The influenza A virus NS1 protein binds small interfering RNAs and suppresses RNA silencing in plants

Journal of General Virology

Volumn 85, Issue 4, 2004, Pages 983-991

  Bucher, Etienne ^a   Hemmes, Hans ^a   de Haan, Peter ^b   Goldbach, Rob ^a   Prins, Marcel ^a  

^a WAGENINGEN UNIVERSITY   (Netherlands)

^b Viruvation BV   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; PROTEIN NS1; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VIRUS PROTEIN;

EUKARYOTE; GENE REPRESSION; GENE SILENCING; GENETIC CODE; INFLUENZA VIRUS A; MOLECULAR SIZE; NONHUMAN; PLANT DEVELOPMENT; PLANT VIRUS; PRIORITY JOURNAL; PROTEIN RNA BINDING; REVIEW; RNA DEGRADATION; VIRUS IMMUNITY; VIRUS INHIBITION; VIRUS REPLICATION;

BASE SEQUENCE; BINDING SITES; DNA, VIRAL; HUMANS; INFLUENZA A VIRUS; PLANT VIRUSES; PLANTS; PLANTS, GENETICALLY MODIFIED; POTEXVIRUS; RECOMBINANT FUSION PROTEINS; RNA INTERFERENCE; RNA, DOUBLE-STRANDED; RNA, SMALL INTERFERING; TOBACCO; VIRAL NONSTRUCTURAL PROTEINS; VIRULENCE;

ANIMALIA; EUKARYOTA; FUNGI; INFLUENZA A VIRUS; VERTEBRATA;

EID: 1842832222     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.19734-0     Document Type: Review

References (60)

1. Andino, R. (2003). RNAi puts a lid on virus replication. Nat Biotechnol 21, 629-630.
2. Aragon, T., de la Luna, S., Novoa, I., Carrasco, L., Ortin, J. & Nieto, A. (2000). Eukaryotic translation initiation factor 4GI is a cellular target for NS1 protein, a translational activator of influenza virus. Mol Cell Biol 20, 6259-6268.
3. Beclin, C., Berthome, R., Palauqui, J. C., Tepfer, M. & Vaucheret, H. (1998). Infection of tobacco or Arabidopsis plants by CMV counter-acts systemic post-transcriptional silencing of nonviral (trans)genes. Virology 252, 313-317.
4. Bergmann, M., Garcia-Sastre, A., Carnero, E., Pehamberger, H., Wolff, K., Palese, P. & Muster, T. (2000). Influenza virus NS1 protein counteracts PKR-mediated inhibition of replication. J Virol 74, 6203-6206.
5. Bernstein, E., Caudy, A. A., Hammond, S. M. & Hannon, G. J. (2001). Role for a bidentate ribonuclease in the initiation step of RNA interference. Nature 409, 363-366.
6. Bridge, A. J., Pebernard, S., Ducraux, A., Nicoulaz, A. & Iggo, R. (2003). Induction of an interferon response by RNAi vectors in mammalian cells. Nat Genet 34, 263-264.
7. Brigneti, G., Voinnet, O., Li, W. X., Ji, L. H., Ding, S. W. & Baulcombe, D. C. (1998). Viral pathogenicity determinants are suppressors of transgene silencing in Nicotiana benthamiana. EMBO J 17, 6739-6746.
8. Bucher, E., Sijen, T., De Haan, P., Goldbach, R. & Prins, M. (2003). Negative-strand tospoviruses and tenuiviruses carry a gene for a suppressor of gene silencing at analogous genomic positions. J Virol 77, 1329-1336.
9. Chen, Z., Li, Y. & Krug, R. M. (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. Cogoni, C. & Macino, G. (1997). Isolation of quelling-defective (qde) mutants impaired in posttranscriptional transgene-induced gene silencing in Neurospora crassa. Proc Natl Acad Sci U S A 94, 10233-10238.
11. Dalmay, T., Hamilton, A., Rudd, S., Angell, S. & Baulcombe, D. C. (2000). An RNA-dependent RNA polymerase gene in Arabidopsis is required for posttranscriptional gene silencing mediated by a transgene but not by a virus. Cell 101, 543-553.
12. de Haan, P., Gielen, J. J. L., Prins, M., Wijkamp, I. G., Van Schepen, A., Peters, D., Van Grinsven, M. Q. J. M. & Goldach, R. (1992). Characterization of RNA-mediated resistance to tomato spotted wilt virus in transgenic plants. Bio/Technology 10, 1133-1137.
13. Delgadillo, M. O., Sáenz, P., Salvador, B., García, J. A. & Simón-Mateo, C. (2004). Human influenza virus NS1 protein enhances viral pathogenicity and acts as an RNA silencing suppressor in plants. J Gen Virol 85, 993-999.
14. Elbashir, S. M., Harborth, J., Lendeckel, W., Yalcin, A., Weber, K. & Tuschl, T. (2001). Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411, 494-498.
15. English, J. J., Mueller, E. & Baulcombe, D. C. (1996). Suppression of virus accumulation in transgenic plants exhibiting silencing of nuclear genes. Plant Cell 8, 179-188.
16. Fire, A., Xu, S., Montgomery, M. K., Kostas, S. A., Driver, S. E. & Mello, C. C. (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391, 806-811.
17. Garcia-Sastre, A. (2001). Inhibition of interferon-mediated antiviral responses by influenza A viruses and other negative-strand RNA viruses. Virology 279, 375-384.
18. Garcia-Sastre, A., Egorov, A., Matassov, D., Brandt, S., Levy, D. E., Durbin, J. E., Palese, P. & Muster, T. (1998). Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252, 324-330.
19. Gitlin, L., Karelsky, S. & Andino, R. (2002). Short interfering RNA confers intracellular antiviral immunity in human cells. Nature 418, 430-434.
20. Hall, I. M., Noma, K. & Grewal, S. I. (2003). RNA interference machinery regulates chromosome dynamics during mitosis and meiosis in fission yeast. Proc Natl Acad Sci U S A 100, 193-198.
21. Hamilton, A. J. & Baulcombe, D. C. (1999). A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950-952.
22. Hamilton, A., Voinnet, O., Chappell, L. & Baulcombe, D. (2002). Two classes of short interfering RNA in RNA silencing. EMBO J 21, 4671-4679.
23. Hatada, E. & Fukuda, R. (1992). Binding of influenza A virus NS1 protein to dsRNA in vitro. J Gen Virol 73, 3325-3329.
24. Johansen, L. K. & Carrington, J. C. (2001). Silencing on the spot. Induction and suppression of RNA silencing in the Agrobacterium-mediated transient expression system. Plant Physiol 126, 930-938.
25. Kaufman, R. J. (1999). Double-stranded RNA-activated protein kinase mediates virus-induced apoptosis: a new role for an old actor. Proc Natl Acad Sci U S A 96, 11693-11695.
26. Ketting, R. F., Haverkamp, T. H., Van Luenen, H. G. & Plasterk, R. H. (1999). Mut-7 of C. elegans, required for transposon silencing and RNA interference, is a homolog of Werner syndrome helicase and RNaseD. Cell 99, 133-141.
27. Krug, R. M., Yuan, W., Noah, D. L. & Latham, A. G. (2003). Intracellular warfare between human influenza viruses and human cells: the roles of the viral NS1 protein. Virology 309, 181-189.
28. Li, W. X. & Ding, S. W. (2001). Viral suppressors of RNA silencing. Curr Opin Biotechnol 12, 150-154.
29. Li, H., Li, W. X. & Ding, S. W. (2002). Induction and suppression of RNA silencing by an animal virus. Science 296, 1319-1321.
30. Lichner, Z., Silhavy, D. & Burgyan, J. (2003). Double-stranded RNA-binding proteins could suppress RNA interference-mediated antiviral defences. J Gen Virol 84, 975-980.
31. Lindbo, J. A. & Dougherty, W. G. (1992). Untranslatable transcripts of the tobacco etch virus coat protein gene sequence can interfere with tobacco etch virus replication in transgenic plants and protoplasts. Virology 189, 725-733.
32. Lipardi, C., Wei, Q. & Paterson, B. M. (2001). RNAi as random degradative PCR: siRNA primers convert mRNA into dsRNAs that are degraded to generate new siRNAs. Cell 107, 297-307.
33. Llave, C., Kasschau, K. D. & Carrington, J. C. (2000). Virus-encoded suppressor of posttranscriptional gene silencing targets a maintenance step in the silencing pathway. Proc Natl Acad Sci U S A 97, 13401-13406.
34. Llave, C., Xie, Z., Kasschau, K. D. & Carrington, J. C. (2002). Cleavage of scarecrow-like mRNA targets directed by a class of Arabidopsis miRNA. Science 297, 2053-2056.
35. Lu, Y., Wambach, M., Katze, M. G. & Krug, R. M. (1995). Binding of the influenza virus NS1 protein to double-stranded RNA inhibits the activation of the protein kinase that phosphorylates the elF-2 translation initiation factor. Virology 214, 222-228.
36. McCaffrey, A. P., Meuse, L., Pham, T. T., Conklin, D. S., Hannon, G. J. & Kay, M. A. (2002). RNA interference in adult mice. Nature 418, 38-39.
37. Mallory, A. C., Ely, L., Smith, T. H. & 7 other authors (2001). HC-Pro suppression of transgene silencing eliminates the small RNAs but not transgene methylation or the mobile signal. Plant Cell 13, 571-583.
38. Mourrain, P., Beclin, C., Elmayan, T. & 11 other authors (2000). Arabidopsis SGS2 and SGS3 genes are required for posttranscriptional gene silencing and natural virus resistance. Cell 101, 533-542.
39. Napoli, C. (1990). Introduction of chalcone synthase gene into Petunia results in reversible co-suppression of homologous genes in trans. Plant Cell 2, 279-289.
40. Palatnik, J. F., Allen, E., Wu, X., Schommer, C., Schwab, R., Carrington, J. C. & Weigel, D. (2003). Control of leaf morphogenesis by microRNAs. Nature 425, 257-263.
41. Qu, F. & Morris, T. J. (2002). Efficient infection of Nicotiana benthamiana by Tomato bushy stunt virus is facilitated by the coat protein and maintained by p19 through suppression of gene silencing. Mol Plant Microbe Interact 15, 193-202.
42. Rebouillat, D. & Hovanessian, A. G. (1999). The human 2′,5′-oligoadenylate synthetase family: interferon-induced proteins with unique enzymatic properties. J Interferon Cytokine Res 19, 295-308.
43. Sharma, A. D., Gill, P. K. & Singh, P. (2003). RNA isolation from plant tissues rich in polysaccharides. Anal Biochem 314, 319-321.
44. Sharp, P. A. (2001). RNA interference - 2001. Genes Dev 15, 485-490.
45. Sijen, T., Fleenor, J., Simmer, F., Thijssen, K. L., Parrish, S., Timmons, L., Plasterk, R. H. & Fire, A. (2001). On the role of RNA amplification in dsRNA-triggered gene silencing. Cell 107, 465-476.
46. Silhavy, D., Molnar, A., Lucioli, A., Szittya, G., Hornyik, C., Tavazza, M. & Burgyan, J. (2002). A viral protein suppresses RNA silencing and binds silencing-generated, 21- to 25-nucleotide double-stranded RNAs. EMBO J 21, 3070-3080.
47. Sledz, C. A., Holko, M., de Veer, M. J., Silverman, R. H. & Williams, B. R. (2003). Activation of the interferon system by short-interfering RNAs. Nat Cell Biol 5, 834-839.
48. Tabara, H., Sarkissian, M., Kelly, W. G., Fleenor, J., Grishok, A., Timmons, L., Fire, A. & Mello, C. C. (1999). The rde-1 gene, RNA interference, and transposon silencing in C. elegans. Cell 99, 123-132.
49. Tuschl, T., Zamore, P. D., Lehmann, R., Bartel, D. P. & Sharp, P. A. (1999). Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 13, 3191-3197.
50. Van der Krol, A. R., Mur, L. A., Beld, M., Mol, J. N. & Stuitje, A. R. (1990). Flavonoid genes in petunia: addition of a limited number of gene copies may lead to a suppression of gene expression. Plant Cell 2, 291-299.
51. Van Regenmortel, M. H. V., Fauquet, C. M., Bishop, D. H. L. & 8 other (editors) (2000). Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses. San Diego: Academic Press.
52. Vaucheret, H. & Fagard, M. (2001). Transcriptional gene silencing in plants: targets, inducers and regulators. Trends Genet 17, 29-35.
53. Vende, P., Taraporewala, Z. F. & Patton, J. T. (2002). RNA-binding activity of the rotavirus phosphoprotein NSP5 includes affinity for double-stranded RNA. J Virol 76, 5291-5299.
54. Voinnet, O., Pinto, Y. M. & Baulcombe, D. C. (1999). Suppression of gene silencing: a general strategy used by diverse DNA and RNA viruses of plants. Proc Natl Acad Sci U S A 96, 14147-14152.
55. Voinnet, O., Lederer, C. & Baulcombe, D. C. (2000). A viral movement protein prevents spread of the gene silencing signal in Nicotiana benthamiana. Cell 103, 157-167.
56. Wang, W., Riedel, K., Lynch, P., Chien, C. Y., Montelione, G. T. & Krug, R. M. (1999). RNA binding by the novel helical domain of the influenza virus NS1 protein requires its dimer structure and a small number of specific basic amino acids. RNA 5, 195-205.
57. Wang, X., Li, M., Zheng, H., Muster, T., Palese, P., Beg, A. A. & Garcia-Sastre, A. (2000). Influenza A virus NS1 protein prevents activation of NF-κB and induction of alpha/beta interferon. J Virol 74, 11566-11573.
58. Wang, X., Basler, C. F., Williams, B. R., Silverman, R. H., Palese, P. & Garcia-Sastre, A. (2002). Functional replacement of the carboxy-terminal two-thirds of the influenza A virus NS1 protein with short heterologous dimerization domains. J Virol 76, 12951-12962.
59. Williams, B. R. (1999). PKR; a sentinel kinase for cellular stress. Oncogene 18, 6112-6120.
60. Zamore, P. D. (2002). Ancient pathways programmed by small RNAs. Science 296, 1265-1269.