CTLA-4 ligation blocks CD28-dependent T cell activation [published erratum appears in J Exp Med 1996 Jul 1;184(1):301]

doi:10.1084/jem.183.6.2541

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CTLA-4 ligation blocks CD28-dependent T cell activation [published erratum appears in J Exp Med 1996 Jul 1;184(1):301]

TL Walunas, CY Bakker and JA Bluestone
Department of Pathology, Ben May Institute for Cancer Research, University of Chicago, Illinois 60637, USA.

CTLA-4 is a CD28 homologue believed to be a negative regulator of T cell function. However, the mechanism of this downregulatory activity is not well understood. The present study was designed to examine the effect of CTLA-4 ligation on cytokine production, cell survival, and cell cycle progression. The results demonstrate that the primary effect of CTLA-4 ligation is not the induction of apoptosis. Instead, CTLA-4 signaling blocks IL-2 production, IL-2 receptor expression, and cell cycle progression of activated T cells. Moreover, the effect of CTLA-4 signaling was manifested after initial T cell activation. Inhibition of IL-2 receptor expression and cell cycle progression was more pronounced at late (72 h) time points after initial activation. The effects of anti-CTLA-4 mAbs were most apparent in the presence of optimal CD28- mediated costimulation consistent with the finding that CTLA-4 upregulation was CD28-dependent. Finally, the addition of exogenous IL- 2 to the cultures restored IL-2 receptor expression and T cell proliferation. These results suggest that CTLA-4 signaling does not regulate cell survival or responsiveness to IL-2, but does inhibit CD28- dependent IL-2 production.
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Morales, V. M., Christ, A., Watt, S. M., Kim, H. S., Johnson, K. W., Utku, N., Texieira, A. M., Mizoguchi, A., Mizoguchi, E., Russell, G. J., Russell, S. E., Bhan, A. K., Freeman, G. J., Blumberg, R. S. (1999). Regulation of Human Intestinal Intraepithelial Lymphocyte Cytolytic Function by Biliary Glycoprotein (CD66a). J. Immunol. 163: 1363-1370 [Abstract] [Full Text]
Perrin, P. J., June, C. H., Maldonado, J. H., Ratts, R. B., Racke, M. K. (1999). Blockade of CD28 During In Vitro Activation of Encephalitogenic T Cells or After Disease Onset Ameliorates Experimental Autoimmune Encephalomyelitis. J. Immunol. 163: 1704-1710 [Abstract] [Full Text]
Barrat, F. J., Le Deist, F., Benkerrou, M., Bousso, P., Feldmann, J., Fischer, A., de Saint Basile, G. (1999). Defective CTLA-4 cycling pathway in Chediak-Higashi syndrome: A possible mechanism for deregulation of T lymphocyte activation. Proc. Natl. Acad. Sci. USA 96: 8645-8650 [Abstract] [Full Text]
Deeths, M. J., Kedl, R. M., Mescher, M. F. (1999). CD8+ T Cells Become Nonresponsive (Anergic) Following Activation in the Presence of Costimulation. J. Immunol. 163: 102-110 [Abstract] [Full Text]
GUDMUNDSDOTTIR, H., TURKA, L. A. (1999). T Cell Costimulatory Blockade: New Therapies for TransplantRejection. J. Am. Soc. Nephrol. 10: 1356-1365 [Abstract] [Full Text]
Blazar, B. R., Taylor, P. A., Panoskaltsis-Mortari, A., Sharpe, A. H., Vallera, D. A. (1999). Opposing Roles of CD28:B7 and CTLA-4:B7 Pathways in Regulating In Vivo Alloresponses in Murine Recipients of MHC Disparate T Cells. J. Immunol. 162: 6368-6377 [Abstract] [Full Text]
Khattri, R., Auger, J. A., Griffin, M. D., Sharpe, A. H., Bluestone, J. A. (1999). Lymphoproliferative Disorder in CTLA-4 Knockout Mice Is Characterized by CD28-Regulated Activation of Th2 Responses. J. Immunol. 162: 5784-5791 [Abstract] [Full Text]
Brunner, M. C., Chambers, C. A., Chan, F. K.-M., Hanke, J., Winoto, A., Allison, J. P. (1999). CTLA-4-Mediated Inhibition of Early Events of T Cell Proliferation. J. Immunol. 162: 5813-5820 [Abstract] [Full Text]
Olsson, C., Riebeck, K., Dohlsten, M., Michaelsson, E. (1999). CTLA-4 Ligation Suppresses CD28-induced NF-kappa B and AP-1 Activity in Mouse T Cell Blasts. J. Biol. Chem. 274: 14400-14405 [Abstract] [Full Text]
Metzler, B., Burkhart, C., Wraith, D. C. (1999). Phenotypic analysis of CTLA-4 and CD28 expression during transient peptide-induced T cell activation in vivo. Int Immunol 11: 667-675 [Abstract] [Full Text]
McCoy, K. D., Hermans, I. F., Henry Fraser, J., Le Gros, G., Ronchese, F. (1999). Cytotoxic T Lymphocyte-associated Antigen 4 (CTLA-4) Can Regulate Dendritic Cell-induced Activation and Cytotoxicity of CD8+ T Cells Independently of CD4+T Cell Help. JEM 189: 1157-1162 [Abstract] [Full Text]
Judge, T. A., Wu, Z., Zheng, X.-G., Sharpe, A. H., Sayegh, M. H., Turka, L. A. (1999). The Role of CD80, CD86, and CTLA4 in Alloimmune Responses and the Induction of Long-Term Allograft Survival. J. Immunol. 162: 1947-1951 [Abstract] [Full Text]