1887

Abstract

The exogenous siRNA pathway is important in restricting arbovirus infection in mosquitoes. Less is known about the role of the PIWI-interacting RNA pathway, or piRNA pathway, in antiviral responses. Viral piRNA-like molecules have recently been described following infection of mosquitoes and derived cell lines with several arboviruses. The piRNA pathway has thus been suggested to function as an additional small RNA-mediated antiviral response to the known infection-induced siRNA response. Here we show that piRNA-like molecules are produced following infection with the naturally mosquito-borne Semliki Forest virus in mosquito cell lines. We show that knockdown of piRNA pathway proteins enhances the replication of this arbovirus and defines the contribution of piRNA pathway effectors, thus characterizing the antiviral properties of the piRNA pathway. In conclusion, arbovirus infection can trigger the piRNA pathway in mosquito cells, and knockdown of piRNA proteins enhances virus production.

  • This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.053850-0
2013-07-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/94/7/1680.html?itemId=/content/journal/jgv/10.1099/vir.0.053850-0&mimeType=html&fmt=ahah

References

  1. Anderson J. F., Main A. J., Cheng G., Ferrandino F. J., Fikrig E. 2012; Horizontal and vertical transmission of West Nile virus genotype NY99 by Culex salinarius and genotypes NY99 and WN02 by Culex tarsalis . Am J Trop Med Hyg 86:134–139 [View Article][PubMed]
    [Google Scholar]
  2. Blair C. D. 2011; Mosquito RNAi is the major innate immune pathway controlling arbovirus infection and transmission. Future Microbiol 6:265–277 [View Article][PubMed]
    [Google Scholar]
  3. Brackney D. E., Scott J. C., Sagawa F., Woodward J. E., Miller N. A., Schilkey F. D., Mudge J., Wilusz J., Olson K. E.& other authors ( 2010; C6/36 Aedes albopictus cells have a dysfunctional antiviral RNA interference response. PLoS Negl Trop Dis 4:e856 [View Article][PubMed]
    [Google Scholar]
  4. Brennecke J., Aravin A. A., Stark A., Dus M., Kellis M., Sachidanandam R., Hannon G. J. 2007; Discrete small RNA-generating loci as master regulators of transposon activity in Drosophila . Cell 128:1089–1103 [View Article][PubMed]
    [Google Scholar]
  5. Campbell C. L., Black W. C. IV, Hess A. M., Foy B. D. 2008a; Comparative genomics of small RNA regulatory pathway components in vector mosquitoes. BMC Genomics 9:425 [View Article][PubMed]
    [Google Scholar]
  6. Campbell C. L., Keene K. M., Brackney D. E., Olson K. E., Blair C. D., Wilusz J., Foy B. D. 2008b; Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol 8:47 [View Article][PubMed]
    [Google Scholar]
  7. Chotkowski H. L., Ciota A. T., Jia Y., Puig-Basagoiti F., Kramer L. D., Shi P. Y., Glaser R. L. 2008; West Nile virus infection of Drosophila melanogaster induces a protective RNAi response. Virology 377:197–206 [View Article][PubMed]
    [Google Scholar]
  8. Donald C. L., Kohl A., Schnettler E. 2012; New insights into control of arbovirus replication and spread by insect RNA interference pathways. Insects 3:511–531 [View Article]
    [Google Scholar]
  9. Hess A. M., Prasad A. N., Ptitsyn A., Ebel G. D., Olson K. E., Barbacioru C., Monighetti C., Campbell C. L. 2011; Small RNA profiling of Dengue virus-mosquito interactions implicates the PIWI RNA pathway in anti-viral defense. BMC Microbiol 11:45 [View Article][PubMed]
    [Google Scholar]
  10. Hoa N. T., Keene K. M., Olson K. E., Zheng L. 2003; Characterization of RNA interference in an Anopheles gambiae cell line. Insect Biochem Mol Biol 33:949–957 [View Article][PubMed]
    [Google Scholar]
  11. Keene K. M., Foy B. D., Sanchez-Vargas I., Beaty B. J., Blair C. D., Olson K. E. 2004; RNA interference acts as a natural antiviral response to O’nyong-nyong virus (Alphavirus; Togaviridae) infection of Anopheles gambiae . Proc Natl Acad Sci U S A 101:17240–17245 [View Article][PubMed]
    [Google Scholar]
  12. Léger P., Lara E., Jagla B., Sismeiro O., Mansuroglu Z., Coppée J. Y., Bonnefoy E., Bouloy M. 2013; Dicer-2 and Piwi mediated RNA interference in Rift Valley Fever virus infected mosquito cells. J Virol 87:1631–1648 [View Article][PubMed]
    [Google Scholar]
  13. Morazzani E. M., Wiley M. R., Murreddu M. G., Adelman Z. N., Myles K. M. 2012; Production of virus-derived ping-pong-dependent piRNA-like small RNAs in the mosquito soma. PLoS Pathog 8:e1002470 [View Article][PubMed]
    [Google Scholar]
  14. Mulyatno K. C., Yamanaka A., Yotopranoto S., Konishi E. 2012; Vertical transmission of dengue virus in Aedes aegypti collected in Surabaya, Indonesia, during 2008-2011. Jpn J Infect Dis 65:274–276 [View Article][PubMed]
    [Google Scholar]
  15. Saito K., Siomi M. C. 2010; Small RNA-mediated quiescence of transposable elements in animals. Dev Cell 19:687–697 [View Article][PubMed]
    [Google Scholar]
  16. Sánchez-Vargas I., Scott J. C., Poole-Smith B. K., Franz A. W., Barbosa-Solomieu V., Wilusz J., Olson K. E., Blair C. D. 2009; Dengue virus type 2 infections of Aedes aegypti are modulated by the mosquito’s RNA interference pathway. PLoS Pathog 5:e1000299 [View Article][PubMed]
    [Google Scholar]
  17. Schnettler E., Ratinier M., Watson M., Shaw A. E., McFarlane M., Varela M., Elliott R. M., Palmarini M., Kohl A. 2013; RNA interference targets arbovirus replication in Culicoides cells. J Virol 87:2441–2454 [View Article][PubMed]
    [Google Scholar]
  18. Scott J. C., Brackney D. E., Campbell C. L., Bondu-Hawkins V., Hjelle B., Ebel G. D., Olson K. E., Blair C. D. 2010; Comparison of dengue virus type 2-specific small RNAs from RNA interference-competent and -incompetent mosquito cells. PLoS Negl Trop Dis 4:e848 [View Article][PubMed]
    [Google Scholar]
  19. Senti K. A., Brennecke J. 2010; The piRNA pathway: a fly’s perspective on the guardian of the genome. Trends Genet 26:499–509 [View Article][PubMed]
    [Google Scholar]
  20. Siomi M. C., Miyoshi T., Siomi H. 2010; piRNA-mediated silencing in Drosophila germlines. Semin Cell Dev Biol 21:754–759 [View Article][PubMed]
    [Google Scholar]
  21. Siomi M. C., Sato K., Pezic D., Aravin A. A. 2011; PIWI-interacting small RNAs: the vanguard of genome defence. Nat Rev Mol Cell Biol 12:246–258 [View Article][PubMed]
    [Google Scholar]
  22. Siu R. W., Fragkoudis R., Simmonds P., Donald C. L., Chase-Topping M. E., Barry G., Attarzadeh-Yazdi G., Rodriguez-Andres J., Nash A. A.& other authors ( 2011; Antiviral RNA interference responses induced by Semliki Forest virus infection of mosquito cells: characterization, origin, and frequency-dependent functions of virus-derived small interfering RNAs. J Virol 85:2907–2917 [View Article][PubMed]
    [Google Scholar]
  23. van Rij R. P., Berezikov E. 2009; Small RNAs and the control of transposons and viruses in Drosophila . Trends Microbiol 17:163–171 [View Article][PubMed]
    [Google Scholar]
  24. van Rij R. P., Saleh M. C., Berry B., Foo C., Houk A., Antoniewski C., Andino R. 2006; The RNA silencing endonuclease Argonaute 2 mediates specific antiviral immunity in Drosophila melanogaster . Genes Dev 20:2985–2995 [View Article][PubMed]
    [Google Scholar]
  25. Vodovar N., Bronkhorst A. W., van Cleef K. W., Miesen P., Blanc H., van Rij R. P., Saleh M. C. 2012; Arbovirus-derived piRNAs exhibit a ping-pong signature in mosquito cells. PLoS ONE 7:e30861 [View Article][PubMed]
    [Google Scholar]
  26. Wu Q., Luo Y., Lu R., Lau N., Lai E. C., Li W. X., Ding S. W. 2010; Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc Natl Acad Sci U S A 107:1606–1611 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.053850-0
Loading
/content/journal/jgv/10.1099/vir.0.053850-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error