Skip to main content
Clinical and Experimental Immunology logoLink to Clinical and Experimental Immunology
. 1992 Nov;90(2):204–208. doi: 10.1111/j.1365-2249.1992.tb07929.x

Phenotypic analysis of lymphocyte populations in the lungs and regional lymphoid tissue of sheep naturally infected with maedi visna virus.

N J Watt 1, N MacIntyre 1, D Collie 1, D Sargan 1, I McConnell 1
PMCID: PMC1554601  PMID: 1385026

Abstract

We have analysed the phenotype of lymphocytes in lung and regional lymph node of symptomatic and asymptomatic sheep infected with the ovine lentivirus, maedi visna virus (MVV). Compared to equivalent tissues from age-matched, non-infected controls, MVV-infected sheep show increased numbers of lymphocytes in the lung, both in the bronchus-associated lymphoid tissue (BALT) and in the alveolar septae. Both CD8+ and CD4+ T lymphocyte numbers in alveolar septae were increased, particularly in animals with clinical respiratory disease. The ratio of CD8+ to CD4+ lymphocytes was similar to that in normal lung. In both MVV-infected and uninfected animals a high proportion of pulmonary lymphocytes, particularly in the alveolar septae, did not express the CD5 antigen, suggesting that they were activated. The number of activated cells was higher in infected sheep. Variable numbers of alveolar macrophages containing MVV-core protein were present in alveolar lumina, the majority of positive cells showing morphological evidence of activation. In regional lymphoid tissue there were increased numbers of CD8+ and gamma delta expressing T cells in lymphoid follicles and germinal centres of infected animals. The specificity of these cells is unknown and we could find no evidence for the presence of cells productively infected with the virus in these structures. This study shows that activated T lymphocytes, particularly of the CD8 subset, play a major part in the pathogenesis of MVV-induced pulmonary and regional lymph node lesions.

Full text

PDF
204

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Augustin A., Kubo R. T., Sim G. K. Resident pulmonary lymphocytes expressing the gamma/delta T-cell receptor. Nature. 1989 Jul 20;340(6230):239–241. doi: 10.1038/340239a0. [DOI] [PubMed] [Google Scholar]
  2. Biberfeld P., Chayt K. J., Marselle L. M., Biberfeld G., Gallo R. C., Harper M. E. HTLV-III expression in infected lymph nodes and relevance to pathogenesis of lymphadenopathy. Am J Pathol. 1986 Dec;125(3):436–442. [PMC free article] [PubMed] [Google Scholar]
  3. Collins P. L., Hightower L. E. Newcastle disease virus stimulates the cellular accumulation of stress (heat shock) mRNAs and proteins. J Virol. 1982 Nov;44(2):703–707. doi: 10.1128/jvi.44.2.703-707.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dawson M., Biront P., Houwers D. J. Comparison of serological tests used in three state veterinary laboratories to identify maedi-visna virus infection. Vet Rec. 1982 Nov 6;111(19):432–434. doi: 10.1136/vr.111.19.432. [DOI] [PubMed] [Google Scholar]
  5. Gendelman H. E., Narayan O., Kennedy-Stoskopf S., Kennedy P. G., Ghotbi Z., Clements J. E., Stanley J., Pezeshkpour G. Tropism of sheep lentiviruses for monocytes: susceptibility to infection and virus gene expression increase during maturation of monocytes to macrophages. J Virol. 1986 Apr;58(1):67–74. doi: 10.1128/jvi.58.1.67-74.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Haas W., Kaufman S., Martinez C. The development and function of gamma delta T cells. Immunol Today. 1990 Oct;11(10):340–343. doi: 10.1016/0167-5699(90)90133-t. [DOI] [PubMed] [Google Scholar]
  7. Haase A. T. Pathogenesis of lentivirus infections. Nature. 1986 Jul 10;322(6075):130–136. doi: 10.1038/322130a0. [DOI] [PubMed] [Google Scholar]
  8. Holoshitz J., Koning F., Coligan J. E., De Bruyn J., Strober S. Isolation of CD4- CD8- mycobacteria-reactive T lymphocyte clones from rheumatoid arthritis synovial fluid. Nature. 1989 May 18;339(6221):226–229. doi: 10.1038/339226a0. [DOI] [PubMed] [Google Scholar]
  9. Hopkins J., Dutia B. M. Monoclonal antibodies to the sheep analogues of human CD45 (leucocyte common antigen), MHC class I and CD5. Differential expression after lymphocyte activation in vivo. Vet Immunol Immunopathol. 1990 Apr;24(4):331–346. doi: 10.1016/0165-2427(90)90004-c. [DOI] [PubMed] [Google Scholar]
  10. La Thangue N. B., Latchman D. S. A cellular protein related to heat-shock protein 90 accumulates during herpes simplex virus infection and is overexpressed in transformed cells. Exp Cell Res. 1988 Sep;178(1):169–179. doi: 10.1016/0014-4827(88)90388-6. [DOI] [PubMed] [Google Scholar]
  11. Mackay C. R., Beya M. F., Matzinger P. Gamma/delta T cells express a unique surface molecule appearing late during thymic development. Eur J Immunol. 1989 Aug;19(8):1477–1483. doi: 10.1002/eji.1830190820. [DOI] [PubMed] [Google Scholar]
  12. Mackay C. R., Maddox J. F., Gogolin-Ewens K. J., Brandon M. R. Characterization of two sheep lymphocyte differentiation antigens, SBU-T1 and SBU-T6. Immunology. 1985 Aug;55(4):729–737. [PMC free article] [PubMed] [Google Scholar]
  13. Mackay C. Sheep leukocyte molecules: a review of their distribution, structure and possible function. Vet Immunol Immunopathol. 1988 Jul;19(1):1–20. doi: 10.1016/0165-2427(88)90042-6. [DOI] [PubMed] [Google Scholar]
  14. Maddox J. F., Mackay C. R., Brandon M. R. Surface antigens, SBU-T4 and SBU-T8, of sheep T lymphocyte subsets defined by monoclonal antibodies. Immunology. 1985 Aug;55(4):739–748. [PMC free article] [PubMed] [Google Scholar]
  15. Meeusen E., Barcham G. J., Gorrell M. D., Rickard M. D., Brandon M. R. Cysticercosis: cellular immune responses during primary and secondary infection. Parasite Immunol. 1990 Jul;12(4):403–418. doi: 10.1111/j.1365-3024.1990.tb00977.x. [DOI] [PubMed] [Google Scholar]
  16. Mwangi D. M., Hopkins J., Luckins A. G. Immunohistology of lymph nodes draining local skin reactions (chancres) in sheep infected with Trypanosoma congolense. J Comp Pathol. 1991 Jul;105(1):27–35. doi: 10.1016/s0021-9975(08)80059-x. [DOI] [PubMed] [Google Scholar]
  17. Myer M. S., Huchzermeyer H. F., York D. F., Hunter P., Verwoerd D. W., Garnett H. M. The possible involvement of immunosuppression caused by a lentivirus in the aetiology of jaagsiekte and pasteurellosis in sheep. Onderstepoort J Vet Res. 1988 Sep;55(3):127–133. [PubMed] [Google Scholar]
  18. Nathanson N., Panitch H., Palsson P. A., Petursson G., Georgsson G. Pathogenesis of visna. II. Effect of immunosuppression upon early central nervous system lesions. Lab Invest. 1976 Nov;35(5):444–451. [PubMed] [Google Scholar]
  19. Oliver R. E., Gorham J. R., Parish S. F., Hadlow W. J., Narayan O. Ovine progressive pneumonia: pathologic and virologic studies on the naturally occurring disease. Am J Vet Res. 1981 Sep;42(9):1554–1559. [PubMed] [Google Scholar]
  20. Rácz P., Tenner-Rácz K., Kahl C., Feller A. C., Kern P., Dietrich M. Spectrum of morphologic changes of lymph nodes from patients with AIDS or AIDS-related complexes. Prog Allergy. 1986;37:81–181. doi: 10.1159/000318442. [DOI] [PubMed] [Google Scholar]
  21. Sonigo P., Alizon M., Staskus K., Klatzmann D., Cole S., Danos O., Retzel E., Tiollais P., Haase A., Wain-Hobson S. Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell. 1985 Aug;42(1):369–382. doi: 10.1016/s0092-8674(85)80132-x. [DOI] [PubMed] [Google Scholar]
  22. Spour E. F., Leemhuis T., Jenski L., Redmond R., Fillak D., Jansen J. Characterization of normal human CD3+ CD5- and gamma delta T cell receptor positive T lymphocytes. Clin Exp Immunol. 1990 Apr;80(1):114–121. doi: 10.1111/j.1365-2249.1990.tb06450.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. van der Molen E. J., Vecht U., Houwers D. J. A chronic indurative mastitis in sheep, associated with maedi/visna virus infection. Vet Q. 1985 Apr;7(2):112–119. doi: 10.1080/01652176.1985.9693966. [DOI] [PubMed] [Google Scholar]

Articles from Clinical and Experimental Immunology are provided here courtesy of British Society for Immunology

RESOURCES