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Ovine aortic smooth muscle cells allow the replication of visna-maedi virus in vitro

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Summary

Visna-maedi virus induces in sheep an interstitial lung disease characterised by an accumulation of smooth muscle cells (SMC) or myomatosis. Infection by HIV-1 has been recently associated with disorders of the vessel-derived cells: primary pulmonary hypertension, coronary artery disease and smooth muscle tumors in humans. We hypothesized that, besides their regular targets (i.e. macrophages and lymphocytes), lentiviruses could infect smooth muscle cells. Smooth muscle cell cultures derived from ovine aorta were infected with visna-maedi virus strain K1514. The cultured cells were smooth muscle cells as demonstrated by their antigenic expression of α-actin and vimentin. The lentiviral infection of the smooth muscle cells was demonstrated by a typical cytopathic effect (syncytia), the expression of virus specific antigens, and the presence of genomic RNA detected by Northern blot analysis and RT PCR. The detection of a reverse transcriptase activity, the presence of viral RNA in supernatants of infected smooth muscle cells detected by RT PCR and their ability to infect ovine permissive fibroblasts demonstrated a productive infection. The ability of smooth muscle cells to be infected by lentiviruses may participate in the pathogenesis of the tissue damage associated with the lentiviruses such as myomatosis in sheep and vascular disease in humans.

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References

  1. Baskerville A, Ramsay AD, Addis BJ, Dennis MJ, Cook RW, Cranage MP, Greenaway PJ (1992) Interstitial pneumonia in simian immunodeficiency virus infection. Am J Pathol 167: 241–247

    Google Scholar 

  2. Calabrese LH, Proffitt MR, Yen-Lieberman B, Hobbs RE, Ratliff NB (1987) Congestive cardiomyopathy and illness related to the acquired immunodeficiency syndrome (AIDS) associated with the isolation of retrovirus from myocardium. Ann Int Med 107: 691–692

    Google Scholar 

  3. Cao Y, Friedman-Kien AE, Huang Y, Mirabile M, Moudgil T, Zucker-Franklin D, Ho DD (1990) CD4-independent productive human immunodeficiency virus type 1 infection of hepatoma cell lines in vitro. J Virol 64: 2553–2559

    Google Scholar 

  4. Chalifoux LV, Simon MA, Pauley DR, MacKey JJ, Wyands MS, Ringler DJ (1992) Arteriopathy in macques infected with simian immunodeficiency virus. Lab Invest 67: 338–349

    Google Scholar 

  5. Chamley-Campbell J, Campbell GR, Ross R (1979) The smooth muscle cells in culture. Physiol Rev 59: 1–61

    Google Scholar 

  6. Crane SE, Buzy J, Clements JE (1991) Identification of cell membrane proteins that binds visna virus. J Virol 65: 6137–6143

    Google Scholar 

  7. Dalziel RG, Hopkins J, Watt NJ, Dutia BM, Clarke HA, McConnell I (1991) Identification of a putative cellular receptor for the lentivirus visna virus. J Gen Virol 72: 1905–1911

    Google Scholar 

  8. Folks TM, Kessler SW, Orenstein JM, Justement JS, Jaffe ES, Fauci AS (1988) Infection and replication of HIV-1 in purified progenitor cells of normal human bone marrow. Science 242: 919–922

    Google Scholar 

  9. Georgsson G, Houwers DJ, Palsson PA, Petursson G (1989) Expression of viral antigens in the central nervous system of visna-infected sheep: an immunohistochemical study on experimental visna induced by virus strains of increased virulence. Acta Neuropathol 77: 299–306

    Google Scholar 

  10. Georgsson G, Palsson PA (1971) The histopathology of maedi. A slow viral pneumonia of sheep. Vet Pathol 8: 63–80

    Google Scholar 

  11. Grody WW, Cheng L, Lewis W (1990) Infection of the heart by the human immunodeficiency virus. Am J Cardiol 66: 203–206

    Google Scholar 

  12. Hansson GK, Jonasson L, Holm J, Clowes MM, Clowes AW (1988) γ-interferon regulates vascular smooth muscle proliferation and Ia antigen expression in vivo and in vitro. Circ Res 63: 712–719

    Google Scholar 

  13. Harouse JM, Kunsch C, Hartle HT, Laughlin MA, Hoxie JA, Wigdall B, Gonzales-Scarano FG (1989) CD4-independent infection of human neural cells by human immunodeficiency virus type 1. J Virol 63: 2527–2533

    Google Scholar 

  14. Heise C, Dandekar S, Kumar P, Duplantier R, Donovan RM, Halsted C (1991) Human immunodeficiency virus infection of enterocytes and mononuclear cells in human jejunal mucosa. Gastroenterology 100: 1521–1527

    Google Scholar 

  15. Jonasson L, Holm J, Hansson GK (1988) Smooth muscle cells express Ia antigens during arterial response to injury. Lab Invest 3: 310–315

    Google Scholar 

  16. Kennedy-Stoskopf S, Zink MC, Narayan O (1989) Pathogenesis of ovine lentivirus-induced arthritis: phenotypic evaluation of T lymphocytes in synovial fluid, synovium, and peripheral circulation. Clin Immunol Immunopathol 52: 323–330

    Google Scholar 

  17. Koyagani Y, Miles S, Mitsuyasu RT, Merril JE, Vinters HV, Chen IS (1987) Dual infection of the central nervous system by AIDS viruses with distinct cellular tropisms. Science 236: 819–822

    Google Scholar 

  18. Lairmore MD, Butera ST, Callahan GN, DeMartini JC (1988) Spontaneous interferon production by pulmonary leukocytes is associated with lentivirus-induced lymphoid interstitial pneumonia. J Immunol 140: 779–785

    Google Scholar 

  19. Lyon M, Huppert J (1983) Depression of reverse activity by hybridoma supernatants: a potential problem in screening for retroviral contamination. Biochem Biophys Res Commun 112: 265–272

    Google Scholar 

  20. Mellert W, Kleinschmidt A, Schmidt J, Festl H, Emler S, Roth WK, Erfle V (1990) Infection of human fibroblast and osteoblast-like cells with HIV-1. AIDS 4: 527–535

    Google Scholar 

  21. Mette SA, Palevsky HI, Pietra GG, Williams TM, Bruder E, Prestipino AJ, Patrick AM, Wirth JA (1992) Primary pulmonary hypertension in association with human immunodeficiency virus infection: a possible viral etiology for some forms of hypertensive pulmonary arteriopathy. Am Rev Respir Dis 145: 1196–1200

    Google Scholar 

  22. Moyer MP, Huot RI, Ramirez A, Joe S, Meltzer MS, Gendelman HE (1990) Infection of human gastrointestinal cells by HIV-1. AIDS Res Hum Retroviruses 6: 1409–1415

    Google Scholar 

  23. Mueller BU, Butler KM, Higham MC, Husson RN, Montrella KA, Pizzo PA, Feuerstein IM, Manjunayh K (1992) Smooth muscle tumors in children with human immunodeficiency virus infection. Pediatrics 90: 460–463

    Google Scholar 

  24. Narayan O, Clements JE (1990) Lentiviruses. In: Fields BN, Knipe DM (eds) Virology. Raven Press, New York, pp 1571–1592

    Google Scholar 

  25. Plata F, Garcia-Pons F, Ryter A, Lebargy F, Goodenow MM, Dat MHQ, Autran B, Mayaud C (1990) HIV-1 infection of the lung alveolar fibroblasts and macrophages in humans. AIDS Res Hum Retroviruses 6: 979–986

    Google Scholar 

  26. Polos PG, Wolfe D, Harley RA, Strange C, Sahn SA (1992) Pulmonary hypertension and human immunodeficiency virus infection. Two reports and a review of literature. Chest 101: 474–478

    Google Scholar 

  27. Rodriguez ER, Nasim S, Hsia J, Sandin RL, Ferreira A, Hilliard BA, Ross AM, Garrett CT (1991) Cardiac myocytes and dendritic cells harbor human immunodeficiency virus in infected patients with and without cardiac dysfunction: detection by multiplex, nested, polymerase chain reaction in individually microdissected cells from right ventricular endomyocardial biopsy tissue. Am J Cardiol 68: 1511–1520

    Google Scholar 

  28. Sakaguchi M, Sato T, Groopman JE (1991) Human immunodeficiency virus infection of megakaryocytic cells. Blood 3: 481–485

    Google Scholar 

  29. Sigurdson B, Thormar M, Palsson PA (1960) Cultivation of visna virus in tissue culture. Arch Ges Virusforsch 10: 368–381

    Google Scholar 

  30. Sonigo P, Alizon M, Staskus K, Klatzmann D, Cole S, Danos O, Retzel E, Tiollais P, Haase AP, Wain-Hobson S (1985) Nucleotide sequence of the visna lentivirus: relationship to the AIDS virus. Cell 42: 369–382

    Google Scholar 

  31. Speir E, Modali R, Huang ES, Leon MB, Shawl F, Finkel T, Epstein SE (1994) Potential role of human cytomegalovirus and p53 interaction in coronary restenosis. Science 265: 391–394

    Google Scholar 

  32. Steffan AM, Lafon ME, Gendrault JL, Schweitzer C, Royer C, Jaeck D, Arnaud JP, Schmitt MP, Aubertin AM, Kirn A (1992) Primary cultures of endothelial cells from the human liver sinusoid are permissive for human immunodeficiency virus type 1. Proc Natl Acad Sci USA 89: 1582–1586

    Google Scholar 

  33. Tabib A, Greenland T, Mercier I, Loire R, Mornex JF (1992) Coronary lesions in young HIV positive subjects at necropsy. Lancet 340: 730

    Google Scholar 

  34. Tateno M, Gonzales-Scarano F, Levy JA (1989) Human immunodeficiency virus can infect CD4-negative human fibroblastoid cells. Proc Natl Acad Sci USA 86: 4287–4290

    Google Scholar 

  35. Vigne R, Barban V, Quérat G, Mazarin V, Gourdou I (1987) Transcription of visna virus during its lytic cycle: evidence for a sequential early and late gene expression. Virology 161: 218–227

    Google Scholar 

  36. Warner SJC, Friedman GB, Libby P (1989) Regulation of major histocompatibility gene expression in human vascular smooth muscle cells. Arteriosclerosis 9: 279–288

    Google Scholar 

  37. Zucker-Franklin D, Cao Y (1989) Megakaryocytes of human immunodeficiency virus-infected individuals express viral RNA. Proc Natl Acad Sci USA 86: 5595–5599

    Google Scholar 

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Leroux, C., Cordier, G., Mercier, I. et al. Ovine aortic smooth muscle cells allow the replication of visna-maedi virus in vitro. Archives of Virology 140, 1–11 (1995). https://doi.org/10.1007/BF01309719

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