1887

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Volume 89, Issue 7

Ovine herpesvirus 2 replicates initially in the lung of experimentally infected sheep Free

Abstract

Ovine herpesvirus 2 (OvHV-2), a rhadinovirus in the subfamily , is the causative agent of sheep-associated malignant catarrhal fever (SA-MCF), a frequently fatal lymphoproliferative disease primarily of ruminants worldwide. Inability to propagate the virus has made it difficult to study OvHV-2 replication. Aerosol inoculation of sheep with OvHV-2 from nasal secretions collected from naturally infected sheep during shedding episodes results in infection of naive sheep, providing an excellent system to study OvHV-2 initial replication in the natural host. In this study, we showed that OvHV-2 delivered through the nasal route by nebulization resulted in infection in all lambs, but no infection was established in any lambs after intravenous or intraperitoneal injection. In nebulized lambs, while it was not detected initially in any other tissues, OvHV-2 DNA became detectable in the lung at 3 days post-infection (p.i.), increased to about 900 copies per 50 ng DNA at 5 days p.i., reached peak levels (∼7500 copies) at 7 days p.i., and then declined to an average of 800 copies at 9 days p.i. Transcripts of OvHV-2 open reading frame 25 (coding for the capsid protein), an indicator of virus replication, were only detected in lung tissues, and were positively correlated with OvHV-2 DNA levels in the lungs. In addition, selected immune response genes were also highly expressed in the lung at 5 and 7 days p.i. The data indicate that lung is the primary replication site for OvHV-2 during initial infection in sheep and suggest that viral replication is promptly controlled by a host defence mechanism.

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2008-07-01
2024-04-20
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References

  1. Baxter S. I. F., Pow I., Bridgen A., Reid H. W. 1993; PCR detection of the sheep-associated agent of malignant catarrhal fever. Arch Virol 132:145–159 [CrossRef]
     [Google Scholar]
  2. Borza C. M., Hutt-Fletcher L. M. 2002; Alternate replication in B cells and epithelial cells switches tropism of Epstein–Barr virus. Nat Med 8:594–599 [CrossRef]
     [Google Scholar]
  3. Callan M. F. 2004; The immune response to Epstein–Barr virus. Microbes Infect 6:937–945 [CrossRef]
     [Google Scholar]
  4. Crawford T., O'Toole D. T., Li H. 1999; Malignant catarrhal fever. In Current Veterinary Therapy 4: Food Animal Practice . , 4th edn. pp 306–309Edited by Howell J., Smith R. A. Oklahoma: W.B. Saunders Company;
  5. Cunha C. W., Traul D. L., Taus N. S., Oaks J. L., O'Toole D., Davitt C. M., Li H. 2008; Detection of ovine herpesvirus 2 major capsid gene transcripts as an indicator of virus replication in shedding sheep and clinically affected animals. Virus Res 132:69–75 [CrossRef]
     [Google Scholar]
  6. Daniels P. W., Sudurisman W. A., Ronohardjo P. 1988; Epidemiological aspects of malignant catarrhal fever in Indonesia. In Malignant Catarrhal Fever in Asian Livestock pp 20–31Edited by Daniels P. W., Sudurisman W. A., Ronohardjo P. Canberra (Australia): Australian Centre for International Agricultural Research;
     [Google Scholar]
  7. Dewals B., Boudry C., Farnir F., Drion P. V., Vanderplasschen A. 2008; Malignant catarrhal fever induced by alcelaphine herpesvirus 1 is associated with proliferation of CD8 T cells supporting a latent infection. PLoS ONE 3:e1627 [CrossRef]
     [Google Scholar]
  8. Gailbreath K. L., Taus N. S., Cunha C. W., Knowles D. P., Li H. 2008; Experimental infection of rabbits with ovine herpesvirus 2 from sheep nasal secretions. Vet Microbiol (in press
    [Google Scholar]
  9. Heuschele W. P., Fletcher H. R. 1984; Recent findings on the epidemiology of malignant catarrhal fever in exotic ruminants. Proceeding of the Annual Meeting, American Association of Zoo Veterinarians 1984 Louisville, Kentucky: pp 95–96
     [Google Scholar]
  10. Hoshino Y., Morishima T., Kimura H., Nishikawa K., Tsurumi T., Kuzushima K. 1999; Antigen-driven expansion and contraction of CD8+-activated T cells in primary EBV infection. J Immunol 163:5735–5740
     [Google Scholar]
  11. Hussy D., Stauber N., Leutenegger C. M., Rieder S., Ackermann M. 2001; Quantitative fluorogenic PCR assay for measuring ovine herpesvirus 2 replication in sheep. Clin Diagn Lab Immunol 8:123–128
     [Google Scholar]
  12. Lee B. J., Reiter S. K., Anderson M., Sarawar S. R. 2002; CD28−/− mice show defects in cellular and humoral immunity but are able to control infection with murine gammaherpesvirus 68. J Virol 76:3049–3053 [CrossRef]
     [Google Scholar]
  13. Li H., Shen D. T., Knowles D. P., Gorham J. R., Crawford T. B. 1994; Competitive inhibition enzyme-linked immunosorbent assay for antibody in sheep and other ruminants to a conserved epitope of malignant catarrhal fever virus. J Clin Microbiol 32:1674–1679
     [Google Scholar]
  14. Li H., Shen D. T., O'Toole D. T., Knowles D. P., Gorham J. R., Crawford T. B. 1995; Investigation of sheep-associated malignant catarrhal fever virus infection in ruminants by PCR and competitive inhibition enzyme-linked immunosorbent assay. J Clin Microbiol 33:2048–2053
     [Google Scholar]
  15. Li H., Snowder G., O'Toole D. T., Crawford T. B. 1998; Transmission of ovine herpesvirus 2 in lambs. J Clin Microbiol 36:223–226
     [Google Scholar]
  16. Li H., Snowder G., Crawford T. B. 1999; Production of malignant catarrhal fever virus-free sheep. Vet Microbiol 65:167–172 [CrossRef]
     [Google Scholar]
  17. Li H., Snowder G., O'Toole D. T., Crawford T. B. 2000; Transmission of ovine herpesvirus 2 among adult sheep. Vet Microbiol 71:27–35 [CrossRef]
     [Google Scholar]
  18. Li H., McGuire T. C., Muller-Doblies U. U., Crawford T. B. 2001; A simpler, more sensitive competitive inhibition ELISA for detection of antibody to malignant catarrhal fever viruses. J Vet Diagn Invest 13:361–364 [CrossRef]
     [Google Scholar]
  19. Li H., Snowder G., Crawford T. B. 2002; Effect of passive transfer of maternal immune components on infection with ovine herpesvirus 2 in lambs. Am J Vet Res 63:631–633 [CrossRef]
     [Google Scholar]
  20. Li H., Taus N. S., Lewis G. S., Kim O., Traul D. L., Crawford T. B. 2004; Shedding of ovine herpesvirus 2 in sheep nasal secretions: the predominant mode for transmission. J Clin Microbiol 42:5558–5564 [CrossRef]
     [Google Scholar]
  21. Li H., O'Toole D., Kim O., Oaks J. L., Crawford T. B. 2005; Malignant catarrhal fever-like disease in sheep after intranasal inoculation with ovine herpesvirus-2. J Vet Diagn Invest 17:171–175 [CrossRef]
     [Google Scholar]
  22. Li H., Taus N. S., Jones C., Murphy B., Evermann J. F., Crawford T. B. 2006; A devastating outbreak of malignant catarrhal fever in a bison feedlot. J Vet Diagn Invest 18:119–123 [CrossRef]
     [Google Scholar]
  23. Livak K. J., Schmittgen T. D. 2001; Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔ C T Method. Methods 25:402–408 [CrossRef]
     [Google Scholar]
  24. Mackintosh C. 1993; Importance of infectious diseases of New Zealand farmed deer. Surveillance 20:24–26
     [Google Scholar]
  25. Mushi E. Z., Wafula J. S. 1983; Infectivity of cell-free malignant catarrhal fever virus in rabbit and cattle. Vet Res Commun 6:153–155 [CrossRef]
     [Google Scholar]
  26. O'Toole D., Li H., Sourk C., Montgomery D. L., Crawford T. B. 2002; Malignant catarrhal fever in a bison feedlot, 1994 - 2000. J Vet Diagn Invest 14:183–193 [CrossRef]
     [Google Scholar]
  27. O'Toole D., Taus D. N., Montgomery D. L., Oaks J. L., Crawford T. B., Li H. 2007; Intra-nasal inoculation of American bison ( Bison bison ) with OvHV-2 reliably reproduces malignant catarrhal fever. Vet Pathol 44:655–662 [CrossRef]
     [Google Scholar]
  28. Plowright W. 1990; Malignant catarrhal fever virus. In Virus Infections of Ruminants . , 3rd edn. pp 123–150Edited by Dinter Z., Morein B. New York: Elsevier Science Publishers B.V;
  29. Plowright W., Herniman K. A. J., Jessett D. M., Kalunda M., Rampton C. S. 1975; Immunisation of cattle against the herpesvirus of malignant catarrhal fever: failure of inactivated culture vaccines with adjuvant. Res Vet Sci 19:159–166
     [Google Scholar]
  30. Roizman B. 2000; Family Herpesviridae . In Virus Taxonomy . pp 202–225Edited by van Regenmortel M. H. V., Fauquet C. M., Bishop D. H. L. San Diego: Academic Press;
  31. Rossiter P. B., Mushi E. Z., Plowright W. 1977; The development of antibodies in rabbits and cattle infected experimentally with an African strain of malignant catarrhal fever virus. Vet Microbiol 2:57–66 [CrossRef]
     [Google Scholar]
  32. Schultheiss P. C., Collins J. K., Spraker T. R., DeMartini J. C. 2000; Epizootic malignant catarrhal fever in three bison herds: differences from cattle and association with ovine herpesvirus-2. J Vet Diagn Invest 12:497–502 [CrossRef]
     [Google Scholar]
  33. Stevenson P. G., Belz G. T., Altman J. D., Doherty P. C. 1999; Changing patterns of dominance in the CD8+ T cell response during acute and persistent murine γ -herpesvirus infection. Eur J Immunol 29:1059–1067 [CrossRef]
     [Google Scholar]
  34. Taus N. S., Traul D. L., Oaks J. L., Crawford T. B., Lewis G. S., Li H. 2005; Experimental infection of sheep with ovine herpesvirus 2 via aerosolization of nasal secretions. J Gen Virol 86:575–579 [CrossRef]
     [Google Scholar]
  35. Taus N. S., Oaks J. L., Gailbreath K., Traul D. L., O'Toole D., Li H. 2006; Experimental aerosol infection of cattle ( Bos taurus ) with ovine herpesvirus 2 using nasal secretions from infected sheep. Vet Microbiol 116:29–36 [CrossRef]
     [Google Scholar]
  36. Traul D. L., Taus N. S., Lindsay O. J., O'Toole D., Rurangirwa F. R., Baszler T. V., Li H. 2007; Validation of nonnested and real-time PCR for diagnosis of sheep-associated malignant catarrhal fever in clinical samples. J Vet Diagn Invest 19:405–408 [CrossRef]
     [Google Scholar]
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Ovine herpesvirus 2 replicates initially in the lung of experimentally infected sheep
J. Gen. Virol. 89, 1699 (2008); https://doi.org/10.1099/vir.0.2008/000554-0
/content/journal/jgv/10.1099/vir.0.2008/000554-0
/content/journal/jgv/10.1099/vir.0.2008/000554-0
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