Conserved charged amino acids within sendai virus C protein play multiple roles in the evasion of innate immune responses

PLoS ONE

Volumn 5, Issue 5, 2010, Pages

  Irie, Takashi ^a   Nagata, Natsuko ^a   Igarashi, Tomoki ^a   Okamoto, Isao ^a   Sakaguchi, Takemasa ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; AMINO ACID; ASPARTIC ACID; BETA INTERFERON; CYSTEINE; CYTOKINE; DOUBLE STRANDED RNA; GLUTAMIC ACID; INTERFERON REGULATORY FACTOR 3; LYSINE; PHENYLALANINE; PROTEIN C; SERINE; VIRUS RNA; IRF3 PROTEIN, HUMAN; NONSTRUCTURAL C PROTEIN, SENDAI VIRUS; POLYINOSINIC POLYCYTIDYLIC ACID; VIRUS PROTEIN;

AMINO ACID SUBSTITUTION; ANIMAL CELL; ARTICLE; CELL DEATH; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPATHOGENIC EFFECT; ENZYME ACTIVATION; GENE TRANSLOCATION; GENETIC CONSERVATION; HUMAN; HUMAN CELL; INNATE IMMUNITY; MUTATIONAL ANALYSIS; NONHUMAN; PROTEIN DEPLETION; PROTEIN FUNCTION; RNA SYNTHESIS; SENDAI VIRUS; SIGNAL TRANSDUCTION; VIROGENESIS; VIRUS RECOMBINANT; VIRUS REPLICATION; BIOSYNTHESIS; CELL NUCLEUS; CHEMISTRY; DRUG EFFECT; GENETIC RECOMBINATION; GENETICS; HELA CELL; IMMUNE EVASION; IMMUNOLOGY; KINETICS; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN TRANSPORT; RESPIROVIRUS INFECTION; STRUCTURE ACTIVITY RELATION; VIRION; VIROLOGY; VIRUS GENOME;

MUS; SENDAI VIRUS;

AMINO ACIDS; CELL NUCLEUS; CONSERVED SEQUENCE; CYTOPATHOGENIC EFFECT, VIRAL; GENOME, VIRAL; HELA CELLS; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; INTERFERON REGULATORY FACTOR-3; INTERFERON-BETA; KINETICS; MUTATION; POLY I-C; PROTEIN TRANSPORT; RECOMBINATION, GENETIC; RESPIROVIRUS INFECTIONS; RNA, DOUBLE-STRANDED; SENDAI VIRUS; SIGNAL TRANSDUCTION; STRUCTURE-ACTIVITY RELATIONSHIP; VIRAL PROTEINS; VIRION;

EID: 77956292108     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0010719     Document Type: Article

References (39)

1. Lamb RA, Parks GD (2006) Paramyxoviridae: the viruses and their replication. In: Knipe DM, Howley PM, eds. Fields virology, 5th ed. PhiladelphiaPA: Lippincott, Williams & Wilkins. pp 1449-1496.
2. Garcin D, Latorre P, Kolakofsky D (1999) Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J Virol 73: 6559-6565.
3. Garcin D, Curran J, Itoh M, Kolakofsky D (2001) Longer and shorter forms of Sendai virus C proteins play different roles in modulating the cellular antiviral response. J Virol 75: 6800-6807.
4. Garcin D, Marq JB, Strahle L, le Mercier P, Kolakofsky D (2002) All four Sendai Virus C proteins bind Stat1, but only the larger forms also induce its mono-ubiquitination and degradation. Virology 295: 256-265.
5. Kato A, Ohnishi Y, Hishiyama M, Kohase M, Saito S, et al. (2002) The aminoterminal half of Sendai virus C protein is not responsible for either counteracting the antiviral action of interferons or down-regulating viral RNA synthesis. J Virol 76: 7114-7124.
6. Kato A, Ohnishi Y, Kohase M, Saito S, Tashiro M, et al. (2001) Y2, the smallest of the Sendai virus C proteins, is fully capable of both counteracting the antiviral action of interferons and inhibiting viral RNA synthesis. J Virol 75: 3802-3810.
7. Gotoh B, Takeuchi K, Komatsu T, Yokoo J (2003) The STAT2 activation process is a crucial target of Sendai virus C protein for the blockade of alpha interferon signaling. J Virol 77: 3360-3370.
8. Komatsu T, Takeuchi K, Yokoo J, Gotoh B (2002) Sendai virus C protein impairs both phosphorylation and dephosphorylation processes of Stat1. FEBS Lett 511: 139-144.
9. Takeuchi K, Komatsu T, Yokoo J, Kato A, Shioda T, et al. (2001) Sendai virus C protein physically associates with Stat1. Genes Cells 6: 545-557.
10. Kato A, Kiyotani K, Kubota T, Yoshida T, Tashiro M, et al. (2007) Importance of the anti-interferon capacity of Sendai virus C protein for pathogenicity in mice. J Virol 81: 3264-3271.
11. Kato A, Cortese-Grogan C, Moyer SA, Sugahara F, Sakaguchi T, et al. (2004) Characterization of the amino acid residues of sendai virus C protein that are critically involved in its interferon antagonism and RNA synthesis downregulation. J Virol 78: 7443-7454.
12. Koyama AH, Irie H, Kato A, Nagai Y, Adachi A (2003) Virus multiplication and induction of apoptosis by Sendai virus: role of the C proteins. Microbes Infect 5: 373-378.
13. Curran J, Marq JB, Kolakofsky D (1992) The Sendai virus nonstructural C proteins specifically inhibit viral mRNA synthesis. Virology 189: 647-656.
14. Curran J, Boeck R, Kolakofsky D (1991) The Sendai virus P gene expresses both an essential protein and an inhibitor of RNA synthesis by shuffling modules via mRNA editing. EMBO J 10: 3079-3085.
15. Cadd T, Garcin D, Tapparel C, Itoh M, Homma M, et al. (1996) The Sendai paramyxovirus accessory C proteins inhibit viral genome amplification in a promoter-specific fashion. J Virol 70: 5067-5074.
16. Tapparel C, Hausmann S, Pelet T, Curran J, Kolakofsky D, et al. (1997) Inhibition of Sendai virus genome replication due to promoter-increased selectivity: a possible role for the accessory C proteins. J Virol 71: 9588-9599.
17. Grogan CC, Moyer SA (2001) Sendai virus wild-type and mutant C proteins show a direct correlation between L polymerase binding and inhibition of viral RNA synthesis. Virology 288: 96-108.
18. Irie T, Nagata N, Yoshida T, Sakaguchi T (2008) Paramyxovirus Sendai virus C proteins are essential for maintenance of negative-sense RNA genome in virus particles. Virology 374: 495-505.
19. Hasan MK, Kato A, Muranaka M, Yamaguchi R, Sakai Y, et al. (2000) Versatility of the accessory C proteins of Sendai virus: contribution to virus assembly as an additional role. J Virol 74: 5619-5628.
20. Sakaguchi T, Kato A, Sugahara F, Shimazu Y, Inoue M, et al. (2005) AIP1/Alix is a binding partner of Sendai virus C protein and facilitates virus budding. J Virol 79: 8933-8941.
21. Sugahara F, Uchiyama T, Watanabe H, Shimazu Y, Kuwayama M, et al. (2004) Paramyxovirus Sendai virus-like particle formation by expression of multiple viral proteins and acceleration of its release by C protein. Virology 325: 1-10.
22. Itoh M, Hotta H, Homma M (1998) Increased induction of apoptosis by a Sendai virus mutant is associated with attenuation of mouse pathogenicity. J Virol 72: 2927-2934.
23. Kurotani A, Kiyotani K, Kato A, Shioda T, Sakai Y, et al. (1998) Sendai virus C proteins are categorically nonessential gene products but silencing their expression severely impairs viral replication and pathogenesis. Genes Cells 3: 111-124.
24. Gotoh B, Takeuchi K, Komatsu T, Yokoo J, Kimura Y, et al. (1999) Knockout of the Sendai virus C gene eliminates the viral ability to prevent the interferonalpha/ beta-mediated responses. FEBS Lett 459: 205-210.
25. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A, et al. (2006) 59-Triphosphate RNA is the ligand for RIG-I. Science 314: 994-997.
26. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T, et al. (2008) Lengthdependent recognition of double-stranded ribonucleic acids by retinoic acidinducible gene-I and melanoma differentiation-associated gene 5. J Exp Med 205: 1601-1610.
27. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M, et al. (2006) Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441: 101-105.
28. Loo YM, Fornek J, Crochet N, Bajwa G, Perwitasari O, et al. (2008) Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J Virol 82: 335-345.
29. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P, et al. (2006) RIG-Imediated antiviral responses to single-stranded RNA bearing 59 phosphates. Science 314: 997-1001.
30. Takeuchi K, Komatsu T, Kitagawa Y, Sada K, Gotoh B (2008) Sendai virus C protein plays a role in restricting PKR activation by limiting the generation of intracellular double-stranded RNA. J Virol 82: 10102-10110.
31. Irie T, Nagata N, Yoshida T, Sakaguchi T (2008) Recruitment of Alix/AIP1 to the plasma membrane by Sendai virus C protein facilitates budding of virus-like particles. Virology 371: 108-120.
32. Plumet S, Herschke F, Bourhis JM, Valentin H, Longhi S, et al. (2007) Cytosolic 59-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2: e279.
33. Childs K, Stock N, Ross C, Andrejeva J, Hilton L, et al. (2007) mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359: 190-200.
34. Andrejeva J, Childs KS, Young DF, Carlos TS, Stock N, et al. (2004) The V proteins of paramyxoviruses bind the IFN-inducible RNA helicase, mda 5, and inhibit its activation of the IFN-beta promoter. Proc Natl Acad Sci U S A 101: 17264-17269.
35. Grandvaux N, Gaboriau F, Harris J, tenOever BR, Lin R, et al. (2005) Regulation of arginase II by interferon regulatory factor 3 and the involvement of polyamines in the antiviral response. FEBS J 272: 3120-3131.
36. Kiyotani K, Takao S, Sakaguchi T, Yoshida T (1990) Immediate protection of mice from lethal wild-type Sendai virus (HVJ) infections by a temperaturesensitive mutant, HVJpi, possessing homologous interfering capacity. Virology 177: 65-74.
37. Fuerst TR, Niles EG, Studier FW, Moss B (1986) Eukaryotic transientexpression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc Natl Acad Sci U S A 83: 8122-8126.
38. Kato A, Sakai Y, Shioda T, Kondo T, Nakanishi M, et al. (1996) Initiation of Sendai virus multiplication from transfected cDNA or RNA with negative or positive sense. Genes Cells 1: 569-579.
39. Nishimura K, Segawa H, Goto T, Morishita M, Masago A, et al. (2007) Persistent and stable gene expression by a cytoplasmic RNA replicon based on a noncytopathic variant Sendai virus. J Biol Chem 282: 27383-27391.