1887

Abstract

Epstein-Barr (EB) virus-immortalized B lymphocytes coexpress the EB viral latent gene products (EB viral nuclear antigens 1 to 6, the latent membrane protein and the terminal protein gene products) and the cellular activation antigen CD23. Immortalized B cells can be separated from those which are infected but not immortalized on the basis of CD23 expression as early as 2 days after infection. In the present report we have confirmed these data, but show that if left in culture for 7 days after infection before separation the CD23-negative cells show a donor-related ability to become CD23-positive and immortalize. CD23-nega- tive cells separated 2 days after infection can be induced to immortalize by the addition of low M B cell growth factor but not by the addition of recombinant interleukin 1, 4 or soluble CD23. At 2 to 3 days after infection the EB viral nuclear antigens 1, 2 and the high species 3, 4 and 6, as well as the latent membrane protein can be detected in the CD23-positive fraction. In contrast at this time only nuclear antigens 1 and 2 could be detected in the CD23-negative fraction. This difference in gene expression may account for the inability of the CD23-negative fraction to immortalize. In the light of these observations the mechanism of viral persistence is discussed.

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1990-03-01
2024-12-09
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References

  1. Allday M. J., Crawford D. H., Griffin B. E. 1988; Prediction and demonstration of a novel Epstein-Barr virus nuclear antigen. Nucleic Acids Research 16:4365–4367
    [Google Scholar]
  2. Allday M. J., Crawford D. H., Griffin B. E. 1989; Epstein-Barr virus latent gene expression during the initiation of B cell immortalization. Journal of General Virology 70:1755–1764
    [Google Scholar]
  3. Azim T., Crawford D. H. 1988; Lymphocytes activated by the Epstein-Barr virus to produce immunoglobulin do not express CD23 or become immortalised. International Journal of Cancer 42:23–28
    [Google Scholar]
  4. Blazar B. A., Murphy A. M. 1987; Comparison of interleukin-1 with endogenous B-cell factors for effects on lymphoma cell growth after EBV conversion. In Epstein-Barr Virus and Human Disease pp. 275–279 Levine P. H., Ablashi D. V., Nonoyama M., Pearson G. R., Glaser R. Edited by Clifton: Humana Press;
    [Google Scholar]
  5. Calender A., Billaud M., Aubry J. P., Banchereau J., Vuillaume M., Lenoir G. M. 1987; Epstein-Barr virus (EBV) induces expression of B-cell activation markers on in vitro infection of EBV-negative B-lymphoma cells. Proceedings of the National Academy of Sciences, U.S.A 84:8060–8064
    [Google Scholar]
  6. Cleary M. L., Dorfman R. F., Sklar J. 1986; Failure in immunological control of the virus infection: post-transplant lymphomas. In The Epstein-Barr Virus: Recent Advances pp. 163–182 Epstein M. A., Achong B. G. Edited by London: William Heinemann;
    [Google Scholar]
  7. Crawford D. H., Ando I. 1986; EB virus induction is associated with B cell maturation. Immunology 59:405–409
    [Google Scholar]
  8. Dambaugh T., Hennessy K., Chamnankit L., Kieff E. 1984; U2 region of Epstein-Barr virus DNA may encode Epstein-Barr nuclear antigen 2. Proceedings of the National Academy of Sciences, U.S.A 81:7632–7636
    [Google Scholar]
  9. Defrance T., Aubry J. P., Rousset F., Vandervliet B., Bonnyfoy J. Y., Arai W., Takebe Y., Yokota T., Lee F., Arai K., De Vries J., Banchereau J. 1987; Human recombinant interleukin 4 induces Fc receptors (CD23) on normal human B lymphocytes. Journal of Experimental Medicine 165:1459–1467
    [Google Scholar]
  10. Dillner J., Kallin B. 1988; The Epstein-Barr virus proteins. Advances in Cancer Research 50:95–158
    [Google Scholar]
  11. Gordon J., Webb A. J., Walker L., Guy G. R., Rowe M. 1986; Evidence for an association between CD23 and the receptor for a low molecular weight B cell growth factor. European Journal of Immunology 16:1627–1630
    [Google Scholar]
  12. Hammerschmidt W., Sugden B. 1989; Genetic analysis of immortalising functions of Epstein-Barr virus in human B lymphocytes. Nature; London: 340393–397
    [Google Scholar]
  13. Henle G., Henle W., Diehl V. 1968; Relation of Burkitt’s tumor-associated herpes-type virus to infectious mononucleosis. Proceedings of the National Academy of Sciences, U.S.A. 59:94–101
    [Google Scholar]
  14. Hurley E. A., Thorley-Lawson D. A. 1988; B cell activation and the establishment of Epstein-Barr virus latency. Journal of Experimental Medicine 168:2059–2075
    [Google Scholar]
  15. Klein G. 1989; Viral latency and transformation: the strategy of Epstein-Barr virus. Cell 58:5–8
    [Google Scholar]
  16. Laux G., Perricaudet M., Farrell P. J. 1988; A spliced Epstein-Barr virus gene expressed in immortalised lymphocytes is created by circularisation of the linear viral genome. EMBO Journal 7:769–774
    [Google Scholar]
  17. Lindahl T., Adams A., Bjursell G., Bornkamm G., Kaschka-Dierich C., Jehn U. 1976; Covalently closed circular duplex DNA of EBV in a human lymphoid cell line. Journal of Molecular Biology 102:511–530
    [Google Scholar]
  18. Mann K. P., Staunton D., Thorley-Lawson D. A. 1985; Epstein-Barr virus-encoded protein found in plasma membranes of transformed cells. Journal of Virology 55:710–720
    [Google Scholar]
  19. Miller G., Shope T., Lisco H., Stitt D., Lipman M. 1972; Epstein-Barr virus: transformation, cytopathic changes and viral antigens in squirrel monkey and marmoset leucocytes. Proceedings of the National Academy of Sciences, U.S.A 69:383–387
    [Google Scholar]
  20. Moss D. J., Misko I. S., Burrows S. R., Burman K., Mccarthy R., Sculley T. B. 1988; Cytotoxic T-cell clones discriminate between A- and B-type Epstein-Barr virus transformants. Nature; London: 331719–721
    [Google Scholar]
  21. Nemerow G. R., Wolfert R., Mcnaughton M. E., Cooper N. R. 1985; Identification and characterisation of the EBV receptor on human B lymphocytes and its relationship to the C3d receptor (CR2). Journal of Virology 55:347–351
    [Google Scholar]
  22. Rowe M., Gregory C. 1989; Epstein-Barr virus and Burkitt’s lymphoma. In Advances in Viral Oncology pp. 237–259 Klein G. Edited by New York: Raven Press;
    [Google Scholar]
  23. Rowe M., Evans H. S., Young L. S., Hennessy K., Kieff E., Rickinson A. B. 1987; Monoclonal antibodies to the latent membrane protein of Epstein-Barr virus reveal heterogeneity of the protein and inducible expression in virus-transformed cells. Journal of General Virology 68:1575–1586
    [Google Scholar]
  24. Swendeman S., Thorley-Lawson D. A. 1987; The activation antigen Blast-2, when shed, is an autocrine BCGF for normal and transformed B cells. EMBO Journal 6:1637–1642
    [Google Scholar]
  25. Thorley-Lawson D. A., Mann K. P. 1985; Early events in Epstein-Barr virus infection provide a model for B cell activation. Journal of Experimental Medicine 162:45–59
    [Google Scholar]
  26. Thorley-Lawson D. A., Nadler L. M., Bhan A. K., Schooley R. T. 1985; Blast-2 (EBVCs), an early cell surface marker of human B cell activation is superinduced by EBV. Journal of Immunology 134:3007–3012
    [Google Scholar]
  27. Walls E. V., Doyle M. G., Patel K. K., Allday M. J., Catovsky D., Crawford D. H. 1990; Activation and immortalisation of leukaemic B cells by Epstein-Barr virus. International Journal of Cancer 44:846–853
    [Google Scholar]
  28. Wang D., Liebowitz D., Kieff E. 1985; An EBV membrane protein expressed in immortalised lymphocytes transforms established rodent cells. Cell 43:831–840
    [Google Scholar]
  29. Wang D., Liebowitz D., Wang F., Gregory C., Rickinson A., Larson R., Springer T., Kieff E. 1988; Epstein-Barr virus latent infectious membrane protein alters the human B-lymphocyte phenotype: deletion of the amino terminus abolishes activity. Journal of Virology 62:4173–4184
    [Google Scholar]
  30. Wang F., Gregory C. D., Rowe M., Rickinson A. B., Wang D., Birkenbach M., Kikutani H., Kishimoto T., Kieff E. 1987; Epstein-Barr virus nuclear antigen 2 specifically induced expression of the B cell activation antigen CD23. Proceedings of the National Academy of Sciences, U.S.A 84:3452–3456
    [Google Scholar]
  31. Yates J. L., Warren N., Sugden B. 1985; Stable replication of plasmids derived from Epstein-Barr virus in mammalian cells. Nature; London: 313812–815
    [Google Scholar]
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