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Abstract

Arthropod-borne viruses – arboviruses – are a significant threat to public health. Whilst there is considerable knowledge about arbovirus interactions with vertebrate immunity, relatively little is known about how vectors such as mosquitoes control arbovirus infections. In this review, we discuss novel findings in the field of mosquito antiviral responses to arboviruses, in particular RNA interference, the up-and-coming field of general immune-signalling pathways, and cell death/apoptosis.

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2009-09-01
2024-04-19
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References

  1. Aguilar, P. V., Weaver, S. C. & Basler, C. F.(2007). Capsid protein of eastern equine encephalitis virus inhibits host cell gene expression. J Virol 81, 3866–3876.[CrossRef] [Google Scholar]
  2. Aliyari, R., Wu, Q., Li, H. W., Wang, X. H., Li, F., Green, L. D., Han, C. S., Li, W. X. & Ding, S. W.(2008). Mechanism of induction and suppression of antiviral immunity directed by virus-derived small RNAs in Drosophila. Cell Host Microbe 4, 387–397.[CrossRef] [Google Scholar]
  3. Alphey, L.(2009). Natural and engineered mosquito immunity. J Biol 8, 40[CrossRef] [Google Scholar]
  4. Angelini, R., Finarelli, A. C., Angelini, P., Po, C., Petropulacos, K., Macini, P., Fiorentini, C., Fortuna, C., Venturi, G. & other authors(2007). An outbreak of chikungunya fever in the province of Ravenna, Italy. Euro Surveill 12, E070906 [Google Scholar]
  5. Atasheva, S., Garmashova, N., Frolov, I. & Frolova, E.(2008). Venezuelan equine encephalitis virus capsid protein inhibits nuclear import in mammalian but not in mosquito cells. J Virol 82, 4028–4041.[CrossRef] [Google Scholar]
  6. Attarzadeh-Yazdi, G., Fragkoudis, R., Chi, Y., Siu, R. W., Ulper, L., Barry, G., Rodriguez-Andres, J., Nash, A. A., Bouloy, M. & other authors(2009). Cell-to-cell spread of the RNA interference response suppresses Semliki Forest virus (SFV) infection of mosquito cell cultures and cannot be antagonized by SFV. J Virol 83, 5735–5748.[CrossRef] [Google Scholar]
  7. Barillas-Mury, C. & Kumar, S.(2005). Plasmodium–mosquito interactions: a tale of dangerous liaisons. Cell Microbiol 7, 1539–1545.[CrossRef] [Google Scholar]
  8. Barillas-Mury, C., Han, Y. S., Seeley, D. & Kafatos, F. C.(1999).Anopheles gambiae Ag-STAT, a new insect member of the STAT family, is activated in response to bacterial infection. EMBO J 18, 959–967.[CrossRef] [Google Scholar]
  9. Best, S. M.(2008). Viral subversion of apoptotic enzymes: escape from death row. Annu Rev Microbiol 62, 171–192.[CrossRef] [Google Scholar]
  10. Bian, G., Shin, S. W., Cheon, H. M., Kokoza, V. & Raikhel, A. S.(2005). Transgenic alteration of Toll immune pathway in the female mosquito Aedes aegypti. Proc Natl Acad Sci U S A 102, 13568–13573.[CrossRef] [Google Scholar]
  11. Blair, C. D., Adelman, Z. N. & Olson, K. E.(2000). Molecular strategies for interrupting arthropod-borne virus transmission by mosquitoes. Clin Microbiol Rev 13, 651–661.[CrossRef] [Google Scholar]
  12. Blakqori, G., Delhaye, S., Habjan, M., Blair, C. D., Sanchez-Vargas, I., Olson, K. E., Attarzadeh-Yazdi, G., Fragkoudis, R., Kohl, A. & other authors(2007). La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81, 4991–4999.[CrossRef] [Google Scholar]
  13. Blitvich, B. J., Blair, C. D., Kempf, B. J., Hughes, M. T., Black, W. C., Mackie, R. S., Meredith, C. T., Beaty, B. J. & Rayms-Keller, A.(2002). Developmental- and tissue-specific expression of an inhibitor of apoptosis protein 1 homologue from Aedes triseriatus mosquitoes. Insect Mol Biol 11, 431–442.[CrossRef] [Google Scholar]
  14. Borucki, M. K., Kempf, B. J., Blitvich, B. J., Blair, C. D. & Beaty, B. J.(2002). La Crosse virus: replication in vertebrate and invertebrate hosts. Microbes Infect 4, 341–350.[CrossRef] [Google Scholar]
  15. Bowers, D. F., Coleman, C. G. & Brown, D. T.(2003). Sindbis virus-associated pathology in Aedes albopictus (Diptera: Culicidae). J Med Entomol 40, 698–705.[CrossRef] [Google Scholar]
  16. Bowie, A. G. & Unterholzner, L.(2008). Viral evasion and subversion of pattern-recognition receptor signalling. Nat Rev Immunol 8, 911–922.[CrossRef] [Google Scholar]
  17. Breakwell, L., Dosenovic, P., Karlsson Hedestam, G. B., D'Amato, M., Liljestrom, P., Fazakerley, J. & McInerney, G. M.(2007). Semliki Forest virus nonstructural protein 2 is involved in suppression of the type I interferon response. J Virol 81, 8677–8684.[CrossRef] [Google Scholar]
  18. 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[CrossRef] [Google Scholar]
  19. 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[CrossRef] [Google Scholar]
  20. Caudy, A. A., Myers, M., Hannon, G. J. & Hammond, S. M.(2002). Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev 16, 2491–2496.[CrossRef] [Google Scholar]
  21. Caudy, A. A., Ketting, R. F., Hammond, S. M., Denli, A. M., Bathoorn, A. M., Tops, B. B., Silva, J. M., Myers, M. M., Hannon, G. J. & Plasterk, R. H.(2003). A micrococcal nuclease homologue in RNAi effector complexes. Nature 425, 411–414.[CrossRef] [Google Scholar]
  22. 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.[CrossRef] [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.[CrossRef] [Google Scholar]
  24. Christophides, G. K., Vlachou, D. & Kafatos, F. C.(2004). Comparative and functional genomics of the innate immune system in the malaria vector Anopheles gambiae. Immunol Rev 198, 127–148.[CrossRef] [Google Scholar]
  25. Cirimotich, C. M., Scott, J. C., Phillips, A. T., Geiss, B. J. & Olson, K. E.(2009). Suppression of RNA interference increases alphavirus replication and virus-associated mortality in Aedes aegypti mosquitoes. BMC Microbiol 9, 49[CrossRef] [Google Scholar]
  26. Condreay, L. D. & Brown, D. T.(1988). Suppression of RNA synthesis by a specific antiviral activity in Sindbis virus-infected Aedes albopictus cells. J Virol 62, 346–348. [Google Scholar]
  27. Deddouche, S., Matt, N., Budd, A., Mueller, S., Kemp, C., Galiana-Arnoux, D., Dostert, C., Antoniewski, C., Hoffmann, J. A. & Imler, J. L.(2008). The DExD/H-box helicase Dicer-2 mediates the induction of antiviral activity in Drosophila. Nat Immunol 9, 1425–1432.[CrossRef] [Google Scholar]
  28. Ding, S. W. & Voinnet, O.(2007). Antiviral immunity directed by small RNAs. Cell 130, 413–426.[CrossRef] [Google Scholar]
  29. Dixon, L. K., Rock, D. L. & Vinuela, E.(1995). African swine fever-like viruses. Arch Virol 10 (Suppl.), 92–94. [Google Scholar]
  30. 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.[CrossRef] [Google Scholar]
  31. Ferrandon, D., Imler, J. L., Hetru, C. & Hoffmann, J. A.(2007). The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat Rev Immunol 7, 862–874.[CrossRef] [Google Scholar]
  32. Flynt, A., Liu, N., Martin, R. & Lai, E. C.(2009). Dicing of viral replication intermediates during silencing of latent Drosophila viruses. Proc Natl Acad Sci U S A 106, 5270–5275.[CrossRef] [Google Scholar]
  33. Fragkoudis, R., Chi, Y., Siu, R. W., 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.[CrossRef] [Google Scholar]
  34. Franz, A. W., Sanchez-Vargas, I., Adelman, Z. N., Blair, C. D., Beaty, B. J., James, A. A. & Olson, K. E.(2006). Engineering RNA interference-based resistance to dengue virus type 2 in genetically modified Aedes aegypti. Proc Natl Acad Sci U S A 103, 4198–4203.[CrossRef] [Google Scholar]
  35. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J. A. & Imler, J. L.(2006). Essential function in vivo for Dicer-2 in host defense against RNA viruses in Drosophila. Nat Immunol 7, 590–597.[CrossRef] [Google Scholar]
  36. Garcia, S., Billecocq, A., Crance, J. M., Munderloh, U., Garin, D. & Bouloy, M.(2005). Nairovirus RNA sequences expressed by a Semliki Forest virus replicon induce RNA interference in tick cells. J Virol 79, 8942–8947.[CrossRef] [Google Scholar]
  37. Garcia, S., Billecocq, A., Crance, J. M., Prins, M., Garin, D. & Bouloy, M.(2006). Viral suppressors of RNA interference impair RNA silencing induced by a Semliki Forest virus replicon in tick cells. J Gen Virol 87, 1985–1989.[CrossRef] [Google Scholar]
  38. Garmashova, N., Gorchakov, R., Frolova, E. & Frolov, I.(2006). Sindbis virus nonstructural protein nsP2 is cytotoxic and inhibits cellular transcription. J Virol 80, 5686–5696.[CrossRef] [Google Scholar]
  39. Garmashova, N., Atasheva, S., Kang, W., Weaver, S. C., Frolova, E. & Frolov, I.(2007a). Analysis of Venezuelan equine encephalitis virus capsid protein function in the inhibition of cellular transcription. J Virol 81, 13552–13565.[CrossRef] [Google Scholar]
  40. Garmashova, N., Gorchakov, R., Volkova, E., Paessler, S., Frolova, E. & Frolov, I.(2007b). The Old World and New World alphaviruses use different virus-specific proteins for induction of transcriptional shutoff. J Virol 81, 2472–2484.[CrossRef] [Google Scholar]
  41. Geiss, B. J., Pierson, T. C. & Diamond, M. S.(2005). Actively replicating West Nile virus is resistant to cytoplasmic delivery of siRNA. Virol J 2, 53[CrossRef] [Google Scholar]
  42. Gillies, S. & Stollar, V.(1982a). Conditions necessary for inhibition of protein synthesis and production of cytopathic effect in Aedes albopictus cells infected with vesicular stomatitis virus. Mol Cell Biol 2, 66–75. [Google Scholar]
  43. Gillies, S. & Stollar, V.(1982b). Protein synthesis in lysates of Aedes albopictus cells infected with vesicular stomatitis virus. Mol Cell Biol 2, 1174–1186. [Google Scholar]
  44. Girard, Y. A., Popov, V., Wen, J., Han, V. & Higgs, S.(2005). Ultrastructural study of West Nile virus pathogenesis in Culex pipiens quinquefasciatus (Diptera: Culicidae). J Med Entomol 42, 429–444.[CrossRef] [Google Scholar]
  45. Girard, Y. A., Schneider, B. S., McGee, C. E., Wen, J., Han, V. C., Popov, V., Mason, P. W. & Higgs, S.(2007). Salivary gland morphology and virus transmission during long-term cytopathologic West Nile virus infection in Culex mosquitoes. Am J Trop Med Hyg 76, 118–128. [Google Scholar]
  46. Gordon, K. H. & Waterhouse, P. M.(2006). Small RNA viruses of insects: expression in plants and RNA silencing. Adv Virus Res 68, 459–502. [Google Scholar]
  47. Gordon, K. H. & Waterhouse, P. M.(2007). RNAi for insect-proof plants. Nat Biotechnol 25, 1231–1232.[CrossRef] [Google Scholar]
  48. Gould, E. A., Higgs, S., Buckley, A. & Gritsun, T. S.(2006). Potential arbovirus emergence and implications for the United Kingdom. Emerg Infect Dis 12, 549–555.[CrossRef] [Google Scholar]
  49. Halstead, S. B.(2008). Dengue virus–mosquito interactions. Annu Rev Entomol 53, 273–291.[CrossRef] [Google Scholar]
  50. Hedges, L. M. & Johnson, K. N.(2008). Induction of host defence responses by Drosophila C virus. J Gen Virol 89, 1497–1501.[CrossRef] [Google Scholar]
  51. Hedges, L. M., Brownlie, J. C., O'Neill, S. L. & Johnson, K. N.(2008).Wolbachia and virus protection in insects. Science 322, 702[CrossRef] [Google Scholar]
  52. Hirai, M., Terenius, O., Li, W. & Faye, I.(2004). Baculovirus and dsRNA induce hemolin, but no antibacterial activity, in Antheraea pernyi. Insect Mol Biol 13, 399–405.[CrossRef] [Google Scholar]
  53. Ho, T., Pallett, D., Rusholme, R., Dalmay, T. & Wang, H.(2006). A simplified method for cloning of short interfering RNAs from Brassica juncea infected with Turnip mosaic potyvirus and Turnip crinkle carmovirus. J Virol Methods 136, 217–223.[CrossRef] [Google Scholar]
  54. Holt, R. A., Subramanian, G. M., Halpern, A., Sutton, G. G., Charlab, R., Nusskern, D. R., Wincker, P., Clark, A. G., Ribeiro, J. M. & other authors(2002). The genome sequence of the malaria mosquito Anopheles gambiae. Science 298, 129–149.[CrossRef] [Google Scholar]
  55. Itaya, A., Zhong, X., Bundschuh, R., Qi, Y., Wang, Y., Takeda, R., Harris, A. R., Molina, C., Nelson, R. S. & Ding, B.(2007). A structured viroid RNA serves as a substrate for dicer-like cleavage to produce biologically active small RNAs but is resistant to RNA-induced silencing complex-mediated degradation. J Virol 81, 2980–2994.[CrossRef] [Google Scholar]
  56. Kang, S., Sim, C., Byrd, B. D., Collins, F. H. & Hong, Y. S.(2008).Ex vivo promoter analysis of antiviral heat shock cognate 70B gene in Anopheles gambiae. Virol J 5, 136[CrossRef] [Google Scholar]
  57. Karpf, A. R., Blake, J. M. & Brown, D. T.(1997). Characterization of the infection of Aedes albopictus cell clones by Sindbis virus. Virus Res 50, 1–13.[CrossRef] [Google Scholar]
  58. 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.[CrossRef] [Google Scholar]
  59. Kemp, C. & Imler, J. L.(2009). Antiviral immunity in Drosophila. Curr Opin Immunol 21, 3–9.[CrossRef] [Google Scholar]
  60. Kuno, G. & Chang, G. J.(2005). Biological transmission of arboviruses: reexamination of and new insights into components, mechanisms, and unique traits as well as their evolutionary trends. Clin Microbiol Rev 18, 608–637.[CrossRef] [Google Scholar]
  61. Kyle, J. L. & Harris, E.(2008). Global spread and persistence of dengue. Annu Rev Microbiol 62, 71–92.[CrossRef] [Google Scholar]
  62. Lambrechts, L. & Scott, T. W.(2009). Mode of transmission and the evolution of arbovirus virulence in mosquito vectors. Proc Biol Sci 276, 1369–1378.[CrossRef] [Google Scholar]
  63. Landeg, F.(2007). Bluetongue outbreak in the UK. Vet Rec 161, 534–535.[CrossRef] [Google Scholar]
  64. Lemaitre, B. & Hoffmann, J.(2007). The host defense of Drosophila melanogaster. Annu Rev Immunol 25, 697–743.[CrossRef] [Google Scholar]
  65. Li, H. W. & Ding, S. W.(2005). Antiviral silencing in animals. FEBS Lett 579, 5965–5973.[CrossRef] [Google Scholar]
  66. Li, F. & Ding, S. W.(2006). Virus counterdefense: diverse strategies for evading the RNA-silencing immunity. Annu Rev Microbiol 60, 503–531.[CrossRef] [Google Scholar]
  67. Li, W. X., Li, H., Lu, R., Li, F., Dus, M., Atkinson, P., Brydon, E. W., Johnson, K. L., Garcia-Sastre, A. & other authors(2004). Interferon antagonist proteins of influenza and vaccinia viruses are suppressors of RNA silencing. Proc Natl Acad Sci U S A 101, 1350–1355.[CrossRef] [Google Scholar]
  68. Lin, C. C., Chou, C. M., Hsu, Y. L., Lien, J. C., Wang, Y. M., Chen, S. T., Tsai, S. C., Hsiao, P. W. & Huang, C. J.(2004). Characterization of two mosquito STATs, AaSTAT and CtSTAT. Differential regulation of tyrosine phosphorylation and DNA binding activity by lipopolysaccharide treatment and by Japanese encephalitis virus infection. J Biol Chem 279, 3308–3317. [Google Scholar]
  69. Lin, R. J., Chang, B. L., Yu, H. P., Liao, C. L. & Lin, Y. L.(2006). Blocking of interferon-induced Jak-Stat signaling by Japanese encephalitis virus NS5 through a protein tyrosine phosphatase-mediated mechanism. J Virol 80, 5908–5918.[CrossRef] [Google Scholar]
  70. 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.[CrossRef] [Google Scholar]
  71. Medeiros, R. B., Resende Rde, O. & de Avila, A. C.(2004). The plant virus Tomato spotted wilt tospovirus activates the immune system of its main insect vector, Frankliniella occidentalis. J Virol 78, 4976–4982.[CrossRef] [Google Scholar]
  72. Meister, S., Kanzok, S. M., Zheng, X. L., Luna, C., Li, T. R., Hoa, N. T., Clayton, J. R., White, K. P., Kafatos, F. C. & other authors(2005). Immune signaling pathways regulating bacterial and malaria parasite infection of the mosquito Anopheles gambiae. Proc Natl Acad Sci U S A 102, 11420–11425.[CrossRef] [Google Scholar]
  73. Mims, C. A., Day, M. F. & Marshall, I. D.(1966). Cytopathic effect of Semliki Forest virus in the mosquito Aedes aegypti. Am J Trop Med Hyg 15, 775–784. [Google Scholar]
  74. Molnar, A., Csorba, T., Lakatos, L., Varallyay, E., Lacomme, C. & Burgyan, J.(2005). Plant virus-derived small interfering RNAs originate predominantly from highly structured single-stranded viral RNAs. J Virol 79, 7812–7818.[CrossRef] [Google Scholar]
  75. Myles, K. M., Wiley, M. R., Morazzani, E. M. & Adelman, Z. N.(2008). Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc Natl Acad Sci U S A 105, 19938–19943.[CrossRef] [Google Scholar]
  76. Myles, K. M., Morazzani, E. M. & Adelman, Z. N.(2009). Origins of alphavirus-derived small RNAs in mosquitoes. RNA Biol (in press). http://www.landesbioscience.com/journals/rnabiology/article/MylesRNA6-4.pdf [Google Scholar]
  77. Nene, V., Wortman, J. R., Lawson, D., Haas, B., Kodira, C., Tu, Z. J., Loftus, B., Xi, Z., Megy, K. & other authors(2007). Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316, 1718–1723.[CrossRef] [Google Scholar]
  78. Newton, S. E. & Dalgarno, L.(1983). Antiviral activity released from Aedes albopictus cells persistently infected with Semliki Forest virus. J Virol 47, 652–655. [Google Scholar]
  79. Obbard, D. J., Jiggins, F. M., Halligan, D. L. & Little, T. J.(2006). Natural selection drives extremely rapid evolution in antiviral RNAi genes. Curr Biol 16, 580–585.[CrossRef] [Google Scholar]
  80. Olson, K. E., Adelman, Z. N., Travanty, E. A., Sanchez-Vargas, I., Beaty, B. J. & Blair, C. D.(2002). Developing arbovirus resistance in mosquitoes. Insect Biochem Mol Biol 32, 1333–1343.[CrossRef] [Google Scholar]
  81. Osta, M. A., Christophides, G. K., Vlachou, D. & Kafatos, F. C.(2004). Innate immunity in the malaria vector Anopheles gambiae: comparative and functional genomics. J Exp Biol 207, 2551–2563.[CrossRef] [Google Scholar]
  82. Parikh, G. R., Oliver, J. D. & Bartholomay, L. C.(2009). A haemocyte tropism for an arbovirus. J Gen Virol 90, 292–296.[CrossRef] [Google Scholar]
  83. Powers, A. M. & Logue, C. H.(2007). Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. J Gen Virol 88, 2363–2377.[CrossRef] [Google Scholar]
  84. Randall, R. E. & Goodbourn, S.(2008). Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J Gen Virol 89, 1–47.[CrossRef] [Google Scholar]
  85. Robalino, J., Browdy, C. L., Prior, S., Metz, A., Parnell, P., Gross, P. & Warr, G.(2004). Induction of antiviral immunity by double-stranded RNA in a marine invertebrate. J Virol 78, 10442–10448.[CrossRef] [Google Scholar]
  86. Robalino, J., Bartlett, T., Shepard, E., Prior, S., Jaramillo, G., Scura, E., Chapman, R. W., Gross, P. S., Browdy, C. L. & Warr, G. W.(2005). Double-stranded RNA induces sequence-specific antiviral silencing in addition to nonspecific immunity in a marine shrimp: convergence of RNA interference and innate immunity in the invertebrate antiviral response? J Virol 79, 13561–13571.[CrossRef] [Google Scholar]
  87. Robalino, J., Bartlett, T. C., Chapman, R. W., Gross, P. S., Browdy, C. L. & Warr, G. W.(2007). Double-stranded RNA and antiviral immunity in marine shrimp: inducible host mechanisms and evidence for the evolution of viral counter-responses. Dev Comp Immunol 31, 539–547.[CrossRef] [Google Scholar]
  88. Sabatier, L., Jouanguy, E., Dostert, C., Zachary, D., Dimarcq, J. L., Bulet, P. & Imler, J. L.(2003). Pherokine-2 and -3. Eur J Biochem 270, 3398–3407.[CrossRef] [Google Scholar]
  89. Saleh, M. C., Tassetto, M., van Rij, R. P., Goic, B., Gausson, V., Berry, B., Jacquier, C., Antoniewski, C. & Andino, R.(2009). Antiviral immunity in Drosophila requires systemic RNA interference spread. Nature 458, 346–350.[CrossRef] [Google Scholar]
  90. Sanchez-Vargas, I., Travanty, E. A., Keene, K. M., Franz, A. W., Beaty, B. J., Blair, C. D. & Olson, K. E.(2004). RNA interference, arthropod-borne viruses, and mosquitoes. Virus Res 102, 65–74.[CrossRef] [Google Scholar]
  91. Sanchez-Vargas, I., Scott, J. C., Poole-Smith, B. K., Franz, A. W. E., 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[CrossRef] [Google Scholar]
  92. Sanders, H. R., Foy, B. D., Evans, A. M., Ross, L. S., Beaty, B. J., Olson, K. E. & Gill, S. S.(2005). Sindbis virus induces transport processes and alters expression of innate immunity pathway genes in the midgut of the disease vector, Aedes aegypti. Insect Biochem Mol Biol 35, 1293–1307.[CrossRef] [Google Scholar]
  93. Sarver, N. & Stollar, V.(1977). Sindbis virus-induced cytopathic effect in clones of Aedes albopictus (Singh) cells. Virology 80, 390–400.[CrossRef] [Google Scholar]
  94. Scholthof, H. B.(2006). The Tombusvirus-encoded P19: from irrelevance to elegance. Nat Rev Microbiol 4, 405–411.[CrossRef] [Google Scholar]
  95. Shelly, S., Lukinova, N., Bambina, S., Berman, A. & Cherry, S.(2009). Autophagy is an essential component of Drosophila immunity against vesicular stomatitis virus. Immunity 30, 588–598.[CrossRef] [Google Scholar]
  96. Shin, S. W., Kokoza, V., Ahmed, A. & Raikhel, A. S.(2002). Characterization of three alternatively spliced isoforms of the Rel/NF-kappa B transcription factor Relish from the mosquito Aedes aegypti. Proc Natl Acad Sci U S A 99, 9978–9983.[CrossRef] [Google Scholar]
  97. Shin, S. W., Kokoza, V., Lobkov, I. & Raikhel, A. S.(2003). Relish-mediated immune deficiency in the transgenic mosquito Aedes aegypti. Proc Natl Acad Sci U S A 100, 2616–2621.[CrossRef] [Google Scholar]
  98. Shin, S. W., Kokoza, V., Bian, G., Cheon, H. M., Kim, Y. J. & Raikhel, A. S.(2005). REL1, a homologue of Drosophila dorsal, regulates toll antifungal immune pathway in the female mosquito Aedes aegypti. J Biol Chem 280, 16499–16507.[CrossRef] [Google Scholar]
  99. Sim, C., Hong, Y. S., Vanlandingham, D. L., Harker, B. W., Christophides, G. K., Kafatos, F. C., Higgs, S. & Collins, F. H.(2005). Modulation of Anopheles gambiae gene expression in response to o'nyong-nyong virus infection. Insect Mol Biol 14, 475–481.[CrossRef] [Google Scholar]
  100. Sim, C., Hong, Y. S., Tsetsarkin, K. A., Vanlandingham, D. L., Higgs, S. & Collins, F. H.(2007).Anopheles gambiae heat shock protein cognate 70B impedes o'nyong-nyong virus replication. BMC Genomics 8, 231[CrossRef] [Google Scholar]
  101. Soldan, S. S., Plassmeyer, M. L., Matukonis, M. K. & Gonzalez-Scarano, F.(2005). La Crosse virus nonstructural protein NSs counteracts the effects of short interfering RNA. J Virol 79, 234–244.[CrossRef] [Google Scholar]
  102. Stalder, J., Reigel, F. & Koblet, H.(1983). Defective viral RNAs in Aedes albopictus C6/36 cells persistently infected with Semliki Forest virus. Virology 129, 247–254.[CrossRef] [Google Scholar]
  103. Stollar, V., Shenk, T. E. & Stollar, B. D.(1972). Double-stranded RNA in hamster, chick, and mosquito cells infected with Sindbis virus. Virology 47, 122–132.[CrossRef] [Google Scholar]
  104. Stollar, V., Harrap, K. A., Thomas, V. & Sarver, N.(1979). Observations related to cytopathic effect in Aedes albopictus cells infected with Sindbis virus. In Arctic and Tropical Arboviruses, pp. 277–296. Edited by E. Kurstak. New York: Academic Press.
  105. Teixeira, L., Ferreira, A. & Ashburner, M.(2008). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6, e2 [Google Scholar]
  106. Tortosa, P., Courtiol, A., Moutailler, S., Failloux, A. B. & Weill, M.(2008). Chikungunya–Wolbachia interplay in Aedes albopictus. Insect Mol Biol 17, 677–684.[CrossRef] [Google Scholar]
  107. Travanty, E. A., Adelman, Z. N., Franz, A. W., Keene, K. M., Beaty, B. J., Blair, C. D., James, A. A. & Olson, K. E.(2004). Using RNA interference to develop dengue virus resistance in genetically modified Aedes aegypti. Insect Biochem Mol Biol 34, 607–613.[CrossRef] [Google Scholar]
  108. Vaidyanathan, R. & Scott, T. W.(2006). Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11, 1643–1651.[CrossRef] [Google Scholar]
  109. van Rij, R. P. & Berezikov, E.(2009). Small RNAs and the control of transposons and viruses in Drosophila. Trends Microbiol 17, 163–171.[CrossRef] [Google Scholar]
  110. 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.[CrossRef] [Google Scholar]
  111. Voinnet, O.(2005). Non-cell autonomous RNA silencing. FEBS Lett 579, 5858–5871.[CrossRef] [Google Scholar]
  112. Wang, X. H., Aliyari, R., Li, W. X., Li, H. W., Kim, K., Carthew, R., Atkinson, P. & Ding, S. W.(2006). RNA interference directs innate immunity against viruses in adult Drosophila. Science 312, 452–454.[CrossRef] [Google Scholar]
  113. Wang, H., Blair, C. D., Olson, K. E. & Clem, R. J.(2008). Effects of inducing or inhibiting apoptosis on Sindbis virus replication in mosquito cells. J Gen Virol 89, 2651–2661.[CrossRef] [Google Scholar]
  114. 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.[CrossRef] [Google Scholar]
  115. Weaver, S. C.(2006). Evolutionary influences in arboviral disease. Curr Top Microbiol Immunol 299, 285–314. [Google Scholar]
  116. Weaver, S. C. & Barrett, A. D.(2004). Transmission cycles, host range, evolution and emergence of arboviral disease. Nat Rev Microbiol 2, 789–801.[CrossRef] [Google Scholar]
  117. Weaver, S. C., Scott, T. W., Lorenz, L. H., Lerdthusnee, K. & Romoser, W. S.(1988). Togavirus-associated pathologic changes in the midgut of a natural mosquito vector. J Virol 62, 2083–2090. [Google Scholar]
  118. Weaver, S. C., Lorenz, L. H. & Scott, T. W.(1992). Pathologic changes in the midgut of Culex tarsalis following infection with western equine encephalomyelitis virus. Am J Trop Med Hyg 47, 691–701. [Google Scholar]
  119. Whitten, M. M., Shiao, S. H. & Levashina, E. A.(2006). Mosquito midguts and malaria: cell biology, compartmentalization and immunology. Parasite Immunol 28, 121–130.[CrossRef] [Google Scholar]
  120. Xi, Z., Ramirez, J. L. & Dimopoulos, G.(2008). The Aedes aegypti toll pathway controls dengue virus infection. PLoS Pathog 4, e1000098[CrossRef] [Google Scholar]
  121. Xie, Q. & Guo, H. S.(2006). Systemic antiviral silencing in plants. Virus Res 118, 1–6.[CrossRef] [Google Scholar]
  122. Yoneyama, M. & Fujita, T.(2009). RNA recognition and signal transduction by RIG-I-like receptors. Immunol Rev 227, 54–65.[CrossRef] [Google Scholar]
  123. Yoo, B. C., Kragler, F., Varkonyi-Gasic, E., Haywood, V., Archer-Evans, S., Lee, Y. M., Lough, T. J. & Lucas, W. J.(2004). A systemic small RNA signaling system in plants. Plant Cell 16, 1979–2000.[CrossRef] [Google Scholar]
  124. 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.[CrossRef] [Google Scholar]
  125. Zambon, R. A., Vakharia, V. N. & Wu, L. P.(2006). RNAi is an antiviral immune response against a dsRNA virus in Drosophila melanogaster. Cell Microbiol 8, 880–889.[CrossRef] [Google Scholar]
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