Interferon in lyssavirus infection

Berliner und Munchener Tierarztliche Wochenschrift

Volumn 125, Issue 5-6, 2012, Pages 209-218

  Rieder, Martina ^a   Finke, Stefan ^b   Conzelmann, Karl Klaus ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

Author keywords

Antiviral; Inflammation; Innate immunity; Zoonosis

Indexed keywords

INTERFERON; PHOSPHOPROTEIN; STAT PROTEIN;

ANIMAL; ARTICLE; CLASSIFICATION; GENETICS; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; RABIES; RABIES VIRUS; RHABDOVIRUS INFECTION; SIGNAL TRANSDUCTION; VIROLOGY;

ANIMALS; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERONS; LYSSAVIRUS; PHOSPHOPROTEINS; RABIES; RABIES VIRUS; RHABDOVIRIDAE INFECTIONS; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

ANIMALIA; LYSSAVIRUS; RABIES VIRUS;

EID: 84866148477     PISSN: 00059366     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (102)

1. Albertini AA, Schoehn G, Weissenborn W, Ruigrok RW (2008): Structural aspects of rabies virus replication. Cell Mol Life Sei 65: 282-294.
2. Astic L, Saucier D, Coulon P, Lafay F, Flamand A (1993): The CVS strain of rabies virus as transneuronal tracer in the olfactory system of mice. Brain Res 619: 146-156.
3. Badrane H, Bahloul C, Perrin P, Tordo N (2001): Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immu-nogenicity. J Virol 75: 3268-3276.
4. Balachandran S, Roberts PC, Brown LE, Truong H, Pattnaik AK, Archer DR, Barber GN (2000): Essential role for the dsR-NAdependent protein kinase PKR in innate immunity to viral infection. Immunity 13: 129-141.
5. Blondel D, Kheddache S, Lahaye X, Dianoux L, Chelbi-Alix MK (2010): Resistance to rabies virus infection conferred by the PMLIVisoform. J Virol 84: 10719-10726.
6. Blondel D, Regad T, Poisson N, Pavie B, Harper F, Pandolfi PP, De The H, Chelbi-Alix MK (2002): Rabies virus P and small P products interact directly with PML and reorganize PML nuclear bodies. Oncogene 21: 7957-7970.
7. Botvinkin AD, Poleschuk EM, Kuzmin IV, Borisova TI, Gazaryan SV, Yager P, Rupprecht CE (2003): Novel lyssaviruses isolated from bats in Russia. Emerg Infect Dis 9: 1623-1625.
8. Boulger LR, Porterfield JS (1958): Isolation of a virus from Nigerian fruit bats. Trans R SocTrop Med Hyg 52: 421-424.
9. Brzözka K, Finke S, Conzelmann KK (2006): Inhibition of interferon signaling by rabies virus phosphoprotein P: activation-dependent binding of STAT1 and STAT2. J Virol 80: 2675-2683.
10. Calam DH (1980): Nomenclature of interferons. Lancet 2: 259.
11. Chenik M, Chebli K, Blondel D (1995): Translation initiation at alternate in-frame AUG codons in the rabies virus phosphoprotein mRNA is mediated by a ribosomal leaky scanning mechanism. J Virol 69: 707-712.
12. Chopy D, Detje CN, Lafage M, Kalinke U, Lafon M (2011): The type I interferon response bridles rabies virus infection and reduces pathogenicity. J Neurovirol 17: 353-367.
13. Cui S, Eisenacher K, Kirchhofer A, Brzözka K, Lammens A, Lammens K, Fujita T, Conzelmann KK, Krug A, Hopfner KP (2008): The C-terminal regulatory domain is the RNA 5'-triphosphate sensor of RIG-I. Mol. Cell 29: 169-179.
14. Dietzschold B, Li J, Faber M, Schnell M (2008): Concepts in the pathogenesis of rabies. Future Virol 3: 481-490.
15. Etessami R, Conzelmann KK, Fadai-Ghotbi B, Natelson B, Tsiang H, Ceccaldi PE (2000): Spread and pathogenic characteristics of a G-deficient rabies virus recombinant: an in vitro and in vivo study. J Gen Virol 81: 2147-2153.
16. Faul EJ, Wanjalla CN, McGettigan JP, Schnell MJ (2008): Inter-feron-beta expressed by a rabies virus-based HIV-1 vaccine vector serves as a molecular adjuvant and decreases pathogenicity. Virology 382: 226-238.
17. Faul EJ, Wanjalla CN, Suthar MS, Gale M, Wirblich C, Schnell MJ (2010): Rabies virus infection induces type I interferon production in an.IPS-1 dependent manner while dendritic cell activation relies on IFNAR signaling. PLoS Rathog 6: el001016.
18. Finke S, Conzelmann KK (2003): Dissociation of rabies virus matrix protein functions in regulation of viral RNA synthesis and virus assembly. J Virol 77: 12074-12082.
19. Finke S, Conzelmann KK (2005): Replication strategies of rabies virus. Virus Res 111: 120-131.
20. Fitzgerald KA, McWhirter SM, Faia KL, Rowe DC, Latz E, Golenbock DT, Coyle AJ, Liao SM, Maniatis T (2003): IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4: 491-496.
21. Ford E, Thanos D (2010): The transcriptional code of human IFN-beta gene expression. Biochim Biophys Acta 1799: 328-336.
22. Fräser GC, Hooper PT, Lunt RA, Gould AR, Gleeson LJ, Hyatt AD, Russell GM, Kattenbelt JA (1996): Encephalitis caused by a Lyssavirus in fruit bats in Australia. Emerg Infect Dis 2: 327-331.
23. Freuling CM, Beer M, Conraths FJ, Finke S, Hoffmann B, Keller B, Kliemt J, Mettenleiter TC, Muhlbach E, Teifke JP, Wohlsein P, MullerT (2011): Novel Lyssavirus in Natterer's Bat, Germany. Emerg Infect Dis 17: 1519-1522.
24. Fu ZF (2005): Genetic comparison of the rhabdoviruses from animals and plants. CurrTop Microbiol Immunol 292: 1-24.
25. Fu ZF, Jackson AC (2005): Neuronal dysfunction and death in rabies virus infection. J Neurovirol 11: 101-106.
26. Gerard FC, Ribeiro EA Jr., Leyrat C, Ivanov I, Blondel D, Longhi S, Ruigrok RW, Jamin M (2009): Modular organization of rabies virus phosphoprotein. J Mol Biol 388: 978-996.
27. Gerlier D, Lyles DS (2011): Interplay between innate immunity and negative-strand RNA viruses: towards a rational model. Microbiol Mol Biol Rev 75: 468-490.
28. Gitlin L, Benoit L, Song C, Cella M, Gilfillan S, Holtzman MJ, Colonna M (2010): Melanoma differentiation-associated gene 5 (MDA5) is involved in the innate immune response to Paramyxaoiridae infection in vivo. PLoS Pathog 6: el000734.
29. Haller O, Kochs G (2011): Human MxA protein: an interferon-induced dynamin-like GTRase with broad antiviral activity. J Interferon Cytokine Res 31: 79-87.
30. Honda K, Taniguchi T (2006): IRFs: master regulators of signalling by Toll-like receptors and cytosolic pattern-recognition receptors. Nat Rev Immunol 6: 644-658.
31. Hornung V, Ellegast J, Kim S, Brzözka K, Jung A, Kato H, Poeck H, Akira S, Conzelmann KK, Schlee M, Endres S, Hartmann G (2006): 5'-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
32. Hornung V, Schlender J, Guenthner-Biller M, Rothenfusser S, Endres S, Conzelmann KK, Hartmann G (2004): Replication-dependent potent IFN-alpha induction in human plasmacytoid dendritic cells by a single-stranded RNA virus. J Immunol 173: 5935-5943.
33. Hou F, Sun L, Zheng H, Skaug B, Jiang QX, Chen ZJ (2011): MAVS Forms Functional Prion-like Aggregates to Activate and Propagate Antiviral Innate Immune Response. Cell 146: 448-461.
34. Ikegame S, Takeda M, Ohno S, Nakatsu Y, Nakanishi Y, Yanagi Y (2010): Both RIG-I and MDA5 RNA helicases contribute to the induction of alpha/beta interferon in measles virus-infected human cells. J Virol 84: 372-379.
35. I to N, Moseley GW, Blondel D, Shimizu K, Rowe CL, Ito Y, Masatani T, Nakagawa K, Jans DA, Sugiyama M (2010): The Role of Interferon-Antagonist Activity of Rabies Virus Phosphoprotein in Viral Pathogenicity. J Virol 84: 6699-6710.
36. Janeway CA Jr, Medzhitov R (2002): Innate immune recognition. Annu Rev Immunol 20: 197-216.
37. Johnson N, McKimmie CS, Mansfield KL, Wakeley PR, Brookes SM, Fazakerley JK, Fooks AR (2006): Lyssavirus infection activates interferon gene expression in the brain. J Gen Virol 87: 2663-2667.
38. Johnson N, Vos A, Freuling C, Tordo N, Fooks AR, Muller T (2010): Human rabies due to lyssavirus infection of bat origin. Vet Microbiol 142: 151-159.
39. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, Matsui K, Uematsu S, Jung A, Kawai T, Ishii KJ, Yamaguchi O, Otsu K, Tsujimura T, Koh CS, Reis e Sousa, Matsuura Y, Fujita T, Akira S (2006): Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
40. Kawai T, Akira S (2010): The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11: 373-384.
41. Kawai T, Takahashi K, Sato S, Coban C, Kumar H, Kato H, Ishii KJ, Takeuchi O, Akira S (2005): IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat Immunol 6: 981-988.
42. Kerr IM, Brown RE, Ball LA (1974): Increased sensitivity of cell-free protein synthesis to double-stranded RNA after interferon treatment. Nature 250: 57-59.
43. Klingen Y, Conzelmann KK, Finke S (2007): Double-Labeled Rabies Virus Live tracking of enveloped virus transport. J Virol 82: 237-245.
44. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M, Shah NK, Langer JA, Sheikh F, Dickensheets H, Donnelly RP (2003): IFN-lambdas mediate antiviral protection through a distinct class II cytokine receptor complex. Nat Immunol 4: 69-77.
45. Kuz'min IV, Botvinki AD, Khabilov TK (2002): A lyssavirus was isolated from a whiskered bat in Northern Tajikistan. Plecotus et al. 4, 75-81.
46. Kuz'min IV, Botvinkin AD, Rybin SN, Baialiev AB (1992): [A lyssavirus with an unusual antigenic structure isolated from a bat in southern Kyrgyzstan].VoprVirusol 37: 256-259.
47. Kuz'min IV, Mayer AE, Niezgoda M, Markotter W, Agwanda B, Breiman RF, Rupprecht CE (2010): Shimoni bat virus, a new representative of the Lyssavirus genus. Virus Res 149: 197-210.
48. Lafon M (2005): Rabies virus receptors. J Neurovirol 11: 82-87.
49. Lafon M (2008): Immune evasion, a critical strategy for rabies virus. Dev Biol (Basel) 131: 413-419.
50. Le Goffic R, Bailoy V, Lagranderie M, Alexopoulou L, Escriou N, Flavell R, Chignard M, Si-Tahar M (2006): Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog 2: e53.
51. Lebleu B, Sen GC, Shaila S, Cabrer B, Lengyel P (1976): Interferon, double-stranded RNA, and protein phosphorylation. Proc Natl Acad Sei USA 73: 3107-3111.
52. Leppert M, Rittenhouse L, Perrault J, Summers DF, Kolakofsky D (1979): Plus and minus strand leader RNAs in negative strand virus-infected cells. Cell 18: 735-747.
53. Leroy M, Pire G, Baise E, Desmecht D (2006): Expression of the interferon-alpha/beta-inducible bovine Mxl dynamin interferes with replication of rabies virus. Neurobiol Dis 21: 515-521.
54. Li J, Faber M, Dietzschold B, Hooper DC (2011): The role of tolllike receptors in the induction of immune responses during rabies virus infection. Adv Virus Res 79: 115-26.
55. Li M, Liu X, Zhou Y, Su SB (2009): Interferon-lambdas: The modulators of antivirus, antitumor, and immune responses. J Leukoc Biol 86: 23-32.
56. Lumio J, Hillbom M, Roine R, Ketonen L, Haltia M, Valle M, Neuvonen E, Lahdevirta J (1986): Human rabies of bat origin in Europe. Lancet 1: 378.
57. Lund JM, Alexopoulou L, Sato A, Karow M, Adams NC, Gale NW, Iwasaki A, Flavell RA (2004): Recognition of single-stranded RNA viruses by Toll-like receptor 7. Proc Natl Acad Sei USA 101: 5598-5603.
58. Marcovistz R, Galabru J, Tsiang H, Hovanessian AG (1986): Neutralization of interferon produced early during rabies virus infection in mice. J Gen Vtrol 67 (Pt 2): 387-390.
59. Marcovistz R, Germano PM, Riviere Y, Tsiang H, Hovanessian AG (1987): The effect of interferon treatment in rabies prophylaxis in immunocompetent, immunosuppressed, and immuno-deficient mice. J Interferon Res 7: 17-27.
60. Marcovistz R, Leal EC, Matos DC, Tsiang H (1994): Interferon production and immune response induction in apathogenic rabies virus-infected mice. Acta Virol 38: 193-197.
61. Marschalek A, Drechsel L, Conzelmann KK (2011): The importance of being short: The role of rabies virus phosphoprotein isoforms assessed by differential IRES translation initiation. Eur J Cell Biol, doi: 10.1016/j.ejcb.2011.01.009.
62. Marschalek A, Finke S, Schwemmle M, Mayer D, Heimlich B, Stitz L, Conzelmann KK (2009): Attenuation of rabies virus replication and virulence by Picornavirus internal ribosome entiy site elements. J Virol 83: 1911-1919.
63. Masatani T, Ito N, Shimizu K, Ito Y, Nakagawa K, Sawaki Y, Koyama H, Sugiyama M (2010): Rabies virus nucleoprotein functions to evade activation of the RIG-I-mediated antiviral response. J Virol 84: 4002-4012.
64. Menager P, Roux P, Megret F, Bourgeois JP, Le Sourd AM, Danckaert A, Lafage M, Prehaud C, Lafon M (2009): Toll-like receptor 3 (TLR3) plays a major role in the formation of rabies virus Negri Bodies. PLoS Räthog 5: el000315.
65. Meredith CD, Prossouw AP, Koch HP (1971): An unusual case of human rabies thought to be of chiropteran origin. S Afr Med J 45: 767-769.
66. Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, Tschopp J (2005): Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437: 1167-1172.
67. Moseley GW, Filmer RP, Dejesus MA, Jans DA (2007): Nucleo-cytoplasmic Distribution of Rabies Virus P-Protein Is Regulated by Phosphorylation Adjacent to C-Terminal Nuclear Import and Export Signals. Biochemistry 46: 12053-12061.
68. Nadin-Davis SA, Fehlner-Gardiner C (2008): Lyssaviruses: current trends. Adv Virus Res 71: 207-250.
69. Platanias LC (2005): Mechanisms of type-I- and type-II-inter-feron- mediated signalling. Nat Rev Immunol 5: 375-386.
70. Postic B, Fenje P (1971): Effect of administered interferon on rabies in rabbits. Appl Microbiol 22: 428-431.
71. Prehaud C, Wolff N, Temen E, Lafage M, Megret F, Babault N, Cordier F, Tan GS, Maitrepierre E, Menager P, Chopy D, Hoos S, England P, Delepierre M, Schnell MJ, Buc H, Lafon M (2010): Attenuation of rabies virulence: takeover by the cytoplasmic domain of its envelope protein. Sei Signal 3: ra5.
72. Randall RE, Goodbourn S (2008): Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89: 1-47.
73. Rieder M, Brzözka K, Pfaller CK, Cox JH, Stitz L, Conzelmann KK (2011): Genetic dissection of interferon-antagonistic functions of rabies virus phosphoprotein: inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J Virol 85: 842-852.
74. Rieder M, Conzelmann KK (2011): Interferon in rabies virus infection. Adv Virus Res 79: 91-114.
75. Schneider LG, Barnard BJH, Schneider HP (1985): 1. African viruses: Application of monoclonal antibodies for epidemiological investigations and oral vaccination studies. In: Kuwert E, Merieux C, Koprowski H, Bogel K (eds.), Rabies in the Tropics, 47-59, Springer-Verlag, Berlin, Heidelberg, New York, Tokyo.
76. Schnell MJ, McGettigan JP, Wirblich C, Papaneri A (2010): The cell biology of rabies virus: using stealth to reach the brain. Nat Rev Microbiol 8: 51-61.
77. Seth RB, Sun L, Ea CK, Chen ZJ (2005): Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-kappaB and IRF 3. Cell 122: 669-682.
78. Sharma S, tenOever BR, Grandvaux N, Zhou GP, Lin R, Hiscott J (2003): Triggering the interferon antiviral response through an IKK-related pathway. Science 300: 1148-1151.
79. Shope RE, Murphy FA, Harrison AK, Causey OR, Kemp GE, Simpson DI, Moore DL (1970): Two African viruses serologically and morphologically related to rabies virus. J Virol 6: 690-692.
80. Silverman RH (2007): Viral Encounters with OAS and RNase L during the IFN Antiviral Response. J Virol 81: 12720-12729.
81. Sodja I (1975): Interferon production by rabies strains isolated from wild rodents. Acta Virol 19: 84-87.
82. Stewart WE, Sulkin SE (1966): Interferon production in hamsters experimentally infected with rabies virus. Proc Soc Exp Biol Med 123: 650-654.
83. Stojdl DF, Abraham N, Knowles S, Marius R, Brasey A, Lichty BD, Brown EG, Sonenberg N, Bell JC (2000): The murine dou-ble-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J Virol 74: 9580-9585.
84. Theodorides J (1986): Histoire de la rage, Paris, 289.
85. Theofilopoulos AN, Baccala R, Beutler B, Kono DH (2005): Type I interferons (alpha/beta) in immunity and autoimmunity. Ann Rev Immunol 23: 307-335.
86. Ugolini G (2008): Use of rabies virus as a transneuronal tracer of neuronal connections: implications for the understanding of rabies pathogenesis. Dev Biol (Basel) 131: 493-506.
87. Vidal S, Kolakofsky D (1989): Modified model for the switch from Sendai virus transcription to replication. J Virol 63: 1951-1958.
88. Vidy A, Chelbi-Alix M, Blondel D (2005): Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J Virol 79: 14411-14420.
89. Vidy A, EI Bougrini J, Chelbi-Alix MK, Blondel D (2007): The nucleocytoplasmic rabies virus P protein counteracts interferon signaling by inhibiting both nuclear accumulation and DNA binding of STAT1. J Virol 81: 4255-4263.
90. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA (2004): Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat Med 10: 1366-1373.
91. Wang ZW, Sarmento L, Wang Y, Li XQ, Dhingra V, Tseggai T, Jiang B, Fu ZF (2005): Attenuated rabies virus activates, while pathogenic rabies virus evades, the host innate immune responses in the central nervous system. J Virol 79: 12554-12565.
92. Warrell MJ, Warrell DA (2004): Rabies and other lyssavirus diseases. Lancet 363: 959-969.
93. Weber F, Wagner V, Rasmussen SB, Hartmann R, Paludan SR (2006): Double-stranded RNA is produced by positive-strand RNA viruses and DNA viruses but not in detectable amounts by negative-strand RNA viruses. J Virol 80: 5059-5064.
94. Weinmann E, Majer M, Hilfenhaus J (1979): Intramuscular and/ or intralumbar postexposure treatment of rabies virus-infected cynomolgus monkeys with human interferon. Infect Immun 24: 24-31.
95. Whelan SP, Barr JN, Wertz GW (2004): Transcription and replication of nonsegmented negative-strand RNA viruses. Curr Top Microbiol Immunol 283: 61-119.
96. WHO (2005): WHO Expert Consultation on rabies. World Health Organ Tech Rep Ser 931: 1-88.
97. Wickersham IR, Finke S, Conzelmann KK, Callaway EM (2007a): Retrograde neuronal tracing with a deletion-mutant rabies virus. Nat Methods 4: 47-49.
98. Wickersham IR, Lyon DC, Barnard RJ, Mori T, Finke S, Conzelmann KK, Young JA, Callaway EM (2007b): Monosynaptic restriction of transsynaptic tracing from single, genetically targeted neurons. Neuron 53: 639-647.
99. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB (2005): VISA is an adapter protein required for virus-triggered IFN-beta signaling. Mol Cell 19: 727-740.
100. Yoneyama M, Fujita T (2010): Recognition of viral nucleic acids in innate immunity. Rev Med Virol 20: 4-22.
101. Yoneyama M, Kikuchi M, Natsukawa T, Shinobu N, Imaizumi T, Miyagishi M, Taira K, Akira S, Fujita T (2004): The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 5: 730-737.
102. Yoneyama M, Suhara W, Fukuhara Y, Fukuda M, Nishida E, Fujita T (1998): Direct triggering of the type I interferon system by virus infection: activation of a transcription factor complex containing IRF-3 and CBP/p300. EMBO J 17: 1087-1095.