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Article

USP28 Is Recruited to Sites of DNA Damage by the Tandem BRCT Domains of 53BP1 but Plays a Minor Role in Double-Strand Break Metabolism

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Pages 2062-2074 | Received 11 Feb 2014, Accepted 20 Mar 2014, Published online: 20 Mar 2023

REFERENCES

  • Jackson SP, Bartek J. 2009. The DNA-damage response in human biology and disease. Nature 461:1071–1078. http://dx.doi.org/10.1038/nature08467.
  • 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.
  • Stracker TH, Petrini JH. 2011. The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell Biol. 12:90–103. http://dx.doi.org/10.1038/nrm3047.
  • Stracker TH, Roig I, Knobel PA, Marjanovic M. 2013. The ATM signaling network in development and disease. Front Genet. 4:37. http://dx.doi.org/10.3389/fgene.2013.00037.
  • Jackson SP, Durocher D. 2013. Regulation of DNA damage responses by ubiquitin and SUMO. Mol. Cell 49:795–807. http://dx.doi.org/10.1016/j.molcel.2013.01.017.
  • Cohen P, Tcherpakov M. 2010. Will the ubiquitin system furnish as many drug targets as protein kinases? Cell 143:686–693. http://dx.doi.org/10.1016/j.cell.2010.11.016.
  • Ruffner H, Joazeiro CA, Hemmati D, Hunter T, Verma IM. 2001. Cancer-predisposing mutations within the RING domain of BRCA1: loss of ubiquitin protein ligase activity and protection from radiation hypersensitivity. Proc. Natl. Acad. Sci. U. S. A. 98:5134–5139. http://dx.doi.org/10.1073/pnas.081068398.
  • Xia Y, Pao GM, Chen HW, Verma IM, Hunter T. 2003. Enhancement of BRCA1 E3 ubiquitin ligase activity through direct interaction with the BARD1 protein. J. Biol. Chem. 278:5255–5263. http://dx.doi.org/10.1074/jbc.M204591200.
  • Zgheib O, Pataky K, Brugger J, Halazonetis TD. 2009. An oligomerized 53BP1 tudor domain suffices for recognition of DNA double-strand breaks. Mol. Cell. Biol. 29:1050–1058. http://dx.doi.org/10.1128/MCB.01011-08.
  • 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.
  • 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. http://dx.doi.org/10.1016/j.cell.2006.10.043.
  • Difilippantonio S, Gapud E, Wong N, Huang CY, Mahowald G, Chen HT, Kruhlak MJ, Callen E, Livak F, Nussenzweig MC, Sleckman BP, Nussenzweig A. 2008. 53BP1 facilitates long-range DNA end-joining during V(D)J. recombination. Nature 456:529–533. http://dx.doi.org/10.1038/nature07476.
  • Dimitrova N, Chen YC, Spector DL, de Lange T. 2008. 53BP1 promotes non-homologous end joining of telomeres by increasing chromatin mobility. Nature 456:524–528. http://dx.doi.org/10.1038/nature07433.
  • Manis JP, Morales JC, Xia Z, Kutok JL, Alt FW, Carpenter PB. 2004. 53BP1 links DNA damage-response pathways to immunoglobulin heavy chain class-switch recombination. Nat. Immunol. 5:481–487. http://dx.doi.org/10.1038/ni1067.
  • Ward IM, Reina-San-Martin B, Olaru A, Minn K, Tamada K, Lau JS, Cascalho M, Chen L, Nussenzweig A, Livak F, Nussenzweig MC, Chen J. 2004. 53BP1 is required for class switch recombination. J. Cell Biol. 165:459–464. http://dx.doi.org/10.1083/jcb.200403021.
  • Morales JC, Xia Z, Lu T, Aldrich MB, Wang B, Rosales C, Kellems RE, Hittelman WN, Elledge SJ, Carpenter PB. 2003. Role for the BRCA1 C-terminal repeats (BRCT) protein 53BP1 in maintaining genomic stability. J. Biol. Chem. 278:14971–14977. http://dx.doi.org/10.1074/jbc.M212484200.
  • Ward IM, Minn K, van Deursen J, Chen J. 2003. p53 binding protein 53BP1 is required for DNA damage responses and tumor suppression in mice. Mol. Cell. Biol. 23:2556–2563. http://dx.doi.org/10.1128/MCB.23.7.2556-2563.2003.
  • 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.
  • 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.
  • Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, Haffty BG, Tommiska J, Blomqvist C, Drapkin R, Adams DJ, Nevanlinna H, Bartek J, Tarsounas M, Ganesan S, Jonkers J. 2010. 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat. Struct. Mol. Biol. 17:688–695. http://dx.doi.org/10.1038/nsmb.1831.
  • Jaspers JE, Kersbergen A, Boon U, Sol W, van Deemter L, Zander SA, Drost R, Wientjens E, Ji J, Aly A, Doroshow JH, Cranston A, Martin NM, Lau A, O'Connor MJ, Ganesan S, Borst P, Jonkers J, Rottenberg S. 2012. Loss of 53BP1 causes PARP inhibitor resistance in Brca1-mutated mouse mammary tumors. Cancer Discov. 3:68–81. http://dx.doi.org/10.1158/2159-8290.CD-12-0049.
  • Jacq X, Kemp M, Martin NM, Jackson SP. 2013. Deubiquitylating enzymes and DNA damage response pathways. Cell Biochem. Biophys. 67:25–43. http://dx.doi.org/10.1007/s12013-013-9635-3.
  • Zhang D, Zaugg K, Mak TW, Elledge SJ. 2006. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126:529–542. http://dx.doi.org/10.1016/j.cell.2006.06.039.
  • Bassermann F, Frescas D, Guardavaccaro D, Busino L, Peschiaroli A, Pagano M. 2008. The Cdc14B-Cdh1-Plk1 axis controls the G2 DNA-damage-response checkpoint. Cell 134:256–267. http://dx.doi.org/10.1016/j.cell.2008.05.043.
  • Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R, Moll R, Elledge SJ, Eilers M. 2007. The ubiquitin-specific protease USP28 is required for MYC stability. Nat. Cell Biol. 9:765–774. http://dx.doi.org/10.1038/ncb1601.
  • Schoppy DW, Ragland RL, Gilad O, Shastri N, Peters AA, Murga M, Fernandez-Capetillo O, Diehl JA, Brown EJ. 2012. Oncogenic stress sensitizes murine cancers to hypomorphic suppression of ATR. J. Clin. Invest. 122:241–252. http://dx.doi.org/10.1172/JCI58928.
  • Campaner S, Amati B. 2012. Two sides of the Myc-induced DNA damage response: from tumor suppression to tumor maintenance. Cell Div. 7:6. http://dx.doi.org/10.1186/1747-1028-7-6.
  • Popov N, Herold S, Llamazares M, Schulein C, Eilers M. 2007. Fbw7 and Usp28 regulate myc protein stability in response to DNA damage. Cell Cycle 6:2327–2331. http://dx.doi.org/10.4161/cc.6.19.4804.
  • Welcker M, Orian A, Jin J, Grim JE, Harper JW, Eisenman RN, Clurman BE. 2004. The Fbw7 tumor suppressor regulates glycogen synthase kinase 3 phosphorylation-dependent c-Myc protein degradation. Proc. Natl. Acad. Sci. U. S. A. 101:9085–9090. http://dx.doi.org/10.1073/pnas.0402770101.
  • Yada M, Hatakeyama S, Kamura T, Nishiyama M, Tsunematsu R, Imaki H, Ishida N, Okumura F, Nakayama K, Nakayama KI. 2004. Phosphorylation-dependent degradation of c-Myc is mediated by the F-box protein Fbw7. EMBO J. 23:2116–2125. http://dx.doi.org/10.1038/sj.emboj.7600217.
  • Galanty Y, Belotserkovskaya R, Coates J, Polo S, Miller KM, Jackson SP. 2009. Mammalian SUMO E3-ligases PIAS1 and PIAS4 promote responses to DNA double-strand breaks. Nature 462:935–939. http://dx.doi.org/10.1038/nature08657.
  • Limoli CL, Ward JF. 1993. A new method for introducing double-strand breaks into cellular DNA. Radiat Res. 134:160–169.
  • Cescutti R, Negrini S, Kohzaki M, Halazonetis TD. 2010. TopBP1 functions with 53BP1 in the G1 DNA damage checkpoint. EMBO J. 39:3723–3732. http://dx.doi.org/10.1038/emboj.2010.238.
  • Certo MT, Ryu BY, Annis JE, Garibov M, Jarjour J, Rawlings DJ, Scharenberg AM. 2011. Tracking genome engineering outcome at individual DNA breakpoints. Nat. Methods 8:671–676. http://dx.doi.org/10.1038/nmeth.1648.
  • Lista F, Bertness V, Guidos CJ, Danska JS, Kirsch IR. 1997. The absolute number of trans-rearrangements between the TCRG and TCRB loci is predictive of lymphoma risk: a severe combined immune deficiency (SCID) murine model. Cancer Res. 57:4408–4413.
  • Iwabuchi K, Basu BP, Kysela B, Kurihara T, Shibata M, Guan D, Cao Y, Hamada T, Imamura K, Jeggo PA, Date T, Doherty AJ. 2003. Potential role for 53BP1 in DNA end-joining repair through direct interaction with DNA. J. Biol. Chem. 278:36487–36495. http://dx.doi.org/10.1074/jbc.M304066200.
  • Ward IM, Minn K, Jorda KG, Chen J. 2003. Accumulation of checkpoint protein 53BP1 at DNA breaks involves its binding to phosphorylated histone H2AX. J. Biol. Chem. 278:19579–19582. http://dx.doi.org/10.1074/jbc.C300117200.
  • Polo SE, Jackson SP. 2011. Dynamics of DNA damage response proteins at DNA breaks: a focus on protein modifications. Genes Dev. 25:409–433. http://dx.doi.org/10.1101/gad.2021311.
  • Huen MS, Huang J, Leung JW, Sy SM, Leung KM, Ching YP, Tsao SW, Chen J. 2010. Regulation of chromatin architecture by the PWWP domain-containing DNA damage-responsive factor EXPAND1/MUM1. Mol. Cell 37:854–864. http://dx.doi.org/10.1016/j.molcel.2009.12.040.
  • 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.
  • Kobayashi Y, Tycko B, Soreng AL, Sklar J. 1991. Transrearrangements between antigen receptor genes in normal human lymphoid tissues and in ataxia telangiectasia. J. Immunol. 147:3201–3209.
  • Takai H, Naka K, Okada Y, Watanabe M, Harada N, Saito S, Anderson CW, Appella E, Nakanishi M, Suzuki H, Nagashima K, Sawa H, Ikeda K, Motoyama N. 2002. Chk2-deficient mice exhibit radioresistance and defective p53-mediated transcription. EMBO J. 21:5195–5205. http://dx.doi.org/10.1093/emboj/cdf506.
  • Stracker TH, Couto SS, Cordon-Cardo C, Matos T, Petrini JH. 2008. Chk2 suppresses the oncogenic potential of DNA replication-associated DNA damage. Mol. Cell 31:21–32. http://dx.doi.org/10.1016/j.molcel.2008.04.028.
  • Bohgaki T, Bohgaki M, Cardoso R, Panier S, Zeegers D, Li L, Stewart GS, Sanchez O, Hande MP, Durocher D, Hakem A, Hakem R. 2011. Genomic instability, defective spermatogenesis, immunodeficiency, and cancer in a mouse model of the RIDDLE syndrome. PLoS Genet. 7(4):e1001381. http://dx.doi.org/10.1371/journal.pgen.1001381.
  • 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.
  • Ramachandran S, Chahwan R, Nepal RM, Frieder D, Panier S, Roa S, Zaheen A, Durocher D, Scharff MD, Martin A. 2010. The RNF8/RNF168 ubiquitin ligase cascade facilitates class switch recombination. Proc. Natl. Acad. Sci. U. S. A. 107:809–814. http://dx.doi.org/10.1073/pnas.0913790107.
  • Santos MA, Huen MS, Jankovic M, Chen HT, Lopez-Contreras AJ, Klein IA, Wong N, Barbancho JL, Fernandez-Capetillo O, Nussenzweig MC, Chen J, Nussenzweig A. 2010. Class switching and meiotic defects in mice lacking the E3 ubiquitin ligase RNF8. J. Exp. Med. 207:973–981. http://dx.doi.org/10.1084/jem.20092308.
  • 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.
  • Hao Z, Duncan GS, Su YW, Li WY, Silvester J, Hong C, You H, Brenner D, Gorrini C, Haight J, Wakeham A, You-Ten A, McCracken S, Elia A, Li Q, Detmar J, Jurisicova A, Hobeika E, Reth M, Sheng Y, Lang PA, Ohashi PS, Zhong Q, Wang X, Mak TW. 2012. The E3 ubiquitin ligase Mule acts through the ATM-p53 axis to maintain B lymphocyte homeostasis. J. Exp. Med. 209:173–186. http://dx.doi.org/10.1084/jem.20111363.
  • Li L, Halaby MJ, Hakem A, Cardoso R, El Ghamrasni S, Harding S, Chan N, Bristow R, Sanchez O, Durocher D, Hakem R. 2010. Rnf8 deficiency impairs class switch recombination, spermatogenesis, and genomic integrity and predisposes for cancer. J. Exp. Med. 207:983–997. http://dx.doi.org/10.1084/jem.20092437.
  • 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.
  • Lottersberger F, Bothmer A, Robbiani DF, Nussenzweig MC, de Lange T. 2013. Role of 53BP1 oligomerization in regulating double-strand break repair. Proc. Natl. Acad. Sci. U. S. A. 110:2146–2151. http://dx.doi.org/10.1073/pnas.1222617110.
  • Derbyshire DJ, Basu BP, Serpell LC, Joo WS, Date T, Iwabuchi K, Doherty AJ. 2002. Crystal structure of human 53BP1 BRCT domains bound to p53 tumour suppressor. EMBO J. 21:3863–3872. http://dx.doi.org/10.1093/emboj/cdf383.
  • Joo WS, Jeffrey PD, Cantor SB, Finnin MS, Livingston DM, Pavletich NP. 2002. Structure of the 53BP1 BRCT region bound to p53 and its comparison to the Brca1 BRCT structure. Genes Dev. 16:583–593. http://dx.doi.org/10.1101/gad.959202.
  • Iwabuchi K, Bartel PL, Li B, Marraccino R, Fields S. 1994. Two cellular proteins that bind to wild-type but not mutant p53. Proc. Natl. Acad. Sci. U. S. A. 91:6098–6102.
  • Parrinello S, Samper E, Krtolica A, Goldstein J, Melov S, Campisi J. 2003. Oxygen sensitivity severely limits the replicative lifespan of murine fibroblasts. Nat. Cell Biol. 5:741–747. http://dx.doi.org/10.1038/ncb1024.
  • Yu X, Chini CC, He M, Mer G, Chen J. 2003. The BRCT domain is a phospho-protein binding domain. Science 302:639–642. http://dx.doi.org/10.1126/science.1088753.
  • Manke IA, Lowery DM, Nguyen A, Yaffe MB. 2003. BRCT repeats as phosphopeptide-binding modules involved in protein targeting. Science 302:636–639. http://dx.doi.org/10.1126/science.1088877.
  • Wang Z, Inuzuka H, Zhong J, Wan L, Fukushima H, Sarkar FH, Wei W. 2012. Tumor suppressor functions of FBW7 in cancer development and progression. FEBS Lett. 586:1409–1418. http://dx.doi.org/10.1016/j.febslet.2012.03.017.
  • Welcker M, Clurman BE. 2008. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat. Rev. Cancer. 8:83–93. http://dx.doi.org/10.1038/nrc2290.
  • Bohgaki M, Hakem A, Halaby MJ, Bohgaki T, Li Q, Bissey PA, Shloush J, Kislinger T, Sanchez O, Sheng Y, Hakem R. 2013. The E3 ligase PIRH2 polyubiquitylates CHK2 and regulates its turnover. Cell Death Differ 20:812–822. http://dx.doi.org/10.1038/cdd.2013.7.
  • Hakem A, Bohgaki M, Lemmers B, Tai E, Salmena L, Matysiak-Zablocki E, Jung YS, Karaskova J, Kaustov L, Duan S, Madore J, Boutros P, Sheng Y, Chesi M, Bergsagel PL, Perez-Ordonez B, Mes-Masson AM, Penn L, Squire J, Chen X, Jurisica I, Arrowsmith C, Sanchez O, Benchimol S, Hakem R. 2011. Role of Pirh2 in mediating the regulation of p53 and c-Myc. PLoS Genet. 7(11):e1002360. http://dx.doi.org/10.1371/journal.pgen.1002360.
  • Halaby MJ, Hakem R, Hakem A. 2013. Pirh2: an E3 ligase with central roles in the regulation of cell cycle, DNA damage response, and differentiation. Cell Cycle 12:2733–2737. http://dx.doi.org/10.4161/cc.25785.
  • Mosammaparast N, Kim H, Laurent B, Zhao Y, Lim HJ, Majid MC, Dango S, Luo Y, Hempel K, Sowa ME, Gygi SP, Steen H, Harper JW, Yankner B, Shi Y. 2013. The histone demethylase LSD1/KDM1A promotes the DNA damage response. J. Cell Biol. 203:457–470. http://dx.doi.org/10.1083/jcb.201302092.
  • Wu Y, Wang Y, Yang XH, Kang T, Zhao Y, Wang C, Evers BM, Zhou BP. 2013. The deubiquitinase USP28 stabilizes LSD1 and confers stem-cell-like traits to breast cancer cells. Cell Rep. 5:224–236. http://dx.doi.org/10.1016/j.celrep.2013.08.030.
  • Wang J, Scully K, Zhu X, Cai L, Zhang J, Prefontaine GG, Krones A, Ohgi KA, Zhu P, Garcia-Bassets I, Liu F, Taylor H, Lozach J, Jayes FL, Korach KS, Glass CK, Fu XD, Rosenfeld MG. 2007. Opposing LSD1 complexes function in developmental gene activation and repression programmes. Nature 446:882–887. http://dx.doi.org/10.1038/nature05671.
  • Fernandez-Capetillo O, Chen HT, Celeste A, Ward I, Romanienko PJ, Morales JC, Naka K, Xia Z, Camerini-Otero RD, Motoyama N, Carpenter PB, Bonner WM, Chen J, Nussenzweig A. 2002. DNA damage-induced G2-M checkpoint activation by histone H2AX and 53BP1. Nat. Cell Biol. 4:993–997. http://dx.doi.org/10.1038/ncb884.
  • Jankovic M, Feldhahn N, Oliveira TY, Silva IT, Kieffer-Kwon KR, Yamane A, Resch W, Klein I, Robbiani DF, Casellas R, Nussenzweig MC. 2013. 53BP1 Alters the Landscape of DNA rearrangements and suppresses AID-induced B cell lymphoma. Mol. Cell 49:623–631. http://dx.doi.org/10.1016/j.molcel.2012.11.029.
  • Dominguez-Sola D, Victora GD, Ying CY, Phan RT, Saito M, Nussenzweig MC, Dalla-Favera R. 2012. The proto-oncogene MYC is required for selection in the germinal center and cyclic reentry. Nat. Immunol. 13:1083–1091. http://dx.doi.org/10.1038/ni.2428.
  • Flugel D, Gorlach A, Kietzmann T. 2012. GSK-3β regulates cell growth, migration, and angiogenesis via Fbw7 and USP28-dependent degradation of HIF-1α. Blood 119:1292–1301. http://dx.doi.org/10.1182/blood-2011-08-375014.
  • Biton S, Dar I, Mittelman L, Pereg Y, Barzilai A, Shiloh Y. 2006. Nuclear ataxia-telangiectasia mutated (ATM) mediates the cellular response to DNA double strand breaks in human neuron-like cells. J. Biol. Chem. 281:17482–17491. http://dx.doi.org/10.1074/jbc.M601895200.

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