The Intrinsically Disordered W Protein Is Multifunctional during Henipavirus Infection, Disrupting Host Signalling Pathways and Nuclear Import
Abstract
1. Introduction
2. Virion Organisation
3. The Henipavirus Replication Cycle within the Host Cell
4. Innate Immune Antagonism and Virus Pathogenesis
5. W Protein Is Intrinsically Disordered and Binds Multiple Host Proteins Involved in the Suppression of Innate Immunity
5.1. W Binds Impα3 and Impα4 for Nuclear Import
5.2. W Protein Inhibits Type I IFN Response
5.3. W Protein Binds Host STAT to Create High Molecular Weight Complexes that Inhibit Type I IFN Signalling
5.4. W Binds Host 14-3-3 Proteins to Modulate Diverse Host Signalling Pathways
6. Conclusions
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Rima, B.; Balkema-Buschmann, A.; Dundon, W.G.; Duprex, P.; Easton, A.; Fouchier, R.; Kurath, G.; Lamb, R.; Lee, B.; Rota, P.; et al. ICTV Virus Taxonomy Profile: Paramyxoviridae. J. Gen. Virol. 2019, 100, 1593–1594. [Google Scholar] [CrossRef]
- Schneider, W.M.; Chevillotte, M.D.; Rice, C.M. Interferon-stimulated genes: A complex web of host defenses. Annu. Rev. Immunol. 2014, 32, 513–545. [Google Scholar] [CrossRef] [PubMed]
- Murray, K.; Selleck, P.; Hooper, P.; Hyatt, A.; Gould, A.; Gleeson, L.; Westbury, H.; Hiley, L.; Selvey, L.; Rodwell, B.; et al. A morbillivirus that caused fatal disease in horses and humans. Science 1995, 268, 94–97. [Google Scholar] [CrossRef] [PubMed]
- Field, H.E. Hendra virus ecology and transmission. Curr. Opin. Virol. 2016, 16, 120–125. [Google Scholar] [CrossRef] [PubMed]
- Ang, B.S.P.; Lim, T.C.C.; Wang, L. Nipah Virus Infection. J. Clin. Microbiol. 2018, 56, e01875. [Google Scholar] [CrossRef] [PubMed]
- Luby, S.P.; Hossain, M.J.; Gurley, E.S.; Ahmed, B.N.; Banu, S.; Khan, S.U.; Homaira, N.; Rota, P.A.; Rollin, P.E.; Comer, J.A.; et al. Recurrent zoonotic transmission of Nipah virus into humans, Bangladesh, 2001–2007. Emerg. Infect. Dis. 2009, 15, 1229–1235. [Google Scholar] [CrossRef]
- Goldsmith, C.S.; Whistler, T.; Rollin, P.E.; Ksiazek, T.G.; Rota, P.A.; Bellini, W.J.; Daszak, P.; Wong, K.T.; Shieh, W.J.; Zaki, S.R. Elucidation of Nipah virus morphogenesis and replication using ultrastructural and molecular approaches. Virus Res. 2003, 92, 89–98. [Google Scholar] [CrossRef]
- Patch, J.R.; Crameri, G.; Wang, L.-F.; Eaton, B.T.; Broder, C.C. Quantitative analysis of Nipah virus proteins released as virus-like particles reveals central role for the matrix protein. Virol. J. 2007, 4, 1. [Google Scholar] [CrossRef]
- Wang, L.F.; Yu, M.; Hansson, E.; Pritchard, L.I.; Shiell, B.; Michalski, W.P.; Eaton, B.T. The exceptionally large genome of Hendra virus: Support for creation of a new genus within the family Paramyxoviridae. J. Virol. 2000, 74, 9972–9979. [Google Scholar] [CrossRef]
- Enchéry, F.; Horvat, B. Understanding the Interaction between Henipaviruses and Their Natural Host, Fruit Bats: Paving the Way Toward Control of Highly Lethal Infection in Humans. Int. Rev. Immunol. 2017, 36, 1–14. [Google Scholar] [CrossRef]
- Hausmann, S.; Garcin, D.; Delenda, C.; Kolakofsky, D. The versatility of paramyxovirus RNA polymerase stuttering. J. Virol. 1999, 73, 5568–5576. [Google Scholar] [CrossRef] [PubMed]
- Lo, M.K.; Harcourt, B.H.; Mungall, B.A.; Tamin, A.; Peeples, M.E.; Bellini, W.J.; Rota, P.A. Determination of the henipavirus phosphoprotein gene mRNA editing frequencies and detection of the C, V and W proteins of Nipah virus in virus-infected cells. J. Gen. Virol. 2009, 90, 398–404. [Google Scholar] [CrossRef] [PubMed]
- Battisti, A.J.; Meng, G.; Winkler, D.C.; McGinnes, L.W.; Plevka, P.; Steven, A.C.; Morrison, T.G.; Rossmann, M.G. Structure and assembly of a paramyxovirus matrix protein. Proc. Natl. Acad. Sci. USA 2012, 109, 13996–14000. [Google Scholar] [CrossRef] [PubMed]
- Singh, M.; Berger, B.; Kim, P.S. LearnCoil-VMF: Computational evidence for coiled-coil-like motifs in many viral membrane-fusion proteins. J. Mol. Biol. 1999, 290, 1031–1041. [Google Scholar] [CrossRef] [PubMed]
- Langedijk, J.P.; Daus, F.J.; van Oirschot, J.T. Sequence and structure alignment of Paramyxoviridae attachment proteins and discovery of enzymatic activity for a morbillivirus hemagglutinin. J. Virol. 1997, 71, 6155–6167. [Google Scholar] [CrossRef] [PubMed]
- Crennell, S.; Takimoto, T.; Portner, A.; Taylor, G. Crystal structure of the multifunctional paramyxovirus hemagglutinin-neuraminidase. Nat. Struct. Biol. 2000, 7, 1068–1074. [Google Scholar] [PubMed]
- Negrete, O.A.; Levroney, E.L.; Aguilar, H.C.; Bertolotti-Ciarlet, A.; Nazarian, R.; Tajyar, S.; Lee, B. EphrinB2 is the entry receptor for Nipah virus, an emergent deadly paramyxovirus. Nature 2005, 436, 401–405. [Google Scholar] [CrossRef] [PubMed]
- Aguilar, H.C.; Iorio, R.M. Henipavirus membrane fusion and viral entry. Curr. Top. Microbiol. Immunol. 2012, 359, 79–94. [Google Scholar]
- Pernet, O.; Wang, Y.E.; Lee, B. Henipavirus receptor usage and tropism. Curr. Top. Microbiol. Immunol. 2012, 359, 59–78. [Google Scholar]
- Pentecost, M.; Vashisht, A.A.; Lester, T.; Voros, T.; Beaty, S.M.; Park, A.; Wang, Y.E.; Yun, T.E.; Freiberg, A.N.; Wohlschlegel, J.A.; et al. Evidence for Ubiquitin-Regulated Nuclear and Subnuclear Trafficking among Paramyxovirinae Matrix Proteins. PLoS Pathog. 2015, 11, e1004739. [Google Scholar] [CrossRef]
- Wang, Y.E.; Park, A.; Lake, M.; Pentecost, M.; Torres, B.; Yun, T.E.; Wolf, M.C.; Holbrook, M.R.; Freiberg, A.N.; Lee, B. Ubiquitin-regulated nuclear-cytoplasmic trafficking of the Nipah virus matrix protein is important for viral budding. PLoS Pathog. 2010, 6, e1001186. [Google Scholar] [CrossRef]
- Waning, D.L.; Schmitt, A.P.; Leser, G.P.; Lamb, R.A. Roles for the cytoplasmic tails of the fusion and hemagglutinin-neuraminidase proteins in budding of the paramyxovirus simian virus 5. J. Virol. 2002, 76, 9284–9297. [Google Scholar] [CrossRef]
- Pantua, H.D.; McGinnes, L.W.; Peeples, M.E.; Morrison, T.G. Requirements for the assembly and release of Newcastle disease virus-like particles. J. Virol. 2006, 80, 11062–11073. [Google Scholar] [CrossRef]
- Harrison, M.S.; Sakaguchi, T.; Schmitt, A.P. Paramyxovirus assembly and budding: Building particles that transmit infections. Int. J. Biochem. Cell Biol. 2010, 42, 1416–1429. [Google Scholar] [CrossRef]
- Ghildyal, R.; Mills, J.; Murray, M.; Vardaxis, N.; Meanger, J. Respiratory syncytial virus matrix protein associates with nucleocapsids in infected cells. J. Gen. Virol. 2002, 83, 753–757. [Google Scholar] [CrossRef]
- Goh, K.J.; Tan, C.T.; Chew, N.K.; Tan, P.S.; Kamarulzaman, A.; Sarji, S.A.; Wong, K.T.; Abdullah, B.J.; Chua, K.B.; Lam, S.K. Clinical features of Nipah virus encephalitis among pig farmers in Malaysia. N. Engl. J. Med. 2000, 342, 1229–1235. [Google Scholar] [CrossRef] [PubMed]
- Wong, K.T.; Shieh, W.J.; Kumar, S.; Norain, K.; Abdullah, W.; Guarner, J.; Goldsmith, C.S.; Chua, K.B.; Lam, S.K.; Tan, C.T.; et al. Nipah virus infection: Pathology and pathogenesis of an emerging paramyxoviral zoonosis. Am. J. Pathol. 2002, 161, 2153–2167. [Google Scholar] [CrossRef]
- Satterfield, B.A.; Cross, R.W.; Fenton, K.A.; Agans, K.N.; Basler, C.F.; Geisbert, T.W.; Mire, C.E. The immunomodulating V and W proteins of Nipah virus determine disease course. Nat. Commun. 2015, 6, 7483. [Google Scholar] [CrossRef] [PubMed]
- Shaw, M.L.; Cardenas, W.B.; Zamarin, D.; Palese, P.; Basler, C.F. Nuclear localization of the Nipah virus W protein allows for inhibition of both virus- and toll-like receptor 3-triggered signaling pathways. J. Virol. 2005, 79, 6078–6088. [Google Scholar] [CrossRef]
- Satterfield, B.A.; Cross, R.W.; Fenton, K.A.; Borisevich, V.; Agans, K.N.; Deer, D.J.; Graber, J.; Basler, C.F.; Geisbert, T.W.; Mire, C.E. Nipah Virus C and W Proteins Contribute to Respiratory Disease in Ferrets. J. Virol. 2016, 90, 6326–6343. [Google Scholar] [CrossRef]
- Kolakofsky, D.; Roux, L.; Garcin, D.; Ruigrok, R.W.H. Paramyxovirus mRNA editing, the “rule of six” and error catastrophe: A hypothesis. J. Gen. Virol. 2005, 86, 1869–1877. [Google Scholar] [CrossRef]
- Curran, J.; Kolakofsky, D. Sendai virus P gene produces multiple proteins from overlapping open reading frames. Enzyme 1990, 44, 244–249. [Google Scholar] [CrossRef]
- Karlin, D.; Longhi, S.; Receveur, V.; Canard, B. The N-terminal domain of the phosphoprotein of Morbilliviruses belongs to the natively unfolded class of proteins. Virology 2002, 296, 251–262. [Google Scholar] [CrossRef]
- Curran, J.; Boeck, R.; Lin-Marq, N.; Lupas, A.; Kolakofsky, D. Paramyxovirus phosphoproteins form homotrimers as determined by an epitope dilution assay, via predicted coiled coils. Virology 1995, 214, 139–149. [Google Scholar] [CrossRef]
- Jensen, M.R.; Yabukarski, F.; Communie, G.; Condamine, E.; Mas, C.; Volchkova, V.; Tarbouriech, N.; Bourhis, J.M.; Volchkov, V.; Blackledge, M.; et al. Structural Description of the Nipah Virus Phosphoprotein and Its Interaction with STAT1. Biophys. J. 2020. [Google Scholar] [CrossRef]
- Karlin, D.; Belshaw, R. Detecting remote sequence homology in disordered proteins: Discovery of conserved motifs in the N-termini of Mononegavirales phosphoproteins. PLoS ONE 2012, 7, e31719. [Google Scholar] [CrossRef] [PubMed]
- Edwards, M.R.; Hoad, M.; Tsimbalyuk, S.; Menicucci, A.R.; Messaoudi, I.; Forwood, J.K.; Basler, C.F. Henipavirus W proteins interact with 14-3-3 to modulate host gene expression. J. Virol. 2020. [Google Scholar] [CrossRef]
- Parisien, J.P.; Lau, J.F.; Rodriguez, J.J.; Ulane, C.M.; Horvath, C.M. Selective STAT protein degradation induced by paramyxoviruses requires both STAT1 and STAT2 but is independent of alpha/beta interferon signal transduction. J. Virol. 2002, 76, 4190–4198. [Google Scholar] [CrossRef] [PubMed]
- Shaw, M.L.; García-Sastre, A.; Palese, P.; Basler, C.F. Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J. Virol. 2004, 78, 5633–5641. [Google Scholar] [CrossRef]
- Erdős, G.; Dosztányi, Z. Analyzing Protein Disorder with IUPred2A. Curr. Protoc. Bioinform. 2020, 70, e99. [Google Scholar] [CrossRef] [PubMed]
- Lo, M.K.; Miller, D.; Aljofan, M.; Mungall, B.A.; Rollin, P.E.; Bellini, W.J.; Rota, P.A. Characterization of the antiviral and inflammatory responses against Nipah virus in endothelial cells and neurons. Virology 2010, 404, 78–88. [Google Scholar] [CrossRef] [PubMed]
- Martinez-Gil, L.; Vera-Velasco, N.M.; Mingarro, I. Exploring the Human-Nipah Virus Protein-Protein Interactome. J. Virol. 2017, 91, e01461. [Google Scholar] [CrossRef] [PubMed]
- Lange, A.; Mills, R.E.; Lange, C.J.; Stewart, M.; Devine, S.E.; Corbett, A.H. Classical nuclear localization signals: Definition, function, and interaction with importin alpha. J. Biol. Chem. 2007, 282, 5101–5105. [Google Scholar] [CrossRef]
- Stewart, M. Molecular mechanism of the nuclear protein import cycle. Nat. Rev. Mol. Cell Biol. 2007, 8, 195–208. [Google Scholar] [CrossRef]
- Goldfarb, D.S.; Corbett, A.H.; Mason, D.A.; Harreman, M.T.; Adam, S.A. Importin alpha: A multipurpose nuclear-transport receptor. Trends Cell Biol. 2004, 14, 505–514. [Google Scholar] [CrossRef]
- Garcia-Sastre, A. Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes Infect. 2002, 4, 647–655. [Google Scholar] [CrossRef]
- Smith, K.M.; Tsimbalyuk, S.; Edwards, M.R.; Cross, E.M.; Batra, J.; Soares da Costa, T.P.; Aragao, D.; Basler, C.F.; Forwood, J.K. Structural basis for importin alpha 3 specificity of W proteins in Hendra and Nipah viruses. Nat. Commun. 2018, 9, 3703. [Google Scholar] [CrossRef]
- Kumar, K.P.; McBride, K.M.; Weaver, B.K.; Dingwall, C.; Reich, N.C. Regulated nuclear-cytoplasmic localization of interferon regulatory factor 3, a subunit of double-stranded RNA-activated factor 1. Mol. Cell Biol. 2000, 20, 4159–4168. [Google Scholar] [CrossRef]
- Zhu, M.; Fang, T.; Li, S.; Meng, K.; Guo, D. Bipartite Nuclear Localization Signal Controls Nuclear Import and DNA-Binding Activity of IFN Regulatory Factor 3. J. Immunol. 2015, 195, 289–297. [Google Scholar] [CrossRef]
- Seth, R.B.; Sun, L.; Chen, Z.J. Antiviral innate immunity pathways. Cell Res. 2006, 16, 141–147. [Google Scholar] [CrossRef] [PubMed]
- Braciale, T.J.; Hahn, Y.S. Immunity to viruses. Immunol. Rev. 2013, 255, 5–12. [Google Scholar] [CrossRef] [PubMed]
- Ivashkiv, L.B.; Donlin, L.T. Regulation of type I interferon responses. Nat. Rev. Immunol. 2014, 14, 36–49. [Google Scholar] [CrossRef] [PubMed]
- Gay, N.J.; Symmons, M.F.; Gangloff, M.; Bryant, C.E. Assembly and localization of Toll-like receptor signalling complexes. Nat. Rev. Immunol. 2014, 14, 546–558. [Google Scholar] [CrossRef] [PubMed]
- Chiang, H.S.; Liu, H.M. The Molecular Basis of Viral Inhibition of IRF- and STAT-Dependent Immune Responses. Front. Immunol. 2018, 9, 3086. [Google Scholar] [CrossRef] [PubMed]
- Liao, Y.; Goraya, M.U.; Yuan, X.; Zhang, B.; Chiu, S.H.; Chen, J.L. Functional Involvement of Interferon-Inducible Transmembrane Proteins in Antiviral Immunity. Front. Microbiol. 2019, 10, 1097. [Google Scholar] [CrossRef] [PubMed]
- Basler, C.F.; Garcia-Sastre, A. Viruses and the type I interferon antiviral system: Induction and evasion. Int. Rev. Immunol. 2002, 21, 305–337. [Google Scholar] [CrossRef] [PubMed]
- Basler, C.F.; Mikulasova, A.; Martinez-Sobrido, L.; Paragas, J.; Mühlberger, E.; Bray, M.; Klenk, H.D.; Palese, P.; García-Sastre, A. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 2003, 77, 7945–7956. [Google Scholar] [CrossRef]
- Ronco, L.V.; Karpova, A.Y.; Vidal, M.; Howley, P.M. Human papillomavirus 16 E6 oncoprotein binds to interferon regulatory factor-3 and inhibits its transcriptional activity. Genes Dev. 1998, 12, 2061–2072. [Google Scholar] [CrossRef]
- Lin, R.; Genin, P.; Mamane, Y.; Sgarbanti, M.; Battistini, A.; Harrington, W.J., Jr.; Barber, G.N.; Hiscott, J. HHV-8 encoded vIRF-1 represses the interferon antiviral response by blocking IRF-3 recruitment of the CBP/p300 coactivators. Oncogene 2001, 20, 800–811. [Google Scholar] [CrossRef]
- Talon, J.; Horvath, C.M.; Polley, R.; Basler, C.F.; Muster, T.; Palese, P.; García-Sastre, A. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 2000, 74, 7989–7996. [Google Scholar] [CrossRef]
- Xiang, Y.; Condit, R.C.; Vijaysri, S.; Jacobs, B.; Williams, B.R.; Silverman, R.H. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J. Virol. 2002, 76, 5251–5259. [Google Scholar] [CrossRef] [PubMed]
- Jacobs, B.L.; Langland, J.O. When two strands are better than one: The mediators and modulators of the cellular responses to double-stranded RNA. Virology 1996, 219, 339–349. [Google Scholar] [CrossRef] [PubMed]
- Akira, S.; Takeda, K. Toll-like receptor signalling. Nat. Rev. Immunol. 2004, 4, 499–511. [Google Scholar] [CrossRef] [PubMed]
- Hoffmann, J.A. The immune response of Drosophila. Nature 2003, 426, 33–38. [Google Scholar] [CrossRef] [PubMed]
- Alexopoulou, L.; Holt, A.C.; Medzhitov, R.; Flavell, R.A. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413, 732–738. [Google Scholar] [CrossRef] [PubMed]
- Maes, T.; Mascaró, C.; Tirapu, I.; Estiarte, A.; Ciceri, F.; Lunardi, S.; Guibourt, N.; Perdones, A.; Lufino, M.M.P.; Somervaille, T.C.P.; et al. ORY-1001, a Potent and Selective Covalent KDM1A Inhibitor, for the Treatment of Acute Leukemia. Cancer Cell 2018, 33, 495–511. [Google Scholar] [CrossRef]
- Fitzgerald, K.A.; McWhirter, S.M.; Faia, K.L.; Rowe, D.C.; Latz, E.; Golenbock, D.T.; Coyle, A.J.; Liao, S.M.; Maniatis, T. IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat. Immunol. 2003, 4, 491–496. [Google Scholar] [CrossRef]
- Sharma, S.; tenOever, B.R.; Grandvaux, N.; Zhou, G.P.; Lin, R.; Hiscott, J. Triggering the interferon antiviral response through an IKK-related pathway. Science 2003, 300, 1148–1151. [Google Scholar] [CrossRef]
- Lin, R.; Heylbroeck, C.; Pitha, P.M.; Hiscott, J. Virus-dependent phosphorylation of the IRF-3 transcription factor regulates nuclear translocation, transactivation potential, and proteasome-mediated degradation. Mol. Cell Biol. 1998, 18, 2986–2996. [Google Scholar] [CrossRef]
- Yoneyama, M.; Suhara, W.; Fukuhara, Y.; Fukuda, M.; Nishida, E.; Fujita, T. Direct triggering of the type I interferon system by virus infection: Activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J. 1998, 17, 1087–1095. [Google Scholar] [CrossRef]
- Grandvaux, N.; Servant, M.J.; tenOever, B.; Sen, G.C.; Balachandran, S.; Barber, G.N.; Lin, R.; Hiscott, J. Transcriptional profiling of interferon regulatory factor 3 target genes: Direct involvement in the regulation of interferon-stimulated genes. J. Virol. 2002, 76, 5532–5539. [Google Scholar] [CrossRef] [PubMed]
- Peters, K.L.; Smith, H.L.; Stark, G.R.; Sen, G.C. 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. USA 2002, 99, 6322–6327. [Google Scholar] [CrossRef] [PubMed]
- Sato, M.; Suemori, H.; Hata, N.; Asagiri, M.; Ogasawara, K.; Nakao, K.; Nakaya, T.; Katsuki, M.; Noguchi, S.; Tanaka, N.; et al. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 2000, 13, 539–548. [Google Scholar] [CrossRef]
- Iampietro, M.; Aurine, N.; Dhondt, K.P.; Dumont, C.; Pelissier, R.; Spanier, J.; Vallve, A.; Raoul, H.; Kalinke, U.; Horvat, B. Control of Nipah Virus Infection in Mice by the Host Adaptors Mitochondrial Antiviral Signaling Protein (MAVS) and Myeloid Differentiation Primary Response 88 (MyD88). J. Infect. Dis. 2020, 221, S401–S406. [Google Scholar] [CrossRef]
- He, B.; Paterson, R.G.; Stock, N.; Durbin, J.E.; Durbin, R.K.; Goodbourn, S.; Randall, R.E.; Lamb, R.A. Recovery of paramyxovirus simian virus 5 with a V protein lacking the conserved cysteine-rich domain: The multifunctional V protein blocks both interferon-beta induction and interferon signaling. Virology 2002, 303, 15–32. [Google Scholar] [CrossRef]
- Poole, E.; He, B.; Lamb, R.A.; Randall, R.E.; Goodbourn, S. The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 2002, 303, 33–46. [Google Scholar] [CrossRef]
- Komatsu, T.; Takeuchi, K.; Yokoo, J.; Gotoh, B. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-beta production. Virology 2004, 325, 137–148. [Google Scholar] [CrossRef]
- Kumthip, K.; Chusri, P.; Jilg, N.; Zhao, L.; Fusco, D.N.; Zhao, H.; Goto, K.; Cheng, D.; Schaefer, E.A.; Zhang, L.; et al. Hepatitis C virus NS5A disrupts STAT1 phosphorylation and suppresses type I interferon signaling. J. Virol. 2012, 86, 8581–8591. [Google Scholar] [CrossRef]
- Sen, A.; Rott, L.; Phan, N.; Mukherjee, G.; Greenberg, H.B. Rotavirus NSP1 Protein Inhibits Interferon-Mediated STAT1 Activation. J. Virol. 2014, 88, 41. [Google Scholar] [CrossRef]
- Valmas, C.; Grosch, M.N.; Schümann, M.; Olejnik, J.; Martinez, O.; Best, S.M.; Krähling, V.; Basler, C.F.; Mühlberger, E. Marburg virus evades interferon responses by a mechanism distinct from ebola virus. PLoS Pathog. 2010, 6, e1000721. [Google Scholar] [CrossRef]
- Didcock, L.; Young, D.F.; Goodbourn, S.; Randall, R.E. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 1999, 73, 9928–9933. [Google Scholar] [CrossRef] [PubMed]
- Parisien, J.-P.; Lau, J.F.; Rodriguez, J.J.; Sullivan, B.M.; Moscona, A.; Parks, G.D.; Lamb, R.A.; Horvath, C.M. The V Protein of Human Parainfluenza Virus 2 Antagonizes Type I Interferon Responses by Destabilizing Signal Transducer and Activator of Transcription 2. Virology 2001, 283, 230–239. [Google Scholar] [CrossRef] [PubMed]
- Kubota, T.; Yokosawa, N.; Yokota, S.-I.; Fujii, N. C Terminal CYS-RICH Region of Mumps Virus Structural V Protein Correlates with Block of Interferon α and γ Signal Transduction Pathway through Decrease of STAT 1-α. Biochem. Biophys. Res. Commun. 2001, 283, 255–259. [Google Scholar] [CrossRef] [PubMed]
- Rodriguez, J.J.; Parisien, J.-P.; Horvath, C.M. Nipah virus V protein evades alpha and gamma interferons by preventing STAT1 and STAT2 activation and nuclear accumulation. J. Virol. 2002, 76, 11476–11483. [Google Scholar] [CrossRef]
- Rodriguez, J.J.; Cruz, C.D.; Horvath, C.M. Identification of the nuclear export signal and STAT-binding domains of the Nipah virus V protein reveals mechanisms underlying interferon evasion. J. Virol. 2004, 78, 5358–5367. [Google Scholar] [CrossRef]
- Park, M.-S.; Shaw, M.L.; Muñoz-Jordan, J.; Cros, J.F.; Nakaya, T.; Bouvier, N.; Palese, P.; García-Sastre, A.; Basler, C.F. Newcastle disease virus (NDV)-based assay demonstrates interferon-antagonist activity for the NDV V protein and the Nipah virus V, W, and C proteins. J. Virol. 2003, 77, 1501–1511. [Google Scholar] [CrossRef]
- Ciancanelli, M.J.; Volchkova, V.A.; Shaw, M.L.; Volchkov, V.E.; Basler, C.F. Nipah virus sequesters inactive STAT1 in the nucleus via a P gene-encoded mechanism. J. Virol. 2009, 83, 7828–7841. [Google Scholar] [CrossRef]
- Hagmaier, K.; Stock, N.; Goodbourn, S.; Wang, L.-F.; Randall, R. A single amino acid substitution in the V protein of Nipah virus alters its ability to block interferon signalling in cells from different species. J. Gen. Virol. 2006, 87, 3649–3653. [Google Scholar] [CrossRef]
- Satterfield, B.A.; Borisevich, V.; Foster, S.L.; Rodriguez, S.E.; Cross, R.W.; Fenton, K.A.; Agans, K.N.; Basler, C.F.; Geisbert, T.W.; Mire, C.E. Antagonism of STAT1 by Nipah virus P gene products modulates disease course but not lethal outcome in the ferret model. Sci. Rep. 2019, 9, 16710. [Google Scholar] [CrossRef]
- Pichlmair, A.; Kandasamy, K.; Alvisi, G.; Mulhern, O.; Sacco, R.; Habjan, M.; Binder, M.; Stefanovic, A.; Eberle, C.A.; Goncalves, A.; et al. Viral immune modulators perturb the human molecular network by common and unique strategies. Nature 2012, 487, 486–490. [Google Scholar] [CrossRef]
- Aghazadeh, Y.; Papadopoulos, V. The role of the 14-3-3 protein family in health, disease, and drug development. Drug Discov. Today 2016, 21, 278–287. [Google Scholar] [CrossRef] [PubMed]
- Fu, H.; Subramanian, R.R.; Masters, S.C. 14-3-3 proteins: Structure, function, and regulation. Annu. Rev. Pharmacol. Toxicol. 2000, 40, 617–647. [Google Scholar] [CrossRef] [PubMed]
- Tzivion, G.; Shen, Y.H.; Zhu, J. 14-3-3 proteins; bringing new definitions to scaffolding. Oncogene 2001, 20, 6331–6338. [Google Scholar] [CrossRef] [PubMed]
- Dougherty, M.K.; Morrison, D.K. Unlocking the code of 14-3-3. J. Cell Sci. 2004, 117, 1875–1884. [Google Scholar] [CrossRef]
- Wang, B.; Yang, H.; Liu, Y.C.; Jelinek, T.; Zhang, L.; Ruoslahti, E.; Fu, H. Isolation of high-affinity peptide antagonists of 14-3-3 proteins by phage display. Biochemistry 1999, 38, 12499–12504. [Google Scholar] [CrossRef]
- Lin, J.P.; Fan, Y.K.; Liu, H.M. The 14-3-3η chaperone protein promotes antiviral innate immunity via facilitating MDA5 oligomerization and intracellular redistribution. PLoS Pathog. 2019, 15, e1007582. [Google Scholar] [CrossRef]
- Liu, H.M.; Loo, Y.M.; Horner, S.M.; Zornetzer, G.A.; Katze, M.G.; Gale, M., Jr. The mitochondrial targeting chaperone 14-3-3ε regulates a RIG-I translocon that mediates membrane association and innate antiviral immunity. Cell Host Microbe 2012, 11, 528–537. [Google Scholar] [CrossRef]
- Riedl, W.; Acharya, D.; Lee, J.H.; Liu, G.; Serman, T.; Chiang, C.; Chan, Y.K.; Diamond, M.S.; Gack, M.U. Zika Virus NS3 Mimics a Cellular 14-3-3-Binding Motif to Antagonize RIG-I- and MDA5-Mediated Innate Immunity. Cell Host Microbe 2019, 26, 493–503. [Google Scholar] [CrossRef]
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Tsimbalyuk, S.; Cross, E.M.; Hoad, M.; Donnelly, C.M.; Roby, J.A.; Forwood, J.K. The Intrinsically Disordered W Protein Is Multifunctional during Henipavirus Infection, Disrupting Host Signalling Pathways and Nuclear Import. Cells 2020, 9, 1913. https://doi.org/10.3390/cells9081913
Tsimbalyuk S, Cross EM, Hoad M, Donnelly CM, Roby JA, Forwood JK. The Intrinsically Disordered W Protein Is Multifunctional during Henipavirus Infection, Disrupting Host Signalling Pathways and Nuclear Import. Cells. 2020; 9(8):1913. https://doi.org/10.3390/cells9081913
Chicago/Turabian StyleTsimbalyuk, Sofiya, Emily M. Cross, Mikayla Hoad, Camilla M. Donnelly, Justin A. Roby, and Jade K. Forwood. 2020. "The Intrinsically Disordered W Protein Is Multifunctional during Henipavirus Infection, Disrupting Host Signalling Pathways and Nuclear Import" Cells 9, no. 8: 1913. https://doi.org/10.3390/cells9081913
APA StyleTsimbalyuk, S., Cross, E. M., Hoad, M., Donnelly, C. M., Roby, J. A., & Forwood, J. K. (2020). The Intrinsically Disordered W Protein Is Multifunctional during Henipavirus Infection, Disrupting Host Signalling Pathways and Nuclear Import. Cells, 9(8), 1913. https://doi.org/10.3390/cells9081913