Overproduction of double-stranded RNA in vesicular stomatitis virus-infected cells activates a constitutive cell-type-specific antiviral response

Journal of Virology

Volumn 81, Issue 2, 2007, Pages 503-513

  Ostertag, Derek ^a,b   Hoblitzell Ostertag, Traci M ^a,c   Perrault, Jacques ^a  

^a SAN DIEGO STATE UNIVERSITY   (United States)

^b BURNHAM INSTITUTE   (United States)

^c LIGAND PHARMACEUTICALS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; GREEN FLUORESCENT PROTEIN; INTERFERON; PROTEIN C; PROTEIN POLR; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; VIRUS PROTEIN; VIRUS RNA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANTIVIRAL ACTIVITY; ARTICLE; CELL SPECIFICITY; CELL STRAIN L 929; CELL TYPE; CONTROLLED STUDY; INFLUENZA VIRUS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA VIRUS INFECTION; SENDAI VIRUS; SUPERINFECTION; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIROGENESIS; VIRUS EXPRESSION; VIRUS GENOME; VIRUS IMMUNITY; VIRUS INFECTIVITY; VIRUS INHIBITION; VIRUS PARTICLE; WILD TYPE;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CRICETINAE; DNA-DIRECTED RNA POLYMERASES; L CELLS (CELL LINE); MICE; RATS; RNA, DOUBLE-STRANDED; RNA, VIRAL; RNA-BINDING PROTEINS; SPECIES SPECIFICITY; UP-REGULATION; VACCINIA VIRUS; VESICULAR STOMATITIS-INDIANA VIRUS; VIRUS REPLICATION;

ORTHOMYXOVIRIDAE; SENDAI VIRUS; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS;

EID: 33846117090     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01218-06     Document Type: Article

References (67)

1. Ahmed, M., M. O. McKenzie, S. Puckett, M. Hojnacki, L. Poliquin, and D. S. Lyles. 2003. Ability of the matrix protein of vesicular stomatitis virus to suppress beta interferon gene expression is genetically correlated with the inhibition of host RNA and protein synthesis. J. Virol. 77:4646-4657.
2. Andrejeva, J., K. S. Childs, D. F. Young, T. S. Carlos, N. Stock, S. Goodbourn, and R. E. Randall. 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. USA 101:17264-17269.
3. Balachandran, S., P. C. Roberts, L. E. Brown, H. Truong, A. K. Pattnaik, D. R. Archer, and G. N. Barber. 2000. Essential role for the dsRNA-dependent protein kinase PKR in innate immunity to viral infection. Immunity 13:129-141.
4. Barber, G. N. 2005. The dsRNA-dependent protein kinase, PKR and cell death. Cell Death Differ. 12:563-570.
5. Bergmann, M., A. Garcia-Sastre, E. Carnero, H. Pehamberger, K. Wolf, P. Palese, and T. Muster. 2000. Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J. Virol. 74:6203-6206.
6. Bernstein, E., A. A. Caudy, S. M. Hammond, and G. J. Hannon. 2001. Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409:363-366.
7. Black, B. L., and D. S. Lyles. 1992. Vesicular stomatitis virus matrix protein inhibits host cell-directed transcription of target genes in vivo. J. Virol. 66:4058-4064.
8. Brandt, T., M. C. Heck, S. Vijaysri, G. M. Jentarra, J. M. Cameron, and B. L. Jacobs. 2005. The N-terminal domain of the vaccinia virus E3L-protein is required for neurovirulence, but not induction of a protective immune response. Virology 333:263-270.
9. Chen, Z., Y. Li, and R. M. Krug. 1999. Influenza A virus NS1 protein targets poly(A)-binding protein II of the cellular 3′-end processing machinery. EMBO J. 18:2273-2283.
10. Chien, C. Y., Y. Xu, R. Xiao, J. M. Aramini, P. V. Sahasrabudhe, R. M. Krug, and G. T. Montelione. 2004. Biophysical characterization of the complex between double-stranded RNA and the N-terminal domain of the NS1 protein from influenza A virus: evidence for a novel RNA-binding mode. Biochemistry 43:1950-1962.
11. Chuang, J. L. 1997. Vesicular stomatitis virus transcription and replication; insights derived from the poIR mutants. Ph.D. thesis. University of California-San Diego and San Diego State University.
12. Chuang, J. L., R. L. Jackson, and J. Perrault. 1997. Isolation and characterization of vesicular stomatitis virus PoIR revenants: polymerase readthrough of the leader-N gene junction is linked to an ATP-dependent function. Virology 229:57-67.
13. Chuang, J. L., and J. Perrault. 1997. Initiation of vesicular stomatitis virus mutant polR1 transcription internally at the N gene in vitro. J. Virol. 71:1466-1475.
14. Connor, J. H., and D. S. Lyles. 2005. Inhibition of host and viral translation during vesicular stomatitis virus infection. eIF2 is responsible for the inhibition of viral but not host translation. J. Biol. Chem. 280:13512-13519.
15. Connor, J. H., and D. S. Lyles. 2002. Vesicular stomatitis virus infection alters the eIF4F translation initiation complex and causes dephosphorylation of the eIF4E binding protein 4E-BP1. J. Virol. 76:10177-10187.
16. Daigneault, L., A. Haggarty, Q. H. Meng, and D. Skup. 1992. Two distinct pathways of interferon induction as revealed by 2-aminopurine. Nucleic Acids Res. 20:2749-2754.
17. Donelan, N. R., C. F. Basler, and A. Garcia-Sastre. 2003. A recombinant influenza A virus expressing an RNA-binding-defective NS1 protein induces high levels of beta interferon and is attenuated in mice. J. Virol. 77:13257-13266.
18. Donelan, N. R., B. Dauber, X. Wang, C. F. Basler, T. Wolff, and A. Garcia-Sastre. 2004. The N- and C-terminal domains of the NS1 protein of influenza B virus can independently inhibit IRF-3 and beta interferon promoter activation. J. Virol. 78:11574-11582.
19. Durbin, R. K., S. E. Mertz, A. E. Koromilas, and J. E. Durbin. 2002. PKR protection against intranasal vesicular stomatitis virus infection is mouse strain dependent. Viral Immunol. 15:41-51.
20. Enninga, J., D. E. Levy, G. Blobel, and B. M. Fontoura. 2002. Role of nucleoporin induction in releasing an mRNA nuclear export block. Science 295:1523-1525.
21. Faria, P. A., P. Chakraborty, A. Levay, G. N. Barber, H. J. Ezelle, J. Enninga, C. Arana, J. van Deursen, and B. M. Fontoura. 2005. VSV disrupts the Rae1/mrnp41 mRNA nuclear export pathway. Mol. Cell 17:93-102.
22. Fuerst, T. R., E. G. Niles, F. W. Studier, and B. Moss. 1986. Eukaryotic transient-expression system based on recombinant vaccinia virus that synthesizes bacteriophage T7 RNA polymerase. Proc. Natl. Acad. Sci. USA 83:8122-8126.
23. Garcia-Sastre, A. 2002. Mechanisms of inhibition of the host interferon alpha/beta-mediated antiviral responses by viruses. Microbes Infect. 4:647-655.
24. Garcia-Sastre, A., A. Egorov, D. Matassov, S. Brandt, D. E. Levy, J. E. Durbin, P. Palese, and T. Muster. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330.
25. Garcin, D., J. Curran, M. Itoh, and D. Kolakofsky. 2001. Longer and shorter forms of Sendai virus C proteins play different roles in modulating the cellular antiviral response. J. Virol. 75:6800-6807.
26. Garcin, D., J. Curran, and D. Kolakofsky. 2000. Sendai virus C proteins must interact directly with cellular components to interfere with interferon action. J. Virol. 74:8823-5830.
27. Garcin, D., P. Latorre, and D. Kolakofsky. 1999. Sendai virus C proteins counteract the interferon-mediated induction of an antiviral state. J. Virol. 73:6559-6565.
28. Garcin, D., J. B. Marq, F. Iseni, S. Martin, and D. Kolakofsky. 2004. A short peptide at the amino terminus of the Sendai virus C protein acts as an independent element that induces STAT1 instability. J. Virol. 78:8799-8811.
29. Haller, O., G. Kochs, and F. Weber. 2006. The interferon response circuit: induction and suppression by pathogenic viruses. Virology 344:119-130.
30. Hengel, H., U. H. Koszinowski, and K. K. Conzelmann. 2005. Viruses know it all: new insights into IFN networks. Trends Immunol. 26:396-401.
31. Jackson, R. L., D. Spadafora, and J. Perrault. 1995. Hierarchal constitutive phosphorylation of the vesicular stomatitis virus P protein and lack of effect on P1 to P2 conversion. Virology 214:189-197.
32. Kato, A., Y. Ohnishi, M. Kohase, S. Saito, M. Tashiro, and Y. Nagai. 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.
33. Katze, M. G., Y. He, and M. Gale, Jr. 2002. Viruses and interferon: a fight for supremacy. Nat. Rev. Immunol. 2:675-687.
34. Kawai, T., and S. Akira. 2006. Innate immune recognition of viral infection. Nat. Immunol. 7:131-137.
35. Krug, R. M., W. Yuan, D. L. Noah, and A. G. Latham. 2003. Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309:181-189.
36. Kwon, J. A., and A. Rich. 2005. Biological function of the vaccinia virus Z-DNA-binding protein E3L: gene transactivation and antiapoptotic activity in HeLa cells. Proc. Natl. Acad. Sci. USA 102:12759-12764.
37. Langland, J. O., and B. L. Jacobs. 2004. Inhibition of PKR by vaccinia virus: role of the N- and C-terminal domains of E3L. Virology 324:419-429.
38. Langland, J. O., and B. L. Jacobs. 2002. The role of the PKR-inhibitory genes, E3L and K3L, in determining vaccinia virus host range. Virology 299:133-141.
39. Lawson, N. D., E. A. Stillman, M. A. Whitt, and J. K. Rose. 1995. Recombinant vesicular stomatitis viruses from DNA. Proc. Natl. Acad. Sci. USA 92:4477-4481.
40. Li, S., J. Y. Min, R. M. Krug, and G. C. Sen. 2006. Binding of the influenza A virus NS1 protein to PKR mediates the inhibition of its activation by either PACT or double-stranded RNA. Virology 349:13-21.
41. Marcus, P. I., and M. J. Sekellick. 1977. Defective interfering particles with covalently linked [+/-]RNA induce interferon. Nature 266:815-819.
42. Marcus, P. I., and M. J. Sekellick. 1988. Interferon induction by viruses. XVI. 2-Aminopurine blocks selectively and reversibly an early stage in interferon induction. J. Gen. Virol. 69:1637-1645.
43. McWhirter, S. M., B. R. Tenoever, and T. Maniatis. 2005. Connecting mitochondria and innate immunity. Cell 122:645-647.
44. Meager, A. 2002. Biological assays for interferons. J. Immunol. Methods 261:21-36.
45. Ostertag, D., T. M. Hoblitzell-Ostertag, and J. Perrault. 2007. Cell-type-specific growth restriction of vesicular stomatitis virus poIR mutants is linked to defective viral polymerase function. J. Virol. 81:492-502.
46. Perrault, J., G. M. Clinton, and M. A. McClure. 1983. RNP template of vesicular stomatitis virus regulates transcription and replication functions. Cell 35:175-185.
47. Romano, P. R., F. Zhang, S. L. Tan, M. T. Garcia-Barrio, M. G. Katze, T. E. Dever, and A. G. Hinnebusch. 1998. Inhibition of double-stranded RNA-dependent protein kinase PKR by vaccinia virus E3: role of complex formation and the E3 N-terminal domain. Mol. Cell. Biol. 18:7304-7316.
48. Rose, J. K., and M. A. Whitt. 2001. Rhabdoviridae: the viruses and their replication, p. 1221-1244. In D. M. Knipe and P. M. Howley (ed.), Fields virology, 4th ed., vol. 1. Lippincott Williams and Wilkins, Philadelphia, PA.
49. Samuel, C. E. 1991. Antiviral actions of interferon. Interferon-regulated cellular proteins and their surprisingly selective antiviral activities. Virology 183:1-11.
50. Saunders, L. R., and G. N. Barber. 2003. The dsRNA binding protein family: critical roles, diverse cellular functions. FASEB J. 17:961-983.
51. Schnell, M. J., L. Buonocore, M. A. Whitt, and J. K. Rose. 1996. The minimal conserved transcription stop-start signal promotes stable expression of a foreign gene in vesicular stomatitis virus. J. Virol. 70:2318-2323.
52. Schroder, M., and A. G. Bowie. 2005. TLR3 in antiviral immunity: key player or bystander? Trends Immunol. 26:462-468.
53. Sen, G. C., and S. N. Sarkar. 2005. Transcriptional signaling by double-stranded RNA: role of TLR3. Cytokine Growth Factor Rev. 16:1-14.
54. Shors, S. T., E. Beattie, E. Paoletti, J. Tartaglia, and B. L. Jacobs. 1998. Role of the vaccinia virus E3L and K3L gene products in rescue of VSV and EMCV from the effects of IFN-alpha. J. Interferon Cytokine Res. 18:721-729.
55. Spadafora, D., D. M. Canter, R. L. Jackson, and J. Perrault. 1996. Constitutive phosphorylation of the vesicular stomatitis virus P protein modulates polymerase complex formation but is not essential for transcription or replication. J. Virol. 70:4538-4548.
56. Stillman, E. A., J. K. Rose, and M. A. Whitt. 1995. Replication and amplification of novel vesicular stomatitis virus minigenomes encoding viral structural proteins. J. Virol. 69:2946-2953.
57. Stojdl, D. F., N. Abraham, S. Knowles, R. Marius, A. Brasey, B. D. Lichty, E. G. Brown, N. Sonenberg, and J. C. Bell. 2000. The murine double-stranded RNA-dependent protein kinase PKR is required for resistance to vesicular stomatitis virus. J. Virol. 74:9580-9585.
58. Talon, J., C. M. Horvath, R. Polley, C. F. Basler, T. Muster, P. Palese, and A. Garcia-Sastre. 2000. Activation of interferon regulatory factor 3 is inhibited by the influenza A virus NS1 protein. J. Virol. 74:7989-7996.
59. Tan, S. L., and M. G. Katze. 1998. Biochemical and genetic evidence for complex formation between the influenza A virus NS1 protein and the interferon-induced PKR protein kinase. J. Interferon Cytokine Res. 18:757-766.
60. Vidal, S., and D. Kolakofsky. 1989. Modified model for the switch from Sendai virus transcription to replication. J. Virol. 63:1951-1958.
61. Wang, W., and R. M. Krug. 1996. The RNA-binding and effector domains of the viral NS1 protein are conserved to different extents among influenza A and B viruses. Virology 223:41-50.
62. Whitaker-Dowling, P., and J. S. Youngner. 1983. Vaccinia rescue of VSV from interferon-induced resistance: reversal of translation block and inhibition of protein kinase activity. Virology 131:128-136.
63. Whitaker-Dowling, P., and J. S. Youngner. 1988. Vaccinia virus stimulates the growth of vesicular stomatitis virus at the level of protein synthesis in mouse L cells. Virus Res. 10:215-224.
64. Williams, B. R. 2001. Signal integration via PKR. Sci. STKE 2001:RE2.
65. Yoneyama, M., and T. Fujita. 2004. RIG-I: critical regulator for virus-induced innate immunity. Tanpakushitsu Kakusan Koso 49:2571-2578. (In Japanese.)
66. Yoneyama, M., M. Kikuchi, T. Natsukawa, N. Shinobu, T. Imaizumi, M. Miyagishi, K. Taira, S. Akira, and T. Fujita. 2004. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat. Immunol. 5:730-737.
67. Yuan, W., and R. M. Krug. 2001. Influenza B virus NS1 protein inhibits conjugation of the interferon (IFN)-induced ubiquitin-like ISG15 protein. EMBO J. 20:362-371.