1887

Abstract

(WNV) has successfully spread throughout the USA, Canada, Mexico, the Caribbean and parts of Central and South America since its 1999 introduction into North America. Despite infecting a broad range of both mosquito and avian species, the virus remains highly genetically conserved. This lack of evolutionary change over space and time is common with many arboviruses and is frequently attributed to the adaptive constraints resulting from the virus cycling between vertebrate hosts and invertebrate vectors. WNV, like most RNA viruses studied thus far, has been shown in nature to exist as a highly genetically diverse population of genotypes. Few studies have directly evaluated the role of these mutant spectra in viral fitness and adaptation. Using clonal analysis and reverse genetics experiments, this study evaluated genotype diversity and the importance of consensus change in producing the adaptive phenotype of WNV following sequential mosquito cell passage. The results indicated that increases in the replicative ability of WNV in mosquito cells correlate with increases in the size of the mutant spectrum, and that consensus change is not solely responsible for alterations in viral fitness and adaptation of WNV. These data provide evidence of the importance of quasispecies dynamics in the adaptation of a flavivirus to new and changing environments and hosts, with little evidence of significant genetic change.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82606-0
2007-03-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/88/3/865.html?itemId=/content/journal/jgv/10.1099/vir.0.82606-0&mimeType=html&fmt=ahah

References

  1. Aaskov J., Buzacott K., Thu H. M., Lowry K., Holmes E. C. 2006; Long-term transmission of defective RNA viruses in humans and Aedes mosquitoes. Science 311:236–238 [CrossRef]
    [Google Scholar]
  2. Anderson J. F., Vossbrinck C. R., Andreadis T. G., Iton A., Beckwith W. H., Mayo D. R. 2001; Characterization of West Nile virus from five species of mosquitoes, nine species of birds, and one mammal. Ann N Y Acad Sci 951:328–331
    [Google Scholar]
  3. Arias A., Lazaro E., Escarmis C., Domingo E. 2001; Molecular intermediates of fitness gain of an RNA virus: characterization of a mutant spectrum by biological and molecular cloning. J Gen Virol 82:1049–1060
    [Google Scholar]
  4. Arias A., Ruiz-Jarabo C. M., Escarmis C., Domingo E. 2004; Fitness increase of memory genomes in a viral quasispecies. J Mol Biol 339:405–412 [CrossRef]
    [Google Scholar]
  5. 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]
  6. Beasley D. W., Davis C. T., Guzman H., Vanlandingham D. L., Travassos da Rosa A. P. A., Parsons R. E., Higgs S., Tesh R. B., Barrett A. D. T. 2003; Limited evolution of West Nile virus has occurred during its southwesterly spread in the United States. Virology 309:190–195 [CrossRef]
    [Google Scholar]
  7. 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]
  8. 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]
  9. Cilnis M. J., Kang W., Weaver S. C. 1996; Genetic conservation of Highlands J viruses. Virology 218:343–351 [CrossRef]
    [Google Scholar]
  10. 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. 2007; Cell-specific adaptation of two flaviviruses following serial passage in mosquito cell culture. Virology 357:165–174 [CrossRef]
    [Google Scholar]
  11. 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. 2005; Short report: serological evidence of West Nile virus activity in El Salvador. Am J Trop Med Hyg 72:612–615
    [Google Scholar]
  12. Davis C. T., Ebel G. D., Lanciotti R. S., Brault A. C., Guzman H., Siirin M., Lambert A., Parsons R. E., Beasley D. W. 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]
  13. Domingo E., Escarmis C., Sevilla N., Baranowski E. 1998; Population dynamics in the evolution of RNA viruses. Adv Exp Med Biol 440:721–727
    [Google Scholar]
  14. Drake J. W., Holland J. J. 1999; Mutation rates among RNA viruses. Proc Natl Acad Sci U S A 96:13910–13913 [CrossRef]
    [Google Scholar]
  15. Duarte E. A., Novella I. S., Ledesma S., Clarke D. K., Moya A., Elena S. F., Domingo E., Holland J. J. 1994; Subclonal components of consensus fitness in an RNA virus clone. J Virol 68:4295–4301
    [Google Scholar]
  16. Dupuis A. P. II, Marra P. P., Kramer L. D. 2003; Serologic evidence of West Nile virus transmission, Jamaica, West Indies. Emerg Infect Dis 9:860–863 [CrossRef]
    [Google Scholar]
  17. Dupuis A. P. II, 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]
  18. 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]
  19. Ebel G. D., Carricaburu J., Young D., Bernard K. A., Kramer L. D. 2004; Genetic and phenotypic variation of West Nile virus in New York, 2000–2003. Am J Trop Med Hyg 71:493–500
    [Google Scholar]
  20. Eigen M. 1993; Viral quasispecies. Sci Am 269:42–49
    [Google Scholar]
  21. Eigen M., Biebricher D. K. 1988; Sequence space and quasispecies distribution. In RNA Genetics pp 211–245 Edited by Domingo E., Holland J. J., Ahlquist P. Boca Raton, FL: CRC Press;
    [Google Scholar]
  22. Elizondo-Quiroga D., Davis C. T., Fernandez-Salas I., Escobar-Lopez R., Olmos D. V., Gastalum L. C. S., Acosta M. A., Elizondo-Quiroga A., Gonzalez-Rojas J. I. other authors 2005; West Nile virus isolation in human and mosquitoes, Mexico. Emerg Infect Dis 11:1449–1452
    [Google Scholar]
  23. Farci P., Shimoda A., Coiana A., Diaz G., Peddis G., Melpolder J. C., Strazzera A., Chien D. Y., Munoz S. J. other authors 2000; The outcome of acute hepatitis C predicted by the evolution of the viral quasispecies. Science 288:339–344 [CrossRef]
    [Google Scholar]
  24. Farci P., Strazzera R., Alter H. J., Farci S., Degioannis D., Coiana A., Peddis G., Usai F., Serra G. other authors 2002; Early changes in hepatitis C viral quasispecies during interferon therapy predict the therapeutic outcome. Proc Natl Acad Sci U S A 99:3081–3086 [CrossRef]
    [Google Scholar]
  25. Frost S. D. W., Wrin T., Smith D. M., Kosakovsky Pond S. L., Liu Y., Paxinos E., Chappey C., Galovich J., Beauchaine J. other authors 2005; Neutralizing antibody responses drive the evolution of human immunodeficiency virus type 1 envelope during recent HIV infection. Proc Natl Acad Sci U S A 102:18514–18519 [CrossRef]
    [Google Scholar]
  26. Geffin R., Hutto C., Andrew C., Scott G. B. 2003; A longitudinal assessment of autologous neutralizing antibodies in children perinatally infected with human immunodeficiency virus type 1. Virology 310:207–215 [CrossRef]
    [Google Scholar]
  27. 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]
  28. 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]
  29. Hayes E. B., Komar N., Nasci R. S., Montgomery S. P., O'Leary D. R., Campbell G. L. 2005; Epidemiology and transmission dynamics of West Nile virus disease. Emerg Infect Dis 11:1167–1173 [CrossRef]
    [Google Scholar]
  30. 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]
  31. Holland J. J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. 1982; Rapid evolution of RNA genomes. Science 215:1577–1585 [CrossRef]
    [Google Scholar]
  32. Holmes E. C. 2003; Patterns of intra- and interhost nonsynonymous variation reveal strong purifying selection in dengue virus. J Virol 77:11296–11298 [CrossRef]
    [Google Scholar]
  33. Holmes E. C., Moya A. 2002; Is the quasispecies concept relevant to RNA viruses?. J Virol 76:460–465 [CrossRef]
    [Google Scholar]
  34. Holmes E. C., Worobey M., Rambaut A. 1999; Phylogenetic evidence for recombination in dengue virus. Mol Biol Evol 16:405–409 [CrossRef]
    [Google Scholar]
  35. Jenkins G. M., Rambaut A., Pybus O. G., Holmes E. C. 2002; Rates of molecular evolution in RNA viruses: a quantitative phylogenetic analysis. J Mol Evol 54:156–165 [CrossRef]
    [Google Scholar]
  36. 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]
  37. Kramer L. D., Bernard K. A. 2001; West Nile virus in the western hemisphere. Curr Opin Infect Dis 14:519–525 [CrossRef]
    [Google Scholar]
  38. Lanciotti R. S., Ebel G. D., Deubel V., Kerst A. J., Murri S., Meyer R., Bowen M., McKinney N., Morrill W. E. other authors 2002; Complete genome sequences and phylogenetic analysis of West Nile virus strains isolated from the United States, Europe, and the Middle East. Virology 298:96–105 [CrossRef]
    [Google Scholar]
  39. 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]
  40. Martinez M. A., Carrillo C., Gonzalez-Candelas F., Moya A., Domingo E., Sobrino F. 1991; Fitness alteration of foot-and-mouth disease virus mutants: measurement of adaptability of viral quasispecies. J Virol 65:3954–3957
    [Google Scholar]
  41. 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]
  42. Novella I. S., Ebendick-Corpus B. E. 2004; Molecular basis of fitness loss and fitness recovery in vesicular stomatitis virus. J Mol Biol 342:1423–1430 [CrossRef]
    [Google Scholar]
  43. Novella I. S., Hershey C. L., Escarmis C., Domingo E., Holland J. J. 1999; Lack of evolutionary stasis during alternating replication of an arbovirus in insect and mammalian cells. J Mol Biol 287:459–465 [CrossRef]
    [Google Scholar]
  44. 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]
  45. Rozas J., Rozas R. 1999; DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15:174–175 [CrossRef]
    [Google Scholar]
  46. Ruiz-Jarabo C. M., Arias A., Baranowski E., Escarmis C., Domingo E. 2000; Memory in viral quasispecies. J Virol 74:3543–3547 [CrossRef]
    [Google Scholar]
  47. Ruiz-Jarabo C. M., Arias A., Molina-Paris C., Briones C., Baranowski E., Escarmis C., Domingo E. 2002; Duration and fitness dependence of quasispecies memory. J Mol Biol 315:285–296 [CrossRef]
    [Google Scholar]
  48. Sauder C. J., Vandenburgh K. M., Iskow R. C., Malik T., Carbone K. M., Rubin S. A. 2006; Changes in mumps virus neurovirulence phenotype associated with quasispecies heterogeneity. Virology 350:48–57 [CrossRef]
    [Google Scholar]
  49. 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]
  50. Schneider W. L., Roossinck M. J. 2001; Genetic diversity in RNA virus quasispecies is controlled by host–virus interactions. J Virol 75:6566–6571 [CrossRef]
    [Google Scholar]
  51. Scott T. W., Weaver S. C., Mallampalli V. L. 1994; Evolution of mosquito-borne viruses. In The Evolutionary Biology of Viruses pp 293–324 Edited by Morse S. S. New York: Raven Press Ltd;
    [Google Scholar]
  52. Shi P.--Y., Tilgner M., Lo M. K. 2002; a Construction and characterization of subgenomic replicons of New York strain of West Nile virus. Virology 296:219–233 [CrossRef]
    [Google Scholar]
  53. Shi P.-Y., Tilgner M., Lo M. K., Kent K. A., Bernard K. A. 2002; b Infectious cDNA clone of the epidemic West Nile virus from New York City. J Virol 76:5847–5856 [CrossRef]
    [Google Scholar]
  54. Twiddy S. S., Holmes E. C. 2003; The extent of recombination in members of the genus Flavivirus . J Gen Virol 84:429–440 [CrossRef]
    [Google Scholar]
  55. Vignuzzi M., Stone J. K., Arnold J. J., Cameron C. E., Andino R. 2006; Quasispecies diversity determines pathogenesis through cooperative interactions in a viral population. Nature 439:344–348 [CrossRef]
    [Google Scholar]
  56. 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]
  57. 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]
  58. Weiner A., Erickson A. L., Kansopon J., Crawford K., Muchmore E., Hughes A. L., Houghton M., Walker C. M. 1995; Persistent hepatitis C virus infection in a chimpanzee is associated with emergence of a Cytotoxic T Lymphocyte escape variant. Proc Natl Acad Sci U S A 92:2755–2759 [CrossRef]
    [Google Scholar]
  59. Woelk C. H., Holmes E. C. 2002; Reduced positive selection in vector-borne RNA viruses. Mol Biol Evol 19:2333–2336 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82606-0
Loading
/content/journal/jgv/10.1099/vir.0.82606-0
Loading

Data & Media loading...

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