2,836
Views
91
CrossRef citations to date
0
Altmetric
Original Articles

Middle East respiratory syndrome coronavirus M protein suppresses type I interferon expression through the inhibition of TBK1-dependent phosphorylation of IRF3

, , , , , , , , & show all
Pages 1-9 | Received 13 Nov 2015, Accepted 06 Jan 2016, Published online: 25 Jan 2019

  • ZakiAM,van BoheemenS,BestebroerTM,OsterhausAD,FouchierRA.Isolation of a novel coronavirus from a man with pneumonia in Saudi Arabia.N Engl J Med2012; 367:1814–1820.
  • Centers for Disease Control and Prevention (CDC).Severe respiratory illness associated with a novel coronavirus-Saudi Arabia and Qatar,2012.MMWR Morb Mortal Wkly Rep2012; 61:820.
  • BerminghamA,ChandMA,BrownCSet al.Severe respiratory illness caused by a novel coronavirus, in a patient transferred to the United Kingdom from the Middle East, September 2012.Euro Surveill2012; 17:20290.
  • MaillesA,BlanckaertK,ChaudPet al.First cases of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infections in France, investigations and implications for the prevention of human-to-human transmission, France, May 2013.Euro Surveill2013; 18:20502.
  • PuzelliS,AzziA,SantiniMGet al.Investigation of an imported case of Middle East Respiratory Syndrome Coronavirus (MERS-CoV) infection in Florence, Italy, May to June 2013.Euro Surveill2013; 18:20564.
  • TsiodrasS,BakaA,MentisAet al.A case of imported Middle East Respiratory Syndrome coronavirus infection and public health response, Greece, April 2014.Euro Surveill2014; 19:20782.
  • BialekSR,AllenD,Alvarado-RamyFet al.First confirmed cases of Middle East respiratory syndrome coronavirus (MERS-CoV) infection in the United States, updated information on the epidemiology of MERS-CoV infection, and guidance for the public, clinicians, and public health authorities - May 2014.MMWR2014; 63:431–436.
  • ChanJF,LauSK,ToKK,ChengVC,WooPC,YuenKY.Middle East respiratory syndrome coronavirus: another zoonotic betacoronavirus causing SARS-like disease.Clin Microbiol Rev2015; 28:465–522.
  • HuiDS,PerlmanS,ZumlaA.Spread of MERS to South Korea and China.Lancet Respir Med2015; 3:509–510.
  • World Health Organization (WHO).Middle East respiratory syndrome coronavirus (MERS-CoV). 2015.WHO: Geneva,2015.Available athttp://www.who.int/emergencies/mers-cov/enaccessed 5 November 2015.
  • de GrootRJ,BakerSC,BaricRSet al.Middle East respiratory syndrome coronavirus (MERS-CoV): announcement of the Coronavirus Study Group.J Virol2013; 87:7790–7792.
  • LuL,LiuQ,DuL,JiangS.Middle East respiratory syndrome coronavirus (MERS-CoV): challenges in identifying its source and controlling its spread.Microbes Infect2013; 15:625–629.
  • van BoheemenS,de GraafM,LauberCet al.Genomic characterization of a newly discovered coronavirus associated with acute respiratory distress syndrome in humans.MBio2012; 3:e00473–e00512.
  • DuraiP,BatoolM,ShahM,ChoiS.Middle East respiratory syndrome coronavirus: transmission, virology and therapeutic targeting to aid in outbreak control.Exp Mol Med2015; 47:e181.
  • ZieleckiF,WeberM,EickmannMet al.Human cell tropism and innate immune system interactions of human respiratory coronavirus EMC compared to those of severe acute respiratory syndrome coronavirus.J Virol2013; 87:5300–5304.
  • ChanRW,ChanMC,AgnihothramSet al.Tropism of and innate immune responses to the novel human betacoronavirus lineage C virus in human ex vivo respiratory organ cultures.J Virol2013; 87:6604–6614.
  • LauSK,LauCC,ChanKHet al.Delayed induction of proinflammatory cytokines and suppression of innate antiviral response by the novel Middle East respiratory syndrome coronavirus: implications for pathogenesis and treatment.J Gen Virol2013; 94:2679–2690.
  • ZhouJ,ChuH,LiCet al.Active replication of Middle East respiratory syndrome coronavirus and aberrant induction of inflammatory cytokines and chemokines in human macrophages: implications for pathogenesis.J Infect Dis2014; 209:1331–1342.
  • FaureE,PoissyJ,GoffardAet al.Distinct immune response in two MERS-CoV-infected patients: can we go from bench to bedside?PLoS One2014; 9:e88716.
  • ChanJF,YaoY,YeungMLet al.Treatment With Lopinavir/Ritonavir or interferon-β1b improves outcome of MERS-CoV infection in a nonhuman primate model of common marmoset.J Infect Dis2015; 212:1904–1913.
  • AgrawalAS,GarronT,TaoXet al.Generation of a transgenic mouse model of Middle East respiratory syndrome coronavirus infection and disease.J Virol2015; 89:3659–3670.
  • YangY,ZhangL,GengHet al.The structural and accessory proteins M, ORF 4a, ORF 4b, and ORF 5 of Middle East respiratory syndrome coronavirus (MERS-CoV) are potent interferon antagonists.Protein Cell2013; 4:951–961.
  • MatthewsKL,ColemanCM,van der MeerY,SnijderEJ,FriemanMB.The ORF4b-encoded accessory proteins of Middle East respiratory syndrome coronavirus and two related bat coronaviruses localize to the nucleus and inhibit innate immune signalling.J Gen Virol2014; 95:874–882.
  • NiemeyerD,ZillingerT,MuthDet al.Middle East respiratory syndrome coronavirus accessory protein 4a is a type I interferon antagonist.J Virol2013; 87:12489–12495.
  • SiuKL,YeungML,KokKHet al.Middle east respiratory syndrome coronavirus 4a protein is a double-stranded RNA-binding protein that suppresses PACT-induced activation of RIG-I and MDA5 in the innate antiviral response.J Virol2014; 88:4866–4876.
  • YangX,ChenX,BianGet al.Proteolytic processing, deubiquitinase and interferon antagonist activities of Middle East respiratory syndrome coronavirus papain-like protease.J Gen Virol2014; 95:614–626.
  • ChuH,ZhouJ,WongBHet al.Productive replication of Middle East respiratory syndrome coronavirus in monocyte-derived dendritic cells modulates innate immune response.Virology2014; 454-455:197–205.
  • YoneyamaM,KikuchiM,NatsukawaTet al.The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses.Nat Immunol2004; 5:730–737.
  • KatoH,SatoS,YoneyamaMet al.Cell type-specific involvement of RIG-I in antiviral response.Immunity2005; 23:19–28.
  • SiuKL,KokKH,NgMHet al.Severe acute respiratory syndrome coronavirus M protein inhibits type I interferon production by impeding the formation of TRAF3·TANK·TBK1/IKKϵ complex.J Biol Chem2009; 284:16202–16209.
  • NeumanBW,KissG,KundingAHet al.A structural analysis of M protein in coronavirus assembly and morphology.J Struct Biol2011; 174:11–22.
  • SiuKL,ChanCP,KokKH,WooPCY,JinDY.Suppression of innate antiviral response by severe acute respiratory syndrome coronavirus M protein is mediated through the first transmembrane domain.Cell Mol Immunol2014; 11:141–149.
  • DoyleS,VaidyaS,O'ConnellRet al.IRF3 mediates a TLR3/TLR4-specific antiviral gene program.Immunity2002; 17:251–263.
  • GuoB,ChengG.Modulation of the interferon antiviral response by the TBK1/IKKi adapter protein TANK.J Biol Chem2007; 282:11817–11826.
  • NgMH,HoTH,KokKH,SiuKL,LiJ,JinDY.. MIP-T3 is a negative regulator of innate type I IFN response.J Immunol2011; 187:6473–6482.
  • KokKH,LuiPY,NgMH,SiuKL,AuSW,JinDY.The double-stranded RNA-binding protein PACT functions as a cellular activator of RIG-I to facilitate innate antiviral response.Cell Host Microbe2011; 9:299–309.
  • ChaudharyV,ZhangS,YuenKSet al.Suppression of type I and type III interferon signalling by NSs protein of severe fever-with-thrombocytopenia syndrome virus through inhibition of STAT1 phosphorylation and activation.J Gen Virol2015; 96:3204–3211.
  • SiuKL,ChanCP,KokKH,WooPC,JinDY.Comparative analysis of the activation of unfolded protein response by spike proteins of severe acute respiratory syndrome coronavirus and human coronavirus HKU1.Cell Biosci2014; 4:3.
  • IwamuraT,YoneyamaM,YamaguchiKet al.Induction of IRF-3/-7 kinase and NF-κB in response to double-stranded RNA and virus infection: common and unique pathways.Genes Cells2001; 6:375–388.
  • KewC,LuiPY,ChanCPet al.Suppression of PACT-induced type I interferon production by herpes simplex virus 1 Us11 protein.J Virol2013; 87:13141–13149.
  • SieversF,WilmA,DineenDet al.Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega.Mol Syst Biol2011; 7:539.
  • DeberCM,WangC,LiuLPet al.TM Finder: a prediction program for transmembrane protein segments using a combination of hydrophobicity and nonpolar phase helicity scales.Protein Sci2001; 10:212–219.
  • ThanosD,ManiatisT.Virus induction of human IFNβ gene expression requires the assembly of an enhanceosome.Cell1995; 83:1091–1100.
  • SethRB,SunL,EaCK,ChenZJ.Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3.Cell2005; 122:669–682.
  • KawaiT,TakahashiK,SatoSet al.IPS-1, an adapter triggering RIG-I- and Mda5-mediated type I interferon induction.Nat Immunol2005; 6:981–988.
  • XuLG,WangYY,HanKJ,LiLY,ZhaiZet al.VISA is an adapter protein required for virus-triggered IFN-β signaling.Mol Cell2005; 19:727–740.
  • PoeckH,BscheiderM,GrossOet al.Recognition of RNA virus by RIG-I results in activation of CARD9 and inflammasome signaling for interleukin 1β production.Nat Immunol2010; 11:63–69.
  • FitzgeraldKA,McWhirterSM,FaiaKLet al.IKKϵ and TBK1 are essential components of the IRF3 signaling pathway.Nat Immunol2003; 4:491–496.
  • McWhirterSM,FitzgeraldKA,RosainsJ,RoweDC,GolenbockDT,ManiatisT.IFN-regulatory factor 3-dependent gene expression is defective in Tbk1-deficient mouse embryonic fibroblasts.Proc Natl Acad Sci USA2004; 101:233–238.
  • SankarS,ChanH,RomanowWJ,LiJ,BatesRJ.IKK-i signals through IRF3 and NFkappaB to mediate the production of inflammatory cytokines.Cell Signal2006; 18:982–993.
  • LiuS,CaiX,WuJet al.Phosphorylation of innate immune adapter proteins MAVS, STING, and TRIF induces IRF3 activation.Science2015; 347:aaa2630.
  • LinR,HeylbroeckC,PithaPM,HiscottJ.Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation.Mol Cell Biol1998; 18:2986–2996.
  • SahaSK,PietrasEM,HeJQet al.Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif.EMBO J2006; 25:3257–3263.
  • van ZuylenWJ,DoyonP,ClémentJFet al.Proteomic profiling of the TRAF3 interactome network reveals a new role for the ER-to-Golgi transport compartments in innate immunity.PLoS Pathog2012; 8:e1002747.
  • ChenWH,DuL,ChagSMet al.Yeast-expressed recombinant protein of the receptor-binding domain in SARS-CoV spike protein with deglycosylated forms as a SARS vaccine candidate.Hum Vaccin Immunother2014; 10:648–658.
  • LuL,LiuQ,ZhuYet al.Structure-based discovery of Middle East respiratory syndrome coronavirus fusion inhibitor.Nat Commun2014; 5:3067.
  • YingT,LiH,LuL,DimitrovDS,JiangS.Development of human neutralizing monoclonal antibodies for prevention and therapy of MERS-CoV infections.Microbes Infect2015; 17:142–148.
  • ToturaAL,BaricRS.SARS coronavirus pathogenesis: host innate immune responses and viral antagonism of interferon.Curr Opin Virol2012; 2:264–275.
  • KindlerE,ThielV.To sense or not to sense viral RNA—essentials of coronavirus innate immune evasion.Curr Opin Microbiol2014; 20:69–75.
  • WongLYR,LuiPY,JinDY.A molecular arms race between host innate antiviral response and emerging human coronaviruses.Virol Sin2016; 31:12–23.
  • YangY,YeF,ZhuNet al.Middle East respiratory syndrome coronavirus ORF4b protein inhibits type I interferon production through both cytoplasmic and nuclear targets.Sci Rep2015; 5:17554.