1887

Abstract

Horizontally transmitted mosquito-borne viruses enter the midgut with a blood meal then disseminate to infect the salivary glands. En route to the salivary glands, these viruses encounter the plasma (haemolymph) and blood cells (haemocytes). Haemocytes respond to a variety of micro-organisms, but their role in virus replication and dissemination has not been described. To look for a potential haemocyte tropism for an arbovirus, a Sindbis virus was injected intrathoracically into four species of mosquito. Virus infects haemocytes as early as 6 h post injection (p.i.) and infection was evident in these cells for as long as 4 days p.i. More than 90 % of haemocytes were infected, most often the phagocytic granulocytes. Virus titres in the haemolymph increased from 24 h p.i. through 60 h p.i. Similar results were found when mosquitoes were injected with orally infectious Sindbis. These data prove that an arbovirus infects, and replicates in, haemocytes.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.005116-0
2009-02-01
2020-01-17
Loading full text...

Full text loading...

/deliver/fulltext/jgv/90/2/292.html?itemId=/content/journal/jgv/10.1099/vir.0.005116-0&mimeType=html&fmt=ahah

References

  1. Bartholomay, L. C., Fuchs, J. F., Cheng, L. L., Beck, E. T., Vizioli, J., Lowenberger, C. & Christensen, B. M. ( 2004; ). Reassessing the role of defensin in the innate immune response of the mosquito, Aedes aegypti. Insect Mol Biol 13, 125–132.[CrossRef]
    [Google Scholar]
  2. Black, W. C., IV, Bennett, K. E., Gorrochótegui-Escalante, N., Barillas-Mury, C. V., Fernández-Salas, I., de Lourdes Muñoz, M., Fárfan-Alé, J. A., Olson, K. E. & Beaty, B. J. ( 2002; ). Flavivirus susceptibility in Aedes aegypti. Arch Med Res 33, 379–388.[CrossRef]
    [Google Scholar]
  3. 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.[CrossRef]
    [Google Scholar]
  4. 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]
  5. Castillo, J. C., Robertson, A. E. & Strand, M. R. ( 2006; ). Characterization of hemocytes from the mosquitoes Anopheles gambiae and Aedes aegypti. Insect Biochem Mol Biol 36, 891–903.[CrossRef]
    [Google Scholar]
  6. Clarke, T. E. & Clem, R. J. ( 2002; ). Lack of involvement of haemocytes in the establishment and spread of infection in Spodoptera frugiperda larvae infected with the baculovirus Autographa californica M nucleopolyhedrovirus by intrahaemocoelic injection. J Gen Virol 83, 1565–1572.
    [Google Scholar]
  7. Engelhard, E. K., Kam-Morgan, L. N., Washburn, J. O. & Volkman, L. E. ( 1994; ). The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc Natl Acad Sci U S A 91, 3224–3227.[CrossRef]
    [Google Scholar]
  8. Feng, G., Yu, Q., Hu, C., Wang, Y., Yuan, G., Chen, Q., Yang, K. & Pang, Y. ( 2007; ). Apoptosis is induced in the haemolymph and fat body of Spodoptera exigua larvae upon oral inoculation with Spodoptera litura nucleopolyhedrovirus. J Gen Virol 88, 2185–2193.[CrossRef]
    [Google Scholar]
  9. Foy, B. D., Myles, K. M., Pierro, D. J., Sanchez-Vargas, I., Uhlirova, M., Jindra, M., Beaty, B. J. & Olson, K. E. ( 2004; ). Development of a new Sindbis virus transducing system and its characterization in three Culicine mosquitoes and two Lepidopteran species. Insect Mol Biol 13, 89–100.[CrossRef]
    [Google Scholar]
  10. Girard, Y. A., Klingler, K. A. & Higgs, S. ( 2004; ). West Nile virus dissemination and tissue tropisms in orally infected Culex pipiens quinquefasciatus. Vector Borne Zoonotic Dis 4, 109–122.[CrossRef]
    [Google Scholar]
  11. Hardy, J. L., Houk, E. J., Kramer, L. D. & Reeves, W. C. ( 1983; ). Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Annu Rev Entomol 28, 229–262.[CrossRef]
    [Google Scholar]
  12. Hernandez-Martinez, S., Lanz, H., Rodriguez, M. H., Gonzalez-Ceron, L. & Tsutsumi, V. ( 2002; ). Cellular-mediated reactions to foreign organisms inoculated into the hemocoel of Anopheles albimanus (Diptera: Culicidae). J Med Entomol 39, 61–69.[CrossRef]
    [Google Scholar]
  13. Hillyer, J. F. & Christensen, B. M. ( 2002; ). Characterization of hemocytes from the yellow fever mosquito, Aedes aegypti. Histochem Cell Biol 117, 431–440.[CrossRef]
    [Google Scholar]
  14. Hillyer, J. F., Schmidt, S. L. & Christensen, B. M. ( 2003a; ). Hemocyte-mediated phagocytosis and melanization in the mosquito Armigeres subalbatus following immune challenge by bacteria. Cell Tissue Res 313, 117–127.[CrossRef]
    [Google Scholar]
  15. Hillyer, J. F., Schmidt, S. L. & Christensen, B. M. ( 2003b; ). Rapid phagocytosis and melanization of bacteria and Plasmodium sporozoites by hemocytes of the mosquito Aedes aegypti. J Parasitol 89, 62–69.[CrossRef]
    [Google Scholar]
  16. Hillyer, J. F., Schmidt, S. L. & Christensen, B. M. ( 2004; ). The antibacterial innate immune response by the mosquito Aedes aegypti is mediated by hemocytes and independent of Gram type and pathogenicity. Microbes Infect 6, 448–459.[CrossRef]
    [Google Scholar]
  17. Infanger, L. C., Rocheleau, T. A., Bartholomay, L. C., Johnson, J. K., Fuchs, J., Higgs, S., Chen, C. C. & Christensen, B. M. ( 2004; ). The role of phenylalanine hydroxylase in melanotic encapsulation of filarial worms in two species of mosquitoes. Insect Biochem Mol Biol 34, 1329–1338.[CrossRef]
    [Google Scholar]
  18. Keddie, B. A., Aponte, G. W. & Volkman, L. E. ( 1989; ). The pathway of infection of Autographa californica nuclear polyhedrosis virus in an insect host. Science 243, 1728–1730.[CrossRef]
    [Google Scholar]
  19. Lai, S. C., Chen, C. C. & Hou, R. F. ( 2001; ). Electron microscopic observations on wound-healing in larvae of the mosquito Armigeres subalbatus (Diptera: Culicidae). J Med Entomol 38, 836–843.[CrossRef]
    [Google Scholar]
  20. Lowenberger, C. ( 2001; ). Innate immune response of Aedes aegypti. Insect Biochem Mol Biol 31, 219–229.[CrossRef]
    [Google Scholar]
  21. Myles, K. M., Pierro, D. J. & Olson, K. E. ( 2003; ). Deletions in the putative cell receptor-binding domain of Sindbis virus strain MRE16 E2 glycoprotein reduce midgut infectivity in Aedes aegypti. J Virol 77, 8872–8881.[CrossRef]
    [Google Scholar]
  22. Olson, K. E., Higgs, S., Gaines, P. J., Powers, A. M., Davis, B. S., Kamrud, K. I., Carlson, J. O., Blair, C. D. & Beaty, B. J. ( 1996; ). Genetically engineered resistance to dengue-2 virus transmission in mosquitoes. Science 272, 884–886.[CrossRef]
    [Google Scholar]
  23. Olson, K. E., Myles, K. M., Seabaugh, R. C., Higgs, S., Carlson, J. O. & Beaty, B. J. ( 2000; ). Development of a Sindbis virus expression system that efficiently expresses green fluorescent protein in midguts of Aedes aegypti following per os infection. Insect Mol Biol 9, 57–65.[CrossRef]
    [Google Scholar]
  24. Pierro, D. J., Myles, K. M., Foy, B. D., Beaty, B. J. & Olson, K. E. ( 2003; ). Development of an orally infectious Sindbis virus transducing system that efficiently disseminates and expresses green fluorescent protein in Aedes aegypti. Insect Mol Biol 12, 107–116.[CrossRef]
    [Google Scholar]
  25. Pierro, D. J., Powers, E. L. & Olson, K. E. ( 2007; ). Genetic determinants of Sindbis virus strain TR339 affecting midgut infection in the mosquito Aedes aegypti. J Gen Virol 88, 1545–1554.[CrossRef]
    [Google Scholar]
  26. Romoser, W. S., Wasieloski, L. P., Jr, Pushko, P., Kondig, J. P., Lerdthusnee, K., Neira, M. & Ludwig, G. V. ( 2004; ). Evidence for arbovirus dissemination conduits from the mosquito (Diptera: Culicidae) midgut. J Med Entomol 41, 467–475.[CrossRef]
    [Google Scholar]
  27. Salazar, M. I., Richardson, J. H., Sanchez-Vargas, I., Olson, K. E. & Beaty, B. J. ( 2007; ). Dengue virus type 2: replication and tropisms in orally infected Aedes aegypti mosquitoes. BMC Microbiol 7, 9 [CrossRef]
    [Google Scholar]
  28. Shiao, S. H., Higgs, S., Adelman, Z., Christensen, B. M., Liu, S. H. & Chen, C. C. ( 2001; ). Effect of prophenoloxidase expression knockout on the melanization of microfilariae in the mosquito Armigeres subalbatus. Insect Mol Biol 10, 315–321.[CrossRef]
    [Google Scholar]
  29. Sriurairatna, S. & Bhamarapravati, N. ( 1977; ). Replication of dengue-2 virus in Aedes albopictus mosquitoes. An electron microscopic study. Am J Trop Med Hyg 26, 1199–1205.
    [Google Scholar]
  30. Tamang, D., Tseng, S. M., Huang, C. Y., Tsao, I. Y., Chou, S. Z., Higgs, S., Christensen, B. M. & Chen, C. C. ( 2004; ). The use of a double subgenomic Sindbis virus expression system to study mosquito gene function: effects of antisense nucleotide number and duration of viral infection on gene silencing efficiency. Insect Mol Biol 13, 595–602.[CrossRef]
    [Google Scholar]
  31. Trudeau, D., Washburn, J. O. & Volkman, L. E. ( 2001; ). Central role of hemocytes in Autographa californica M nucleopolyhedrovirus pathogenesis in Heliothis virescens and Helicoverpa zea. J Virol 75, 996–1003.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.005116-0
Loading
/content/journal/jgv/10.1099/vir.0.005116-0
Loading

Data & Media loading...

Most cited articles

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