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. 1983 Jul;41(1):67–73. doi: 10.1128/iai.41.1.67-73.1983

Activation of caprine arthritis-encephalitis virus expression during maturation of monocytes to macrophages.

O Narayan, S Kennedy-Stoskopf, D Sheffer, D E Griffin, J E Clements
PMCID: PMC264744  PMID: 6862634

Abstract

Lentiviruses, which cause arthritis-encephalitis and maedi-visna in goats and sheep, respectively, cause persistent infections in these animals. The viruses replicate productively at low levels in macrophages in diseased organs such as the "maedi lung" and nonproductively in other cell types such as leukocytes in peripheral blood. Nonproductive infections become productive during in vitro cultivation of the cells. This study showed that monocytes were the only cells in the peripheral blood leukocytes of an infected animal in which virus was detected and that virus activation occurred only when these cells matured into macrophages. Only a minute fraction of cultured monocytes matured into macrophages, and viral infectivity was associated exclusively with this fraction. Antiglobulin-coated glass wool fragments were lethal for monocyte macrophages because of toxic phagocytosis, but had no effect on B or T lymphocytes. The simultaneous addition of the glass fragments and leukocytes to culture dishes resulted in no macrophage maturation and no virus production. The addition of the fragments to virus-producing macrophages caused the death of the cells and a decline in virus production. Virus production in less avidly phagocytic cells was unaffected by the glass. Thus, although macrophages may be permissive for virus replication, one mechanism for restricted virus expression in vivo may be physiological factors controlling the maturation of these cells.

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Selected References

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

  1. Alberto B. P., Callahan L. F., Pincus T. Evidence that retrovirus expression in mouse spleen cells results from B cell differentiation. J Immunol. 1982 Dec;129(6):2768–2772. [PubMed] [Google Scholar]
  2. Allison A. C., Harington J. S., Birbeck M. An examination of the cytotoxic effects of silica on macrophages. J Exp Med. 1966 Aug 1;124(2):141–154. doi: 10.1084/jem.124.2.141. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brahic M., Stowring L., Ventura P., Haase A. T. Gene expression in visna virus infection in sheep. Nature. 1981 Jul 16;292(5820):240–242. doi: 10.1038/292240a0. [DOI] [PubMed] [Google Scholar]
  4. Böyum A. Isolation of mononuclear cells and granulocytes from human blood. Isolation of monuclear cells by one centrifugation, and of granulocytes by combining centrifugation and sedimentation at 1 g. Scand J Clin Lab Invest Suppl. 1968;97:77–89. [PubMed] [Google Scholar]
  5. Cork L. C., Hadlow W. J., Crawford T. B., Gorham J. R., Piper R. C. Infectious leukoencephalomyelitis of young goats. J Infect Dis. 1974 Feb;129(2):134–141. doi: 10.1093/infdis/129.2.134. [DOI] [PubMed] [Google Scholar]
  6. Cork L. C., Narayan O. The pathogenesis of viral leukoencephalomyelitis-arthritis of goats. I. Persistent viral infection with progressive pathologic changes. Lab Invest. 1980 Jun;42(6):596–602. [PubMed] [Google Scholar]
  7. Cowing C., Pincus S. H., Sachs D. H., Dickler H. B. A subpopulation of adherent accessory cells bearing both I-A and I-E or C subregion antigens is required for antigen-specific murine T lymphocyte proliferation. J Immunol. 1978 Nov;121(5):1680–1686. [PubMed] [Google Scholar]
  8. Crawford T. B., Adams D. S., Cheevers W. P., Cork L. C. Chronic arthritis in goats caused by a retrovirus. Science. 1980 Feb 29;207(4434):997–999. doi: 10.1126/science.6153243. [DOI] [PubMed] [Google Scholar]
  9. De Boer G. F., Terpstra C., Houwers D. J., Hendriks J. Studies in epidemiology of maedi/visna in sheep. Res Vet Sci. 1979 Mar;26(2):202–208. [PubMed] [Google Scholar]
  10. Griffin D. E., Narayan O., Adams R. J. Early immune responses in visna, a slow viral disease of sheep. J Infect Dis. 1978 Sep;138(3):340–350. doi: 10.1093/infdis/138.3.340. [DOI] [PubMed] [Google Scholar]
  11. Haase A. T., Stowring L., Narayan P., Griffin D., Price D. Slow persistent infection caused by visna virus: role of host restriction. Science. 1977 Jan 14;195(4274):175–177. doi: 10.1126/science.188133. [DOI] [PubMed] [Google Scholar]
  12. Kenyon S. J., Piper C. E. Cellular basis of persistent lymphocytosis in cattle infected with bovine leukemia virus. Infect Immun. 1977 Jun;16(3):891–897. doi: 10.1128/iai.16.3.891-897.1977. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Lee K. C., Wong M. Functional heterogeneity of culture-grown bone marrow-derived macrophages. I. Antigen presenting function. J Immunol. 1980 Jul;125(1):86–95. [PubMed] [Google Scholar]
  14. Mage M. G., McHugh L. L., Rothstein T. L. Mouse lymphocytes with and without surface immunoglobulin: preparative scale separation in polystyrene tissue culture dishes coated with specifically purified anti-immunoglobulin. J Immunol Methods. 1977;15(1):47–56. doi: 10.1016/0022-1759(77)90016-3. [DOI] [PubMed] [Google Scholar]
  15. Marcelletti J., Furmanski P. Infection of macrophages with Friend virus: relationship to the spontaneous regression of viral erythroleukemia. Cell. 1979 Mar;16(3):649–659. doi: 10.1016/0092-8674(79)90038-2. [DOI] [PubMed] [Google Scholar]
  16. Narayan O., Clements J. E., Strandberg J. D., Cork L. C., Griffin D. E. Biological characterization of the virus causing leukoencephalitis and arthritis in goats. J Gen Virol. 1980 Sep;50(1):69–79. doi: 10.1099/0022-1317-50-1-69. [DOI] [PubMed] [Google Scholar]
  17. Narayan O., Griffin D. E., Silverstein A. M. Slow virus infection: replication and mechanisms of persistence of visna virus in sheep. J Infect Dis. 1977 May;135(5):800–806. doi: 10.1093/infdis/135.5.800. [DOI] [PubMed] [Google Scholar]
  18. Narayan O., Wolinsky J. S., Clements J. E., Strandberg J. D., Griffin D. E., Cork L. C. Slow virus replication: the role of macrophages in the persistence and expression of visna viruses of sheep and goats. J Gen Virol. 1982 Apr;59(Pt 2):345–356. doi: 10.1099/0022-1317-59-2-345. [DOI] [PubMed] [Google Scholar]
  19. Pétursson G., Nathanson N., Georgsson G., Panitch H., Pálsson P. A. Pathogenesis of visna. I. Sequential virologic, serologic, and pathologic studies. Lab Invest. 1976 Oct;35(4):402–412. [PubMed] [Google Scholar]
  20. Roberson S. M., McGuire T. C., Klevjer-Anderson P., Gorham J. R., Cheevers W. P. Caprine arthritis-encephalitis virus is distinct from visna and progressive pneumonia viruses as measured by genome sequence homology. J Virol. 1982 Nov;44(2):755–758. doi: 10.1128/jvi.44.2.755-758.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Roubin R., Zolla-Pazner S. Markers of macrophage heterogeneity. I. Studies of macrophages from various organs of normal mice. Eur J Immunol. 1979 Dec;9(12):972–978. doi: 10.1002/eji.1830091211. [DOI] [PubMed] [Google Scholar]
  22. SIGURDSSON B., PALSSON P., GRIMSSON H. Visna, a demyelinating transmissible disease of sheep. J Neuropathol Exp Neurol. 1957 Jul;16(3):389–403. doi: 10.1097/00005072-195707000-00010. [DOI] [PubMed] [Google Scholar]
  23. Schroff G., Neumann C., Sorg C. Transglutaminase as a marker for subsets of murine macrophages. Eur J Immunol. 1981 Aug;11(8):637–642. doi: 10.1002/eji.1830110809. [DOI] [PubMed] [Google Scholar]
  24. Sheffield W. D., Narayan O., Strandberg J. D., Adams R. J. Visna-maedi-like disease associated with an ovine retrovirus infection in a Corriedale sheep. Vet Pathol. 1980 Sep;17(5):544–552. doi: 10.1177/030098588001700503. [DOI] [PubMed] [Google Scholar]
  25. van Furth R. Current view of the mononuclear phagocyte system. Haematol Blood Transfus. 1981;27:3–10. doi: 10.1007/978-3-642-81696-3_1. [DOI] [PubMed] [Google Scholar]
  26. van oud Alblas A. B., van Furth R. Origin, Kinetics, and characteristics of pulmonary macrophages in the normal steady state. J Exp Med. 1979 Jun 1;149(6):1504–1518. doi: 10.1084/jem.149.6.1504. [DOI] [PMC free article] [PubMed] [Google Scholar]

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