1887

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Volume 89, Issue 7

Characterization of mosquito-adapted West Nile virus Free

Abstract

West Nile virus (WNV), a mosquito-borne flavivirus, has significantly expanded its geographical and host range since its 1999 introduction into North America. The underlying mechanisms of evolution of WNV and other arboviruses are still poorly understood. Studies evaluating virus adaptation and fitness in relevant systems are largely lacking. In order to evaluate the capacity for host-specific adaptation and the genetic correlates of adaptation , this study measured phenotypic and genotypic changes in WNV resulting from passage in mosquitoes. An increase in replicative ability of WNV in was attained for the two lineages of WNV tested. This adaptation for replication in mosquitoes did not result in a replicative cost in chickens, but did decrease cell-to-cell spread of virus in vertebrate cell culture. Genetic analyses of one mosquito-adapted lineage revealed a total of nine consensus nucleotide substitutions with no accumulation of a significant mutant spectrum. These results differed significantly from previous studies. When St Louis encephalitis virus (SLEV), a closely related flavivirus, was passaged in , moderately attenuated growth in was observed for two lineages tested. These results suggest that significant differences in the capacity for mosquito adaptation may exist between WNV and SLEV, and demonstrate that further comparative studies in relevant systems will help elucidate the still largely unknown mechanisms of arboviral adaptation in ecologically relevant hosts.

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2008-07-01
2024-04-24
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References

  1. Aitken T. H. G. 1977; An in vitro feeding technique for artificially demonstrating virus transmission by mosquitoes. Mosq News 37:130–133
     [Google Scholar]
  2. Austin R. J., Whiting T. L., Anderson R. A., Drebot M. A. 2004; An outbreak of West Nile virus-associated disease in domestic geese ( Anser anser domesticus ) upon initial introduction to a geographic region, with evidence of bird to bird transmission. Can Vet J 45:117–123
     [Google Scholar]
  3. Carrillo C., Borca M., Moore D. M., Morgan D. O., Sobrino F. 1998; In vivo analysis of the stability and fitness of variants recovered from foot-and-mouth disease virus quasispecies. J Gen Virol 79:1699–1706
     [Google Scholar]
  4. Chamberlain R. W. 1980; History of St Louis encephalitis. In St Louis Encephalitis pp 3–61Edited by Monath T. P. Washington, DC: American Public Health Assoc;
     [Google Scholar]
  5. Chambers T. J., Hahn C. S., Galler R., Rice C. M. 1990; Flavivirus genome organization, expression, and replication. Annu Rev Microbiol 44:649–688 [CrossRef]
     [Google Scholar]
  6. Chandler L. J., Parsons R., Randle Y. 2001; Multiple genotypes of St Louis encephalitis virus (Flaviviridae: Flavivirus ) circulate in Harris County, Texas. Am J Trop Med Hyg 64:12–19
     [Google Scholar]
  7. Chen W. J., Wu H. R., Chiou S. S. 2003; E/NS1 modifications of dengue 2 virus after serial passages in mammalian and/or mosquito cells. Intervirology 46:289–295 [CrossRef]
     [Google Scholar]
  8. Ciota A. T., Lovelace A. O., Ngo K. A., Le A. N., Maffei J. G., Franke M. A., Payne A. F., Jones S. A., Kauffman E. B., Kramer L. D. 2007a; Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology 357:165–174 [CrossRef]
     [Google Scholar]
  9. Ciota A. T., Ngo K. A., Lovelace A. O., Payne A. F., Zhou Y., Shi P.-Y., Kramer L. D. 2007b; Role of the mutant spectrum in adaptation and replication of West Nile virus. J Gen Virol 88:865–874 [CrossRef]
     [Google Scholar]
  10. Ciota A. T., Lovelace A. O., Jones S. A., Payne A., Kramer L. D. 2007c; Adaptation of two flaviviruses results in differences in genetic heterogeneity and virus adaptability. J Gen Virol 88:2398–2406 [CrossRef]
     [Google Scholar]
  11. Cooper L. A., Scott T. W. 2001; Differential evolution of eastern equine encephalitis virus populations in response to host cell type. Genetics 157:1403–1412
     [Google Scholar]
  12. Cruz L., Cardenas V. M., Abarca M., Rodriguez T., Reyna R. F., Serpas M. V., Fontaine R. E., Beasley D. W., Da Rosa A. P. other authors 2005; Short report: serological evidence of West Nile virus activity in El Salvador. Am J Trop Med Hyg 72:612–615
     [Google Scholar]
  13. Davis C. T., Ebel G. D., Lanciotti R. S., Brault A. C., Guzman H., Siirin M., Lambert A., Parsons R. E., Beasley D. W. other authors 2005; Phylogenetic analysis of North American West Nile virus isolates, 2001–2004: evidence for the emergence of a dominant genotype. Virology 342:252–265 [CrossRef]
     [Google Scholar]
  14. Day J. F., Stark L. M. 2000; Frequency of Saint Louis encephalitis virus in humans from. Florida, USA: 1990–1999 J Med Entomol 37:626–633 [CrossRef]
     [Google Scholar]
  15. Dupuis A. P., Marra P. P., Reitsma R., Jones M. J., Louie K. L., Kramer L. D. 2005; Serologic evidence for West Nile virus transmission in Puerto Rico and Cuba. Am J Trop Med Hyg 73:474–476
     [Google Scholar]
  16. Ebel G. D., Dupuis A. P., , II, Ngo K. A., Nicholas D., Kauffman E., Jones S. A., Young D., Maffei J., Shi P. Y. other authors 2001; Partial genetic characterization of West Nile virus strains, New York State. Emerg Infect Dis 7:650–653 [CrossRef]
     [Google Scholar]
  17. Ebel G. D., Rochlin I., Longacker J., Kramer L. D. 2005; Culex restuans (Diptera: Culicidae) relative abundance and vector competence for West Nile virus. J Med Entomol 42:838–843 [CrossRef]
     [Google Scholar]
  18. Elizondo-Quiroga D. 2005; West Nile virus isolation in human and mosquitoes, Mexico. Emerg Infect Dis 11:1449–1452
     [Google Scholar]
  19. Granwehr B. P., Lillibridge K. M., Higgs S., Mason P. W., Aronson J. F., Campbell G. A., Barrett A. D. T. 2004; West Nile virus: where are we now?. Lancet Infect Dis 4:547–556 [CrossRef]
     [Google Scholar]
  20. Greene I. P., Wang E., Deardorff E. R., Milleron R., Domingo E., Weaver S. C. 2005; Effect of alternating passage on adaptation of Sindbis virus to vertebrate and invertebrate cells. J Virol 79:14253–14260 [CrossRef]
     [Google Scholar]
  21. Grimstad P. R., Paulson S. L., Craig G. B. Jr 1985; Vector competence of Aedes hendersoni (Diptera: Culicidae) for La Crosse virus and evidence of a salivary-gland escape barrier. J Med Entomol 22:447–453 [CrossRef]
     [Google Scholar]
  22. Higgs S., Snow K., Gould E. A. 2004; The potential for West Nile virus to establish outside of its natural range: a consideration of potential mosquito vectors in the United Kingdom. Trans R Soc Trop Med Hyg 98:82–87 [CrossRef]
     [Google Scholar]
  23. Holland J. J., De La Torre J. C., Clarke D. K., Duarte E. 1991; Quantitation of relative fitness and great adaptability of clonal populations of RNA viruses. J Virol 65:2960–2967
     [Google Scholar]
  24. Jerzak G., Bernard K. A., Kramer L. D., Ebel G. D. 2005; Genetic variation in West Nile virus from naturally infected mosquitoes and birds suggests quasispecies structure and strong purifying selection. J Gen Virol 86:2175–2183 [CrossRef]
     [Google Scholar]
  25. Jerzak G. V., Bernard K., Kramer L. D., Shi P. Y., Ebel G. D. 2007; The West Nile virus mutant spectrum is host-dependant and a determinant of mortality in mice. Virology 360:469–476 [CrossRef]
     [Google Scholar]
  26. Komar N., Langevin S., Hinten S., Nemeth N., Edwards E., Hettler D., Davis B., Bowen R., Bunning M. 2003; Experimental infection of North American birds with the New York 1999 strain of West Nile virus. Emerg Infect Dis 9:311–322 [CrossRef]
     [Google Scholar]
  27. Kramer L. D., Bernard K. A. 2001; West Nile virus infection in birds and mammals. Ann N Y Acad Sci 951:84–93
     [Google Scholar]
  28. Kramer L. D., Chandler L. J. 2001; Phylogenetic analysis of the envelope gene of St Louis encephalitis virus. Arch Virol 146:2341–2355 [CrossRef]
     [Google Scholar]
  29. 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
     [Google Scholar]
  30. Lanciotti R. S., Roehrig J. T., Deubel V., Smith J., Parker M., Steele K., Crise B., Volpe K. E., Crabtree M. B. other authors 1999; Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286:2333–2337 [CrossRef]
     [Google Scholar]
  31. Lenhoff R. J., Luscombe C. A., Summers J. 1998; Competition in vivo between a cytopathic variant and a wild-type duck hepatitis B virus. Virology 251:85–95 [CrossRef]
     [Google Scholar]
  32. Marra P. P., Griffing S. M., McLean R. G. 2003; West Nile virus and wildlife health. Emerg Infect Dis 9:898–899 [CrossRef]
     [Google Scholar]
  33. Marra P. P., Griffing S. M., Caffrey C., Kilpatrick A. M., McLean R., Brand C., Saito E., Dupuis A. P., Kramer L., Novak R. 2004; West Nile virus and wildlife. Bioscience 54:393–402 [CrossRef]
     [Google Scholar]
  34. Monath T. P., Heinz F. X. 1996; Flaviviruses. In Fields Virology . , 3rd edn. pp 961–1034Edited by Fields B. N., Knipe D. M., Howley P. M. Philadelphia: Lippincott Williams and Wilkins;
  35. Morales M. A., Barrandeguy M., Fabbri C., Garcia J. B., Vissani A., Trono K., Gutierrez G., Pigretti S., Menchaca H. other authors 2006; West Nile virus isolation from equines in Argentina, 2006. Emerg Infect Dis 12:1559–1561 [CrossRef]
     [Google Scholar]
  36. Novella I. S., Hershey C. L., Escarmis C., Domingo E., Holland J. J. 1999a; Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287:459–465 [CrossRef]
     [Google Scholar]
  37. Novella I. S., Quer J., Domingo E., Holland J. J. 1999b; Exponential fitness gains of RNA virus populations are limited by bottleneck effects. J Virol 73:1668–1671
     [Google Scholar]
  38. Payne A. F., Binduga-Gajewska I., Kauffman E. B., Kramer L. D. 2006; Quantitation of flaviviruses by fluorescent focus assay. J Virol Methods 134:183–187 [CrossRef]
     [Google Scholar]
  39. Reisen W. K. 2003; Epidemiology of St. Louis encephalitis virus. Adv Virus Res 61:139–183
     [Google Scholar]
  40. Rosen L., Gubler D. 1974; The use of mosquitoes to detect and propagate dengue viruses. Am J Trop Med Hyg 23:1153–1160
     [Google Scholar]
  41. Scherret J. H., MacKenzie J. S., Khromykh A. A., Hall R. A. 2001; Biological significance of glycosylation of the envelope protein of Kunjin virus. Ann N Y Acad Sci 951:361–363
     [Google Scholar]
  42. Scott T. W., Weaver S. C., Mallampalli V. L. 1994; Evolution of mosquito-borne viruses. In The Evolutionary Biology of Viruses pp 293–324Edited by Morse S. S. New York: Raven Press;
     [Google Scholar]
  43. Shirato K., Miyoshi H., Goto A., Ako Y., Ueki T., Kariwa H., Takashima I. 2004; Viral envelope protein glycosylation is a molecular determinant of the neuroinvasiveness of the New York strain of West Nile virus. J Gen Virol 85:3637–3645 [CrossRef]
     [Google Scholar]
  44. Turell M. J., O'Guinn M. L., Dohm D. J., Jones J. W. 2001a; Vector competence of North American mosquitoes (Diptera: Culicidae) for West Nile virus. J Med Entomol 38:130–134 [CrossRef]
     [Google Scholar]
  45. Turell M. J., Sardelis M. R., Dohm D. J., O'Guinn M. L. 2001b; Potential North American vectors of West Nile virus. Ann N Y Acad Sci 951:317–324
     [Google Scholar]
  46. Turell M. J., Dohm D. J., Sardelis M. R., Oguinn M. L., Andreadis T. G., Blow J. A. 2005; An update on the potential of North American mosquitoes (Diptera: Culicidae) to transmit West Nile Virus. J Med Entomol 42:57–62 [CrossRef]
     [Google Scholar]
  47. Weaver S. C., Rico-Hesse R., Scott T. W. 1992; Genetic diversity and slow rates of evolution in New World alphaviruses. Curr Top Microbiol Immunol 176:99–117
     [Google Scholar]
  48. Weaver S. C., Brault A. C., Kang W., Holland J. J. 1999; Genetic and fitness changes accompanying adaptation of an arbovirus to vertebrate and invertebrate cells. J Virol 73:4316–4326
     [Google Scholar]
  49. Woodring J. L., Higgs S., Beaty B. J. 1996; Natural cycles of vector-borne pathogens. In The Biology of Disease Vectors pp 51–72Edited by Beaty B. J., Marquardt W. C. Niwot, CO: University Press of Colorado;
     [Google Scholar]
  50. Zarate S., Novella I. S. 2004; Vesicular stomatitis virus evolution during alternation between persistent infection in insect cells and acute infection in mammalian cells is dominated by the persistence phase. J Virol 78:12236–12242 [CrossRef]
     [Google Scholar]
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Characterization of mosquito-adapted West Nile virus
J. Gen. Virol. 89, 1633 (2008); https://doi.org/10.1099/vir.0.2008/000893-0
/content/journal/jgv/10.1099/vir.0.2008/000893-0
/content/journal/jgv/10.1099/vir.0.2008/000893-0
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