Resistance to rhabdoviridae infection and subversion of antiviral responses

Viruses

Volumn 7, Issue 7, 2015, Pages 3675-3702

  Blondel, Danielle ^a   Maarifi, Ghizlane ^b   Nisole, Sébastien ^b   Chelbi Alix, Mounira K ^b  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b faculté des sciences fondamentales et biomédicales   (France)

Author keywords

Interferon; ISG; Rabies virus; Rhabdoviruses; Vesicular stomatitis virus

Indexed keywords

INTERFERON; INTERFERON STIMULATED GENE FACTOR 3; MEMBRANE FUSION PROTEIN; PATTERN RECOGNITION RECEPTOR; PEPTIDES AND PROTEINS; RNA POLYMERASE; TETHERIN; TRIPARTITE MOTIF PROTEIN 19; UNCLASSIFIED DRUG;

ANTIVIRAL ACTIVITY; GENE; GENE EXPRESSION; GENE INDUCTION; GENE SILENCING; GENETIC ASSOCIATION; GENETIC TRANSCRIPTION; INFECTION RESISTANCE; INNATE IMMUNITY; INTERFERON INDUCED PROTEINS WITH TETRATRICOPEPTIDE REPEATS GENE; INTERFERON STIMULATED GENE; MEMBRANE BIOLOGY; MOLECULAR INTERACTION; NONHUMAN; PHOSPHORYLATION; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN SYNTHESIS INHIBITION; REGULATORY MECHANISM; REVIEW; RHABDOVIRIDAE; RHABDOVIRUS INFECTION; RNA SPLICING; RNA TRANSLATION; SIGNAL TRANSDUCTION; VIRION; VIRUS DETECTION; VIRUS REPLICATION; ANIMAL; GENETICS; HUMAN; IMMUNOLOGY; PHYSIOLOGY; VIROLOGY;

RABIES VIRUS; RHABDOVIRIDAE; VESICULAR STOMATITIS VIRUS;

ANIMALS; HUMANS; INTERFERONS; RHABDOVIRIDAE; RHABDOVIRIDAE INFECTIONS;

EID: 84936944026     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v7072794     Document Type: Review

References (129)

1. Kuzmin, I.V.; Novella, I.S.; Dietzgen, R.G.; Padhi, A.; Rupprecht, C.E. The rhabdoviruses: Biodiversity, phylogenetics, and evolution. Infect. Genet. Evol. 2009, 9, 541–553.
2. Basak, S.; Mondal, A.; Polley, S.; Mukhopadhyay, S.; Chattopadhyay, D. Reviewing Chandipura: A vesiculovirus in human epidemics. Biosci. Rep. 2007, 27, 275–298.
3. Ahmed, M.; McKenzie, M.O.; Puckett, S.; Hojnacki, M.; Poliquin, L.; Lyles, D.S. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 2003, 77, 4646–4657.
4. Connor, J.H.; Lyles, D.S. Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J. Virol. 2002, 76, 10177–10187.
5. Connor, J.H.; Lyles, D.S. Inhibition of host and viral translation during vesicular stomatitis virus infection. eIF2 is responsible for the inhibition of viral but not host translation. J. Biol. Chem. 2005, 280, 13512–13519.
6. Kopecky, S.A.; Willingham, M.C.; Lyles, D.S. Matrix protein and another viral component contribute to induction of apoptosis in cells infected with vesicular stomatitis virus. J. Virol. 2001, 75, 12169–12181.
7. Schnell, M.J.; McGettigan, J.P.; Wirblich, C.; Papaneri, A. The cell biology of rabies virus: Using stealth to reach the brain. Nat. Rev. Microbiol. 2010, 8, 51–61.
8. Matsumoto, S. Electron microscopy of nerve cells infected with street rabies virus. Virology 1962, 17, 198–202.
9. Tordo, N.; Poch, O.; Ermine, A.; Keith, G.; Rougeon, F. Completion of the rabies virus genome sequence determination: Highly conserved domains among the L (polymerase) proteins of unsegmented negative-strand RNA viruses. Virology 1988, 165, 565–576.
10. Walker, P.J.; Firth, C.; Widen, S.G.; Blasdell, K.R.; Guzman, H.; Wood, T.G.; Paradkar, P.N.; Holmes, E.C.; Tesh, R.B.; Vasilakis, N.; et al. Evolution of genome size and complexity in the rhabdoviridae. PLoS Pathog. 2015, 11, e1004664.
11. Lahaye, X.; Vidy, A.; Pomier, C.; Obiang, L.; Harper, F.; Gaudin, Y.; Blondel, D. Functional characterization of Negri bodies (NBs) in rabies virus-infected cells: Evidence that NBs are sites of viral transcription and replication. J. Virol. 2009, 83, 7948–7958.
12. Heinrich, B.S.; Cureton, D.K.; Rahmeh, A.A.; Whelan, S.P. Protein expression redirects vesicular stomatitis virus RNA synthesis to cytoplasmic inclusions. PLoS Pathog. 2010, 6, e1000958.
13. Mavrakis, M.; Mehouas, S.; Real, E.; Iseni, F.; Blondel, D.; Tordo, N.; Ruigrok, R.W. Rabies virus chaperone: Identification of the phosphoprotein peptide that keeps nucleoprotein soluble and free from non-specific RNA. Virology 2006, 349, 422–429.
14. Bruni, D.; Chazal, M.; Sinigaglia, L.; Chauveau, L.; Schwartz, O.; Despres, P.; Jouvenet, N. Viral entry route determines how human plasmacytoid dendritic cells produce type I interferons. Sci. Signal. 2015, 8, ra25.
15. 1 -Triphosphate RNA is the ligand for RIG-I. Science 2006, 314, 994–997.
16. Kato, H.; Takeuchi, O.; Sato, S.; Yoneyama, M.; Yamamoto, M.; Matsui, K.; Uematsu, S.; Jung, A.; Kawai, T.; Ishii, K.J.; et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441, 101–105.
17. 1 -phosphates. Science 2006, 314, 997–1001.
18. 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.
19. Menager, P.; Roux, P.; Megret, F.; Bourgeois, J.P.; le Sourd, A.M.; Danckaert, A.; Lafage, M.; Prehaud, C.; Lafon, M. Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Pathog. 2009, 5, e1000315.
20. Lund, J.M.; Alexopoulou, L.; Sato, A.; Karow, M.; Adams, N.C.; Gale, N.W.; Iwasaki, A.; Flavell, R.A. Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc. Natl. Acad. Sci. USA 2004, 101, 5598–5603.
21. Faul, E.J.; Wanjalla, C.N.; Suthar, M.S.; Gale, M.; Wirblich, C.; Schnell, M.J. Rabies virus infection induces type I interferon production in an IPS-1 dependent manner while dendritic cell activation relies on IFNAR signaling. PLoS Pathog. 2010, 6, e1001016.
22. Kubota, T.; Matsuoka, M.; Chang, T.H.; Tailor, P.; Sasaki, T.; Tashiro, M.; Kato, A.; Ozato, K. Virus infection triggers SUMOylation of IRF3 and IRF7, leading to the negative regulation of type I interferon gene expression. J. Biol. Chem. 2008, 283, 25660–25670.
23. Fu, J.; Xiong, Y.; Xu, Y.; Cheng, G.; Tang, H. MDA5 is SUMOylated by PIAS2beta in the upregulation of type I interferon signaling. Mol. Immunol. 2011, 48, 415–422.
24. Mi, Z.; Fu, J.; Xiong, Y.; Tang, H. SUMOylation of RIG-I positively regulates the type I interferon signaling. Protein Cell 2010, 1, 275–283.
25. Isaacs, A.; Lindenmann, J. Virus interference. I. The interferon. Proc. R. Soc. Lond. Ser. B Biol. Sci. 1957, 147, 258–267.
26. Schneider, W.M.; Chevillotte, M.D.; Rice, C.M. Interferon-stimulated genes: A complex web of host defenses. Annu. Rev. Immunol. 2014, 32, 513–545.
27. Prokunina-Olsson, L.; Muchmore, B.; Tang, W.; Pfeiffer, R.M.; Park, H.; Dickensheets, H.; Hergott, D.; Porter-Gill, P.; Mumy, A.; Kohaar, I.; et al. A variant upstream of IFNL3 (IL28B) creating a new interferon gene IFNL4 is associated with impaired clearance of hepatitis C virus. Nat. Genet. 2013, 45, 164–171.
28. Blaszczyk, K.; Olejnik, A.; Nowicka, H.; Ozgyin, L.; Chen, Y.L.; Chmielewski, S.; Kostyrko, K.; Wesoly, J.; Balint, B.L.; Lee, C.K.; et al. STAT2/IRF9 directs a prolonged ISGF3-like transcriptional response and antiviral activity in the absence of STAT1. Biochem. J. 2015, 466, 511–524.
29. Fink, K.; Grandvaux, N. STAT2 and IRF9: Beyond ISGF3. JAK-STAT 2013, 2, e27521.
30. Sommereyns, C.; Paul, S.; Staeheli, P.; Michiels, T. IFN-lambda (IFN-lambda) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLoS Pathog. 2008, 4, e1000017.
31. Pedersen, I.M.; Cheng, G.; Wieland, S.; Volinia, S.; Croce, C.M.; Chisari, F.V.; David, M. Interferon modulation of cellular microRNAs as an antiviral mechanism. Nature 2007, 449, 919–922.
32. Hou, J.; Wang, P.; Lin, L.; Liu, X.; Ma, F.; An, H.; Wang, Z.; Cao, X. MicroRNA-146a feedback inhibits RIG-I-dependent Type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 2009, 183, 2150–2158.
33. Zhou, A.; Paranjape, J.M.; Der, S.D.; Williams, B.R.; Silverman, R.H. Interferon action in triply deficient mice reveals the existence of alternative antiviral pathways. Virology 1999, 258, 435–440.
34. Balachandran, S.; Roberts, P.C.; Brown, L.E.; Truong, H.; Pattnaik, A.K.; Archer, D.R.; Barber, G.N. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 2000, 13, 129–141.
35. Pavlovic, J.; Zurcher, T.; Haller, O.; Staeheli, P. Resistance to influenza virus and vesicular stomatitis virus conferred by expression of human MxA protein. J. Virol. 1990, 64, 3370–3375. [PubMed]
36. Takaoka, A.; Hayakawa, S.; Yanai, H.; Stoiber, D.; Negishi, H.; Kikuchi, H.; Sasaki, S.; Imai, K.; Shibue, T.; Honda, K.; et al. Integration of interferon-alpha/beta signalling to p53 responses in tumour suppression and antiviral defence. Nature 2003, 424, 516–523.
37. Espert, L.; Degols, G.; Gongora, C.; Blondel, D.; Williams, B.R.; Silverman, R.H.; Mechti, N. ISG20, a new interferon-induced RNase specific for single-stranded RNA, defines an alternative antiviral pathway against RNA genomic viruses. J. Biol. Chem. 2003, 278, 16151–16158.
38. Fensterl, V.; Wetzel, J.L.; Ramachandran, S.; Ogino, T.; Stohlman, S.A.; Bergmann, C.C.; Diamond, M.S.; Virgin, H.W.; Sen, G.C. Interferon-induced Ifit2/ISG54 protects mice from lethal VSV neuropathogenesis. PLoS Pathog. 2012, 8, e1002712.
39. Weidner, J.M.; Jiang, D.; Pan, X.B.; Chang, J.; Block, T.M.; Guo, J.T. Interferon-induced cell membrane proteins, IFITM3 and tetherin, inhibit vesicular stomatitis virus infection via distinct mechanisms. J. Virol. 2010, 84, 12646–12657.
40. Liu, S.Y.; Aliyari, R.; Chikere, K.; Li, G.; Marsden, M.D.; Smith, J.K.; Pernet, O.; Guo, H.; Nusbaum, R.; Zack, J.A.; et al. Interferon-inducible cholesterol-25-hydroxylase broadly inhibits viral entry by production of 25-hydroxycholesterol. Immunity 2013, 38, 92–105.
41. Chelbi-Alix, M.K.; Quignon, F.; Pelicano, L.; Koken, M.H.; de The, H. Resistance to virus infection conferred by the interferon-induced promyelocytic leukemia protein. J. Virol. 1998, 72, 1043–1051.
42. El Asmi, F.; Maroui, M.A.; Dutrieux, J.; Blondel, D.; Nisole, S.; Chelbi-Alix, M.K. Implication of PMLIV in both intrinsic and innate immunity. PLoS Pathog. 2014, 10, e1003975.
43. 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.
44. Schoggins, J.W. Interferon-stimulated genes: Roles in viral pathogenesis. Curr. Opin. Virol. 2014, 6, 40–46.
45. Liu, S.Y.; Sanchez, D.J.; Aliyari, R.; Lu, S.; Cheng, G. Systematic identification of type I and type II interferon-induced antiviral factors. Proc. Natl. Acad. Sci. USA 2012, 109, 4239–4244.
46. Staeheli, P.; Pavlovic, J. Inhibition of vesicular stomatitis virus mRNA synthesis by human MxA protein. J. Virol. 1991, 65, 4498–4501
47. Stojdl, D.F.; Abraham, N.; Knowles, S.; Marius, R.; Brasey, A.; Lichty, B.D.; Brown, E.G.; Sonenberg, N.; Bell, J.C. The murine double-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J. Virol. 2000, 74, 9580–9585.
48. Blondel, D.; Kheddache, S.; Lahaye, X.; Dianoux, L.; Chelbi-Alix, M.K. Resistance to rabies virus infection conferred by the PMLIV isoform. J. Virol. 2010, 84, 10719–10726.
49. Blondel, D.; Regad, T.; Poisson, N.; Pavie, B.; Harper, F.; Pandolfi, P.P.; de The, H.; Chelbi-Alix, M.K. Rabies virus P and small P products interact directly with PML and reorganize PML nuclear bodies. Oncogene 2002, 21, 7957–7970.
50. Smith, S.E.; Gibson, M.S.; Wash, R.S.; Ferrara, F.; Wright, E.; Temperton, N.; Kellam, P.; Fife, M. Chicken interferon-inducible transmembrane protein 3 restricts influenza viruses and lyssaviruses in vitro. J. Virol. 2013, 87, 12957–12966.
51. Versteeg, G.A.; Benke, S.; Garcia-Sastre, A.; Rajsbaum, R. InTRIMsic immunity: Positive and negative regulation of immune signaling by tripartite motif proteins. Cytokine Growth Factor Rev. 2014, 25, 563–576.
52. Panda, D.; Das, A.; Dinh, P.X.; Subramaniam, S.; Nayak, D.; Barrows, N.J.; Pearson, J.L.; Thompson, J.; Kelly, D.L.; Ladunga, I.; et al. RNAi screening reveals requirement for host cell secretory pathway in infection by diverse families of negative-strand RNA viruses. Proc. Natl. Acad. Sci. USA 2011, 108, 19036–19041.
53. Das, A.; Dinh, P.X.; Panda, D.; Pattnaik, A.K. Interferon-inducible protein IFI35 negatively regulates RIG-I antiviral signaling and supports vesicular stomatitis virus replication. J. Virol. 2014, 88, 3103–3113.
54. Bailey, C.C.; Zhong, G.; Huang, I.C.; Farzan, M. IFITM-Family Proteins: The Cell’s First Line of Antiviral Defense. Annu. Rev. Virol. 2014, 1, 261–283.
55. Siegrist, F.; Ebeling, M.; Certa, U. The small interferon-induced transmembrane genes and proteins. J. Interferon Cytokine Res. 2011, 31, 183–197.
56. Brass, A.L.; Huang, I.C.; Benita, Y.; John, S.P.; Krishnan, M.N.; Feeley, E.M.; Ryan, B.J.; Weyer, J.L.; van der Weyden, L.; Fikrig, E.; et al. The IFITM proteins mediate cellular resistance to influenza A H1N1 virus, West Nile virus, and dengue virus. Cell 2009, 139, 1243–1254.
57. Alber, D.; Staeheli, P. Partial inhibition of vesicular stomatitis virus by the interferon-induced human 9-27 protein. J. Interferon Cytokine Res. 1996, 16, 375–380.
58. Huang, I.C.; Bailey, C.C.; Weyer, J.L.; Radoshitzky, S.R.; Becker, M.M.; Chiang, J.J.; Brass, A.L.; Ahmed, A.A.; Chi, X.; Dong, L.; et al. Distinct patterns of IFITM-mediated restriction of filoviruses, SARS coronavirus, and influenza A virus. PLoS Pathog. 2011, 7, e1001258.
59. Jiang, D.; Weidner, J.M.; Qing, M.; Pan, X.B.; Guo, H.; Xu, C.; Zhang, X.; Birk, A.; Chang, J.; Shi, P.Y.; et al. Identification of five interferon-induced cellular proteins that inhibit west nile virus and dengue virus infections. J. Virol. 2010, 84, 8332–8341.
60. Li, K.; Markosyan, R.M.; Zheng, Y.M.; Golfetto, O.; Bungart, B.; Li, M.; Ding, S.; He, Y.; Liang, C.; Lee, J.C.; et al. IFITM proteins restrict viral membrane hemifusion. PLoS Pathog. 2013, 9, e1003124.
61. Feeley, E.M.; Sims, J.S.; John, S.P.; Chin, C.R.; Pertel, T.; Chen, L.M.; Gaiha, G.D.; Ryan, B.J.; Donis, R.O.; Elledge, S.J.; et al. IFITM3 inhibits influenza A virus infection by preventing cytosolic entry. PLoS Pathog. 2011, 7, e1002337.
62. Holmes, R.S.; Vandeberg, J.L.; Cox, L.A. Genomics and proteomics of vertebrate cholesterol ester lipase (LIPA) and cholesterol 25-hydroxylase (CH25H). 3 Biotech 2011, 1, 99–109.
63. Aebi, M.; Fah, J.; Hurt, N.; Samuel, C.E.; Thomis, D.; Bazzigher, L.; Pavlovic, J.; Haller, O.; Staeheli, P. cDNA structures and regulation of two interferon-induced human Mx proteins. Mol. Cell. Boil. 1989, 9, 5062–5072.
64. Chang, K.C.; Hansen, E.; Foroni, L.; Lida, J.; Goldspink, G. Molecular and functional analysis of the virus- and interferon-inducible human MxA promoter. Arch. Virol. 1991, 117, 1–15.
65. Verhelst, J.; Hulpiau, P.; Saelens, X.; Mx proteins: Antiviral gatekeepers that restrain the uninvited. Microbiol. Mol. Boil. Rev. 2013, 77, 551–566.
66. Haller, O.; Kochs, G. Interferon-induced mx proteins: Dynamin-like GTPases with antiviral activity. Traffic 2002, 3, 710–717.
67. Haller, O.; Staeheli, P.; Schwemmle, M.; Kochs, G. Mx GTPases: Dynamin-like antiviral machines of innate immunity. Trends Microbial. 2015, 23, 154–163.
68. Meier, E.; Fah, J.; Grob, M.S.; End, R.; Staeheli, P.; Haller, O. A family of interferon-induced Mx-related mRNAs encodes cytoplasmic and nuclear proteins in rat cells. J. Virol. 1988, 62, 2386–2393. [PubMed]
69. Zurcher, T.; Pavlovic, J.; Staeheli, P. Mouse Mx2 protein inhibits vesicular stomatitis virus but not influenza virus. Virology 1992, 187, 796–800.
70. Leroy, M.; Pire, G.; Baise, E.; Desmecht, D. Expression of the interferon-alpha/beta-inducible bovine Mx1 dynamin interferes with replication of rabies virus. Neurobiol. Dis. 2006, 21, 515–521.
71. Nisole, S.; Stoye, J.P.; Saib, A. TRIM family proteins: Retroviral restriction and antiviral defence. Nat. Rev. Microbiol. 2005, 3, 799–808.
72. Ishov, A.M.; Sotnikov, A.G.; Negorev, D.; Vladimirova, O.V.; Neff, N.; Kamitani, T.; Yeh, E.T.; Strauss, J.F., 3rd; Maul, G.G. PML is critical for ND10 formation and recruits the PML-interacting protein daxx to this nuclear structure when modified by SUMO-1. J. Cell Boil. 1999, 147, 221–234.
73. Bernardi, R.; Papa, A.; Pandolfi, P.P. Regulation of apoptosis by PML and the PML-NBs. Oncogene 2008, 27, 6299–6312.
74. Nisole, S.; Maroui, M.A.; Mascle, X.H.; Aubry, M.; Chelbi-Alix, M.K. Differential Roles of PML Isoforms. Front. Oncol. 2013, 3.
75. Geoffroy, M.C.; Chelbi-Alix, M.K. Role of promyelocytic leukemia protein in host antiviral defense. J. Interferon Cytokine Res. 2011, 31, 145–158.
76. Everett, R.D.; Chelbi-Alix, M.K. PML and PML nuclear bodies: Implications in antiviral defence. Biochimie 2007, 89, 819–830.
77. Kamitani, T.; Nguyen, H.P.; Kito, K.; Fukuda-Kamitani, T.; Yeh, E.T. Covalent modification of PML by the sentrin family of ubiquitin-like proteins. J. Biol. Chem. 1998, 273, 3117–3120.
78. Jensen, K.; Shiels, C.; Freemont, P.S. PML protein isoforms and the RBCC/TRIM motif. Oncogene 2001, 20, 7223–7233.
79. Saitoh, T.; Tun-Kyi, A.; Ryo, A.; Yamamoto, M.; Finn, G.; Fujita, T.; Akira, S.; Yamamoto, N.; Lu, K.P.; Yamaoka, S.; et al. Negative regulation of interferon-regulatory factor 3-dependent innate antiviral response by the prolyl isomerase Pin1. Nat. Immunol. 2006, 7, 598–605.
80. Gongora, C.; Degols, G.; Espert, L.; Hua, T.D.; Mechti, N. A unique ISRE, in the TATA-less human Isg20 promoter, confers IRF-1-mediated responsiveness to both interferon type I and type II. Nucleic Acids Res. 2000, 28, 2333–2341.
81. Nguyen, L.H.; Espert, L.; Mechti, N.; Wilson, D.M., 3rd. The human interferon- and estrogen-regulated ISG20/HEM45 gene product degrades single-stranded RNA and DNA in vitro. Biochemistry 2001, 40, 7174–7179.
82. Espert, L.; Rey, C.; Gonzalez, L.; Degols, G.; Chelbi-Alix, M.K.; Mechti, N.; Gongora, C. Theexonuclease ISG20 is directly induced by synthetic dsRNA via NF-kappaB and IRF1 activation. Oncogene 2004, 23, 4636–4640.
83. Lewin, A.R.; Reid, L.E.; McMahon, M.; Stark, G.R.; Kerr, I.M. Molecular analysis of a human interferon-inducible gene family. Eur. J. Biochem. 1991, 199, 417–423.
84. Fensterl, V.; Sen, G.C. The ISG56/IFIT1 gene family. J. Interferon Cytokine Res. 2011, 31, 71–78.
85. Diamond, M.S.; Farzan, M. The broad-spectrum antiviral functions of IFIT and IFITM proteins. Nat. Rev. Immunol. 2013, 13, 46–57.
86. Vladimer, G.I.; Gorna, M.W.; Superti-Furga, G. IFITs: Emerging Roles as Key Anti-Viral Proteins. Front. Immunol. 2014, 5.
87. 1 -O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 2010, 468, 452–456.
88. 1 -PPP-RNA recognition by human IFIT proteins. Nature 2013, 494, 60–64.
89. Guo, J.; Sen, G.C. Characterization of the interaction between the interferon-induced protein P56 and the Int6 protein encoded by a locus of insertion of the mouse mammary tumor virus. J. Virol. 2000, 74, 1892–1899.
90. Schmeisser, H.; Mejido, J.; Balinsky, C.A.; Morrow, A.N.; Clark, C.R.; Zhao, T.; Zoon, K.C. Identification of alpha interferon-induced genes associated with antiviral activity in Daudi cells and characterization of IFIT3 as a novel antiviral gene. J. Virol. 2010, 84, 10671–10680.
91. Blasius, A.L.; Giurisato, E.; Cella, M.; Schreiber, R.D.; Shaw, A.S.; Colonna, M. Bone marrow stromal cell antigen 2 is a specific marker of type I IFN-producing cells in the naive mouse, but a promiscuous cell surface antigen following IFN stimulation. J. Immunol. 2006, 177, 3260–3265.
92. 92. Kupzig, S.; Korolchuk, V.; Rollason, R.; Sugden, A.; Wilde, A.; Banting, G. Bst-2/HM1.24 is a raft-associated apical membrane protein with an unusual topology. Traffic 2003, 4, 694–709.
93. Rollason, R.; Korolchuk, V.; Hamilton, C.; Jepson, M.; Banting, G. A CD317/tetherin-RICH2 complex plays a critical role in the organization of the subapical actin cytoskeleton in polarized epithelial cells. J. Cell Boil. 2009, 184, 721–736.
94. Wynn, T.A.; Nicolet, C.M.; Paulnock, D.M. Identification and characterization of a new gene family induced during macrophage activation. J. Immunol. 1991, 147, 4384–4392. [PubMed]
95. Vopel, T.; Syguda, A.; Britzen-Laurent, N.; Kunzelmann, S.; Ludemann, M.B.; Dovengerds, C.; Sturzl, M.; Herrmann, C. Mechanism of GTPase-activity-induced self-assembly of human guanylate binding protein 1. J. Mol. Boil. 2010, 400, 63–70.
96. Cheng, Y.S.; Colonno, R.J.; Yin, F.H. Interferon induction of fibroblast proteins with guanylate binding activity. J. Biol. Chem. 1983, 258, 7746–7750. [PubMed]
97. Anderson, S.L.; Carton, J.M.; Lou, J.; Xing, L.; Rubin, B.Y. Interferon-induced guanylatebinding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 1999, 256, 8–14.
98. Meurs, E.F.; Watanabe, Y.; Kadereit, S.; Barber, G.N.; Katze, M.G.; Chong, K.; Williams, B.R.; Hovanessian, A.G. Constitutive expression of human double-stranded RNA-activated p68 kinase in murine cells mediates phosphorylation of eukaryotic initiation factor 2 and partial resistance to encephalomyocarditis virus growth. J. Virol. 1992, 66, 5805–5814.
99. Swiecki, M.; Wang, Y.; Gilfillan, S.; Lenschow, D.J.; Colonna, M. Cutting edge: Paradoxical roles of BST2/tetherin in promoting type I IFN response and viral infection. J. Immunol. 2012, 188, 2488–2492.
100. Goodbourn, S.; Didcock, L.; Randall, R.E. Interferons: Cell signalling, immune modulation, antiviral response and virus countermeasures. J. Gen. Virol. 2000, 81, 2341–2364. [PubMed]
101. Regad, T.; Chelbi-Alix, M.K. Role and fate of PML nuclear bodies in response to interferon and viral infections. Oncogene 2001, 20, 7274–7286.
102. Wertz, G.W.; Youngner, J.S. Interferon production and inhibition of host synthesis in cells infected with vesicular stomatitis virus. J. Virol. 1970, 6, 476–484. [PubMed]
103. Blondel, D.; Harmison, G.G.; Schubert, M. Role of matrix protein in cytopathogenesis of vesicular stomatitis virus. J. Virol. 1990, 64, 1716–1725. [PubMed]
104. Melki, R.; Gaudin, Y.; Blondel, D. Interaction between tubulin and the viral matrix protein of vesicular stomatitis virus: Possible implications in the viral cytopathic effect. Virology 1994, 202, 339–347.
105. Black, B.L.; Rhodes, R.B.; McKenzie, M.; Lyles, D.S. The role of vesicular stomatitis virus matrix protein in inhibition of host-directed gene expression is genetically separable from its function in virus assembly. J. Virol. 1993, 67, 4814–4821. [PubMed]
106. Yuan, H.; Yoza, B.K.; Lyles, D.S. Inhibition of host RNA polymerase II-dependent transcription by vesicular stomatitis virus results from inactivation of TFIID. Virology 1998, 251, 383–392.
107. Petersen, J.M.; Her, L.S.; Varvel, V.; Lund, E.; Dahlberg, J.E. The matrix protein of vesicular stomatitis virus inhibits nucleocytoplasmic transport when it is in the nucleus and associated with nuclear pore complexes. Mol. Cell. Boil. 2000, 20, 8590–8601.
108. Enninga, J.; Levy, D.E.; Blobel, G.; Fontoura, B.M. Role of nucleoporin induction in releasing an mRNA nuclear export block. Science 2002, 295, 1523–1525.
109. Von Kobbe, C.; van Deursen, J.M.; Rodrigues, J.P.; Sitterlin, D.; Bachi, A.; Wu, X.; Wilm, M.; Carmo-Fonseca, M.; Izaurralde, E. Vesicular stomatitis virus matrix protein inhibits host cell gene expression by targeting the nucleoporin Nup98. Mol. Cell 2000, 6, 1243–1252.
110. Faria, P.; Chakraborty, P.; Lavay, A.; Barber, G.; Ezelle, H.; Enninga, J.; Fontoura, B. VSV disrupts the Rae/mrnp40 mRNA nuclear export pathway. Mol. Cell 2005, 17, 93–102.
111. Brzozka, K.; Finke, S.; Conzelmann, K.K. Identification of the rabies virus alpha/beta interferon antagonist: Phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J. Virol. 2005, 79, 7673–7681.
112. 112 . Rieder, M.; Brzozka, K.; Pfaller, C.K.; Cox, J.H.; Stitz, L.; Conzelmann, K.K. Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: Inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J. Virol. 2011, 85, 842–852.
113. Patton, J.T.; Davis, N.L.; Wertz, G.W. N protein alone satisfies the requirement for protein synthesis during RNA replication of vesicular stomatitis virus. J. Virol. 1984, 49, 303–309. [PubMed]
114. Masatani, T.; Ito, N.; Shimizu, K.; Ito, Y.; Nakagawa, K.; Sawaki, Y.; Koyama, H.; Sugiyama, M. Rabies virus nucleoprotein functions to evade activation of the RIG-I-mediated antiviral response. J. Virol. 2010, 84, 4002–4012.
115. Cardenas, W.B.; Loo, Y.M.; Gale, M., Jr.; Hartman, A.L.; Kimberlin, C.R.; Martinez-Sobrido, L.; Saphire, E.O.; Basler, C.F. Ebola virus VP35 protein binds double-stranded RNA and inhibits alpha/beta interferon production induced by RIG-I signaling. J. Virol. 2006, 80, 5168–5178.
116. Wang, J.; Basagoudanavar, S.H.; Wang, X.; Hopewell, E.; Albrecht, R.; Garcia-Sastre, A.; Balachandran, S.; Beg, A.A. NF-kappa B RelA subunit is crucial for early IFN-beta expression and resistance to RNA virus replication. J. Immunol. 2010, 185, 1720–1729.
117. Luco, S.; Delmas, O.; Vidalain, P.O.; Tangy, F.; Weil, R.; Bourhy, H. RelAp43, a member of the NF-kappaB family involved in innate immune response against Lyssavirus infection. PLoS Pathog. 2012, 8, e1003060.
118. Chenik, M.; Chebli, K.; Blondel, D. Translation initiation at alternate in-frame AUG codons in the rabies virus phosphoprotein mRNA is mediated by a ribosomal leaky scanning mechanism. J. Virol. 1995, 69, 707–712. [PubMed]
119. Pasdeloup, D.; Poisson, N.; Raux, H.; Gaudin, Y.; Ruigrok, R.W.; Blondel, D. Nucleocytoplasmic shuttling of the rabies virus P protein requires a nuclear localization signal and a CRM1-dependent nuclear export signal. Virology 2005, 334, 284–293.
120. Oksayan, S.; Wiltzer, L.; Rowe, C.L.; Blondel, D.; Jans, D.A.; Moseley, G.W. A novel nuclear trafficking module regulates the nucleocytoplasmic localization of the rabies virus interferon antagonist, P protein. J. Biol. Chem. 2012, 287, 28112–28121.
121. Moseley, G.W.; Filmer, R.P.; DeJesus, M.A.; Jans, D.A. Nucleocytoplasmic distribution of rabies virus P-protein is regulated by phosphorylation adjacent to C-terminal nuclear import and export signals. Biochemistry 2007, 46, 12053–12061.
122. Vidy, A.; el Bougrini, J.; Chelbi-Alix, M.K.; Blondel, D. The nucleocytoplasmic rabies virus P protein counteracts interferon signaling by inhibiting both nuclear accumulation and DNA binding of STAT1. J. Virol. 2007, 81, 4255–4263.
123. Vidy, A.; Chelbi-Alix, M.; Blondel, D. Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J. Virol. 2005, 79, 14411–14420.
124. Brzozka, K.; Finke, S.; Conzelmann, K.K. Inhibition of interferon signaling by rabies virus phosphoprotein P: Activation-dependent binding of STAT1 and STAT2. J. Virol. 2006, 80, 2675–2683.
125. 125 . Moseley, G.W.; Lahaye, X.; Roth, D.M.; Oksayan, S.; Filmer, R.P.; Rowe, C.L.; Blondel, D.; Jans, D.A. Dual modes of rabies P-protein association with microtubules: A novel strategy to suppress the antiviral response. J. Cell Sci. 2009, 122, 3652–3662.
126. Wiltzer, L.; Larrous, F.; Oksayan, S.; Ito, N.; Marsh, G.A.; Wang, L.F.; Blondel, D.; Bourhy, H.; Jans, D.A.; Moseley, G.W.; et al. Conservation of a unique mechanism of immune evasion across the Lyssavirus genus. J. Virol. 2012, 86, 10194–10199.
127. Ito, N.; Moseley, G.W.; Blondel, D.; Shimizu, K.; Rowe, C.L.; Ito, Y.; Masatani, T.; Nakagawa, K.; Jans, D.A.; Sugiyama, M.; et al. Role of interferon antagonist activity of rabies virus phosphoprotein in viral pathogenicity. J. Virol. 2010, 84, 6699–6710.
128. Shaw, M.L.; Garcia-Sastre, A.; Palese, P.; Basler, C.F. Nipah virus V and W proteins have a common STAT1-binding domain yet inhibit STAT1 activation from the cytoplasmic and nuclear compartments, respectively. J. Virol. 2004, 78, 5633–5641.
129. Shaw, M.L.; Cardenas, W.B.; Zamarin, D.; Palese, P.; Basler, C.F. Nuclear localization of the Nipah virus W protein allows for inhibition of both virus- and toll-like receptor 3-triggered signaling pathways. J. Virol. 2005, 79, 6078–6088.