1887

Abstract

Vector-borne viral diseases pose significant risks to human health. To control the transmission of these viruses, a number of approaches are required. The ability of the intracellular bacteria to limit viral accumulation and transmission in some arthropod hosts, highlights its potential as a biocontrol agent. Whilst can reduce the transmission of several epidemiologically important viruses, protection is not consistent amongst all insects, viruses and strains of , which confounds elucidation of the mechanisms that underly this protection. Evidence of different mechanisms has emerged, but is not always consistent, suggesting the tripartite interaction may be complex. Here we provide evidence that -mediated antiviral protection is dependent on the presence of in individual cells, and cannot be conferred to surrounding cells. Our results suggest that protection is cell-autonomous, and this has several mechanistic implications, which can direct future research.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.001342
2019-10-10
2019-10-15
Loading full text...

Full text loading...

References

  1. Hilgenboecker K, Hammerstein P, Schlattmann P, Telschow A, Werren JH. How many species are infected with Wolbachia?--A statistical analysis of current data. FEMS Microbiol Lett 2008;281:215–220 [CrossRef]
    [Google Scholar]
  2. Zug R, Hammerstein P. Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PLoS One 2012;7:e38544 [CrossRef]
    [Google Scholar]
  3. Weinert LA, Araujo-Jnr EV, Ahmed MZ, Welch JJ. The incidence of bacterial endosymbionts in terrestrial arthropods. Proc Biol Sci 2015;282:20150249 [CrossRef]
    [Google Scholar]
  4. Werren JH, Baldo L, Clark ME. Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 2008;6:741–751 [CrossRef]
    [Google Scholar]
  5. Teixeira L, Ferreira Álvaro, Ashburner M. The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 2008;6:e1000002 [CrossRef]
    [Google Scholar]
  6. Hedges LM, Brownlie JC, O'Neill SL, Johnson KN. Wolbachia and virus protection in insects. Science 2008;322:702 [CrossRef]
    [Google Scholar]
  7. Bian G, Xu Y, Lu P, Xie Y, Xi Z. The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti. PLoS Pathog 2010;6:e1000833 [CrossRef]
    [Google Scholar]
  8. Xi Z, Khoo CCH, Dobson SL. Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 2005;310:326328 [CrossRef]
    [Google Scholar]
  9. McMeniman CJ, Lane RV, Cass BN, Fong AWC, Sidhu M et al. Stable introduction of a life-shortening Wolbachia infection into the mosquito Aedes aegypti. Science 2009;323:141–144 [CrossRef]
    [Google Scholar]
  10. Aliota MT, Walker EC, Uribe Yepes A, Dario Velez I, Christensen BM et al. The wMel strain of Wolbachia reduces transmission of chikungunya virus in Aedes aegypti. PLoS Negl Trop Dis 2016;10:e0004677 [CrossRef]
    [Google Scholar]
  11. Aliota MT, Peinado SA, Velez ID, Osorio JE. The wMel strain of Wolbachia reduces transmission of zika virus by Aedes aegypti. Sci Rep 2016;6:28792 [CrossRef]
    [Google Scholar]
  12. Walker T, Johnson PH, Moreira LA, Iturbe-Ormaetxe I, Frentiu FD et al. The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 2011;476:450–453 [CrossRef]
    [Google Scholar]
  13. van den Hurk AF, Hall-Mendelin S, Pyke AT, Frentiu FD, McElroy K et al. Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti. PLoS Negl Trop Dis 2012;6:e1892 [CrossRef]
    [Google Scholar]
  14. Moreira LA, Iturbe-Ormaetxe I, Jeffery JA, Lu G, Pyke AT et al. A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium. Cell 2009;139:1268–1278 [CrossRef]
    [Google Scholar]
  15. Dutra HLC, Rocha MN, Dias FBS, Mansur SB, Caragata EP et al. Wolbachia blocks currently circulating Zika Virus Isolates in brazilian Aedes aegypti mosquitoes. Cell Host Microbe 2016;19:771–774 [CrossRef]
    [Google Scholar]
  16. Martinez J, Longdon B, Bauer S, Chan Y-S, Miller WJ et al. Symbionts commonly provide broad spectrum resistance to viruses in insects: a comparative analysis of Wolbachia strains. PLoS Pathog 2014;10:e1004369 [CrossRef]
    [Google Scholar]
  17. Osborne SE, Leong YS, O'Neill SL, Johnson KN. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 2009;5:e1000656 [CrossRef]
    [Google Scholar]
  18. Chrostek E, Marialva MSP, Esteves SS, Weinert LA, Martinez J et al. Wolbachia variants induce differential protection to viruses in Drosophila melanogaster: a phenotypic and phylogenomic analysis. PLoS Genet 2013;9:e1003896 [CrossRef]
    [Google Scholar]
  19. Dodson BL, Hughes GL, Paul O, Matacchiero AC, Kramer LD et al. Wolbachia enhances West Nile virus (WNV) infection in the mosquito Culex tarsalis. PLoS Negl Trop Dis 2014;8:e2965 [CrossRef]
    [Google Scholar]
  20. Skelton E, Rancès E, Frentiu FD, Kusmintarsih ES, Iturbe-Ormaetxe I et al. A native Wolbachia endosymbiont does not limit dengue virus infection in the mosquito Aedes notoscriptus (Diptera: Culicidae). J Med Entomol 2016;53:401408 [CrossRef]
    [Google Scholar]
  21. Micieli MV, Glaser RL. Somatic Wolbachia (Rickettsiales: Rickettsiaceae) levels in Culex quinquefasciatus and Culex pipiens (Diptera: Culicidae) and resistance to West Nile virus infection. J Med Entomol 2014;51:189–199 [CrossRef]
    [Google Scholar]
  22. Joubert DA, O’Neill SL. Comparison of stable and transient Wolbachia infection models in Aedes aegypti to block dengue and West Nile viruses. PLoS Negl Trop Dis 2017;11:e0005275 [CrossRef]
    [Google Scholar]
  23. Johnson KN. The impact of Wolbachia on virus infection in mosquitoes. Viruses 2015;7:5705–5717 [CrossRef]
    [Google Scholar]
  24. Kean J, Rainey SM, McFarlane M, Donald CL, Schnettler E et al. Fighting arbovirus transmission: natural and engineered control of vector competence in Aedes mosquitoes. Insects 2015;6:236–278 [CrossRef]
    [Google Scholar]
  25. Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 2012;6:e1754 [CrossRef]
    [Google Scholar]
  26. Osborne SE, Leong YS, O'Neill SL, Johnson KN. Variation in antiviral protection mediated by different Wolbachia strains in Drosophila simulans. PLoS Pathog 2009;5:e1000656 [CrossRef]
    [Google Scholar]
  27. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 2012;78:6922–6929 [CrossRef]
    [Google Scholar]
  28. Pan X, Zhou G, Wu J, Bian G, Lu P et al. Wolbachia induces reactive oxygen species (ROS)-dependent activation of the Toll pathway to control dengue virus in the mosquito Aedes aegypti. Proc Natl Acad Sci USA 2012;109:E23–E31 [CrossRef]
    [Google Scholar]
  29. Wong ZS, Brownlie JC, Johnson KN. Oxidative stress correlates with Wolbachia-mediated antiviral protection in Wolbachia-Drosophila associations. Appl Environ Microbiol 2015;81:30013005 [CrossRef]
    [Google Scholar]
  30. Rancès E, Ye YH, Woolfit M, McGraw EA, O'Neill SL. The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 2012;8:e1002548 [CrossRef]
    [Google Scholar]
  31. Wong ZS, Hedges LM, Brownlie JC, Johnson KN. Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS One 2011;6:e25430 [CrossRef]
    [Google Scholar]
  32. Caragata EP, Rancès E, Hedges LM, Gofton AW, Johnson KN et al. Dietary cholesterol modulates pathogen blocking by Wolbachia. PLoS Pathog 2013;9:e1003459 [CrossRef]
    [Google Scholar]
  33. Bian G, Zhou G, Lu P, Xi Z. Replacing a native Wolbachia with a novel strain results in an increase in endosymbiont load and resistance to dengue virus in a mosquito vector. PLoS Negl Trop Dis 2013;7:e2250 [CrossRef]
    [Google Scholar]
  34. Frentiu FD, Robinson J, Young PR, McGraw EA, O'Neill SL. Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS One 2010;5:e13398 [CrossRef]
    [Google Scholar]
  35. Osborne SE, Iturbe-Ormaetxe I, Brownlie JC, O'Neill SL, Johnson KN. Antiviral protection and the importance of Wolbachia density and tissue tropism in Drosophila simulans. Appl Environ Microbiol 2012;78:6922–6929 [CrossRef]
    [Google Scholar]
  36. Amuzu HE, McGraw EA. Wolbachia-based dengue virus inhibition is not tissue-specific in Aedes aegypti. PLoS Negl Trop Dis 2016;10:e0005145 [CrossRef]
    [Google Scholar]
  37. Rainey SM, Martinez J, McFarlane M, Juneja P, Sarkies P et al. Wolbachia blocks viral genome replication early in infection without a transcriptional response by the endosymbiont or host small RNA pathways. PLoS Pathog 2016;12:e1005536 [CrossRef]
    [Google Scholar]
  38. Tsai KH, Huang CG, Wu WJ, Chuang CK, Lin CC et al. Parallel infection of Japanese encephalitis virus and Wolbachia within cells of mosquito salivary glands. J Med Entomol 2006;43:752–756 [CrossRef]
    [Google Scholar]
  39. Serbus LR, Landmann F, Bray WM, White PM, Ruybal J et al. A cell-based screen reveals that the albendazole metabolite, albendazole sulfone, targets Wolbachia. PLoS Pathog 2012;8:e1002922 [CrossRef]
    [Google Scholar]
  40. Bhattacharya T, Newton ILG, Hardy RW. Wolbachia elevates host methyltransferase expression to block an RNA virus early during infection. PLoS Pathog 2017;13:e1006427 [CrossRef]
    [Google Scholar]
  41. Serbus LR, Ferreccio A, Zhukova M, McMorris CL, Kiseleva E et al. A feedback loop between Wolbachia and the Drosophila gurken mRNP complex influences Wolbachia titer. J Cell Sci 2011;124:4299–4308 [CrossRef]
    [Google Scholar]
  42. White PM, Serbus LR, Debec A, Codina A, Bray W et al. Reliance of Wolbachia on high rates of host proteolysis revealed by a genome-wide RNAi screen of Drosophila cells. Genetics 2017;205:1473–1488 [CrossRef]
    [Google Scholar]
  43. Lu P, Bian G, Pan X, Xi Z. Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 2012;6:e1754 [CrossRef]
    [Google Scholar]
  44. Bian G, Joshi D, Dong Y, Lu P, Zhou G et al. Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 2013;340:748–751 [CrossRef]
    [Google Scholar]
  45. Ryu JH, Ha EM, Lee WJ. Innate immunity and gut-microbe mutualism in Drosophila. Dev Comp Immunol 2010;34:369–376 [CrossRef]
    [Google Scholar]
  46. Kuraishi T, Hori A, Kurata S. Host-microbe interactions in the gut of Drosophila melanogaster. Front Physiol 2013;4:375 [CrossRef]
    [Google Scholar]
  47. Sigle LT, McGraw EA. Expanding the canon: non-classical mosquito genes at the interface of arboviral infection. Insect Biochem Mol Biol 2019;109:7280 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.001342
Loading
/content/journal/jgv/10.1099/jgv.0.001342
Loading

Data & Media loading...

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