1887

Abstract

West Nile virus (WNV) occurs as a population of genetic variants (quasispecies) infecting a single animal. Previous low-resolution viral genetic diversity estimates in sampled wild birds and mosquitoes, and in multiple-passage adaptation studies or in cell culture, suggest that WNV genetic diversification is mostly limited to the mosquito vector. This study investigated genetic diversification of WNV in avian hosts during a single passage using next-generation sequencing. Wild-captured carrion crows were subcutaneously infected using a clonal Middle-East WNV. Blood samples were collected 2 and 4 days post-infection. A reverse-transcription (RT)-PCR approach was used to amplify the WNV genome directly from serum samples prior to next-generation sequencing resulting in an average depth of at least 700 ×  in each sample. Appropriate controls were sequenced to discriminate biologically relevant low-frequency variants from experimentally introduced errors. The WNV populations in the wild crows showed significant diversification away from the inoculum virus quasispecies structure. By contrast, WNV populations in intracerebrally infected day-old chickens did not diversify from that of the inoculum. Where previous studies concluded that WNV genetic diversification is only experimentally demonstrated in its permissive insect vector species, we have experimentally shown significant diversification of WNV populations in a wild bird reservoir species.

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2015-10-01
2024-03-28
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References

  1. Anthony K.G., Bai F., Krishnan M.N., Fikrig E., Koski R.A. 2009; Effective siRNA targeting of the 3′ untranslated region of the West Nile virus genome. Antiviral Res 82:166–168 [View Article][PubMed]
    [Google Scholar]
  2. Bahuon C., Desprès P., Pardigon N., Panthier J.J., Cordonnier N., Lowenski S., Richardson J., Zientara S., Lecollinet S. 2012; IS-98-ST1 West Nile virus derived from an infectious cDNA clone retains neuroinvasiveness and neurovirulence properties of the original virus. PLoS One 7:e47666 [View Article][PubMed]
    [Google Scholar]
  3. Barzon L., Lavezzo E., Militello V., Toppo S., Palù G. 2011; Applications of next-generation sequencing technologies to diagnostic virology. Int J Mol Sci 12:7861–7884 [View Article][PubMed]
    [Google Scholar]
  4. Brackney D.E., Beane J.E., Ebel G.D. 2009; RNAi targeting of West Nile virus in mosquito midguts promotes virus diversification. PLoS Pathog 5:e1000502 [View Article][PubMed]
    [Google Scholar]
  5. Brinton M.A. 2014; Replication cycle and molecular biology of the West Nile virus. Viruses 6:13–53 [View Article][PubMed]
    [Google Scholar]
  6. Brinton M.A., Dispoto J.H. 1988; Sequence and secondary structure analysis of the 5′-terminal region of flavivirus genome RNA. Virology 162:290–299 [View Article][PubMed]
    [Google Scholar]
  7. Brinton M.A., Fernandez A.V., Dispoto J.H. 1986; The 3′-nucleotides of flavivirus genomic RNA form a conserved secondary structure. Virology 153:113–121 [View Article][PubMed]
    [Google Scholar]
  8. Bunnik E.M., Pisas L., van Nuenen A.C., Schuitemaker H. 2008; Autologous neutralizing humoral immunity and evolution of the viral envelope in the course of subtype B human immunodeficiency virus type 1 infection. J Virol 82:7932–7941 [View Article][PubMed]
    [Google Scholar]
  9. Campbell C.L., Keene K.M., Brackney D.E., Olson K.E., Blair C.D., Wilusz J., Foy B.D. 2008; Aedes aegypti uses RNA interference in defense against Sindbis virus infection. BMC Microbiol 8:47 [View Article][PubMed]
    [Google Scholar]
  10. Coia G., Parker M.D., Speight G., Byrne M.E., Westaway E.G. 1988; Nucleotide and complete amino acid sequences of Kunjin virus: definitive gene order and characteristics of the virus-specified proteins. J Gen Virol 69:1–21 [View Article][PubMed]
    [Google Scholar]
  11. Deardorff E.R., Fitzpatrick K.A., Jerzak G.V.S., Shi P.Y., Kramer L.D., Ebel G.D. 2011; West Nile virus experimental evolution in vivo and the trade-off hypothesis. PLoS Pathog 7:e1002335 [View Article][PubMed]
    [Google Scholar]
  12. Deas T.S., Binduga-Gajewska I., Tilgner M., Ren P., Stein D.A., Moulton H.M., Iversen P.L., Kauffman E.B., Kramer L.D., Shi P.-Y. 2005; Inhibition of flavivirus infections by antisense oligomers specifically suppressing viral translation and RNA replication. J Virol 79:4599–4609 [View Article][PubMed]
    [Google Scholar]
  13. Deas T.S., Bennett C.J., Jones S.A., Tilgner M., Ren P., Behr M.J., Stein D.A., Iversen P.L., Kramer L.D., other authors. 2007; In vitro resistance selection and in vivo efficacy of morpholino oligomers against West Nile virus. Antimicrob Agents Chemother 51:2470–2482 [View Article][PubMed]
    [Google Scholar]
  14. Dridi M., Rauw F., Muylkens B., Lecollinet S., van den Berg T., Lambrecht B. 2013; Setting up a SPF chicken model for the pathotyping of West Nile virus (WNV) strains. Transbound Emerg Dis 60:(Suppl. 2)51–62 [View Article][PubMed]
    [Google Scholar]
  15. Ebel G.D., Fitzpatrick K.A., Lim P.-Y., Bennett C.J., Deardorff E.R., Jerzak G.V.S., Kramer L.D., Zhou Y., Shi P.-Y., Bernard K.A. 2011; Nonconsensus West Nile virus genomes arising during mosquito infection suppress pathogenesis and modulate virus fitness in vivo. J Virol 85:12605–12613 [View Article][PubMed]
    [Google Scholar]
  16. Eigen M., Schuster P. 1978; The Hypercycle. Naturwissenschaften 65:7–41 [View Article]
    [Google Scholar]
  17. Elghonemy S., Davis W.G., Brinton M.A. 2005; The majority of the nucleotides in the top loop of the genomic 3′ terminal stem loop structure are cis-acting in a West Nile virus infectious clone. Virology 331:238–246 [View Article][PubMed]
    [Google Scholar]
  18. Grubaugh N.D., Smith D.R., Brackney D.E., Bosco-Lauth A.M., Fauver J.R., Campbell C.L., Felix T.A., Romo H., Duggal N.K., other authors. 2015; Experimental evolution of an RNA virus in wild birds: evidence for host-dependent impacts on population structure and competitive fitness. PLoS Pathog 11:e1004874[PubMed] [CrossRef]
    [Google Scholar]
  19. Henn M.R., Boutwell C.L., Charlebois P., Lennon N.J., Power K.A., Macalalad A.R., Berlin A.M., Malboeuf C.M., Ryan E.M., other authors. 2012; Whole genome deep sequencing of HIV-1 reveals the impact of early minor variants upon immune recognition during acute infection. PLoS Pathog 8:e1002529 [View Article][PubMed]
    [Google Scholar]
  20. Holland J., Spindler K., Horodyski F., Grabau E., Nichol S., VandePol S. 1982; Rapid evolution of RNA genomes. Science 215:1577–1585 [View Article][PubMed]
    [Google Scholar]
  21. Hubálek Z., Halouzka J. 1999; West Nile fever—a reemerging mosquito-borne viral disease in Europe. Emerg Infect Dis 5:643–650[PubMed] [CrossRef]
    [Google Scholar]
  22. 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 [View Article][PubMed]
    [Google Scholar]
  23. Jerzak G.V.S., 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 [View Article][PubMed]
    [Google Scholar]
  24. Jerzak G.V.S., Brown I., Shi P.Y., Kramer L.D., Ebel G.D. 2008; Genetic diversity and purifying selection in West Nile virus populations are maintained during host switching. Virology 374:256–260 [View Article][PubMed]
    [Google Scholar]
  25. Joshi N.A., Fass J.N. 2011; Sickle: A sliding-window, adaptive, quality-based trimming tool for FastQ files (version 1.33). Available at https://github.com/najoshi/sickle
  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 [View Article][PubMed]
    [Google Scholar]
  27. Li X.-F., Jiang T., Yu X.-D., Deng Y.-Q., Zhao H., Zhu Q.-Y., Qin E.-D., Qin C.-F. 2010; RNA elements within the 5′ untranslated region of the West Nile virus genome are critical for RNA synthesis and virus replication. J Gen Virol 91:1218–1223 [View Article][PubMed]
    [Google Scholar]
  28. Manzin A., Solforosi L., Petrelli E., Macarri G., Tosone G., Piazza M., Clementi M. 1998; Evolution of hypervariable region 1 of hepatitis C virus in primary infection. J Virol 72:6271–6276[PubMed]
    [Google Scholar]
  29. Murray K.O., Mertens E., Desprès P. 2010; West Nile virus and its emergence in the United States of America. Vet Res 41:67 [View Article][PubMed]
    [Google Scholar]
  30. Myles K.M., Wiley M.R., Morazzani E.M., Adelman Z.N. 2008; Alphavirus-derived small RNAs modulate pathogenesis in disease vector mosquitoes. Proc Natl Acad Sci U S A 105:19938–19943 [View Article][PubMed]
    [Google Scholar]
  31. Pfeffer M., Dobler G. 2010; Emergence of zoonotic arboviruses by animal trade and migration. Parasit Vectors 3:35 [View Article][PubMed]
    [Google Scholar]
  32. Phipps L.P., Gough R.E., Ceeraz V., Cox W.J., Brown I.H. 2007; Detection of West Nile virus in the tissues of specific pathogen free chickens and serological response to laboratory infection: a comparative study. Avian Pathol 36:301–305 [View Article][PubMed]
    [Google Scholar]
  33. R Core Team 2014; R: A language and environment for statistical computing. R Found Stat Comput Vienna, Austria http://www.R-project.org/
    [Google Scholar]
  34. Senne D.A., Pedersen J.C., Hutto D.L., Taylor W.D., Schmitt B.J., Panigrahy B. 2000; Pathogenicity of West Nile virus in chickens. Avian Dis 44:642–649 [View Article][PubMed]
    [Google Scholar]
  35. Shirafuji H., Kanehira K., Kubo M., Shibahara T., Kamio T. 2009; Experimental West Nile virus infection in Aigamo ducks, a cross between wild ducks (Anas platyrhynchos) and domestic ducks (Anas platyrhynchos var. domesticus). Avian Dis 53:239–244 [View Article][PubMed]
    [Google Scholar]
  36. Smits J.E.G., Bortolotti G.R. 2008; Immunological development in nestling American kestrels Falco sparverius: post-hatching ontogeny of the antibody response. Comp Biochem Physiol A Mol Integr Physiol 151:711–716 [View Article][PubMed]
    [Google Scholar]
  37. Tang Y., Liu B., Hapip C.A., Xu D., Fang C.T. 2008; Genetic analysis of West Nile virus isolates from US blood donors during 2002-2005. J Clin Virol 43:292–297 [View Article][PubMed]
    [Google Scholar]
  38. Totani M., Yoshii K., Kariwa H., Takashima I. 2011; Glycosylation of the envelope protein of West Nile virus affects its replication in chicks. Avian Dis 55:561–568 [CrossRef]
    [Google Scholar]
  39. Turell M.J., O'Guinn M.L., Jones J.W., Sardelis M.R., Dohm D.J., Watts D.M., Fernandez R., Travassos da Rosa A., Guzman H., other authors. 2005; Isolation of viruses from mosquitoes (Diptera: Culicidae) collected in the Amazon Basin region of Peru. J Med Entomol 42:891–898 [View Article][PubMed]
    [Google Scholar]
  40. Van Borm S., Belák S., Freimanis G., Fusaro A., Granberg F., Höper D., King D.P., Monne I., Orton R., Rosseel T. 2015; Next-generation sequencing in veterinary medicine: how can the massive amount of information arising from high-throughput technologies improve diagnosis, control, and management of infectious diseases?. Methods Mol Biol 1247:415–436 [View Article][PubMed]
    [Google Scholar]
  41. Van der Meulen K.M., Pensaert M.B., Nauwynck H.J. 2005; West Nile virus in the vertebrate world. Arch Virol 150:637–657 [View Article][PubMed]
    [Google Scholar]
  42. Van Slyke G.A., Ciota A.T., Willsey G.G., Jaeger J., Shi P.Y., Kramer L.D. 2012; Point mutations in the West Nile virus (Flaviviridae, Flavivirus) RNA-dependent RNA polymerase alter viral fitness in a host-dependent manner in vitro and in vivo . Virology 427:18–24 [View Article][PubMed]
    [Google Scholar]
  43. 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 [View Article][PubMed]
    [Google Scholar]
  44. Villarreal L.P., Witzany G. 2013; Rethinking quasispecies theory: from fittest type to cooperative consortia. World J Biol Chem 4:79–90[PubMed]
    [Google Scholar]
  45. Westerdahl H., Wittzell H., von Schantz T., Bensch S. 2004; MHC class I typing in a songbird with numerous loci and high polymorphism using motif-specific PCR and DGGE. Heredity (Edinb) 92:534–542 [View Article][PubMed]
    [Google Scholar]
  46. Wheeler S.S., Barker C.M., Fang Y., Armijos M.V., Carroll B.D., Husted S., Johnson W.O., Reisen W.K. 2009; Differential impact of West Nile virus on California birds. Condor 111:1–20 [View Article][PubMed]
    [Google Scholar]
  47. Wilm A., Aw P.P.K., Bertrand D., Yeo G.H.T., Ong S.H., Wong C.H., Khor C.C., Petric R., Hibberd M.L., Nagarajan N. 2012; LoFreq: a sequence-quality aware, ultra-sensitive variant caller for uncovering cell-population heterogeneity from high-throughput sequencing datasets. Nucleic Acids Res 40:11189–11201 [View Article][PubMed]
    [Google Scholar]
  48. Yang X., Charlebois P., Macalalad A., Henn M.R., Zody M.C. 2013; V-Phaser 2: variant inference for viral populations. BMC Genomics 14:674 [View Article][PubMed]
    [Google Scholar]
  49. Yu L., Markoff L. 2005; The topology of bulges in the long stem of the flavivirus 3′ stem-loop is a major determinant of RNA replication competence. J Virol 79:2309–2324 [View Article][PubMed]
    [Google Scholar]
  50. Zhang Q., Hill G.E., Edwards S.V., Backström N. 2014; A house finch (Haemorhous mexicanus) spleen transcriptome reveals intra- and interspecific patterns of gene expression, alternative splicing and genetic diversity in passerines. BMC Genomics 15:305 [View Article][PubMed]
    [Google Scholar]
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