CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells

doi:10.1084/jem.183.6.2533

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CTLA-4 engagement inhibits IL-2 accumulation and cell cycle progression upon activation of resting T cells

MF Krummel and JP Allison
Department of Molecular and Cell Biology, University of California, Berkeley 94720, USA.

While interactions between CD28 and members of the B7 family costimulate and enhance T cell responses, recent evidence indicates that the CD28 homologue CTLA-4 plays a downregulatory role. The mechanism by which this occurs is not clear, but it has been suggested that CTLA-4 terminates ongoing responses of activated T cells, perhaps by induction of apoptosis. Here we demonstrate that CTLA-4 engagement by antibody cross-linking or binding to B7 inhibits proliferation and accumulation of the primary T cell growth factor, IL-2, by cells stimulated with anti-CD3 and anti-CD28. This inhibition is not a result of enhanced cell death. Rather it appears to result from restriction of transition from the G1 to the S phase of the cell cycle. Our observation that upregulation of both the IL-2R alpha chain and the CD69 activation antigen are inhibited by CTLA-4 engagement supplies further evidence that CTLA-4 restricts the progression of T cells to an activated state. Together this data demonstrates that CTLA-4 can regulate T cell activation in the absence of induction of apoptotic cell death.
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Griffin, M. D., Hong, D. K., Holman, P. O., Lee, K.-M., Whitters, M. J., O'Herrin, S. M., Fallarino, F., Collins, M., Segal, D. M., Gajewski, T. F., Kranz, D. M., Bluestone, J. A. (2000). Blockade of T Cell Activation Using a Surface-Linked Single-Chain Antibody to CTLA-4 (CD152). J. Immunol. 164: 4433-4442 [Abstract] [Full Text]
Kato, T., Nariuchi, H. (2000). Polarization of Naive CD4+ T Cells Toward the Th1 Subset by CTLA-4 Costimulation. J. Immunol. 164: 3554-3562 [Abstract] [Full Text]
Weinberg, A. D., Rivera, M.-M., Prell, R., Morris, A., Ramstad, T., Vetto, J. T., Urba, W. J., Alvord, G., Bunce, C., Shields, J. (2000). Engagement of the OX-40 Receptor In Vivo Enhances Antitumor Immunity. J. Immunol. 164: 2160-2169 [Abstract] [Full Text]
Sakurai, J., Ohata, J., Saito, K., Miyajima, H., Hirano, T., Kohsaka, T., Enomoto, S., Okumura, K., Azuma, M. (2000). Blockade of CTLA-4 Signals Inhibits Th2-Mediated Murine Chronic Graft-Versus-Host Disease by an Enhanced Expansion of Regulatory CD8+ T Cells. J. Immunol. 164: 664-669 [Abstract] [Full Text]
Martin-Fontecha, A., Moro, M., Crosti, M. C., Veglia, F., Casorati, G., Dellabona, P. (2000). Vaccination with Mouse Mammary Adenocarcinoma Cells Coexpressing B7-1 (CD80) and B7-2 (CD86) Discloses the Dominant Effect of B7-1 in the Induction of Antitumor Immunity. J. Immunol. 164: 698-704 [Abstract] [Full Text]
McAdam, A. J., Farkash, E. A., Gewurz, B. E., Sharpe, A. H. (2000). B7 Costimulation Is Critical for Antibody Class Switching and CD8+ Cytotoxic T-Lymphocyte Generation in the Host Response to Vesicular Stomatitis Virus. J. Virol. 74: 203-208 [Abstract] [Full Text]
Slifka, M. K., Whitton, J. L. (2000). Activated and Memory CD8+ T Cells Can Be Distinguished by Their Cytokine Profiles and Phenotypic Markers. J. Immunol. 164: 208-216 [Abstract] [Full Text]
London, C. A., Lodge, M. P., Abbas, A. K. (2000). Functional Responses and Costimulator Dependence of Memory CD4+ T Cells. J. Immunol. 164: 265-272 [Abstract] [Full Text]
Donovan, C. E, Finn, P. W (1999). Immune mechanisms of childhood asthma. Thorax 54: 938-946 [Full Text]
Oki, S., Kohsaka, T., Azuma, M. (1999). Augmentation of CTLA-4 expression by wortmannin: involvement of lysosomal sorting properties of CTLA-4. Int Immunol 11: 1563-1571 [Abstract] [Full Text]
Oosterwegel, M. A., Mandelbrot, D. A., Boyd, S. D., Lorsbach, R. B., Jarrett, D. Y., Abbas, A. K., Sharpe, A. H. (1999). The Role of CTLA-4 in Regulating Th2 Differentiation. J. Immunol. 163: 2634-2639 [Abstract] [Full Text]
Schneider, H., Martin, M., Agarraberes, F. A., Yin, L., Rapoport, I., Kirchhausen, T., Rudd, C. E. (1999). Cytolytic T Lymphocyte-Associated Antigen-4 and the TCR{zeta}/CD3 Complex, But Not CD28, Interact with Clathrin Adaptor Complexes AP-1 and AP-2. J. Immunol. 163: 1868-1879 [Abstract] [Full Text]