1887

Abstract

Arthropod-borne viruses (arboviruses) pose a considerable threat to human and animal health, yet effective control measures have proven difficult to implement, and novel means of controlling their replication in arthropod vectors, such as mosquitoes, are urgently required. One of the most exciting approaches to emerge from research on arthropods is the use of the endosymbiotic intracellular bacterium to control arbovirus transmission from mosquito to vertebrate. These α-proteobacteria propagate through insects, in part through modulation of host reproduction, thus ensuring spread through species and maintenance in nature. Since it was discovered that endosymbiosis inhibits insect virus replication in species, these bacteria have also been shown to inhibit arbovirus replication and spread in mosquitoes. Importantly, it is not clear how these antiviral effects are mediated. This review will summarize recent work and discuss determinants of antiviral effectiveness that may differ between individual /vector/arbovirus interactions. We will also discuss the application of this approach to field settings and the associated risks.

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2014-03-01
2024-03-19
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References

  1. Acosta E. G., Castilla V., Damonte E. B. 2008; Functional entry of dengue virus into Aedes albopictus mosquito cells is dependent on clathrin-mediated endocytosis. J Gen Virol 89:474–484 [View Article][PubMed]
    [Google Scholar]
  2. Acosta E. G., Castilla V., Damonte E. B. 2009; Alternative infectious entry pathways for dengue virus serotypes into mammalian cells. Cell Microbiol 11:1533–1549 [View Article][PubMed]
    [Google Scholar]
  3. Alphey L., McKemey A., Nimmo D., Neira Oviedo M., Lacroix R., Matzen K., Beech C. 2013; Genetic control of Aedes mosquitoes. Pathog Glob Health 107:170–179 [View Article][PubMed]
    [Google Scholar]
  4. Armbruster P., Damsky W. E. Jr, Giordano R., Birungi J., Munstermann L. E., Conn J. E. 2003; Infection of New- and Old-World Aedes albopictus (Diptera: Culicidae) by the intracellular parasite Wolbachia: implications for host mitochondrial DNA evolution. J Med Entomol 40:356–360 [View Article][PubMed]
    [Google Scholar]
  5. Asgari S. 2013; MicroRNA functions in insects. Insect Biochem Mol Biol 43:388–397 [View Article][PubMed]
    [Google Scholar]
  6. Avadhanula V., Weasner B. P., Hardy G. G., Kumar J. P., Hardy R. W. 2009; A novel system for the launch of alphavirus RNA synthesis reveals a role for the Imd pathway in arthropod antiviral response. PLoS Pathog 5:e1000582 [View Article][PubMed]
    [Google Scholar]
  7. Bartholomay L. C., Waterhouse R. M., Mayhew G. F., Campbell C. L., Michel K., Zou Z., Ramirez J. L., Das S., Alvarez K.other authors 2010; Pathogenomics of Culex quinquefasciatus and meta-analysis of infection responses to diverse pathogens. Science 330:88–90 [View Article][PubMed]
    [Google Scholar]
  8. Berticat C., Rousset F., Raymond M., Berthomieu A., Weill M. 2002; High Wolbachia density in insecticide-resistant mosquitoes. Proc Biol Sci 269:1413–1416 [View Article][PubMed]
    [Google Scholar]
  9. Bian G., Xu Y., Lu P., Xie Y., Xi Z. 2010; The endosymbiotic bacterium Wolbachia induces resistance to dengue virus in Aedes aegypti . PLoS Pathog 6:e1000833 [View Article][PubMed]
    [Google Scholar]
  10. Bian G., Joshi D., Dong Y., Lu P., Zhou G., Pan X., Xu Y., Dimopoulos G., Xi Z. 2013a; Wolbachia invades Anopheles stephensi populations and induces refractoriness to Plasmodium infection. Science 340:748–751 [View Article][PubMed]
    [Google Scholar]
  11. Bian G., Zhou G., Lu P., Xi Z. 2013b; 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 7:e2250 [View Article][PubMed]
    [Google Scholar]
  12. Black W. C. IV, Alphey L., James A. A. 2011; Why RIDL is not SIT. Trends Parasitol 27:362–370 [View Article][PubMed]
    [Google Scholar]
  13. Blagrove M. S., Arias-Goeta C., Di Genua C., Failloux A. B., Sinkins S. P. 2013; A Wolbachia wMel transinfection in Aedes albopictus is not detrimental to host fitness and inhibits chikungunya virus. PLoS Negl Trop Dis 7:e2152 [View Article][PubMed]
    [Google Scholar]
  14. 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]
  15. Bourtzis K., Pettigrew M. M., O’Neill S. L. 2000; Wolbachia neither induces nor suppresses transcripts encoding antimicrobial peptides. Insect Mol Biol 9:635–639 [View Article][PubMed]
    [Google Scholar]
  16. 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]
  17. Brown D. T., Condreay L. D. 1986; Replication of alphaviruses in mosquito cells. In The Togaviridae and Flaviviridae pp. 171–207 Edited by Schlesinger M. J. New York: Plenum Publishing; [View Article]
    [Google Scholar]
  18. Brownstein J. S., Hett E., O’Neill S. L. 2003; The potential of virulent Wolbachia to modulate disease transmission by insects. J Invertebr Pathol 84:24–29 [View Article][PubMed]
    [Google Scholar]
  19. Caragata E. P., Rancès E., Hedges L. M., Gofton A. W., Johnson K. N., O’Neill S. L., McGraw E. A. 2013; Dietary cholesterol modulates pathogen blocking by Wolbachia . PLoS Pathog 9:e1003459 [View Article][PubMed]
    [Google Scholar]
  20. Carro A. C., Damonte E. B. 2013; Requirement of cholesterol in the viral envelope for dengue virus infection. Virus Res 174:78–87 [View Article][PubMed]
    [Google Scholar]
  21. Chatterjee P. K., Vashishtha M., Kielian M. 2000; Biochemical consequences of a mutation that controls the cholesterol dependence of Semliki Forest virus fusion. J Virol 74:1623–1631 [View Article][PubMed]
    [Google Scholar]
  22. Cho K. O., Kim G. W., Lee O. K. 2011; Wolbachia bacteria reside in host Golgi-related vesicles whose position is regulated by polarity proteins. PLoS ONE 6:e22703 [View Article][PubMed]
    [Google Scholar]
  23. Christophides G. K., Zdobnov E., Barillas-Mury C., Birney E., Blandin S., Blass C., Brey P. T., Collins F. H., Danielli A.other authors 2002; Immunity-related genes and gene families in Anopheles gambiae . Science 298:159–165 [View Article][PubMed]
    [Google Scholar]
  24. Clayton R. B. 1964; The utilization of sterols by insects. J Lipid Res 5:3–19[PubMed]
    [Google Scholar]
  25. Costa A., Jan E., Sarnow P., Schneider D. 2009; The Imd pathway is involved in antiviral immune responses in Drosophila . PLoS ONE 4:e7436 [View Article][PubMed]
    [Google Scholar]
  26. Dobson S. L., Bourtzis K., Braig H. R., Jones B. F., Zhou W., Rousset F., O’Neill S. L. 1999; Wolbachia infections are distributed throughout insect somatic and germ line tissues. Insect Biochem Mol Biol 29:153–160 [View Article][PubMed]
    [Google Scholar]
  27. 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]
  28. Dostert C., Jouanguy E., Irving P., Troxler L., Galiana-Arnoux D., Hetru C., Hoffmann J. A., Imler J. L. 2005; The Jak-STAT signaling pathway is required but not sufficient for the antiviral response of Drosophila . Nat Immunol 6:946–953 [View Article][PubMed]
    [Google Scholar]
  29. Dutton T. J., Sinkins S. P. 2004; Strain-specific quantification of Wolbachia density in Aedes albopictus and effects of larval rearing conditions. Insect Mol Biol 13:317–322 [View Article][PubMed]
    [Google Scholar]
  30. Echaubard P., Duron O., Agnew P., Sidobre C., Noël V., Weill M., Michalakis Y. 2010; Rapid evolution of Wolbachia density in insecticide resistant Culex pipiens . Heredity (Edinb) 104:15–19 [View Article][PubMed]
    [Google Scholar]
  31. Engelstädter J., Telschow A. 2009; Cytoplasmic incompatibility and host population structure. Heredity (Edinb) 103:196–207 [View Article][PubMed]
    [Google Scholar]
  32. Fragkoudis R., Chi Y., Siu R. W. C., Barry G., Attarzadeh-Yazdi G., Merits A., Nash A. A., Fazakerley J. K., Kohl A. 2008; Semliki Forest virus strongly reduces mosquito host defence signaling. Insect Mol Biol 17:647–656 [View Article][PubMed]
    [Google Scholar]
  33. Fragkoudis R., Attarzadeh-Yazdi G., Nash A. A., Fazakerley J. K., Kohl A. 2009; Advances in dissecting mosquito innate immune responses to arbovirus infection. J Gen Virol 90:2061–2072 [View Article][PubMed]
    [Google Scholar]
  34. Frentiu F. D., Robinson J., Young P. R., McGraw E. A., O’Neill S. L. 2010; Wolbachia-mediated resistance to dengue virus infection and death at the cellular level. PLoS ONE 5:e13398 [View Article][PubMed]
    [Google Scholar]
  35. Glaser R. L., Meola M. A. 2010; The native Wolbachia endosymbionts of Drosophila melanogaster and Culex quinquefasciatus increase host resistance to West Nile virus infection. PLoS ONE 5:e11977 [View Article][PubMed]
    [Google Scholar]
  36. Hafer A., Whittlesey R., Brown D. T., Hernandez R. 2009; Differential incorporation of cholesterol by Sindbis virus grown in mammalian or insect cells. J Virol 83:9113–9121 [View Article][PubMed]
    [Google Scholar]
  37. Haine E. R., Pickup N. J., Cook J. M. 2005; Horizontal transmission of Wolbachia in a Drosophila community. Ecol Entomol 30:464–472 [View Article]
    [Google Scholar]
  38. Halstead S. B. 2012; Dengue vaccine development: a 75 % solution?. Lancet 380:1535–1536 [View Article][PubMed]
    [Google Scholar]
  39. Hancock P. A., Godfray H. C. 2012; Modelling the spread of Wolbachia in spatially heterogeneous environments. J R Soc Interface 9:3045–3054 [View Article][PubMed]
    [Google Scholar]
  40. Heath B. D., Butcher R. D. J., Whitfield W. G. F., Hubbard S. F. 1999; Horizontal transfer of Wolbachia between phylogenetically distant insect species by a naturally occurring mechanism. Curr Biol 9:313–316 [View Article][PubMed]
    [Google Scholar]
  41. Hedges L. M., Brownlie J. C., O’Neill S. L., Johnson K. N. 2008; Wolbachia and virus protection in insects. Science 322:702 [View Article][PubMed]
    [Google Scholar]
  42. Hedges L. M., Yamada R., O'Neill S. L., Johnson K. N. 2012; The siRNA pathway is not essential for Wolbachia-mediated antiviral protection in Drosophila . Appl Environ Microbiol 78:6773–6776 [View Article][PubMed]
    [Google Scholar]
  43. Hertig M., Wolbach S. B. 1924; Studies on Rickettsia-like micro-organisms in insects. J Med Res 44:329–374, 7[PubMed]
    [Google Scholar]
  44. Hilgenboecker K., Hammerstein P., Schlattmann P., Telschow A., Werren J. H. 2008; How many species are infected with Wolbachia?–A statistical analysis of current data. FEMS Microbiol Lett 281:215–220 [View Article][PubMed]
    [Google Scholar]
  45. Hoffmann A. A., Turelli M. 2013; Facilitating Wolbachia introductions into mosquito populations through insecticide-resistance selection. Proc Biol Sci 280:20130371 [View Article][PubMed]
    [Google Scholar]
  46. Hoffmann A. A., Montgomery B. L., Popovici J., Iturbe-Ormaetxe I., Johnson P. H., Muzzi F., Greenfield M., Durkan M., Leong Y. S.other authors 2011; Successful establishment of Wolbachia in Aedes populations to suppress dengue transmission. Nature 476:454–457 [View Article][PubMed]
    [Google Scholar]
  47. Huang Z., Kingsolver M. B., Avadhanula V., Hardy R. W. 2013; An antiviral role for antimicrobial peptides during the arthropod response to alphavirus replication. J Virol 87:4272–4280 [View Article][PubMed]
    [Google Scholar]
  48. Hughes H., Britton N. F. 2013; Modelling the use of Wolbachia to control dengue fever transmission. Bull Math Biol 75:796–818 [View Article][PubMed]
    [Google Scholar]
  49. Huigens M. E., Luck R. F., Klaassen R. H. G., Maas M. F. P. M., Timmermans M. J. T. N., Stouthamer R. 2000; Infectious parthenogenesis. Nature 405:178–179 [View Article][PubMed]
    [Google Scholar]
  50. Huigens M. E., de Almeida R. P., Boons P. A. H., Luck R. F., Stouthamer R. 2004; Natural interspecific and intraspecific horizontal transfer of parthenogenesis-inducing Wolbachia in Trichogramma wasps. Proc Biol Sci 271:509–515 [View Article][PubMed]
    [Google Scholar]
  51. Hussain M., Frentiu F. D., Moreira L. A., O’Neill S. L., Asgari S. 2011; Wolbachia uses host microRNAs to manipulate host gene expression and facilitate colonization of the dengue vector Aedes aegypti . Proc Natl Acad Sci U S A 108:9250–9255 [View Article][PubMed]
    [Google Scholar]
  52. Hussain M., Lu G., Torres S., Edmonds J. H., Kay B. H., Khromykh A. A., Asgari S. 2013; Effect of Wolbachia on replication of West Nile virus in a mosquito cell line and adult mosquitoes. J Virol 87:851–858 [View Article][PubMed]
    [Google Scholar]
  53. Jones E. O., White A., Boots M. 2011; The evolution of host protection by vertically transmitted parasites. Proc Biol Sci 278:863–870 [View Article][PubMed]
    [Google Scholar]
  54. Kambhampati S., Rai K. S., Burgun S. J. 1993; Unidirectional cytoplasmic incompatibility in the mosquito, Aedes-Albopictus . Evolution 47:673–677 [View Article]
    [Google Scholar]
  55. Kambris Z., Blagborough A. M., Pinto S. B., Blagrove M. S., Godfray H. C., Sinden R. E., Sinkins S. P. 2010; Wolbachia stimulates immune gene expression and inhibits plasmodium development in Anopheles gambiae . PLoS Pathog 6:e1001143 [View Article][PubMed]
    [Google Scholar]
  56. Kielian M. 1995; Membrane fusion and the alphavirus life cycle. Adv Virus Res 45:113–151 [View Article][PubMed]
    [Google Scholar]
  57. Kittayapong P., Baisley K. J., Baimai V., O’Neill S. L. 2000; Distribution and diversity of Wolbachia infections in Southeast Asian mosquitoes (Diptera: Culicidae). J Med Entomol 37:340–345 [View Article][PubMed]
    [Google Scholar]
  58. Kraaijeveld K., Franco P., de Knijff P., Stouthamer R., van Alphen J. J. 2011; Clonal genetic variation in a Wolbachia-infected asexual wasp: horizontal transmission or historical sex?. Mol Ecol 20:3644–3652[PubMed]
    [Google Scholar]
  59. Krejbich-Trotot P., Gay B., Li-Pat-Yuen G., Hoarau J. J., Jaffar-Bandjee M. C., Briant L., Gasque P., Denizot M. 2011; Chikungunya triggers an autophagic process which promotes viral replication. Virol J 8:432 [View Article][PubMed]
    [Google Scholar]
  60. Kremer N., Voronin D., Charif D., Mavingui P., Mollereau B., Vavre F. 2009; Wolbachia interferes with ferritin expression and iron metabolism in insects. PLoS Pathog 5:e1000630 [View Article][PubMed]
    [Google Scholar]
  61. Lacroix R., McKemey A. R., Raduan N., Kwee Wee L., Hong Ming W., Guat Ney T., Rahidah A A S., Salman S., Subramaniam S.other authors 2012; Open field release of genetically engineered sterile male Aedes aegypti in Malaysia. PLoS ONE 7:e42771 [View Article][PubMed]
    [Google Scholar]
  62. Landmann F., Orsi G. A., Loppin B., Sullivan W. 2009; Wolbachia-mediated cytoplasmic incompatibility is associated with impaired histone deposition in the male pronucleus. PLoS Pathog 5:e1000343 [View Article][PubMed]
    [Google Scholar]
  63. Lange Y., Ye J., Rigney M., Steck T. L. 1999; Regulation of endoplasmic reticulum cholesterol by plasma membrane cholesterol. J Lipid Res 40:2264–2270[PubMed]
    [Google Scholar]
  64. Laven H. 1967; Eradication of Culex pipiens fatigans through cytoplasmic incompatibility. Nature 216:383–384 [View Article][PubMed]
    [Google Scholar]
  65. Le Clec’h W., Braquart-Varnier C., Raimond M., Ferdy J. B., Bouchon D., Sicard M. 2012; High virulence of Wolbachia after host switching: when autophagy hurts. PLoS Pathog 8:e1002844 [View Article][PubMed]
    [Google Scholar]
  66. Lee Y. R., Lei H. Y., Liu M. T., Wang J. R., Chen S. H., Jiang-Shieh Y. F., Lin Y. S., Yeh T. M., Liu C. C., Liu H. S. 2008; Autophagic machinery activated by dengue virus enhances virus replication. Virology 374:240–248 [View Article][PubMed]
    [Google Scholar]
  67. Lemaitre B., Hoffmann J. 2007; The host defense of Drosophila melanogaster . Annu Rev Immunol 25:697–743 [View Article][PubMed]
    [Google Scholar]
  68. Lin M., Rikihisa Y. 2003; Ehrlichia chaffeensis and Anaplasma phagocytophilum lack genes for lipid A biosynthesis and incorporate cholesterol for their survival. Infect Immun 71:5324–5331 [View Article][PubMed]
    [Google Scholar]
  69. Lipsitch M., Moxon E. R. 1997; Virulence and transmissibility of pathogens: what is the relationship?. Trends Microbiol 5:31–37 [View Article][PubMed]
    [Google Scholar]
  70. Lu Y. E., Cassese T., Kielian M. 1999; The cholesterol requirement for Sindbis virus entry and exit and characterization of a spike protein region involved in cholesterol dependence. J Virol 73:4272–4278[PubMed]
    [Google Scholar]
  71. Lu P., Bian G., Pan X., Xi Z. 2012; Wolbachia induces density-dependent inhibition to dengue virus in mosquito cells. PLoS Negl Trop Dis 6:e1754 [View Article][PubMed]
    [Google Scholar]
  72. Mackenzie J. M., Khromykh A. A., Parton R. G. 2007; Cholesterol manipulation by West Nile virus perturbs the cellular immune response. Cell Host Microbe 2:229–239 [View Article][PubMed]
    [Google Scholar]
  73. Marquardt M. T., Phalen T., Kielian M. 1993; Cholesterol is required in the exit pathway of Semliki Forest virus. J Cell Biol 123:57–65 [View Article][PubMed]
    [Google Scholar]
  74. McMeniman C. J., Lane A. M., Fong A. W., Voronin D. A., Iturbe-Ormaetxe I., Yamada R., McGraw E. A., O’Neill S. L. 2008; Host adaptation of a Wolbachia strain after long-term serial passage in mosquito cell lines. Appl Environ Microbiol 74:6963–6969 [View Article][PubMed]
    [Google Scholar]
  75. 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 . Science 323:141–144 [View Article][PubMed]
    [Google Scholar]
  76. Merkling S. H., van Rij R. P. 2013; Beyond RNAi: antiviral defense strategies in Drosophila and mosquito. J Insect Physiol 59:159–170 [View Article][PubMed]
    [Google Scholar]
  77. Miller W. J., Riegler M. 2006; Evolutionary dynamics of wAu-like Wolbachia variants in neotropical Drosophila spp. Appl Environ Microbiol 72:826–835 [View Article][PubMed]
    [Google Scholar]
  78. Min K. T., Benzer S. 1997; Wolbachia, normally a symbiont of Drosophila, can be virulent, causing degeneration and early death. Proc Natl Acad Sci U S A 94:10792–10796 [View Article][PubMed]
    [Google Scholar]
  79. Mitsuhashi J., Nakasone S., Horie Y. 1983; Sterol-free eukaryotic cells from continuous cell lines of insects. Cell Biol Int Rep 7:1057–1062 [View Article][PubMed]
    [Google Scholar]
  80. 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.other authors 2009; A Wolbachia symbiont in Aedes aegypti limits infection with dengue, chikungunya, and Plasmodium . Cell 139:1268–1278 [View Article][PubMed]
    [Google Scholar]
  81. Mosso C., Galván-Mendoza I. J., Ludert J. E., del Angel R. M. 2008; Endocytic pathway followed by dengue virus to infect the mosquito cell line C6/36 HT. Virology 378:193–199 [View Article][PubMed]
    [Google Scholar]
  82. Mousson L., Martin E., Zouache K., Madec Y., Mavingui P., Failloux A. B. 2010; Wolbachia modulates chikungunya replication in Aedes albopictus . Mol Ecol 19:1953–1964 [View Article][PubMed]
    [Google Scholar]
  83. Mousson L., Zouache K., Arias-Goeta C., Raquin V., Mavingui P., Failloux A. B. 2012; The native Wolbachia symbionts limit transmission of dengue virus in Aedes albopictus . PLoS Negl Trop Dis 6:e1989 [View Article][PubMed]
    [Google Scholar]
  84. 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 Pathog 5:e1000656 [View Article][PubMed]
    [Google Scholar]
  85. 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 Microbiol 78:6922–6929 [View Article][PubMed]
    [Google Scholar]
  86. Osei-Amo S., Hussain M., O’Neill S. L., Asgari S. 2012; Wolbachia-induced aae-miR-12 miRNA negatively regulates the expression of MCT1 and MCM6 genes in Wolbachia-infected mosquito cell line. PLoS ONE 7:e50049 [View Article][PubMed]
    [Google Scholar]
  87. Osei-Poku J., Han C., Mbogo C. M., Jiggins F. M. 2012; Identification of Wolbachia strains in mosquito disease vectors. PLoS ONE 7:e49922 [View Article][PubMed]
    [Google Scholar]
  88. Pan X., Zhou G., Wu J., Bian G., Lu P., Raikhel A. S., Xi Z. 2012; 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 U S A 109:E23–E31 [View Article][PubMed]
    [Google Scholar]
  89. Phalen T., Kielian M. 1991; Cholesterol is required for infection by Semliki Forest virus. J Cell Biol 112:615–623 [View Article][PubMed]
    [Google Scholar]
  90. Popovici J., Moreira L. A., Poinsignon A., Iturbe-Ormaetxe I., McNaughton D., O’Neill S. L. 2010; Assessing key safety concerns of a Wolbachia-based strategy to control dengue transmission by Aedes mosquitoes. Mem Inst Oswaldo Cruz 105:957–964 [View Article][PubMed]
    [Google Scholar]
  91. Rancès E., Ye Y. H., Woolfit M., McGraw E. A., O’Neill S. L. 2012; The relative importance of innate immune priming in Wolbachia-mediated dengue interference. PLoS Pathog 8:e1002548 [View Article][PubMed]
    [Google Scholar]
  92. Rancès E., Johnson T. K., Popovici J., Iturbe-Ormaetxe I., Zakir T., Warr C. G., O’Neill S. L. 2013; The toll and Imd pathways are not required for Wolbachia-mediated dengue virus interference. J Virol 87:11945–11949 [View Article][PubMed]
    [Google Scholar]
  93. Read A. F., Lynch P. A., Thomas M. B. 2009; How to make evolution-proof insecticides for malaria control. PLoS Biol 7:e1000058 [View Article][PubMed]
    [Google Scholar]
  94. Riegler M., Sidhu M., Miller W. J., O’Neill S. L. 2005; Evidence for a global Wolbachia replacement in Drosophila melanogaster . Curr Biol 15:1428–1433 [View Article][PubMed]
    [Google Scholar]
  95. Rodriguez-Andres J., Rani S., Varjak M., Chase-Topping M. E., Beck M. H., Ferguson M. C., Schnettler E., Fragkoudis R., Barry G.other authors 2012; Phenoloxidase activity acts as a mosquito innate immune response against infection with Semliki Forest virus. PLoS Pathog 8:e1002977 [View Article][PubMed]
    [Google Scholar]
  96. Rothwell C., Lebreton A., Young Ng C., Lim J. Y., Liu W., Vasudevan S., Labow M., Gu F., Gaither L. A. 2009; Cholesterol biosynthesis modulation regulates dengue viral replication. Virology 389:8–19 [View Article][PubMed]
    [Google Scholar]
  97. Rottschaefer S. M., Lazzaro B. P. 2012; No effect of Wolbachia on resistance to intracellular infection by pathogenic bacteria in Drosophila melanogaster . PLoS ONE 7:e40500 [View Article][PubMed]
    [Google Scholar]
  98. Russell J. A., Goldman-Huertas B., Moreau C. S., Baldo L., Stahlhut J. K., Werren J. H., Pierce N. E. 2009; Specialization and geographic isolation among Wolbachia symbionts from ants and lycaenid butterflies. Evolution 63:624–640 [View Article][PubMed]
    [Google Scholar]
  99. Schofield P. 2002; Spatially explicit models of Turelli-Hoffmann Wolbachia invasive wave fronts. J Theor Biol 215:121–131 [View Article][PubMed]
    [Google Scholar]
  100. Schraiber J. G., Kaczmarczyk A. N., Kwok R., Park M., Silverstein R., Rutaganira F. U., Aggarwal T., Schwemmer M. A., Hom C. L.other authors 2012; Constraints on the use of lifespan-shortening Wolbachia to control dengue fever. J Theor Biol 297:26–32 [View Article][PubMed]
    [Google Scholar]
  101. 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]
  102. Serbus L. R., Casper-Lindley C., Landmann F., Sullivan W. 2008; The genetics and cell biology of Wolbachia-host interactions. Annu Rev Genet 42:683–707 [View Article][PubMed]
    [Google Scholar]
  103. Serbus L. R., Landmann F., Bray W. M., White P. M., Ruybal J., Lokey R. S., Debec A., Sullivan W. 2012; A cell-based screen reveals that the albendazole metabolite, albendazole sulfone, targets Wolbachia . PLoS Pathog 8:e1002922 [View Article][PubMed]
    [Google Scholar]
  104. Shaw A. E., Veronesi E., Maurin G., Ftaich N., Guiguen F., Rixon F., Ratinier M., Mertens P., Carpenter S.other authors 2012; Drosophila melanogaster as a model organism for bluetongue virus replication and tropism. J Virol 86:9015–9024 [View Article][PubMed]
    [Google Scholar]
  105. Silberkang M., Havel C. M., Friend D. S., McCarthy B. J., Watson J. A. 1983; Isoprene synthesis in isolated embryonic Drosophila cells. I. Sterol-deficient eukaryotic cells. J Biol Chem 258:8503–8511[PubMed]
    [Google Scholar]
  106. Sinkins S. P. 2004; Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 34:723–729 [View Article][PubMed]
    [Google Scholar]
  107. Sinkins S. P., Braig H. R., O’Neill S. L. 1995; Wolbachia superinfections and the expression of cytoplasmic incompatibility. Proc Biol Sci 261:325–330 [View Article][PubMed]
    [Google Scholar]
  108. Smartt C. T., Richards S. L., Anderson S. L., Erickson J. S. 2009; West Nile virus infection alters midgut gene expression in Culex pipiens quinquefasciatus Say (Diptera: Culicidae). Am J Trop Med Hyg 81:258–263[PubMed]
    [Google Scholar]
  109. Smit J. M., Bittman R., Wilschut J. 1999; Low-pH-dependent fusion of Sindbis virus with receptor-free cholesterol- and sphingolipid-containing liposomes. J Virol 73:8476–8484[PubMed]
    [Google Scholar]
  110. Sousa I. P. Jr, Carvalho C. A., Ferreira D. F., Weissmüller G., Rocha G. M., Silva J. L., Gomes A. M. 2011; Envelope lipid-packing as a critical factor for the biological activity and stability of alphavirus particles isolated from mammalian and mosquito cells. J Biol Chem 286:1730–1736 [View Article][PubMed]
    [Google Scholar]
  111. Souza-Neto J. A., Sim S., Dimopoulos G. 2009; An evolutionary conserved function of the JAK-STAT pathway in anti-dengue defense. Proc Natl Acad Sci U S A 106:17841–17846 [View Article][PubMed]
    [Google Scholar]
  112. Stouthamer R., Breeuwer J. A. J., Hurst G. D. D. 1999; Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53:71–102 [View Article][PubMed]
    [Google Scholar]
  113. Tchankouo-Nguetcheu S., Khun H., Pincet L., Roux P., Bahut M., Huerre M., Guette C., Choumet V. 2010; Differential protein modulation in midguts of Aedes aegypti infected with chikungunya and dengue 2 viruses. PLoS ONE 5:e13149 [View Article][PubMed]
    [Google Scholar]
  114. Teixeira L., Ferreira A., Ashburner M. 2008; The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster . PLoS Biol 6:e2 [View Article][PubMed]
    [Google Scholar]
  115. Thomas P., Kenny N., Eyles D., Moreira L. A., O’Neill S. L., Asgari S. 2011; Infection with the wMel and wMelPop strains of Wolbachia leads to higher levels of melanization in the hemolymph of Drosophila melanogaster, Drosophila simulans and Aedes aegypti . Dev Comp Immunol 35:360–365 [View Article][PubMed]
    [Google Scholar]
  116. Tram U., Sullivan W. 2002; Role of delayed nuclear envelope breakdown and mitosis in Wolbachia-induced cytoplasmic incompatibility. Science 296:1124–1126 [View Article][PubMed]
    [Google Scholar]
  117. Tram U., Fredrick K., Werren J. H., Sullivan W. 2006; Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype. J Cell Sci 119:3655–3663 [View Article][PubMed]
    [Google Scholar]
  118. Tsai K. H., Huang C. G., Wu W. J., Chuang C. K., Lin C. C., Chen W. J. 2006; Parallel infection of Japanese encephalitis virus and Wolbachia within cells of mosquito salivary glands. J Med Entomol 43:752–756 [View Article][PubMed]
    [Google Scholar]
  119. Tsetsarkin K. A., McGee C. E., Higgs S. 2011; Chikungunya virus adaptation to Aedes albopictus mosquitoes does not correlate with acquisition of cholesterol dependence or decreased pH threshold for fusion reaction. Virol J 8:376 [View Article][PubMed]
    [Google Scholar]
  120. Turelli M. 2010; Cytoplasmic incompatibility in populations with overlapping generations. Evolution 64:232–241 [View Article][PubMed]
    [Google Scholar]
  121. Turelli M., Hoffmann A. A. 1991; Rapid spread of an inherited incompatibility factor in California Drosophila . Nature 353:440–442 [View Article][PubMed]
    [Google Scholar]
  122. Turelli M., Hoffmann A. A. 1995; Cytoplasmic incompatibility in Drosophila simulans: dynamics and parameter estimates from natural populations. Genetics 140:1319–1338[PubMed]
    [Google Scholar]
  123. Umashankar M., Sánchez-San Martín C., Liao M., Reilly B., Guo A., Taylor G., Kielian M. 2008; Differential cholesterol binding by class II fusion proteins determines membrane fusion properties. J Virol 82:9245–9253 [View Article][PubMed]
    [Google Scholar]
  124. van den Hurk A. F., Hall-Mendelin S., Pyke A. T., Frentiu F. D., McElroy K., Day A., Higgs S., O’Neill S. L. 2012; Impact of Wolbachia on infection with chikungunya and yellow fever viruses in the mosquito vector Aedes aegypti . PLoS Negl Trop Dis 6:e1892 [View Article][PubMed]
    [Google Scholar]
  125. Vavre F., Charlat S. 2012; Making (good) use of Wolbachia: what the models say. Curr Opin Microbiol 15:263–268 [View Article][PubMed]
    [Google Scholar]
  126. Vavre F., Fleury F., Lepetit D., Fouillet P., Boulétreau M. 1999; Phylogenetic evidence for horizontal transmission of Wolbachia in host-parasitoid associations. Mol Biol Evol 16:1711–1723 [View Article][PubMed]
    [Google Scholar]
  127. Voronin D., Cook D. A., Steven A., Taylor M. J. 2012; Autophagy regulates Wolbachia populations across diverse symbiotic associations. Proc Natl Acad Sci U S A 109:E1638–E1646 [View Article][PubMed]
    [Google Scholar]
  128. Waldock J., Olson K. E., Christophides G. K. 2012; Anopheles gambiae antiviral immune response to systemic o’nyong-nyong infection. PLoS Negl Trop Dis 6:e1565 [View Article][PubMed]
    [Google Scholar]
  129. Walker T., Johnson P. H., Moreira L. A., Iturbe-Ormaetxe I., Frentiu F. D., McMeniman C. J., Leong Y. S., Dong Y., Axford J.other authors 2011; The wMel Wolbachia strain blocks dengue and invades caged Aedes aegypti populations. Nature 476:450–453 [View Article][PubMed]
    [Google Scholar]
  130. Waterhouse R. M., Kriventseva E. V., Meister S., Xi Z., Alvarez K. S., Bartholomay L. C., Barillas-Mury C., Bian G., Blandin S.other authors 2007; Evolutionary dynamics of immune-related genes and pathways in disease-vector mosquitoes. Science 316:1738–1743 [View Article][PubMed]
    [Google Scholar]
  131. Weaver S. C., Reisen W. K. 2010; Present and future arboviral threats. Antiviral Res 85:328–345 [View Article][PubMed]
    [Google Scholar]
  132. Welsch S., Miller S., Romero-Brey I., Merz A., Bleck C. K., Walther P., Fuller S. D., Antony C., Krijnse-Locker J., Bartenschlager R. 2009; Composition and three-dimensional architecture of the dengue virus replication and assembly sites. Cell Host Microbe 5:365–375 [View Article][PubMed]
    [Google Scholar]
  133. Werren J. H., Zhang W., Guo L. R. 1995; Evolution and phylogeny of Wolbachia: reproductive parasites of arthropods. Proc Biol Sci 261:55–63 [View Article][PubMed]
    [Google Scholar]
  134. Werren J. H., Baldo L., Clark M. E. 2008; Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751 [View Article][PubMed]
    [Google Scholar]
  135. Wilke A. B., Marrelli M. T. 2012; Genetic control of mosquitoes: population suppression strategies. Rev Inst Med Trop Sao Paulo 54:287–292 [View Article][PubMed]
    [Google Scholar]
  136. Wong Z. S., Hedges L. M., Brownlie J. C., Johnson K. N. 2011; Wolbachia-mediated antibacterial protection and immune gene regulation in Drosophila. PLoS ONE 6:e25430 [View Article][PubMed]
    [Google Scholar]
  137. Xi Z., Khoo C. C., Dobson S. L. 2005; Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326–328 [View Article][PubMed]
    [Google Scholar]
  138. Xi Z., Ramirez J. L., Dimopoulos G. 2008; The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4:e1000098 [View Article][PubMed]
    [Google Scholar]
  139. Ye Y. H., Woolfit M., Huttley G. A., Rances E., Caragata E. P., Popovici J., O'Neill S. L., McGraw E. A. 2013; Infection with a virulent strain of Wolbachia disrupts genome wide-patterns of cytosine methylation in the mosquito Aedes aegypti . PLoS ONE 8:e66482 [View Article][PubMed]
    [Google Scholar]
  140. Yeap H. L., Mee P., Walker T., Weeks A. R., O’Neill S. L., Johnson P., Ritchie S. A., Richardson K. M., Doig C.other authors 2011; Dynamics of the “popcorn” Wolbachia infection in outbred Aedes aegypti informs prospects for mosquito vector control. Genetics 187:583–595 [View Article][PubMed]
    [Google Scholar]
  141. Yen J. H., Barr A. R. 1971; New hypothesis of the cause of cytoplasmic incompatibility in Culex pipiens L. Nature 232:657–658 [View Article][PubMed]
    [Google Scholar]
  142. Yen J. H., Barr A. R. 1973; The etiological agent of cytoplasmic incompatibility in Culex pipiens . J Invertebr Pathol 22:242–250 [View Article][PubMed]
    [Google Scholar]
  143. Zambon R. A., Nandakumar M., Vakharia V. N., Wu L. P. 2005; The Toll pathway is important for an antiviral response in Drosophila . Proc Natl Acad Sci U S A 102:7257–7262 [View Article][PubMed]
    [Google Scholar]
  144. Zhang G., Hussain M., O’Neill S. L., Asgari S. 2013; Wolbachia uses a host microRNA to regulate transcripts of a methyltransferase, contributing to dengue virus inhibition in Aedes aegypti . Proc Natl Acad Sci U S A 110:10276–10281 [View Article][PubMed]
    [Google Scholar]
  145. Zug R., Hammerstein P. 2012; Still a host of hosts for Wolbachia: analysis of recent data suggests that 40 % of terrestrial arthropod species are infected. PLoS ONE 7:e38544 [View Article][PubMed]
    [Google Scholar]
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