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. 1990 Mar;64(3):1398–1401. doi: 10.1128/jvi.64.3.1398-1401.1990

Epstein-Barr virus (EBV) antigens processed and presented by B cells, B blasts, and macrophages trigger T-cell-mediated inhibition of EBV-induced B-cell transformation.

M T Bejarano 1, M G Masucci 1, A Morgan 1, B Morein 1, G Klein 1, E Klein 1
PMCID: PMC249265  PMID: 2154620

Abstract

The ability of B cells, B blasts, and macrophages to present Epstein-Barr virion antigens to autologous T cells and trigger their capacity to inhibit Epstein-Barr virus-induced B-cell transformation was tested. Macrophages were as efficient as B cells and B blasts in presenting the virus to T lymphocytes. This function required antigen processing, because it was inhibited by chloroquine treatment and by fixation of the antigen-presenting cells immediately after viral exposure but not 18 h later. T cells exposed to the purified Epstein-Barr virus envelope antigen gp350 coupled to immunostimulating complexes also showed inhibitory function. These results suggest that recognition of processed virion antigens elicits the generation of T-cell-mediated inhibition of Epstein-Barr virus-induced B-cell transformation.

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Selected References

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

  1. Asarnow D. M., Kuziel W. A., Bonyhadi M., Tigelaar R. E., Tucker P. W., Allison J. P. Limited diversity of gamma delta antigen receptor genes of Thy-1+ dendritic epidermal cells. Cell. 1988 Dec 2;55(5):837–847. doi: 10.1016/0092-8674(88)90139-0. [DOI] [PubMed] [Google Scholar]
  2. Bejarano M. T., Masucci M. G., Klein G., Klein E. T-cell-mediated inhibition of EBV-induced B-cell transformation: recognition of virus particles. Int J Cancer. 1988 Sep 15;42(3):359–364. doi: 10.1002/ijc.2910420309. [DOI] [PubMed] [Google Scholar]
  3. Bhan A. K., Nadler L. M., Stashenko P., McCluskey R. T., Schlossman S. F. Stages of B cell differentiation in human lymphoid tissue. J Exp Med. 1981 Sep 1;154(3):737–749. doi: 10.1084/jem.154.3.737. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Bonneville M., Janeway C. A., Jr, Ito K., Haser W., Ishida I., Nakanishi N., Tonegawa S. Intestinal intraepithelial lymphocytes are a distinct set of gamma delta T cells. Nature. 1988 Dec 1;336(6198):479–481. doi: 10.1038/336479a0. [DOI] [PubMed] [Google Scholar]
  5. David E. M., Morgan A. J. Efficient purification of Epstein-Barr virus membrane antigen gp340 by fast protein liquid chromatography. J Immunol Methods. 1988 Apr 6;108(1-2):231–236. doi: 10.1016/0022-1759(88)90424-3. [DOI] [PubMed] [Google Scholar]
  6. Hoffman G. J., Lazarowitz S. G., Hayward S. D. Monoclonal antibody against a 250,000-dalton glycoprotein of Epstein-Barr virus identifies a membrane antigen and a neutralizing antigen. Proc Natl Acad Sci U S A. 1980 May;77(5):2979–2983. doi: 10.1073/pnas.77.5.2979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hosken N. A., Bevan M. J., Carbone F. R. Class I-restricted presentation occurs without internalization or processing of exogenous antigenic peptides. J Immunol. 1989 Feb 15;142(4):1079–1083. [PubMed] [Google Scholar]
  8. Inada S., Brown E. J., Gaither T. A., Hammer C. H., Takahashi T., Frank M. M. C3d receptors are expressed on human monocytes after in vitro cultivation. Proc Natl Acad Sci U S A. 1983 Apr;80(8):2351–2355. doi: 10.1073/pnas.80.8.2351. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Janeway C. A., Jr, Jones B., Hayday A. Specificity and function of T cells bearing gamma delta receptors. Immunol Today. 1988 Mar;9(3):73–76. doi: 10.1016/0167-5699(88)91267-4. [DOI] [PubMed] [Google Scholar]
  10. Klein G. Viral latency and transformation: the strategy of Epstein-Barr virus. Cell. 1989 Jul 14;58(1):5–8. doi: 10.1016/0092-8674(89)90394-2. [DOI] [PubMed] [Google Scholar]
  11. Lewin N., Aman P., Masucci M. G., Klein E., Klein G., Oberg B., Strander H., Henle W., Henle G. Characterization of EBV-carrying B-cell populations in healthy seropositive individuals with regard to density, release of transforming virus and spontaneous outgrowth. Int J Cancer. 1987 Apr 15;39(4):472–476. doi: 10.1002/ijc.2910390411. [DOI] [PubMed] [Google Scholar]
  12. Lövgren K., Morein B. The requirement of lipids for the formation of immunostimulating complexes (iscoms). Biotechnol Appl Biochem. 1988 Apr;10(2):161–172. [PubMed] [Google Scholar]
  13. Masucci M. G., Bejarano M. T., Masucci G., Klein E. Large granular lymphocytes inhibit the in vitro growth of autologous Epstein-Barr virus-infected B cells. Cell Immunol. 1983 Mar;76(2):311–321. doi: 10.1016/0008-8749(83)90374-x. [DOI] [PubMed] [Google Scholar]
  14. Masucci M. G., Klein E. Role of T cell subpopulations in the control of the proliferative potential of EBV transformed B cells. Behring Inst Mitt. 1983 May;(72):163–168. [PubMed] [Google Scholar]
  15. Mold C., Bradt B. M., Nemerow G. R., Cooper N. R. Activation of the alternative complement pathway by EBV and the viral envelope glycoprotein, gp350. J Immunol. 1988 Jun 1;140(11):3867–3874. [PubMed] [Google Scholar]
  16. Morein B., Sundquist B., Höglund S., Dalsgaard K., Osterhaus A. Iscom, a novel structure for antigenic presentation of membrane proteins from enveloped viruses. 1984 Mar 29-Apr 4Nature. 308(5958):457–460. doi: 10.1038/308457a0. [DOI] [PubMed] [Google Scholar]
  17. Morgan A. J., Finerty S., Lovgren K., Scullion F. T., Morein B. Prevention of Epstein-Barr (EB) virus-induced lymphoma in cottontop tamarins by vaccination with the EB virus envelope glycoprotein gp340 incorporated into immune-stimulating complexes. J Gen Virol. 1988 Aug;69(Pt 8):2093–2096. doi: 10.1099/0022-1317-69-8-2093. [DOI] [PubMed] [Google Scholar]
  18. Morrison L. A., Lukacher A. E., Braciale V. L., Fan D. P., Braciale T. J. Differences in antigen presentation to MHC class I-and class II-restricted influenza virus-specific cytolytic T lymphocyte clones. J Exp Med. 1986 Apr 1;163(4):903–921. doi: 10.1084/jem.163.4.903. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Moss D. J., Misko I. S., Burrows S. R., Burman K., McCarthy R., Sculley T. B. Cytotoxic T-cell clones discriminate between A- and B-type Epstein-Barr virus transformants. Nature. 1988 Feb 25;331(6158):719–721. doi: 10.1038/331719a0. [DOI] [PubMed] [Google Scholar]
  20. Nemerow G. R., Mold C., Schwend V. K., Tollefson V., Cooper N. R. Identification of gp350 as the viral glycoprotein mediating attachment of Epstein-Barr virus (EBV) to the EBV/C3d receptor of B cells: sequence homology of gp350 and C3 complement fragment C3d. J Virol. 1987 May;61(5):1416–1420. doi: 10.1128/jvi.61.5.1416-1420.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Qualtiere L. F., Chase R., Pearson G. R. Purification and biologic characterization of a major Epstein Barr virus-induced membrane glycoprotein. J Immunol. 1982 Aug;129(2):814–818. [PubMed] [Google Scholar]
  22. Rickinson A. B., Moss D. J., Allen D. J., Wallace L. E., Rowe M., Epstein M. A. Reactivation of Epstein-Barr virus-specific cytotoxic T cells by in vitro stimulation with the autologous lymphoblastoid cell line. Int J Cancer. 1981 May 15;27(5):593–601. doi: 10.1002/ijc.2910270505. [DOI] [PubMed] [Google Scholar]
  23. Rickinson A. B., Moss D. J., Wallace L. E., Rowe M., Misko I. S., Epstein M. A., Pope J. H. Long-term T-cell-mediated immunity to Epstein-Barr virus. Cancer Res. 1981 Nov;41(11 Pt 1):4216–4221. [PubMed] [Google Scholar]
  24. Sairenji T., Bertoni G., Medveczky M. M., Medveczky P. G., Nguyen Q. V., Humphreys R. E. Inhibition of Epstein-Barr virus (EBV) release from P3HR-1 and B95-8 cell lines by monoclonal antibodies to EBV membrane antigen gp350/220. J Virol. 1988 Aug;62(8):2614–2621. doi: 10.1128/jvi.62.8.2614-2621.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sample J., Liebowitz D., Kieff E. Two related Epstein-Barr virus membrane proteins are encoded by separate genes. J Virol. 1989 Feb;63(2):933–937. doi: 10.1128/jvi.63.2.933-937.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Sellins K. S., Cohen J. J. Polyomavirus DNA is damaged in target cells during cytotoxic T-lymphocyte-mediated killing. J Virol. 1989 Feb;63(2):572–578. doi: 10.1128/jvi.63.2.572-578.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Shimonkevitz R., Kappler J., Marrack P., Grey H. Antigen recognition by H-2-restricted T cells. I. Cell-free antigen processing. J Exp Med. 1983 Aug 1;158(2):303–316. doi: 10.1084/jem.158.2.303. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sixbey J. W., Vesterinen E. H., Nedrud J. G., Raab-Traub N., Walton L. A., Pagano J. S. Replication of Epstein-Barr virus in human epithelial cells infected in vitro. Nature. 1983 Dec 1;306(5942):480–483. doi: 10.1038/306480a0. [DOI] [PubMed] [Google Scholar]
  29. Sugamura K., Tanaka Y., Hinuma Y. Expression of target antigen for Epstein-Barr virus-specific cytotoxic T cells on BJAB cells freshly infected with EBV. Microbiol Immunol. 1982;26(7):575–583. doi: 10.1111/mim.1982.26.7.575. [DOI] [PubMed] [Google Scholar]
  30. Thorley-Lawson D. A., Geilinger K. Monoclonal antibodies against the major glycoprotein (gp350/220) of Epstein-Barr virus neutralize infectivity. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5307–5311. doi: 10.1073/pnas.77.9.5307. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Thorley-Lawson D. A., Israelsohn E. S. Generation of specific cytotoxic T cells with a fragment of the Epstein-Barr virus-encoded p63/latent membrane protein. Proc Natl Acad Sci U S A. 1987 Aug;84(15):5384–5388. doi: 10.1073/pnas.84.15.5384. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Townsend A. R., Gotch F. M., Davey J. Cytotoxic T cells recognize fragments of the influenza nucleoprotein. Cell. 1985 Sep;42(2):457–467. doi: 10.1016/0092-8674(85)90103-5. [DOI] [PubMed] [Google Scholar]
  33. Ulaeto D., Wallace L., Morgan A., Morein B., Rickinson A. B. In vitro T cell responses to a candidate Epstein-Barr virus vaccine: human CD4+ T cell clones specific for the major envelope glycoprotein gp340. Eur J Immunol. 1988 Nov;18(11):1689–1697. doi: 10.1002/eji.1830181106. [DOI] [PubMed] [Google Scholar]
  34. Vik D. P., Fearon D. T. Neutrophils express a receptor for iC3b, C3dg, and C3d that is distinct from CR1, CR2, and CR3. J Immunol. 1985 Apr;134(4):2571–2579. [PubMed] [Google Scholar]
  35. Walker C. M., Moody D. J., Stites D. P., Levy J. A. CD8+ lymphocytes can control HIV infection in vitro by suppressing virus replication. Science. 1986 Dec 19;234(4783):1563–1566. doi: 10.1126/science.2431484. [DOI] [PubMed] [Google Scholar]
  36. Wells A., Koide N., Klein G. Two large virion envelope glycoproteins mediate Epstein-Barr virus binding to receptor-positive cells. J Virol. 1982 Jan;41(1):286–297. doi: 10.1128/jvi.41.1.286-297.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Yao Q. Y., Rickinson A. B., Epstein M. A. A re-examination of the Epstein-Barr virus carrier state in healthy seropositive individuals. Int J Cancer. 1985 Jan 15;35(1):35–42. doi: 10.1002/ijc.2910350107. [DOI] [PubMed] [Google Scholar]
  38. Yao Q. Y., Rickinson A. B., Gaston J. S., Epstein M. A. In vitro analysis of the Epstein-Barr virus: host balance in long-term renal allograft recipients. Int J Cancer. 1985 Jan 15;35(1):43–49. doi: 10.1002/ijc.2910350108. [DOI] [PubMed] [Google Scholar]

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