Inhibition of the Type I Interferon Antiviral Response During Arenavirus Infection
Abstract
:1. Arenaviruses as Important Model Systems to Study Virus-host Interactions and as Clinically Relevant Human Pathogens
1.1. LCMV Infection of the Mouse: The Rosetta Stone of Virus-host Interactions
1.2. Arenaviruses and Their Impact on Human Health
2. Molecular and Cell Biology of Arenaviruses
3. Type I IFN Antiviral Response and Innate Immunity
3.1. Type I IFNs and Their Roles in the Innate Response
3.1.1. Cellular Sources of IFN-I Production
3.1.2. Pleiotropic Effects of IFN-I
3.1.3. Down-regulation of IFN-I Production
3.2. Pathways Leading to IFN-I Induction
3.2.1. TLR-dependent Pathways for IFN-I Induction
3.2.2. TLR-independent Pathways for IFN-I Induction
3.3. Viral Strategies to Counteract Induction of IFN-I Production
3.3.1. Viral Effects on the Number and Function of Specialized IFN-producing Cells
3.3.2. Restricted Access of PRRs to PAMPs
3.3.3. Disruption of Cell Signaling Pathways Leading to IFN-I Induction in Infected Cells
3.3.4. Virus Interference with Mechanisms for Amplification of IFN-I Production
4. The IFN-I Response during Arenavirus Infections
4.1. IFN-I Production in Acute and Chronic LCMV Infections
4.1.1. The IFN-I Response in Acute LCMV Infection
4.1.2. Mechanisms by Which IFN-I Mediate Control of LCMV Infection
4.1.3. IFN-I Production during Chronic LCMV Infection
4.1.4. Cellular Sources of IFN-I Production in LCMV-infected Mice
4.1.5. Pathways Involved in IFN-I Induction During LCMV Infection
4.1.6. Down-regulation of IFN-I Production in LCMV-infected Mice
4.2. Effects of LCMV on DC Biology
4.2.1. DC Activation
4.2.2. DC Loss
4.2.3. Impairment of DC Functions
4.3. Molecular Mechanisms of LCMV Inhibition of Induction of IFN-I
4.3.1. Differential Inhibition of IFN-I by Arenavirus NPs
4.3.2. Amino Acid Residues Critical for the Anti-IFN-I Activity of LCMV-NP
Acknowledgements
Abbreviations
References and Notes
- Zinkernagel, R.M. On cross-priming of MHC class I-specific CTL: Rule or exception? Eur. J. Immunol. 2002, 32, 2385–2392. [Google Scholar] [CrossRef] [PubMed]
- Oldstone, M.B. Arenaviruses. I. The epidemiology molecular and cell biology of arenaviruses. Introduction. Curr. Top. Microbiol. Immunol. 2002, 262, V–XII. [Google Scholar]
- Buchmeier, M.J.; de la Torre, J.C.; Peters, C.J. Arenaviridae: The viruses and their replication. In Fields Virology, 5th ed.; Lippincott Williams & Wilkins: Philadelphia, PA, USA, 2007; Volume 2, pp. 1791–1827. [Google Scholar]
- McCormick, J.B.; Fisher-Hoch, S.P. Lassa fever. Curr. Top. Microbiol. Immunol. 2002, 262, 75–109. [Google Scholar]
- Peters, C.J.; Khan, A.S. Hantavirus pulmonary syndrome: The new American hemorrhagic fever. Clin. Infect. Dis. 2002, 34, 1224–1231. [Google Scholar] [CrossRef]
- Freedman, D.O.; Kozarsky, P.E.; Weld, L.H.; Cetron, M.S. GeoSentinel: The global emerging infections sentinel network of the International Society of Travel Medicine. J. Travel. Med. 1999, 6, 94–98. [Google Scholar] [CrossRef] [PubMed]
- Holmes, G.P.; McCormick, J.B.; Trock, S.C.; Chase, R.A.; Lewis, S.M.; Mason, C.A.; Hall, P.A.; Brammer, L.S.; Perez-Oronoz, G.I.; McDonnell, M.K.; et al. Lassa fever in the United States. Investigation of a case and new guidelines for management. N. Engl. J. Med. 1990, 323, 1120–1123. [Google Scholar] [CrossRef]
- Isaacson, M. Viral hemorrhagic fever hazards for travelers in Africa. Clin. Infect. Dis. 2001, 33, 1707–1712. [Google Scholar] [CrossRef] [PubMed]
- Weissenbacher, M.C.; Laguens, R.P.; Coto, C.E. Argentine hemorrhagic fever. Curr. Top. Microbiol. Immunol. 1987, 134, 79–116. [Google Scholar]
- Harrison, L.H.; Halsey, N.A.; McKee, K.T., Jr.; Peters, C.J.; Barrera Oro, J.G.; Briggiler, A.M.; Feuillade, M.R.; Maiztegui, J.I. Clinical case definitions for Argentine hemorrhagic fever. Clin. Infect. Dis. 1999, 28, 1091–1094. [Google Scholar] [CrossRef]
- Barton, L.L.; Mets, M.B.; Beauchamp, C.L. Lymphocytic choriomeningitis virus: Emerging fetal teratogen. Am. J. Obstet. Gynecol. 2002, 187, 1715–1716. [Google Scholar] [CrossRef]
- Jahrling, P.B.; Peters, C.J. Lymphocytic choriomeningitis virus. A neglected pathogen of man. Arch. Pathol. Lab. Med. 1992, 116, 486–488. [Google Scholar]
- Mets, M.B.; Barton, L.L.; Khan, A.S.; Ksiazek, T.G. Lymphocytic choriomeningitis virus: An underdiagnosed cause of congenital chorioretinitis. Am. J. Ophthalmol. 2000, 130, 209–215. [Google Scholar] [CrossRef] [PubMed]
- Fischer, J.E. Surgical practice and medicine in the USA. Surgeon 2006, 4, 267–271. [Google Scholar] [CrossRef] [PubMed]
- Peters, C.J. Lymphocytic choriomeningitis virus—An old enemy up to new tricks. N. Engl. J. Med. 2006, 354, 2208–2211. [Google Scholar] [CrossRef]
- Palacios, G.; Druce, J.; Du, L.; Tran, T.; Birch, C.; Briese, T.; Conlan, S.; Quan, P.L.; Hui, J.; Marshall, J.; Simons, J.F.; Egholm, M.; Paddock, C.D.; Shieh, W.J.; Goldsmith, C.S.; Zaki, S.R.; Catton, M.; Lipkin, W.I. A new arenavirus in a cluster of fatal transplant-associated diseases. N. Engl. J. Med. 2008, 358, 991–998. [Google Scholar] [CrossRef] [PubMed]
- Southern, P.J.; Singh, M.K.; Riviere, Y.; Jacoby, D.R.; Buchmeier, M.J.; Oldstone, M.B. Molecular characterization of the genomic S RNA segment from lymphocytic choriomeningitis virus. Virology 1987, 157, 145–155. [Google Scholar] [CrossRef] [PubMed]
- Meyer, B.J.; Southern, P.J. Sequence heterogeneity in the termini of lymphocytic choriomeningitis virus genomic and antigenomic RNAs. J. Virol. 1994, 68, 7659–7664. [Google Scholar] [CrossRef] [PubMed]
- Tortorici, M.A.; Albarino, C.G.; Posik, D.M.; Ghiringhelli, P.D.; Lozano, M.E.; Rivera Pomar, R.; Romanowski, V. Arenavirus nucleocapsid protein displays a transcriptional antitermination activity in vivo. Virus Res. 2001, 73, 41–55. [Google Scholar] [CrossRef]
- Cao, W.; Henry, M.D.; Borrow, P.; Yamada, H.; Elder, J.H.; Ravkov, E.V.; Nichol, S.T.; Compans, R.W.; Campbell, K.P.; Oldstone, M.B. Identification of alpha-dystroglycan as a receptor for lymphocytic choriomeningitis virus and Lassa fever virus. Science 1998, 282, 2079–2081. [Google Scholar] [CrossRef]
- Spiropoulou, C.F.; Kunz, S.; Rollin, P.E.; Campbell, K.P.; Oldstone, M.B. New World arenavirus clade C, but not clade A and B viruses, utilizes alpha-dystroglycan as its major receptor. J. Virol. 2002, 76, 5140–5146. [Google Scholar] [CrossRef]
- Borrow, P.; Oldstone, M.B. Mechanism of lymphocytic choriomeningitis virus entry into cells. Virology 1994, 198, 1–9. [Google Scholar] [CrossRef] [PubMed]
- Radoshitzky, S.R.; Abraham, J.; Spiropoulou, C.F.; Kuhn, J.H.; Nguyen, D.; Li, W.; Nagel, J.; Schmidt, P.J.; Nunberg, J.H.; Andrews, N.C.; Farzan, M.; Choe, H. Transferrin receptor 1 is a cellular receptor for New World haemorrhagic fever arenaviruses. Nature 2007, 446, 92–96. [Google Scholar] [CrossRef]
- Pho, M.T.; Ashok, A.; Atwood, W.J. JC virus enters human glial cells by clathrin-dependent receptor-mediated endocytosis. J. Virol. 2000, 74, 2288–2292. [Google Scholar] [CrossRef]
- Di Simone, C.; Buchmeier, M.J. Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 1995, 209, 3–9. [Google Scholar] [CrossRef]
- Castilla, V.; Mersich, S.E.; Candurra, N.A.; Damonte, E.B. The entry of Junin virus into Vero cells. Arch. Virol. 1994, 136, 363–374. [Google Scholar] [CrossRef]
- York, J.; Nunberg, J.H. Role of the stable signal peptide of Junin arenavirus envelope glycoprotein in pH-dependent membrane fusion. J. Virol. 2006, 80, 7775–7780. [Google Scholar] [CrossRef] [PubMed]
- Gallaher, W.R.; DiSimone, C.; Buchmeier, M.J. The viral transmembrane superfamily: Possible divergence of Arenavirus and Filovirus glycoproteins from a common RNA virus ancestor. BMC Microbiol. 2001, 1, 1. [Google Scholar] [CrossRef] [PubMed]
- Eschli, B.; Quirin, K.; Wepf, A.; Weber, J.; Zinkernagel, R.; Hengartner, H. Identification of an N-terminal trimeric coiled-coil core within arenavirus glycoprotein 2 permits assignment to class I viral fusion proteins. J. Virol. 2006, 80, 5897–5907. [Google Scholar] [CrossRef]
- Perez, M.; Craven, R.C.; de la Torre, J.C. The small RING finger protein Z drives arenavirus budding: Implications for antiviral strategies. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 12978–12983. [Google Scholar] [CrossRef]
- Strecker, T.; Eichler, R.; Meulen, J.; Weissenhorn, W.; Dieter Klenk, H.; Garten, W.; Lenz, O. Lassa virus Z protein is a matrix protein and sufficient for the release of virus-like particles [corrected]. J. Virol. 2003, 77, 10700–10705. [Google Scholar] [CrossRef]
- Urata, S.; Noda, T.; Kawaoka, Y.; Yokosawa, H.; Yasuda, J. Cellular factors required for Lassa virus budding. J. Virol. 2006, 80, 4191–4195. [Google Scholar] [CrossRef]
- Freed, E.O. Viral late domains. J. Virol. 2002, 76, 4679–4687. [Google Scholar] [CrossRef] [PubMed]
- Neuman, B.W.; Adair, B.D.; Burns, J.W.; Milligan, R.A.; Buchmeier, M.J.; Yeager, M. Complementarity in the supramolecular design of arenaviruses and retroviruses revealed by electron cryomicroscopy and image analysis. J. Virol. 2005, 79, 3822–3830. [Google Scholar] [CrossRef]
- Capul, A.A.; Perez, M.; Burke, E.; Kunz, S.; Buchmeier, M.J.; de la Torre, J.C. Arenavirus Z-glycoprotein association requires Z myristoylation but not functional RING or late domains. J. Virol. 2007, 81, 9451–9460. [Google Scholar] [CrossRef]
- Cornu, T.I.; de la Torre, J.C. RING finger Z protein of lymphocytic choriomeningitis virus (LCMV) inhibits transcription and RNA replication of an LCMV S-segment minigenome. J. Virol. 2001, 75, 9415–9426. [Google Scholar] [CrossRef]
- Perez, M.; de la Torre, J.C. Characterization of the genomic promoter of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 2003, 77, 1184–1194. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.J.; Perez, M.; Pinschewer, D.D.; de la Torre, J.C. Identification of the lymphocytic choriomeningitis virus (LCMV) proteins required to rescue LCMV RNA analogs into LCMV-like particles. J. Virol. 2002, 76, 6393–6397. [Google Scholar] [CrossRef] [PubMed]
- Pinschewer, D.D.; Perez, M.; Sanchez, A.B.; de la Torre, J.C. Recombinant lymphocytic choriomeningitis virus expressing vesicular stomatitis virus glycoprotein. Proc. Natl. Acad. Sci. U. S. A. 2003, 100, 7895–7900. [Google Scholar] [CrossRef]
- Pinschewer, D.D.; Perez, M.; de la Torre, J.C. Role of the virus nucleoprotein in the regulation of lymphocytic choriomeningitis virus transcription and RNA replication. J. Virol. 2003, 77, 3882–3887. [Google Scholar] [CrossRef]
- Sanchez, A.B.; de la Torre, J.C. Rescue of the prototypic Arenavirus LCMV entirely from plasmid. Virology 2006, 350, 370–380. [Google Scholar] [CrossRef]
- Flatz, L.; Bergthaler, A.; de la Torre, J.C.; Pinschewer, D.D. Recovery of an arenavirus entirely from RNA polymerase I/II-driven cDNA. Proc. Natl. Acad. Sci. U. S. A. 2006, 103, 4663–4668. [Google Scholar] [CrossRef] [PubMed]
- Albarino, C.G.; Bergeron, E.; Erickson, B.R.; Khristova, M.L.; Rollin, P.E.; Nichol, S.T. Efficient reverse genetics generation of infectious junin viruses differing in glycoprotein processing. J. Virol. 2009, 83, 5606–5614. [Google Scholar] [CrossRef]
- Lan, S.; McLay Schelde, L.; Wang, J.; Kumar, N.; Ly, H.; Liang, Y. Development of infectious clones for virulent and avirulent pichinde viruses: A model virus to study arenavirus-induced hemorrhagic fevers. J. Virol. 2009, 83, 6357–6362. [Google Scholar] [CrossRef] [PubMed]
- Isaacs, A.; Lindenmann, J. Virus interference. 1. The interferon. Proc. R. Soc. Lond. B Biol. Sci. 1957, 147, 258–267. [Google Scholar] [PubMed]
- Gresser, I.; Tovey, M.G.; Maury, C.; Bandu, M.T. Role of interferon in the pathogenesis of virus diseases in mice as demonstrated by the use of anti-interferon serum. II. Studies with herpes simplex, Moloney sarcoma, vesicular stomatitis, Newcastle disease, and influenza viruses. J. Exp. Med. 1976, 144, 1316–1323. [Google Scholar] [CrossRef]
- Moskophidis, D.; Battegay, M.; Bruendler, M.A.; Laine, E.; Gresser, I.; Zinkernagel, R.M. Resistance of lymphocytic choriomeningitis virus to alpha/beta interferon and to gamma interferon. J. Virol. 1994, 68, 1951–1955. [Google Scholar] [CrossRef]
- Muller, U.; Steinhoff, U.; Reis, L.F.L.; Hemmi, S.; Pavlovic, J.; Zinkernagel, R.M.; Aguet, M. Functional role of type I and type II interferons in antiviral defense. Science 1994, 264, 1918–1921. [Google Scholar] [CrossRef]
- Van den Broek, M.F.; Muller, U.; Huang, S.; Aguet, M.; Zinkernagel, R.M. Antiviral defense in mice lacking both alpha/beta and gamma interferon receptors. J. Virol. 1995, 69, 4792–4796. [Google Scholar] [CrossRef]
- Fiette, L.; Aubert, C.; Muller, U.; Huang, S.; Aguet, M.; Brahic, M.; Bureau, J.F. Theiler's virus infection of 129Sv mice that lack the interferon alpha/beta or interferon gamma receptors. J. Exp. Med. 1995, 181, 2069–2076. [Google Scholar] [CrossRef]
- Dupuis, S.; Jouanguy, E.; Al-Hajjar, S.; Fieschi, C.; Al-Mohsen, I.Z.; Al-Jumaah, S.; Yang, K.; Chapgier, A.; Eidenschenk, C.; Eid, P.; Al Ghonaium, A.; Tufenkeji, H.; Frayha, H.; Al-Gazlan, S.; Al-Rayes, H.; Schreiber, R.D.; Gresser, I.; Casanova, J.L. Impaired response to interferon-alpha/beta and lethal viral disease in human STAT1 deficiency. Nat. Genet. 2003, 33, 388–391. [Google Scholar] [CrossRef]
- Minegishi, Y.; Saito, M.; Morio, T.; Watanabe, K.; Agematsu, K.; Tsuchiya, S.; Takada, H.; Hara, T.; Kawamura, N.; Ariga, T.; Kaneko, H.; Kondo, N.; Tsuge, I.; Yachie, A.; Sakiyama, Y.; Iwata, T.; Bessho, F.; Ohishi, T.; Joh, K.; Imai, K.; Kogawa, K.; Shinohara, M.; Fujieda, M.; Wakiguchi, H.; Pasic, S.; Abinun, M.; Ochs, H.D.; Renner, E.D.; Jansson, A.; Belohradsky, B.H.; Metin, A.; Shimizu, N.; Mizutani, S.; Miyawaki, T.; Nonoyama, S.; Karasuyama, H. Human tyrosine kinase 2 deficiency reveals its requisite roles in multiple cytokine signals involved in innate and acquired immunity. Immunity 2006, 25, 745–755. [Google Scholar] [CrossRef] [PubMed]
- Casrouge, A.; Zhang, S.Y.; Eidenschenk, C.; Jouanguy, E.; Puel, A.; Yang, K.; Alcais, A.; Picard, C.; Mahfoufi, N.; Nicolas, N.; Lorenzo, L.; Plancoulaine, S.; Sénéchal, B.; Geissmann, F.; Tabeta, K.; Hoebe, K.; Du, X.; Miller, R.L.; Héron, B.; Mignot, C.; de Villemeur, T.B.; Lebon, P.; Dulac, O.; Rozenberg, F.; Beutler, B.; Tardieu, M.; Abel, L.; Casanova, J.L. Herpes simplex virus encephalitis in human UNC-93B deficiency. Science 2006, 314, 308–312. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.Y.; Boisson-Dupuis, S.; Chapgier, A.; Yang, K.; Bustamante, J.; Puel, A.; Picard, C.; Abel, L.; Jouanguy, E.; Casanova, J.L. Inborn errors of interferon (IFN)-mediated immunity in humans: Insights into the respective roles of IFN-alpha/beta, IFN-gamma, and IFN-lambda in host defense. Immunol. Rev. 2008, 226, 29–40. [Google Scholar] [CrossRef] [PubMed]
- Randall, R.E.; Goodbourn, S. Interferons and viruses: An interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89, 1–47. [Google Scholar] [CrossRef]
- Gale, M.J.; Sen, G.C. Viral evasion of the interferon system. J. Interferon Cytokine Res. 2009, 29, 475–476. [Google Scholar] [CrossRef]
- Kawai, T.; Akira, S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol. 2010, 11, 373–384. [Google Scholar] [CrossRef]
- Colonna, M.; Trinchieri, G.; Liu, Y.J. Plasmacytoid dendritic cells in immunity. Nat. Immunol. 2004, 5, 1219–1226. [Google Scholar] [CrossRef]
- Liu, Y.-J. IPC: Professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu. Rev. Immunol. 2005, 23, 275–306. [Google Scholar] [CrossRef]
- Cao, W.; Liu, Y.-J. Innate immune functions of plasmacytoid dendritic cells. Curr. Opin. Immunol. 2007, 19, 24–30. [Google Scholar] [CrossRef]
- García-Sastre, A.; Biron, C.A. Type 1 interferons and the virus-host relationship: A lesson in détente. Science 2006, 312, 879–882. [Google Scholar] [CrossRef]
- Der, S.D.; Zhou, A.; Williams, B.R.; Silverman, R.H. Identification of genes differentially regulated by interferon alpha, beta, or gamma using oligonucleotide arrays. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 5623–5628. [Google Scholar] [CrossRef]
- Van Boxel-Dezaire, A.; Rani, M.R.; Stark, G.R. Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 2006, 25, 361–372. [Google Scholar] [CrossRef] [PubMed]
- Stetson, D.B.; Medzhitov, R. Type I interferons in host defense. Immunity 2006, 25, 373–381. [Google Scholar] [CrossRef]
- Gale, M., Jr.; Katze, M.G. Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol. Ther. 1998, 78, 29–46. [Google Scholar] [CrossRef] [PubMed]
- Williams, B.R. PKR; A sentinel kinase for cellular stress. Oncogene 1999, 18, 6112–6120. [Google Scholar] [CrossRef]
- Silverman, R.H. Fascination with 2–5A-dependent RNase: A unique enzyme that functions in interferon action. J. Interferon Res. 1994, 14, 101–104. [Google Scholar] [CrossRef]
- Kochs, G.; Haener, M.; Aebi, U.; Haller, O. Self-assembly of human MxA GTPase into highly ordered dynamin-like oligomers. J. Biol. Chem. 2002, 277, 14172–14176. [Google Scholar] [CrossRef]
- Haller, O.; Kochs, G. Interferon-induced mx proteins: Dynamin-like GTPases with antiviral activity. Traffic 2002, 3, 710–717. [Google Scholar] [CrossRef] [PubMed]
- Katze, M.G.; He, Y.; Gale, M., Jr. Viruses and interferon: A fight for supremacy. Nat. Rev. Immunol. 2002, 2, 675–687. [Google Scholar] [CrossRef]
- Katze, M.G. Interferon, PKR, virology, and genomics: What is past and what is next in the new millennium? J. Interferon Cytokine Res. 2002, 22, 283–286. [Google Scholar] [CrossRef]
- Sadler, A.J.; Willimas, B.R.G. Interferon-inducible antiviral effectors. Nat. Rev. Immunol. 2008, 8, 559–568. [Google Scholar] [CrossRef] [PubMed]
- Stark, G.R.; Kerr, I.M.; Williams, B.R.; Silverman, R.H.; Schreiber, R.D. How cells respond to interferons. Annu. Rev. Biochem. 1998, 67, 227–264. [Google Scholar] [CrossRef] [PubMed]
- Biron, C.A.; Nguyen, K.B.; Pien, G.C. Innate immune responses to LCMV infections: Natural killer cells and cytokines. Curr. Top. Microbiol. Immunol. 2002, 263, 7–27. [Google Scholar]
- Aguet, M.; Vignaux, F.; Fridman, W.H.; Gresser, I. Enhancement of Fc gamma receptor expression in interferon-treated mice. Eur. J. Immunol. 1981, 11, 926–930. [Google Scholar] [CrossRef]
- Ito, T.; Amakawa, R.; Inaba, M.; Ikehara, S.; Inaba, K.; Fukuhara, S. Differential regulation of human blood dendritic cell subsets by IFNs. J. Immunol. 2001, 166, 2961–2969. [Google Scholar] [CrossRef]
- Jarrossay, D.; Napolitani, G.; Colonna, M.; Sallusto, F.; Lanzavecchia, A. Specialization and complementarity in microbial molecule recognition by human myeloid and plasmacytoid dendritic cells. Eur. J. Immunol. 2001, 31, 3388–3393. [Google Scholar] [CrossRef]
- Tough, D.F. Type I interferon as a link between innate and adaptive immunity through dendritic cell stimulation. Leuk. Lymphoma 2004, 45, 257–264. [Google Scholar] [CrossRef]
- Brinkmann, V.; Geiger, T.; Alkan, S.; Heusser, C.H. Interferon α increases the frequency of interferon γ-producing human CD4+ T cells. J. Exp. Med. 1993, 178, 1655–1663. [Google Scholar] [CrossRef] [PubMed]
- Cella, M.; Facchetti, F.; Lanzavecchia, A.; Colonna, M. Plasmacytoid dendritic cells activated by influenza virus and CD40L drive a potent TH1 polarization. Nat. Immunol. 2000, 1, 305–310. [Google Scholar] [CrossRef]
- Kolumam, G.A.; Thomas, S.; Thompson, L.J.; Sprent, J.; Murali-Krishna, K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J. Exp. Med. 2005, 202, 637–650. [Google Scholar] [CrossRef]
- Le Bon, A.; Durand, V.; Kamphuis, E.; Thompson, C.; Bulfone-Paus, S.; Rossmann, C.; Kalinke, U.; Tough, D.F. Direct stimulation of T cells by type I IFN enhances the CD8+ T cell response during cross-priming. J. Immunol. 2006, 176, 4682–4689. [Google Scholar] [CrossRef] [PubMed]
- Bekeredjian-Ding, I.B.; Wagner, M.; Hornung, V.; Giese, T.; Schnurr, M.; Endres, S.; Hartmann, G. Plasmacytoid dendritic cells control TLR7 sensitivity of naive B cells via type I IFN. J. Immunol. 2005, 174, 4043–4050. [Google Scholar] [CrossRef] [PubMed]
- Le Bon, A.; Thompson, C.; Kamphuis, E.; Durand, V.; Rossmann, C.; Kalinke, U.; Tough, D.F. Cutting edge: Enhancement of antibody responses through direct stimulation of B and T cells by type I IFN. J. Immunol. 2006, 176, 2074–2078. [Google Scholar] [CrossRef]
- Coro, E.S.; Chang, W.L.; Baumgarth, N. Type I IFN receptor signals directly stimulate local B cells early following influenza virus infection. J. Immunol. 2006, 176, 4343–4351. [Google Scholar] [CrossRef]
- Degli-Esposti, M.A.; Smyth, M.J. Close encounters of different kinds: Dendritic cells and NK cells take centre stage. Nat. Rev. Immunol. 2005, 5, 112–124. [Google Scholar] [CrossRef] [PubMed]
- Miyagi, T.; Gil, M.P.; Wang, X.; Louten, J.; Chu, W.M.; Biron, C.A. High basal STAT4 balanced by STAT1 induction to control type 1 interferon effects in natural killer cells. J. Exp. Med. 2007, 204, 2383–2396. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, K.B.; Watford, W.T.; Salomon, R.; Hofmann, S.R.; Pien, G.C.; Morinobu, A.; Gadina, M.; O’Shea, J.J.; Biron, C.A. Critical role for STAT4 activation by type 1 interferons in the interferon-gamma response to viral infection. Science 2002, 297, 2063–2066. [Google Scholar] [CrossRef]
- Gil, M.P.; Salomon, R.; Louten, J.; Biron, C.A. Modulation of STAT1 protein levels: A mechanism shaping CD8 T-cell responses in vivo. Blood 2006, 107, 987–993. [Google Scholar] [CrossRef]
- Merigan, T.C. Pharmacokinetics and side effects of interferon in man. Tex. Rep. Biol. Med. 1977, 35, 541–547. [Google Scholar]
- Gresser, I.; Morel-Maroger, L.; Riviere, Y.; Guillon, J.C.; Tovey, M.G.; Woodrow, D.; Sloper, J.C.; Moss, J. Interferon-induced disease in mice and rats. Ann. N. Y. Acad. Sci. 1980, 350, 12–20. [Google Scholar] [CrossRef]
- Banchereau, J.; Pascual, V. Type I interferon in systemic lupus erythematosus and other autoimmune diseases. Immunity 2006, 25, 383–392. [Google Scholar] [CrossRef] [PubMed]
- Cao, W.; Bover, L.; Cho, M.; Wen, X.; Hanabuchi, S.; Bao, M.; Rosen, D.B.; Wang, Y.H.; Shaw, J.L.; Du, Q.; Li, C.; Arai, N.; Yao, Z.; Lanier, L.L.; Liu, Y.-J. Regulation of TLR7/9 responses in plasmacytoid dendritic cells by BST2 and ILT7 receptor interaction. J. Exp. Med. 2009, 206, 1603–1614. [Google Scholar] [CrossRef] [PubMed]
- Janeway, C.A.J.; Medzhitov, R. Innate immune recognition. Annu. Rev. Immunol. 2002, 20, 197–216. [Google Scholar] [CrossRef]
- Iwasaki, A.; Medzhitov, R. Regulation of adaptive immunity by the innate immune system. Science 2010, 327, 291–295. [Google Scholar] [CrossRef]
- Ishii, K.J.; Koyama, S.; Nakagawa, A.; Coban, C.; Akira, S. Host innate immune receptors and beyond: Making sense of microbial infections. Cell Host Microbe 2008, 3, 352–363. [Google Scholar] [CrossRef] [PubMed]
- Beutler, B.A. TLRs and innate immunity. Blood 2009, 113, 1399–1407. [Google Scholar] [CrossRef] [PubMed]
- Martinon, F.; Gaide, O.; Petrilli, V.; Mayor, A.; Tschopp, J. NALP inflammasomes: A central role in innate immunity. Semin. Immunopathol. 2007, 29, 213–229. [Google Scholar] [CrossRef]
- Yoneyama, M.; Fujita, T. RNA recognition and signal transduction by RIG-I-like receptors. Immunol. Rev. 2009, 227, 54–65. [Google Scholar] [CrossRef]
- Wilkins, C.; Gale, M.J. Recognition of viruses by cytoplasmic sensors. Curr. Opin. Immunol. 2010, 22, 41–47. [Google Scholar] [CrossRef] [PubMed]
- Kawai, T.; Akira, S. Innate immune recognition of viral infection. Nat. Immunol. 2006, 7, 131–137. [Google Scholar] [CrossRef]
- Lee, M.S.; Kim, Y.J. Signaling pathways downstream of pattern recognition receptors and their cross talk. Annu. Rev. Biochem. 2007, 76, 447–480. [Google Scholar] [CrossRef] [PubMed]
- Palm, N.W.; Medzhitov, R. Pattern recognition receptors and control of adaptive immunity. Immunol. Rev. 2009, 227, 221–233. [Google Scholar] [CrossRef] [PubMed]
- Blasius, A.L.; Beutler, B. Intracellular toll-like receptors. Immunity 2010, 32, 305–315. [Google Scholar] [CrossRef]
- O'Neill, L.A. The interleukin-1 receptor/Toll-like receptor superfamily: 10 years of progress. Immunol. Rev. 2008, 226, 10–18. [Google Scholar] [CrossRef] [PubMed]
- Carpenter, S.; O'Neill, L.A. Recent insights into the structure of Toll-like receptors and post-translational modifications of their associated signalling proteins. Biochem. J. 2009, 422, 1–10. [Google Scholar] [CrossRef]
- Kumar, H.; Kawai, T.; Akira, S. Toll-like receptors and innate immunity. Biochem. Biophys. Res. Commun. 2009, 388, 621–625. [Google Scholar] [CrossRef]
- Kim, Y.M.; Brinkmann, M.M.; Paquet, M.E.; Ploegh, H.L. UNC93B1 delivers nucleotide-sensing Toll-like receptors to endolysosomes. Nature 2008, 452, 234–238. [Google Scholar] [CrossRef]
- Häcker, H.; Redecke, V.; Blagoev, B.; Kratchmarova, I.; Hsu, L.C.; Wang, G.G.; Kamps, M.P.; Raz, E.; Wagner, H.; Häcker, G.; Mann, M.; Karin, M. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 2006, 439, 204–207. [Google Scholar] [CrossRef]
- Oganesyan, G.; Saha, S.K.; Guo, B.; He, J.Q.; Shahangian, A.; Zarnegar, B.; Perry, A.; Cheng, G. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 2006, 439, 208–211. [Google Scholar] [CrossRef]
- Wang, C.; Chen, T.; Zhang, J.; Yang, M.; Li, N.; Xu, X.; Cao, X. The E3 ubiquitin ligase Nrdp1 'preferentially' promotes TLR-mediated production of type I interferon. Nat. Immunol. 2009, 10, 744–752. [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] [PubMed]
- 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] [PubMed]
- Servant, M.J.; ten Oever, B.; LePage, C.; Conti, L.; Gessani, S.; Julkunen, I.; Lin, R.; Hiscott, J. Identification of distinct signaling pathways leading to the phosphorylation of interferon regulatory factor 3. J. Biol. Chem. 2001, 276, 355–363. [Google Scholar] [CrossRef]
- Sato, M.; Suemori, H.; Hata, N.; Asagiri, M.; Ogasawara, K.; Nakao, K.; Nakaya, T.; Katsuki, M.; Noguchi, S.; Tanaka, N.; Taniguchi, T. 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] [PubMed]
- Izaguirre, A.; Barnes, B.J.; Amrute, S.; Yeow, W.S.; Megjugorac, N.; Dai, J.; Feng, D.; Chung, E.; Pitha, P.M.; Fitzgerald-Bocarsly, P. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J. Leukoc. Biol. 2003, 74, 1125–1138. [Google Scholar] [CrossRef]
- Coccia, E.M.; Severa, M.; Giacomini, E.; Monneron, D.; Remoli, M.E.; Julkunen, I.; Cella, M.; Lande, R.; Uzé, G. Viral infection and Toll-like receptor agonists induce a differential expression of type I and lambda interferons in human plasmacytoid and monocyte-derived dendritic cells. Eur. J. Immunol. 2004, 34, 796–805. [Google Scholar] [CrossRef] [PubMed]
- Sato, M.; Hata, N.; Asagiri, M.; Nakaya, T.; Taniguchi, T.; Tanaka, N. Positive feedback regulation of type I IFN genes by the IFN-inducible transcription factor IRF-7. FEBS Lett. 1998, 441, 106–110. [Google Scholar] [CrossRef] [PubMed]
- Marie, I.; Durbin, J.E.; Levy, D.E. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 1998, 17, 6660–6669. [Google Scholar] [CrossRef]
- Honda, K.; Taniguchi, T. IRFs: Master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat. Rev. Immunol. 2006, 6, 644–658. [Google Scholar] [CrossRef]
- Honda, K.; Ohba, Y.; Yanai, H.; Negishi, H.; Mizutani, T.; Takaoka, A.; Taya, C.; Taniguchi, T. Spatiotemporal regulation of MyD88–IRF-7 signalling for robust type-I interferon induction. Nature 2005, 434, 1035–1040. [Google Scholar] [CrossRef]
- Honda, K.; Yanai, H.; Mizutani, T.; Negishi, H.; Shimada, N.; Suzuki, N.; Ohba, Y.; Takaoka, A.; Yeh, W.; Taniguchi, T. Role of a transductional-transcriptional processor complex involving MyD88 and IRF-7 in Toll-like receptor signaling. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 15416–15421. [Google Scholar] [CrossRef] [PubMed]
- Kawai, T.; Sato, S.; Ishii, K.J.; Coban, C.; Hemmi, H.; Yamamoto, M.; Terai, K.; Matsuda, M.; Inoue, J.; Uematsu, S.; Takeuchi, O.; Akira, S. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 2004, 5, 1061–1068. [Google Scholar] [CrossRef] [PubMed]
- Hoshino, K.; Sugiyama, T.; Matsumoto, M.; Tanaka, T.; Saito, M.; Hemmi, H.; Ohara, O.; Akira, S.; Kaisho, T. IκB kinase-α is critical for interferon-α production induced by Toll-like receptors 7 and 9. Nature 2006, 440, 949–953. [Google Scholar] [CrossRef] [PubMed]
- Uematsu, S.; Sato, S.; Yamamoto, M.; Hirotani, T.; Kato, H.; Takeshita, F.; Matsuda, M.; Coban, C.; Ishii, K.J.; Kawai, T.; Takeuchi, O.; Akira, S. Interleukin-1 receptor-associated kinase-1 plays an essential role for Toll-like receptor (TLR)7- and TLR9-mediated interferon-α induction. J. Exp. Med. 2005, 201, 915–923. [Google Scholar] [CrossRef] [PubMed]
- Honda, K.; Yanai, H.; Negishi, H.; Asagiri, M.; Sato, M.; Mizutani, T.; Shimada, N.; Ohba, Y.; Takaoka, A.; Yoshida, N.; Taniguchi, T. IRF-7 is the master regulator of type-I interferon dependent immune responses. Nature 2005, 434, 772–777. [Google Scholar] [CrossRef]
- Beutler, B.; Eidenschenk, C.; Crozat, K.; Imler, J.L.; Takeuchi, O.; Hoffmann, J.A.; Akira, S. Genetic analysis of resistance to viral infection. Nat. Rev. Immunol. 2007, 7, 753–766. [Google Scholar] [CrossRef]
- Seth, R.B.; Sun, L.; Ea, C.K.; Chen, Z.J. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005, 122, 669–682. [Google Scholar] [CrossRef]
- Xu, L.G.; Wang, Y.Y.; Han, K.J.; Li, L.Y.; Zhai, Z.; Shu, H.B. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 2005, 19, 727–740. [Google Scholar] [CrossRef]
- Meylan, E.; Curran, J.; Hofmann, K.; Moradpour, D.; Binder, M.; Bartenschlager, R.; Tschopp, J. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437, 1167–1172. [Google Scholar] [CrossRef]
- Andrejeva, J.; Childs, K.S.; Young, D.F.; Carlos, T.S.; Stock, N.; Goodbourn, S.; Randall, R.E. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda-5, and inhibit its activation of the IFN-beta promoter. Proc. Natl. Acad. Sci. U. S. A. 2004, 101, 17264–17269. [Google Scholar] [CrossRef]
- Gotoh, B.; Komatsu, T.; Takeuchi, K.; Yokoo, J. Paramyxovirus accessory proteins as interferon antagonists. Microbiol. Immunol. 2001, 45, 787–800. [Google Scholar] [CrossRef]
- Gotoh, B.; Komatsu, T.; Takeuchi, K.; Yokoo, J. Paramyxovirus strategies for evading the interferon response. Rev. Med. Virol. 2002, 12, 337–357. [Google Scholar] [CrossRef] [PubMed]
- Yoneyama, M.; Kikuchi, M.; Matsumoto, K.; Imaizumi, T.; Miyagishi, M.; Taira, K.; Foy, E.; Loo, Y.M.; Gale, M., Jr.; Akira, S.; Yonehara, S.; Kato, A.; Fujita, T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175, 2851–2858. [Google Scholar] [CrossRef] [PubMed]
- Soumelis, V.; Scott, I.; Gheyas, F.; Bouhour, D.; Cozon, G.; Cotte, L.; Huang, L.; Levy, J.A.; Liu, Y.-J. Depletion of circulating natural type 1 interferon-producing cells in HIV-infected AIDS patients. Blood 2001, 98, 906–912. [Google Scholar] [CrossRef] [PubMed]
- Feldman, S.; Stein, D.; Amrute, S.; Denny, T.; Garcia, Z.; Kloser, P.; Sun, Y.; Megjugorac, N.; Fitzgerald-Bocarsly, P. Decreased interferon-alpha production in HIV-infected patients correlates with numerical and functional deficiencies in circulating type 2 dendritic cell precursors. Clin. Immunol. 2001, 101, 201–210. [Google Scholar] [CrossRef]
- Otero, M.; Nunnari, G.; Leto, D.; Sullivan, J.; Wang, F.X.; Frank, I.; Xu, Y.; Patel, C.; Dornadula, G.; Kulkosky, J.; Pomerantz, R.J. Peripheral blood Dendritic cells are not a major reservoir for HIV type 1 in infected individuals on virally suppressive HAART. AIDS Res. Hum. Retroviruses 2003, 19, 1097–1103. [Google Scholar] [CrossRef]
- Malleret, B.; Manéglier, B.; Karlsson, I.; Lebon, P.; Nascimbeni, M.; Perié, L.; Brochard, P.; Delache, B.; Calvo, J.; Andrieu, T.; Spreux-Varoquaux, O.; Hosmalin, A.; Le Grand, R.; Vaslin, B. Primary infection with simian immunodeficiency virus: Plasmacytoid dendritic cell homing to lymph nodes, type I interferon, and immune suppression. Blood 2008, 112, 4598–4608. [Google Scholar] [CrossRef]
- Brown, K.N.; Wijewardana, V.; Liu, X.; Barratt-Boyes, S.M. Rapid influx and death of plasmacytoid dendritic cells in lymph nodes mediate depletion in acute simian immunodeficiency virus infection. PLoS Pathog. 2009, 5, e1000413. [Google Scholar] [CrossRef]
- Szabo, G.; Dolganiuc, A. Subversion of plasmacytoid and myeloid dendritic cell functions in chronic HCV infection. Immunobiology 2005, 210, 237–247. [Google Scholar] [CrossRef]
- Van der Molen, R.; Sprengers, D.; Binda, R.; de Jong, E.; Niesters, H.; Kusters, J.; Kwekkeboom, J.; Janssen, H. Functional impairment of myeloid and plasmacytoid dendritic cells of patients with chronic hepatitis B. Hepatology 2004, 40, 738–746. [Google Scholar] [CrossRef]
- Hishizawa, M.; Imada, K.; Kitawaki, T.; Ueda, M.; Kadowaki, N.; Uchiyama, T. Depletion and impaired interferon-α-producing capacity of blood plasmacytoid dendritic cells in human T-cell leukaemia virus type I-infected individuals. Br. J. Haematol. 2004, 125, 568–575. [Google Scholar] [CrossRef] [PubMed]
- Shiina, M.; Rehermann, B. Cell culture-produced hepatitis C virus impairs plasmacytoid dendritic cell function. Hepatology 2008, 47, 385–395. [Google Scholar] [CrossRef] [PubMed]
- Iqbal, M.; Poole, E.; Goodbourn, S.; McCauley, J.W. Role for bovine viral diarrhea virus Erns glycoprotein in the control of activation of beta interferon by double-stranded RNA. J. Virol. 2004, 78, 136–145. [Google Scholar] [CrossRef] [PubMed]
- Li, K.; Foy, E.; Ferreon, J.C.; Nakamura, M.; Ferreon, A.C.; Ikeda, M.; Ray, S.C.; Gale, M.J.; Lemon, S.M. Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc. Natl. Acad. Sci. U. S. A. 2005, 102, 2992–2997. [Google Scholar] [CrossRef]
- Goodbourn, S.; Randall, R.E. The regulation of type I interferon production by paramyxoviruses. J. Interferon Cytokine Res. 2009, 29, 539–547. [Google Scholar] [CrossRef]
- Juang, Y.T.; Lowther, W.; Kellum, M.; Au, W.C.; Lin, R.; Hiscott, J.; Pitha, P.M. Primary activation of interferon A and interferon B gene transcription by interferon regulatory factor 3. Proc. Natl. Acad. Sci. U. S. A. 1998, 95, 9837–9842. [Google Scholar] [CrossRef]
- Sato, M.; Tanaka, N.; Hata, N.; Oda, E.; Taniguchi, T. Involvement of the IRF family transcription factor IRF-3 in virus-induced activation of the IFN-beta gene. FEBS Lett. 1998, 425, 112–116. [Google Scholar] [CrossRef]
- Merigan, T.C.; Oldstone, M.B.; Welsh, R.M. Interferon production during lymphocytic choriomeningitis virus infection of nude and normal mice. Nature 1977, 268, 67–68. [Google Scholar] [CrossRef]
- Louten, J.; van Rooijen, N.; Biron, C.A. Type 1 IFN deficiency in the absence of normal splenic architecture during lymphocytic choriomeningitis virus infection. J. Immunol. 2006, 177, 3266–3272. [Google Scholar] [CrossRef]
- Zuniga, E.I.; Liou, L.Y.; Mack, L.; Mendoza, M.; Oldstone, M.B. Persistent virus infection inhibits type I interferon production by plasmacytoid dendritic cells to facilitate opportunistic infections. Cell Host Microbe 2008, 4, 374–386. [Google Scholar] [CrossRef]
- Lee, L.N.; Burke, S.; Montoya, M.; Borrow, P. Multiple mechanisms contribute to impairment of type 1 interferon production during chronic lymphocytic choriomeningitis virus infection of mice. J. Immunol. 2009, 182, 7178–7189. [Google Scholar] [CrossRef] [PubMed]
- Cousens, L.P.; Peterson, R.; Hsu, S.; Dorner, A.; Altman, J.D.; Ahmed, R.; Biron, C.A. Two roads diverged: Interferon alpha/beta- and interleukin 12-mediated pathways in promoting T cell interferon gamma responses during viral infection. J. Exp. Med. 1999, 189, 1315–1328. [Google Scholar] [CrossRef] [PubMed]
- Sandberg, K.; Eloranta, M.L.; Campbell, I.L. Expression of alpha/beta interferons (IFN-alpha/beta) and their relationship to IFN-alpha/beta-induced genes in lymphocytic choriomeningitis. J. Virol. 1994, 68, 7358–7366. [Google Scholar] [CrossRef] [PubMed]
- Hinson, E.R.; Joshi, N.S.; Chen, J.H.; Rahner, C.; Jung, Y.W.; Wang, X.; Kaech, S.M.; Cresswell, P. Viperin is highly induced in neutrophils and macrophages during acute and chronic lymphocytic choriomeningitis virus infection. J. Immunol. 2010, 184, 5723–5731. [Google Scholar] [CrossRef] [PubMed]
- Djavani, M.; Rodas, J.; Lukashevich, I.S.; Horejsh, D.; Pandolfi, P.P.; Borden, K.L.; Salvato, M.S. Role of the promyelocytic leukemia protein PML in the interferon sensitivity of lymphocytic choriomeningitis virus. J. Virol. 2001, 75, 6204–6208. [Google Scholar] [CrossRef]
- Bonilla, W.V.; Pinschewer, D.D.; Klenerman, P.; Rousson, V.; Gaboli, M.; Pandolfi, P.P.; Zinkernagel, R.M.; Salvato, M.S.; Hengartner, H. Effects of promyelocytic leukemia protein on virus-host balance. J. Virol. 2002, 76, 3810–3818. [Google Scholar] [CrossRef] [PubMed]
- Asper, M.; Sternsdorf, T.; Hass, M.; Drosten, C.; Rhode, A.; Schmitz, H.; Gunther, S. Inhibition of different Lassa virus strains by alpha and gamma interferons and comparison with a less pathogenic arenavirus. J. Virol. 2004, 78, 3162–3169. [Google Scholar] [CrossRef]
- Zahn, R.C.; Schelp, I.; Utermohlen, O.; von Laer, D. A-to-G hypermutation in the genome of lymphocytic choriomeningitis virus. J. Virol. 2007, 81, 457–464. [Google Scholar] [CrossRef]
- Osiak, A.; Utermohlen, O.; Niendorf, S.; Horak, I.; Knobeloch, K.P. ISG15, an interferon-stimulated ubiquitin-like protein, is not essential for STAT1 signaling and responses against vesicular stomatitis and lymphocytic choriomeningitis virus. Mol. Cell Biol 2005, 25, 6338–6345. [Google Scholar] [CrossRef]
- Ritchie, K.J.; Hahn, C.S.; Kim, K.I.; Yan, M.; Rosario, D.; Li, L.; de la Torre, J.C.; Zhang, D.E. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 2004, 10, 1374–1378. [Google Scholar] [CrossRef]
- Sakuma, T.; Noda, T.; Urata, S.; Kawaoka, Y.; Yasuda, J. Inhibition of Lassa and Marburg virus production by tetherin. J. Virol. 2009, 83, 2382–2385. [Google Scholar] [CrossRef] [PubMed]
- Radoshitzky, S.R.; Dong, L.; Chi, X.; Clester, J.C.; Retterer, C.; Spurgers, K.; Kuhn, J.H.; Sandwick, S.; Ruthel, G.; Kota, K.; Boltz, D.; Warren, T.; Kranzusch, P.J.; Whelan, S.P.; Bavari, S. Infectious Lassa virus, but not filoviruses, is restricted by BST-2/tetherin. J. Virol. 2010, 84, 10569–10580. [Google Scholar] [CrossRef] [PubMed]
- Biron, C.A.; Sonnenfeld, G.; Welsh, R.M. Interferon induces natural killer cell blastogenesis in vivo. J. Leukoc. Biol. 1984, 35, 31–37. [Google Scholar] [CrossRef]
- Bukowski, J.F.; Woda, B.A.; Habu, S.; Okumura, K.; Welsh, R.M. Natural killer cell depletion enhances virus synthesis and virus-induced hepatitis in vivo. J. Immunol. 1983, 131, 1531–1538. [Google Scholar] [CrossRef] [PubMed]
- Welsh, R.M.; Brubaker, J.O.; Vargas-Cortes, M.; O'Donnell, C.L. Natural killer (NK) cell response to virus infections in mice with severe combined immunodeficiency. The stimulation of NK cells and the NK cell-dependent control of virus infections occur independently of T and B cell function. J. Exp. Med. 1991, 173, 1053–1063. [Google Scholar] [CrossRef] [PubMed]
- Montoya, M.; Edwards, M.J.; Reid, D.M.; Borrow, P. Rapid activation of spleen dendritic cell subsets following lymphocytic choriomeningitis virus infection of mice: Analysis of the involvement of type 1 IFN. J. Immunol. 2005, 174, 1851–1861. [Google Scholar] [CrossRef]
- Le Bon, A.; Etchart, N.; Rossmann, C.; Ashton, M.; Hou, S.; Gewert, D.; Borrow, P.; Tough, D.F. Cross-priming of CD8+ T cells stimulated by virus-induced type I interferon. Nat. Immunol. 2003, 4, 1009–1015. [Google Scholar] [CrossRef]
- Thompson, L.J.; Kolumam, G.A.; Thomas, S.; Murali-Krishna, K. Innate inflammatory signals induced by various pathogens differentially dictate the IFN-I dependence of CD8 T cells for clonal expansion and memory formation. J. Immunol. 2006, 177, 1746–1754. [Google Scholar] [CrossRef]
- Ou, R.; Zhou, S.; Huang, L.; Moskophidis, D. Critical role for alpha/beta and gamma interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J. Virol. 2001, 75, 8407–8423. [Google Scholar] [CrossRef]
- Moskophidis, D.; Lechner, F.; Pircher, H.; Zinkernagel, R.M. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature 1993, 362, 758–761. [Google Scholar] [CrossRef]
- Zajac, A.J.; Blattman, J.N.; Murali-Krishna, K.; Sourdive, D.J.D.; Suresh, M.; Altman, J.D.; Ahmed, R. Viral immune evasion due to persistence of activated T cells without effector function. J. Exp. Med. 1998, 188, 2205–2213. [Google Scholar] [CrossRef] [PubMed]
- Saron, M.F.; Riviere, Y.; Hovanessian, A.G.; Guillon, J.C. Chronic production of interferon in carrier mice congenitally infected with lymphocytic choriomeningitis virus. Virology 1982, 117, 253–256. [Google Scholar] [CrossRef]
- Bukowski, J.F.; Biron, C.A.; Welsh, R.M. Elevated natural killer cell-mediated cytotoxicity, plasma interferon, and tumor cell rejection in mice persistently infected with lymphocytic choriomeningitis virus. J. Immunol. 1983, 131, 991–996. [Google Scholar] [CrossRef] [PubMed]
- Truong, P.; Heydari, S.; Garidou, L.; McGavern, D.B. Persistent viral infection elevates central nervous system MHC class I through chronic production of interferons. J. Immunol. 2009, 183, 3895–3905. [Google Scholar] [CrossRef]
- Guidotti, L.G.; Borrow, P.; Hobbs, M.V.; Matzke, B.; Gresser, I.; Oldstone, M.B.; Chisari, F.V. Viral cross talk: Intracellular inactivation of the hepatitis B virus during an unrelated viral infection of the liver. Proc. Natl. Acad. Sci. U. S. A. 1996, 93, 4589–4594. [Google Scholar] [CrossRef]
- Kunz, S.; Rojek, J.M.; Roberts, A.J.; McGavern, D.B.; Oldstone, M.B.; de la Torre, J.C. Altered central nervous system gene expression caused by congenitally acquired persistent infection with lymphocytic choriomeningitis virus. J. Virol. 2006, 80, 9082–9092. [Google Scholar] [CrossRef]
- Mims, C.A.; Subrahmanyan, T.P. Immunofluorescence study of the mechanism of resistance to superinfection in mice carrying the lymphocytic choriomeningitis virus. J. Pathol. Bacteriol. 1966, 91, 403–415. [Google Scholar] [CrossRef] [PubMed]
- Hong Diet, N.; Libíková, H. Selective resistance to togaviral superinfection in mice with tolerant lymphocytic choriomeningitis virus infection. Acta Virol. 1979, 23, 385–392. [Google Scholar]
- Rivière, Y.; Gresser, I.; Guillon, J.C.; Tovey, M.G. Inhibition by anti-interferon serum of lymphocytic choriomeningitis virus disease in suckling mice. Proc. Natl. Acad. Sci. U. S. A. 1977, 74, 2135–2139. [Google Scholar] [CrossRef]
- Rivière, Y.; Gresser, I.; Guillon, J.C.; Bandu, M.T.; Ronco, P.; Morel-Maroger, L.; Verroust, P. Severity of lymphocytic choriomeningitis virus disease in different strains of suckling mice correlates with increasing amounts of endogenous interferon. J. Exp. Med. 1980, 152, 633–640. [Google Scholar] [CrossRef]
- Gresser, J.; Morel-Maroger, L.; Verroust, P.; Rivière, Y.; Guillon, J.C. Anti-interferon globulin inhibits the development of glomerulonephritis in mice infected at birth with lymphocytic choriomeningitis virus. Proc. Natl. Acad. Sci. U. S. A. 1978, 75, 3413–3416. [Google Scholar] [CrossRef]
- Woodrow, D.; Ronco, P.; Riviere, Y.; Moss, J.; Gresser, I.; Guillon, J.C.; Morel-Maroger, L.; Sloper, J.C.; Verroust, P. Severity of glomerulonephritis induced in different strains of suckling mice by infection with lymphocytic choriomeningitis virus: Correlation with amounts of endogenous interferon and circulating immune complexes. J. Pathol. 1982, 138, 325–336. [Google Scholar] [CrossRef]
- Garza, K.M.; Chan, S.M.; Suri, R.; Nguyen, L.T.; Odermatt, B.; Schoenberger, S.P.; Ohashi, P.S. Role of antigen-presenting cells in mediating tolerance and autoimmunity. J. Exp. Med. 2000, 191, 2021–2027. [Google Scholar] [CrossRef]
- Homann, D.; McGavern, D.B.; Oldstone, M.B. Visualizing the viral burden: Phenotypic and functional alterations of T cells and APCs during persistent infection. J. Immunol. 2004, 172, 6239–6250. [Google Scholar] [CrossRef] [PubMed]
- Jung, A.; Kato, H.; Kumagai, Y.; Kumar, H.; Kawai, T.; Takeuchi, O.; Akira, S. Lymphocytoid choriomeningitis virus activates plasmacytoid dendritic cells and induces a cytotoxic T-cell response via MyD88. J. Virol. 2008, 82, 196–206. [Google Scholar] [CrossRef] [PubMed]
- Diebold, S.S.; Montoya, M.; Unger, H.; Alexopoulou, L.; Roy, P.; Haswell, L.E.; Al-Shamkhani, A.; Flavell, R.; Borrow, P.; Reis e Sousa, C. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003, 424, 324–328. [Google Scholar] [CrossRef]
- Dalod, M.; Salazar-Mather, T.P.; Malmgaard, L.; Lewis, C.; Asselin-Paturel, C.; Brière, F.; Trinchieri, G.; Biron, C.A. Interferon alpha/beta and interleukin 12 responses to viral infections: Pathways regulating dendritic cell cytokine expression in vivo. J. Exp. Med. 2002, 195, 517–528. [Google Scholar] [CrossRef]
- Borrow, P.; Evans, C.F.; Oldstone, M.B. Virus-induced immunosuppression: Immune system-mediated destruction of virus-infected dendritic cells results in generalized immune suppression. J. Virol. 1995, 69, 1059–1070. [Google Scholar] [CrossRef] [PubMed]
- Müller, S.; Hunziker, L.; Enzler, S.; Bühler-Jungo, M.; Di Santo, J.P.; Zinkernagel, R.M.; Mueller, C. Role of an intact splenic microarchitecture in early lymphocytic choriomeningitis virus production. J. Virol. 2002, 76, 2375–2383. [Google Scholar] [CrossRef]
- Zhou, S.; Cerny, A.M.; Zacharia, A.; Fitzgerald, K.A.; Kurt-Jones, E.A.; Finberg, R.W. Induction and inhibition of type I interferon responses by distinct components of lymphocytic choriomeningitis virus. J. Virol. 2010, 84, 9452–9462. [Google Scholar] [CrossRef]
- Marq, J.B.; Kolakofsky, D.; Garcin, D. Unpaired 5' ppp-nucleotides, as found in arenavirus double-stranded RNA panhandles, are not recognized by RIG-I. J. Biol. Chem. 2010, 285, 18208–18216. [Google Scholar] [CrossRef] [PubMed]
- Kawagoe, T.; Sato, S.; Jung, A.; Yamamoto, M.; Matsui, K.; Kato, H.; Uematsu, S.; Takeuchi, O.; Akira, S. Essential role of IRAK-4 protein and its kinase activity in Toll-like receptor-mediated immune responses but not in TCR signaling. J. Exp. Med. 2007, 204, 1013–1024. [Google Scholar] [CrossRef] [PubMed]
- Lye, E.; Dhanji, S.; Calzascia, T.; Elford, A.R.; Ohashi, P.S. IRAK-4 kinase activity is required for IRAK-4-dependent innate and adaptive immune responses. Eur. J. Immunol. 2008, 38, 870–876. [Google Scholar] [CrossRef]
- Suzuki, N.; Suzuki, S.; Duncan, G.S.; Millar, D.G.; Wada, T.; Mirtsos, C.; Takada, H.; Wakeham, A.; Itie, A.; Li, S.; Penninger, J.M.; Wesche, H.; Ohashi, P.S.; Mak, T.W.; Yeh, W.C. Severe impairment of interleukin-1 and Toll-like receptor signalling in mice lacking IRAK-4. Nature 2002, 416, 750–756. [Google Scholar] [CrossRef] [PubMed]
- Zhou, S.; Halle, A.; Kurt-Jones, E.A.; Cerny, A.M.; Porpiglia, E.; Rogers, M.; Golenbock, D.T.; Finberg, R.W. Lymphocytic choriomeningitis virus (LCMV) infection of CNS glial cells results in TLR2-MyD88/Mal-dependent inflammatory responses. J. Neuroimmunol. 2008, 194, 70–82. [Google Scholar] [CrossRef]
- Edelmann, K.H.; Richardson-Burns, S.; Alexopoulou, L.; Tyler, K.L.; Flavell, R.A.; Oldstone, M.B. Does Toll-like receptor 3 play a biological role in virus infections? Virology 2004, 322, 231–238. [Google Scholar] [CrossRef]
- Sevilla, N.; McGavern, D.B.; Teng, C.; Kunz, S.; Oldstone, M.B. Viral targeting of hematopoietic progenitors and inhibition of DC maturation as a dual strategy for immune subversion. J. Clin. Invet. 2004, 113, 737–745. [Google Scholar] [CrossRef]
- Junt, T.; Scandella, E.; Förster, R.; Krebs, P.; Krautwald, S.; Lipp, M.; Hengartner, H.; Ludewig, B. Impact of CCR7 on priming and distribution of antiviral effector and memory CTL. J. Immunol. 2004, 173, 6684–6693. [Google Scholar] [CrossRef]
- Probst, H.C.; van den Broek, M. Priming of CTLs by lymphocytic choriomeningitis virus depends on dendritic cells. J. Immunol. 2005, 174, 3920–3924. [Google Scholar] [CrossRef]
- Belz, G.T.; Shortman, K.; Bevan, M.J.; Heath, W.R. CD8alpha+ dendritic cells selectively present MHC class I-restricted noncytolytic viral and intracellular bacterial antigens in vivo. J. Immunol. 2005, 175, 196–200. [Google Scholar] [CrossRef]
- Ruedl, C.; Kopf, M.; Bachmann, M.F. CD8(+) T cells mediate CD40-independent maturation of dendritic cells in vivo. J. Exp. Med. 1999, 189, 1875–1884. [Google Scholar] [CrossRef] [PubMed]
- Diana, J.; Griseri, T.; Lagaye, S.; Beaudoin, L.; Autrusseau, E.; Gautron, A.S.; Tomkiewicz, C.; Herbelin, A.; Barouki, R.; von Herrath, M.; Dalod, M.; Lehuen, A. NKT cell-plasmacytoid dendritic cell cooperation via OX40 controls viral infection in a tissue-specific manner. Immunity 2009, 30, 289–299. [Google Scholar] [CrossRef] [PubMed]
- Sevilla, N.; Kunz, S.; Holz, A.; Lewicki, H.; Homann, D.; Yamada, H.; Campbell, K.P.; de La Torre, J.C.; Oldstone, M.B. Immunosuppression and resultant viral persistence by specific viral targeting of dendritic cells. J. Exp. Med. 2000, 192, 1249–1260. [Google Scholar] [CrossRef]
- Kamath, A.T.; Pooley, J.; O’Keeffe, M.A.; Vremec, D.; Zhan, Y.; Lew, A.M.; D’Amico, A.; Wu, L.; Tough, D.F.; Shortman, K. The development, maturation, and turnover rate of mouse spleen dendritic cell populations. J. Immunol. 2000, 165, 6762–6770. [Google Scholar] [CrossRef]
- Bahl, K.; Hüebner, A.; Davis, R.J.; Welsh, R.M. Analysis of apoptosis of memory T cells and dendritic cells during the early stages of viral infection or exposure to toll-like receptor agonists. J. Virol. 2010, 84, 4866–4877. [Google Scholar] [CrossRef]
- Bro-Jorgensen, K.; Knudtzon, S. Changes in hemopoiesis during the course of acute LCM virus infection in mice. Blood 1977, 49, 47–57. [Google Scholar] [CrossRef] [PubMed]
- Binder, D.; Fehr, J.; Hengartner, H.; Zinkernagel, R.M. Virus-induced transient bone marrow aplasia: Major role of interferon-alpha/beta during acute infection with the noncytopathic lymphocytic choriomeningitis virus. J. Exp. Med. 1997, 185, 517–530. [Google Scholar] [CrossRef] [PubMed]
- Pozner, R.G.; Ure, A.E.; Jaquenod de Giusti, C.; D'Atri, L.P.; Italiano, J.E.; Torres, O.; Romanowski, V.; Schattner, M.; Gomez, R.M. Junin virus infection of human hematopoietic progenitors impairs in vitro proplatelet formation and platelet release via a bystander effect involving type I IFN signaling. PLoS Pathog. 2010, 6, e1000847. [Google Scholar] [CrossRef] [PubMed]
- Hahm, B.; Trifilo, M.J.; Zuniga, E.I.; Oldstone, M.B. Viruses evade the immune system through type I interferon-mediated STAT2-dependent, but STAT1-independent, signaling. Immunity 2005, 22, 247–257. [Google Scholar] [CrossRef]
- Tishon, A.; Borrow, P.; Evans, C.; Oldstone, M.B. Virus-induced immunosuppression. 1. Age at infection relates to a selective or generalized defect. Virology 1993, 195, 397–405. [Google Scholar] [CrossRef]
- Martínez-Sobrido, L.; Zúñiga, E.I.; Rosario, D.; García-Sastre, A.; de la Torre, J.C. Inhibition of the type I interferon response by the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 2006, 80, 9192–9199. [Google Scholar] [CrossRef] [PubMed]
- Martínez-Sobrido, L.; Giannakas, P.; Cubitt, B.; García-Sastre, A.; de la Torre, J.C. Differential inhibition of type I interferon induction by arenavirus nucleoproteins. J. Virol. 2007, 81, 12696–12703. [Google Scholar] [CrossRef] [PubMed]
- Fan, L.; Briese, T.; Lipkin, W.I. Z proteins of New World arenaviruses bind RIG-I and interfere with type I interferon induction. J. Virol. 2009, 84, 1785–1791. [Google Scholar] [CrossRef] [PubMed]
- Downs, W.G.; Anderson, C.R. Spence, L.; Aitken, T.H.G.; Greenhall, A.H. Tacaribe Virus, a New Agent Isolated from Artibeus Bats and Mosquitoes in Trinidad, West Indies. Am. J. Trop. Med. Hyg. 1963, 12, 640–646. [Google Scholar] [CrossRef] [PubMed]
- Hai, R.; Martinez-Sobrido, L.; Fraser, K.A.; Ayllon, J.; Garcia-Sastre, A.; Palese, P. Influenza B virus NS1-truncated mutants: Live-attenuated vaccine approach. J. Virol. 2008, 82, 10580–10590. [Google Scholar] [CrossRef]
- Kochs, G.; Garcia-Sastre, A.; Martinez-Sobrido, L. Multiple anti-interferon actions of the influenza A virus NS1 protein. J. Virol. 2007, 81, 7011–7021. [Google Scholar] [CrossRef]
- Mibayashi, M.; Martinez-Sobrido, L.; Loo, Y.M.; Cardenas, W.B.; Gale, M., Jr.; Garcia-Sastre, A. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 2007, 81, 514–524. [Google Scholar] [CrossRef]
- Basler, C.F.; Mikulasova, A.; Martinez-Sobrido, L.; Paragas, J.; Muhlberger, E.; Bray, M.; Klenk, H.D.; Palese, P.; Garcia-Sastre, A. The Ebola virus VP35 protein inhibits activation of interferon regulatory factor 3. J. Virol. 2003, 77, 7945–7956. [Google Scholar] [CrossRef]
- Lee, K.J.; Novella, I.S.; Teng, M.N.; Oldstone, M.B.; de La Torre, J.C. NP and L proteins of lymphocytic choriomeningitis virus (LCMV) are sufficient for efficient transcription and replication of LCMV genomic RNA analogs. J. Virol. 2000, 74, 3470–3477. [Google Scholar] [CrossRef]
- Martinez-Sobrido, L.; Emonet, S.; Giannakas, P.; Cubitt, B.; Garcia-Sastre, A.; de la Torre, J.C. Identification of amino acid residues critical for the anti-interferon activity of the nucleoprotein of the prototypic arenavirus lymphocytic choriomeningitis virus. J. Virol. 2009, 83, 11330–11340. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2010 by the authors; licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution license (http://creativecommons.org/licenses/by/3.0/).
Share and Cite
Borrow, P.; Martínez-Sobrido, L.; De la Torre, J.C. Inhibition of the Type I Interferon Antiviral Response During Arenavirus Infection. Viruses 2010, 2, 2443-2480. https://doi.org/10.3390/v2112443
Borrow P, Martínez-Sobrido L, De la Torre JC. Inhibition of the Type I Interferon Antiviral Response During Arenavirus Infection. Viruses. 2010; 2(11):2443-2480. https://doi.org/10.3390/v2112443
Chicago/Turabian StyleBorrow, Persephone, Luis Martínez-Sobrido, and Juan Carlos De la Torre. 2010. "Inhibition of the Type I Interferon Antiviral Response During Arenavirus Infection" Viruses 2, no. 11: 2443-2480. https://doi.org/10.3390/v2112443