:27278-27289. http://dx.doi.org/10.1074/jbc.M114.589812.
212. Zhang L, Lubin A, Chen H, Sun Z, Gong F. 2012. The deubiquitinating protein USP24 interacts with DDB2 and regulates DDB2 stability. Cell Cycle 11:4378-4384. http://dx.doi.org/10.4161/cc.22688.
213. Zhang L, Nemzow L, Chen H, Lubin A, Rong X, Sun Z, Harris TK, Gong F. 2015. The deubiquitinating enzyme USP24 is a regulator of the UV damage response. Cell Rep 10:140-147. http://dx.doi.org/10.1016/j.celrep.2014.12.024.
214. Parsons JL, Dianov GL. 2013. Co-ordination of base excision repair and genome stability. DNA Repair (Amst) 12:326-333. http://dx.doi.org/10.1016/j.dnarep.2013.02.001.
215. Dianov GL, Parsons JL. 2007. Co-ordination of DNA single strand break repair. DNA Repair (Amst) 6:454-460. http://dx.doi.org/10.1016/j.dnarep.2006.10.009.
216. Horton JK, Watson M, Stefanick DF, Shaughnessy DT, Taylor JA, Wilson SH. 2008. XRCC1 and DNA polymerase beta in cellular protection against cytotoxic DNA single-strand breaks. Cell Res 18:48-63. http://dx.doi.org/10.1038/cr.2008.7.
217. Ochs K, Sobol RW, Wilson SH, Kaina B. 1999. Cells deficient in DNA polymerase beta are hypersensitive to alkylating agent-induced apoptosis and chromosomal breakage. Cancer Res 59:1544-1551.
218. Cabelof DC, Guo Z, Raffoul JJ, Sobol RW, Wilson SH, Richardson A, Heydari AR. 2003. Base excision repair deficiency caused by polymerase beta haploinsufficiency: accelerated DNA damage and increased mutational response to carcinogens. Cancer Res 63:5799-5807.
219. Canitrot Y, Frechet M, Servant L, Cazaux C, Hoffmann JS. 1999. Overexpression of DNA polymerase beta: a genomic instability enhancer process. FASEB J 13:1107-1111.
220. Chan K, Houlbrook S, Zhang QM, Harrison M, Hickson ID, Dianov GL. 2007. Overexpression of DNA polymerase beta results in an increased rate of frameshift mutations during base excision repair. Mutagenesis 22:183-188. http://dx.doi.org/10.1093/mutage/gel070.
221. Parsons JL, Tait PS, Finch D, Dianova II, Allinson SL, Dianov GL. 2008. CHIP-mediated degradation and DNA damage-dependent stabilization regulate base excision repair proteins. Mol Cell 29:477-487. http://dx.doi.org/10.1016/j.molcel.2007.12.027.
222. Parsons JL, Tait PS, Finch D, Dianova II, Edelmann MJ, Khoronenkova SV, Kessler BM, Sharma RA, McKenna WG, Dianov GL. 2009. Ubiquitin ligase ARF-BP1/Mule modulates base excision repair. EMBOJ 28:3207-3215. http://dx.doi.org/10.1038/emboj.2009.243.
223. Parsons JL, Dianova II, Khoronenkova SV, Edelmann MJ, Kessler BM, Dianov GL. 2011. USP47 is a deubiquitylating enzyme that regulates base excision repair by controlling steady-state levels of DNA polymerase beta. Mol Cell 41:609-615. http://dx.doi.org/10.1016/j.molcel.2011.02.016.
224. Khoronenkova SV, Dianov GL. 2013. USP7S-dependent inactivation of Mule regulates DNA damage signalling and repair. Nucleic Acids Res 41:1750-1756. http://dx.doi.org/10.1093/nar/gks1359.
225. Khoronenkova SV, Dianova II, Ternette N, Kessler BM, Parsons JL, Dianov GL. 2012. ATM-dependent downregulation of USP7/HAUSP by PPM1G activates p53 response to DNA damage. Mol Cell 45:801-813. http://dx.doi.org/10.1016/j.molcel.2012.01.021.
226. Edmonds MJ, Parsons JL. 2014. Regulation of base excision repair proteins by ubiquitylation. Exp Cell Res 329:132-138. http://dx.doi.org/10.1016/j.yexcr.2014.07.031.
227. De Bont R, van Larebeke N. 2004. Endogenous DNA damage in humans: a review of quantitative data. Mutagenesis 19:169-185. http://dx.doi.org/10.1093/mutage/geh025.
228. Sedgwick B, Bates PA, Paik J, Jacobs SC, Lindahl T. 2007. Repair of alkylated DNA: recent advances. DNA Repair (Amst) 6:429-442. http://dx.doi.org/10.1016/j.dnarep.2006.10.005.
229. Zhao Y, Majid MC, Soll JM, Brickner JR, Dango S, Mosammaparast N. 2015. Noncanonical regulation of alkylation damage resistance by the OTUD4 deubiquitinase. EMBO J 34:1687-1703. http://dx.doi.org/10.15252/embj.201490497.
230. 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 285:30971-30981. http://dx.doi.org/10.1074/jbc.M110.135319.
231. Shao G, Patterson-Fortin J, Messick TE, Feng D, Shanbhag N, Wang Y, Greenberg RA. 2009. MERIT40 controls BRCA1-Rap80 complex integrity and recruitment to DNA double-strand breaks. Genes Dev 23:740-754. http://dx.doi.org/10.1101/gad.1739609.
232. Kee Y, Yang K, Cohn MA, Haas W, Gygi SP, D'Andrea AD. 2010. WDR20regulates activity of the USP12 x UAF1 deubiquitinating enzyme complex. J Biol Chem 285:11252-11257. http://dx.doi.org/10.1074/jbc.M109.095141.
233. Lim KH, Baek KH. 2013. Deubiquitinating enzymes as therapeutic targets in cancer. Curr Pharm Des 19:4039-4052. http://dx.doi.org/10.2174/1381612811319220013.
234. Sippl W, Collura V, Colland F. 2011. Ubiquitin-specific proteases as cancer drug targets. Future Oncol 7:619-632. http://dx.doi.org/10.2217/fon.11.39.
235. Nicholson B, Suresh Kumar KG. 2011. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem Biophys 60:61-68. http://dx.doi.org/10.1007/s12013-011-9185-5.
236. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, Yue P, Dornan D, Huang DC, Dixit VM. 2010. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463:103-107. http://dx.doi.org/10.1038/nature08646.
237. Liang Q, Dexheimer TS, Zhang P, Rosenthal AS, Villamil MA, You C, Zhang Q, Chen J, Ott CA, Sun H, Luci DK, Yuan B, Simeonov A, Jadhav A, Xiao H, Wang Y, Maloney DJ, Zhuang Z. 2014. A selective USP1-UAF1 inhibitor links deubiquitination to DNA damage responses. Nat Chem Biol 10:298-304. http://dx.doi.org/10.1038/nchembio.1455.
238. Park E, Kim H, Kim JM, Primack B, Vidal-Cardenas S, Xu Y, Price BD, Mills AA, D'Andrea AD. 2013. FANCD2 activates transcription of TAp63 and suppresses tumorigenesis. Mol Cell 50:908-918. http://dx.doi.org/10.1016/j.molcel.2013.05.017.
239. 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. http://dx.doi.org/10.1016/j.cell.2010.04.038.
240. Ismail IH, Gagne JP, Genois MM, Strickfaden H, McDonald D, Xu Z, Poirier GG, Masson JY, Hendzel MJ. 2015. The RNF138 E3 ligase displaces Ku to promote DNA end resection and regulate DNA repair pathway choice. Nat Cell Biol 17:1446-1457. http://dx.doi.org/10.1038/ncb3259.
241. O'Connor HF, Lyon N, Leung JW, Agarwal P, Swaim CD, Miller KM, Huibregtse JM. 2015. Ubiquitin-activated interaction traps (UBAITs) identify E3 ligase binding partners. EMBO Rep 16:1699-1712. http://dx.doi.org/10.15252/embr.201540620.
242. Meyer HJ, Rape M. 2014. Enhanced protein degradation by branched ubiquitin chains. Cell 157:910-921. http://dx.doi.org/10.1016/j.cell.2014.03.037.
243. Silva GM, Finley D, Vogel C. 2015. K63 polyubiquitination is a new modulator of the oxidative stress response. Nat Struct Mol Biol 22:116-123. http://dx.doi.org/10.1038/nsmb.2955.