1887

Abstract

Experiments were performed to determine whether visna/maedi virus (VMV), a small ruminant lentivirus (SRLV), could infect sheep via ocular tissues. The EV1 strain of VMV was administered into the conjunctival space of uninfected sheep, and the animals monitored for the presence of provirus DNA and anti-VMV antibodies in blood. The results showed that provirus DNA appeared in peripheral blood mononuclear cells of all animals within a few weeks of receiving either 10 TCID or 10 TCID of VMV. Of the animals receiving the higher dose of virus via the conjunctival space, two seroconverted by 7 and 10 weeks post-infection, one seroconverted 8 months post-infection, and one had not seroconverted by 15 months post-infection. With the lower virus dose, the animals infected via the trachea seroconverted by 4 and 14 weeks, respectively. After ocular infection with this dose, one animal showed a transitory seroconversion with low levels of antibody, peaking at 2 weeks post-administration. The remaining three of the animals infected via the eyes did not seroconvert over a period of 13 months. At post-mortem, evidence for the presence of proviral DNA was obtained from ocular tissue, lungs or mediastinal lymph node in both groups of animals. Histological analysis of lung tissue from animals receiving the lower dose of virus showed the presence of early inflammatory lesions. The results thus show for the first time that transmission of VMV can occur via ocular tissues, suggesting that the conjunctival space may be an additional route of natural transmission.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.2008/000133-0
2008-06-01
2019-11-12
Loading full text...

Full text loading...

/deliver/fulltext/jgv/89/6/1329.html?itemId=/content/journal/jgv/10.1099/vir.0.2008/000133-0&mimeType=html&fmt=ahah

References

  1. Adams, D. S., Klevjer-Anderson, P., Carlson, J. L., McGuire, T. C. & Gorham, J. R. ( 1983; ). Transmission and control of caprine arthritis-encephalitis virus. Am J Vet Res 44, 1670–1675.
    [Google Scholar]
  2. Baba, M. A., Sinha, R. D. & Prasad, R. ( 1995; ). Comparative histological studies on the third eyelid of goat and sheep. Indian Vet J 72, 1166–1169.
    [Google Scholar]
  3. Bell, J. A., Huebner, R. J., Paffenbarger, R. S., Jr, Rowe, W. P., Suskind, R. G. & Ward, J.G. ( 1956; ). Studies of adenoviruses (APC) in volunteers. Am J Public Health 46, 1130–1146.[CrossRef]
    [Google Scholar]
  4. Blacklaws, B. A., Berriatua, E., Torsteinsdóttir, 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]
  5. 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]
  6. Brellou, G. D., Angelopoulou, K., Poutahidis, T. & Vlemmas, I. ( 2007; ). Detection of maedi-visna virus in the liver and heart of naturally infected sheep. J Comp Pathol 136, 27–35.[CrossRef]
    [Google Scholar]
  7. 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]
  8. Capucchio, M. T., Sanna, E., Sanna, M. P., Farigu, S., Minelli, R. & Guarda, F. ( 2003; ). Maedi-visna detection in ovine third eyelids. J Comp Pathol 129, 37–43.[CrossRef]
    [Google Scholar]
  9. Cheevers, W. P., Knowles, D. P., McGuire, T. C., Cunningham, D. R., Adams, D. S. & Gorham, J. R. ( 1988; ). Chronic disease in goats orally infected with two isolates of the caprine arthritis-encephalitis lentivirus. Lab Invest 58, 510–517.
    [Google Scholar]
  10. Clerici, M., Berzofsky, J. A., Shearer, G. M. & Tacket, C. O. ( 1991; ). Exposure to human immunodeficiency virus (HIV) type I indicated by HIV-specific T helper cell responses before detection of infection by polymerase chain reaction and serum antibodies. J Infect Dis 164, 178–182.[CrossRef]
    [Google Scholar]
  11. Cutlip, R. C., Lehmkuhl, H. D., Brogden, K. A. & Bolin, S. R. ( 1985; ). Mastitis associated with ovine progressive pneumonia virus infection in sheep. Am J Vet Res 46, 326–328.
    [Google Scholar]
  12. de Andrés, D., Klein, D., Watt, N. J., Berriatua, E., Torsteinsdóttir, S., Blacklaws, B. A. & Harkiss, G. D. ( 2005; ). Diagnostic tests for small ruminant lentiviruses. Vet Microbiol 107, 49–62.[CrossRef]
    [Google Scholar]
  13. De Boer, G. F., Terpstra, C. & Houwers, D. J. ( 1979; ). Studies in epidemiology of maedi/visna in sheep. Res Vet Sci 26, 202–208.
    [Google Scholar]
  14. 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]
  15. Eriksson, K., McInnes, E., Ryan, S., Tonks, P., McConnell, I. & Blacklaws, B. ( 1999; ). CD4+ T-cells are required for the establishment of maedi-visna virus infection in macrophages but not dendritic cells in vivo. Virology 258, 355–364.[CrossRef]
    [Google Scholar]
  16. 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]
  17. 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]
  18. Georgsson, G. & Palsson, P. A. ( 1971; ). The histopathology of maedi a slow, viral pneumonia of sheep. Vet Pathol 8, 63–80.
    [Google Scholar]
  19. Gorrell, M. D., Brandon, M. R., Sheffer, D., Adams, R. J. & Narayan, O. ( 1992; ). Ovine lentivirus is macrophagetropic and does not replicate productively in T lymphocytes. J Virol 66, 2679–2688.
    [Google Scholar]
  20. Haase, A. T. ( 1986; ). Pathogenesis of lentivirus infections. Nature 322, 130–136.[CrossRef]
    [Google Scholar]
  21. 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]
  22. Hopper, C. D., Sparkes, A. H., Gruffydd-Jones, T. J., Crispin, S. M., Muir, P., Harbour, D. A. & Stokes, C. R. ( 1989; ). Clinical and laboratory findings in cats infected with feline immunodeficiency virus. Vet Rec 125, 341–346.[CrossRef]
    [Google Scholar]
  23. Horsburgh, C. R., Jr, Ou, C. Y., Jason, J., Holmberg, S. D., Longini, I. M., Jr, Schable, C., Mayer, K. H., Lifson, A. R., Schochetman, G. & other authors ( 1989; ). Duration of human immunodeficiency virus infection before detection of antibody. Lancet 2, 637–640.
    [Google Scholar]
  24. Houwers, D. J. & van der Molen, E. J. ( 1987; ). A five-year serological study of natural transmission of maedi-visna virus in a flock of sheep, completed with post mortem investigation. Zentralbl Veterinarmed B 34, 421–431.
    [Google Scholar]
  25. Jaax, N. K., Davis, K. J., Geisbert, T. J., Vogel, P., Jaax, G. P., Topper, M. & Jahrling, P. B. ( 1996; ). Lethal experimental infection of rhesus monkeys with Ebola-Zaire (Mayinga) virus by the oral and conjunctival route of exposure. Arch Pathol Lab Med 120, 140–155.
    [Google Scholar]
  26. Juste, R. A., Kwang, J. & de la Concha-Bermejillo, A. ( 1998; ). Dynamics of cell-associated viremia and antibody response during the early phase of lentivirus infection in sheep. Am J Vet Res 59, 563–568.
    [Google Scholar]
  27. Kageyama, M., Nakatsuka, K., Yamaguchi, T., Owen, R. L. & Shimada, T. ( 2006; ). Ocular defense mechanisms with special reference to the demonstration and functional morphology of the conjunctiva-associated lymphoid tissue in Japanese monkeys. Arch Histol Cytol 69, 311–322.[CrossRef]
    [Google Scholar]
  28. Knop, N. & Knop, E. ( 2005; ). Ultrastructural anatomy of CALT follicles in the rabbit reveals characteristics of M-cells, germinal centres and high endothelial venules. J Anat 207, 409–426.[CrossRef]
    [Google Scholar]
  29. Larsen, H. J., Hyllseth, B. & Krogsrud, J. ( 1982a; ). Experimental maedi virus infection in sheep: early cellular and humoral immune response following parenteral inoculation. Am J Vet Res 43, 379–383.
    [Google Scholar]
  30. Larsen, H. J., Hyllseth, B. & Krogsrud, J. ( 1982b; ). Experimental maedi virus infection in sheep: cellular and humoral immune response during three years following intranasal inoculation. Am J Vet Res 43, 384–389.
    [Google Scholar]
  31. 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]
  32. McGuire, T. C., Adams, D. S., Johnson, G. C., Klevjer-Anderson, P., Barbee, D. D. & Gorham, J. R. ( 1986; ). Acute arthritis in caprine arthritis-encephalitis virus challenge exposure of vaccinated or persistently infected goats. Am J Vet Res 47, 537–540.
    [Google Scholar]
  33. McNeilly, T. N., Tennant, P., Lujan, L., Perez, M. & Harkiss, G. D. ( 2007; ). Differential infection efficiencies of peripheral lung and tracheal tissues in sheep infected with visna/maedi virus via the respiratory tract. J Gen Virol 88, 670–679.[CrossRef]
    [Google Scholar]
  34. Mordasini, F., Vogt, H-R., Zahno, M-L, Maeschli, A., Nenci, C., Zanoni, R., Peterhans, E. & Bertoni, G. ( 2006; ). Analysis of the antibody response to an immunodominant epitope of the envelope glycoprotein of a lentivirus and its diagnostic potential. J Clin Microbiol 44, 981–991.[CrossRef]
    [Google Scholar]
  35. Narayan, O. & Clements, J. E. ( 1989; ). Biology and pathogenesis of lentiviruses. J Gen Virol 70, 1617–1639.[CrossRef]
    [Google Scholar]
  36. Narayan, O., Wolinsky, J. S., Clements, J. E., Strandberg, J. D., Griffin, D. E. & Cork, L. C. ( 1982; ). Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. J Gen Virol 59, 345–356.[CrossRef]
    [Google Scholar]
  37. Narayan, O., Kennedy-Stoskopf, S., Sheffer, D., Griffin, D. E. & Clements, J. E. ( 1983; ). Activation of caprine arthritis-encephalitis virus expression during maturation of monocytes to macrophages. Infect Immun 41, 67–73.
    [Google Scholar]
  38. Nathanson, N., Panitch, H., Palsson, P. A., Petursson, G. & Georgsson, G. ( 1976; ). Pathogenesis of visna. II. Effect of immunosuppression upon early central nervous system lesions. Lab Invest 35, 444–451.
    [Google Scholar]
  39. Nenci, C., Zahno, M. L., Vogt, H. R., Obexer-Ruff, G., Doherr, M. G., Zanoni, R., Peterhans, E. & Bertoni, G. ( 2007; ). Vaccination with a T-cell-priming Gag peptide of caprine arthritis encephalitis virus enhances virus replication transiently in vivo. J Gen Virol 88, 1589–1593.[CrossRef]
    [Google Scholar]
  40. Olofsson, S., Kumlin, U., Dimock, K. & Arnberg, N. ( 2005; ). Avian influenza and sialic acid receptors: more than meets the eye. Lancet Infect Dis 5, 184–188.[CrossRef]
    [Google Scholar]
  41. Orlando, J. S., Balliet, J. W., Kushnir, A. S., Astor, T. L., Kosz-Vnenchak, M., Rice, S. A., Knipe, D. M. & Schaffer, P. A. ( 2006; ). ICP22 is required for wild-type composition and infectivity of herpes simplex virus type 1 virions. J Virol 80, 9381–9390.[CrossRef]
    [Google Scholar]
  42. Palsson, P. A. ( 1976; ). Maedi and visna in sheep. Front Biol 44, 17–43.
    [Google Scholar]
  43. 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]
  44. Peterhans, E., Greenland, T., Badiola, J., Harkiss, G., Bertoni, G., Amorena, B., Eliaszewicz, M., Juste, R., 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]
  45. Petursson, G., Nathanson, N., Georgsson, G., Panitch, H. & Palsson, P. A. ( 1976; ). Pathogenesis of visna. I. Sequential virologic, serologic, and pathologic studies. Lab Invest 35, 402–412.
    [Google Scholar]
  46. Rimstad, E., East, N. E., Torten, M., Higgins, J., DeRock, E. & Pedersen, N. C. ( 1993; ). Delayed seroconversion following naturally acquired caprine arthritis-encephalitis virus infection in goats. Am J Vet Res 54, 1858–1862.
    [Google Scholar]
  47. Robert, P. Y., Adenis, J. P., Denis, F. & Ranger-Rogez, S. ( 2005; ). Transmission of viruses through corneal transplants. Clin Lab 51, 419–423.
    [Google Scholar]
  48. Rozina, E. E., Khudaverdyan, O. E., Brudno, I. A., Dorofeev, V. M., Kropotova, N. S. & Shteinberg, L. S. ( 1988; ). Comparative clinico-morphological investigations of the CNS of monkeys and of the eye teguments of guinea pigs infected with different measles virus strains. Acta Virol 32, 123–128.
    [Google Scholar]
  49. 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]
  50. Saman, E., Van Eynde, G., Lujan, L., Extramiana, B., Harkiss, G., Tolari, F., Gonzàlez, 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]
  51. 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]
  52. Small, J. A., Bieberich, C., Ghotbi, Z., Hess, J., Scangos, G. A. & Clements, J. E. ( 1989; ). The visna virus long terminal repeat directs expression of a reporter gene in activated macrophages, lymphocytes, and the central nervous systems of transgenic mice. J Virol 63, 1891–1896.
    [Google Scholar]
  53. 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]
  54. Streilein, J. W. ( 1999; ). Immunoregulatory mechanisms of the eye. Prog Retin Eye Res 18, 357–370.[CrossRef]
    [Google Scholar]
  55. Torsteinsdóttir, S., Agnarsdóttir, G., Matthíasdóttir, S., Rafnar, B., Andrésdóttir, V., Andrésson, O. S., Staskus, K., Pétursson, G., Pálsson, P. A. & Georgsson, G. ( 1997; ). In vivo and in vitro infection with two different molecular clones of visna virus. Virology 229, 370–380.[CrossRef]
    [Google Scholar]
  56. Torsteinsdóttir, 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]
  57. van der Molen, E. J. & Houwers, D. J. ( 1987; ). Indurative lymphocytic mastitis in sheep after experimental infection with maedivisna virus. Vet Q 9, 193–202.[CrossRef]
    [Google Scholar]
  58. 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]
  59. Villinger, F., Powell, J. D., Jehuda-Cohen, T., Neckelmann, N., Vuchetich, M., De, B., Folks, T. M., McClure, H. M. & Ansari, A. A. ( 1991; ). Detection of occult simian immunodeficiency virus SIVsmm infection in asymptomatic seronegative nonhuman primates and evidence for variation in SIV gag sequence between in vivo- and in vitro-propagated virus. J Virol 65, 1855–1862.
    [Google Scholar]
  60. Zhang, M., Zhou, J., Marshall, B., Xin, H. & Atherton, S. S. ( 2007; ). Lack of iNOS facilitates MCMV spread in the retina. Invest Ophthalmol Vis Sci 48, 285–292.[CrossRef]
    [Google Scholar]
  61. Zink, M. C. & Narayan, O. ( 1989; ). Lentivirus-induced interferon inhibits maturation and proliferation of monocytes and restricts the replication of caprine arthritis-encephalitis virus. J Virol 63, 2578–2584.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.2008/000133-0
Loading
/content/journal/jgv/10.1099/vir.0.2008/000133-0
Loading

Data & Media loading...

Most Cited This Month

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