1887

Abstract

Apoptosis is observed during a spectrum of conditions including exogenous virus infection and endogenous cellular turnover. Adult female mosquitoes challenged with increasing titres of Sindbis virus (SINV) via intrathoracic inoculation demonstrated that the injection dosage did not result in significantly different levels of virus growth or mosquito survival at day 10 post-infection. Tissues probed for apoptosis using an TUNEL assay revealed SINV-associated apoptotic cells scattered throughout the proximal and distal regions of the salivary gland (SG) lateral lobes but which were not detected in the median lobe or the midgut and hindgut. Apoptosis was also identified in SG duct cells in both infected and uninfected mosquitoes, suggesting routine tissue homeostasis. SINV-associated apoptosis sequestered to the SG lateral lobes indicates a differential epithelial cell response to an arbovirus and provides insight into mosquito defence mechanisms against pathogens and SG infection barriers, hurdles to transmission of arboviruses of public health concern.

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2012-11-01
2024-04-20
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References

  1. Almeras L. A., Fontaine A., Belghazi M., Bourdon S., Boucomont-Chapeaublanc E., Orlandi-Pradines E., Baragatti M., Corre-Catelin N., Reiter P.other authors 2010; Salivary gland protein repertoire from Aedes aegypti mosquitoes. Vector Borne Zoonotic Dis 10:391–402 [View Article][PubMed]
    [Google Scholar]
  2. Arcà B., Lombardo F., Francischetti I. M., Pham V. M., Mestres-Simon M., Andersen J. F., Ribeiro J. M. 2007; An insight into the sialome of the adult female mosquito Aedes albopictus. Insect Biochem Mol Biol 37:107–127 [View Article][PubMed]
    [Google Scholar]
  3. Barreau C., Conrad J., Fischer E., Lujan H. D., Vernick K. D. 1999; Identification of surface molecules on salivary glands of the mosquito, Aedes aegypti, by a panel of monoclonal antibodies. Insect Biochem Mol Biol 29:515–526 [View Article][PubMed]
    [Google Scholar]
  4. Bowers D. F., Abell B. A., Brown D. T. 1995; Replication and tissue tropism of the alphavirus Sindbis in the mosquito Aedes albopictus. Virology 212:1–12 [View Article][PubMed]
    [Google Scholar]
  5. 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 [View Article][PubMed]
    [Google Scholar]
  6. Burge B. W., Pfefferkorn E. R. 1966; Complementation between temperature-sensitive mutants of Sindbis virus. Virology 30:214–223 [View Article][PubMed]
    [Google Scholar]
  7. Chamberlin R. W. 1980; Epidemiology of arthropod-borne Togaviruses: the role of arthropods as hosts and vectors and of vertebrate hosts in natural transmission cycles. In Togaviridae and Flaviridae pp. 175–227 Edited by Schleisinger S., Schleisinger J. J. New York: Plenum Press;
    [Google Scholar]
  8. Clements A. N. 1996a; Adult food and feeding mechanisms. In The Biology of Mosquitoes pp. 222 London: Chapman and Hall;
    [Google Scholar]
  9. Clements A. N. 1996b; Adult salivary glands and their secretions. In The Biology of Mosquitoes pp. 251–262 London: Chapman and Hall;
    [Google Scholar]
  10. Cooper D. M., Pio F., Thi E. P., Theilmann D., Lowenberger C. 2007; Characterization of Aedes Dredd: a novel initiator caspase from the yellow fever mosquito, Aedes aegypti. Insect Biochem Mol Biol 37:559–569 [View Article][PubMed]
    [Google Scholar]
  11. Fields B. N., Howley P. M., Griffin D. E., Lamb R. A., Martin M. A., Roizman B., Strausm B., Snipe D. M. 2001 Fields Virology, 4th edn. New York: Lippincott Williams & Wilkins;
    [Google Scholar]
  12. Gerberg E. J. 1970 Manual for Mosquito Rearing and Experimental Techniques California: American Mosquito Control Assocociation, Inc;
    [Google Scholar]
  13. 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 [View Article][PubMed]
    [Google Scholar]
  14. 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[PubMed]
    [Google Scholar]
  15. Jacobson M. D., Weil M., Raff M. C. 1997; Programmed cell death in animal development. Cell 88:347–354 [View Article][PubMed]
    [Google Scholar]
  16. Juhn J., Naeem-Ullah U., Maciel Guedes B. A., Majid A., Coleman J., Paolucci Pimenta P. F., Akram W., James A. A., Marinotti O. 2011; Spatial mapping of gene expression in the salivary glands of the dengue vector mosquito, Aedes aegypti. Parasit Vectors 4:1–13 [View Article][PubMed]
    [Google Scholar]
  17. Karpf A. R., Brown D. T. 1998; Comparison of Sindbis virus-induced pathology in mosquito and vertebrate cell cultures. Virology 240:193–201 [View Article][PubMed]
    [Google Scholar]
  18. Kerr J. F. R., Winterford C. M., Harmon B. V. 1994; Apoptosis. Its significance in cancer and cancer therapy. Cancer 73:2013–2026 [View Article][PubMed]
    [Google Scholar]
  19. Krakauer D. C., Payne R. J. H. 1997; The evolution of virus-induced apoptosis. Proc Biol Sci 264:1757–1762 [View Article][PubMed]
    [Google Scholar]
  20. Kramer L. D., Hardy J. L., Presser S. B., Houk E. J. 1981; Dissemination barriers for western equine encephalomyelitis virus in Culex tarsalis infected after ingestion of low viral doses. Am J Trop Med Hyg 30:190–197[PubMed]
    [Google Scholar]
  21. 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 [View Article][PubMed]
    [Google Scholar]
  22. Levine B., Huang Q., Isaacs J. T., Reed J. C., Griffin D. E., Hardwick J. M. 1993; Conversion of lytic to persistent alphavirus infection by the bcl-2 cellular oncogene. Nature 361:739–742 [View Article][PubMed]
    [Google Scholar]
  23. Lewis J., Wesselingh S. L., Griffin D. E., Hardwick J. M. 1996; Alphavirus-induced apoptosis in mouse brains correlates with neurovirulence. J Virol 70:1828–1835[PubMed]
    [Google Scholar]
  24. McCall K., Peterson J. S. 2004; Detection of apoptosis in Drosophila. In Apoptosis Methods and Protocols pp. 191–206 Edited by Brady H. J. M. Totowa, NJ: Humana Press; [View Article]
    [Google Scholar]
  25. 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[PubMed]
    [Google Scholar]
  26. Parikh G. R., Oliver J. D., Bartholomay L. C. 2009; A haemocyte tropism for an arbovirus. J Gen Virol 90:292–296 [View Article][PubMed]
    [Google Scholar]
  27. Platt K. B., Linthicum K. J., Myint K. S. A., Innis B. L., Lerdthusnee K., Vaughn D. W. 1997; Impact of dengue virus infection on feeding behavior of Aedes aegypti. Am J Trop Med Hyg 57:119–125[PubMed]
    [Google Scholar]
  28. Qualls W. A., Day J. F., Xue R.-D., Bowers D. F. 2012; Sindbis virus infection alters blood feeding responses and DEET repellency in Aedes aegypti (Diptera: Culicidae). J Med Entomol 49:418–423 [View Article][PubMed]
    [Google Scholar]
  29. Renz D., Brown D. T. 1976; Characteristics of Sindbis virus temperature-sensitive mutants in cultured BHK-21 and Aedes albopictus (mosquito) cells. J Virol 19:775–781[PubMed]
    [Google Scholar]
  30. Ribeiro J. M. C. 1992; Characterization of a vasodilator from the salivary glands of the yellow fever mosquito Aedes aegypti. J Exp Biol 165:61–71[PubMed]
    [Google Scholar]
  31. Rosen L., Gubler D. 1974; The use of mosquitoes to detect and propagate dengue viruses. Am J Trop Med Hyg 23:1153–1160[PubMed]
    [Google Scholar]
  32. Seron T. J., Hill J., Linser P. J. 2004; A GPI-linked carbonic anhydrase expressed in the larval mosquito midgut. J Exp Biol 207:4559–4572 [View Article][PubMed]
    [Google Scholar]
  33. Singh K. R. P. 1967; Cell cultures derived from larvae of Aedes albopictus (Skuse) and Aedes aegypti. Curr Sci 36:506–508
    [Google Scholar]
  34. Vaidyanathan R., Scott T. W. 2006; Apoptosis in mosquito midgut epithelia associated with West Nile virus infection. Apoptosis 11:1643–1651 [View Article][PubMed]
    [Google Scholar]
  35. Vo M., Bowers D. F. 2006; The arbovirus lifecycle: links in a chain. Tech Bull Fl Mosq Contr Assoc 7:31–34
    [Google Scholar]
  36. Vo M., Linser P. J., Bowers D. F. 2010; Organ-associated muscles in Aedes albopictus (Diptera: Culicidae) respond differentially to Sindbis virus. J Med Entomol 47:215–225 [View Article][PubMed]
    [Google Scholar]
  37. 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 [View Article][PubMed]
    [Google Scholar]
  38. Wang H., Gort T., Boyle D. L., Clem R. J. 2012; Effects of manipulating apoptosis on Sindbis virus infection of Aedes aegypti mosquitoes. J Virol 86:6546–6554 [View Article][PubMed]
    [Google Scholar]
  39. 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[PubMed]
    [Google Scholar]
  40. 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[PubMed]
    [Google Scholar]
  41. Wyllie A. H. 1997; Apoptosis: an overview. Br Med Bull 53:451–465 [View Article][PubMed]
    [Google Scholar]
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