1887

Journal of General Virology header logo

Volume 75, Issue 12

Feline immunodeficiency virus can productively infect cultured endothelial cells from cat brain microvessels Free

Abstract

Feline immunodeficiency virus (FIV) provokes a disease in cats characterized by histopathological lesions similar to those observed in AIDS patients. In order to determine whether endothelial cells from brain microvessels are involved in the central nervous system disease to the same extent as macrophages and microglia, cells were isolated from healthy cat brains, cultured and infected with the FIV Villefranche IFFA 1/88 strain. The isolated cells displayed typical endothelial cell ultrastructural features and were characterized further by von Willebrand factor-labelling and the binding of specific lectins such as lectin on their membrane. They were also able to take up acetylated low density lipoproteins. Two weeks after infection, significant amounts of FIV p24 antigen were detected by indirect immunofluorescence in syncytia and single cells. Concomitantly, the same antigen could be detected in the culture medium of the infected cells by an ELISA technique. Numerous viral particles as well as different steps in the process of viral budding were observed under transmission electron microscopy. The synthesis of FIV p24 antigens still occurred in cells in which replication was blocked in the G phase with taxol. Our results suggest the possibility of a productive infection of brain microvascular endothelial cells by FIV , which could lead to important perturbations in the functions of the blood-brain barrier.

  • Received:
  • Accepted:
  • Published Online:
© The Journal of General Virology 1994
Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-75-12-3647
1994-12-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/jgv/75/12/JV0750123647.html?itemId=/content/journal/jgv/10.1099/0022-1317-75-12-3647&mimeType=html&fmt=ahah

References

  1. Beebe A. M., Dua N., Faith T. G., Moore P. F., Pedersen N. C., Dandekar S. 1994; Primary stage of feline immunodeficiency virus infection: viral dissemination and cellular targets. Journal of Virology 68:3080–3091
     [Google Scholar]
  2. Brinkmann R., Schwinn A., Narayan O., Zink C., Kreth H. W., Roggendorf W., Dörries R., Schwender S., Imrich H., ter Meulen V. 1992; Human immunodeficiency virus infection in microglia: correlation between cells infected in the brain and cells cultured from infectious brain tissue. Annals of Neurology 31:361–365
     [Google Scholar]
  3. Brooks B. R., Madden R., Stone C. M., Schultz K. T., Panga-Niban A., Eckdahl T. 1991; Simian immunodeficiency virus (SlV)-cell interactions in vitro: productive SIV infection is enhanced in large vessel aortic and central nervous system (CNS) white matter and testis gradient purified microvascular endothelial cells (EC). Proceedings of the IXth Symposium on Nonhuman Primate Models for AIDS, Seattle Abstract 56
    [Google Scholar]
  4. Brüstle O., Spiegel H., Leib S. L., Finn T., Stein H., Kleihues P., Wiestler O. D. 1992; Distribution of human immunodeficiency virus (HIV) in the CNS of children with severe HIV encephalo-myelopathy. Acta Neuropalhologica 84:24–31
     [Google Scholar]
  5. Budka H., Costanzi G., Cristina S., Lechi A., Parravicini C., Trabattoni R., Vago L. 1987; Brain pathology induced by infection with the human immunodeficiency virus (HIV). A histological, immunocytochemical, and electron microscopical study of 100 autopsy cases. Acta Neuropathologica 75:185–198
     [Google Scholar]
  6. Burns D. K. 1992; The neuropathology of pediatric acquired immunodeficiency syndrome. Journal of Child Neurology 7:332–346
     [Google Scholar]
  7. Chakrabarti L., Hurtrel M., Maire M. A., Vazeux R., Dormont D., Montagnier L., Hurtrel B. 1991; Early viral replication in the brain of SIV-infected rhesus monkeys. American Journal of Pathology 139:1273–1280
     [Google Scholar]
  8. Chakrabarti R., Hofman F. M., Pandey R., Mathes L. E., Roy-Burman P. 1994; Recombination between feline exogenous and endogenous retroviral sequences generates tropism for cerebral endothelial cells. American Journal of Pathology 144:348–358
     [Google Scholar]
  9. Clapham P. R., Weber J. N., Whitby D., Mcintosh K., Dalgleish A. G., Maddon P. J., Deen K. C., Sweet R. W., Weiss R. A. 1989; Soluble CD4 blocks the infectivity of diverse strains of HIV and SIV for T cells and monocytes but not for brain and muscle cells. Nature; London: 337368–370
     [Google Scholar]
  10. Connor R. I., Ho D. D. 1992; Pathogenesis of human immunodeficiency virus. Seminars in Virology 3:213–224
     [Google Scholar]
  11. Dorovini-Zis K., Prameya R., Bowman P. D. 1991; Culture and characterization of microvascular endothelial cells derived from human brain. Laboratory Investigation 64:425–436
     [Google Scholar]
  12. Dow S. W., Poss M. L., Hoover E. A. 1990; Feline immunodeficiency virus: a neurotropic lentivirus. Journal of Acquired Immune Deficiency Syndromes 3:658–668
     [Google Scholar]
  13. Dow S. W., Dreitz M. J., Hoover E. A. 1992; Feline immunodeficiency virus neurotropism: evidence that astrocytes and microglia are the primary target cells. Veterinary Immunology and Immuno-pathology 3:23–35
     [Google Scholar]
  14. Drouet L., Scrobohaci M. L., Janier M., Baudin B. 1990; Endothelial cells: target for the HIV1 virus?. Nouvelle Revue Frangaise d’Hémalotogie 32:103–106
     [Google Scholar]
  15. Engelberg H. 1989; Endothelium in health and disease. Seminars in Thrombosis and Hemostasis 15:178–183
     [Google Scholar]
  16. Epstein L. G., Gendelman H. E. 1993; Human immunodeficiency virus type 1 infection of the nervous system: pathogenetic mechanisms. Annals of Neurology 33:429–436
     [Google Scholar]
  17. Epstein L. G., Sharer L. R., Cho E. S., Myenhofer M., Navia B. A., Price R. W. 1985; HTLV-III/LAV-like retrovirus particles in the brains of patients with AIDS encephalopathy. AIDS Research 1:447–454
     [Google Scholar]
  18. Ewert D. L., Steiner I., Duhadaway J. 1990; In ovo infection with the avian retrovirus RAV-1 leads to persistent infection of the central nervous system. Laboratory Investigation 62:156–162
     [Google Scholar]
  19. Geleziunas R., Schipper H. M., Wainberg M. A. 1992; Pathogenesis and therapy of HIV-1 infection of the central nervous system. AIDS 6:1411–1426
     [Google Scholar]
  20. Genis P., Jett M., Bernton E. W., Boyle T., Gelbard H. A., Dzenko K., Keane R. W., Resnick L., Mizrachi Y., Volsky D. J., Epstein L. G., Gendelman H. E. 1992; Cytokines and arachidonic metabolites produced during human immunodeficiency virus (HlV)-infected macrophage-astroglia interactions: implication for the neuropathogenesis of HIV disease. Journal of Experimental Medicine 176:1703–1718
     [Google Scholar]
  21. Gonzalez-Scarano F., Harouse J. M., Kenny J. J., Kunsch C., Spitalnik S. L., Wigdahl B. 1992; Human immunodeficiency virus infection of neural cells. Seminars in Virology 3:225–234
     [Google Scholar]
  22. Gray F., Hurtrel M., Hurtrel B. 1993; Early central nervous system changes in human immunodeficiency virus (HlV)-infection. Neuropathology and Applied Neurobiology 19:3–9
     [Google Scholar]
  23. Gyorkey F., Melnick J. L., Gyorkey P. 1987; Human immunodeficiency virus in brain biopsies of patients with AIDS and progressive encephalopathy. Journal of Infectious Diseases 155:870–876
     [Google Scholar]
  24. Hall W. W., Farmer P. M., Takahashi H., Tanaka S., Furuta Y., Nagashima K. 1991; Pathological features of virus infections of the central nervous system (CNS) in the acquired immunodeficiency syndrome (AIDS). Acta Pathologica Japonica 41:172–181
     [Google Scholar]
  25. Holthöfer H., Virtanen I., Kariniemi A. L., Hormia M., Linder E., Miettinen A. 1982; Ulex europaeus I lectin as a marker for vascular endothelium in human tissues. Laboratory Investigation 47:60–66
     [Google Scholar]
  26. Hurtrel M., Ganiere J. P., Guelfi J. F., Chakrabarti L., Maire M. A., Gray F., Montagnier L., Hurtrel B. 1992; Comparison of early and late feline immunodeficiency virus encephalopathies. AIDS 6:399–406
     [Google Scholar]
  27. Kawaguchi Y., Maeda K., Tohya Y., Furuya T., Miyazawa T., Horimoto T., Norimine J., Kai C., Mikami T. 1992; Replicative difference in early-passage feline brain cells among feline immunodeficiency virus isolates. Archives of Virology 125:347–354
     [Google Scholar]
  28. Kay D. G., Gravel C., Robitaille Y., Jolicoeur P. 1991; Retrovirus-induced spongiform myeloencephalopathy in mice: regional distribution of infected target cells and neuronal loss occurring in the absence of viral expression in neurons. Proceedings of the National Academy of Sciences, U.S.A 88:1281–1285
     [Google Scholar]
  29. Koenig S., Gendelman H. E., Orenstein J. M., Dal Canto M. C., Pezeshkpour G. H., Yungbluth M., Janotta F., Aksamit A., Martin M. A., Fauci A. S. 1986; Detection of AIDS virus in macrophages in brain tissue from AIDS patients with encephalopathy. Science 233:1089–1093
     [Google Scholar]
  30. Kure K., Lyman W. D., Weidenheim K. M., Dickson D. W. 1990; Cellular localization of an HIV-1 antigen in subacute AIDS encephalitis using an improved double-labeling immunohistochemi-cal method. American Journal of Pathology 136:1085–1092
     [Google Scholar]
  31. Lackner A. A., Smith M. O., Munn R. J., Martfeld D. J., Gardner M. B., Marx P. A., Dandekar S. 1991; Localization of simian immunodeficiency virus in the central nervous system of rhesus monkeys. American Journal of Pathology 139:609–621
     [Google Scholar]
  32. Lafeuillade A., Alessi M. C., Poizot-Martin I., Boyer-Neumann C., Zandotti C., Quilichini R., Aubert L., Tamalet C., Juhan-Vague I., Gastaut J. A. 1992; Endothelial cell dysfunction in HIV infection. Journal of Acquired Immune Deficiency Syndromes 5:127–131
     [Google Scholar]
  33. Lewis P., Hensel M., Emerman M. 1992; Human immunodeficiency virus infection of cells arrested in the cell cycle. EMBO Journal 11:3053–3058
     [Google Scholar]
  34. Li X. L., Moudgil T., Vinters H. V., Ho D. D. 1990; CD4-independent, productive infection of a neuronal cell line by human immunodeficiency virus type 1. Journal of Virology 64:1383–1387
     [Google Scholar]
  35. Masuda M., Hoffman P. M., Ruscetti S. K. 1993; Viral determinants that control the neuropathogenicity of PVC-211 murine leukemia virus in vivo determine brain capillary endothelial cell tropism of the virus in vitro . Journal of Virology 67:4580–4587
     [Google Scholar]
  36. Mirra S. S., del Rio C. 1989; The fine structure of acquired immunodeficiency syndrome encephalopathy. Archives of Pathology and Laboratory Medicine 113:858–865
     [Google Scholar]
  37. Moses A. V., Bloom F. E., Pauza C. D., Nelson J. A. 1993; Human immunodeficiency virus infection of human brain capillary endothelial cells occurs via a CD4/galactosylceramide-independent mechanism. Proceedings of the National Academy of Sciences, U.S.A 90:10474–10478
     [Google Scholar]
  38. Park B. H., Lavi E., Blank K., Gaulton G. N. 1993; Intercerebral hemorrhages and syncytium formation induced by endothelial cell infection with a murine leukemia virus. Journal of Virology 67:6015–6024
     [Google Scholar]
  39. Park B. H., Lavi E., Stieber A., Gaulton G. N. 1994; Pathogenesis a cerebral infarction and hemorrhage induced by a murine leukemia virus. Laboratory Investigation 71:78–85
     [Google Scholar]
  40. Parravicini C. L., Petrén A. L., Vago L., Costanzi G., Gluckman J. C., Gallo R. C., Biberfeld P. 1989; HIV encephalopathy and lymphadenopathy: cells associated with viral antigens. Acta Pathologica, Microbiologica et Immunologica Scandinavica Supplementum 8:33–39
     [Google Scholar]
  41. Phillips T. R., Talbott R. L., Lamont C., Muir S., Lovelace K., Elder J. H. 1990; Comparison of two host cell range variants of feline immunodeficiency virus. Journal of Virology 64:4605–4613
     [Google Scholar]
  42. Popovic M., Mellert W., Erfle V., Gartner S. 1988; Role of mononuclear phagocytes and accessory cells in human immunodeficiency virus type I infection of the brain. Annals of Neurology Supplementum 23:S74–S77
     [Google Scholar]
  43. Power C., Kong P. A., Crawford T. O., Wesselingh S., Glass J. D., Mcarthur J. C., Trapp B. D. 1993; Cerebral white matter changes in acquired immunodeficiency syndrome dementia: alterations of the blood-brain barrier. Annals of Neurology 34:339–350
     [Google Scholar]
  44. Pumarola-Sune T., Navia B. A., Cordon-Cardo C., Cho E. S., Price R. W. 1987; HIV antigen in the brains of patients with the AIDS dementia complex. Annals of Neurology 21:490–496
     [Google Scholar]
  45. Rao C., Anzil A. P., Hollenberg Sher J. 1993; The neuropathology of AIDS: a review. Advances in Neuroimmunology 3:1–15
     [Google Scholar]
  46. Rosenblum W. I. 1986; Aspects of endothelial malfunction and function in cerebral microvessels. Laboratory Investigation 55:252–268
     [Google Scholar]
  47. Rostad S. W., Sumi S. M., Shaw C. M., Olson C., Mcdougall J. K. 1987; Human immunodeficiency virus (HIV) infection in brains with AIDS-related leukoencephalopathy. AIDS Research and Human Retroviruses 3:363–373
     [Google Scholar]
  48. Sasseville V. G., Newman W. A., Lackner A. A., Smith M. O., Lausen N. C. G., Beall D., Ringler D. J. 1992; Elevated vascular cell adhesion molecule-1 in AIDS encephalitis induced by simian immunodeficiency virus. American Journal of Pathology 141:1021–1030
     [Google Scholar]
  49. Schiff P. B., Horwitz S. B. 1980; Taxol stabilizes microtubules in mouse fibroblast cells. Proceedings of the National Academy of Sciences, U.S.A 77:1561–1565
     [Google Scholar]
  50. Sharer L. R. 1992; Pathology of HIV-1 infection of the central nervous system. A review. Journal of Neuropathology and Experimental Neurology 51:3–11
     [Google Scholar]
  51. Smith T. W., Degirolami U., Henin D., Bolgert F., Hauw J. J. 1990; Human immunodeficiency virus (HIV) leukoencephalopathy and the microcirculation. Journal of Neuropathology and Experimental Neurology 49:357–370
     [Google Scholar]
  52. Steffan A. M., Lafon M. E., Gendrault J. L., Schweitzer C., Royer C., Jaeck D., Arnaud J. P., Schmitt M. P., Aubertin A. M., Kirn A. 1992; Primary cultures of endothelial cells from the human liver sinusoid are permissive for human immunodeficiency virus type 1. Proceedings of the National Academy of Sciences, U.S.A 89:1582–1586
     [Google Scholar]
  53. Steffan A. M., Lafon M. E., Gendrault J. L., Nonnenmacher H., Koehren F., Gut J. P., de Monte M., Martin J. P., Royer C., Kirn A. 1993; The feline immunodeficiency virus (FIV) productively infects endothelial cells of the cat liver sinusoid in vitro . In Cells of the Hepatic Sinusoid 4 pp. 117–120 Knook D. L., Wisse E. Edited by Leiden: The Kupffer Cell Foundation;
     [Google Scholar]
  54. Teitel J. M., Shore A., Read S. E., Schiavone A. 1989; Immune function of vascular endothelial cells is impaired by HIV. Journal of Infectious Diseases 160:551–552
     [Google Scholar]
  55. Voyta J. C., Via D. P., Butterfield C. E., Zetter B. R. 1984; Identification and isolation of endothelial cells based on their increased uptake of acetylated-low density lipoprotein. Journal of Cell Biology 99:2034–2040
     [Google Scholar]
  56. Ward J. M., O’Leary T. J., Baskin G. B., Benveniste R., Harris C. A., Nara P. L., Rhodes R. H. 1987; Immunohistochemical localization of human and simian immunodeficiency viral antigens in fixed tissue sections. American Journal of Pathology 127:199–205
     [Google Scholar]
  57. Wiley C. A., Nelson J. A. 1988; Role of human immunodeficiency virus and cytomegalovirus in AIDS encephalitis. American Journal of Pathology 133:73–81
     [Google Scholar]
  58. Wiley C. A., Schrier R. D., Nelson J. A., Lampert P. W., Oldstone M. B. A. 1986; Cellular localization of human immunodeficiency virus infection within the brains of acquired immune deficiency syndrome patients. Proceedings of the National Academy of Sciences, U.S.A 83:7089–7093
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-75-12-3647
Loading
Feline immunodeficiency virus can productively infect cultured endothelial cells from cat brain microvessels
J. Gen. Virol. 75, 3647 (1994); https://doi.org/10.1099/0022-1317-75-12-3647
/content/journal/jgv/10.1099/0022-1317-75-12-3647
/content/journal/jgv/10.1099/0022-1317-75-12-3647
Loading

Data & Media loading...

Most cited 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