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Walter W. Shuford^*, Kerry Klussman^*, Douglas D. Tritchler^*, Deryk T. Loo^*, Jan Chalupny^*, Anthony W. Siadak^*, T. Joseph Brown^*, John Emswiler^*, Hong Raecho, Christian P. Larsen, Thomas C. Pearson, Jeffrey A. Ledbetter^*, Alejandro Aruffo^*, and Robert S. Mittler^*

From the ^* Bristol-Myers Squibb Pharmaceutical Research Institute, Seattle, Washington 98121; and Department of Surgery, Emory University School of Medicine, Atlanta, Georgia 30322

The 4-1BB receptor is an inducible type I membrane protein and member of the tumor necrosis factor receptor (TNFR) superfamily that is rapidly expressed on the surface of CD4⁺ and CD8⁺ T cells after antigen- or mitogen-induced activation. Cross-linking of 4-1BB and the T cell receptor (TCR) on activated T cells has been shown to deliver a costimulatory signal to T cells. Here, we expand upon previously published studies by demonstrating that CD8⁺ T cells when compared with CD4⁺ T cells are preferentially responsive to both early activation events and proliferative signals provided via the TCR and 4-1BB. In comparison, CD28-mediated costimulatory signals appear to function in a reciprocal manner to those induced through 4-1BB costimulation. In vivo examination of the effects of anti-4-1BB monoclonal antibodies (mAbs) on antigen-induced T cell activation have shown that the administration of epitope-specific anti-4-1BB mAbs amplified the generation of H-2^d–specific cytotoxic T cells in a murine model of acute graft versus host disease (GVHD) and enhanced the rapidity of cardiac allograft or skin transplant rejection in mice. Cytokine analysis of in vitro activated CD4⁺ and CD8⁺ T cells revealed that anti-4-1BB costimulation markedly enhanced interferon- production by CD8⁺ T cells and that anti-4-1BB mediated proliferation of CD8⁺ T cells appears to be IL-2 independent. The results of these studies suggest that regulatory signals delivered by the 4-1BB receptor play an important role in the regulation of cytotoxic T cells in cellular immune responses to antigen.

¹Abbreviations used in this paper: 4-1BBL, 4-1BB ligand; EU, endotoxin units; FBS, fetal bovine serum; NGFR, nerve growth factor receptor; SN, activated T cell supernatants.

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• Wilcox, R. A., Chapoval, A. I., Gorski, K. S., Otsuji, M., Shin, T., Flies, D. B., Tamada, K., Mittler, R. S., Tsuchiya, H., Pardoll, D. M., Chen, L. (2002). Expression of Functional CD137 Receptor by Dendritic Cells. J. Immunol. 168: 4262-4267 [Abstract] [Full Text]  
• van Mierlo, G. J. D., den Boer, A. Th., Medema, J. P., van der Voort, E. I. H., Fransen, M. F., Offringa, R., Melief, C. J. M., Toes, R. E. M. (2002). CD40 stimulation leads to effective therapy of CD40- tumors through induction of strong systemic cytotoxic T lymphocyte immunity. Proc. Natl. Acad. Sci. USA 99: 5561-5566 [Abstract] [Full Text]  
• Diehl, L., van Mierlo, G. J. D., den Boer, A. T., van der Voort, E., Fransen, M., van Bostelen, L., Krimpenfort, P., Melief, C. J. M., Mittler, R., Toes, R. E. M., Offringa, R. (2002). In Vivo Triggering Through 4-1BB Enables Th-Independent Priming of CTL in the Presence of an Intact CD28 Costimulatory Pathway. J. Immunol. 168: 3755-3762 [Abstract] [Full Text]  
• Bertram, E. M., Lau, P., Watts, T. H. (2002). Temporal Segregation of 4-1BB Versus CD28-Mediated Costimulation: 4-1BB Ligand Influences T Cell Numbers Late in the Primary Response and Regulates the Size of the T Cell Memory Response Following Influenza Infection. J. Immunol. 168: 3777-3785 [Abstract] [Full Text]  
• Fischbein, M. P., Yun, J., Laks, H., Irie, Y., Fishbein, M. C., Bonavida, B., Ardehali, A. (2002). Role of CD8+ lymphocytes in chronic rejection of transplanted hearts. J. Thorac. Cardiovasc. Surg. 123: 803-809 [Abstract] [Full Text]  
• Futagawa, T., Akiba, H., Kodama, T., Takeda, K., Hosoda, Y., Yagita, H., Okumura, K. (2002). Expression and function of 4-1BB and 4-1BB ligand on murine dendritic cells. Int Immunol 14: 275-286 [Abstract] [Full Text]  
• Yamada, A., Salama, A. D., Sayegh, M. H. (2002). The Role of Novel T Cell Costimulatory Pathways in Autoimmunity and Transplantation. J. Am. Soc. Nephrol. 13: 559-575 [Full Text]  
• Sun, Y., Lin, X., Chen, H. M., Wu, Q., Subudhi, S. K., Chen, L., Fu, Y.-X. (2002). Administration of Agonistic Anti-4-1BB Monoclonal Antibody Leads to the Amelioration of Experimental Autoimmune Encephalomyelitis. J. Immunol. 168: 1457-1465 [Abstract] [Full Text]  
• Kelleher, M., Beverley, P. C. L. (2001). Lipopolysaccharide Modulation of Dendritic Cells Is Insufficient to Mature Dendritic Cells to Generate CTLs from Naive Polyclonal CD8+ T Cells In Vitro, Whereas CD40 Ligation Is Essential. J. Immunol. 167: 6247-6255 [Abstract] [Full Text]  
• Zheng, G., Chen, A., Sterner, R. E., Zhang, P. J., Pan, T., Kiyatkin, N., Tykocinski, M. L. (2001). Induction of Antitumor Immunity via Intratumoral Tetra-Costimulator Protein Transfer. Cancer Res. 61: 8127-8134 [Abstract] [Full Text]  
• Nozawa, K., Ohata, J., Sakurai, J., Hashimoto, H., Miyajima, H., Yagita, H., Okumura, K., Azuma, M. (2001). Preferential Blockade of CD8+ T Cell Responses by Administration of Anti-CD137 Ligand Monoclonal Antibody Results in Differential Effect on Development of Murine Acute and Chronic Graft-Versus-Host Diseases. J. Immunol. 167: 4981-4986 [Abstract] [Full Text]  
• Zhu, G., Flies, D. B., Tamada, K., Sun, Y., Rodriguez, M., Fu, Y.-X., Chen, L. (2001). Progressive Depletion of Peripheral B Lymphocytes in 4-1BB (CD137) Ligand/I-E{alpha}-Transgenic Mice. J. Immunol. 167: 2671-2676 [Abstract] [Full Text]  
• Cannons, J. L., Lau, P., Ghumman, B., DeBenedette, M. A., Yagita, H., Okumura, K., Watts, T. H. (2001). 4-1BB Ligand Induces Cell Division, Sustains Survival, and Enhances Effector Function of CD4 and CD8 T Cells with Similar Efficacy. J. Immunol. 167: 1313-1324 [Abstract] [Full Text]  
• Kim, J. A., Averbook, B. J., Chambers, K., Rothchild, K., Kjaergaard, J., Papay, R., Shu, S. (2001). Divergent Effects of 4-1BB Antibodies on Antitumor Immunity and on Tumor-reactive T-Cell Generation. Cancer Res. 61: 2031-2037 [Abstract] [Full Text]  
• Blazar, B. R., Kwon, B. S., Panoskaltsis-Mortari, A., Kwak, K. B., Peschon, J. J., Taylor, P. A. (2001). Ligation of 4-1BB (CDw137) Regulates Graft-Versus-Host Disease, Graft-Versus-Leukemia, and Graft Rejection in Allogeneic Bone Marrow Transplant Recipients. J. Immunol. 166: 3174-3183 [Abstract] [Full Text]  
• Edelmann, K. H., Wilson, C. B. (2001). Role of CD28/CD80-86 and CD40/CD154 Costimulatory Interactions in Host Defense to Primary Herpes Simplex Virus Infection. J. Virol. 75: 612-621 [Abstract] [Full Text]  
• Broeren, C. P. M., Gray, G. S., Carreno, B. M., June, C. H. (2000). Costimulation Light: Activation of CD4+ T Cells with CD80 or CD86 Rather Than Anti-CD28 Leads to a Th2 Cytokine Profile. J. Immunol. 165: 6908-6914 [Abstract] [Full Text]  
• Cannons, J. L., Choi, Y., Watts, T. H. (2000). Role of TNF Receptor-Associated Factor 2 and p38 Mitogen-Activated Protein Kinase Activation During 4-1BB-Dependent Immune Response. J. Immunol. 165: 6193-6204 [Abstract] [Full Text]  
• Blazar, B. R., Lees, C. J., Martin, P. J., Noelle, R. J., Kwon, B., Murphy, W., Taylor, P. A. (2000). Host T Cells Resist Graft-Versus-Host Disease Mediated by Donor Leukocyte Infusions. J. Immunol. 165: 4901-4909 [Abstract] [Full Text]  
• Lanzavecchia, A., Sallusto, F. (2000). Dynamics of T Lymphocyte Responses: Intermediates, Effectors, and Memory Cells. Science 290: 92-97 [Abstract] [Full Text]  

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