1887

Abstract

Ovine lentiviruses and caprine arthritis-encephalitis virus (CAEV) are prototypic lentiviruses that replicate predominantly in macrophages of infected animals. In situ hybridization of pathologically affected tissues from diseased animals has shown that viral RNA exists in permissive macrophages as well as in non-macrophage cell types that do not support productive virus replication. These findings raise questions about the cellular tropism of these viruses in vivo and how this may relate to their pathogenesis and the establishment of persistent infections. In this study, the susceptibility of macrophages and fibro-epithelial cells derived from goat synovial membrane (GSM) to infection by 14 North American ovine lentivirus strains was examined. All 14 strains were macrophage-tropic, as indicated by expression of viral proteins and by fusion and development of syncytial cytopathic effects following co-culture of infected macrophages with GSM cells. In contrast, neither viral DNA nor viral proteins was detected in GSM cells inoculated with cell-free virus from nine of the 14 strains. Specific virus proteins were immunoprecipitated from restrictive GSM cells following culture with infected macrophages and serial passage of GSM cells to remove the macrophages. The lack of infection of GSM cells by cell-free virus from some ovine lentivirus field strains was circumvented by cell-associated virus infection from infected macrophages to GSM cells following cell-to-cell contact. This strategy could be one of the mechanisms involved in the escape from immune surveillance and establishment of persistent infection in infected animals.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-80-6-1437
1999-06-01
2022-08-16
Loading full text...

Full text loading...

/deliver/fulltext/jgv/80/6/0801437a.html?itemId=/content/journal/jgv/10.1099/0022-1317-80-6-1437&mimeType=html&fmt=ahah

References

  1. 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. American Journal of Pathology 146:250–263
    [Google Scholar]
  2. Chebloune Y., Sheffer D., Karr B. M., Stephens E., Narayan O. 1996a; Restrictive type of replication of ovine/caprine lentiviruses in ovine fibroblast cell cultures. Virology 222:21–30
    [Google Scholar]
  3. Chebloune Y., Karr B., Sheffer D., Leung K., Narayan O. 1996b; Variations in lentiviral gene expression in monocyte-derived macrophages from naturally infected sheep. Journal of General Virology 77:2037–2051
    [Google Scholar]
  4. Chebloune Y., Karr B. M., Raghavan R., Singh D. K., Leung K., Sheffer D., Pinson D., Foresman L., Narayan O. 1998; Neuroinvasion by ovine lentivirus in infected sheep mediated by inflammatory cells associated with experimental allergic encephalomyelitis. Journal of Neurovirology 4:38–48
    [Google Scholar]
  5. Crawford T. B., Adams D. S., Cheevers W. P., Cork L. C. 1980; Chronic arthritis in goats caused by a retrovirus. Science 207:997–999
    [Google Scholar]
  6. Deng H., Liu R., Ellmeier W., Choe S., Unutmaz D., Burkhart M., Di Marzio P., Marmon S., Sutton R. E., Hill C. M., Davis C. B., Peiper S. C., Schall T. J., Littman D. R., Landau N. R. 1996; Identification of a major co-receptor for primary isolates of HIV-1. Nature 381:661–666
    [Google Scholar]
  7. Doranz B. J., Rucker J., Yi Y., Smyth R. J., Samson M., Peiper S. C., Parmentier M., Collman R. G., Doms R. W. 1996; A dual-tropic primary HIV-1 isolate that uses fusin and the beta-chemokine receptors CKR-5, CKR-3, and CKR-2b as fusion cofactors. Cell 85:1149–1158
    [Google Scholar]
  8. Dragic T., Litwin V., Allaway G. P., Martin S. R., Huang Y., Nagashima K. A., Cayanan C., Maddon P. J., Koup R. A., Moore J. P., Paxton W. A. 1996; HIV-1 entry into CD4 + cells is mediated by the chemokine receptor CC-CKR-5. Nature 381:667–673
    [Google Scholar]
  9. Feng Y., Broder C. C., Kennedy P. E., Berger E. A. 1996; HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272:872–877
    [Google Scholar]
  10. 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. Proceedings of the National Academy of Sciences, USA 82:7086–7090
    [Google Scholar]
  11. 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. Journal of Virology 58:67–74
    [Google Scholar]
  12. 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. Journal of Virology 66:2679–2688
    [Google Scholar]
  13. Haase A. T., Retzel E. F., Staskus K. A. 1990; Amplification and detection of lentiviral DNA inside cells. Proceedings of the National Academy of Sciences USA 87:4971–4975
    [Google Scholar]
  14. Joag S. V., Stephens E. B., Adams R. J., Foresman L., Narayan O. 1994; Pathog enesis of SIVmac infection in Chinese and Indian rhesus macaques: effects of splenectomy on virus burden. Virology 200:436–446
    [Google Scholar]
  15. Kennedy-Stoskopf S., Narayan O., Strandberg J. D. 1985; The mammary gland as a target organ for infection with caprine arthritis-encephalitis virus. Journal of Comparative Pathology 95:609–617
    [Google Scholar]
  16. Koot M., Keet I. P. M., Vos A. H. V., de Goede R. E. Y., Roos M. T. L., Coutinho R. A., Miedema F., Schellekens P. T. A., Tersmette M. 1993; Prognostic value of HIV-1 syncytium-inducing phenotype for rate of CD4 + cell depletion and progression to AIDS. Annals of Internal Medicine 118:681–688
    [Google Scholar]
  17. Lairmore M. D., Akita G. Y., Russell H. I., DeMartini J. C. 1987; Replication and cytopathic effects of ovine lentivirus strains in alveolar macrophages correlate with in vivo pathogenicity. Journal of Virology 61:4038–4042
    [Google Scholar]
  18. Lairmore M. D., Poulson J. M., Adducci T. A., DeMartini J. C. 1988; Lentivirus-induced lymphoproliferative disease. Comparative pathogenicity of phenotypically distinct ovine lentivirus strains. American Journal of Pathology 130:80–90
    [Google Scholar]
  19. Lerondelle C., Fleury C., Vialard J. 1989; The mammary gland: target organ for infection with the caprine arthritis and encephalitis virus. Annales de Recherches Veterinaires 20:57–63 (in French)
    [Google Scholar]
  20. Mselli-Lakhal L., Guiguen F., Fornazero C., Du J., Favier C., Durand J., Grezel D., Mornex J. F., Chebloune Y. 1999; Goat milk epithelial cells are permissive to caprine arthritis encephalitis virus replication. Virology (in press)
    [Google Scholar]
  21. Narayan O., Griffin D. E., Silverstein A. M. 1977; Slow virus infection: replication and mechanisms of persistence of visna virus in sheep. Journal of Infectious Diseases 135:800–806
    [Google Scholar]
  22. Narayan O., Clements J. E., Strandberg J. D., Cork L. C., Griffin D. E. 1980; Biological characterization of the virus causing leukoencephalitis and arthritis in goats. Journal of General Virology 50:69–79
    [Google Scholar]
  23. 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. Infection and Immunity 41:67–73
    [Google Scholar]
  24. Petursson G., Nathanson N., Georgsson G., Panitch H., Palsson P. A. 1976; Pathog enesis of visna. I. Sequential virologic, serologic, and pathologic studies. Laboratory Investigation 35:402–412
    [Google Scholar]
  25. Querat G., Audoly G., Sonigo P., Vigne R. 1990; Nucleotide sequence analysis of SA-OMVV, a visna-related ovine lentivirus: phylogenetic history of lentiviruses. Virology 175:434–447
    [Google Scholar]
  26. Saltarelli M. J., Querat G., Konings D. A., Vigne R., Clements J. E. 1990; Nucleotide sequence and transcriptional analysis of molecular clones of CAEV which generate infectious virus. Virology 179:347–364
    [Google Scholar]
  27. Schuitemaker H., Kootstra N. A., de Goede R. E. Y., de Wolf F., Miedema F., Tersmette M. 1991; Monocytotropic human immunodeficiency virus type 1 (HIV-1) variants detectable in all stages of HIV-1 infection lack T-cell line tropism and syncytium-inducing ability in primary T-cell culture. Journal of Virology 65:356–363
    [Google Scholar]
  28. Sigurdsson B. 1954; Maedi, a slow progressive pneumonia of sheep: an epizoological and pathological study. British Veterinary Journal 110:255–270
    [Google Scholar]
  29. 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. Microbial Pathogenesis 11:67–76
    [Google Scholar]
  30. Tersmette M., Gruters R. A., de Wolf F., de Goede R. E. Y., Lange J. M. A., Schellekens P. T. A., Goudsmit J., Huisman H. G., Miedema F. 1989; Evidence for a role of virulent human immunodeficiency virus (HIV) variants in the pathogenesis of acquired immunodeficiency syndrome: studies on sequential HIV isolates. Journal of Virology 63:2118–2125
    [Google Scholar]
  31. Zhu T., Mo H., Wang N., Nam D. S., Cao Y., Koup R. A., Ho D. D. 1993; Genotypic and phenotypic characterization of HIV-1 in patients with primary infection. Science 261:1179–1181
    [Google Scholar]
  32. Zink M. C., Yager J. A., Myers J. D. 1990; Pathog enesis of caprine arthritis encephalitis virus. Cellular localization of viral transcripts in tissues of infected goats. American Journal of Pathology 136:843–854
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-80-6-1437
Loading
/content/journal/jgv/10.1099/0022-1317-80-6-1437
Loading

Data & Media loading...

Most cited this month Most Cited RSS feed

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