1887

Abstract

The main routes of transmission of (VMV), an ovine lentivirus, are thought to be through ingestion of infected colostrum and/or milk or through inhalation of respiratory secretions. Whereas oral transmission appears to be mediated via epithelial cells within the small intestine, the mechanism of virus uptake in the respiratory tract is unknown. In addition, it is not known whether infection is mediated by cell-associated or cell-free VMV, previous studies having not addressed this question. Intratracheal (i.t.) injection of VMV is known to be a highly efficient method of experimental infection, requiring as little as 10 TCID VMV for successful infection. However, using a tracheal organ culture system, we show here that ovine tracheal mucosa is relatively resistant to VMV, with detectable infection only seen after incubation with high titres of virus (⩾10 TCID ml). We also demonstrate that i.t. injection results in exposure of both trachea and the lower lung and that the time taken for viraemia and seroconversion to occur after lower lung instillation of VMV was significantly shorter than that observed for tracheal instillation of an identical titre of virus (=0.030). This indicates that lower lung and not the trachea is a highly efficient site for VMV entry . Furthermore, cell-free virus was identified within the lung-lining fluid of naturally infected sheep for the first time. Together, these results suggest that respiratory transmission of VMV is mediated by inhalation of aerosols containing free VMV, with subsequent virus uptake in the lower lung.

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2007-02-01
2020-01-18
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References

  1. Anderton, T. L., Maskell, D. J. & Preston, A. ( 2004; ). Ciliostasis is a key early event during colonization of canine tracheal tissue by Bordetella bronchiseptica. Microbiology 150, 2843–2855.[CrossRef]
    [Google Scholar]
  2. Blacklaws, B. A., Berriatua, E., Torsteinsdottir, S., Watt, N. J., de Andres, D., Klein, D. & Harkiss, G. D. ( 2004; ). Transmission of small ruminant lentiviruses. Vet Microbiol 101, 199–208.[CrossRef]
    [Google Scholar]
  3. Brahic, M., Stowring, L., Ventura, P. & Haase, A. T. ( 1981; ). Gene expression in visna virus infection in sheep. Nature 292, 240–242.[CrossRef]
    [Google Scholar]
  4. Brodie, S. J., Pearson, L. D., Zink, M. C., Bickle, H. M., Anderson, B. C., Marcom, K. A. & DeMartini, J. C. ( 1995; ). Ovine lentivirus expression and disease. Virus replication, but not entry, is restricted to macrophages of specific tissues. Am J Pathol 146, 250–263.
    [Google Scholar]
  5. Campbell, R. S., Rae, A., Sharp, J. M. & Smith, W. ( 1979; ). Infection of tracheal organ cultures with ovine adenovirus type 2. J Comp Pathol 89, 107–114.[CrossRef]
    [Google Scholar]
  6. Carrozza, M. L., Mazzei, M., Bandecchi, P., Arispici, M. & Tolari, F. ( 2003; ). In situ PCR-associated immunohistochemistry identifies cell types harbouring the Maedi-Visna virus genome in tissue sections of sheep infected naturally. J Virol Methods 107, 121–127.[CrossRef]
    [Google Scholar]
  7. Craig, L. E., Nealen, M. L., Strandberg, J. D. & Zink, M. C. ( 1997; ). Differential replication of ovine lentivirus in endothelial cells cultured from different tissues. Virology 238, 316–326.[CrossRef]
    [Google Scholar]
  8. Dhinakar Raj, G. & Jones, R. C. ( 1996; ). Protectotypic differentiation of avian infectious bronchitis viruses using an in vitro challenge model. Vet Microbiol 53, 239–252.[CrossRef]
    [Google Scholar]
  9. Ebrahimi, B., Allsopp, T. E., Fazakerley, J. K. & Harkiss, G. D. ( 2000; ). Phenotypic characterisation and infection of ovine microglial cells with Maedi-Visna virus. J Neurovirol 6, 320–328.[CrossRef]
    [Google Scholar]
  10. Fennelly, K. P., Martyny, J. W., Fulton, K. E., Orme, I. M., Cave, D. M. & Heifets, L. B. ( 2004; ). Cough-generated aerosols of Mycobacterium tuberculosis: a new method to study infectiousness. Am J Respir Crit Care Med 169, 604–609.[CrossRef]
    [Google Scholar]
  11. Gelmetti, D., Gibelli, L., Brocchi, E. & Cammarata, G. ( 2000; ). Using a panel of monoclonal antibodies to detect Maedi virus (MV) in chronic pulmonary distress of sheep. J Virol Methods 88, 9–14.[CrossRef]
    [Google Scholar]
  12. Gendelman, H. E., Narayan, O., Molineaux, S., Clements, J. E. & Ghotbi, Z. ( 1985; ). Slow, persistent replication of lentiviruses: role of tissue macrophages and macrophage precursors in bone marrow. Proc Natl Acad Sci U S A 82, 7086–7090.[CrossRef]
    [Google Scholar]
  13. Gendelman, H. E., Narayan, O., Kennedy-Stoskopf, S., Kennedy, P. G., Ghotbi, Z., Clements, J. E., Stanley, J. & Pezeshkpour, G. ( 1986; ). Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages. J Virol 58, 67–74.
    [Google Scholar]
  14. Gordon, S. B. & Read, R. C. ( 2002; ). Macrophage defences against respiratory tract infections. Br Med Bull 61, 45–61.[CrossRef]
    [Google Scholar]
  15. Haase, A. T., Stowring, L., Narayan, P., Griffin, D. & Price, D. ( 1977; ). Slow persistent infection caused by visna virus: role of host restriction. Science 195, 175–177.[CrossRef]
    [Google Scholar]
  16. Haase, A. T., Stowring, L., Harris, J. D., Traynor, B., Ventura, P., Peluso, R. & Brahic, M. ( 1982; ). Visna DNA synthesis and the tempo of infection in vitro. Virology 119, 399–410.[CrossRef]
    [Google Scholar]
  17. Hirsch, J. I., Tisnado, J., Cho, S. R. & Beachley, M. C. ( 1982; ). Use of isosulfan blue for identification of lymphatic vessels: experimental and clinical evaluation. AJR Am J Roentgenol 139, 1061–1064.[CrossRef]
    [Google Scholar]
  18. Kennedy-Stoskopf, S. & Narayan, O. ( 1986; ). Neutralizing antibodies to visna lentivirus: mechanism of action and possible role in virus persistence. J Virol 59, 37–44.
    [Google Scholar]
  19. Lee, W. C., McConnell, I. & Blacklaws, B. A. ( 1996; ). Electron microscope studies of the replication of a British isolate of maedi visna virus in macrophages and skin cell lines. Vet Microbiol 49, 93–104.[CrossRef]
    [Google Scholar]
  20. Leginagoikoa, I., Juste, R. A., Barandika, J., Amorena, B., de Andres, D., Lujan, L., Badiola, J. & Berriatua, E. ( 2006; ). Extensive rearing hinders Maedi-Visna virus (VMV) infection in sheep. Vet Res 37, 767–778.[CrossRef]
    [Google Scholar]
  21. Lehnert, B. E. ( 1992; ). Pulmonary and thoracic macrophage subpopulations and clearance of particles from the lung. Environ Health Perspect 97, 17–46.[CrossRef]
    [Google Scholar]
  22. Lerondelle, C., Godet, M. & Mornex, J. F. ( 1999; ). Infection of primary cultures of mammary epithelial cells by small ruminant lentiviruses. Vet Res 30, 467–474.
    [Google Scholar]
  23. Leroux, C., Cordier, G., Mercier, I., Chastang, J., Lyon, M., Querat, G., Greenland, T., Vigne, R. & Mornex, J. F. ( 1995; ). Ovine aortic smooth muscle cells allow the replication of visna-maedi virus in vitro. Arch Virol 140, 1–11.[CrossRef]
    [Google Scholar]
  24. Lin, C., Holland, R. E., Jr, Williams, N. M. & Chambers, T. M. ( 2001; ). Cultures of equine respiratory epithelial cells and organ explants as tools for the study of equine influenza virus infection. Arch Virol 146, 2239–2247.[CrossRef]
    [Google Scholar]
  25. Lujan, L., Begara, I., Collie, D. & Watt, N. J. ( 1994; ). Ovine lentivirus (maedi-visna virus) protein expression in sheep alveolar macrophages. Vet Pathol 31, 695–703.[CrossRef]
    [Google Scholar]
  26. Lund, S. J., Rowe, H. A., Parton, R. & Donachie, W. ( 2001; ). Adherence of ovine and human Bordetella parapertussis to continuous cell lines and ovine tracheal organ culture. FEMS Microbiol Lett 194, 197–200.[CrossRef]
    [Google Scholar]
  27. McGorum, B. C., Dixon, P. M., Halliwell, R. E. & Irving, P. ( 1993; ). Evaluation of urea and albumen as endogenous markers of dilution of equine bronchoalveolar lavage fluid. Res Vet Sci 55, 52–56.[CrossRef]
    [Google Scholar]
  28. McOrist, S., Boid, R. & Lawson, G. H. ( 1989; ). Antigenic analysis of Campylobacter species and an intracellular Campylobacter-like organism associated with porcine proliferative enteropathies. Infect Immun 57, 957–962.
    [Google Scholar]
  29. Pepin, M., Vitu, C., Russo, P., Mornex, J. F. & Peterhans, E. ( 1998; ). Maedi-visna virus infection in sheep: a review. Vet Res 29, 341–367.
    [Google Scholar]
  30. Peterhans, E., Greenland, T., Badiola, J., Harkiss, G., Bertoni, G., Amorena, B., Eliaszewicz, M., Juste, R. A., Krassnig, R. & other authors ( 2004; ). Routes of transmission and consequences of small ruminant lentiviruses (SRLVs) infection and eradication schemes. Vet Res 35, 257–274.[CrossRef]
    [Google Scholar]
  31. Preziuso, S., Renzoni, G., Allen, T. E., Taccini, E., Rossi, G., DeMartini, J. C. & Braca, G. ( 2004; ). Colostral transmission of maedi visna virus: sites of viral entry in lambs born from experimentally infected ewes. Vet Microbiol 104, 157–164.[CrossRef]
    [Google Scholar]
  32. Reyburn, H. T., Roy, D. J., Blacklaws, B. A., Sargan, D. R. & McConnell, I. ( 1992; ). Expression of maedi-visna virus major core protein, p25: development of a sensitive p25 antigen detection assay. J Virol Methods 37, 305–320.[CrossRef]
    [Google Scholar]
  33. Rutman, A., Dowling, R., Wills, P., Feldman, C., Cole, P. J. & Wilson, R. ( 1998; ). Effect of dirithromycin on Haemophilus influenzae infection of the respiratory mucosa. Antimicrob Agents Chemother 42, 772–778.
    [Google Scholar]
  34. Ryan, S., Tiley, L., McConnell, I. & Blacklaws, B. ( 2000; ). Infection of dendritic cells by the Maedi-Visna lentivirus. J Virol 74, 10096–10103.[CrossRef]
    [Google Scholar]
  35. Saman, E., Van Eynde, G., Lujan, L., Extramiana, B., Harkiss, G., Tolari, F., Gonzalez, L., Amorena, B., Watt, N. & Badiola, J. ( 1999; ). A new sensitive serological assay for detection of lentivirus infections in small ruminants. Clin Diagn Lab Immunol 6, 734–740.
    [Google Scholar]
  36. Sargan, D. R., Bennet, I. D., Cousens, C., Roy, D. J., Blacklaws, B. A., Dalziel, R. G., Watt, N. J. & McConnell, I. ( 1991; ). Nucleotide sequence of EV1, a British isolate of maedi-visna virus. J Gen Virol 72, 1893–1903.[CrossRef]
    [Google Scholar]
  37. Sigurdsson, B. & Palsson, P. A. ( 1958; ). Visna of sheep; a slow, demyelinating infection. Br J Exp Pathol 39, 519–528.
    [Google Scholar]
  38. Sigurdsson, B., Grimsson, H. & Palsson, P. A. ( 1952; ). Maedi, a chronic, progressive infection of sheep's lungs. J Infect Dis 90, 233–241.[CrossRef]
    [Google Scholar]
  39. Staskus, K. A., Couch, L., Bitterman, P., Retzel, E. F., Zupancic, M., List, J. & Haase, A. T. ( 1991; ). In situ amplification of visna virus DNA in tissue sections reveals a reservoir of latently infected cells. Microb Pathog 11, 67–76.[CrossRef]
    [Google Scholar]
  40. Torsteinsdottir, S., Matthiasdottir, S., Vidarsdottir, N., Svansson, V. & Petursson, G. ( 2003; ). Intratracheal inoculation as an efficient route of experimental infection with maedi-visna virus. Res Vet Sci 75, 245–247.[CrossRef]
    [Google Scholar]
  41. Vigne, R., Barban, V., Querat, G., Mazarin, V., Gourdou, I. & Sauze, N. ( 1987; ). Transcription of visna virus during its lytic cycle: evidence for a sequential early and late gene expression. Virology 161, 218–227.[CrossRef]
    [Google Scholar]
  42. Welsh, D. A. & Mason, C. M. ( 2001; ). Host defense in respiratory infections. Med Clin North Am 85, 1329–1347.[CrossRef]
    [Google Scholar]
  43. Yamamoto, Y., Klein, T. W. & Friedman, H. ( 1994; ). Legionella and macrophages. Immunol Ser 60, 329–348.
    [Google Scholar]
  44. Zhang, P., Summer, W. R., Bagby, G. J. & Nelson, S. ( 2000; ). Innate immunity and pulmonary host defense. Immunol Rev 173, 39–51.[CrossRef]
    [Google Scholar]
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