1887

Abstract

The attenuated West Nile virus 25A strain (WN25A) was investigated for its neuroinvasive properties in B-cell-deficient (μMT) mice. After peripheral inoculation, WN25A caused fatal encephalitis in the majority of 6–8-week-old mice, characterized by a systemic infection with viraemia, moderate virus burdens in peripheral tissues and a high titre of brain-associated virus. Mice generally succumbed to infection within a few weeks of infection. However, others survived for as long as 10 weeks, and some for even longer. Normal age-matched C57BL/6 mice showed no signs of illness after inoculation with WN25A virus. Nucleotide sequencing of WN25A viruses recovered from the brains of B-cell-deficient mice revealed that the conserved -linked glycosylation site in the viral envelope protein was abolished by substitution of a serine residue at position 155. This was found to be a pseudoreversion relative to the wild-type WN-Israel strain, based on virulence testing of one such brain-associated virus in both B-cell-deficient and normal C57BL/6 mice. This study provides further characterization of the mouse virulence properties of the attenuated WN25A virus in the context of B-cell deficiency. Replication in these mice does not involve rapid neuroadaptation or reversion of WN25A virus to a neuroinvasive phenotype. Molecular modelling studies suggest a difference in local structure of the E protein associated with either an asparagine or serine residue at position 155 compared with the tyrosine found in the virulent parental WN-Israel virus.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.83297-0
2008-03-01
2020-01-21
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/3/627.html?itemId=/content/journal/jgv/10.1099/vir.0.83297-0&mimeType=html&fmt=ahah

References

  1. Beasley, D. W., Li, L., Suderman, M. T. & Barrett, A. D. ( 2001; ). West Nile virus strains differ in mouse neurovirulence and binding to mouse or human brain membrane receptor preparations. Ann N Y Acad Sci 951, 332–335.
    [Google Scholar]
  2. Beasley, D. W., Li, L., Suderman, M. T. & Barrett, A. D. ( 2002; ). Mouse neuroinvasive phenotype of West Nile virus strains varies depending upon virus genotype. Virology 296, 17–23.[CrossRef]
    [Google Scholar]
  3. Beasley, D. W. C., Whiteman, M. C., Zhang, S., Huang, C. Y.-H., Schneider, B. S., Smith, D. R., Gromowski, G. D., Higgs, S., Kinney, R. M. & Barrett, A. D. T. ( 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]
  4. Ben-Nathan, D., Lustig, S. & Feuerstein, G. ( 1989; ). The influence of cold or isolation stress on neuroinvasiveness and virulence of an attenuated variant of West Nile virus. Arch Virol 109, 1–10.[CrossRef]
    [Google Scholar]
  5. Ben-Nathan, D., Huitinga, I., Lustig, S., van Rooijen, N. & Kobiler, D. ( 1996; ). West Nile virus neuroinvasion and encephalitis induced by macrophage depletion in mice. Arch Virol 141, 459–469.[CrossRef]
    [Google Scholar]
  6. Ben-Nathan, D., Lustig, S., Tam, G., Robinzon, S., Segal, S. & Rager-Zisman, B. ( 2003; ). Prophylactic and therapeutic efficacy of human intravenous immunoglobulin in treating West Nile virus infection in mice. J Infect Dis 188, 5–12.[CrossRef]
    [Google Scholar]
  7. Berthet, F. X., Zeller, H. G., Drouet, M. T., Rauzier, J., Digoutte, J. P. & Deubel, V. ( 1997; ). Extensive nucleotide changes and deletions within the envelope glycoprotein gene of Euro-African West Nile viruses. J Gen Virol 78, 2293–2297.
    [Google Scholar]
  8. Bondre, V. P., Jadi, R. S., Mishra, A. C., Yergolkar, P. N. & Arankalle, V. A. ( 2007; ). West Nile virus isolates from India: evidence for a distinct genetic lineage. J Gen Virol 88, 875–884.[CrossRef]
    [Google Scholar]
  9. Brandriss, M. W., Schlesinger, J. J., Walsh, E. E. & Briselli, M. ( 1986; ). Lethal 17D yellow fever encephalitis in mice. I. Passive protection by monoclonal antibodies to the envelope proteins of 17D yellow fever and dengue 2 viruses. J Gen Virol 67, 229–234.[CrossRef]
    [Google Scholar]
  10. Broom, A. K., Wallace, M. J., Mackenzie, J. S., Smith, D. W. & Hall, R. A. ( 2000; ). Immunisation with gamma globulin to Murray Valley encephalitis virus and with an inactivated Japanese encephalitis virus vaccine as prophylaxis against Australian encephalitis: evaluation in a mouse model. J Med Virol 61, 259–265.[CrossRef]
    [Google Scholar]
  11. Burke, S. D. & Monath, T. P. ( 2001; ). Flaviviruses. In Fields Virology, vol. 1, 4th edn, pp. 1043–125. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: Lippincott–Raven.
  12. Burt, F. J., Grobbelaar, A. A., Leman, P. A., Anthony, F. S., Gibson, G. V. & Swanepoel, R. ( 2002; ). Phylogenetic relationships of Southern African West Nile virus isolates. Emerg Infect Dis 8, 820–826.[CrossRef]
    [Google Scholar]
  13. Chambers, T. J., Halevy, M., Nestorowicz, A., Rice, C. M. & Lustig, S. ( 1998; ). West Nile virus envelope proteins: nucleotide sequence analysis of strains differing in mouse neuroinvasiveness. J Gen Virol 79, 2375–2380.
    [Google Scholar]
  14. Davis, C. T., Beasley, D. W., Guzman, H., Siirin, M., Parsons, R. E., Tesh, R. B. & Barrett, A. D. ( 2004; ). Emergence of attenuated West Nile virus variants in Texas, 2003. Virology 330, 342–350.[CrossRef]
    [Google Scholar]
  15. Diamond, M. S., Shrestha, B., Marri, A., Mahan, D. & Engle, M. ( 2003; ). B cells and antibody play critical roles in the immediate defense of disseminated infection by West Nile encephalitis virus. J Virol 77, 2578–2586.[CrossRef]
    [Google Scholar]
  16. Goldblum, N., Strek, V. V. & Padersky, B. ( 1954; ). West Nile fever: the clinical features of the disease and isolation of West Nile from the blood of nine human cases. Am J Hyg 59, 89–103.
    [Google Scholar]
  17. Halevy, M., Akov, Y., Ben-Nathan, B., Kobiler, D., Lachmi, B. & Lustig, S. ( 1994; ). Loss of active neuroinvasiveness in attenuated strains of West Nile virus: pathogenicity in immunocompetent and SCID mice. Arch Virol 137, 355–370.[CrossRef]
    [Google Scholar]
  18. Katz, Y., Lustig, S., Ben-Shlomo, I., Kobiler, D. & Ben-Nathan, D. ( 2002; ). Inhalation anesthetic-induced neuroinvasion by an attenuated strain of West Nile virus in mice. J Med Virol 66, 576–580.[CrossRef]
    [Google Scholar]
  19. Kimura-Kuroda, J. & Yasui, K. ( 1988; ). Protection of mice against Japanese encephalitis virus by passive administration with monoclonal antibodies. J Immunol 141, 3606–3610.
    [Google Scholar]
  20. Kobiler, D., Lustig, S., Gozes, Y., Ben-Nathan, D. & Akov, Y. ( 1989; ). Sodium dodecylsulphate induces a breach in the blood–brain barrier and enables a West Nile virus variant to penetrate into mouse brain. Brain Res 496, 314–316.[CrossRef]
    [Google Scholar]
  21. 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]
  22. Lee, E., Hall, R. A. & Lobigs, M. ( 2004; ). Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J Virol 78, 8271–8280.[CrossRef]
    [Google Scholar]
  23. Lustig, S., Danenberg, H. D., Kafri, Y., Kobiler, D. & Ben-Nathan, D. ( 1992; ). Viral neuroinvasion and encephalitis induced by lipopolysaccharide and its mediators. J Exp Med 176, 707–712.[CrossRef]
    [Google Scholar]
  24. Lustig, S., Olshevsky, U., Ben-Nathan, D., Lachmi, B. E., Malkinson, M., Kobiler, D. & Halevy, M. ( 2000; ). A live attenuated West Nile virus strain as a potential veterinary vaccine. Viral Immunol 13, 401–410.[CrossRef]
    [Google Scholar]
  25. Mathews, J. H. & Roehrig, J. T. ( 1984; ). Elucidation of the topography and determination of the protective epitopes on the E glycoprotein of Saint Louis encephalitis virus by passive transfer with monoclonal antibodies. J Immunol 132, 1533–1537.
    [Google Scholar]
  26. Nybakken, G. E., Nelson, C. A., Chen, B. R., Diamond, M. S. & Fremont, D. H. ( 2006; ). Crystal structure of the West Nile virus envelope glycoprotein. J Virol 80, 11467–11474.[CrossRef]
    [Google Scholar]
  27. Petersen, L. R. & Roehrig, J. T. ( 2001; ). West Nile virus: a reemerging global pathogen. Emerg Infect Dis 7, 611–614.[CrossRef]
    [Google Scholar]
  28. Phillpotts, R. J., Stephenson, J. R. & Porterfield, J. S. ( 1987; ). Passive immunization of mice with monoclonal antibodies raised against tick-borne encephalitis virus: brief report. Arch Virol 93, 295–301.[CrossRef]
    [Google Scholar]
  29. Price, W. H. & O'Leary, W. ( 1967; ). Geographic variation in the antigenic character of West Nile virus. Am J Epidemiol 85, 84–86.
    [Google Scholar]
  30. Rappole, J. H., Derrickson, S. R. & Hubalek, Z. ( 2000; ). Migratory birds and spread of West Nile virus in the western hemisphere. Emerg Infect Dis 6, 319–328.[CrossRef]
    [Google Scholar]
  31. Roehrig, J. T., Staudinger, L. A., Hunt, A. R., Mathews, J. H. & Blair, C. D. ( 2001; ). Antibody prophylaxis and therapy for flavivirus encephalitis infections. Ann N Y Acad Sci 951, 286–297.
    [Google Scholar]
  32. Roehrig, J. T., Layton, M., Smith, P., Campbell, G. L., Nasci, R. & Lanciotti, R. S. ( 2002; ). The emergence of West Nile virus in North America: ecology, epidemiology, and surveillance. Curr Top Microbiol Immunol 267, 223–240.
    [Google Scholar]
  33. Scherret, J. H., Poidinger, M., Mackenzie, J. S., Broom, A. K., Deubel, V., Lipkin, W. I., Briese, T., Gould, E. A. & Hall, R. A. ( 2001; ). The relationships between West Nile and Kunjin viruses. Emerg Infect Dis 7, 697–705.[CrossRef]
    [Google Scholar]
  34. Scherret, J. H., Mackenzie, J. S., Hall, R. A., Deubel, V. & Gould, E. A. ( 2002; ). Phylogeny and molecular epidemiology of West Nile and Kunjin viruses. Curr Top Microbiol Immunol 267, 373–390.
    [Google Scholar]
  35. Schlesinger, J. J., Brandriss, M. W. & Walsh, E. E. ( 1985; ). Protection against 17D yellow fever encephalitis in mice by passive transfer of monoclonal antibodies to the nonstructural glycoprotein gp48 and by active immunization with gp48. J Immunol 135, 2805–2809.
    [Google Scholar]
  36. 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]
  37. Shrestha, B. & Diamond, M. S. ( 2004; ). Role of CD8+ T cells in control of West Nile virus infection. J Virol 78, 8312–8321.[CrossRef]
    [Google Scholar]
  38. Smithburn, K. C., Hughes, T. P., Burke, A. W. & Paul, J. H. ( 1940; ). A neurotropic virus isolated from the blood of a native of Uganda. Am J Trop Med 20, 471–492.
    [Google Scholar]
  39. Wengler, G., Castle, E., Leidner, U., Nowak, T. & Wengler, G. ( 1985; ). Sequence analysis of the membrane protein V3 of the flavivirus West Nile virus and of its gene. Virology 147, 264–267.[CrossRef]
    [Google Scholar]
  40. 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]
  41. Yamshchikov, G., Borisevich, V., Seregin, A., Chaporgina, E., Mishina, M., Mishin, V., Kwok, C. W. & Yamshchikov, V. ( 2004; ). An attenuated West Nile prototype virus is highly immunogenic and protects against the deadly NY99 strain: a candidate for live WN vaccine development. Virology 330, 304–312.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.83297-0
Loading
/content/journal/jgv/10.1099/vir.0.83297-0
Loading

Data & Media loading...

Most cited articles

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