Interaction of Rabies virus P-protein with STAT proteins is critical to lethal rabies disease

Journal of Infectious Diseases

Volumn 209, Issue 11, 2014, Pages 1744-1753

  Wiltzer, Linda ^a   Okada, Kazuma ^b   Yamaoka, Satoko ^b   Larrous, Florence ^c,d   Kuusisto, Henna Veera ^a   Sugiyama, Makoto ^b   Blondel, Danielle ^e   Bourhy, Hervé ^c   Jans, David Andrew ^a   Ito, Naoto ^b   Moseley, Gregory William ^a,f  

^a MONASH UNIVERSITY   (Australia)

^b GIFU UNIVERSITY   (Japan)

^c INSTITUT PASTEUR   (France)

^d UNIVERSITÉ PARIS DESCARTES   (France)

^e CNRS   (France)

^f UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Duvenhage virus; immune evasion; interferon; interferon antagonist; lyssavirus; pathogenicity; rabies virus; replication; signal transducers and activators of transcription; Viral disease

Indexed keywords

GUANINE NUCLEOTIDE BINDING PROTEIN; LUCIFERASE; STAT PROTEIN; VIRUS PROTEIN;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; GENE REPLICATION; HYDROPHOBICITY; IMMUNOPRECIPITATION; IN VIVO STUDY; MALE; MOUSE; MUTAGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; RABIES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; STRUCTURE ANALYSIS; VIRUS MUTATION;

DUVENHAGE VIRUS; IMMUNE EVASION; INTERFERON; INTERFERON ANTAGONIST; LYSSAVIRUS; PATHOGENICITY; RABIES VIRUS; REPLICATION; SIGNAL TRANSDUCERS AND ACTIVATORS OF TRANSCRIPTION; VIRAL DISEASE;

ANIMALS; CELL LINE; FEMALE; GENE EXPRESSION REGULATION; GENOME, VIRAL; HUMANS; INTERFERONS; MICE; MODELS, MOLECULAR; MUTATION; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN CONFORMATION; RABIES; RABIES VIRUS; STAT TRANSCRIPTION FACTORS; TWO-HYBRID SYSTEM TECHNIQUES; VIRAL STRUCTURAL PROTEINS; VIRUS REPLICATION;

EID: 84900547119     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jit829     Document Type: Article

References (44)

1. Knobel DL, Cleaveland S, Coleman PG, et al. Re-evaluating the burden of rabies in Africa and Asia. BullWorld Health Organ 2005; 83: 360-8.
2. Evans JS, Horton DL, Easton AJ, Fooks AR, Banyard AC. Rabies virus vaccines: Is there a need for a pan-lyssavirus vaccine? Vaccine 2012; 30: 7447-54.
3. Randall RE, Goodbourn S. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 2008; 89: 1-47.
4. Versteeg GA, Garcia-Sastre A. Viral tricks to grid-lock the type I interferon system. Curr Opin Microbiol 2010; 13: 508-16.
5. Najjar I, Fagard R. STAT1 and pathogens, not a friendly relationship. Biochimie 2010; 92: 425-44.
6. Oksayan S, Ito N, Moseley G, Blondel D. Subcellular trafficking in rhabdovirus infection and immune evasion: a novel target for therapeutics. Infect Disord Drug Targets 2012; 12: 38-58.
7. Devaux P, Hudacek AW, Hodge G, Reyes-Del Valle J, McChesney MB, Cattaneo R. A recombinant measles virus unable to antagonize STAT1 function cannot control inflammation and is attenuated in rhesus monkeys. J Virol 2011; 85: 348-56.
8. Brzozka K, Finke S, Conzelmann KK. Identification of the rabies virus alpha/beta interferon antagonist: phosphoprotein P interferes with phosphorylation of interferon regulatory factor 3. J Virol 2005; 79: 7673-81.
9. Lieu KG, Brice A, Wiltzer L, et al. The Rabies Virus Interferon Antagonist P Protein Interacts with Activated STAT3 and Inhibits Gp130 Receptor Signaling. J Virol 2013; 87: 8261-5.
10. Vidy A, Chelbi-Alix M, Blondel D. Rabies virus P protein interacts with STAT1 and inhibits interferon signal transduction pathways. J Virol 2005; 79: 14411-20.
11. Pasdeloup D, Poisson N, Raux H, Gaudin Y, Ruigrok RW, 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: 284-93.
12. Wiltzer L, Larrous F, Oksayan S, et al. Conservation of a Unique Mechanism of Immune Evasion across the Lyssavirus Genus. J Virol 2012; 86: 10194-9.
13. Assenberg R, Delmas O, Ren J, et al. Structure of the nucleoprotein binding domain of Mokola virus phosphoprotein. J Virol 2010; 84: 1089-96.
14. Mavrakis M, McCarthy AA, Roche S, Blondel D, Ruigrok RW. Structure and function of the C-terminal domain of the polymerase cofactor of rabies virus. J Mol Biol 2004; 343: 819-31.
15. Rothenfusser S, Goutagny N, DiPerna G, et al. The RNA helicase Lgp2 inhibits TLR-independent sensing of viral replication by retinoic acidinducible gene-I. J Immunol 2005; 175: 5260-8.
16. Raux H, Flamand A, Blondel D. Interaction of the rabies virus P protein with the LC8 dynein light chain. J Virol 2000; 74: 10212-6.
17. Ito N, Moseley GW, Blondel D, et al. Role of interferon antagonist activity of rabies virus phosphoprotein in viral pathogenicity. J Virol 2010; 84: 6699-710.
18. Schubert D, Humphreys S, Baroni C, Cohn M. In vitro differentiation of a mouse neuroblastoma. Proc Natl Acad Sci U S A 1969; 64: 316-23.
19. Shimizu K, Ito N, Sugiyama M, Minamoto N. Sensitivity of rabies virus to type I interferon is determined by the phosphoprotein gene. Microbiol Immunol 2006; 50: 975-8.
20. Masatani T, Ito N, Ito Y, et al. Importance of rabies virus nucleoprotein in viral evasion of interferon response in the brain. Microbiol Immunol 2013; 57: 511-7.
21. Koraka P, Martina BE, Roose JM, et al. In vitro and in vivo isolation and characterization of duvenhage virus. PLoS Pathog 2012; 8: e1002682.
22. Brzozka K, Finke S, Conzelmann KK. Inhibition of interferon signaling by rabies virus phosphoprotein P: activation-dependent binding of STAT1 and STAT2. J Virol 2006; 80: 2675-83.
23. Assenberg R, Delmas O, Morin B, et al. Genomics and structure/function studies of Rhabdoviridae proteins involved in replication and transcription. Antiviral Res 2010; 87: 149-61.
24. Niu X, Tang L, Tseggai T, Guo Y, Fu ZF. Wild-type rabies virus phosphoprotein is associated with viral sensitivity to type I interferon treatment. Arch Virol 2013; 158: 2297-305.
25. Leroy M, Baise E, Pire G, Gerardin J, Desmecht D. Resistance of paramyxoviridae to type I interferon-induced Bos taurus Mx1 dynamin. J Interferon Cytokine Res 2005; 25: 192-201.
26. Chenik M, Chebli K, Gaudin Y, Blondel D. In vivo interaction of rabies virus phosphoprotein (P) and nucleoprotein (N): existence of two N-binding sites on P protein. J Gen Virol 1994; 75 (Pt 11): 2889-96.
27. Rieder M, Brzozka K, Pfaller CK, Cox JH, Stitz L, Conzelmann KK. 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: 842-52.
28. Biacchesi S, LeBerre M, Lamoureux A, et al. Mitochondrial antiviral signaling protein plays a major role in induction of the fish innate immune response against RNA and DNA viruses. J Virol 2009; 83: 7815-27.
29. Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol 2004; 5: 730-7.
30. Desmyter J, Melnick JL, Rawls WE. Defectiveness of interferon production and of rubella virus interference in a line of African green monkey kidney cells (Vero). J Virol 1968; 2: 955-61.
31. Lahaye X, Vidy A, Pomier C, et al. 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: 7948-58.
32. Moseley GW, Lahaye X, Roth DM, et al. Dual modes of rabies Pprotein association with microtubules: a novel strategy to suppress the antiviral response. J Cell Sci 2009; 122: 3652-62.
33. Moseley GW, Roth DM, DeJesus MA, et al. Dynein light chain association sequences can facilitate nuclear protein import. Mol Biol Cell 2007; 18: 3204-13.
34. Oksayan S, Wiltzer L, Rowe CL, Blondel D, Jans DA, Moseley GW. A novel nuclear trafficking module regulates the nucleocytoplasmic localization of the rabies virus interferon antagonist, P protein. J Biol Chem 2012; 287: 28112-21.
35. Shimizu K, Ito N, Mita T, et al. Involvement of nucleoprotein, phosphoprotein, and matrix protein genes of rabies virus in virulence for adult mice. Virus Res 2007; 123: 154-60.
36. Sorgeloos F, Kreit M, Hermant P, Lardinois C, Michiels T. Antiviral type I and type III interferon responses in the central nervous system. Viruses 2013; 5: 834-57.
37. Griffin DE. Immune responses to RNA-virus infections of the CNS. Nat Rev Immunol 2003; 3: 493-502.
38. Audsley MD, Moseley GW. Paramyxovirus evasion of innate immunity: Diverse strategies for common targets.World J Virol 2013; 2: 14.
39. Ramachandran A, Horvath CM. Paramyxovirus disruption of interferon signal transduction: STATus report. J Interferon Cytokine Res 2009; 29: 531-7.
40. Ciancanelli MJ, Volchkova VA, Shaw ML, Volchkov VE, Basler CF. Nipah virus sequesters inactive STAT1 in the nucleus via a P geneencoded mechanism. J Virol 2009; 83: 7828-41.
41. Leung DW, Prins KC, Borek DM, et al. Structural basis for dsRNA recognition and interferon antagonism by Ebola VP35. Nat Struct Mol Biol 2010; 17: 165-72.
42. Ye J, Zhu B, Fu ZF, Chen H, Cao S. Immune evasion strategies of flaviviruses. Vaccine 2013; 31: 461-71.
43. Wunner WH, Conzelmann KK. Rabies virus. In: Jackson AC, ed. Rabies: scientific basis of the disease and its management. 3 ed. Academic Press, Elsevier, 2013.
44. Richt JA, Garcia-Sastre A. Attenuated influenza virus vaccines with modified NS1 proteins. Curr TopMicrobiol Immunol 2009; 333: 177-95.