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 ORCID:

Jian YUAN

https://orcid.org/0000-0002-2801-8849

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Journal of Zhejiang University SCIENCE B 2021 Vol.22 No.1 P.63-72

http://doi.org/10.1631/jzus.B2000309


Role of deubiquitinating enzymes in DNA double-strand break repair


Author(s):  Yunhui LI, Jian YUAN

Affiliation(s):  The Key Laboratory of Arrhythmias of the Ministry of Education of China, Research Center for Translational Medicine, East Hospital, Tongji University School of Medicine, Shanghai200120, China; more

Corresponding email(s):   yuanjian229@hotmail.com

Key Words:  Deubiquitinating enzymes (DUBs), DNA double-strand breaks (DSBs), DNA repair, Non-homologous end joining (NHEJ), Homologous recombination (HR)


Yunhui LI, Jian YUAN. Role of deubiquitinating enzymes in DNA double-strand break repair[J]. Journal of Zhejiang University Science B, 2021, 22(1): 63-72.

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author="Yunhui LI, Jian YUAN",
journal="Journal of Zhejiang University Science B",
volume="22",
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pages="63-72",
year="2021",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2000309"
}

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PB - Zhejiang University Press & Springer
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DOI - 10.1631/jzus.B2000309


Abstract: 
DNA is the hereditary material in humans and almost all other organisms. It is essential for maintaining accurate transmission of genetic information. In the life cycle, DNA replication, cell division, or genome damage, including that caused by endogenous and exogenous agents, may cause DNA aberrations. Of all forms of DNA damage, DNA double-strand breaks (DSBs) are the most serious. If the repair function is defective, DNA damage may cause gene mutation, genome instability, and cell chromosome loss, which in turn can even lead to tumorigenesis. DNA damage can be repaired through multiple mechanisms. homologous recombination (HR) and non-homologous end joining (NHEJ) are the two main repair mechanisms for DNA DSBs. Increasing amounts of evidence reveal that protein modifications play an essential role in DNA damage repair. Protein deubiquitination is a vital post-translational modification which removes ubiquitin molecules or polyubiquitinated chains from substrates in order to reverse the ubiquitination reaction. This review discusses the role of deubiquitinating enzymes (DUBs) in repairing DNA DSBs. Exploring the molecular mechanisms of DUB regulation in DSB repair will provide new insights to combat human diseases and develop novel therapeutic approaches.

去泛素化酶在DNA双链损伤修复中的作用研究

摘要:DNA是人类和几乎所有有机体的遗传物质,它对于保持遗传信息的准确传递至关重要。在生命周期中,DNA复制、细胞分裂、基因组损伤,以及由内源性和外源性因素引起的损伤,都可能引起DNA损伤。在所有形式的DNA损伤中,DNA双链断裂(DSB)是最严重的。如果修复功能有缺陷,DNA损伤可能导致基因突变、基因组不稳定、细胞染色体丢失,进而导致肿瘤的发生。DNA损伤可以通过多种机制修复。同源重组(HR)和非同源末端连接(NHEJ)是DSB的两种主要修复机制。另外,大量研究表明,蛋白质修饰在DNA损伤修复中起着至关重要的作用。蛋白质的去泛素化是一种重要的翻译后修饰,它可以从底物中去除泛素分子或多泛素链,从而逆转泛素化降解,稳定底物蛋白。本文综述了去泛素化酶(DUB)在DSB损伤修复中的作用,探讨DUB调控DSB修复的分子机制,为开发人类疾病的新疗法提供了全新思路。

关键词:去泛素化酶(DUB);DNA损伤应答;DNA修复;非同源末端连接(NHEJ);同源重组(HR)

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]AltunM, WalterTS, KramerHB, et al., 2015. The human otubain2-ubiquitin structure provides insights into the cleavage specificity of poly-ubiquitin-linkages. PLoS ONE, 10:e0115344.

[2]BrittonS, CoatesJ, JacksonSP, 2013. A new method for high-resolution imaging of Ku foci to decipher mechanisms of DNA double-strand break repair. J Cell Biol, 202(3):579-595.

[3]ButlerLR, DenshamRM, JiaJY, et al., 2012. The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J, 31(19):3918-3934.

[4]CadetJ, BergerM, DoukiT, et al., 1997. Oxidative damage to DNA: formation, measurement, and biological significance. Rev Physiol Biochem Pharmacol, 131:1-87.

[5]CaiJT, WeiJX, SchrottV, et al., 2018. Induction of deubiquitinating enzyme USP50 during erythropoiesis and its potential role in the regulation of Ku70 stability. J Investig Med, 66(1):1-6.

[6]CeccaldiR, RondinelliB, D'AndreaAD, 2016. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol, 26(1):52-64.

[7]ChauhanD, TianZ, NicholsonB, et al., 2012. A small molecule inhibitor of ubiquitin-specific protease-7 induces apoptosis in multiple myeloma cells and overcomes bortezomib resistance. Cancer Cell, 22(3):345-358.

[8]ChenXW, ArcieroCA, WangCR, et al., 2006. BRCC36 is essential for ionizing radiation-induced BRCA1 phosphorylation and nuclear foci formation. Cancer Res, 66(10):5039-5046.

[9]ChengYC, ShiehSY, 2018. Deubiquitinating enzyme USP3 controls CHK1 chromatin association and activation. Proc Natl Acad Sci USA, 115(21):5546-5551.

[10]ChiruvellaKK, LiangZB, WilsonTE, 2013. Repair of double-strand breaks by end joining. Cold Spring Harbor Perspect Biol, 5(5):a012757.

[11]CohenP, TcherpakovM, 2010. Will the ubiquitin system furnish as many drug targets as protein kinases? Cell, 143(5):686-693.

[12]ColemanKA, GreenbergRA, 2011. The BRCA1-RAP80 complex regulates DNA repair mechanism utilization by restricting end resection. J Biol Chem, 286(15):13669-13680.

[13]CooperEM, CutcliffeC, KristiansenTZ, et al., 2009. K63-specific deubiquitination by two JAMM/MPN+ complexes: BRISC-associated Brcc36 and proteasomal Poh1. EMBO J, 28(6):621-631.

[14]CottarelJ, FritP, BombardeO, et al., 2013. A noncatalytic function of the ligation complex during nonhomologous end joining. J Cell Biol, 200(2):173-186.

[15]DoilC,MailandN, Bekker-JensenS, et al., 2009. RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins. Cell, 136(3):435-446.

[16]DongYS, HakimiMA, ChenXW, et al., 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(5):1087-1099.

[17]DurocherD, JacksonSP, 2001. DNA-PK, ATM and ATR as sensors of DNA damage: variations on a theme? Curr Opin Cell Biol, 13(2):225-231.

[18]FarshiP, DeshmukhRR, NwankwoJO, et al., 2015. Deubiquitinases (DUBs) and DUB inhibitors: a patent review. Expert Opin Ther Pat, 25(10):1191-1208.

[19]FengL, WangJD, ChenJJ, 2010. The Lys63-specific deubiquitinating enzyme BRCC36 is regulated by two scaffold proteins localizing in different subcellular compartments. J Biol Chem, 285(40):30982-30988.

[20]GottliebTM, JacksonSP, 1993. The DNA-dependent protein kinase: requirement for DNA ends and association with Ku antigen. Cell, 72(1):131-142.

[21]GuervillyJH, RenaudE, TakataM, et al., 2011. USP1 deubiquitinase maintains phosphorylated CHK1 by limiting its DDB1-dependent degradation. Hum Mol Genet, 20(11):2171-2181.

[22]GuptaC, HeinenCD, 2019. The mismatch repair-dependent DNA damage response: mechanisms and implications. DNA Repair, 78:60-69.

[23]HanpudeP, BhattacharyaS, DeyAK, et al., 2015. Deubiquitinating enzymes in cellular signaling and disease regulation. IUBMB Life, 67(7):544-555.

[24]HarperJW, ElledgeSJ, 2007. The DNA damage response: ten years after. Mol Cell, 28(5):739-745.

[25]HarriganJA, JacqX, MartinNM, et al., 2018. Deubiquitylating enzymes and drug discovery: emerging opportunities. Nat Rev Drug Discov, 17(1):57-78.

[26]HarrisonJC, HaberJE, 2006. Surviving the breakup: the DNA damage checkpoint. Annu Rev Genet, 40:209-235.

[27]HuX, KimJA, CastilloA, et al., 2011. NBA1/MERIT40 and BRE interaction is required for the integrity of two distinct deubiquitinating enzyme BRCC36-containing complexes. J Biol Chem, 286(13):11734-11745.

[28]HuYD, ScullyR, SobhianB, et al., 2011. RAP80-directed tuning of BRCA1 homologous recombination function at ionizing radiation-induced nuclear foci. Genes Dev, 25(7):685-700.

[29]HuangXD, DixitVM, 2016. Drugging the undruggables: exploring the ubiquitin system for drug development. Cell Res, 26(4):484-498.

[30]HurleyJH, LeeS, PragG, 2006. Ubiquitin-binding domains. Biochem J, 399(Pt 3):361-372.

[31]IsmailIH, DavidsonR, Gagn茅JP, et al., 2014. Germline mutations in BAP1 impair its function in DNA double-strand break repair. Cancer Res, 74(16):4282-4294.

[32]JuangYC, LandryMC, SanchesM, et al., 2012. OTUB1 co-opts Lys48-linked ubiquitin recognition to suppress E2 enzyme function. Mol Cell, 45(3):384-397.

[33]KaHI, LeeS, HanS, et al., 2020. Deubiquitinase USP47-stabilized splicing factor IK regulates the splicing of ATM pre-mRNA. Cell Death Discov, 6:34.

[34]KakarougkasA, JeggoPA, 2014. DNA DSB repair pathway choice: an orchestrated handover mechanism. Br J Radiol, 87(1035):20130685.

[35]KakarougkasA, IsmailA, KatsukiY, et al., 2013. Co-operation of BRCA1 and POH1 relieves the barriers posed by 53BP1 and RAP80 to resection. Nucleic Acids Res, 41(22):10298-10311.

[36]KapuriaV, PetersonLF, FangDX, et al., 2010. Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res, 70(22):9265-9276.

[37]KaranamK, KafriR, LoewerA, et al., 2012. Quantitative live cell imaging reveals a gradual shift between DNA repair mechanisms and a maximal use of HR in mid S phase. Mol Cell, 47(2):320-329.

[38]KatoK, NakajimaK, UiA, et al., 2014. Fine-tuning of DNA damage-dependent ubiquitination by OTUB2 supports the DNA repair pathway choice. Mol Cell, 53(4):617-630.

[39]KawanishiS, HirakuY, PinlaorS, et al., 2006. Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem, 387(4):365-372.

[40]KennedyRD, D'AndreaAD, 2005. The Fanconi Anemia/BRCA pathway: new faces in the crowd. Genes Dev, 19(24):2925-2940.

[41]KerzendorferC, O'DriscollM, 2009. Human DNA damage response and repair deficiency syndromes: linking genomic instability and cell cycle checkpoint proficiency. DNA Repair (Amst), 8(9):1139-1152.

[42]KhannaKK, JacksonSP, 2001. DNA double-strand breaks: signaling, repair and the cancer connection. Nature Genet, 27(3):247-254.

[43]KimH, HuangJ, ChenJJ, 2007a. CCDC98 is a BRCA1-BRCT domain-binding protein involved in the DNA damage response. Nat Struct Mol Biol, 14(8):710-715.

[44]KimH, ChenJJ, YuXC, 2007b. Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response. Science, 316(5828):1202-1205.

[45]KomanderD, ClagueMJ, Urb茅S, 2009. Breaking the chains: structure and function of the deubiquitinases. Nat Rev Mol Cell Biol, 10(8):550-563.

[46]LatifC, den ElzenNR, O'ConnellMJ, 2004. DNA damage checkpoint maintenance through sustained Chk1 activity. J Cell Sci, 117(Pt 16):3489-3498.

[47]LeeBH, LeeMJ, ParkS, et al., 2010. Enhancement of proteasome activity by a small-molecule inhibitor of USP14. Nature, 467(7312):179-184.

[48]LiFZ, SunQQ, LiuK, et al., 2019. The deubiquitinase OTUD5 regulates Ku80 stability and non-homologous end joining. Cell Mol Life Sci, 76(19):3861-3873.

[49]LiYH, LuoKT, YinYJ, et al., 2017. USP13 regulates the RAP80-BRCA1 complex dependent DNA damage response. Nat Commun, 8:15752.

[50]LieberMR, 2008. The mechanism of human nonhomologous DNA end joining. J Biol Chem, 283(1):1-5.

[51]LindahT, BarnesDE, 2000. Repair of endogenous DNA damage. Cold Spring Harb Symp Quant Biol, 65:127-133.

[52]LiuHL, ZhangHX, WangXH, et al., 2015. The deubiquitylating enzyme USP4 cooperates with CtIP in DNA double-strand break end resection. Cell Rep, 13(1):93-107.

[53]LiuJL, XiaHG, KimM, et al., 2011. Beclin1 controls the levels of p53 by regulating the deubiquitination activity of USP10 and USP13. Cell, 147(1):223-234.

[54]LiuZX, WuJX, YuXC, 2007. CCDC98 targets BRCA1 to DNA damage sites. Nat Struct Mol Biol, 14(8):716-720.

[55]LuQ, ZhangFL, LuDY, et al., 2019. USP9X stabilizes BRCA1 and confers resistance to DNA-damaging agents in human cancer cells. Cancer Med, 8(15):6730-6740.

[56]LuoKT, LiL, LiYH, et al., 2016. A phosphorylation-deubiquitination cascade regulates the BRCA2-RAD51 axis in homologous recombination. Genes Dev, 30(23):2581-2595.

[57]MattiroliF, VissersJHA, van DijkWJ, et al., 2012. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell, 150(6):1182-1195.

[58]MeuthM, 2010. Chk1 suppressed cell death. Cell Div, 5:21.

[59]MevissenTET, HospenthalMK, GeurinkPP, et al., 2013. OTU deubiquitinases reveal mechanisms of linkage specificity and enable ubiquitin chain restriction analysis. Cell, 154(1):169-184.

[60]NakadaS, TaiI, PanierS, et al., 2010. Non-canonical inhibition of DNA damage-dependent ubiquitination by OTUB1. Nature, 466(7309):941-946.

[61]NicholsonB, LeachCA, GoldenbergSJ, et al., 2008. Characterization of ubiquitin and ubiquitin-like-protein isopeptidase activities. Protein Sci, 17(6):1035-1043.

[62]NijmanSMB, HuangTT, DiracAMG, et al., 2005a. The deubiquitinating enzyme USP1 regulates the Fanconi anemia pathway. Mol Cell, 17(3):331-339.

[63]NijmanSMB, Luna-VargasMPA, VeldsA, et al., 2005b. A genomic and functional inventory of deubiquitinating enzymes. Cell, 123(5):773-786.

[64]NishiR, WijnhovenP, le SageC, et al., 2014. Systematic characterization of deubiquitylating enzymes for roles in maintaining genome integrity. Nat Cell Biol, 16(10):1016-1026.

[65]NishiR, WijnhovenPWG, KimuraY, et al., 2018. The deubiquitylating enzyme UCHL3 regulates Ku80 retention at sites of DNA damage. Sci Rep, 8:17891.

[66]NowsheenS, DengM, LouZK, 2020. Ubiquitin and the DNA double-strand break repair pathway. Genome Instab Dis, 1(2):69-80.

[67]OlivieriM, ChoT, 脕lvarez-Quil贸nA, et al., 2020. A genetic map of the response to DNA damage in human cells. Cell, 182(2):481-496.e21.

[68]OrthweinA, NoordermeerSM, WilsonMD, et al., 2015. A mechanism for the suppression of homologous recombination in G1 cells. Nature, 528(7582):422-426.

[69]PellegriniL, YuDS, LoT, et al., 2002. Insights into DNA recombination from the structure of a RAD51-BRCA2 complex. Nature, 420(6913):287-293.

[70]PengYH, LiaoQC, TanW, et al., 2019. The deubiquitylating enzyme USP15 regulates homologous recombination repair and cancer cell response to PARP inhibitors. Nat Commun, 10:1224.

[71]PfeifferA, LuijsterburgMS, AcsK, et al., 2017. Ataxin-3 consolidates the MDC1-dependent DNA double-strand break response by counteracting the SUMO-targeted ubiquitin ligase RNF4. EMBO J, 36(8):1066-1083.

[72]RehmanSAA, KristariyantoYA, ChoiSY, et al., 2016. MINDY-1 is a member of an evolutionarily conserved and structurally distinct new family of deubiquitinating enzymes. Mol Cell, 63(1):146-155.

[73]RiballoE, K眉hneM, RiefN, et al., 2004. A pathway of double-strand break rejoining dependent upon ATM, Artemis, and proteins locating to 纬-H2AX foci. Mol Cell, 16(5):715-724.

[74]RodriguezR, MeuthM, 2006. Chk1 and p21 cooperate to prevent apoptosis during DNA replication fork stress. Mol Biol Cell, 17(1):402-412.

[75]san FilippoJ, SungP, KleinH, 2008. Mechanism of eukaryotic homologous recombination. Annu Rev Biochem, 77:229-257.

[76]SartoriAA, LukasC, CoatesJ, et al., 2007. Human CtIP promotes DNA end resection. Nature, 450(7169):509-514.

[77]SchmittE, PaquetC, BeaucheminM, et al., 2007. DNA-damage response network at the crossroads of cell-cycle checkpoints, cellular senescence and apoptosis. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 8(6):377-397.

[78]SchoenfeldAR, ApgarS, DoliosG, et al., 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(17):7444-7455.

[79]ScullyR, PandayA, ElangoR, et al., 2019. DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat Rev Mol Cell Biol, 20(11):698-714.

[80]ShanbhagNM, Rafalska-MetcalfIU, Balane-BolivarC, et al., 2010. ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks. Cell, 141(6):970-981.

[81]ShaoG, LilliDR, Patterson-FortinJ, et al., 2009. The Rap80-BRCC36 de-ubiquitinating enzyme complex antagonizes RNF8-Ubc13-dependent ubiquitination events at DNA double strand breaks. Proc Natl Acad Sci USA, 106(9):3166-3171.

[82]SharmaA, AlswillahT, KapoorI, et al., 2020. USP14 is a deubiquitinase for Ku70 and critical determinant of non-homologous end joining repair in autophagy and PTEN-deficient cells. Nucleic Acids Res, 48(2):736-747.

[83]SobhianB, ShaoG, LilliDR, et al., 2007. RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites. Science, 316(5828):1198-1202.

[84]SuDX, MaS, ShanL, et al., 2018. Ubiquitin-specific protease 7 sustains DNA damage response and promotes cervical carcinogenesis. J Clin Invest, 128(10):4280-4296.

[85]SunYL, JiangXF, ChenSJ, et al., 2005. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA, 102(37):13182-13187.

[86]SymingtonLS, GautierJ, 2011. Double-strand break end resection and repair pathway choice. Annu Rev Genet, 45:247-271.

[87]TakedaS, NakamuraK, TaniguchiY, et al., 2007. Ctp1/CtIP and the MRN complex collaborate in the initial steps of homologous recombination. Mol Cell, 28(3):351-352.

[88]TypasD, LuijsterburgMS, WiegantWW, et al., 2015. The de-ubiquitylating enzymes USP26 and USP37 regulate homologous recombination by counteracting RAP80. Nucleic Acids Res, 43(14):6919-6933.

[89]UckelmannM, DenshamRM, BaasR, et al., 2018. USP48 restrains resection by site-specific cleavage of the BRCA1 ubiquitin mark from H2A. Nat Commun, 9:229.

[90]WangB, ElledgeSJ, 2007. Ubc13/Rnf8 ubiquitin ligases control foci formation of the Rap80/Abraxas/Brca1/Brcc36 complex in response to DNA damage. Proc Natl Acad Sci USA, 104(52):20759-20763.

[91]WangB, MatsuokaS, BallifBA, et al., 2007. Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response. Science, 316(5828):1194-1198.

[92]WangXF, LiuZY, ZhangL, et al., 2018. Targeting deubiquitinase USP28 for cancer therapy. Cell Death Dis, 9:186.

[93]WangZQ, ZhangHL, LiuJ, et al., 2016. USP51 deubiquitylates H2AK13, 15ub and regulates DNA damage response. Genes Dev, 30(8):946-959.

[94]WeakeVM, WorkmanJL, 2008. Histone ubiquitination: triggering gene activity. Mol Cell, 29(6):653-663.

[95]WelchmanRL, GordonC, MayerRJ, 2005. Ubiquitin and ubiquitin-like proteins as multifunctional signals. Nat Rev Mol Cell Biol, 6(8):599-609.

[96]WienerR, ZhangXB, WangT, et al., 2012. The mechanism of OTUB1-mediated inhibition of ubiquitination. Nature, 483(7391):618-622.

[97]WijnhovenP, KonietznyR, BlackfordAN, et al., 2015. USP4 auto-deubiquitylation promotes homologous recombination. Mol Cell, 60(3):362-373.

[98]WrigleyJD, GavoryG, SimpsonI, et al., 2017. Identification and characterization of dual inhibitors of the USP25/28 deubiquitinating enzyme subfamily. ACS Chem Biol, 12(12):3113-3125.

[99]WuJH, ChenYP, GengGH, et al., 2019. USP39 regulates DNA damage response and chemo-radiation resistance by deubiquitinating and stabilizing CHK2. Cancer Lett, 449:114-124.

[100]WuZQ, QiuMH, GuoY, et al., 2019. OTU deubiquitinase 4 is silenced and radiosensitizes non-small cell lung cancer cells via inhibiting DNA repair. Cancer Cell Int, 19:99.

[101]YangYF, YangCZ, LiTT, et al., 2020. The deubiquitinase USP38 promotes NHEJ repair through regulation of HDAC1 activity and regulates cancer cell response to genotoxic insults. Cancer Res, 80(4):719-731.

[102]YuH, PakH, Hammond-MartelI, et al., 2014. Tumor suppressor and deubiquitinase BAP1 promotes DNA double-strand break repair. Proc Natl Acad Sci U S A, 111(1):285-290.

[103]YuanJ, LuoKT, DengM, et al., 2014. HERC2-USP20 axis regulates DNA damage checkpoint through Claspin. Nucleic Acids Res, 42(21):13110-13121.

[104]ZhangD, ZauggK, MakTW, et al., 2006. A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell, 126(3):529-542.

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