TLR3-dependent upregulation of RIG-I leads to enhanced cytokine production from cells infected with the parainfluenza virus SV5

Virology

Volumn 397, Issue 1, 2010, Pages 231-241

  Manuse, Mary J ^a   Parks, Griffith D ^a  

^a WAKE FOREST SCHOOL OF MEDICINE   (United States)

Author keywords

Cyokines; Host cell response; Parainfluenza virus; Paramyxovirus; Simian virus 5; TLR3

Indexed keywords

BETA INTERFERON; CYTOKINE; DOUBLE STRANDED RNA; INTERLEUKIN 6; RETINOIC ACID INDUCIBLE PROTEIN I; RNA BINDING PROTEIN; SMALL INTERFERING RNA; TOLL LIKE RECEPTOR 3;

ARTICLE; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENZYME LINKED IMMUNOSORBENT ASSAY; FLUORESCENCE MICROSCOPY; HUMAN; HUMAN CELL; INNATE IMMUNITY; NONHUMAN; PARAMYXOVIRUS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION; SIMIAN PARAINFLUENZA VIRUS 5; UPREGULATION; VIRUS INFECTION; VIRUS MUTANT; WESTERN BLOTTING;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; CELL LINE; DEAD-BOX RNA HELICASES; HUMANS; INTERFERON-BETA; INTERLEUKIN-6; INTERLEUKIN-8; SIMIAN VIRUS 5; TOLL-LIKE RECEPTOR 3; UP-REGULATION;

PARAINFLUENZA VIRUS; PARAMYXOVIRIDAE; SIMIAN VIRUS 5;

EID: 73949096176     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2009.11.014     Document Type: Article

References (55)

1. Andrejeva J., Childs K.S., Young D.F., Carlos R.S., Stock N., Goodbourn S., and Randall R.E. 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 (2004) 17264-17269
2. Biron C.A., and Sen G.C. Innate responses to viral infections. In: Fields B., Knipe D., and Howley P. (Eds). Fields Virology. 5th ed (2007), Lippincott Williams and Wilkins Publishers, Philadelphia, Pa 249-278
3. Boehme K.W., and Compton T. Innate sensing of viruses by toll-like receptors. J. Virol. 78 (2004) 7867-7873
4. Capraro G.A., Johnson J.J., Kock N.D., and Parks G.D. Growth and antibody responses to respiratory tract infection of ferrets and mice with WT and P/V mutants of the paramyxovirus Simian Virus 5. Virology 376 (2008) 416-428
5. Casola A., Garofalo R.P., Jamaluddin M., Vlahopoulos S., and Brasier A.R. Requirement of a novel upstream response element in respiratory syncytial virus-induced IL-8 gene expression. J. 164 (2000) 5944
6. Chang T.H., Liao C.L., and Lin Y.L. Flavivirus induces interferon-beta gene expression through a pathway involving RIG-I-dependent IRF-3 and PI3K-dependent NF-kappaB activation. Microbes Infect 8 1 (2005) 157-171
7. Chatziandreou N., Young D., Andrejeva J., Goodbourn S., and Randall R.E. Differences in interferon sensitivity and biological properties of two related isolates of simian virus 5: a model for virus persistence. Virology 293 (2002) 234-242
8. Childs K.S., Stock N., Ross C., Andrejeva J., Hilton L., Skinner M., Randall R., and Goodbourn S. mda-5, but not RIG-I, is a common target for paramyxovirus V proteins. Virology 359 (2007) 190-200
9. Childs K.S., Andrejeva J., Randall R.E., and Goodbourn S. Mechanism of mda-5 inhibition by paramyxovirus V proteins. J. Virol. 83 (2009) 1465-1473
10. Choppin P.W. Multiplication of myxovirus (SV5) with minimal cytopathic effects and without interference. Virology 23 (1964) 224-233
11. Conzelmann K.K. Transcriptional activation of alpha/beta interferon genes: interference by nonsegmented negative-strand RNA viruses. J. Virol. 79 (2005) 5241-5248
12. 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
13. Dillon P.J., and Parks G.D. A role for the P subunit of the paramyxovirus polymerase in limiting host cell antiviral responses. J. Virol. 81 (2007) 11116-11127
14. Gale M., and Katze M.G. Molecular mechanisms of interferon resistance mediated by viral-directed inhibition of PKR, the interferon-induced protein kinase. Pharmacol. Ther. 78 (1998) 29-46
15. Gainey M.D., Dillon P.J., Clark K.M., Manuse M.J., and Parks G.D. Paramyxovirus induced shut off of translation: role of P and V proteins in limiting activation of PKR. J. Virol. 82 (2008) 828-839
16. 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
17. Goodbourn S., and Randall R.E. The regulation of type I interferon production by paramyxoviruses. J. Interferon. Cytokine. Res 29 9 (2009) 539-547
18. 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
19. Goto Y., Arigami T., Kitago M., Nguyen S.L., Narita N., Ferrone S., Morton D.L., Irie R.F., and Hoon D.S. Activation of Toll-like receptors 2, 3, and 4 on human melanoma cells induces inflammatory factors. Mol. Cancer Ther. 7 11 (2008) 3642-3653
20. Guillot L., Le Goffic R., Bloch S., Escriou N., Akira S., Chignard M., and Si-Tahar M. Involvement of toll-like receptor 3 in the immune response of lung epithelial cells to double-stranded RNA and influenza A virus. J. Biol. Chem. 280 (2005) 5571-5580
21. He B., Paterson R.G., Ward C.D., and Lamb R.A. Recovery of infectious SV5 from cloned DNA and expression of a foreign gene. Virology 237 (1997) 249-260
22. 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
23. Hiscott J., Pitha P., Genin P., Nguyen H., Heylbroeck C., Mamane Y., Algarte M., and Lin R. Triggering the interferon response: the role of IRF-3 transcription factor. J. Interferon. Cytokine Res. 19 (1999) 1-13
24. Horvath C.M. Weapons of STAT destruction. Interferon evasion by paramyxovirus V protein. Eur. J. Biochem. 271 (2004) 4621-4628
25. Imaizumi T., Hatakeyama M., Yamashita K., Yoshida H., Ishikawa A., Taima K., Satoh K., Mori F., and Wakabayashi K. Interferon-gamma induces retinoic acid-inducible gene-I in endothelial cells. Endothelium 11 3-4 (2004) 169-173
26. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., Ishii K.J., Yamaguchi O., Otsu K., Tsujimura T., Koh C.S., Reis e Sousa C., Matsuura Y., Fujita T., and Akira S. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature. 4 441 7089 (2006) 101-105
27. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., Hiiragi A., Dermody T.S., Fujita T., and Akira S. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205 (2008) 1601-1610
28. Kawai T., and Akira S. Toll-like receptor and RIG-1-like receptor signaling. Ann. N.Y. Acad. Sci. 1143 (2008) 1-20
29. Kobayashi T., Antar A.A.R., Boehme K.W., Danthi P., Eby E.A., Gugliemi K.M., Holm G.H., Johnson E.M., Maginnis M.S., Naik S., Skelton W.B., Wetzel J.D., Wilson G.J., Chapell J.D., and Dermody T.S. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell. Host Microbe 1 (2007) 147-157
30. Lamb R.A., and Parks G.D. Paramyxoviridae: the viruses and their replication. In: Fields B., Knipe D., and Howley P. (Eds). Fields Virology. 5th ed (2007), Lippincott Williams and Wilkins Publishers, Philadelphia, Pa 1449-1496
31. Le Goffic R., Pothlichet J., Vitour D., Fujita T., Meurs E., Chignard M., and Si-Tahar M. Cutting edge: influenza A virus activates TLR3-dependent inflammatory and RIG-I-dependent antiviral responses in human lung epithelial cells. J. Immunol. 178 6 (2007) 3368-3372
32. Liu P., Jamaluddin M., Li K., Garofalo R.P., Casola A., and Brasier A.R. Retinoic acid-inducible gene I mediates early antiviral response and TLR 3 expression in respiratory syncytial virus infected airway epithelial cells. J. Virol. 81 (2007) 1401-1411
33. López C.B., Moltedo B., Alexopoulou L., Bonifaz L., Flavell R.A., and Moran T.M. TLR-independent induction of dendritic cell maturation and adaptive immunity by negative-strand RNA viruses. J. Immunol. 173 11 (2004) 6882-6889
34. Lu L.L., Puri M., Horvath C.M., and Sen G.C. Select paramyxoviral V proteins inhibit IRF3 activation by acting as alternative substrates for inhibitor of kB kinase epsilon (IKKe)/TBK1. J. Biol. Chem. 283 (2008) 14269-14276
35. Manuse M.J., and Parks G.D. A role for the paramyxovirus genomic promoter in limiting host cell antiviral responses and cell killing. J. Virol. 83 (2009) 9057-9067
36. Melchjorsen J., Jensen S.B., Malmgaard L., Rasmussen S.B., Weber F., Bowie A.G., Matikainen S., and Paludan S.R. Activation of innate defense against a paramyxovirus is mediated by RIG-I and TLR7 and TLR8 in a cell-type-specific manner. J. Virol. 79 20 (2005) 12944-12951
37. Meylan E., and Tschopp J. Toll-like receptors and RNA helicases: two parallel ways to trigger antiviral responses. Mol. Cell 22 5 (2006) 561-569
38. O'Neill L.A., and Dinarello C.A. The IL-1 receptor/toll-like receptor superfamily: crucial receptors for inflammation and host defense. Immunol. Today 5 (2000) 206-209
39. Pfaller C.K., and Conzelmann K.K. Measles virus V protein is a decoy substrate for IkappaB kinase alpha and prevents TLR7/9-mediated interferon induction. J. Virol. 82 (2008) 365-12373
40. 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
41. Rudd B.D., Burstein E., Duckett C.S., Li X., and Lukacs N.W. Differential role for TLR3 in respiratory syncytial virus-induced chemokine expression. J. Virol. 79 (2005) 3350-3357
42. Schroder M., and Bowie A.G. TLR3 in antiviral immunity: key player or bystander?. Trends Immunol. 26 (2005) 462-468
43. Schulz O., Diebold S.S., Chen M., Naslund T.I., Nolte M.A., Alexopoulou L., Azuma Y.-T., Flavell T.A., Liljestrom P., and Reis E Sousa C. TLR3 promotes cross-priming to virus infected cells. Nature 433 (2005) 887-892
44. Schlee M., Roth A., Hornung V., Hagmann C.A., Wimmenauer V., Barchet W., Coch C., Janke M., Mihailovic A., Wardle G., Juranek S., Kato H., Kawai T., Poeck H., Fitzgerald K.A., Takeuchi O., Akira S., Tuschl T., Latz E., Ludwig J., and Hartmann G. Recognition of 5′ triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 31 (2009) 25-34
45. Strahle L., Garcin D., and Kolakofsky D. Sendai virus defective-interfering genomes and the activation of interferon-beta. Virology 351 (2006) 101-111
46. Strahle L., Marq J.-B., Brini A., Hausmann S., Kolakofsky D., and Garcin D. Activation of the beta interferon promoter by unnatural Sendai virus infection requires RIG-I and is inhibited by viral C proteins. J. Virol. 81 (2007) 12227-12237
47. Su Z.Z., Sarkar D., Emdad L., Barral P.M., and Fisher P.B. Central role of interferon regulatory factor-1 (IRF-1) in controlling retinoic acid inducible gene-I (RIG-I) expression. J. Cell. Physiol. 213 2 (2007) 502-510
48. Ulane C.M., Kentsis A., Cruz C.D., Parisien J.P., Schneider K.L., and Horvath C.M. Composition and assembly of STAT-targeting ubiquitin ligase complexes: paramyxovirus V protein carboxyl terminus is an oligomerization domain. J. Virol. 79 (2005) 10180-10189
49. Wang T., Town T., Alexopoulou L., Anderson J.F., Fikrig E., and Flavell R.A. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 12 (2004) 1366-1373
50. Wansley E.K., and Parks G.D. Naturally occurring substitutions in the P/V gene convert the noncytopathic paramyxovirus simian virus 5 into a virus that induces alpha/beta interferon synthesis and cell death. J. Virol. 76 (2002) 10109-10121
51. Wilson J.R., de Sessions P.F., Leon M.A., and Scholle F. West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J. Virol. 82 (2008) 8262-8271
52. 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 an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5 (2004) 730-737
53. 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. 1. 175 5 (2005) 2851-2858
54. Young V.A., Dillon P.J., and Parks G.D. Variants of the paramyxovirus simian virus 5 with accelerated or delayed viral gene expression activate proinflammatory cytokine synthesis. Virology 350 (2006) 90-102
55. Yue Z., and Shatkin A.J. Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 234 2 (1997) 364-371