Double-stranded RNA-binding proteins could suppress RNA interference-mediated antiviral defences Free

Abstract

RNA interference (RNAi) is a double-stranded (ds)RNA-inducible, sequence-specific RNA-degradation mechanism that operates as a natural antiviral system in plants and animals. Successful virus infection requires evasion or suppression of RNAi. Indeed, RNAi suppressor proteins have been identified in plant and animal viruses, although the molecular mechanism of silencing inhibition is still poorly understood. Because many RNA viruses encode dsRNA-binding proteins (dsRBPs) and as RNAi is triggered by the accumulation of dsRNAs, dsRBPs were examined to see if they inhibit RNAi. Here, it is shown that heterologous dsRBPs suppressed RNAi in plants, indicating that in natural host–virus interactions, pathogen-encoded dsRBPs could inactivate RNAi-mediated host defences.

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2003-04-01
2024-03-29
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References

  1. 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
    [Google Scholar]
  2. Cullen B. R. 2002; RNA interference: antiviral defense and genetic tool. Nat Immunol 3:597–599
    [Google Scholar]
  3. Dasgupta S., Fernandez L., Kameyama L., Inada T., Nakamura Y., Pappas A., Court D. L. 1998; Genetic uncoupling of the dsRNA-binding and RNA cleavage activities of the Escherichia coli endoribonuclease RNase III: the effect of dsRNA binding on gene expression. Mol Microbiol 28:629–640
    [Google Scholar]
  4. Denzler K. L., Jacobs B. L. 1994; Site-directed mutagenic analysis of reovirus σ 3 protein binding to dsRNA. Virology 204:190–199
    [Google Scholar]
  5. Fierro-Monti I., Mathews M. B. 2000; Proteins binding to duplexed RNA: one motif, multiple functions. Trends Biochem Sci 25:241–246
    [Google Scholar]
  6. Giantini M., Shatkin A. J. 1989; Stimulation of chloramphenicol acetyltransferase mRNA translation by reovirus capsid polypeptide σ 3 in cotransfected COS cells. J Virol 63:2415–2421
    [Google Scholar]
  7. Hamilton A., Voinnet O., Chappell L., Baulcombe D. 2002; Two classes of short interfering RNA in RNA silencing. EMBO J 21:4671–4679
    [Google Scholar]
  8. Hannon G. J. 2002; RNA interference. Nature 418:244–251
    [Google Scholar]
  9. Huismans H., Joklik W. K. 1976; Reovirus-coded polypeptides in infected cells: isolation of two native monomeric polypeptides with affinity for single-stranded and double-stranded RNA, respectively. Virology 70:411–424
    [Google Scholar]
  10. Hutvagner G., McLachlan J., Pasquinelli A. E., Balint E., Tuschl T., Zamore P. D. 2001; A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293:834–838
    [Google Scholar]
  11. 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
    [Google Scholar]
  12. 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
    [Google Scholar]
  13. Ketting R. F., Fischer S. E., Bernstein E., Sijen T., Hannon G. J., Plasterk R. H. 2001; Dicer functions in RNA interference and in synthesis of small RNA involved in developmental timing in C. elegans . Genes Dev 15:2654–2659
    [Google Scholar]
  14. Kharrat A., Macias M. J., Gibson T. J., Nilges M., Pastore A. 1995; Structure of the dsRNA binding domain of E. coli RNase III. EMBO J 14:3572–3584
    [Google Scholar]
  15. Langenberg W. G., Zhang L., Court D. L., Giunchedi L., Mitra A. 1997; Transgenic tobacco plants expressing the bacterial rnc gene resist virus infection. Mol Breeding 3:391–399
    [Google Scholar]
  16. Lee Y., Jeon K., Lee J. T., Kim S., Kim V. N. 2002; MicroRNA maturation: stepwise processing and subcellular localization. EMBO J 21:4663–4670
    [Google Scholar]
  17. Li W. X., Ding S. W. 2001; Viral suppressors of RNA silencing. Curr Opin Biotechnol 12:150–154
    [Google Scholar]
  18. Li H., Li W. X., Ding S. W. 2002; Induction and suppression of RNA silencing by an animal virus. Science 296:1319–1321
    [Google Scholar]
  19. 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
    [Google Scholar]
  20. Llave C., Kasschau K. D., Rector M. A., Carrington J. C. 2002; Endogenous and silencing-associated small RNAs in plants. Plant Cell 14:1605–1619
    [Google Scholar]
  21. Matzke M. A., Matzke A. J., Pruss G. J., Vance V. B. 2001; RNA-based silencing strategies in plants. Curr Opin Genet Dev 11:221–227
    [Google Scholar]
  22. Miller J. E., Samuel C. E. 1992; Proteolytic cleavage of the reovirus σ 3 protein results in enhanced double-stranded RNA-binding activity: identification of a repeated basic amino acid motif within the C-terminal binding region. J Virol 66:5347–5356
    [Google Scholar]
  23. Nicholson A. W. 1999; Function, mechanism and regulation of bacterial ribonucleases. FEMS Microbiol Rev 23:371–390
    [Google Scholar]
  24. Palauqui J. C., Elmayan T., Pollien J. M., Vaucheret H. 1997; Systemic acquired silencing: transgene-specific post-transcriptional silencing is transmitted by grafting from silenced stocks to non-silenced scions. EMBO J 16:4738–4745
    [Google Scholar]
  25. Plasterk R. H. 2002; RNA silencing: the genome's immune system. Science 296:1263–1265
    [Google Scholar]
  26. Reinhart B. J., Weinstein E. G., Rhoades M. W., Bartel B., Bartel D. P. 2002; MicroRNAs in plants. Genes Dev 16:1616–1626
    [Google Scholar]
  27. Sano T., Nagayama A., Ogawa T., Ishida I., Okada Y. 1997; Transgenic potato expressing a double-stranded RNA-specific ribonuclease is resistant to potato spindle tuber viroid. Nat Biotechnol 15:1290–1294
    [Google Scholar]
  28. 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
    [Google Scholar]
  29. 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
    [Google Scholar]
  30. Vance V., Vaucheret H. 2001; RNA silencing in plants: defense and counterdefense. Science 292:2277–2280
    [Google Scholar]
  31. Voinnet O. 2001; RNA silencing as a plant immune system against viruses. Trends Genet 17:449–459
    [Google Scholar]
  32. Voinnet O., Baulcombe D. C. 1997; Systemic signalling in gene silencing. Nature 389:553
    [Google Scholar]
  33. 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
    [Google Scholar]
  34. 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
    [Google Scholar]
  35. Watanabe Y., Ogawa T., Takahashi H., Ishida I., Takeuchi Y., Yamamoto M., Okada Y. 1995; Resistance against multiple plant viruses in plants mediated by a double stranded-RNA specific ribonuclease. FEBS Lett 372:165–168
    [Google Scholar]
  36. Yue Z., Shatkin A. J. 1997; Double-stranded RNA-dependent protein kinase (PKR) is regulated by reovirus structural proteins. Virology 234:364–371
    [Google Scholar]
  37. Zamore P. D. 2001; RNA interference: listening to the sound of silence. Nat Struct Biol 8:746–750
    [Google Scholar]
  38. Zhang L., French R., Langenberg W. G., Mitra A. 2001; Accumulation of barley stripe mosaic virus is significantly reduced in transgenic wheat plants expressing a bacterial ribonuclease. Transgenic Res 10:13–19
    [Google Scholar]
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