Induction and control of the type I interferon pathway by Bluetongue virus

Virus Research

Volumn 182, Issue , 2014, Pages 59-70

  Vitour, Damien ^a   Doceul, Virginie ^a   Ruscanu, Suzana ^b   Chauveau, Emilie ^a   Schwartz Cornil, Isabelle ^b   Zientara, Stéphan ^a  

^a ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^b INRA Institut National de la Recherche Agronomique   (France)

Author keywords

BTV; Immune evasion; Interferon synthesis

Indexed keywords

BETA INTERFERON; MYELOID DIFFERENTIATION FACTOR 88; NONSTRUCTURAL PROTEIN 3; PROTEIN; PROTEIN MDA5; RETINOIC ACID INDUCIBLE PROTEIN I; RNA HELICASE; STRESS ACTIVATED PROTEIN KINASE; TOLL LIKE RECEPTOR 7; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; B LYMPHOCYTE; BLUETONGUE ORBIVIRUS; HUMAN; INNATE IMMUNITY; INTERFERON PRODUCTION; NONHUMAN; PLASMACYTOID DENDRITIC CELL; PRIORITY JOURNAL; T LYMPHOCYTE; VIRUS IMMUNITY;

ARBOVIRUS; BLUETONGUE VIRUS; OVIS ARIES;

BTV; IMMUNE EVASION; INTERFERON SYNTHESIS;

ANIMALS; BLUETONGUE VIRUS; IMMUNE EVASION; INTERFERON TYPE I; RECEPTORS, IMMUNOLOGIC; SHEEP; SIGNAL TRANSDUCTION;

EID: 84896315379     PISSN: 01681702     EISSN: 18727492     Source Type: Journal    
DOI: 10.1016/j.virusres.2013.10.027     Document Type: Article

References (214)

1. Abramovich C., Shulman L.M., et al. Differential tyrosine phosphorylation of the IFNAR chain of the type I interferon receptor and of an associated surface protein in response to IFN-alpha and IFN-beta. EMBO J. 1994, 13(24):5871-5877.
2. Akira S. TLR signaling. Curr. Top. Microbiol. Immunol. 2006, 311:1-16.
3. Akira S., Uematsu S., et al. Pathogen recognition and innate immunity. Cell 2006, 124(4):783-801.
4. Alexopoulou L., Holt A.C., et al. Recognition of double-stranded RNA and activation of NF-kappaB by Toll-like receptor 3. Nature 2001, 413(6857):732-738.
5. Andrejeva J., Childs K.S., et al. 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(49):17264-17269.
6. Ank N., West H., et al. IFN-lambda: novel antiviral cytokines. J. Interferon Cytokine Res. 2006, 26(6):373-379.
7. Arimoto K., Takahashi H., et al. Negative regulation of the RIG-I signaling by the ubiquitin ligase RNF125. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(18):7500-7505.
8. Arnoult D., Carneiro L., et al. The role of mitochondria in cellular defense against microbial infection. Semin. Immunol. 2009, 21(4):223-232.
9. Barro M., Patton J.T. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(11):4114-4119.
10. Barro M., Patton J.T. Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J. Virol. 2007, 81(9):4473-4481.
11. Beadling C., Guschin D., et al. Activation of JAK kinases and STAT proteins by interleukin-2 and interferon alpha, but not the T cell antigen receptor, in human T lymphocytes. EMBO J. 1994, 13(23):5605-5615.
12. Berke I.C., Modis Y. MDA5 cooperatively forms dimers and ATP-sensitive filaments upon binding double-stranded RNA. EMBO J. 2012, 31(7):1714-1726.
13. Beutler B.A. TLRs and innate immunity. Blood 2009, 113(7):1399-1407.
14. Bhanja Chowdhury J., Shrivastava S., et al. Hepatitis C virus infection modulates expression of interferon stimulatory gene IFITM1 by upregulating miR-130A. J. Virol. 2012, 86(18):10221-10225.
15. Boehme K.W., Guerrero M., et al. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 2006, 177(10):7094-7102.
16. Bonjardim C.A. Interferons (IFNs) are key cytokines in both innate and adaptive antiviral immune responses - and viruses counteract IFN action. Microbes Infect. 2005, 7(3):569-578.
17. Bonjardim C.A., Ferreira P.C., et al. Interferons: signaling, antiviral and viral evasion. Immunol. Lett. 2009, 122(1):1-11.
18. Bowie A.G., Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 2008, 8(12):911-922.
19. Broquet A.H., Hirata Y., et al. RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. J. Immunol. 2011, 186(3):1618-1626.
20. Calvo-Pinilla E., Navasa N., et al. Multiserotype protection elicited by a combinatorial prime-boost vaccination strategy against Bluetongue virus. PLoS ONE 2012, 7(4):e34735.
21. Calvo-Pinilla E., Nieto J.M., et al. Experimental oral infection of Bluetongue virus serotype 8 in type I interferon receptor-deficient mice. J. Gen. Virol. 2010, 91(Pt 11):2821-2825.
22. Calvo-Pinilla E., Rodriguez-Calvo T., et al. Establishment of a Bluetongue virus infection model in mice that are deficient in the alpha/beta interferon receptor. PLoS ONE 2009, 4(4):e5171.
23. Calvo-Pinilla E., Rodriguez-Calvo T., et al. Heterologous prime boost vaccination with DNA and recombinant modified vaccinia virus Ankara protects IFNAR(-/-) mice against lethal Bluetongue infection. Vaccine 2009, 28(2):437-445.
24. Caporale M., Wash R., et al. Determinants of Bluetongue virus virulence in murine models of disease. J. Virol. 2011, 85(21):11479-11489.
25. Chauveau E., Doceul V., et al. Sensing and control of Bluetongue virus infection in epithelial cells via RIG-I and MDA5 helicases. J. Virol. 2012, 86(21):11789-11799.
26. Chauveau E., Doceul V., et al. NS3 of Bluetongue virus interferes with the induction of type I interferon. J. Virol. 2013, 87(14):8241-8246.
27. Chen Z., Benureau Y., et al. GB virus B disrupts RIG-I signaling by NS3/4A-mediated cleavage of the adaptor protein MAVS. J. Virol. 2007, 81(2):964-976.
28. Childs K., Stock N., et al. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 2007, 359(1):190-200.
29. Clementz M.A., Chen Z., et al. Deubiquitinating and interferon antagonism activities of coronavirus papain-like proteases. J. Virol. 2010, 84(9):4619-4629.
30. Coen M.L., Ellis J.A., et al. Cytokine modulation of the interaction between Bluetongue virus and endothelial cells in vitro. Vet. Pathol. 1991, 28(6):524-532.
31. Colamonici O., Yan H., et al. Direct binding to and tyrosine phosphorylation of the alpha subunit of the type I interferon receptor by p135tyk2 tyrosine kinase. Mol. Cell. Biol. 1994, 14(12):8133-8142.
32. Colamonici O.R., Domanski P., et al. Vaccinia virus B18R gene encodes a type I interferon-binding protein that blocks interferon alpha transmembrane signaling. J. Biol. Chem. 1995, 270(27):15974-15978.
33. Colamonici O.R., Uyttendaele H., et al. p135tyk2, an interferon-alpha-activated tyrosine kinase, is physically associated with an interferon-alpha receptor. J. Biol. Chem. 1994, 269(5):3518-3522.
34. Cui S., Eisenacher K., et al. The C-terminal regulatory domain is the RNA 5'-triphosphate sensor of RIG-I. Mol. Cell 2008, 29(2):169-179.
35. de Weerd N.A., Samarajiwa S.A., et al. Type I interferon receptors: biochemistry and biological functions. J. Biol. Chem. 2007, 282(28):20053-20057.
36. Deal E.M., Lahl K., et al. Plasmacytoid dendritic cells promote rotavirus-induced human and murine B cell responses. J. Clin. Invest. 2013, 123(6):2464-2474.
37. DeMaula C.D., Jutila M.A., et al. Infection kinetics, prostacyclin release and cytokine-mediated modulation of the mechanism of cell death during Bluetongue virus infection of cultured ovine and bovine pulmonary artery and lung microvascular endothelial cells. J. Gen. Virol. 2001, 82(Pt 4):787-794.
38. DeMaula C.D., Leutenegger C.M., et al. The role of endothelial cell-derived inflammatory and vasoactive mediators in the pathogenesis of Bluetongue. Virology 2002, 296(2):330-337.
39. Diebold S.S., Montoya M., et al. Viral infection switches non-plasmacytoid dendritic cells into high interferon producers. Nature 2003, 424(6946):324-328.
40. Dong B., Silverman R.H. 2-5A-dependent RNase molecules dimerize during activation by 2-5A. J. Biol. Chem. 1995, 270(8):4133-4137.
41. Eisenacher K., Steinberg C., et al. The role of viral nucleic acid recognition in dendritic cells for innate and adaptive antiviral immunity. Immunobiology 2008, 212(9-10):701-714.
42. Eksteen P.A., Huismans H. Interferon induction by Bluetongue virus and Bluetongue virus ribonucleic acid. Onderstepoort J. Vet. Res. 1972, 39(3):125-131.
43. Fasler-Kan E., Pansky A., et al. Interferon-alpha activates signal transducers and activators of transcription 5 and 6 in Daudi cells. Eur. J. Biochem. 1998, 254(3):514-519.
44. Fejer G., Drechsel L., et al. Key role of splenic myeloid DCs in the IFN-alphabeta response to adenoviruses in vivo. PLoS Pathog. 2008, 4(11):e1000208.
45. Fiette L., Aubert C., et al. Theiler's virus infection of 129Sv mice that lack the interferon alpha/beta or interferon gamma receptors. J. Exp. Med. 1995, 181(6):2069-2076.
46. Fiola S., Gosselin D., et al. TLR9 contributes to the recognition of EBV by primary monocytes and plasmacytoid dendritic cells. J. Immunol. 2010, 185(6):3620-3631.
47. Foster N.M., Luedke A.J., et al. Temporal relationships of viremia, interferon activity, and antibody responses of sheep infected with several Bluetongue virus strains. Am. J. Vet. Res. 1991, 52(2):192-196.
48. Fredericksen B.L., Gale M. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J. Virol. 2006, 80(6):2913-2923.
49. Fu X.Y., Schindler C., et al. The proteins of ISGF-3, the interferon alpha-induced transcriptional activator, define a gene family involved in signal transduction. Proc. Natl. Acad. Sci. U. S. A. 1992, 89(16):7840-7843.
50. Fulton R.W., Pearson N.J. Interferon induction in bovine and feline monolayer cultures by four Bluetongue virus serotypes. Can. J. Comp. Med. 1982, 46(1):100-102.
51. Gack M.U., Shin Y.C., et al. TRIM25 RING-finger E3 ubiquitin ligase is essential for RIG-I-mediated antiviral activity. Nature 2007, 446(7138):916-920.
52. Garcia M.A., Meurs E.F., et al. The dsRNA protein kinase PKR: virus and cell control. Biochimie 2007, 89(6-7):799-811.
53. Gauzzi M.C., Velazquez L., et al. Interferon-alpha-dependent activation of Tyk2 requires phosphorylation of positive regulatory tyrosines by another kinase. J. Biol. Chem. 1996, 271(34):20494-20500.
54. Gilfoy F.D., Mason P.W. West Nile virus-induced interferon production is mediated by the double-stranded RNA-dependent protein kinase PKR. J. Virol. 2007, 81(20):11148-11158.
55. Gitlin L., Barchet W., et al. Essential role of mda-5 in type I IFN responses to polyriboinosinic:polyribocytidylic acid and encephalomyocarditis picornavirus. Proc. Natl. Acad. Sci. U. S. A. 2006, 103(22):8459-8464.
56. Goh K.C., deVeer M.J., et al. The protein kinase PKR is required for p38 MAPK activation and the innate immune response to bacterial endotoxin. EMBO J. 2000, 19(16):4292-4297.
57. Gonzalez-Lopez C., Martinez-Costas J., et al. Evidence that avian reovirus sigmaA protein is an inhibitor of the double-stranded RNA-dependent protein kinase. J. Gen. Virol. 2003, 84(Pt 6):1629-1639.
58. Goodman A.G., Smith J.A., et al. The cellular protein P58IPK regulates influenza virus mRNA translation and replication through a PKR-mediated mechanism. J. Virol. 2007, 81(5):2221-2230.
59. Guzylack-Piriou L., Bergamin F., et al. Plasmacytoid dendritic cell activation by foot-and-mouth disease virus requires immune complexes. Eur. J. Immunol. 2006, 36(7):1674-1683.
60. Hacker H., Redecke V., et al. Specificity in Toll-like receptor signalling through distinct effector functions of TRAF3 and TRAF6. Nature 2006, 439(7073):204-207.
61. Haller O., Kochs G., et al. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 2006, 344(1):119-130.
62. Haller O., Kochs G., et al. Interferon, Mx, and viral countermeasures. Cytokine Growth Factor Rev. 2007, 18(5-6):425-433.
63. Haller O., Stertz S., et al. The Mx GTPase family of interferon-induced antiviral proteins. Microbes Infect. 2007, 9(14-15):1636-1643.
64. Hansen T.R., Henkes L.K., et al. Endocrine actions of interferon-tau in ruminants. Soc. Reprod. Fertil. Suppl. 2010, 67:325-340.
65. Hardarson H.S., Baker J.S., et al. Toll-like receptor 3 is an essential component of the innate stress response in virus-induced cardiac injury. Am. J. Physiol. Heart Circ. Physiol. 2007, 292(1):H251-H258.
66. Harte M.T., Haga I.R., et al. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med. 2003, 197(3):343-351.
67. Heil F., Hemmi H., et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science 2004, 303(5663):1526-1529.
68. Hemati B., Contreras V., et al. Bluetongue virus targets conventional dendritic cells in skin lymph. J. Virol. 2009, 83(17):8789-8799.
69. Hemmi H., Takeuchi O., et al. A Toll-like receptor recognizes bacterial DNA. Nature 2000, 408(6813):740-745.
70. Hervas-Stubbs S., Perez-Gracia J.L., et al. Direct effects of type I interferons on cells of the immune system. Clin. Cancer Res. 2011, 17(9):2619-2627.
71. Hiscott J. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 2007, 282(21):15325-15329.
72. Hochrein H., Schlatter B., et al. Herpes simplex virus type-1 induces IFN-alpha production via Toll-like receptor 9-dependent and -independent pathways. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(31):11416-11421.
73. Hoenen A., Liu W., et al. West Nile virus-induced cytoplasmic membrane structures provide partial protection against the interferon-induced antiviral MxA protein. J. Gen. Virol. 2007, 88(Pt 11):3013-3017.
74. Holloway G., Truong T.T., et al. Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-kappaB. J. Virol. 2009, 83(10):4942-4951.
75. Honda K., Yanai H., et al. IRF-7 is the master regulator of type-I interferon-dependent immune responses. Nature 2005, 434(7034):772-777.
76. Hornung V., Ellegast J., et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314(5801):994-997.
77. Hornung V., Schlender J., et al. Replication-dependent potent IFN-alpha induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J. Immunol. 2004, 173(10):5935-5943.
78. Huber J.P., Farrar J.D. Regulation of effector and memory T-cell functions by type I interferon. Immunology 2011, 132(4):466-474.
79. Huismans H. Bluetongue virus-induced interferon synthesis. Onderstepoort J. Vet. Res. 1969, 36(2):181-185.
80. Imani F., Jacobs B.L. Inhibitory activity for the interferon-induced protein kinase is associated with the reovirus serotype 1 sigma 3 protein. Proc. Natl. Acad. Sci. U. S. A. 1988, 85(21):7887-7891.
81. Isaacs A., Lindenmann J. Virus interference. I. The interferon. Proc. R. Soc. Lond. B: Biol. Sci. 1957, 147(927):258-267.
82. Ishikawa H., Barber G.N. STING is an endoplasmic reticulum adaptor that facilitates innate immune signalling. Nature 2008, 455(7213):674-678.
83. Jacobs B.L., Langland J.O. Reovirus sigma 3 protein: dsRNA binding and inhibition of RNA-activated protein kinase. Curr. Top. Microbiol. Immunol. 1998, 233(Pt 1):185-196.
84. Jameson P., Grossberg S.E. Production of interferon in human cell cultures by a new, potent viral inducer. Adv. Exp. Med. Biol. 1978, 110:37-53.
85. Jameson P., Grossberg S.E. Production of interferon by human tumor cell lines. Arch. Virol 1979, 62(3):209-219.
86. Jameson P., Grossberg S.E. Induction of interferon with Bluetongue virus in various cells. Methods Enzymol. 1981, 78(Pt A):254-258.
87. Jameson P., Schoenherr C.K., et al. Bluetongue virus, an exceptionally potent interferon inducer in mice. Infect. Immun. 1978, 20(1):321-323.
88. Joklik W.K. Induction of interferon by nonmultiplying virus. Methods Enzymol. 1981, 79(Pt B):330-336.
89. Kaisho T., Akira S. Toll-like receptor function and signaling. J. Allergy Clin. Immunol. 2006, 117(5):979-987. (quiz 988).
90. Kato H., Sato S., et al. Cell type-specific involvement of RIG-I in antiviral response. Immunity 2005, 23(1):19-28.
91. Kato H., Takeuchi O., et al. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 2008, 205(7):1601-1610.
92. Kato H., Takeuchi O., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441(7089):101-105.
93. Kawai T., Akira S. Antiviral signaling through pattern recognition receptors. J. Biochem. (Tokyo) 2007, 141(2):137-145.
94. Kawai T., Sato S., et al. Interferon-alpha induction through Toll-like receptors involves a direct interaction of IRF7 with MyD88 and TRAF6. Nat. Immunol. 2004, 5(10):1061-1068.
95. Kawai T., Takahashi K., et al. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 6(10):981-988.
96. Kiefer K., Oropallo M.A., et al. Role of type I interferons in the activation of autoreactive B cells. Immunol. Cell Biol. 2012, 90(5):498-504.
97. Kim T., Pazhoor S., et al. Aspartate-glutamate-alanine-histidine box motif (DEAH)/RNA helicase A helicases sense microbial DNA in human plasmacytoid dendritic cells. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(34):15181-15186.
98. Kolakofsky D., Kowalinski E., et al. A structure-based model of RIG-I activation. RNA 2012, 18(12):2118-2127.
99. Komuro A., Horvath C.M. RNA- and virus-independent inhibition of antiviral signaling by RNA helicase LGP2. J. Virol. 2006, 80(24):12332-12342.
100. Kotenko S.V. IFN-lambdas. Curr. Opin. Immunol. 2011, 23(5):583-590.
101. Krishnan K., Yan H., et al. Dimerization of a chimeric CD4-interferon-alpha receptor reconstitutes the signaling events preceding STAT phosphorylation. Oncogene 1996, 13(1):125-133.
102. Kurt-Jones E.A., Popova L., et al. Pattern recognition receptors TLR4 and CD14 mediate response to respiratory syncytial virus. Nat. Immunol. 2000, 1(5):398-401.
103. Lamken P., Lata S., et al. Ligand-induced assembling of the type I interferon receptor on supported lipid bilayers. J. Mol. Biol. 2004, 341(1):303-318.
104. Lee H.R., Kim M.H., et al. Viral interferon regulatory factors. J. Interferon Cytokine Res. 2009, 29(9):621-627.
105. Lee T.G., Tomita J., et al. Purification and partial characterization of a cellular inhibitor of the interferon-induced protein kinase of Mr 68,000 from influenza virus-infected cells. Proc. Natl. Acad. Sci. U. S. A. 1990, 87(16):6208-6212.
106. Lee T.G., Tomita J., et al. Characterization and regulation of the 58,000-dalton cellular inhibitor of the interferon-induced, dsRNA-activated protein kinase. J. Biol. Chem. 1992, 267(20):14238-14243.
107. Lin R., Genin P., et al. HHV-8 encoded vIRF-1 represses the interferon antiviral response by blocking IRF-3 recruitment of the CBP/p300 coactivators. Oncogene 2001, 20(7):800-811.
108. Liu K., Yang X., et al. Rotavirus strategies to evade host antiviral innate immunity. Immunol. Lett. 2009, 127(1):13-18.
109. Liu S.Y., Sanchez D.J., et al. New developments in the induction and antiviral effectors of type I interferon. Curr. Opin. Immunol. 2011, 23(1):57-64.
110. Loiarro M., Sette C., et al. Peptide-mediated interference of TIR domain dimerization in MyD88 inhibits interleukin-1-dependent activation of NF-{kappa}B. J. Biol. Chem. 2005, 280(16):15809-15814.
111. Lu C., Xu H., et al. The structural basis of 5' triphosphate double-stranded RNA recognition by RIG-I C-terminal domain. Structure 2010, 18(8):1032-1043.
112. Luber C.A., Cox J., et al. Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 2010, 32(2):279-289.
113. Lubyova B., Kellum M.J., et al. Kaposi's sarcoma-associated herpesvirus-encoded vIRF-3 stimulates the transcriptional activity of cellular IRF-3 and IRF-7. J. Biol. Chem. 2004, 279(9):7643-7654.
114. Lund J., Sato A., et al. Toll-like receptor 9-mediated recognition of Herpes simplex virus-2 by plasmacytoid dendritic cells. J. Exp. Med. 2003, 198(3):513-520.
115. Lyons S.F., Schoub B.D., et al. Induction of interferon by Sendai virus versus blue tongue virus. J. Interferon Res. 1982, 2(4):543-547.
116. MacLachlan N.J., Schore C.E., et al. Antiviral responses of Bluetongue virus-inoculated bovine fetuses and their dams. Am. J. Vet. Res. 1984, 45(7):1469-1473.
117. MacLachlan N.J., Thompson J. Bluetongue virus-induced interferon in cattle. Am. J. Vet. Res. 1985, 46(6):1238-1241.
118. Malathi K., Dong B., et al. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 2007, 448(7155):816-819.
119. Marques J.T., Devosse T., et al. A structural basis for discriminating between self and nonself double-stranded RNAs in mammalian cells. Nat. Biotechnol. 2006, 24(5):559-565.
120. Martinand C., Montavon C., et al. RNase L inhibitor is induced during human immunodeficiency virus type 1 infection and down regulates the 2-5A/RNase L pathway in human T cells. J. Virol. 1999, 73(1):290-296.
121. Martinand C., Salehzada T., et al. RNase L inhibitor (RLI) antisense constructions block partially the down regulation of the 2-5A/RNase L pathway in encephalomyocarditis-virus-(EMCV)-infected cells. Eur. J. Biochem. 1998, 254(2):248-255.
122. Martinez-Costas J., Gonzalez-Lopez C., et al. Possible involvement of the double-stranded RNA-binding core protein sigmaA in the resistance of avian reovirus to interferon. J. Virol. 2000, 74(3):1124-1131.
123. Matikainen S., Sareneva T., et al. Interferon-alpha activates multiple STAT proteins and upregulates proliferation-associated IL-2Ralpha, c-myc, and pim-1 genes in human T cells. Blood 1999, 93(6):1980-1991.
124. McAllister C.S., Samuel C.E. The RNA-activated protein kinase enhances the induction of interferon-beta and apoptosis mediated by cytoplasmic RNA sensors. J. Biol. Chem. 2009, 284(3):1644-1651.
125. Meinke A., Barahmand-Pour F., et al. Activation of different Stat5 isoforms contributes to cell-type-restricted signaling in response to interferons. Mol. Cell. Biol. 1996, 16(12):6937-6944.
126. Melroe G.T., Silva L., et al. Recruitment of activated IRF-3 and CBP/p300 to herpes simplex virus ICP0 nuclear foci: potential role in blocking IFN-beta induction. Virology 2007, 360(2):305-321.
127. Melville M.W., Tan S.L., et al. The cellular inhibitor of the PKR protein kinase, P58(IPK), is an influenza virus-activated co-chaperone that modulates heat shock protein 70 activity. J. Biol. Chem. 1999, 274(6):3797-3803.
128. Meurs E., Chong K., et al. Molecular cloning and characterization of the human double-stranded RNA-activated protein kinase induced by interferon. Cell 1990, 62(2):379-390.
129. Meylan E., Curran J., et al. Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 2005, 437(7062):1167-1172.
130. Mibayashi M., Martinez-Sobrido L., et al. Inhibition of retinoic acid-inducible gene I-mediated induction of beta interferon by the NS1 protein of influenza A virus. J. Virol. 2007, 81(2):514-524.
131. Muller U., Steinhoff U., et al. Functional role of type I and type II interferons in antiviral defense. Science 1994, 264(5167):1918-1921.
132. Nguyen K.B., Salazar-Mather T.P., et al. Coordinated and distinct roles for IFN-alpha beta, IL-12, and IL-15 regulation of NK cell responses to viral infection. J. Immunol. 2002, 169(8):4279-4287.
133. O'Neill L.A., Bowie A.G. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 2007, 7(5):353-364.
134. Oganesyan G., Saha S.K., et al. Critical role of TRAF3 in the Toll-like receptor-dependent and -independent antiviral response. Nature 2006, 439(7073):208-211.
135. Panne D., Maniatis T., et al. An atomic model of the interferon-beta enhanceosome. Cell 2007, 129(6):1111-1123.
136. Pascale F., Contreras V., et al. Plasmacytoid dendritic cells migrate in afferent skin lymph. J. Immunol. 2008, 180(9):5963-5972.
137. Pauli E.K., Schmolke M., et al. Influenza A virus inhibits type I IFN signaling via NF-kappaB-dependent induction of SOCS-3 expression. PLoS Pathog. 2008, 4(11):e1000196.
138. Pestka S., Krause C.D., et al. Interferons, interferon-like cytokines, and their receptors. Immunol. Rev. 2004, 202:8-32.
139. Pichlmair A., Schulz O., et al. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314(5801):997-1001.
140. Platanias L.C. Mechanisms of type-I- and type-II-interferon-mediated signalling. Nat. Rev. Immunol. 2005, 5(5):375-386.
141. Platanias L.C., Colamonici O.R. Interferon alpha induces rapid tyrosine phosphorylation of the alpha subunit of its receptor. J. Biol. Chem. 1992, 267(33):24053-24057.
142. Platanias L.C., Uddin S., et al. Tyrosine phosphorylation of the alpha and beta subunits of the type I interferon receptor. Interferon-beta selectively induces tyrosine phosphorylation of an alpha subunit-associated protein. J. Biol. Chem. 1994, 269(27):17761-17764.
143. Plumet S., Herschke F., et al. Cytosolic 5'-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS ONE 2007, 2(3):e279.
144. Pothlichet J., Chignard M., et al. Cutting edge: innate immune response triggered by influenza A virus is negatively regulated by SOCS1 and SOCS3 through a RIG-I/IFNAR1-dependent pathway. J. Immunol. 2008, 180(4):2034-2038.
145. Qin L., Ren L., et al. Rotavirus nonstructural protein 1 antagonizes innate immune response by interacting with retinoic acid inducible gene I. Virol. J. 2011, 8:526.
146. Randall R.E., Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 2008, 89(Pt 1):1-47.
147. Ratinier M., Caporale M., et al. Identification and characterization of a novel non-structural protein of Bluetongue virus. PLoS Pathog. 2011, 7(12):e1002477.
148. Rehwinkel J., Tan C.P., et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010, 140(3):397-408.
149. Ren J., Kolli D., et al. Human metapneumovirus inhibits IFN-beta signaling by downregulating Jak1 and Tyk2 cellular levels. PLoS ONE 2011, 6(9):e24496.
150. Rinaldo C.R., Overall J.C., et al. Viral replication and interferon production in fetal and adult ovine leukocytes and spleen cells. Infect. Immun. 1975, 12(5):1070-1077.
151. Roberts R.M., Liu L., et al. The evolution of the type I interferons. J. Interferon Cytokine Res. 1998, 18(10):805-816.
152. Rothenfusser S., Goutagny N., et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acid-inducible gene-I. J. Immunol. 2005, 175(8):5260-5268.
153. Ruscanu S., Jouneau L., et al. Dendritic cell subtypes from lymph nodes and blood show contrasted gene expression programs upon Bluetongue virus infection. J. Virol. 2013, 87(16):9333-9343.
154. Ruscanu S., Pascale F., et al. The double-stranded RNA Bluetongue virus induces type I interferon in plasmacytoid dendritic cells via a MYD88-dependent TLR7/8-independent signaling pathway. J. Virol. 2012, 86(10):5817-5828.
155. Russell H., O'Toole D.T., et al. Comparative effects of Bluetongue virus infection of ovine and bovine endothelial cells. Vet. Pathol. 1996, 33(3):319-331.
156. Ryzhakov G., Randow F. SINTBAD, a novel component of innate antiviral immunity, shares a TBK1-binding domain with NAP1 and TANK. EMBO J. 2007, 26(13):3180-3190.
157. Saha S.K., Pietras E.M., et al. Regulation of antiviral responses by a direct and specific interaction between TRAF3 and Cardif. EMBO J. 2006, 25(14):3257-3263.
158. Saito T., Gale M. Differential recognition of double-stranded RNA by RIG-I-like receptors in antiviral immunity. J. Exp. Med. 2008, 205(7):1523-1527.
159. Saito T., Hirai R., et al. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(2):582-587.
160. Saito T., Owen D.M., et al. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008, 454(7203):523-527.
161. Satoh T., Kato H., et al. LGP2 is a positive regulator of RIG-I- and MDA5-mediated antiviral responses. Proc. Natl. Acad. Sci. U. S. A. 2010, 107(4):1512-1517.
162. Schindler C., Shuai K., et al. Interferon-dependent tyrosine phosphorylation of a latent cytoplasmic transcription factor. Science 1992, 257(5071):809-813.
163. Schmidt A., Schwerd T., et al. 5'-Triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(29):12067-12072.
164. Schoggins J.W., Wilson S.J., et al. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 2011, 472(7344):481-485.
165. Schroder K., Hertzog P.J., et al. Interferon-gamma: an overview of signals, mechanisms and functions. J. Leukoc. Biol. 2004, 75(2):163-189.
166. Schulz O., Pichlmair A., et al. Protein kinase R contributes to immunity against specific viruses by regulating interferon mRNA integrity. Cell Host Microbe 2010, 7(5):354-361.
167. Sen A., Pruijssers A.J., et al. The early interferon response to rotavirus is regulated by PKR and depends on MAVS/IPS-1, RIG-I, MDA-5, and IRF3. J. Virol. 2011, 85(8):3717-3732.
168. Seth R.B., Sun L., et al. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 2005, 122(5):669-682.
169. Shuai K., Liu B. Regulation of JAK-STAT signalling in the immune system. Nat. Rev. Immunol. 2003, 3(11):900-911.
170. Silvennoinen O., Ihle J.N., et al. Interferon-induced nuclear signalling by Jak protein tyrosine kinases. Nature 1993, 366(6455):583-585.
171. Smith E.J., Marie I., et al. IRF3 and IRF7 phosphorylation in virus-infected cells does not require double-stranded RNA-dependent protein kinase R or Ikappa B kinase but is blocked by Vaccinia virus E3L protein. J. Biol. Chem. 2001, 276(12):8951-8957.
172. Sommereyns C., Paul S., et al. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 2008, 4(3):e1000017.
173. Stack J., Haga I.R., et al. Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J. Exp. Med. 2005, 201(6):1007-1018.
174. Stetson D.B., Medzhitov R. Type I interferons in host defense. Immunity 2006, 25(3):373-381.
175. Stewart M.E., Roy P. Role of cellular caspases, nuclear factor-kappa B and interferon regulatory factors in Bluetongue virus infection and cell fate. Virol. J. 2010, 7:362.
176. Symons J.A., Alcami A., et al. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell 1995, 81(4):551-560.
177. Tabeta K., Georgel P., et al. Toll-like receptors 9 and 3 as essential components of innate immune defense against mouse cytomegalovirus infection. Proc. Natl. Acad. Sci. U. S. A. 2004, 101(10):3516-3521.
178. Takahasi K., Kumeta H., et al. Solution structures of cytosolic RNA sensor MDA5 and LGP2 C-terminal domains: identification of the RNA recognition loop in RIG-I-like receptors. J. Biol. Chem. 2009, 284(26):17465-17474.
179. Takahasi K., Yoneyama M., et al. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 2008, 29(4):428-440.
180. Takeda K., Akira S. Toll-like receptors in innate immunity. Int. Immunol. 2005, 17(1):1-14.
181. Taylor D.R., Shi S.T., et al. Inhibition of the interferon-inducible protein kinase PKR by HCV E2 protein. Science 1999, 285(5424):107-110.
182. Taylor J.L., O'Brien W.J. Interferon production and sensitivity of rabbit corneal epithelial and stromal cells. Invest. Ophthalmol. Vis. Sci. 1985, 26(11):1502-1508.
183. Taylor K.E., Mossman K.L. Recent advances in understanding viral evasion of type I interferon. Immunology 2012.
184. Thompson A.J., Locarnini S.A. Toll-like receptors, RIG-I-like RNA helicases and the antiviral innate immune response. Immunol. Cell Biol. 2007, 85(6):435-445.
185. Torpey N., Maher S.E., et al. Interferon alpha but not interleukin 12 activates STAT4 signaling in human vascular endothelial cells. J. Biol. Chem. 2004, 279(25):26789-26796.
186. Tough D.F. Modulation of T-cell function by type I interferon. Immunol. Cell Biol. 2012, 90(5):492-497.
187. Tytell A.A., Lampson G.P., et al. Inducers of interferon and host resistance. 3. Double-stranded RNA from reovirus type 3 virions (reo 3-RNA). Proc. Natl. Acad. Sci. U. S. A. 1967, 58(4):1719-1722.
188. Uddin S., Chamdin A., et al. Interaction of the transcriptional activator Stat-2 with the type I interferon receptor. J. Biol. Chem. 1995, 270(42):24627-24630.
189. Ullman A.J., Hearing P. Cellular proteins PML and Daxx mediate an innate antiviral defense antagonized by the adenovirus E4 ORF3 protein. J. Virol. 2008, 82(15):7325-7335.
190. Ullman A.J., Reich N.C., et al. Adenovirus E4 ORF3 protein inhibits the interferon-mediated antiviral response. J. Virol. 2007, 81(9):4744-4752.
191. Unterholzner L. The interferon response to intracellular DNA: why so many receptors?. Immunobiology 2013, 218(11):1312-1321.
192. Unterholzner L., Bowie A.G. The interplay between viruses and innate immune signaling: recent insights and therapeutic opportunities. Biochem. Pharmacol. 2008, 75(3):589-602.
193. Unterstab G., Ludwig S., et al. Viral targeting of the interferon-{beta}-inducing Traf family member-associated NF-{kappa}B activator (TANK)-binding kinase-1. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(38):13640-13645.
194. Venkataraman T., Valdes M., et al. Loss of DExD/H box RNA helicase LGP2 manifests disparate antiviral responses. J. Immunol. 2007, 178(10):6444-6455.
195. Vercammen E., Staal J., et al. Sensing of viral infection and activation of innate immunity by toll-like receptor 3. Clin. Microbiol. Rev. 2008, 21(1):13-25.
196. Visvanathan K., Skinner N.A., et al. Regulation of Toll-like receptor-2 expression in chronic hepatitis B by the precore protein. Hepatology 2007, 45(1):102-110.
197. Vitour D., Dabo S., et al. Polo-like kinase 1 (PLK1) regulates interferon (IFN) induction by MAVS. J. Biol. Chem. 2009, 284(33):21797-21809.
198. Vitour D., Meurs E.F. Regulation of interferon production by RIG-I and LGP2: a lesson in self-control. Sci. STKE 2007, 2007(384):pe20.
199. Williams B.R. PKR; a sentinel kinase for cellular stress. Oncogene 1999, 18(45):6112-6120.
200. Xu L.G., Wang Y.Y., et al. VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol. Cell 2005, 19(6):727-740.
201. Yamamoto M., Sato S., et al. Role of adaptor TRIF in the MyD88-independent toll-like receptor signaling pathway. Science 2003, 301(5633):640-643.
202. Yan H., Krishnan K., et al. Phosphorylated interferon-alpha receptor 1 subunit (IFNaR1) acts as a docking site for the latent form of the 113kDa STAT2 protein. EMBO J. 1996, 15(5):1064-1074.
203. Yang Y., Liang Y., et al. Disruption of innate immunity due to mitochondrial targeting of a picornaviral protease precursor. Proc. Natl. Acad. Sci. U. S. A. 2007, 104(17):7253-7258.
204. Yang Y.L., Reis L.F., et al. Deficient signaling in mice devoid of double-stranded RNA-dependent protein kinase. EMBO J. 1995, 14(24):6095-6106.
205. Yoneyama M., Kikuchi M., et al. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 2005, 175(5):2851-2858.
206. Yoneyama M., Kikuchi M., et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5(7):730-737.
207. Yue Z., Shatkin A.J. Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 1997, 234(2):364-371.
208. Zhang R., Jha B.K., et al. Homologous 2',5'-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. Proc. Natl. Acad. Sci. U. S. A. 2013, 110(32):13114-13119.
209. Zhang S.Y., Jouanguy E., et al. TLR3 deficiency in patients with herpes simplex encephalitis. Science 2007, 317(5844):1522-1527.
210. Zhang Z., Kim T., et al. DDX1, DDX21, and DHX36 helicases form a complex with the adaptor molecule TRIF to sense dsRNA in dendritic cells. Immunity 2011, 34(6):866-878.
211. Zhao T., Yang L., et al. The NEMO adaptor bridges the nuclear factor-kappaB and interferon regulatory factor signaling pathways. Nat. Immunol. 2007, 8(6):592-600.
212. Zhao W., Lee C., et al. A conserved IFN-alpha receptor tyrosine motif directs the biological response to type I IFNs. J. Immunol. 2008, 180(8):5483-5489.
213. Zucchini N., Bessou G., et al. Individual plasmacytoid dendritic cells are major contributors to the production of multiple innate cytokines in an organ-specific manner during viral infection. Int. Immunol. 2008, 20(1):45-56.
214. Zurney J., Kobayashi T., et al. Reovirus mu2 protein inhibits interferon signaling through a novel mechanism involving nuclear accumulation of interferon regulatory factor 9. J. Virol. 2009, 83(5):2178-2187.