Paramyxovirus Sendai virus V protein counteracts innate virus clearance through IRF-3 activation, but not via interferon, in mice

Virology

Volumn 359, Issue 1, 2007, Pages 82-91

  Kiyotani, Katsuhiro ^a   Sakaguchi, Takemasa ^a   Kato, Atsushi ^b   Nagai, Yoshiyuki ^c   Yoshida, Tetsuya ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c RIKEN YOKOHAMA INSTITUTE   (Japan)

Author keywords

Interferon; IRF 3; Pathogenesis; Sendai virus; V protein

Indexed keywords

INTERFERON; INTERFERON REGULATORY FACTOR 3; VIRUS PROTEIN V;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; DOWN REGULATION; GENE MUTATION; LUNG; MALE; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN INTERACTION; SENDAI VIRUS; VIRUS ACTIVATION; VIRUS REPLICATION; WILD TYPE;

ANIMALS; DISEASE MODELS, ANIMAL; FEMALE; IMMUNITY, NATURAL; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; LUNG; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUTATION; RECEPTORS, INTERFERON; RESPIROVIRUS INFECTIONS; SENDAI VIRUS; SEQUENCE DELETION; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; VIRAL PROTEINS; VIRUS REPLICATION;

MUS; PARAMYXOVIRIDAE; SENDAI VIRUS;

EID: 33846807479     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2006.08.053     Document Type: Article

References (57)

1. Anderson S.L., Carton J.M., Lou J., Xing L., and Rubin B.Y. Interferon-induced guanylate binding protein-1 (GBP-1) mediates an antiviral effect against vesicular stomatitis virus and encephalomyocarditis virus. Virology 256 (1999) 8-14
2. Andrejeva J., Childs K.S., Young D.F., Carlos T.S., Stock N., Goodbourn S., and Randall R.E. The V proteins of paramyxoviruses bind the IFN-inducible RNA helicases, mda-5, and inhibit its activation of the IFN-β promoter. Proc. Natl. Acad. Sci. U.S.A. 101 (2004) 17264-17269
3. Chin K.-C., and Cresswell P. Viperin (cig5), an IFN-inducible antiviral protein directly induced by human cytomegalovirus. Proc. Natl. Acad. Sci. U.S.A. 98 (2001) 15125-15130
4. Curran J., Marq J.B., and Kolakofsky D. The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189 (1992) 647-656
5. Didcock L., Young D.F., Goodbourn S., and Randall R.E. Sendai virus and simian virus 5 block activation of interferon-responsive gene: importance for virus pathogenesis. J. Virol. 73 (1999) 3125-3133
6. Didcock L., Young D.F., Goodbourn S., and Randall R.E. The V protein of simian virus 5 inhibits interferon signaling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73 (1999) 9928-9933
7. Fujii Y., Sakaguchi T., Kiyotani K., Huang C., Fukuhara N., Egi Y., and Yoshida T. Involvement of the leader sequence in Sendai virus pathogenesis revealed by recovery of a pathogenic field isolate from cDNA. J. Virol. 76 (2002) 8540-8547
8. Fukuhara N., Huang C., Kiyotani K., Yoshida T., and Sakaguchi T. Mutational analysis of the Sendai virus V protein: importance of the conserved residues for Zn binding, virus pathogenesis, and efficient RNA editing. Virology 299 (2002) 181-182
9. Garcia-Sastre A. Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279 (2001) 375-384
10. Garcia-Sastre A. Identification and characterization of viral antagonists of type I interferon in negative-strand RNA viruses. Curr. Top. Microbiol. Immunol. 283 (2004) 249-280
11. Garcin D., Latorre P., and Kolakofsky D. Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J. Virol. 73 (1999) 6559-6565
12. Goodbourn S., Didcock L., and Randall R.E. Interferons: cell signaling, immune modulation, antiviral responses and virus countermeasures. J. Gen. Virol. 81 (2000) 2341-2364
13. Gotoh B., Takeuchi K., Komatsu T., Yokoo J., Kimura Y., Kurotani A., Kato A., and Nagai Y. Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferon-alpha/beta-mediated responses. FEBS Lett. 459 (1999) 205-210
14. Gotoh B., Komatsu T., Takeuchi K., and Yokoo J. Paramyxovirus accessory proteins as interferon antagonists. Microbiol. Immunol. 45 (2001) 787-800
15. Gotoh B., Komatsu T., Takeuchi K., and Yokoo J. Paramyxovirus strategies for evading the interferon response. Rev. Med. Virol. 12 (2002) 337-357
16. Gotoh B., Komatsu T., Takeuchi K., and Yokoo J. The C-terminal half-fragment of the Sendai virus C protein prevents the gamma-activated factor from binding to a gamma-activated sequence site. Virology 316 (2003) 29-40
17. Gotoh B., Komatsu T., Takeuchi K., and Yokoo J. The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J. Virol. 77 (2003) 3360-3370
18. Grandvaux N., Servant M.J., tenOever B., Sen G.C., Balachandran S., Barber G.N., Lin R., and Hiscott J. Transcriptional profiling of interferon regulatory factor 3 target genes: distinct involvement in the regulation of interferon-stimulated genes. J. Virol. 76 (2002) 5532-5539
19. Grandvaux N., Gaboriau F., Harris J., tenOever B.R., Lin R., and Hiscott J. Regulation of arginase II by interferon regulatory factor 3 and the involvement of polyamines in the antiviral response. FEBS J. 272 (2005) 3120-3131
20. Hasan M.K., Kato A., Muranaka M., Yamaguchi R., Sakai Y., Hatano I., Tashiro M., and Nagai Y. Versatility of the accessory C proteins of Sendai virus: contribution to virus assembly as an additional role. J. Virol. 74 (2000) 5619-5628
21. He B., Paterson R.G., Stock N., Durbin J.E., Durbin R.K., Goodbourn S., Randall R.E., and Lamb R.A. Recovery of paramyxovirus simian virus 5 with a V protein lacking the conserved cysteine-rich domain: the multifunctional V protein blocks both interferon-beta induction and interferon signaling. Virology 303 (2002) 15-32
22. Heylbroeck C., Balachandran S., Servant M.J., DeLuca C., Barber G.N., Lin R., and Hiscott J. The IRF-3 transcription factor mediates Sendai virus-induced apoptosis. J. Virol. 74 (2000) 3781-3792
23. Horvath C.M. Weapons of STAT destruction. Interferon evasion by paramyxovirus V protein. Eur. J. Biochem. 271 (2004) 4621-4628
24. Honda K., Yanai H., Negishi H., Asagiri M., Sato M., Mizutani T., Shimada N., Ohba Y., Takaoka A., Yoshida N., and Taniguchi T. IRF-7 is the master regulator of type I interferon-dependent immune responses. Nature 434 (2005) 772-777
25. Huang C., Kiyotani K., Fujii Y., Fukuhara N., Kato A., Nagai Y., Yoshida T., and Sakaguchi T. Involvement of the zinc-binding capacity of Sendai virus V protein in viral pathogenesis. J. Virol. 74 (2000) 7834-7841
26. Ishida N., and Homma M. Sendai virus. Adv. Virus Res. 23 (1978) 349-383
27. Izaguirre A., Barnes B.J., Amrute S., Yeow W.-S., Megjugorac N., Dai J., Feng D., Chung E., Pitha P.M., and Fitzgerald-Bocarsly P. Comparative analysis of IRF and IFN-alpha expression in human plasmacytoid and monocyte-derived dendritic cells. J. Leukoc. Biol. 74 (2003) 1125-1138
28. Kato A., Sakai Y., Shioda T., Kondo T., Nakanishi M., and Nagai Y. Initiation of Sendai virus replication from transfected cDNA or RNA with negative or positive sense. Genes Cells 1 (1996) 569-579
29. Kato A., Kiyotani K., Sakai Y., Yoshida T., and Nagai Y. The paramyxovirus, Sendai virus, V protein encodes a luxury function required for viral pathogenesis. EMBO J. 16 (1997) 578-587
30. Kato A., Kiyotani K., Sakai Y., Yoshida T., and Nagai Y. Importance of the cysteine-rich carboxyl-terminal half of V protein for Sendai virus pathogenesis. J. Virol. 71 (1997) 7266-7272
31. Kato A., Cortese-Grogan C., Moyer S.A., Sugahara F., Sakaguchi T., Kubota T., Otsuki N., Kohase M., Tashiro M., and Nagai Y. Characterization of the amino acid residues of Sendai virus C protein that are critically involved in its interferon antagonism and RNA synthesis down-regulation. J. Virol. 78 (2004) 7443-7454
32. Kiyotani K., Takao S., Sakaguchi T., and Yoshida T. Immediate protection of mice from lethal wild-type Sendai virus (HVJ) infections by a temperature-sensitive mutant, HVJpi, possessing homologous interfering capacity. Virology 177 (1990) 65-74
33. Komatsu T., Takeuchi K., Yokoo J., Tanaka Y., and Gotoh B. Sendai virus blocks alpha interferon signaling to signal transducers and activator of transcription. J. Virol. 74 (2000) 2477-2480
34. Komatsu T., Takeuchi K., Yokoo J., and Gotoh B. Sendai virus C protein impairs both phosphorylation and dephosphorylation processes of Stat1. FEBS Lett. 511 (2002) 139-144
35. Komatsu T., Takeuchi K., Yokoo J., and Gotoh B. C and V proteins of Sendai virus target signaling pathways leading to IRF-3 activation for the negative regulation of interferon-β production. Virology 325 (2004) 137-148
36. Kurotani A., Kiyotani K., Kato A., Shioda T., Sakai Y., Mizumoto K., Yoshida T., and Nagai Y. Sendai virus C proteins are categorically nonessential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3 (1998) 111-124
37. Lamb R.A., and Kolakofsky D. Paramyxoviridae: the viruses and their replication. In: Knipe D.M., Howley P.M., et al. (Eds). Fields Virology. 4th ed. vol. 1 (2001), Lippincott Williams and Wilkins, Philadelphia 1305-1340
38. Lenschow D.J., Giannakopoulos N.V., Gunn L.J., Johnston C., O'Guin A.K., Schmidt R.E., Levine B., and Virgin IV H.W. Identification of interferon-stimulated gene 15 as an antiviral molecule during Sindbis virus infection in vivo. J. Virol. 79 (2005) 13974-13983
39. Lin R., Heylbroeck C., Genin P., Pitha P.M., and Hiscott J. Essential role of interferon regulatory factor 3 in direct activation of RANTES chemokine transcription. Mol. Cell. Biol. 19 (1999) 959-966
40. Liston P.D., and Briedis J. Measles virus V protein binds zinc. Virology 198 (1994) 399-404
41. Nagai Y. Paramyxovirus replication and pathogenesis. Reverse genetics transforms understanding. Rev. Med. Virol. 9 (1999) 83-99
42. Nagai Y., and Kato A. Accessory genes of the Paramyxoviridae, a large family of nonsegmented negative strand RNA viruses, as a focus of active investigation by reverse genetics. Curr. Top. Microbiol. Immunol. 283 (2004) 198-248
43. Nakaya T., Sato M., Hata N., Asagiri M., Suemori H., Noguchi S., Tanaka N., and Taniguchi T. Gene induction pathways mediated by distinct IRFs during viral infection. Biochem. Biophys. Res. Commun. 283 (2001) 1150-1156
44. Nicholl M.J., Robinson L.H., and Preston C.M. Activation of cellular interferon-responsive genes after infection of human cells with herpes simplex virus type 1. J. Gen. Virol. 81 (2000) 2215-2218
45. Paterson R.G., Leser G.P., Shaughnessy M.A., and Lamb R.A. The paramyxovirus SV5 V protein binds two atoms of zinc and is a structural component of virions. Virology 208 (1995) 121-131
46. Poole E., He B., Lamb R.A., Randall R.E., and Goodbourn S. The V proteins of simian virus 5 and other paramyxoviruses inhibit induction of interferon-beta. Virology 303 (2002) 33-46
47. Ritchie K.J., Hahn C.S., Kim K., Yan M., Rosario D., Li L., de la Torre J.C., and Zhang D.-E. Role of ISG15 protease UBP43 (USP18) in innate immunity to viral infection. Nat. Med. 10 (2004) 1374-1378
48. Sakaguchi T., Uchiyama T., Fujii Y., Kiyotani K., Kato A., Nagai Y., Kawai A., and Yoshida T. Double-layered membrane vesicles released from mammalian cells infected with Sendai virus expressing the matrix protein of vesicular stomatitis virus. Virology 263 (1999) 230-243
49. Sakaguchi T., Kiyotani K., Watanabe H., Huang C., Fukuhara N., Fujii Y., Shimazu Y., Sugahara F., Nagai Y., and Yoshida T. Masking of the contribution of V protein to Sendai virus pathogenesis in a infection model with a highly virulent field isolate. Virology 313 (2003) 581-587
50. Sen G.C. Viruses and interferons. Annu Rev. Microbiol. 55 (2001) 255-281
51. Steward M., Samson A.C., Errington W., and Emmerson P.T. The Newcastle disease virus V protein binds zinc. Arch. Virol. 140 (1995) 1321-1328
52. Sugahara F., Uchiyama T., Watanabe H., Shimazu Y., Kuwayama M., Fujii Y., Kiyotani K., Adachi A., Kohno N., Yoshida T., and Sakaguchi T. Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325 (2004) 1-10
53. Takeuchi K., Komatsu T., Yokoo J., Kato A., Shioda T., Nagai Y., and Gotoh B. Sendai virus C protein physically associates with Stat1. Genes Cells 6 (2001) 545-557
54. Taniguchi T., and Takaoka A. The interferon-α/β system in antiviral responses: a multimodal machinery of gene regulation by the IRF family of transcription factors. Curr. Opin. Immunol. 14 (2002) 111-116
55. Tashiro M., and Homma M. Pneumotropism of Sendai virus in relation to protease-mediated activation in mouse lung. Infect. Immun. 39 (1983) 879-888
56. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., and Fujita T. The RNA helicase RIG-I has essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
57. Yoneyama M., Kikuchi M., Matsumoto K., Imaizumi T., Miyagishi M., Taira K., Foy E., Loo Y.M., Gale Jr. M., Akira S., Yonehara S., Kato A., and Fujita T. Shared and unique functions of the DExD/H-box helicases RIG-I, MDA5, and LGP2 in antiviral innate immunity. J. Immunol. 175 (2005) 2851-2858