Advertisement

Pathogenesis of Rift Valley fever virus in mosquitoes — tracheal conduits & the basal lamina as an extra-cellular barrier

  • W. S. Romoser
  • M. J. Turell
  • K. Lerdthusnee
  • M. Neira
  • D. Dohm
  • G. Ludwig
  • L. Wasieloski

Summary

Knowledge of the fate of an arbovirus in a mosquito is fundamental to understanding the mosquito’s competence to transmit the virus. When a competent mosquito ingests viremic vertebrate blood, virus infects midgut epithelial cells and replicates, then disseminates to other tissues, including salivary glands and/or ovaries. The virus is then transmitted to the next vertebrate host horizontally via bite and/or vertically to the mosquito’s offspring. Not all mosquitoes that ingest virus become infected or, if infected, transmit virus. Several “barriers” to arbovirus passage, and ultimately transmission, have been identified in incompetent or partially competent mosquitoes, including, among others, gut escape barriers and salivary gland infection barriers. The extra-cellular basal lamina around the midgut epithelium and the basal lamina that surrounds the salivary glands may act as such barriers. Midgut basal lamina pore sizes are significantly smaller than arboviruses and ultrastructural evidence suggests that midgut tracheae and tracheoles may provide a means for viruses to circumvent this barrier. Further, immunocytochemical evidence indicates the existence of a salivary gland infection barrier in Anopheles stephensi. The basal lamina may prevent access to mosquito cell surface virus receptors and help explain why anopheline mosquitoes are relatively incompetent arbovirus transmitters when compared to culicines.

Keywords

Salivary Gland Basal Lamina Rift Valley Fever Rift Valley Fever Virus Midgut Epithelium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Barrett JW, Brownwright AJ, Primavera MJ, Palli SR (1998) Studies of the nucleopolyhedrovirus infection process in insects by using the green fluorescence protein as a reporter. J Virol 72: 3377–3382PubMedGoogle Scholar
  2. 2.
    Bowers DF, Abell BA, Brown DT (1995) Replication and tissue tropism of the Alphavirus Sindbis in the mosquito Aedes albopictus. Virology 212: 1–12PubMedCrossRefGoogle Scholar
  3. 3.
    Chamberlin RW, Sudia WD (1961) Mechanism of transmission of viruses by mosquitoes. Ann Rev Entomol 6: 371–390CrossRefGoogle Scholar
  4. 4.
    Chandler LJ, Blair CD, Beaty BJ (1998) LaCrosse virus infection of Aedes triseriatus (Diptera: Culicidae) ovaries before dissemination of virus from the midgut. J Med Entomol 35: 567–572PubMedGoogle Scholar
  5. 5.
    Engelhard EK, Kam-Morgan LNW, Washburn JO, Volkman LE (1994) The insect tracheal system: a conduit for the systemic spread of Autographa californica M nuclear polyhedrosis virus. Proc Natl Acad Sci USA, Microbiology 91: 3224–3227CrossRefGoogle Scholar
  6. 6.
    Faran ME, Romoser WS, Bailey CL (1986) Use of the avidin-biotin-peroxidase complex immunocytochemical procedure for detection of Rift Valley fever virus in paraffin sections of mosquitoes. Am J Trop Hyg 35: 1061–1067Google Scholar
  7. 7.
    Gargan II TP, Bailey CL, Higbee GA, Gad A, El Said S (1983) The effect of laboratory colonization on the vector pathogen interactions of Egyptian Culex pipiens and Rift Valley fever virus. Am J Trop Med Hyg 32: 1154–1163PubMedGoogle Scholar
  8. 8.
    Hardy JL, Houk EJ, Kramer LD, Reeves WC (1983) Intrinsic factors affecting vector competence of mosquitoes for arboviruses. Ann Rev Entomol 28: 229–262CrossRefGoogle Scholar
  9. 9.
    Hardy JL (1988) Susceptibility and resistance of vector mosquitoes. In: Monath TP (ed) Arboviruses: epidemiology and ecology, vol. 1. CRC Press, Boca Raton, Fl, pp 87–126Google Scholar
  10. 10.
    Hecker H (1977) Structure and function of midgut epithelial cells in Culicidae mosquitoes (Insecta, Diptera). Cell Tiss Res 184: 321–341CrossRefGoogle Scholar
  11. 11.
    Hecker H, Freyvogel TA, Briegel H, Steiger R (1971) The ultrastructure of midgut epithelium in Aedes aegypti (L.) (Insecta, Diptera) males. Acta Trop 28: 275–289PubMedGoogle Scholar
  12. 12.
    Kirkpatrick BA, Washburn JO, Engelhard EK, Volkman LE (1994) Primary infection of insect tracheae by Autographa californica M nuclear polyhedrosis virus. Virology 203: 184–186PubMedCrossRefGoogle Scholar
  13. 13.
    Leake CJ (1992) Arbovirus-mosquito interactions and vector specificity. Parasitology Today 8: 123–128PubMedCrossRefGoogle Scholar
  14. 14.
    Leon CA (1975) Sequelae of Venezuelan equine encephalitis in humans: a four-year follow-up. Int J Epidemiol 4: 131–140PubMedGoogle Scholar
  15. 15.
    Lerdthusnee K, Romoser WS, Faran ME, Dohm DJ (1995) Rift Valley fever virus in the cardia of Culex pipiens: an immunocytochemical and ultrastructural study. Am J Trop Med Hyg 53: 331–337PubMedGoogle Scholar
  16. 16.
    Locke, M (1985) The structure of epidermal feet during their development. Tissue Cell 17: 901–921CrossRefPubMedGoogle Scholar
  17. 17.
    Locke, M (1986) The development of the plasma membrane reticular system in the fat body of an insect. Tissue Cell 18: 853–867CrossRefPubMedGoogle Scholar
  18. 18.
    Maina JN (1989) Scanning and transmission electron microscopic study of the tracheal air sac system in a grasshopper Chrotogonus senegalensis (Kraus)-Orthoptera: Acrididae: Pyrgomorphinae. The Anatomical Record 223: 393–405PubMedCrossRefGoogle Scholar
  19. 19.
    Meegan JM, Khalil GM, Hoogstraal H, Adham FK (1980) Experimental transmission and field isolation studies implicating Culex pipiens as a vector of Rift Valley fever in Egypt. Am J Trop Med Hyg 29: 1405–1410PubMedGoogle Scholar
  20. 20.
    Meegan JM, Bailey CL (1988) Rift Valley fever. In: Monath TP (ed) Arboviruses: epidemiology and ecology, vol. 4. CRC Press, Boca Raton, Fl, pp 51–76Google Scholar
  21. 21.
    Morse, SS (1993) Emerging viruses. New York Oxford, vol 4, Oxford University Press, pp xxiii+317Google Scholar
  22. 22.
    Pro MED, Tuesday 27 Aug 2003. Rift Valley fever — Egypt (Archive 20030827.2158)Google Scholar
  23. 23.
    Reeves WC, Asman SM, Hardy JL, Milby MM, Reisen WK (1990) Epidemiology and control of mosquito-borne arboviruses in California, 1943–1987. California Mosquito and Vector Control Association, Inc., Sacramento, CaliforniaGoogle Scholar
  24. 24.
    Romoser WS, Faran ME, Bailey CL, Lerdthusnee K (1992) An immunocytochemical study of the distribution of Rift Valley fever virus in the mosquito Culex pipiens. Am J Trop Med Hyg 46: 489–501PubMedGoogle Scholar
  25. 25.
    Romoser WS, Wasieloski Jr LP, Pushko P, Kondig JP, Lerdthusnee K, Neira M, Ludwig GV (2004) Experimental and ultrastructural evidence for arbovirus dissemination conduits from the mosquito (Diptera: Culicidae) midgut. J Med Entomol 41: 467–475PubMedCrossRefGoogle Scholar
  26. 26.
    Ryder S (1995) Encefalitis equine Venezolana. Aspectos epidemiologicos de la enfermedad entre 1962 y 1971 en la Guajira Venezolana. Invest Clin 36: 169–214Google Scholar
  27. 27.
    Thompson RE, Wu WK, Verleye D, Rai KS (1993) Midgut basal lamina thickness and dengue-1 virus dissemination rates in laboratory strains of Aedes albopictus (Diptera: Culicidae). J Med Entomol 30: 326–331Google Scholar
  28. 28.
    Turell MJ (1988) Horizontal and vertical transmission of viruses by insect and tick vectors. In: Monath TP (ed) Arboviruses: epidemiology and ecology, vol. 1. CRC Press. Boca Raton, Fl, pp 127–152Google Scholar
  29. 29.
    Turell MJ, Mather TN, Spielman A, Bailey CL (1987) Increased dissemination of dengue 2 virus in Aedes aegypti associated with concurrent ingestion of microfilariae of Brugia malayi. Am J Trop Med Hyg 37: 197–201PubMedGoogle Scholar
  30. 30.
    Turell MJ, Romoser WS (1994) Effect of the developmental stage at infection on the ability of adult Anopheles stephensi to transmit Rift Valley fever virus. Am J Trop Med Hyg 50(4): 448–451PubMedGoogle Scholar
  31. 31.
    Turell MJ, Rossignol PA, Spielman A, Rossi CA, Bailey CL (1984) Enhanced arboviral transmission by mosquitoes that concurrently ingested microfilariae. Science 225: 1039–1041PubMedGoogle Scholar
  32. 32.
    Vaughan JA, Turell MJ (1996) Facilitation of Rift Valley fever virus transmission by Plasmodium berghei sporozoites in Anopheles stephensi mosquitoes. Am J Trop Med Hyg 55: 407–409PubMedGoogle Scholar
  33. 33.
    Vaughan JA, Turell MJ(1996) Dual host infections: enhanced infectivity of eastern equine encephalitis virus to Aedes mosquitoes mediated by Brugia microfilariae. AmJ Trop Med Hyg 54: 105–109Google Scholar
  34. 34.
    Vaughan JA, Trpis M, Turell MJ (1999)Brugia malayi microfilariae (Nematoda: Filaridae) enhance the infectivity of Venezuelan equine encephalitis virus to Aedes mosquitoes (Diptera: Culicidae). J Med Entomol 36: 758–763PubMedGoogle Scholar
  35. 35.
    Volkman LE (1997) Nucleopolyhedrovirus interactions with their insect hosts. Advances in Virus Research 48: 313–348PubMedCrossRefGoogle Scholar
  36. 36.
    Walton TE, Grayson M (1988) Venezuelan equine encephalomyelitis. In: Monath TP (ed) Arboviruses: epidemiology and ecology vol 4. CRC Press, Boca Raton, Fl, pp 203–231Google Scholar
  37. 37.
    Weaver SC, Sherer WF, Cupp EW, Costello DA (1984) Barriers to dissemination of Venezuelan encephalitis viruses in the Middle American enzootic vector mosquito, Culex (Melanoconian) taeniopus. Am J Trop Med Hyg 33: 953–960PubMedGoogle Scholar
  38. 38.
    Hsu SM, Raine L, Fanger H (1981) Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: a comparison between ABC and unlabelled antibody PAP procedures. J Histochem Cytochem 29: 577–580PubMedGoogle Scholar

Copyright information

© Springer-Verlag/Wien 2005

Authors and Affiliations

  • W. S. Romoser
    • 1
  • M. J. Turell
    • 2
  • K. Lerdthusnee
    • 3
  • M. Neira
    • 1
  • D. Dohm
    • 2
  • G. Ludwig
    • 2
  • L. Wasieloski
    • 2
  1. 1.Tropical Disease Institute, Department of Biomedical Sciences, College of Osteopathic MedicineOhio UniversityAthens
  2. 2.U.S. Army Medical Research Institute of Infectious DiseasesFort Detrick, Frederick
  3. 3.Department of Entomology, U.S. Army Medical Component (USAMC)Armed Forces Institute of Medical Research (AFRIMS)BangkokThailand

Personalised recommendations