Identification of multiple RIG-I-specific pathogen associated molecular patterns within the West Nile virus genome and antigenome

Virology

Volumn 432, Issue 1, 2012, Pages 232-238

  Shipley, Jennifer German ^a   Vandergaast, Rianna ^a   Deng, Lu ^a,b   Mariuzza, Roy A ^a,b   Fredericksen, Brenda L ^a  

^a Bldg 142   (United States)

^b UNIVERSITY OF MARYLAND   (United States)

Author keywords

Pathogen associated molecular patterns; Pathogen recognition receptor; RIG I; West Nile virus

Indexed keywords

CELL PROTEIN; PATHOGEN ASSOCIATED MOLECULAR PATTERN; RETINOIC ACID INDUCIBLE PROTEIN I; UNCLASSIFIED DRUG; VIRUS RNA;

3' UNTRANSLATED REGION; 5' UNTRANSLATED REGION; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; GENOME ANALYSIS; IMMUNE EVASION; IMMUNE RESPONSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INDUCTION; PROTEIN SECRETION; RNA PROCESSING; SIGNAL TRANSDUCTION; VIRUS ANTIGENOME; VIRUS CELL INTERACTION; VIRUS GENOME; WEST NILE FLAVIVIRUS;

CELL LINE; DEAD-BOX RNA HELICASES; GENOME, VIRAL; HUMANS; IMMUNE EVASION; RECEPTORS, IMMUNOLOGIC; WEST NILE VIRUS;

WEST NILE VIRUS;

EID: 84864012784     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2012.06.009     Document Type: Article

References (59)

1. Barral P.M., Sarkar D., Fisher P.B., Racaniello V.R. RIG-I is cleaved during picornavirus infection. Virology 2009, 391:171-176.
2. Baum A., Sachidanandam R., Garcia-Sastre A. Preference of RIG-I for short viral RNA molecules in infected cells revealed by next-generation sequencing. Proc. Natl. Acad. Sci. USA 2010, 107:16303-16308.
3. Berg R.K., Melchjorsen J., Rintahaka J., Diget E., Søby S., Horan K.A., Gorelick R.J., Matikainen S., Larsen C.S., et al. Genomic HIV RNA induces innate immune responses through RIG-I-dependent sensing of secondary-structured RNA. PLoS ONE 2012, 7:e29291. (P. Sommer, Ed.).
4. Blight K.J., McKeating J.A., Rice C.M. Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J. Virol. 2002, 76:13001-13014.
5. Bowie A.G., Unterholzner L. Viral evasion and subversion of pattern-recognition receptor signalling. Nat. Rev. Immunol. 2008, 8:911-922.
6. Brinton M.A. Host factors involved in West Nile virus replication. Ann. NY Acad. Sci. 2001, 951:207-219.
7. Brinton M.A. The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu. Rev. Microbiol. 2002, 56:371-402.
8. Brinton M.A., Dispoto J.H. Sequence and secondary structure analysis of the 5'-terminal region of flavivirus genome RNA. Virology 1988, 162:290-299.
9. Brinton M.A., Fernandez A.V., Dispoto J.H. The 3'-nucleotides of flavivirus genomic RNA form a conserved secondary structure. Virology 1986, 153:113-121.
10. Chambers, T.J., Hahn, C.S., Galler, R. , Rice, C.M., 1990. Flavivirus genome organization, expression, and replication. Ann. Rev. Microbiol. 44, 649-88.
11. Doma M.K., Parker R. Endonucleolytic cleavage of eukaryotic mRNAs with stalls in translation elongation. Nature 2006, 440:561-564.
12. Fredericksen B.L., Gale M. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J. Virol. 2006, 80:2913-2923.
13. Fredericksen B.L., Keller B.C., Fornek J., Katze M.G., Gale M. Establishment and maintenance of the innate antiviral response to West Nile virus involves both RIG-I and MDA5 signaling through IPS-1. J. Virol. 2008, 82:609-616.
14. Funk A., Truong K., Nagasaki T., Torres S., Floden N., Balmori Melian E., Edmonds J., Dong H., Shi P.Y., Khromykh A.A. RNA structures required for production of subgenomic flavivirus RNA. J. Virol. 2011, 84:11407-11417.
15. Gack M.U., Albrecht R.A., Urano T., Inn K., Huang I., Carnero E., Farzan M., Inoue S., Jung J., García-Sastre A. Influenza A virus NS1 targets the ubiquitin ligase TRIM25 to evade recognition by the host viral RNA sensor RIG-I. Cell Host and Microbe 2009, 5:439-449.
16. Gillespie L.K., Hoenen A., Morgan G., Mackenzie J.M. The endoplasmic reticulum provides the membrane platform for biogenesis of the flavivirus replication complex. J. Virol. 2010, 84:10438-10447.
17. Grandvaux N., Servant M.J., tenOever B., Sen G.C., Balachandran S., Barber G.N., Lin R., Hiscott J. Transcriptional profiling of interferon regulatory factor 3 target genes: direct involvement in the regulation of interferon-stimulated genes. J. Virol. 2002, 76:5532-5539.
18. Hahn C.S., Hahn Y.S., Rice C.M., Lee E., Dalgarno L., Strauss E.G., Strauss J.H. Conserved elements in the 3' untranslated region of flavivirus RNAs and potential cyclization sequences. J. Mol. Biol. 1987, 198:33-41.
19. Hayes E.B., Gubler D.J. West Nile virus: epidemiology and clinical features of an emerging epidemic in the United States. Annu. Rev. Med. 2006, 57:181-194.
20. Hiscott J. Triggering the innate antiviral response through IRF-3 activation. J. Biol. Chem. 2007, 282:15325-15329.
21. Hornung V., Ellegast J., Kim S., Brzozka K., Jung A., Kato H., Poeck H., Akira S., Conzelmann K.K., et al. 5'-Triphosphate RNA is the ligand for RIG-I. Science 2006, 314:994-997.
22. Kato H., Takeuchi O., Sato S., Yoneyama M., Yamamoto M., Matsui K., Uematsu S., Jung A., Kawai T., et al. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 2006, 441:101-105.
23. Kato H., Takeuchi O., Mikamo-Satoh E., Hirai R., Kawai T., Matsushita K., Hiiragi A., Dermody T.S., Fujita T., 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. 2008, 205:1601-1610.
24. Kawai T., Takahashi K., Sato S., Coban C., Kumar H., Kato H., Ishii K.J., Takeuchi O., Akira S. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 2005, 6:981-988.
25. Khromykh A.A., Meka H., Guyatt K.J., Westaway E.G. Essential role of cyclization sequences in flavivirus RNA replication. J. Virol. 2001, 75:6719-6728.
26. Klee A.L., Maidin B., Edwin B., Poshni I., Mostashari F., Fine A., Layton M., Nash D. Long-term prognosis for clinical West Nile virus infection. Emerg. Infect. Dis. 2004, 10:1405-1411.
27. Lindenbach, B.D., Thiel, H., Rice, C.M., 2007. Flaviviridae: The viruses and their replication. In: Fields Virology, 5th edn. Knipe, D.M., Howley, P.M. eds., Lippincott-Raven Publishers, Philadelphia.
28. Ling Z., Tran K.C., Teng M.N. Human respiratory syncytial virus nonstructural protein NS2 antagonizes the activation of beta interferon transcription by interacting with RIG-I. J. Virol. 2009, 83:3734-3742.
29. Loo Y.M., Fornek J., Crochet N., Bajwa G., Perwitasari O., Martinez-Sobrido L., Akira S., Gill M.A., Garcia-Sastre A., et al. Distinct RIG-I and MDA5 signaling by RNA viruses in innate immunity. J. Virol. 2008, 82:335-345.
30. Lu C., Xu H., Ranjith-Kumar C.T., Brooks M.T., Hou T.Y., Hu F., Herr A.B., Strong R.K., Kao C.C., Li P. The structural basis of 5'-triphosphate double-stranded RNA recognition by RIG-I C-terminal domain. Structure 2010, 18:1032-1043.
31. Malathi K., Saito T., Crochet N., Barton D.J., Gale Jr.M., Silverman R.H. RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP. RNA 2010, 16:2108-2119.
32. Masatani T., Ito N., Shimizu K., Ito Y., Nakagawa K., Sawaki Y., Koyama H., Sugiyama M. Rabies virus nucleoprotein functions to evade activation of the RIG-I-mediated antiviral response. J. Virol. 2010, 84:4002-4012.
33. Myong S., Cui S., Cornish P.V., Kirchhofer A., Gack M.U., Jung J.U., Hopfner K.P., Ha T. Cytosolic viral sensor RIG-I is a 5'-triphosphate-dependent translocase on double-stranded RNA. Science 2009, 323:1070-1074.
34. Nash D., et al. The outbreak of West Nile Virus infection in the New York city area in 1999. N. Engl. J. Med. 2001, 344:1807-1814.
35. Pachler K., Vlasak R. Influenza C virus NS1 protein counteracts RIG-I-mediated IFN signalling. Virology journal 2011, 8:48.
36. Papon L., Oteiza A., Imaizumi T., Kato H., Brocchi E., Lawson T.G., Akira S., Mechti N. The viral RNA recognition sensor RIG-I is degraded during encephalomyocarditis virus (EMCV) infection. Virology 2009, 393:311-318.
37. Petersen L.R., Roehrig J.T. West Nile virus: a reemerging global pathogen. Emerg. Infect. Dis. 2001, 7:611-614.
38. Pichlmair A., Schulz O., Tan C.P., Näslund T.I., Liljeström P., Weber F., Reis e Sousa C RIG-I-mediated antiviral responses to single-stranded RNA bearing 5'-phosphates. Science 2006, 314:997-1001.
39. Pijlman G.P., Funk A., Kondratieva N., Leung J., Torres S., van der Aa L., Liu W.J., Palmenberg A.C., Shi P.Y., et al. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 2008, 4:579-591.
40. Plumet S., Herschke F., Bourhis J.M., Valentin H., Longhi S., Gerlier D. Cytosolic 5'-triphosphate ended viral leader transcript of measles virus as activator of the RIG I-mediated interferon response. PLoS One 2007, 2:e279.
41. Rehwinkel J., Tan C.P., Goubau D., Schulz O., Pichlmair A., Bier K., Robb N., Vreede F., Barclay W., et al. RIG-I detects viral genomic RNA during negative-strand RNA virus infection. Cell 2010, 140:397-408.
42. Saito T., Hirai R., Loo Y.M., Owen D., Johnson C.L., Sinha S.C., Akira S., Fujita T., Gale M. Regulation of innate antiviral defenses through a shared repressor domain in RIG-I and LGP2. Proc. Natl. Acad. Sci. USA 2007, 104:582-587.
43. Saito T., Owen D.M., Jiang F., Marcotrigiano J., Gale M. Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 2008, 454:523-527.
44. Scadden A.D.J. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nat. Struct. Mol. Biol. 2005, 12:489-496.
45. Scherbik S.V., Paranjape J.M., Stockman B.M., Silverman R.H., Brinton M.A. RNase L plays a role in the antiviral response to West Nile virus. J. Virol. 2006, 80:2987-2999.
46. Schlee M., Roth A., Hornung V., Hagmann C.A., Wimmenauer V., Barchet W., Coch C., Janke M., Mihailovic A., et al. Recognition of 5'-triphosphate by RIG-I helicase requires short blunt double-stranded RNA as contained in panhandle of negative-strand virus. Immunity 2009, 31:25-34.
47. Schmidt A., Schwerd T., Hamm W., Hellmuth J.C., Cui S., Wenzel M., Hoffmann F.S., Michallet M.C., Besch R., et al. 5'-triphosphate RNA requires base-paired structures to activate antiviral signaling via RIG-I. Proc. Natl. Acad. Sci. USA 2009, 106:12067-12072.
48. Schuessler A., Funk A., Lazear H., Cooper D.A., Torres S., Daffis S., Jha B.K., Kumagai Y., Takeuchi O., et al. West Nile virus non-coding subgenomic RNA contributes to viral evasion of type I interferon-mediated antiviral response. J. Virol. 2012, 86:5708-5718.
49. Shi P.Y., Tilgner M., Lo M.K., Kent K.A., Bernard K.A. Infectious cDNA Clone of the Epidemic West Nile Virus from New York City. J. Virol. 2002, 76:5847-5856.
50. Stetson D.B., Medzhitov R. Antiviral defense: interferons and beyond. J. Exp. Med. 2006, 203:1837-1841.
51. Sumpter R., Loo Y.M., Foy E., Li K., Yoneyama M., Fujita T., Lemon S.M., Gale M. Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J. Virol. 2005, 79:2689-2699.
52. Takahasi K., Yoneyama M., Nishihori T., Hirai R., Kumeta H., Narita R., Gale M., Inagaki F., Fujita T. Nonself RNA-sensing mechanism of RIG-I helicase and activation of antiviral immune responses. Mol. Cell 2008, 29:428-440.
53. Tomecki R., Dziembowski A. Novel endoribonucleases as central players in various pathways of eukaryotic RNA metabolism. RNA 2010, 16:1692-1724.
54. Umbach J.L., Cullen B.R. The role of RNAi and microRNAs in animal virus replication and antiviral immunity. Genes Dev. 2009, 23:1151-1164.
55. Wang F., Gao X., Barrett J.W., Shao Q., Bartee E., Mohamed M.R., Rahman M., Werden S., Irvine T., et al. RIG-I mediates the co-induction of tumor necrosis factor and type I interferon elicited by myxoma virus in primary human macrophages. PLoS Pathog. 2008, 4:e1000099.
56. Wang R., Kushner S. Construction of versatile low-copy-number vectors for cloning, sequencing and gene expression in Escherichia coli. Gene 1991, 100:195-199.
57. Westaway E.G., Khromykh A.A., Mackenzie J.M. Nascent flavivirus RNA colocalized in situ with double-stranded RNA in stable replication complexes. Virology 1999, 258:108-117.
58. Yoneyama M., Kikuchi M., Natsukawa T., Shinobu N., Imaizumi T., Miyagishi M., Taira K., Akira S., Fujita T. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 2004, 5:730-737.
59. Zhang B., Dong H., Stein D.A., Iversen P.L., Shi P.Y. West Nile virus genome cyclization and RNA replication require two pairs of long-distance RNA interactions. Virology 2008, 373:1-13.