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Review

Epstein–Barr Virus: Overcoming the DNA Damage Response

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Pages 349-360 | Received 01 Feb 2019, Accepted 22 Mar 2019, Published online: 08 May 2019

References

  • Al-Hakim A , Escribano-DiazC, LandryMCet al. The ubiquitous role of ubiquitin in the DNA damage response. DNA Repair (Amst.), 9(12), 1229–1240 (2010).
  • Schwertman P , Bekker-JensenS, MailandN. Regulation of DNA double-strand break repair by ubiquitin and ubiquitin-like modifiers. Nat. Rev. Mol. Cell Biol., 17(6), 379–394 (2016).
  • Hollingworth R , GrandRJ. Modulation of DNA damage and repair pathways by human tumour viruses. Viruses, 7(5), 2542–2591 (2015).
  • Turnell AS , GrandRJ. DNA viruses and the cellular DNA-damage response. J. Gen. Virol., 93(Pt 10), 2076–2097 (2012).
  • Mcfadden K , LuftigMA. Interplay between DNA tumor viruses and the host DNA damage response. Curr. Top. Microbiol. Immunol., 371, 229–257 (2013).
  • Pancholi NJ , PriceAM, WeitzmanMD. Take your PIKK: tumour viruses and DNA damage response pathways. Philos. Trans. R Soc. Lond. B Biol. Sci., 372(1732), (2017).
  • Hau PM , TsaoSW. Epstein–Barr virus hijacks DNA damage response transducers to orchestrate its life cycle. Viruses, 9(11), 652–668 (2017).
  • Dybas JM , HerrmannC, WeitzmanMD. Ubiquitination at the interface of tumor viruses and DNA damage responses. Curr. Opin. Virol., 32, 40–47 (2018).
  • Nikitin PA , YanCM, ForteEet al. An ATM/Chk2-mediated DNA damage-responsive signaling pathway suppresses Epstein–Barr virus transformation of primary human B cells. Cell Host Microbe, 8(6), 510–522 (2010).
  • Nikitin PA , LuftigMA. The DNA damage response in viral-induced cellular transformation. Br. J. Cancer, 106(3), 429–435 (2012).
  • Jha HC , ShuklaSK, LuJ, AjMP, BanerjeeS, RobertsonES. Dissecting the contribution of EBNA3C domains important for EBV-induced B-cell growth and proliferation. Oncotarget, 6(30), 30115–30129 (2015).
  • Jha HC , AjMP, SahaA, BanerjeeS, LuJ, RobertsonES. Epstein–Barr virus essential antigen EBNA3C attenuates H2AX expression. J. Virol., 88(7), 3776–3788 (2014).
  • Hafez AY , MessingerJE, McFaddenKet al. Limited nucleotide pools restrict Epstein–Barr virus-mediated B-cell immortalization. Oncogenesis, 6(6), e349 (2017).
  • Mordasini V , UedaS, AslandogmusRet al. Activation of ATR-Chk1 pathway facilitates EBV-mediated transformation of primary tonsillar B-cells. Oncotarget, 8(4), 6461–6474 (2017).
  • Thorley-Lawson DA . EBV persistence – introducing the virus. Curr. Top. Microbiol. Immunol., 390(Pt 1), 151–209 (2015).
  • Temple RM , ZhuJ, BudgeonL, ChristensenND, MeyersC, SampleCE. Efficient replication of Epstein–Barr virus in stratified epithelium in vitro..Proc. Natl Acad. Sci. USA, 111(46), 16544–16549 (2014).
  • Raab-Traub N . Nasopharyngeal carcinoma: an evolving role for the Epstein–Barr virus. Curr. Top. Microbiol. Immunol., 390(Pt 1), 339–363 (2015).
  • Fukayama M . Epstein–Barr virus and gastric carcinoma. Pathol. Int., 60(5), 337–350 (2010).
  • Morales-Sanchez A , Fuentes-PananaEM. Epstein–Barr virus-associated gastric cancer and potential mechanisms of oncogenesis. Curr. Cancer Drug Targets, 17(6), 534–554 (2017).
  • Skalsky RL , CullenBR. EBV Noncoding RNAs. Curr. Top. Microbiol. Immunol., 391, 181–217 (2015).
  • Wang Y , GuoZ, ShuY, ZhouH, WangH, ZhangW. BART miRNAs: an unimaginable force in the development of nasopharyngeal carcinoma. Eur. J. Cancer Prev., 26(2), 144–150 (2017).
  • Bose S , YapLF, FungMet al. The ATM tumour suppressor gene is down-regulated in EBV-associated nasopharyngeal carcinoma. J. Pathol., 217(3), 345–352 (2009).
  • Lung RW , HauPM, YuKHet al. EBV-encoded miRNAs target ATM-mediated response in nasopharyngeal carcinoma. J. Pathol., 244(4), 394–407 (2018).
  • Zheng X , WangJ, WeiLet al. Epstein–Barr virus microRNA miR-BART5-3p inhibits p53 expression. J. Virol., 92(23), (2018).
  • Wang LW , JiangS, GewurzBE. Epstein–Barr virus LMP1-mediated oncogenicity. J. Virol., 91(21), (2017).
  • Starczynski J , SimmonsW, FlavellJRet al. Variations in ATM protein expression during normal lymphoid differentiation and among B-cell-derived neoplasias. Am. J. Pathol., 163(2), 423–432 (2003).
  • Dutton A , WoodmanCB, ChukwumaMBet al. Bmi-1 is induced by the Epstein–Barr virus oncogene LMP1 and regulates the expression of viral target genes in Hodgkin lymphoma cells. Blood, 109(6), 2597–2603 (2007).
  • Gruhne B , SompallaeR, MasucciMG. Three Epstein–Barr virus latency proteins independently promote genomic instability by inducing DNA damage, inhibiting DNA repair and inactivating cell cycle checkpoints. Oncogene, 28(45), 3997–4008 (2009).
  • Ma X , YangL, XiaoLet al. Down-regulation of EBV-LMP1 radio-sensitizes nasal pharyngeal carcinoma cells via NF-kappaB regulated ATM expression. PLoS ONE, 6(11), e24647 (2011).
  • Wasil LR , WeiL, ChangC, LanL, ShairKH. Regulation of DNA damage signaling and cell death responses by Epstein–Barr virus latent membrane protein 1 (LMP1) and LMP2A in nasopharyngeal carcinoma cells. J. Virol., 89(15), 7612–7624 (2015).
  • Lu J , TangM, LiHet al. EBV-LMP1 suppresses the DNA damage response through DNA-PK/AMPK signaling to promote radioresistance in nasopharyngeal carcinoma. Cancer Lett., 380(1), 191–200 (2016).
  • Frappier L . EBNA1 and host factors in Epstein–Barr virus latent DNA replication. Curr. Opin. Virol., 2(6), 733–739 (2012).
  • Frappier L . The Epstein–Barr virus EBNA1 protein. Scientifica (Cairo), 2012, 438204 (2012).
  • Frappier L . Contributions of Epstein–Barr nuclear antigen 1 (EBNA1) to cell immortalization and survival. Viruses, 4(9), 1537–1547 (2012).
  • Lassoued S , BenAmeur R, AyadiW, GargouriB, BenMansour R, AttiaH. Epstein–Barr virus induces an oxidative stress during the early stages of infection in B lymphocytes, epithelial, and lymphoblastoid cell lines. Mol. Cell Biochem., 313(1–2), 179–186 (2008).
  • Cerimele F , BattleT, LynchRet al. Reactive oxygen signaling and MAPK activation distinguish Epstein–Barr virus (EBV)-positive versus EBV-negative Burkitt’s lymphoma. Proc. Natl Acad. Sci. USA, 102(1), 175–179 (2005).
  • Gruhne B , SompallaeR, MarescottiD, KamranvarSA, GastaldelloS, MasucciMG. The Epstein–Barr virus nuclear antigen-1 promotes genomic instability via induction of reactive oxygen species. Proc. Natl Acad. Sci. USA, 106(7), 2313–2318 (2009).
  • Kamranvar SA , MasucciMG. The Epstein–Barr virus nuclear antigen-1 promotes telomere dysfunction via induction of oxidative stress. Leukemia, 25(6), 1017–1025 (2011).
  • Cao JY , MansouriS, FrappierL. Changes in the nasopharyngeal carcinoma nuclear proteome induced by the EBNA1 protein of Epstein–Barr virus reveal potential roles for EBNA1 in metastasis and oxidative stress responses. J. Virol., 86, 382–394 (2011).
  • Sharpless NE , DepinhoRA. p53: good cop/bad cop. Cell, 110(1), 9–12 (2002).
  • Tavana O , GuW. Modulation of the p53/MDM2 interplay by HAUSP inhibitors. J. Mol. Cell Biol., 9(1), 45–52 (2017).
  • Li M , ChenD, ShilohAet al. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature, 416(6881), 648–653 (2002).
  • Li M , BrooksCL, KonN, GuW. A dynamic role of HAUSP in the p53-Mdm2 pathway. Mol. Cell, 13(6), 879–886 (2004).
  • Cummins JM , RagoC, KohliM, KinzlerKW, LengauerC, VogelsteinB. Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature, 428, 486–487 (2004).
  • Saridakis V , ShengY, SarkariFet al. Structure of the p53 binding domain of HAUSP/USP7 bound to Epstein–Barr nuclear antigen 1 implications for EBV-mediated immortalization. Mol. Cell, 18(1), 25–36 (2005).
  • Sheng Y , SaridakisV, SarkariFet al. Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol., 13(3), 285–291 (2006).
  • Holowaty MN , ShengY, NguyenT, ArrowsmithC, FrappierL. Protein interaction domains of the ubiquitin-specific protease, USP7/HAUSP. J. Biol. Chem., 278(48), 47753–47761 (2003).
  • Holowaty MN , ZeghoufM, WuHet al. Protein profiling with Epstein–Barr nuclear antigen-1 reveals an interaction with the herpesvirus-associated ubiquitin-specific protease HAUSP/USP7. J. Biol. Chem., 278(32), 29987–29994 (2003).
  • Sivachandran N , SarkariF, FrappierL. Epstein–Barr nuclear antigen 1 contributes to nasopharyngeal carcinoma through disruption of PML nuclear bodies. PLoS Pathog., 4(10), e1000170 (2008).
  • Sivachandran N , DawsonCW, YoungLS, LiuFF, MiddeldorpJ, FrappierL. Contributions of the Epstein–Barr virus EBNA1 protein to gastric carcinoma. J. Virol., 86(1), 60–68 (2012).
  • Cheng TC , HsiehSS, HsuWL, ChenYF, HoHH, SheuLF. Expression of Epstein–Barr nuclear antigen 1 in gastric carcinoma cells is associated with enhanced tumorigenicity and reduced cisplatin sensitivity. Int. J. Oncol., 36(1), 151–160 (2010).
  • Pearson M , CarboneR, SebastianiCet al. PML regulates p53 acetylation and premature senescence induced by oncogenic Ras. Nature, 406(6792), 207–210 (2000).
  • Guo A , SalomoniP, LuoJet al. The function of PML in p53-dependent apoptosis. Nat. Cell Biol., 2(10), 730–736 (2000).
  • Sivachandran N , CaoJY, FrappierL. Epstein–Barr virus nuclear antigen 1 hijacks the host kinase CK2 to disrupt PML nuclear bodies. J. Virol., 84(21), 11113–11123 (2010).
  • Su D , MaS, ShanLet al. Ubiquitin-specific protease 7 sustains DNA damage response and promotes cervical carcinogenesis. J. Clin. Invest., 128(10), 4280–4296 (2018).
  • Zhu Q , SharmaN, HeJ, WaniG, WaniAA. USP7 deubiquitinase promotes ubiquitin-dependent DNA damage signaling by stabilizing RNF168. Cell Cycle, 14(9), 1413–1425 (2015).
  • Zlatanou A , SabbionedaS, MillerESet al. USP7 is essential for maintaining Rad18 stability and DNA damage tolerance. Oncogene, 35(8), 965–976 (2015).
  • Dar A , ShibataE, DuttaA. Deubiquitination of Tip60 by USP7 determines the activity of the p53-dependent apoptotic pathway. Mol. Cell Biol., 33(16), 3309–3320 (2013).
  • Styles CT , PaschosK, WhiteRE, FarrellPJ. The cooperative functions of the EBNA3 proteins are central to EBV persistence and latency. Pathogens, 7(1), (2018).
  • Choudhuri T , VermaSC, LanK, MurakamiM, RobertsonES. The ATM/ATR signaling effector Chk2 is targeted by Epstein–Barr virus nuclear antigen 3C to release the G2/M cell cycle block. J. Virol., 81(12), 6718–6730 (2007).
  • Yi F , SahaA, MurakamiMet al. Epstein–Barr virus nuclear antigen 3C targets p53 and modulates its transcriptional and apoptotic activities. Virology, 388(2), 236–247 (2009).
  • Saha A , MurakamiM, KumarP, BajajB, SimsK, RobertsonES. Epstein–Barr virus nuclear antigen 3C augments Mdm2-mediated p53 ubiquitination and degradation by deubiquitinating Mdm2. J. Virol., 83(9), 4652–4669 (2009).
  • Jha HC , YangK, El-NaccacheDW, SunZ, RobertsonES. EBNA3C regulates p53 through induction of Aurora kinase B. Oncotarget, 6(8), 5788–5803 (2015).
  • Kudoh A , FujitaM, ZhangLet al. Epstein–Barr virus lytic replication elicits ATM checkpoint signal transduction while providing an S-phase-like cellular environment. J. Biol. Chem., 280(9), 8156–8163 (2005).
  • Kudoh A , IwahoriS, SatoYet al. Homologous recombinational repair factors are recruited and loaded onto the viral DNA genome in Epstein–Barr virus replication compartments. J. Virol., 83(13), 6641–6651 (2009).
  • Hau PM , DengW, JiaLet al. Role of ATM in the formation of the replication compartment during lytic replication of Epstein–Barr virus in nasopharyngeal epithelial cells. J. Virol., 89(1), 652–668 (2015).
  • Hagemeier SR , BarlowEA, MengQ, KenneySC. The cellular ataxia telangiectasia-mutated kinase promotes Epstein–Barr virus lytic reactivation in response to multiple different types of lytic reactivation-inducing stimuli. J. Virol., 86(24), 13360–13370 (2012).
  • Wang’ondu R , TealS, ParkR, HestonL, DelecluseH, MillerG. DNA damage signaling is induced in the absence of Epstein–Barr virus (EBV) lytic DNA replication and in response to expression of ZEBRA. PLoS ONE, 10(5), e0126088 (2015).
  • Bailey SG , VerrallE, SchelcherC, RhieA, DohertyAJ, SinclairAJ. Functional interaction between Epstein–Barr virus replication protein Zta and host DNA damage response protein 53BP1. J. Virol., 83(21), 11116–11122 (2009).
  • Huang SY , WuCC, ChengYJet al. Epstein–Barr virus BRLF1 induces genomic instability and progressive malignancy in nasopharyngeal carcinoma cells. Oncotarget, 8(45), 78948–78964 (2017).
  • Chiu SH , WuCC, FangCYet al. Epstein–Barr virus BALF3 mediates genomic instability and progressive malignancy in nasopharyngeal carcinoma. Oncotarget, 5(18), 8583–8601 (2014).
  • Wu CC , LiuMT, ChangYTet al. Epstein–Barr virus DNase (BGLF5) induces genomic instability in human epithelial cells. Nucleic Acids Res., 38(6), 1932–1949 (2010).
  • Chang YH , LeeCP, SuMTet al. Epstein–Barr virus BGLF4 kinase retards cellular S-phase progression and induces chromosomal abnormality. PLoS ONE, 7(6), e39217 (2012).
  • Tarakanova VL , Leung-PinedaV, HwangSet al. γ-herpesvirus kinase actively initiates a DNA damage response by inducing phosphorylation of H2AX to foster viral replication. Cell Host Microbe, 1(4), 275–286 (2007).
  • Li R , ZhuJ, XieZet al. Conserved herpesvirus kinases target the DNA damage response pathway and TIP60 histone acetyltransferase to promote virus replication. Cell Host Microbe, 10(4), 390–400 (2011).
  • Li R , LiaoG, NirujogiRSet al. Phosphoproteomic profiling reveals Epstein–Barr virus protein kinase integration of DNA damage response and mitotic signaling. PLoS Pathog., 11(12), e1005346 (2015).
  • Ho TH , SitzJ, ShenQet al. A screen for Epstein–Barr virus proteins that inhibit the DNA damage response reveals a novel histone binding protein. J. Virol., 92(14), (2018).
  • Yang J , DengW, HauPMet al. Epstein–Barr virus BZLF1 protein impairs accumulation of host DNA damage proteins at damage sites in response to DNA damage. Lab. Invest., 95(8), 937–950 (2015).
  • Sato Y , KamuraT, ShirataNet al. Degradation of phosphorylated p53 by viral protein-ECS E3 ligase complex. PLoS Pathog., 5(7), e1000530 (2009).
  • Leung JW , AgarwalP, CannyMDet al. Nucleosome acidic patch promotes RNF168- and RING1B/BMI1-dependent H2AX and H2A ubiquitination and DNA damage signaling. PLoS Genet., 10(3), e1004178 (2014).
  • Mattiroli F , VissersJH, Van DijkWJet al. RNF168 ubiquitinates K13-15 on H2A/H2AX to drive DNA damage signaling. Cell, 150(6), 1182–1195 (2012).
  • Mattiroli F , UckelmannM, SahtoeDD, Van DijkWJ, SixmaTK. The nucleosome acidic patch plays a critical role in RNF168-dependent ubiquitination of histone H2A. Nat. Commun., 5, 3291 (2014).
  • Avgousti DC , DellaFera AN, OtterCJ, HerrmannC, PancholiNJ, WeitzmanMD. Adenovirus core protein VII down-regulates the DNA damage response on the host genome. J. Virol., 91(20), (2017).
  • Avgousti DC , HerrmannC, KulejKet al. A core viral protein binds host nucleosomes to sequester immune danger signals. Nature, 535(7610), 173–177 (2016).
  • Barbera AJ , ChodaparambilJV, Kelley-ClarkeBet al. The nucleosomal surface as a docking station for Kaposi’s sarcoma herpesvirus LANA. Science, 311(5762), 856–861 (2006).
  • Borozan I , ZapatkaM, FrappierL, FerrettiV. Analysis of Epstein–Barr virus genomes and expression profiles in gastric adenocarcinoma. J. Virol., 92(2), e01239–01317 (2018).
  • Cheng AZ , Yockteng-MelgarJ, JarvisMCet al. Epstein–Barr virus BORF2 inhibits cellular APOBEC3B to preserve viral genome integrity. Nat. Microbiol., 4(1), 78–88 (2019).
  • Harris RS , DudleyJP. APOBECs and virus restriction. Virology, 479–480, 131–145 (2015).
  • Strebel K . HIV accessory proteins versus host restriction factors. Curr. Opin. Virol., 3(6), 692–699 (2013).
  • Tatfi M , HermineO, SuarezF. Epstein–Barr virus (EBV)-related lymphoproliferative disorders in ataxia telangiectasia: does ATM regulate EBV life cycle?Front. Immunol., 9, 3060 (2018).
  • Hu L , LinZ, WuYet al. Comprehensive profiling of EBV gene expression in nasopharyngeal carcinoma through paired-end transcriptome sequencing. Front. Med., 10(1), 61–75 (2016).
  • Abate F , AmbrosioMR, MundoLet al. Distinct viral and mutational spectrum of endemic Burkitt lymphoma. PLoS Pathog., 11(10), e1005158 (2015).

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