West Nile virus noncoding subgenomic RNA contributes to viral evasion of the type I interferon-mediated antiviral response

Journal of Virology

Volumn 86, Issue 10, 2012, Pages 5708-5718

  Schuessler, Andrea ^a   Funk, Anneke ^a,g   Lazear, Helen M ^b   Cooper, Daphne A ^c   Torres, Shessy ^a   Daffis, Stephane ^b,h   Jha, Babal Kant ^d   Kumagai, Yutaro ^e   Takeuchi, Osamu ^e   Hertzog, Paul ^f   Silverman, Robert ^d   Akira, Shizuo ^e   Barton, David J ^c   Diamond, Michael S ^b   Khromykh, Alexander A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e OSAKA UNIVERSITY   (Japan)

^f HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

^g EMBO   (Germany)

^h GILEAD SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ALPHA INTERFERON RECEPTOR; ALPHA INTERFERON RECEPTOR 1; BETA INTERFERON RECEPTOR; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 7; RIBONUCLEASE L; UNCLASSIFIED DRUG; UNTRANSLATED RNA; VIRUS RNA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIVIRAL ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; EMBRYO; ENZYME INHIBITION; FLAVIVIRUS INFECTION; GENETIC TRANSFECTION; IMMUNE EVASION; IMMUNOMODULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; SENSITIVITY ANALYSIS; TREATMENT RESPONSE; VIRUS GENOME; VIRUS PATHOGENESIS; VIRUS REPLICATION; WEST NILE FLAVIVIRUS;

ANIMALS; CELL LINE; HUMANS; IMMUNE EVASION; INTERFERON REGULATORY FACTOR-3; INTERFERON TYPE I; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RNA, UNTRANSLATED; RNA, VIRAL; VIRULENCE; WEST NILE FEVER; WEST NILE VIRUS;

FLAVIVIRUS; MUS; SEMLIKI FOREST VIRUS; WEST NILE VIRUS;

EID: 84861312740     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.00207-12     Document Type: Article

References (61)

1. Andersen J, VanScoy S, Cheng TF, Gomez D, Reich NC. 2008. IRF-3-dependent and augmented target genes during viral infection. Genes Immun. 9:168-175.
2. Arjona A, et al. 2007. West Nile virus envelope protein inhibits dsRNAinduced innate immune responses. J. Immunol. 179:8403-8409.
3. Best SM, et al. 2005. Inhibition of interferon-stimulated JAK-STAT signaling by a tick-borne flavivirus and identification of NS5 as an interferon antagonist. J. Virol. 79:12828-12839.
4. Brass AL, et al. 2009. The IFITM proteins mediate cellular resistance to influenzaAH1N1 virus, West Nile virus, and dengue virus. Cell 139:1243-1254.
5. Cazalla D, Yario T, Steitz J. 2010. Down-regulation of a host microRNA by a Herpesvirus saimiri noncoding RNA. Science 328:1563-1566.
6. Clarke PA, Schwemmle M, Schickinger J, Hilse K, Clemens MJ. 1991. Binding of Epstein-Barr virus small RNA EBER-1 to the double-stranded RNA-activated protein kinase DAI. Nucleic Acids Res. 19:243-248.
7. Cook HL, et al. 2005. Small nuclear RNAs encoded by Herpesvirus saimiri upregulate the expression of genes linked to T cell activation in virally transformed T cells. Curr. Biol. 15:974-979.
8. Cullen BR. 2011. Viruses and microRNAs: RISCy interactions with serious consequences. Genes Dev. 25:1881-1894.
9. Daffis S, et al. 2011. The naturally attenuated Kunjin strain of West Nile virus shows enhanced sensitivity to the host type I interferon response. J. Virol. 85:5664-5668.
10. Daffis S, Samuel MA, Keller BC, Gale M, Jr, Diamond MS. 2007. Cell-specific IRF-3 responses protect against West Nile virus infection by interferon-dependent and -independent mechanisms. PLoS Pathog. 3:e106.
11. Daffis S, et al. 2008. Interferon regulatory factor IRF-7 induces the antiviral alpha interferon response and protects against lethal West Nile virus infection. J. Virol. 82:8465-8475.
12. Daffis S, Suthar MS, Gale M, Jr, Diamond MS. 2009. Measure and countermeasure: type I IFN (IFN-alpha/beta) antiviral response against West Nile virus. J. Innate Immun. 1:435-445.
13. Daffis S, Suthar MS, Szretter KJ, Gale M, Jr, Diamond MS. 2009. Induction of IFN-beta and the innate antiviral response in myeloid cells occurs through an IPS-1-dependent signal that does not require IRF-3 and IRF-7. PLoS Pathog. 5:e1000607.
14. Daffis S, et al. 2010. 2=-O methylation of the viral mRNA cap evades host restriction by IFIT family members. Nature 468:452-456.
15. Fredericksen BL, Gale M, Jr. 2006. West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J. Virol. 80: 2913-2923.
16. Fredericksen BL, Smith M, Katze MG, Shi PY, Gale M, Jr. 2004. The host response to West Nile Virus infection limits viral spread through the activation of the interferon regulatory factor 3 pathway. J. Virol. 78:7737-7747.
17. Funk A, et al. 2010. RNA structures required for production of subgenomic flavivirus RNA. J. Virol. 84:11407-11417.
18. Funk A, et al. 2010. RNA structures required for production of subgenomic flavivirus RNA. J. Virol.
19. Gilfoy FD, Mason PW. 2007. West Nile virus-induced interferon production is mediated by the double-stranded RNA-dependent protein kinase PKR. J. Virol. 81:11148-11158.
20. Gubler DJ. 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol. 10:100-103.
21. Guo JT, Hayashi J, Seeger C. 2005. West Nile virus inhibits the signal transduction pathway of alpha interferon. J. Virol. 79:1343-1350.
22. Hall RA, Broom AK, Smith DW, Mackenzie JS. 2002. The ecology and epidemiology of Kunjin virus. Curr. Top. Microbiol. Immunol. 267:253-269.
23. Han JQ, et al. 2007. A phylogenetically conserved RNA structure in the poliovirus open reading frame inhibits the antiviral endoribonuclease RNase L. J. Virol. 81:5561-5572.
24. Honda K, et al. 2005. IRF-7 is the master regulator of type-I interferondependent immune responses. Nature 434:772-777.
25. Jiang D, et al. 2010. Identification of five interferon-induced cellular proteins that inhibit West Nile virus and dengue virus infection. J. Virol. 84:8332-8341.
26. Keller BC, et al. 2006. Resistance to alpha/beta interferon is a determinant of West Nile virus replication fitness and virulence. J. Virol. 80:9424-9434.
27. Khromykh AA, Varnavski AN, Westaway EG. 1998. Encapsidation of the flavivirus Kunjin replicon RNA by using a complementation system providing Kunjin virus structural proteins in trans. J. Virol. 72:5967-5977.
28. Laurent-Rolle M, et al. 2010. The NS5 protein of the virulent West Nile virus NY99 strain is a potent antagonist of type I interferon-mediated JAK-STAT signaling. J. Virol. 84:3503-3515.
29. Lin KC, Chang HL, Chang RY. 2004. Accumulation of a 3=-terminal genome fragment in Japanese encephalitis virus-infected mammalian and mosquito cells. J. Virol. 78:5133-5138.
30. Liu WJ, Chen HB, Khromykh AA. 2003. Molecular and functional analyses of Kunjin virus infectious cDNA clones demonstrate the essential roles for NS2A in virus assembly and for a nonconservative residue in NS3 in RNA replication. J. Virol. 77:7804-7813.
31. Liu WJ, Chen HB, Wang XJ, Huang H, Khromykh AA. 2004. Analysis of adaptive mutations in Kunjin virus replicon RNA reveals a novel role for the flavivirus nonstructural protein NS2A in inhibition of beta interferon promoter-driven transcription. J. Virol. 78:12225-12235.
32. Liu WJ, Sedlak PL, Kondratieva N, Khromykh AA. 2002. Complementation analysis of the flavivirus Kunjin NS3 and NS5 proteins defines the minimal regions essential for formation of a replication complex and shows a requirement of NS3 in cis for virus assembly. J. Virol. 76:10766-10775.
33. Liu WJ, et al. 2006. A single amino acid substitution in the West Nile virus nonstructural protein NS2A disables its ability to inhibit alpha/beta interferon induction and attenuates virus virulence in mice. J. Virol. 80:2396-2404.
34. Liu WJ, et al. 2005. Inhibition of interferon signaling by the New York 99 strain and Kunjin subtype of West Nile virus involves blockage of STAT1 and STAT2 activation by nonstructural proteins. J. Virol. 79:1934-1942.
35. Mackenzie JM, Khromykh AA, Parton RG. 2007. Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe 2:229-239.
36. Mackenzie JS, Gubler DJ, Petersen LR. 2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10:S98-109.
37. Malathi K, Dong B, Gale M, Jr, Silverman RH. 2007. Small self-RNA generated by RNase L amplifies antiviral innate immunity. Nature 448: 816-819.
38. Malathi K, et al. 2010. RNase L releases a small RNA from HCV RNA that refolds into a potent PAMP. RNA 16:2108-2119.
39. Marie I, Durbin JE, Levy DE. 1998. Differential viral induction of distinct interferon-alpha genes by positive feedback through interferon regulatory factor-7. EMBO J. 17:6660-6669.
40. Markoff L. 2003. 5=- And 3=-noncoding regions in flavivirus RNA. Adv. Virus Res. 59:177-228.
41. Mathews MB, Shenk T. 1991. Adenovirus virus-associated RNA and translation control. J. Virol. 65:5657-5662.
42. Mazzon M, Jones M, Davidson A, Chain B, Jacobs M. 2009. Dengue virus NS5 inhibits interferon-alpha signaling by blocking signal transducer and activator of transcription 2 phosphorylation. J. Infect. Dis. 200: 1261-1270.
43. Munoz-Jordan JL, et al. 2005. Inhibition of alpha/beta interferon signaling by the NS4B protein of flaviviruses. J. Virol. 79:8004-8013.
44. Pijlman GP, et al. 2008. A highly structured, nuclease-resistant, noncoding RNA produced by flaviviruses is required for pathogenicity. Cell Host Microbe 4:579-591.
45. R Development Core Team. 2010. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
46. Reeves MB, Davies AA, McSharry BP, Wilkinson GW, Sinclair JH. 2007. Complex I binding by a virally encoded RNA regulates mitochondria-induced cell death. Science 316:1345-1348.
47. Samuel MA, et al. 2006. PKR and RNase L contribute to protection against lethal West Nile Virus infection by controlling early viral spread in the periphery and replication in neurons. J. Virol. 80:7009-7019.
48. Sato M, et al. 2000. Distinct and essential roles of transcription factors IRF-3 and IRF-7 in response to viruses for IFN-alpha/beta gene induction. Immunity 13:539-548.
49. Scherbik SV, Paranjape JM, Stockman BM, Silverman RH, Brinton MA. 2006. RNase L plays a role in the antiviral response to West Nile virus. J. Virol. 80:2987-2999.
50. Sheehan KC, et al. 2006. Blocking monoclonal antibodies specific for mouse IFN-alpha/beta receptor subunit 1 (IFNAR-1) from mice immunized by in vivo hydrodynamic transfection. J. Interferon Cytokine Res. 26:804-819.
51. Silva PA, Pereira CF, Dalebout TJ, Spaan WJ, Bredenbeek PJ. 2010. An RNA pseudoknot is required for production of yellow fever virus subgenomic RNA by the host nuclease XRN1. J. Virol. 84:11395-11406.
52. Silverman RH. 2007. Viral encounters with 2=,5=-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81: 12720-12729.
53. Sullivan CS. 2008. New roles for large and small viral RNAs in evading host defences. Nat. Rev. Genet. 9:503-507.
54. Takeuchi O, Akira S. 2009. Innate immunity to virus infection. Immunol. Rev. 227:75-86.
55. Townsend HL, et al. 2008. A viral RNA competitively inhibits the antiviral endoribonuclease domain of RNase L. RNA 14:1026-1036.
56. Townsend HL, Jha BK, Silverman RH, Barton DJ. 2008. A putative loop E motif and an H-H kissing loop interaction are conserved and functional features in a group C enterovirus RNA that inhibits ribonuclease L. RNA Biol. 5:263-272.
57. Urosevic N, van Maanen M, Mansfield JP, Mackenzie JS, Shellam GR. 1997. Molecular characterization of virus-specific RNA produced in the brains of flavivirus-susceptible and -resistant mice after challenge with Murray Valley encephalitis virus. J. Gen. Virol. 78:23-29.
58. Westaway EG, Mackenzie JM, Khromykh AA. 2003. Kunjin RNA replication and applications of Kunjin replicons. Adv. Virus Res. 59:99-140.
59. Westaway EG, Mackenzie JM, Khromykh AA. 2002. Replication and gene function in Kunjin virus. Curr. Top. Microbiol. Immunol. 267:323-351.
60. Wilson JR, de Sessions PF, Leon MA, Scholle F. 2008. West Nile virus nonstructural protein 1 inhibits TLR3 signal transduction. J. Virol. 82: 8262-8271.
61. Zhou A, et al. 1997. Interferon action and apoptosis are defective in mice devoid of 2',5'-oligoadenylate-dependent RNase L. EMBO J. 16:6355-6363.