1887

Abstract

The NY99 genotype of (WNV) introduced into North America has demonstrated high virulence for American crows (AMCRs), whilst a closely related WNV strain (KEN-3829) from Kenya exhibits substantially reduced virulence in AMCRs [ Brault, A. C., Langevin, S. A., Bowen, R. A., Panella, N. A., Biggerstaff, B. J., Miller, B. R. & Nicholas, K. (2004) . , 2161–2168]. Viruses rescued from infectious cDNA clones of both the NY99 and KEN-3829 strains demonstrated virulence comparable to that of their parental strains in AMCRs. To begin to define parameters that might explain the different virulence phenotypes between these two viruses, temperature-sensitivity assays were performed for both viruses at the high temperatures experienced in viraemic AMCRs. Growth curves of the two WNV strains were performed in African green monkey kidney (Vero; 37–42 °C) and duck embryonic fibroblast (DEF; 37–45 °C) cells cultured at temperatures that were tolerated by the cell line. Unlike the NY99 virus, marked decreases in KEN-3829 viral titres were detected between 36 and 120 h post-infection (p.i.) at temperatures above 43 °C. Replication of KEN-3829 viral RNA was reduced 6500-fold at 72 h p.i. in DEF cells incubated at 44 °C relative to levels of intracellular virus-specific RNA measured at 37 °C. In contrast, replication of virus derived from the NY99 infectious cDNA at 44 °C demonstrated only a 17-fold reduction in RNA level. These results indicated that the ability of WNV NY99 to replicate at the high temperatures measured in infected AMCRs could be an important factor leading to the increased avian virulence and emergence of this strain of WNV.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.82299-0
2006-12-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jgv/87/12/3611.html?itemId=/content/journal/jgv/10.1099/vir.0.82299-0&mimeType=html&fmt=ahah

References

  1. Anderson J. F., Andreadis T. G., Vossbrinck C. R., Tirrell S., Wakem E. M., French R. A., Garmendia A. E., Van Kruiningen H. J. 1999; Isolation of West Nile virus from mosquitoes, crows, and a Cooper's hawk in Connecticut. Science 286:2331–2333 [CrossRef]
    [Google Scholar]
  2. Beasley D. W., Whiteman M. C., Zhang S. & 7 other authors 2005; Envelope protein glycosylation status influences mouse neuroinvasion phenotype of genetic lineage 1 West Nile virus strains. J Virol 79:8339–8347 [CrossRef]
    [Google Scholar]
  3. Bin H., Grossman Z., Pokamunski S. & 11 other authors 2001; West Nile fever in Israel 1999–2000: from geese to humans. Ann N Y Acad Sci 951:127–142
    [Google Scholar]
  4. Brault A. C., Langevin S. A., Bowen R. A., Panella N. A., Biggerstaff B. J., Miller B. R., Nicholas K. 2004; Differential virulence of West Nile strains for American crows. Emerg Infect Dis 10:2161–2168 [CrossRef]
    [Google Scholar]
  5. Butrapet S., Huang C. Y.-H., Pierro D. J., Bhamarapravati N., Gubler D. J., Kinney R. M. 2000; Attenuation markers of a candidate dengue type 2 vaccine virus, strain 16681 (PDK-53), are defined by mutations in the 5′ noncoding region and nonstructural proteins 1 and 3. J Virol 74:3011–3019 [CrossRef]
    [Google Scholar]
  6. Cabanac M., Aizawa S. 2000; Fever and tachycardia in a bird ( Gallus domesticus ) after simple handling. Physiol Behav 69:541–545 [CrossRef]
    [Google Scholar]
  7. Calvert A. E., Huang C. Y.-H., Kinney R. M., Roehrig J. T. 2006; Non-structural proteins of dengue 2 virus offer limited protection to interferon-deficient mice after dengue 2 virus challenge. J Gen Virol 87:339–346 [CrossRef]
    [Google Scholar]
  8. Charrel R. N., Brault A. C., Gallian P. & 8 other authors 2003; Evolutionary relationship between Old World West Nile virus strains. Evidence for viral gene flow between Africa, the Middle East, and Europe. Virology 315:381–388 [CrossRef]
    [Google Scholar]
  9. Eidson M., Komar N., Sorhage F., Nelson R., Talbot T., Mostashari F., McLean R. & the West Nile Virus Avian Mortality Surveillance Group (2001a). Crow deaths as a sentinel surveillance system for West Nile virus in the northeastern United States, 1999. Emerg Infect Dis 7:615–620 [CrossRef]
    [Google Scholar]
  10. Eidson M., Kramer L., Stone W., Hagiwara Y., Schmit K. & the New York State West Nile Virus Avian Surveillance Team (2001b). Dead bird surveillance as an early warning system for West Nile virus. Emerg Infect Dis 7:631–635 [CrossRef]
    [Google Scholar]
  11. Eidson M., Miller J., Kramer L., Cherry B., Hagiwara Y. & the West Nile Virus Bird Mortality Analysis Group (2001c). Dead crow densities and human cases of West Nile virus. New York State 2000 Emerg Infect Dis 7:662–664 [CrossRef]
    [Google Scholar]
  12. Fredericksen B. L., Gale M., Jr. 2006; West Nile virus evades activation of interferon regulatory factor 3 through RIG-I-dependent and -independent pathways without antagonizing host defense signaling. J Virol 80:2913–2923 [CrossRef]
    [Google Scholar]
  13. Fredericksen B. L., Smith M., Katze M. G., Shi P.-Y., Gale M., Jr. 2004; The host response to West Nile virus infection limits viral spread through the activation of the interferon regulatory factor 3 pathway. J Virol 78:7737–7747 [CrossRef]
    [Google Scholar]
  14. 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]
  15. Huang C. Y.-H., Butrapet S., Tsuchiya K. R., Bhamarapravati N., Gubler D. J., Kinney R. M. 2003; Dengue 2 PDK-53 virus as a chimeric carrier for tetravalent dengue vaccine development. J Virol 77:11436–11447 [CrossRef]
    [Google Scholar]
  16. Huang C. Y.-H., Silengo S. J., Whiteman M. C., Kinney R. M. 2005; Chimeric dengue 2 PDK-53/West Nile NY99 viruses retain the phenotypic attenuation markers of the candidate PDK-53 vaccine virus and protect mice against lethal challenge with West Nile virus. J Virol 79:7300–7310 [CrossRef]
    [Google Scholar]
  17. Kendeigh S. C. 1969; Energy responses of birds to their thermal environments. Wilson Bull 81:441–449
    [Google Scholar]
  18. Kinney R. M., Butrapet S., Chang G.-J. J., Tsuchiya K. R., Roehrig J. T., Bhamarapravati N., Gubler D. J. 1997; Construction of infectious cDNA clones for dengue 2 virus: strain 16681 and its attenuated vaccine derivative, strain PDK-53. Virology 230:300–308 [CrossRef]
    [Google Scholar]
  19. 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]
  20. Lanciotti R. S., Roehrig J. T., Deubel V. & 21 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]
  21. Langevin S. A., Arroyo J., Monath T. P., Komar N. 2003; Host-range restriction of chimeric yellow fever-West Nile vaccine in fish crows ( Corvus ossifragus ). Am J Trop Med Hyg 69:78–80
    [Google Scholar]
  22. Langevin S. A., Brault A. C., Panella N. A., Bowen R. A., Komar N. 2005; Variation in virulence of West Nile virus strains for house sparrows ( Passer domesticus ). Am J Trop Med Hyg 72:99–102
    [Google Scholar]
  23. Li J., Bhuvanakantham R., Howe J., Ng M.-L. 2005; Identifying the region influencing the cis -mode of maturation of West Nile (Sarafend) virus using chimeric infectious clones. Biochem Biophys Res Commun 334:714–720 [CrossRef]
    [Google Scholar]
  24. Lindenbach B., Rice C. M. 2003; Structure and replication: molecular biology of the flaviviruses. In The Flaviviruses: Structure, Replication and Evolution Edited by Chambers T. J., Monath T. London: Elsevier;
    [Google Scholar]
  25. Liu W. J., Chen H. B., Wang X. J., Huang H., Khromykh A. A. 2004; Analysis of adaptive mutations in Kunjin virus replicon RNA reveals a novel role for the flavivirus nonstructural protein NS2A in inhibition of beta interferon promoter-driven transcription. J Virol 78:12225–12235 [CrossRef]
    [Google Scholar]
  26. Liu W. J., Wang X. J., Mokhonov V. V., Shi P.-Y., Randall R., Khromykh A. A. 2005; Inhibition of interferon signaling by the New York 99 strain and Kunjin subtype of West Nile virus involves blockage of STAT1 and STAT2 activation by nonstructural proteins. J Virol 79:1934–1942 [CrossRef]
    [Google Scholar]
  27. Liu W. J., Wang X. J., Clark D. C., Lobigs M., Hall R. A., Khromykh A. A. 2006; A single amino acid substitution in the West Nile virus nonstructural protein NS2A disables its ability to inhibit alpha/beta interferon induction and attenuates virus virulence in mice. J Virol 80:2396–2404 [CrossRef]
    [Google Scholar]
  28. Malkinson M., Banet C., Weisman Y., Pokamunski S., King R., Drouet M. T., Deubel V. 2002; Introduction of West Nile virus in the Middle East by migrating white storks. Emerg Infect Dis 8:392–397 [CrossRef]
    [Google Scholar]
  29. McLean R. G., Ubico S. R., Docherty D. E., Hansen W. R., Sileo L., McNamara T. S. 2001; West Nile virus transmission and ecology in birds. Ann N Y Acad Sci 951:54–57
    [Google Scholar]
  30. Miller B. R., Nasci R. S., Godsey M. S., Savage H. M., Lutwama J. J., Lanciotti R. S., Peters C. J. 2000; First field evidence for natural vertical transmission of West Nile virus in Culex univittatus complex mosquitoes from Rift Valley province, Kenya. Am J Trop Med Hyg 62:240–246
    [Google Scholar]
  31. Munir S., Sharma J. M., Kapur V. 2005; Transcriptional response of avian cells to infection with Newcastle disease virus. Virus Res 107:103–108 [CrossRef]
    [Google Scholar]
  32. Muñoz-Jordán J. L., Sánchez-Burgos G. G., Laurent-Rolle M., García-Sastre A. 2003; Inhibition of interferon signaling by dengue virus. Proc Natl Acad Sci U S A 100:14333–14338 [CrossRef]
    [Google Scholar]
  33. O'Leary D. R., Marfin A. A., Montgomery S. P. & 7 other authors 2004; The epidemic of West Nile virus in the United States, 2002. Vector Borne Zoonotic Dis 4:61–70 [CrossRef]
    [Google Scholar]
  34. Page L. 1965; High body temperature of pigeons and sparrows as a factor in their resistance to an agent of the psittacosis group. J Wildl Dis 1:49–53 [CrossRef]
    [Google Scholar]
  35. Panella N. A., Kerst A. J., Lanciotti R. S., Bryant P., Wolf B., Komar N. 2001; Comparative West Nile virus detection in organs of naturally infected American crows ( Corvus brachyrhynchos ). Emerg Infect Dis 7:754–755 [CrossRef]
    [Google Scholar]
  36. Pletnev A. G., Putnak R., Speicher J., Wagar E. J., Vaughn D. W. 2002; West Nile virus/dengue type 4 virus chimeras that are reduced in neurovirulence and peripheral virulence without loss of immunogenicity or protective efficacy. Proc Natl Acad Sci U S A 99:3036–3041 [CrossRef]
    [Google Scholar]
  37. Sen G. C. 2001; Viruses and interferons. Annu Rev Microbiol 55:255–281 [CrossRef]
    [Google Scholar]
  38. Shi P.-Y., Tilgner M., Lo M. K., Kent K. A., Bernard K. A. 2002; Infectious cDNA clone of the epidemic West Nile virus from New York City. J Virol 76:5847–5856 [CrossRef]
    [Google Scholar]
  39. Steele K. E., Linn M. J., Schoepp R. J. & 11 other authors 2000; Pathology of fatal West Nile virus infections in native and exotic birds during the 1999 outbreak in New York City, New York. Vet Pathol 37:208–224 [CrossRef]
    [Google Scholar]
  40. Torre-Bueno J. R. 1976; Temperature regulation and heat dissipation during flight in birds. J Exp Biol 65:471–482
    [Google Scholar]
  41. Verbeek N., Caffrey C. 2002; American crow ( Corvus brachyrhynchos . In The Birds of North America pp  1–35 Edited by Poole A., Gill F. Philadelphia, PA: The Birds of North America, Inc;
    [Google Scholar]
  42. Watson J. T., Jones R. C., Gibbs K., Paul W. 2004; Dead crow reports and location of human West Nile virus cases. Chicago: 2002 Emerg Infect Dis 10:938–940 [CrossRef]
    [Google Scholar]
  43. Weingartl H. M., Neufeld J. L., Copps J., Marszal P. 2004; Experimental West Nile virus infection in blue jays ( Cyanocitta cristata ) and crows ( Corvus brachyrhynchos ). Vet Pathol 41:362–370 [CrossRef]
    [Google Scholar]
  44. Wunschmann A., Shivers J., Carroll L., Bender J. 2004; Pathological and immunohistochemical findings in American crows ( Corvus brachyrhynchos ) naturally infected with West Nile virus. J Vet Diagn Invest 16:329–333 [CrossRef]
    [Google Scholar]
  45. Yamshchikov V. F., Wengler G., Perelygin A. A., Brinton M. A., Compans R. W. 2001; An infectious clone of the West Nile flavivirus. Virology 281:294–304 [CrossRef]
    [Google Scholar]
  46. Yaremych S. A., Warner R. E., Mankin P. C., Brawn J. D., Raim A., Novak R. 2004; West Nile virus and high death rate in American crows. Emerg Infect Dis 10:709–711 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.82299-0
Loading
/content/journal/jgv/10.1099/vir.0.82299-0
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