Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico Free

Abstract

The genus contains approximately 70 single-stranded, positive-sense RNA viruses that are mosquito-borne, tick-borne or have no known vector. Two discoveries support previous suggestions of the existence of a large number of unsampled flaviviruses: (i) a new flavivirus, Kamiti River virus, was recently isolated from Kenyan mosquitoes, and (ii) sequences with high similarity to those of flaviviruses have been found integrated into the genome of mosquitoes, suggesting a past infection with a virus (or viruses) that has yet to be discovered. These sequences were related most closely to a flavivirus that infects insects alone, cell fusing agent virus (CFAV). CFAV was originally isolated in the laboratory from an cell line. To date, this virus had not been found in the wild. In the present study, over 40 isolates of a novel strain of CFAV were discovered from mature mosquitoes sampled from the wild in Puerto Rico. The viral strain was present in a range of mosquito species, including , and sp., from numerous locations across the island and, importantly, in mosquitoes of both sexes, suggesting vertical transmission. Here, results from viral screening, and cell culture and molecular identification of the infected mosquitoes are presented. Experimental-infection tests were also conducted by using the original CFAV strain and a highly efficient reverse-transcription mechanism has been documented, in which initiation of copying occurs at the 3′ terminus of either the genomic RNA or the intermediate of replication, potentially elucidating the mechanism by which flaviviral sequences may have integrated into mosquito genomes.

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2006-04-01
2024-03-29
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References

  1. Altschul S. F., Madden T. L., Schäffer A. A., Zhang J., Zhang Z., Miller W., Lipman D. J. 1997; Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Res 25:3389–3402 [CrossRef]
    [Google Scholar]
  2. Belkin J. N., Heinemann S. J. 1975; Collection records of the project ‘Mosquitoes of middle America’. 2. Puerto Rico (PR, PRA, PRX) and Virgin Is (V VIA). Mosq Syst 7:269–296
    [Google Scholar]
  3. Billoir F., de Chesse R., Tolou H., de Micco P., Gould E. A., de Lamballerie X. 2000; Phylogeny of the genus Flavivirus using complete coding sequences of arthropod-borne viruses and viruses with no known vector. J Gen Virol 81:781–790
    [Google Scholar]
  4. Cammisa-Parks H., Cisar L. A., Kane A., Stollar V. 1992; The complete nucleotide sequence of cell fusing agent (CFA): homology between the nonstructural proteins encoded by CFA and the nonstructural proteins encoded by arthropod-borne flaviviruses. Virology 189:511–524 [CrossRef]
    [Google Scholar]
  5. Cook S., Diallo M., Sall A. A., Cooper A., Holmes E. C. 2005; Mitochondrial markers for molecular identification of Aedes mosquitoes (Diptera: Culicidae) involved in transmission of arboviral disease in West Africa. J Med Entomol 42:19–28 [CrossRef]
    [Google Scholar]
  6. Crabtree M. B., Sang R. C., Stollar V., Dunster L. M., Miller B. R. 2003; Genetic and phenotypic characterization of the newly described insect flavivirus, Kamiti River virus. Arch Virol 148:1095–1118 [CrossRef]
    [Google Scholar]
  7. Crochu S., Cook S., Attoui H., Charrel R. N., De Chesse R., Belhouchet M., Lemasson J.-J., de Micco P., de Lamballerie X. 2004; Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J Gen Virol 85:1971–1980 [CrossRef]
    [Google Scholar]
  8. de Lamballerie X., Zandotti C., Vignoli C., Bollet C., de Micco P. 1992; A one-step microbial DNA extraction method using “Chelex 100” suitable for gene amplification. Res Microbiol 143:785–790 [CrossRef]
    [Google Scholar]
  9. de Lamballerie X., Crochu S., Billoir F., Neyts J., de Micco P., Holmes E. C., Gould E. A. 2002; Genome sequence analysis of Tamana bat virus and its relationship with the genus Flavivirus . J Gen Virol 83:2443–2454
    [Google Scholar]
  10. Goddard J. M., Wolstenholme D. R. 1978; Origin and direction of replication in mitochondrial DNA molecules from Drosophila melanogaster . Proc Natl Acad Sci U S A 75:3886–3890 [CrossRef]
    [Google Scholar]
  11. Gould E. A., de Lamballerie X., Zanotto P. M., Holmes E. C. 2001; Evolution, epidemiology, and dispersal of flaviviruses revealed by molecular phylogenies. Adv Virus Res 57:71–103
    [Google Scholar]
  12. Guzman M. G., Kouri G. 2002; Dengue: an update. Lancet Infect Dis 2:33–42 [CrossRef]
    [Google Scholar]
  13. Halstead S. B., Jacobson J. 2003; Japanese encephalitis. Adv Virus Res 61:103–138
    [Google Scholar]
  14. Harbach R. E. 1988; The mosquitoes of the subgenus Culex in Southwestern Asia and Egypt (Diptera: Culicidae). Contrib Am Entomol Inst 24:1–240
    [Google Scholar]
  15. Heinz F. X., Collett M. S., Purcell R. H., Gould E. A., Howard C. R., Houghton M., Moorman R. J. M., Rice C. M., Thiel H.-J. 2000; Flaviviridae . In Seventh Report of the International Committee on Taxonomy of Viruses pp  859–878 Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L., Carstens E. B., Estes M. K., Lemon S. M., Maniloff J., Mayo M. A., McGeoch D. J., Pringle C. R., Wickner R. B. San Diego, CA: Academic Press;
    [Google Scholar]
  16. Howe D. K., Vodkin M. H., Novak R. J., Mitchell C. J., McLaughlin G. L. 1992; Detection of St Louis encephalitis virus in mosquitoes by use of the polymerase chain reaction. J Am Mosq Control Assoc 8:333–335
    [Google Scholar]
  17. Igarashi A., Harrap K. A., Casals J., Stollar V. 1976; Morphological, biochemical, and serological studies on a viral agent (CFA) which replicates in and causes fusion of Aedes albopictus (Singh) cells. Virology 74:174–187 [CrossRef]
    [Google Scholar]
  18. Jupp P. G., Grobbelaar A. A., Leman P. A., Kemp A., Dunton R. F., Burkot T. R., Ksiazek T. G., Swanepoel R. 2000; Experimental detection of Rift Valley fever virus by reverse transcription-polymerase chain reaction assay in large samples of mosquitoes. J Med Entomol 37:467–471 [CrossRef]
    [Google Scholar]
  19. Kramer L. D., Wolfe T. M., Green E. N., Chiles R. E., Fallah H., Fang Y., Reisen W. K. 2002; Detection of encephalitis viruses in mosquitoes (Diptera: Culicidae) and avian tissues. J Med Entomol 39:312–323 [CrossRef]
    [Google Scholar]
  20. Liu H., Beckenbach A. T. 1992; Evolution of the mitochondrial cytochrome oxidase II gene among 10 orders of insects. Mol Phylogenet Evol 1:41–52 [CrossRef]
    [Google Scholar]
  21. Lunt D. H., Zhang D. X., Szymura J. M., Hewitt G. M. 1996; The insect cytochrome oxidase I gene: evolutionary patterns and conserved primers for phylogenetic studies. Insect Mol Biol 5:153–165 [CrossRef]
    [Google Scholar]
  22. Mackenzie J. S., Gubler D. J., Petersen L. R. 2004; Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat Med 10:S98–S109 [CrossRef]
    [Google Scholar]
  23. Marin M. S., Zanotto P. M. De A., Gritsun T. S., Gould E. A. 1995; Phylogeny of TYU, SRE, and CFA virus: different evolutionary rates in the genus Flavivirus . Virology 206:1133–1139 [CrossRef]
    [Google Scholar]
  24. McNelly J. R. 1989; The CDC trap as a special monitoring tool. In Proceedings of the 76th Annual Meeting of the New Jersey Mosquito Control Association pp  26–33
    [Google Scholar]
  25. Monath T. P. 2001; Yellow fever: an update. Lancet Infect Dis 1:11–20 [CrossRef]
    [Google Scholar]
  26. Monath T. P., Heinz F. X. 1996; Flaviviruses. In Fields Virology , 3rd edn. pp  961–1034 Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia, NY: Lippincott–Raven;
    [Google Scholar]
  27. Porterfield J. S., Casals J., Chumakov M. P. & 8 other authors 1978; Togaviridae . Intervirology9129–148 [CrossRef]
    [Google Scholar]
  28. Price J. L. 1978; Isolation of Rio Bravo and a hitherto undescribed agent, Tamana bat virus, from insectivorous bats in Trinidad, with serological evidence of infection in bats and man. Am J Trop Med Hyg 27:153–161
    [Google Scholar]
  29. Pybus O. G., Rambaut A., Holmes E. C., Harvey P. H. 2002; New inferences from tree shape: numbers of missing taxa and population growth rates. Syst Biol 51:881–888 [CrossRef]
    [Google Scholar]
  30. Sang R. C., Gichogo A., Gachoya J., Dunster M. D., Ofula V., Hunt A. R., Crabtree M. B., Miller B. R., Dunster L. M. 2003; Isolation of a new flavivirus related to Cell fusing agent virus (CFAV) from field-collected flood-water Aedes mosquitoes sampled from a dambo in central Kenya. Arch Virol 148:1085–1093 [CrossRef]
    [Google Scholar]
  31. Schlesinger R. W. 1971; New opportunities in biological research offered by arthropod cell cultures. I. Some speculations on the possible role of arthropods in the evolution of arboviruses. Curr Top Microbiol Immunol 55:241–245
    [Google Scholar]
  32. Stollar V., Thomas V. 1975; An agent in the Aedes aegypti cell line (Peleg) which causes fusion of Aedes albopictus cells. Virology 64:367–377 [CrossRef]
    [Google Scholar]
  33. Strimmer K., von Haeseler A. 1996; Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol Biol Evol 13:964–969 [CrossRef]
    [Google Scholar]
  34. Strode G. K. (editor) 1951 Yellow Fever New York: McGraw–Hill;
    [Google Scholar]
  35. Swofford D. L. 2000 paup*: Phylogenetic Analysis Using Parsimony (*and other methods), version 4 Sunderland, MA: Sinauer Associates;
    [Google Scholar]
  36. Thompson J. D., Gibson T. J., Plewniak F., Jeanmougin F., Higgins D. G. 1997; The clustal_x windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882 [CrossRef]
    [Google Scholar]
  37. Watkins-Riedel T., Woegerbauer M., Hollemann D., Hufnagl P. 2002; Rapid diagnosis of enterovirus infections by real-time PCR on the LightCycler using the TaqMan format. Diagn Microbiol Infect Dis 42:99–105 [CrossRef]
    [Google Scholar]
  38. Whelan S., Goldman N. 2001; A general empirical model of protein evolution derived from multiple protein families using a maximum-likelihood approach. Mol Biol Evol 18:691–699 [CrossRef]
    [Google Scholar]
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