1887

Abstract

Mosquito-borne viruses are known to cause disease in humans and livestock and are often difficult to control due to the lack of specific antivirals and vaccines. The endosymbiont has been widely studied for its ability to restrict positive-strand RNA virus infection in mosquitoes, although little is known about the precise antiviral mechanism. In recent years, a variety of insect-specific viruses have been discovered in mosquitoes and an interaction with mosquito-borne viruses has been reported for some of them; however, nothing is known about the effect of on insect-specific virus infection in mosquitoes. Here, we show that transinfection of the -derived MelPop strain into -derived cells resulted in inhibition and even clearance of the persistent cell-fusing agent flavivirus infection in these cells. This broadens the antiviral activity of from acute infections to persistent infections and from arboviruses to mosquito-specific viruses. In contrast, no effect on the Phasi Charoen-like bunyavirus persistent infection in these cells was observed, suggesting a difference in inhibition between positive- and negative-strand RNA viruses.

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2016-11-10
2020-01-27
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References

  1. Aguiar E. R., Olmo R. P., Paro S., Ferreira F. V., de Faria I. J., Todjro Y. M., Lobo F. P., Kroon E. G., Meignin C. et al. 2015; Sequence-independent characterization of viruses based on the pattern of viral small RNAs produced by the host. Nucleic Acids Res43:6191–6206 [CrossRef][PubMed]
    [Google Scholar]
  2. Bolling B. G., Weaver S. C., Tesh R. B., Vasilakis N.. 2015; Insect-specific virus discovery: significance for the arbovirus community. Viruses7:4911–4928 [CrossRef][PubMed]
    [Google Scholar]
  3. Frentiu F. D., Zakir T., Walker T., Popovici J., Pyke A. T., van den Hurk A., McGraw E. A., O'Neill S. L.. 2014; Limited dengue virus replication in field-collected Aedes aegypti mosquitoes infected with Wolbachia. PLoS Negl Trop Dis8:e2688 [CrossRef][PubMed]
    [Google Scholar]
  4. Hedges L. M., Brownlie J. C., O'Neill S. L., Johnson K. N.. 2008; Wolbachia and virus protection in insects. Science322:702 [CrossRef][PubMed]
    [Google Scholar]
  5. Hoffmann A. A., Montgomery B. L., Popovici J., Iturbe-Ormaetxe I., Johnson P. H., Muzzi F., Greenfield M., Durkan M., Leong Y. S. et al. 2011; Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature476:454–457 [CrossRef][PubMed]
    [Google Scholar]
  6. Hoffmann A. A., Iturbe-Ormaetxe I., Callahan A. G., Phillips B. L., Billington K., Axford J. K., Montgomery B., Turley A. P., O'Neill S. L.. 2014; Stability of the wMel Wolbachia infection following invasion into Aedes aegypti populations. PLoS Negl Trop Dis8:e3115 [CrossRef][PubMed]
    [Google Scholar]
  7. Iturbe-Ormaetxe I., Walker T., O' Neill S. L.. 2011; Wolbachia and the biological control of mosquito-borne disease. EMBO Rep12:508–518 [CrossRef][PubMed]
    [Google Scholar]
  8. Kean J., Rainey S. M., McFarlane M., Donald C. L., Schnettler E., Kohl A., Pondeville E.. 2015; Fighting arbovirus transmission: natural and engineered control of vector competence in Aedes mosquitoes. Insects6:236 [CrossRef][PubMed]
    [Google Scholar]
  9. 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 Virol87:1631–1648 [CrossRef][PubMed]
    [Google Scholar]
  10. Maringer K., Yousuf A., Heesom K., Frnandez-sesma A., Matthews D. A., Davidson A. D.. 2015; De novo ‘proteomics informed by transcriptomics’ analysis of aedes aegypti cells identifies novel ORFs, active transposable elements and persistent viruses. Conference Paper. International meeting on arboviruses and their vectors. 7-8. september 2015. Glasgow, UK
    [Google Scholar]
  11. Marklewitz M., Zirkel F., Kurth A., Drosten C., Junglen S.. 2015; Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc Natl Acad Sci U S A112:7536–7541 [CrossRef][PubMed]
    [Google Scholar]
  12. Martinez J., Longdon B., Bauer S., Chan Y. S., Miller W. J., Bourtzis K., Teixeira L., Jiggins F. M.. 2014; Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog10:e1004369 [CrossRef][PubMed]
    [Google Scholar]
  13. Mayoral J. G., Etebari K., Hussain M., Khromykh A. A., Asgari S.. 2014; Wolbachia infection modifies the profile, shuttling and structure of microRNAs in a mosquito cell line. PLoS One9:e96107 [CrossRef][PubMed]
    [Google Scholar]
  14. McFarlane M., Arias-Goeta C., Martin E., O'Hara Z., Lulla A., Mousson L., Rainey S. M., Misbah S., Schnettler E. et al. 2014; Characterization of Aedes aegypti innate-immune pathways that limit chikungunya virus replication. PLoS Negl Trop Dis8:e2994 [CrossRef][PubMed]
    [Google Scholar]
  15. McMeniman C. J., Lane R. V., Cass B. N., Fong A. W., Sidhu M., Wang Y. F., O'Neill S. L.. 2009; Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science323:141–144 [CrossRef][PubMed]
    [Google Scholar]
  16. Moreira L. A., Iturbe-Ormaetxe I., Jeffery J. A., Lu G., Pyke A. T., Hedges L. M., Rocha B. C., Hall-Mendelin S., Day A. et al. 2009; A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and plasmodium. Cell139:1268–1278 [CrossRef][PubMed]
    [Google Scholar]
  17. Osborne S. E., Leong Y. S., O'Neill S. L., Johnson K. N.. 2009; Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog5:e1000656 [CrossRef][PubMed]
    [Google Scholar]
  18. Osborne S. E., Iturbe-Ormaetxe I., Brownlie J. C., O'Neill S. L., Johnson K. N.. 2012; Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol78:6922–6929 [CrossRef][PubMed]
    [Google Scholar]
  19. Rainey S. M., Shah P., Kohl A., Dietrich I.. 2014; Understanding the Wolbachia-mediated inhibition of arboviruses in mosquitoes: progress and challenges. J Gen Virol95:517–530 [CrossRef][PubMed]
    [Google Scholar]
  20. Rainey S. M., Martinez J., McFarlane M., Juneja P., Sarkies P., Lulla A., Schnettler E., Varjak M., Merits A. et al. 2016; Wolbachia blocks viral genome replication early in infection without a transcriptional response by the endosymbiont or host small RNA pathways. PLoS Pathog12:e1005536 [CrossRef][PubMed]
    [Google Scholar]
  21. Schnettler E., Donald C. L., Human S., Watson M., Siu R. W. C., McFarlane M., Fazakerley J. K., Kohl A., Fragkoudis R.. 2013a; Knockdown of piRNA pathway proteins results in enhanced Semliki forest virus production in mosquito cells. J Gen Virol94:1680–1689 [CrossRef]
    [Google Scholar]
  22. Schnettler E., Ratinier M., Watson M., Shaw A. E., McFarlane M., Varela M., Elliott R. M., Palmarini M., Kohl A.. 2013b; RNA interference targets arbovirus replication in culicoides cells. J Virol87:2441–2454 [CrossRef]
    [Google Scholar]
  23. 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 Dis4:e848 [CrossRef][PubMed]
    [Google Scholar]
  24. Sinkins S. P.. 2004; Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol34:723–729 [CrossRef][PubMed]
    [Google Scholar]
  25. Teixeira L., Ferreira A., Ashburner M.. 2008; The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol6:e1000002 [CrossRef][PubMed]
    [Google Scholar]
  26. Walker T., Johnson P. H., Moreira L. A., Iturbe-Ormaetxe I., Frentiu F. D., McMeniman C. J., Leong Y. S., Dong Y., Axford J. et al. 2011; The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature476:450–453 [CrossRef][PubMed]
    [Google Scholar]
  27. Weaver S. C., Reisen W. K.. 2010; Present and future arboviral threats. Antiviral Res85:328–345 [CrossRef][PubMed]
    [Google Scholar]
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