Contribution of the interaction between the rabies virus P protein and I-kappa B kinase ε to the inhibition of type I IFN induction signalling

Journal of General Virology

Volumn 97, Issue 2, 2016, Pages 316-326

  Masatani, Tatsunori ^a   Ozawa, Makoto ^a   Yamada, Kentaro ^b   Ito, Naoto ^c   Horie, Masayuki ^a   Matsuu, Aya ^a   Okuya, Kosuke ^a   Tsukiyama Kohara, Kyoko ^a   Sugiyama, Makoto ^c   Nishizono, Akira ^b  

^a KAGOSHIMA UNIVERSITY   (Japan)

^b OITA UNIVERSITY   (Japan)

^c GIFU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA INTERFERON; BINDING PROTEIN; GLYCINE DEHYDROGENASE (DECARBOXYLATING); I KAPPA B KINASE EPSILON; INTERFERON; INTERFERON REGULATORY FACTOR 3; TANK BINDING KINASE 1; UNCLASSIFIED DRUG; I KAPPA B KINASE; P PHOSPHOPROTEIN, RABIES VIRUS; PHOSPHOPROTEIN; VIRUS PROTEIN;

ARTICLE; CONTROLLED STUDY; EMBRYO; HUMAN; HUMAN CELL; INNATE IMMUNITY; LYSSAVIRUS; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION; RABIES VIRUS; SIGNAL TRANSDUCTION; VIRUS STRAIN; ANTAGONISTS AND INHIBITORS; CELL LINE; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; IMMUNE EVASION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; PROMOTER REGION; PROTEIN ANALYSIS;

CELL LINE; GENE EXPRESSION REGULATION; HOST-PATHOGEN INTERACTIONS; HUMANS; I-KAPPA B KINASE; IMMUNE EVASION; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; PHOSPHOPROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN INTERACTION MAPPING; RABIES VIRUS; TRANSCRIPTION, GENETIC; VIRAL STRUCTURAL PROTEINS;

EID: 84959077604     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/jgv.0.000362     Document Type: Article

References (43)

1. Adli, M. & Baldwin, A. S. (2006). IKK-i/IKKepsilon controls constitutive, cancer cell-associated NF-kappaB activity via regulation of Ser-536 p65/RelA phosphorylation. J Biol Chem 281, 26976-26984.
2. Akira, S., Uematsu, S. & Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell 124, 783-801.
3. Badrane, H., Bahloul, C., Perrin, P. & Tordo, N. (2001). Evidence of two Lyssavirus phylogroups with distinct pathogenicity and immunogenicity. J Virol 75, 3268-3276.
4. Banyard, A. C., Evans, J. S., Luo, T. R. & Fooks, A. R. (2014). Lyssaviruses and bats: emergence and zoonotic threat. Viruses 6, 2974-2990.
5. Blondel, D., Maarifi, G., Nisole, S. & Chelbi-Alix, M. K. (2015). Resistance to Rhabdoviridae infection and subversion of antiviral responses. Viruses 7, 3675-3702.
6. Bonjardim, C. A. (2005). Interferons (IFNs) are key cytokines in both innate and adaptive antiviral immune responses-and viruses counteract IFN action. Microbes Infect 7, 569-578.
7. Brzózka, K., Finke, S. & Conzelmann, K. K. (2005). Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J Virol 79, 7673-7681.
8. Brzózka, K., Finke, S. & Conzelmann, K. K. (2006). Inhibition of interferon signaling by rabies virus phosphoprotein P: activationdependent binding of STAT1 and STAT2. J Virol 80, 2675-2683.
9. Chenik, M., Chebli, K., Gaudin, Y. & Blondel, D. (1994). In vivo interaction of rabies virus phosphoprotein (P) and nucleoprotein (N): existence of two N-binding sites on P protein. J Gen Virol 75, 2889-2896.
10. Chenik, M., Schnell, M., Conzelmann, K. K. & Blondel, D. (1998). Mapping the interacting domains between the rabies virus polymerase and phosphoprotein. J Virol 72, 1925-1930.
11. Dietzschold, B., Li, J., Faber, M. & Schnell, M. (2008). Concepts in the pathogenesis of rabies. Future Virol 3, 481-490.
12. Finke, S. & Conzelmann, K. K. (2005). Replication strategies of rabies virus. Virus Res 111, 120-131.
13. 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. (2003). IKKepsilon and TBK1 are essential components of the IRF3 signaling pathway. Nat Immunol 4, 491-496.
14. Fouquet, B., Nikolic, J., Larrous, F., Bourhy, H., Wirblich, C., Lagaudriè re-Gesbert, C. & Blondel, D. (2015). Focal adhesion kinase is involved in rabies virus infection through its interaction with viral phosphoprotein P. J Virol 89, 1640-1651.
15. Hornung, V., Ellegast, J., Kim, S., Brzózka, K., Jung, A., Kato, H., Poeck, H., Akira, S., Conzelmann, K. K. & other authors (2006). 59-Triphosphate RNA is the ligand for RIG-I. Science 314, 994-997.
16. Ishikawa, Y., Samejima, T., Nunoya, T., Motohashi, T. & Nomura, Y. (1989). Biological properties of the cell culture-adapted RC-HL strain of rabies virus as a candidate strain for an inactivated vaccine. J Jpn Vet Med Assoc 42, 637-643.
17. Ito, N., Moseley, G. W., Blondel, D., Shimizu, K., Rowe, C. L., Ito, Y., Masatani, T., Nakagawa, K., Jans, D. A. & Sugiyama, M. (2010). Role of interferon antagonist activity of rabies virus phosphoprotein in viral pathogenicity. J Virol 84, 6699-6710.
18. Kato, H., Takeuchi, O., Sato, S., Yoneyama, M., Yamamoto, M., Matsui, K., Uematsu, S., Jung, A., Kawai, T. & other authors (2006). Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441, 101-105.
19. Kobasa, D., Rodgers, M. E., Wells, K. & Kawaoka, Y. (1997). Neuraminidase hemadsorption activity, conserved in avian influenza A viruses, does not influence viral replication in ducks. J Virol 71, 6706-6713.
20. Koraka, P., Martina, B. E., Roose, J. M., van Thiel, P. P., van Amerongen, G., Kuiken, T. & Osterhaus, A. D. (2012). In vitro and in vivo isolation and characterization of Duvenhage virus. PLoS Pathog 8, e1002682.
21. Lépine, P. (1938). On the evolution of fixed strains of rabies virus. J Hyg (Lond) 38, 180-184.
22. Lieu, K. G., Brice, A., Wiltzer, L., Hirst, B., Jans, D. A., Blondel, D. & Moseley, G. W. (2013). The rabies virus interferon antagonist P protein interacts with activated STAT3 and inhibits Gp130 receptor signaling. J Virol 87, 8261-8265.
23. 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.
24. Mifune, K., Makino, Y. & Mannen, K. (1979). Susceptibility of various cell lines to rabies virus. J Trop Med Hyg 7, 201-208.
25. Ng, S. L., Friedman, B. A., Schmid, S., Gertz, J., Myers, R. M., Tenoever, B. R. & Maniatis, T. (2011). IkB kinase epsilon (IKKe) regulates the balance between type I and type II interferon responses. Proc Natl Acad Sci U S A 108, 21170-21175.
26. Niu, X., Tang, L., Tseggai, T., Guo, Y. & Fu, Z. F. (2013). Wild-type rabies virus phosphoprotein is associated with viral sensitivity to type I interferon treatment. Arch Virol 158, 2297-2305.
27. Nolden, T., Banyard, A. C., Finke, S., Fooks, A. R., Hanke, D., Höper, D., Horton, D. L., Mettenleiter, T. C., Müller, T. & other authors (2014). Comparative studies on the genetic, antigenic and pathogenic characteristics of Bokeloh bat lyssavirus. J Gen Virol 95, 1647-1653.
28. Oksayan, S., Nikolic, J., David, C. T., Blondel, D., Jans, D. A. & Moseley, G. W. (2015). Identification of a role for nucleolin in rabies virus infection. J Virol 89, 1939-1943.
29. Pham, A. M. & Tenoever, B. R. (2010). The IKK kinases: operators of antiviral signaling. Viruses 2, 55-72.
30. Randall, R. E. & Goodbourn, S. (2008). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89, 1-47.
31. Rieder, M., Brzózka, K., Pfaller, C. K., Cox, J. H., Stitz, L. & Conzelmann, K. K. (2011). Genetic dissection of interferonantagonistic functions of rabies virus phosphoprotein: inhibition of interferon regulatory factor 3 activation is important for pathogenicity. J Virol 85, 842-852.
32. Schnell, M. J., McGettigan, J. P., Wirblich, C. & Papaneri, A. (2010). The cell biology of rabies virus: using stealth to reach the brain. Nat Rev Microbiol 8, 51-61.
33. Sharma, S., tenOever, B. R., Grandvaux, N., Zhou, G. P., Lin, R. & Hiscott, J. (2003). Triggering the interferon antiviral response through an IKK-related pathway. Science 300, 1148-1151.
34. Shimada, T., Kawai, T., Takeda, K., Matsumoto, M., Inoue, J., Tatsumi, Y., Kanamaru, A. & Akira, S. (1999). IKK-i, a novel lipopolysaccharide-inducible kinase that is related to IkappaB kinases. Int Immunol 11, 1357-1362.
35. Tenoever, B. R., Ng, S. L., Chua, M. A., McWhirter, S. M., García-Sastre, A. & Maniatis, T. (2007). Multiple functions of the IKKrelated kinase IKKepsilon in interferon-mediated antiviral immunity. Science 315, 1274-1278.
36. van Boxel-Dezaire, A. H., Rani, M. R. & Stark, G. R. (2006). Complex modulation of cell type-specific signaling in response to type I interferons. Immunity 25, 361-372.
37. 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.
38. Vidy, A., El Bougrini, J., Chelbi-Alix, M. K. & 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.
39. Wiltzer, L., Larrous, F., Oksayan, S., Ito, N., Marsh, G. A., Wang, L. F., Blondel, D., Bourhy, H., Jans, D. A. & Moseley, G. W. (2012). Conservation of a unique mechanism of immune evasion across the Lyssavirus genus. J Virol 86, 10194-10199.
40. Wiltzer, L., Okada, K., Yamaoka, S., Larrous, F., Kuusisto, H. V., Sugiyama, M., Blondel, D., Bourhy, H., Jans, D. A. & other authors (2014). Interaction of rabies virus P-protein with STAT proteins is critical to lethal rabies disease. J Infect Dis 209, 1744-1753.
41. Yamagata, J., Ahmed, K., Khawplod, P., Mannen, K., Xuyen, D. K., Loi, H. H., Dung, N. V. & Nishizono, A. (2007). Molecular epidemiology of rabies in Vietnam. Microbiol Immunol 51, 833-840.
42. Yoneyama, M., Suhara, W., Fukuhara, Y., Sato, M., Ozato, K. & Fujita, T. (1996). Autocrine amplification of type I interferon gene expression mediated by interferon stimulated gene factor 3 (ISGF3). J Biochem 120, 160-169.
43. Yoneyama, M., Kikuchi, M., Matsumoto, K., Imaizumi, T., Miyagishi, M., Taira, K., Foy, E., Loo, Y. M., Gale, M. Jr. & other authors (2005). Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J Immunol 175, 2851-2858.