1887

Abstract

The oncogenic retrovirus bovine leukaemia virus (BLV) primarily infects B cells. Most infected animals remain asymptomatic for long periods of time before an increase in circulating B cells or localized tumours can be observed. This long clinical latency period may be explained by cells of the monocyte/macrophage lineage (M/M) becoming infected and acting as a reservoir for the virus, as shown for other retroviruses (human immunodeficiency virus-1, feline immunodeficiency virus). M/M cells in different stages of differentiation (HL-60, THP-1, U-937, J774, BGM, PM2, primary macrophages of sheep and cows) were cultured with BLV produced by permanently infected donor cells (FLKBLV and BLV-bat). Donor cells were inhibited from multiplying by either irradiation or treatment with mitomycin C. In other experiments, supernatant from donor cells containing virus was used. In co-culture with the donor cells, the less differentiated monocytic cells showed severe cellular changes such as differentiation, vacuolization, cell lysis and membrane blebbing; apoptosis was a frequent phenomenon. Budding and extracellular viruses were also observed. The more differentiated macrophage cells, although they showed less signs of infection by microscopy, had a complete BLV protein profile, as seen by Western blotting; bands corresponding to p24CA (Gag) and its precursors were clearly seen. In addition, gp51SU was identified by syncytia formation assays. It is concluded that M/M cells may be infected by BLV, the consequences of the infection differing according to the type of cell.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/0022-1317-81-1-109
2000-01-01
2024-03-29
Loading full text...

Full text loading...

/deliver/fulltext/jgv/81/1/0810109a.html?itemId=/content/journal/jgv/10.1099/0022-1317-81-1-109&mimeType=html&fmt=ahah

References

  1. Burny, A., Cleuter, Y., Kettmann, R., Mammerickx, M., Marbaix, G., Portetelle, D., Van den Broeke, A., Willems, L. & Thomas, R. (1988). Bovine leukemia: facts and hypotheses derived from the study of an infectious cancer. Advances in Veterinary Science and Comparative Medicine 32, 149-170. [Google Scholar]
  2. Calafat, J. & Ressang, A. A. (1977). Morphogenesis of bovine leukemia virus. Virology 80, 42-53.[CrossRef] [Google Scholar]
  3. Cascales, M., Alvarez, A., Gasco, P., Fernandez-Simon, L., Sanz, N. & Bosca, L. (1994). Cocaine-induced liver injury in mice elicits specific changes in DNA ploidy and induces programmed death of hepatocytes. Hepatology 20, 992-1001.[CrossRef] [Google Scholar]
  4. Collins, S. J., Ruscetti, F. W., Gallagher, R. E. & Gallo, R. C. (1978). Terminal differentiation of human promyelocytic leukemia cells induced by dimethyl sulfoxide and other polar compounds. Proceedings of the National Academy of Sciences, USA 75, 2458-2462.[CrossRef] [Google Scholar]
  5. Dekegel, D. (1987). Morphology of bovine leukemia virus. In Enzootic Bovine Leukosis and Bovine Leukosis Virus, pp. 91-96. Edited by A. Burny & M. Mammerickx. Boston: Martinus Nijhoff.
  6. Dequiedt, F., Hanon, E., Kerkhofs, P., Pastoret, P.-P., Portetelle, D., Burny, A., Kettmann, R. & Willems, L. (1997). Both wild-type and strongly attenuated bovine leukemia viruses protect peripheral blood mononuclear cells from apoptosis. Journal of Virology 71, 630-639. [Google Scholar]
  7. Dequiedt, F., Cantor, G. H., Hamilton, V. T., Pritchard, S. M., Davis, W. C., Kerkhofs, P., Burny, A., Kettmann, R. & Willems, L. (1999). Bovine leukemia virus-induced persistent lymphocytosis in cattle does not correlate with increased ex vivo survival of B lymphocytes. Journal of Virology 73, 1127-1137. [Google Scholar]
  8. de Revel, T., Mabondzo, A., Gras, G., Delord, B., Roques, P., Boussin, F., Neveux, Y., Bahuau, M., Fleury, H. J. & Dormont, D. (1993).In vitro infection of human macrophages with human T-cell leukemia virus type 1. Blood 81, 1598-1606. [Google Scholar]
  9. Dittmer, U., Petry, H., Stahl-Hennig, C., Nisslein, T., Spring, M., Luke, W., Bodemer, W., Kaup, F. J. & Hunsmann, G. (1996). T cell apoptosis in human immunodeficiency virus type 2- and simian immunodeficiency virus-infected macaques. Journal of General Virology 77, 2433-2436.[CrossRef] [Google Scholar]
  10. Doménech, A., Llames, L., Goyache, J., Suárez, G. & Gómez-Lucı́a, E. (1997). Macrophages infected with bovine leukemia virus (BLV) induce humoral response in rabbits. Veterinary Immunology and Immunopathology 58, 309-320.[CrossRef] [Google Scholar]
  11. Fischinger, P. J., Blevins, C. S. & Nomura, S. (1974). Simple quantitative assay for both xenotropic murine leukemia and ecotropic feline leukemia viruses. Journal of Virology 14, 177-179. [Google Scholar]
  12. Fossum, C., Burny, A., Portetelle, D., Mammerickx, M. & Morein, B. (1988). Detection of B and T cells, with lectins or antibodies, in healthy and bovine leukemia virus-infected cattle. Veterinary Immunology and Immunopathology 18, 269-278.[CrossRef] [Google Scholar]
  13. Fujita, M. & Shiku, H. (1995). Differences in sensitivity to induction of apoptosis among rat fibroblast cells transformed by HTLV-I tax gene or cellular nuclear oncogenes. Oncogene 11, 15-20. [Google Scholar]
  14. Gougeon, M. L. & Montagnier, L. (1993). Apoptosis in AIDS. Science 260, 1269-1270.[CrossRef] [Google Scholar]
  15. Graves, D. C. & Ferrer, J. F. (1976).In vitro transmission and propagation of the bovine leukemia virus in monolayer cell cultures. Cancer Research 36, 4152-4159. [Google Scholar]
  16. Heeney, J. L., Valli, P. J. S., Jacobs, R. M. & Valli, V. E. O. (1992). Evidence for bovine leukemia virus infection of peripheral blood monocytes and limited antigen expression in bovine lymphoid tissue. Laboratory Investigation 66, 608-617. [Google Scholar]
  17. Hoffman, P. M., Dhib-Jalbut, S., Mikovits, J. A., Robbins, D. S., Wolf, A. L., Bergey, G. K., Lohrey, N. C., Weislow, O. S. & Ruscetti, F. W. (1992). Human T-cell leukemia virus type I infection of monocytes and microglial cells in primary human cultures. Proceedings of the National Academy of Sciences, USA 89, 1784-1788. [Google Scholar]
  18. Karimi, S. T., Schloemer, R. H. & Wilde, C. E. (1989). Accumulation of chlamydial lipopolysaccharide antigen in the plasma membranes of infected cells. Infection and Immunity 57, 1780-1785. [Google Scholar]
  19. Kettmann, R., Burny, A., Callebaut, I., Droogmans, L., Mammerickx, M., Willems, L. & Portetelle, D. (1994). Bovine leukemia virus. In The Retroviridae, pp. 39-81. Edited by J. A. Levy. New York: Plenum.
  20. Lagarias, D. M. & Radke, K. (1989). Transcriptional activation of bovine leukemia virus in blood cells from experimentally infected, asymptomatic sheep with latent infections. Journal of Virology 63, 2099-2107. [Google Scholar]
  21. Li, C. J., Friedman, D. J., Wang, C., Metelev, V. & Pardee, A. B. (1995). Induction of apoptosis in uninfected lymphocytes by HIV-1 tat protein. Science 268, 429-431.[CrossRef] [Google Scholar]
  22. Malorni, W., Rivabene, R., Santini, M. T. & Donelli, G. (1993).N-Acetylcysteine inhibits apoptosis and decreases viral particles in HIV-chronically infected U-937 cells. FEBS Letters 32, 75-78. [Google Scholar]
  23. Meiron, R., Brenner, J., Gluckman, A., Avraham, R. & Trainin, Z. (1985). Humoral and cellular responses in calves experimentally infected with bovine leukemia virus (BLV). Veterinary Immunology and Immunopathology 9, 105-114.[CrossRef] [Google Scholar]
  24. Mirsky, M. L., Olmstead, C. A., Da, Y. & Lewin, H. A. (1996). The prevalence of proviral bovine leukemia virus in peripheral blood mononuclear cells at two subclinical stages of infection. Journal of Virology 70, 2178-2183. [Google Scholar]
  25. Momoi, Y., Mizuno, T., Nishimura, Y., Endo, Y., Ohno, K., Watari, T., Goitsuka, R., Tsujimoto, H. & Hasegawa, A. (1996). Detection of apoptosis induced in peripheral blood lymphocytes from cats infected with feline immunodeficiency virus. Archives in Virology 141, 1651-1659.[CrossRef] [Google Scholar]
  26. Mussgay, M. & Kaaden, O. R. (1978). Progress in studies on the etiology and serologic diagnosis of enzootic bovine leukosis. Current Topics in Microbiology and Immunology 79, 43-72. [Google Scholar]
  27. Narayan, O. & Zink, M. C. (1988). Role of macrophages in lentivirus infections. Advances in Veterinary Science and Comparative Medicine 32, 129-147. [Google Scholar]
  28. Paul, P., Pomeroy, K., Castro, A., Johnson, D., Muscoplat, C. & Sorensen, D. (1977). Detection of bovine leukemia virus in B-lymphocytes by the syncytia induction assay. Journal of National Cancer Institute 5, 1269-1272. [Google Scholar]
  29. Powers, M. A. & Radke, K. (1992). Activation of bovine leukemia virus transcription in lymphocytes from infected sheep: rapid transition through early to late gene expression. Journal of Virology 66, 4769-4777. [Google Scholar]
  30. Pyeon, D. & Splitter, G. A. (1998). Interleukin-12 p40 mRNA expression in bovine leukemia virus-infected animals: increase in alymphocytosis but decrease in persistent lymphocytosis. Journal of Virology 72, 6917-6921. [Google Scholar]
  31. Pyeon, D., O’Reilly, K. L. & Splitter, G. A. (1996). Increased interleukin-10 mRNA expression in tumor-bearing or persistently lymphocytotic animals infected with bovine leukemia virus. Journal of Virology 70, 5706-5710. [Google Scholar]
  32. Radke, K. (1994). Bovine leukemia virus. In Encyclopedia of Virology, pp. 166–174. New York: Academic Press.
  33. Radke, K., Sigala, T. J. & Grossman, D. (1992). Transcription of bovine leukemia virus in peripheral blood cells obtained during early infection in vivo. Microbial Pathogenesis 12, 319-331.[CrossRef] [Google Scholar]
  34. Ralph, P. & Nakoinz, I. (1975). Phagocytosis and cytolysis by a macrophage tumour and its cloned cell line. Nature 257, 393-394.[CrossRef] [Google Scholar]
  35. Reinacher, M., Thurmond, M. C., Onuma, M., Portetelle, D., Picanso, J. & Theilen, G. H. (1989). Immunohistological demonstration of virus and tumor associated antigens in tissues in experimental and spontaneous bovine leukemia virus (BLV) infection. Veterinary Immunology and Immunopathology 22, 223-231.[CrossRef] [Google Scholar]
  36. Rojko, J. L., Fulton, R. M., Rezanka, L. J., Williams, L. L., Copelan, E., Cheney, C. M., Reichel, G. S., Neil, J. C., Mathes, L. E. & Fisher, T. G. (1992). Lymphocytotoxic strains of feline leukemia virus induce apoptosis in feline T4-thymic lymphoma cells. Laboratory Investigation 66, 418-426. [Google Scholar]
  37. Schwartz, I., Bensaid, A., Polack, B., Perrin, B., Berthelemy, M. & Levy, D. (1994).In vivo leukocyte tropism of bovine leukemia virus in sheep and cattle. Journal of Virology 68, 4589-4596. [Google Scholar]
  38. Schwartz-Cornil, I., Chevallier, N., Belloc, C., Le Rhun, D., Laine, V., Berthelemy, M., Mateo, A. & Levy, D. (1997). Bovine leukaemia virus-induced lymphocytosis in sheep is associated with reduction of spontaneous B cell apoptosis. Journal of General Virology 78, 153-162. [Google Scholar]
  39. Sundström, C. & Nilsson, K. (1976). Establishment and characterization of a human histiocytic lymphoma cell line (U-937). International Journal of Cancer 17, 565-577.[CrossRef] [Google Scholar]
  40. Tsuchiya, S., Yamabe, M., Yamaguchi, Y., Kobayashi, Y., Konno, T. & Tada, K. (1980). Establishment and characterization of a human acute monocytic leukemia cell line (THP-1). International Journal of Cancer 26, 171-176.[CrossRef] [Google Scholar]
  41. Tsukahara, T., Kannagi, M., Ohashi, T., Kato, H., Arai, M., Nunez, G., Iwanaga, Y., Yamamoto, N., Ohtani, K., Nakamura, M. & Fujii, M. (1999). Induction of bcl-x(L) expression by human T-cell leukemia virus type 1 tax through NF-κB in apoptosis-resistant T-cell transfectants with Tax. Journal of Virology 73, 7981-7987. [Google Scholar]
  42. Van der Maaten, M. J. & Miller, J. M. (1976). Replication of bovine leukemia virus in monolayer cell cultures. In Comparative Leukemia Research. Bibl Haemat 43, pp. 260-362. Edited by J. Clemmesen & D. S. Yohn. Basel: S. Karger AG.
  43. Van der Maaten, M. J., Miller, J. M. & Boothe, A. D. (1974). Replicating type-C virus particles in monolayer cell cultures of tissues from cattle with lymphosarcoma. Journal of National Cancer Institute 52, 491-494. [Google Scholar]
  44. Werling, D., Sileghem, M., Lutz, H. & Langhans, W. (1995). Effect of bovine leukemia virus infection on bovine peripheral blood monocyte responsiveness to lipopolysaccharide stimulation in vitro. Veterinary Immunology and Immunopathology 48, 77-88.[CrossRef] [Google Scholar]
  45. Werling, D., Howard, C. J., Niederer, E., Straub, O. C., Saalmüller, A. & Langhans, W. (1998). Analysis of the phenotype and phagocytic activity of monocytes/macrophages from cattle infected with the bovine leukemia virus. Veterinary Immunology and Immunopathology 62, 185-195.[CrossRef] [Google Scholar]
  46. Wyatt, C. R., Wingett, D., White, J. S., Buck, C. D., Knowless, D., Reeves, R. & Magnuson, N. S. (1989). Persistent infection of rabbits with bovine leukemia virus associated with development of immune dysfunction. Journal of Virology 63, 4498-4506. [Google Scholar]
  47. Yamada, T., Yamaoka, S., Goto, T., Nakai, M., Tsujimoto, Y. & Hatanaka, M. (1994). The human T-cell leukemia virus type I tax protein induces apoptosis which is blocked by the Bcl-2 protein. Journal of Virology 68, 3374-3379. [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/0022-1317-81-1-109
Loading
/content/journal/jgv/10.1099/0022-1317-81-1-109
Loading

Data & Media loading...

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