Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells

doi:10.1084/jem.184.1.19

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Interleukin-10 induces a long-term antigen-specific anergic state in human CD4+ T cells

H Groux, M Bigler, JE de Vries and MG Roncarolo
Human Immunology Department, DNAX Research Institute of Molecular and Cellular Biology, Inc., Palo Alto, California 94304-1104, USA.

Human CD4+ T cells, activated by allogeneic monocytes in a primary mixed lymphocyte reaction in the presence of exogenous interleukin (IL) 10, specifically failed to proliferate after restimulation with the same alloantigens. A comparable state of T cell unresponsiveness could be induced by activation of CD4+ T cells by cross-linked anti-CD3 monoclonal antibodies (mAbs) in the presence of exogenous IL-10. The anergic T cells failed to produce IL-2, IL-5, IL-10, interferon gamma, tumor necrosis factor alpha, and granulocyte/macrophage colony- stimulating factor. The IL-10-induced anergic state was long-lasting. T cell anergy could not be reversed after restimulation of the cells with anti-CD3 and anti-CD28 mAbs, although CD3 and CD28 expression was normal. In addition, restimulation of anergized T cells with anti-CD3 mAbs induced normal Ca2+ fluxes and resulted in increased CD3, CD28, and class II major histocompatibility complex expression, indicating that calcineurin-mediated signaling occurs in these anergic cells. However, the expression of the IL-2 receptor alpha chain was not upregulated, which may account for the failure of exogenous IL-2 to reverse the anergic state. Interestingly, anergic T cells and their nonanergic counterparts showed comparable levels of proliferation and cytokine production after activation with phorbol myristate acetate and Ca2+ ionophore, indicating that a direct activation of a protein kinase C-dependent pathway can overcome the tolerizing effect of IL-10. Taken together, these data demonstrate that IL-10 induces T cell anergy and therefore may play an important role in the induction and maintenance of antigen-specific T cell tolerance.
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Ostlie, N. S., Karachunski, P. I., Wang, W., Monfardini, C., Kronenberg, M., Conti-Fine, B. M. (2001). Transgenic Expression of IL-10 in T Cells Facilitates Development of Experimental Myasthenia Gravis. J. Immunol. 166: 4853-4862 [Abstract] [Full Text]
Xiong, Y., Luscher, M. A., Altman, J. D., Hulsey, M., Robinson, H. L., Ostrowski, M., Barber, B. H., MacDonald, K. S. (2001). Simian Immunodeficiency Virus (SIV) Infection of a Rhesus Macaque Induces SIV-Specific CD8+ T Cells with a Defect in Effector Function That Is Reversible on Extended Interleukin-2 Incubation. J. Virol. 75: 3028-3033 [Abstract] [Full Text]
Deng, C., Goluszko, E., Christadoss, P. (2001). Fas/Fas Ligand Pathway, Apoptosis, and Clonal Anergy Involved in Systemic Acetylcholine Receptor T Cell Epitope Tolerance. J. Immunol. 166: 3458-3467 [Abstract] [Full Text]
Weinberg, K., Blazar, B. R., Wagner, J. E., Agura, E., Hill, B. J., Smogorzewska, M., Koup, R. A., Betts, M. R., Collins, R. H., Douek, D. C. (2001). Factors affecting thymic function after allogeneic hematopoietic stem cell transplantation. Blood 97: 1458-1466 [Abstract] [Full Text]
Prager, E., Staffler, G., Majdic, O., Saemann, M. D., Godar, S., Zlabinger, G. J., Stockinger, H. (2001). Induction of Hyporesponsiveness and Impaired T Lymphocyte Activation by the CD31 Receptor:Ligand Pathway in T Cells. J. Immunol. 166: 2364-2371 [Abstract] [Full Text]
Qin, L., Ding, Y., Tahara, H., Bromberg, J. S. (2001). Viral IL-10-Induced Immunosuppression Requires Th2 Cytokines and Impairs APC Function Within the Allograft. J. Immunol. 166: 2385-2393 [Abstract] [Full Text]
Boussiotis, V. A., Chen, Z.-M., Zeller, J. C., Murphy, W. J., Berezovskaya, A., Narula, S., Roncarolo, M. G., Blazar, B. R. (2001). Altered T-cell receptor + CD28-mediated signaling and blocked cell cycle progression in interleukin 10 and transforming growth factor-{beta}-treated alloreactive T cells that do not induce graft-versus-host disease. Blood 97: 565-571 [Abstract] [Full Text]
ASSEMAN, C., FOWLER, S., POWRIE, F. (2000). Control of Experimental Inflammatory Bowel Disease by Regulatory T cells. Am. J. Respir. Crit. Care Med. 162: S185-189 [Abstract] [Full Text]
Astori, M., von Garnier, C., Kettner, A., Dufour, N., Corradin, G., Spertini, F. (2000). Inducing Tolerance by Intranasal Administration of Long Peptides in Naive and Primed CBA/J Mice. J. Immunol. 165: 3497-3505 [Abstract] [Full Text]
Verhoef, A., Lamb, J. R. (2000). Threshold Signaling of Human Th0 Cells in Activation and Anergy: Modulation of Effector Function by Altered TCR Ligand. J. Immunol. 164: 6034-6040 [Abstract] [Full Text]
Santin, A. D., Hermonat, P. L., Ravaggi, A., Bellone, S., Pecorelli, S., Roman, J. J., Parham, G. P., Cannon, M. J. (2000). Interleukin-10 Increases Th1 Cytokine Production and Cytotoxic Potential in Human Papillomavirus-Specific CD8+ Cytotoxic T Lymphocytes. J. Virol. 74: 4729-4737 [Abstract] [Full Text]
Koenen, H. J. P. M., Joosten, I. (2000). Blockade of CD86 and CD40 induces alloantigen-specific immunoregulatory T cells that remain anergic even after reversal of hyporesponsiveness. Blood 95: 3153-3161 [Abstract] [Full Text]
Ito, K., Takaishi, H., Jin, Y., Song, F., Denning, T. L., Ernst, P. B. (2000). Staphylococcal Enterotoxin B Stimulates Expansion of Autoreactive T Cells That Induce Apoptosis in Intestinal Epithelial Cells: Regulation of Autoreactive Responses by IL-10. J. Immunol. 164: 2994-3001 [Abstract] [Full Text]
Wendling, U., Paul, L., van der Zee, R., Prakken, B., Singh, M., van Eden, W. (2000). A Conserved Mycobacterial Heat Shock Protein (hsp) 70 Sequence Prevents Adjuvant Arthritis upon Nasal Administration and Induces IL-10-Producing T Cells That Cross-React with the Mammalian Self-hsp70 Homologue. J. Immunol. 164: 2711-2717 [Abstract] [Full Text]
Hoyne, G. F., Le Roux, I., Corsin-Jimenez, M., Tan, K., Dunne, J., Forsyth, L. M. G., Dallman, M. J., Owen, M. J., Ish-Horowicz, D., Lamb, J. R. (2000). Serrate1-induced Notch signalling regulates the decision between immunity and tolerance made by peripheral CD4+ T cells. Int Immunol 12: 177-185 [Abstract] [Full Text]
Grundstrom, S., Dohlsten, M., Sundstedt, A. (2000). IL-2 Unresponsiveness in Anergic CD4+ T Cells Is Due to Defective Signaling Through the Common {gamma}-Chain of the IL-2 Receptor. J. Immunol. 164: 1175-1184 [Abstract] [Full Text]
Taylor, P. A., Panoskaltsis-Mortari, A., Noelle, R. J., Blazar, B. R. (2000). Analysis of the Requirements for the Induction of CD4+ T Cell Alloantigen Hyporesponsiveness by Ex Vivo Anti-CD40 Ligand Antibody. J. Immunol. 164: 612-622 [Abstract] [Full Text]