1887

Abstract

Impaired proliferative response of lymphocytes after mitogenic stimulation is a key feature of the generalized immunosuppression induced by measles virus (MV). Compelling evidence suggests that negative signalling by the MV glycoprotein (gp) complex and the surface of uninfected lymphocytes is essential for this effect. So far, the inhibitory activity of this complex applied to all lymphocyte subpopulations irrespective of the mode of stimulation and could not be overcome by external stimulation. This study shows that the isopentenyl pyrophosphate (IPP)/IL-2-stimulated expansion of human / T cell receptor (TCR) T cells from peripheral blood mononuclear cells (PBMCs) is inhibited efficiently when the MV gp complex is expressed on the surface of persistently MV-infected T or monocytic cells. In contrast, persistently infected B cells or infected human dendritic cells (DCs) do not interfere with expansion of / TCR T cells from PBMCs. These particular two cell populations, however, efficiently inhibit IPP/IL-2-stimulated expansion of / TCR T cells from purified T cells and this is reverted by resubstitution with monocytes. As revealed by filter experiments, cocultivation with B cells and DCs empower monocytes, at least partially by soluble mediators, to provide membrane contact-dependent costimulatory signals that neutralize the inhibitory effect of the MV gp complex. Thus, / TCR T cells are sensitive to MV gp-mediated inhibition; however, this is overcome efficiently by signals delivered from monocytes conditioned by B cells and DCs.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.19027-0
2003-05-01
2019-12-11
Loading full text...

Full text loading...

/deliver/fulltext/jgv/84/5/vir841179.html?itemId=/content/journal/jgv/10.1099/vir.0.19027-0&mimeType=html&fmt=ahah

References

  1. Addae, M. M., Komada, Y., Zhang, X. L. & Sakurai, M. ( 1995; ). Immunological unresponsiveness and apoptotic cell death of T cells in measles virus infection. Acta Paediatr Jpn 37, 308–314.[CrossRef]
    [Google Scholar]
  2. Avota, E., Avots, A., Niewiesk, N., Kane, L. P., Bommhardt, U., ter Meulen, V. & Schneider-Schaulies, S. ( 2001; ). Disruption of Akt kinase activation is important for immunosuppression induced by measles virus. Nat Med 7, 725–731.[CrossRef]
    [Google Scholar]
  3. Bahram, S., Bresnahan, M., Geraghty, D. E. & Spies, T. ( 1994; ). A second lineage of mammalian histocompatibility complex class I genes. Proc Natl Acad Sci U S A 91, 6259–6263.[CrossRef]
    [Google Scholar]
  4. Borrow, P. & Oldstone, M. B. A. ( 1995; ). Measles virus–mononuclear cell interactions. In Measles Virus, pp. 85–100. Edited by M. A. Billeter & V. ter Meulen. New York: Springer-Verlag.
  5. De Libero, G. ( 1997; ). Sentinel function of broadly reactive human γ/δ T cells. Immunol Today 18, 22–26.
    [Google Scholar]
  6. Dubois, B., Lamy, P. J., Chemin, K., Lachaux, A. & Kaiserlian, D. ( 2001; ). Measles virus exploits dendritic cells to suppress CD4+ T-cell proliferation via expression of surface viral glycoproteins independently of T-cell trans-infection. Cell Immunol 214, 173–183.[CrossRef]
    [Google Scholar]
  7. Engelking, O., Fedorov, L. M., Lilischkis, R., ter Meulen, V. & Schneider-Schaulies, S. ( 1999; ). Measles virus-induced immunosuppression in vitro is associated with deregulation of G1 cell cycle control proteins. J Gen Virol 80, 1599–1608.
    [Google Scholar]
  8. Esolen, L. M., Ward, B. J., Mönch, T. R. & Griffin, D. E. ( 1993; ). Infection of monocytes during measles. J Infect Dis 168, 47–52.[CrossRef]
    [Google Scholar]
  9. Fickenscher, H., Bökel, C., Knappe, A., Biesinger, B., Meinl, E., Fleischer, B., Fleckenstein, B. & Bröker, B. M. ( 1997; ). Functional phenotype of transformed human αβ and γδ T cells determined by different subgroup C strains of herpesvirus saimiri. J Virol 71, 2252–2263.
    [Google Scholar]
  10. Fujinami, R. S., Sun, X., Howell, J. M., Jenkin, J. C. & Burns, J. B. ( 1998; ). Modulation of immune system function by measles virus infection: role of soluble factor and direct infection. J Virol 72, 9421–9427.
    [Google Scholar]
  11. Giuliani, A., Prete, S. P., Graziani, G. & 9 other authors ( 2001; ). Influence of Mycobacterium bovis bacillus Calmette Guerin on in vitro induction of CD1 molecules in adherent mononuclear cells. Infect Immun 69, 7461–7470.[CrossRef]
    [Google Scholar]
  12. Hayday, A. C. ( 2000; ). γδ cells: a right time and a right place for a conserved third way of protection. Annu Rev Immunol 18, 975–1026.[CrossRef]
    [Google Scholar]
  13. Hayes, S. M. & Love, P. E. ( 2002; ). Distinct structure and signaling potential of the γδ TCR complex. Immunity 16, 827–838.[CrossRef]
    [Google Scholar]
  14. Karp, C. L., Wysocka, M., Wahl, L. M., Ahearn, J. M., Cuomo, P. J., Sherry, B., Trinchieri, G. & Griffin, D. E. ( 1996; ). Mechanism of suppression of cell-mediated immunity by measles virus. Science 273, 228–231.[CrossRef]
    [Google Scholar]
  15. Kasinrerk, W., Baumruker, T., Majdic, O., Knapp, W. & Stockinger, H. ( 1993; ). CD1 molecule expression on human monocytes induced by granulocyte-macrophage colony-stimulating factor. J Immunol 150, 579–584.
    [Google Scholar]
  16. Kaufmann, S. H. E. ( 1996; ). γ/δ and other unconventional T lymphocytes: what do they see and what do they do? Proc Natl Acad Sci U S A 93, 2272–2279.[CrossRef]
    [Google Scholar]
  17. Klagge, I. M., ter Meulen, V. & Schneider-Schaulies, S. ( 2000; ). Measles virus-induced promotion of dendritic cell maturation by soluble mediators does not overcome the immunosuppressive activity of viral glycoproteins on the cell surface. Eur J Immunol 30, 2741–2750.[CrossRef]
    [Google Scholar]
  18. Miyagawa, F., Tanaka, Y., Yamashita, S. & Minato, N. ( 2001; ). Essential requirement of antigen presentation by monocyte lineage cells for the activation of primary human γδ T cells by aminobisphosphonate antigen. J Immunol 166, 5508–5514.[CrossRef]
    [Google Scholar]
  19. Naniche, D., Reed, S. I. & Oldstone, M. B. A. ( 1999; ). Cell cycle arrest during measles virus infection: a G0-like block leads to suppression of retinoblastoma protein expression. J Virol 73, 1894–1901.
    [Google Scholar]
  20. Niewiesk, S., Ohnimus, H., Schnorr, J.-J., Götzelmann, M., Schneider-Schaulies, S., Jassoy, C. & ter Meulen, V. ( 1999; ). Measles virus-induced immunosuppression in cotton rats is associated with cell cycle retardation in uninfected lymphocytes. J Gen Virol 80, 2023–2029.
    [Google Scholar]
  21. Rothenfusser, S., Hornung, V., Krug, A., Towarowski, A., Krieg, A. M., Endres, S. & Hartmann, G. ( 2001; ). Distinct CpG oligonucleotide sequences activate human γδ T cells via interferon-α/-β. Eur J Immunol 31, 3525–3534.[CrossRef]
    [Google Scholar]
  22. Schlender, J., Schnorr, J. J., Spielhoffer, P., Cathomen, T., Cattaneo, R., Billeter, M. A., ter Meulen, V. & Schneider-Schaulies, S. ( 1996; ). Interaction of measles virus glycoproteins with the surface of uninfected peripheral blood lymphocytes induces immunosuppression in vitro. Proc Natl Acad Sci U S A 93, 13194–13199.[CrossRef]
    [Google Scholar]
  23. Schneider-Schaulies, S., Kreth, H. W., Hofmann, G., Billeter, M. & ter Meulen, V. ( 1991; ). Expression of measles virus RNA in peripheral blood mononuclear cells of patients with measles, SSPE, and autoimmune diseases. Virology 182, 703–711.[CrossRef]
    [Google Scholar]
  24. Schneider-Schaulies, S., Niewiesk, S., Schneider-Schaulies, J. & ter Meulen, V. ( 2001; ). Measles virus induced immunosuppression: targets and effector mechanisms. Curr Mol Med 1, 163–182.[CrossRef]
    [Google Scholar]
  25. Schnorr, J. J., Seufert, M., Schlender, J., Borst, J., Johnston, I. C., ter Meulen, V. & Schneider-Schaulies, S. ( 1997a; ). Cell cycle arrest rather than apoptosis is associated with measles virus contact-mediated immunosuppression in vitro. J Gen Virol 78, 3217–3226.
    [Google Scholar]
  26. Schnorr, J. J., Xanthakos, S., Keikavoussi, P., Kaempgen, E., ter Meulen, V. & Schneider-Schaulies, S. ( 1997b; ). Induction of maturation of human blood dendritic cell precursors by measles virus is associated with immunosuppression. Proc Natl Acad Sci U S A 94, 5326–5331.[CrossRef]
    [Google Scholar]
  27. Sciammas, R., Johnson, R. M., Sperling, A. I., Brady, W., Linsley, P. S., Spear, P. G., Fitch, F. W. & Bluestone, J. A. ( 1994; ). Unique antigen recognition by a herpesvirus-specific TCR-γ/δ cell. J Immunol 152, 5392–5397.
    [Google Scholar]
  28. Servet-Delprat, C., Vidalain, P. O., Azocar, O., Le Deist, F., Fischer, A. & Rabourdin-Combe, C. ( 2000; ). Consequences of Fas-mediated human dendritic cell apoptosis induced by measles virus. J Virol 74, 4387–4393.[CrossRef]
    [Google Scholar]
  29. Ulrichs, T. & Porcelli, S. A. ( 2000; ). CD1 proteins: targets of T cell recognition in innate and adaptive immunity. Rev Immunogenet 2, 416–432.
    [Google Scholar]
  30. Vidalain, P. O., Azocar, O., Lamouille, B., Astier, A., Rabourdin-Combe, C. & Servet-Delprat, C. ( 2000; ). Measles virus induces functional TRAIL production by human dendritic cells. J Virol 74, 556–559.[CrossRef]
    [Google Scholar]
  31. Wang, P. & Malkovsky, M. ( 2000; ). Different roles of the CD2 and LFA-1 T-cell co-receptors for regulating cytotoxicity, proliferative, and cytokine responses of human Vγ9/Vδ2 T cells. Mol Med 6, 196–207.
    [Google Scholar]
  32. Wesch, D., Marx, S. & Kabelitz, D. ( 1997; ). Comparative analysis of α/β and γ/δ T cell activation by Mycobacterium tuberculosis and isopentenyl pyrophosphate. Eur J Immunol 27, 952–956.[CrossRef]
    [Google Scholar]
  33. Yanagi, Y., Cubitt, B. A. & Oldstone, M. B. ( 1992; ). Measles virus inhibits mitogen-induced T cell proliferation but does not directly perturb the T cell activation process inside the cell. Virology 187, 280–289.[CrossRef]
    [Google Scholar]
  34. Zwirner, N. W., Dole, K. & Stastny, P. ( 1999; ). Differential surface expression of MICA by endothelial cells, fibroblasts, keratinocytes, and monocytes. Hum Immunol 60, 323–330.[CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.19027-0
Loading
/content/journal/jgv/10.1099/vir.0.19027-0
Loading

Data & Media loading...

Most Cited This Month

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