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Original Articles

Enterovirus 71 induces dsRNA/PKR-dependent cytoplasmic redistribution of GRP78/BiP to promote viral replication

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Pages 1-12 | Received 07 Sep 2015, Accepted 23 Nov 2015, Published online: 25 Jan 2019

References

  • RacanielloVR.Picornaviridae: The viruses and their replication. In: David M, Knipe PMH, Malcolm A Martin, Diane E Griffin, Robert A Lamb, Bernard Roizman, Stephen E Straus(eds).Fields Virology,5th ednvol. 1.Lippincott Williams & Wilkins: Philadelphia.2007,795–838.
  • SolomonT,LewthwaiteP,PereraDet al.Virology, epidemiology, pathogenesis, and control of enterovirus 71.Lancet Infect Dis2010; 10:778–790.
  • FengQ,HatoSV,LangereisMAet al.MDA5 detects the double-stranded RNA replicative form in picornavirus-infected cells.Cell Rep2012; 2:1187–1196.
  • NanduriS,CarpickBW,YangYet al.Structure of the double-stranded RNA-binding domain of the protein kinase PKR reveals the molecular basis of its dsRNA-mediated activation.EMBO J1998; 17:5458–5465.
  • LiuL,WiseDR,DiehlJAet al.Hypoxic reactive oxygen species regulate the integrated stress response and cell survival.J Biol Chem2008; 283:31153–31162.
  • KozutsumiY,NormingtonK,PressEet al.Identification of immunoglobulin heavy chain binding protein as glucose-regulated protein 78 on the basis of amino acid sequence, immunological cross-reactivity, and functional activity.J Cell Sci Suppl1989; 11:115–137.
  • FlahertyKM,DeLuca-FlahertyC,McKayDB.Three-dimensional structure of the ATPase fragment of a 70 K heat-shock cognate protein.Nature1990; 346:623–628.
  • ZhuX,ZhaoX,BurkholderWFet al.Structural analysis of substrate binding by the molecular chaperone DnaK.Science1996; 272:1606–1614.
  • WangH,KurochkinAV,PangYet al.NMR solution structure of the 21 kDa chaperone protein DnaK substrate binding domain: a preview of chaperone-protein interaction.Biochemistry1998; 37:7929–7940.
  • FreemanBC,MyersMP,SchumacherRet al.Identification of a regulatory motif in Hsp70 that affects ATPase activity, substrate binding and interaction with HDJ-1.EMBO J1995; 14:2281–2292.
  • NiM,ZhangY,LeeAS.Beyond the endoplasmic reticulum: atypical GRP78 in cell viability, signalling and therapeutic targeting.Biochem J2011; 434:181–188.
  • ZhangY,TsengCC,TsaiYLet al.Cancer cells resistant to therapy promote cell surface relocalization of GRP78 which complexes with PI3K and enhances PI(3,4,5)P3 production.PLoS One2013; 8:e80071.
  • MisraUK,Gonzalez-GronowM,GawdiGet al.A novel receptor function for the heat shock protein Grp78: silencing of Grp78 gene expression attenuates alpha2M*-induced signalling.Cell Signal2004; 16:929–938.
  • NiM,ZhouH,WeySet al.Regulation of PERK signaling and leukemic cell survival by a novel cytosolic isoform of the UPR regulator GRP78/BiP.PLoS One2009; 4:e6868.
  • JindadamrongwechS,ThepparitC,SmithDR.Identification of GRP 78 (BiP) as a liver cell expressed receptor element for dengue virus serotype 2.Arch Virol2004; 149:915–927.
  • DuriezM,RossignolJM,SitterlinD.The hepatitis B virus precore protein is retrotransported from endoplasmic reticulum (ER) to cytosol through the ER-associated degradation pathway.J Biol Chem2008; 283:32352–32360.
  • LeeAS.The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress.Methods2005; 35:373–381.
  • JhengJR,HoJY,HorngJT.ER stress, autophagy, and RNA viruses.Front Microbiol2014; 5:388.
  • ChanSW.Unfolded protein response in hepatitis C virus infection.Front Microbiol2014; 5:233.
  • KePY,ChenSS.Activation of the unfolded protein response and autophagy after hepatitis C virus infection suppresses innate antiviral immunity in vitro.J Clin Invest2011; 121:37–56.
  • PenaJ,HarrisE.Dengue virus modulates the unfolded protein response in a time-dependent manner.J Biol Chem2011; 286:14226–14236.
  • SuHL,LiaoCL,LinYL.Japanese encephalitis virus infection initiates endoplasmic reticulum stress and an unfolded protein response.J Virol2002; 76:4162–4171.
  • JhengJR,LauKS,TangWFet al.Endoplasmic reticulum stress is induced and modulated by enterovirus 71.Cell Microbiol2010; 12:796–813.
  • ChangCW,LeuYL,HorngJT.Daphne Genkwa sieb. Et zucc. Water-soluble extracts act on enterovirus 71 by inhibiting viral entry.Viruses2012; 4:539–556.
  • WongWR,ChenYY,YangSMet al.Phosphorylation of PI3K/Akt and MAPK/ERK in an early entry step of enterovirus 71.Life Sci2005; 78:82–90.
  • TangWF,YangSY,WuBWet al.Reticulon 3 binds the 2C protein of enterovirus 71 and is required for viral replication.J Biol Chem2007; 282:5888–5898.
  • YamayoshiS,YamashitaY,LiJet al.Scavenger receptor B2 is a cellular receptor for enterovirus 71.Nat Med2009; 15:798–801.
  • JhengJR,LinCY,HorngJTet al.Inhibition of enterovirus 71 entry by transcription factor XBP1.Biochem Biophys Res Commun2012; 420:882–887.
  • WangP,LiB,ZhouLet al.The KDEL receptor induces autophagy to promote the clearance of neurodegenerative disease-related proteins.Neuroscience2011; 190:43–55.
  • WuYP,ChangCM,HungCYet al.Japanese encephalitis virus co-opts the ER-stress response protein GRP78 for viral infectivity.Virol J2011; 8:128.
  • MunroS,PelhamHR.A C-terminal signal prevents secretion of luminal ER proteins.Cell1987; 48:899–907.
  • CancinoJ,CapalboA,Di CampliAet al.Control systems of membrane transport at the interface between the endoplasmic reticulum and the Golgi.Dev Cell2014; 30:280–294.
  • AlexopoulouL,HoltAC,MedzhitovRet al.Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3.Nature2001; 413:732–738.
  • LemairePA,AndersonE,LaryJet al.Mechanism of PKR Activation by dsRNA.J Mol Biol2008; 381:351–360.
  • PengH,ShiM,ZhangLet al.Activation of JNK1/2 and p38 MAPK signaling pathways promotes enterovirus 71 infection in immature dendritic cells.BMC Microbiol2014; 14:147.
  • PetersKL,SmithHL,StarkGRet al.IRF-3-dependent, NFkappa B- and JNK-independent activation of the 561 and IFN-beta genes in response to double-stranded RNA.Proc Natl Acad Sci USA2002; 99:6322–6327.
  • GilJ,EstebanM.Induction of apoptosis by the dsRNA-dependent protein kinase (PKR): mechanism of action.Apoptosis2000; 5:107–114.
  • WangX,OlberdingKE,WhiteCet al.Bcl-2 proteins regulate ER membrane permeability to luminal proteins during ER stress-induced apoptosis.Cell Death Differ2011; 18:38–47.
  • ZongWX,LiC,HatzivassiliouGet al.Bax and Bak can localize to the endoplasmic reticulum to initiate apoptosis.J Cell Biol2003; 162:59–69.
  • TraheyM,OhHS,CameronCE,HayJC.Poliovirus infection transiently increases COPII vesicle budding.J Virol2012; 86:9675–9682.
  • SchlegelA,GiddingsTHJr,LadinskyMSet al.Cellular origin and ultrastructure of membranes induced during poliovirus infection.J Virol1996; 70:6576–6588.
  • van KuppeveldFJ,HoenderopJG,SmeetsRLet al.Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release.EMBO J1997; 16:3519–3532.
  • ChenYH,DuW,HagemeijerMCet al.Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses.Cell2015; 160:619–630.
  • BirdSW,MaynardND,CovertMWet al.Nonlytic viral spread enhanced by autophagy components.Proc Natl Acad Sci USA2014; 111:13081–13086.
  • LiWW,AlexandreS,CaoXet al.Transactivation of the grp78 promoter by Ca2+ depletion. A comparative analysis with A23187 and the endoplasmic reticulum Ca(2+)-ATPase inhibitor thapsigargin.J Biol Chem1993; 268:12003–12009.
  • LuoS,BaumeisterP,YangSet al.Induction of Grp78/BiP by translational block: activation of the Grp78 promoter by ATF4 through and upstream ATF/CRE site independent of the endoplasmic reticulum stress elements.J Biol Chem2003; 278:37375–37385.
  • MacejakDG,SarnowP.Internal initiation of translation mediated by the 5' leader of a cellular mRNA.Nature1991; 353:90–94.
  • DaiRY,ChenSK,YanDMet al.PI3K/Akt promotes GRP78 accumulation and inhibits endoplasmic reticulum stress-induced apoptosis in HEK293 cells.Folia Biol (Praha)2010; 56:37–46.
  • OuyangYB,LuY,YueSet al.miR-181 regulates GRP78 and influences outcome from cerebral ischemia in vitro and in vivo.Neurobiol Dis2012; 45:555–563.
  • BuchkovichNJ,YuY,PiercieyFJJret al.Human cytomegalovirus induces the endoplasmic reticulum chaperone BiP through increased transcription and activation of translation by using the BiP internal ribosome entry site.J Virol2010; 84:11479–11486.
  • LibermanE,FongYL,SelbyMJet al.Activation of the grp78 and grp94 promoters by hepatitis C virus E2 envelope protein.J Virol1999; 73:3718–3722.
  • PriceNT,WelshGI,ProudCG.Phosphorylation of only serine-51 in protein synthesis initiation factor-2 is associated with inhibition of peptide-chain initiation in reticulocyte lysates.Biochem Biophys Res Commun1991; 176:993–999.
  • PestovaTV,de BreyneS,PisarevAVet al.eIF2-dependent and eIF2-independent modes of initiation on the CSFV IRES: a common role of domain II.EMBO J2008; 27:1060–1072.
  • GerlitzG,JagusR,Elroy-SteinO.Phosphorylation of initiation factor-2 alpha is required for activation of internal translation initiation during cell differentiation.Eur J Biochem2002; 269:2810–2819.
  • SarnowP.Translation of glucose-regulated protein 78/immunoglobulin heavy-chain binding protein mRNA is increased in poliovirus-infected cells at a time when cap-dependent translation of cellular mRNAs is inhibited.Proc Natl Acad Sci USA1989; 86:5795–5799.
  • RaoRV,PeelA,LogvinovaAet al.Coupling endoplasmic reticulum stress to the cell death program: role of the ER chaperone GRP78.FEBS Lett2002; 514:122–128.
  • CallusBA,VauxDL.Caspase inhibitors: viral, cellular and chemical.Cell Death Differ2007; 14:73–78.
  • UrbanowskiMD,HobmanTC.The West Nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism.J Virol2013; 87:872–881.