J. Exp. Med., Volume 188, Number 12, December 21, 1998 2357-2368

The Central Role of CD4⁺ T Cells in the Antitumor Immune Response

By Kenneth Hung,^* Robert Hayashi,^§ Anne Lafond-Walker, Charles Lowenstein, Drew Pardoll,^* and Hyam Levitsky^*

From the ^* Department of Oncology and the  Department of Cardiology, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205; and the ^§ Department of Pediatrics, Washington University School of Medicine, St. Louis, Missouri 63110

The induction of optimal systemic antitumor immunity involves the priming of both CD4⁺ and CD8⁺ T cells specific for tumor-associated antigens. The role of CD4⁺ T helper cells (Th) in this response has been largely attributed to providing regulatory signals required for the priming of major histocompatibility complex class I restricted CD8⁺ cytolytic T lymphocytes, which are thought to serve as the dominant effector cell mediating tumor killing. However, analysis of the effector phase of tumor rejection induced by vaccination with irradiated tumor cells transduced to secrete granulocyte/macrophage colony-stimulating factor indicates a far broader role for CD4⁺ T cells in orchestrating the host response to tumor. This form of immunization leads to the simultaneous induction of Th1 and Th2 responses, both of which are required for maximal systemic antitumor immunity. Cytokines produced by these CD4⁺ T cells activate eosinophils as well as macrophages that produce both superoxide and nitric oxide. Both of these cell types then collaborate within the site of tumor challenge to cause its destruction.

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• Bonehill, A., Heirman, C., Tuyaerts, S., Michiels, A., Breckpot, K., Brasseur, F., Zhang, Y., van der Bruggen, P., Thielemans, K. (2004). Messenger RNA-Electroporated Dendritic Cells Presenting MAGE-A3 Simultaneously in HLA Class I and Class II Molecules. J. Immunol. 172: 6649-6657 [Abstract] [Full Text]  
• Leitch, J., Fraser, K., Lane, C., Putzu, K., Adema, G. J., Zhang, Q.-J., Jefferies, W. A., Bramson, J. L., Wan, Y. (2004). CTL-Dependent and -Independent Antitumor Immunity Is Determined by the Tumor Not the Vaccine. J. Immunol. 172: 5200-5205 [Abstract] [Full Text]  
• Mihalyo, M. A., Doody, A. D. H., McAleer, J. P., Nowak, E. C., Long, M., Yang, Y., Adler, A. J. (2004). In Vivo Cyclophosphamide and IL-2 Treatment Impedes Self-Antigen-Induced Effector CD4 Cell Tolerization: Implications for Adoptive Immunotherapy. J. Immunol. 172: 5338-5345 [Abstract] [Full Text]  
• Ruiz, M., Kobayashi, H., Lasarte, J. J., Prieto, J., Borras-Cuesta, F., Celis, E., Sarobe, P. (2004). Identification and Characterization of a T-Helper Peptide from Carcinoembryonic Antigen. Clin. Cancer Res. 10: 2860-2867 [Abstract] [Full Text]  
• Hanson, H. L., Kang, S. S., Norian, L. A., Matsui, K., O'Mara, L. A., Allen, P. M. (2004). CD4-Directed Peptide Vaccination Augments an Antitumor Response, but Efficacy Is Limited by the Number of CD8+ T Cell Precursors. J. Immunol. 172: 4215-4224 [Abstract] [Full Text]  
• Lu, J., Higashimoto, Y., Appella, E., Celis, E. (2004). Multiepitope Trojan Antigen Peptide Vaccines for the Induction of Antitumor CTL and Th Immune Responses. J. Immunol. 172: 4575-4582 [Abstract] [Full Text]  
• Mapara, M. Y., Sykes, M. (2004). Tolerance and Cancer: Mechanisms of Tumor Evasion and Strategies for Breaking Tolerance. JCO 22: 1136-1151 [Abstract] [Full Text]  
• Dissanayake, S. K., Thompson, J. A., Bosch, J. J., Clements, V. K., Chen, P. W., Ksander, B. R., Ostrand-Rosenberg, S. (2004). Activation of Tumor-specific CD4+ T Lymphocytes by Major Histocompatibility Complex Class II Tumor Cell Vaccines: A Novel Cell-based Immunotherapy. Cancer Res. 64: 1867-1874 [Abstract] [Full Text]  
• Atanackovic, D., Altorki, N. K., Stockert, E., Williamson, B., Jungbluth, A. A., Ritter, E., Santiago, D., Ferrara, C. A., Matsuo, M., Selvakumar, A., Dupont, B., Chen, Y.-T., Hoffman, E. W., Ritter, G., Old, L. J., Gnjatic, S. (2004). Vaccine-Induced CD4+ T Cell Responses to MAGE-3 Protein in Lung Cancer Patients. J. Immunol. 172: 3289-3296 [Abstract] [Full Text]  
• Friedman, R. S., Bangur, C. S., Zasloff, E. J., Fan, L., Wang, T., Watanabe, Y., Kalos, M. (2004). Molecular and Immunological Evaluation of the Transcription Factor SOX-4 as a Lung Tumor Vaccine Antigen. J. Immunol. 172: 3319-3327 [Abstract] [Full Text]  
• Godfrey, W. R., Krampf, M. R., Taylor, P. A., Blazar, B. R. (2004). Ex vivo depletion of alloreactive cells based on CFSE dye dilution, activation antigen selection, and dendritic cell stimulation. Blood 103: 1158-1165 [Abstract] [Full Text]  
• Schultz, E. S., Schuler-Thurner, B., Stroobant, V., Jenne, L., Berger, T. G., Thielemanns, K., van der Bruggen, P., Schuler, G. (2004). Functional Analysis of Tumor-Specific Th Cell Responses Detected in Melanoma Patients after Dendritic Cell-Based Immunotherapy. J. Immunol. 172: 1304-1310 [Abstract] [Full Text]  
• Hu, D.-E., Dyke, S. O. M., Moore, A. M., Thomsen, L. L., Brindle, K. M. (2004). Tumor Cell-Derived Nitric Oxide Is Involved in the Immune-Rejection of an Immunogenic Murine Lymphoma. Cancer Res. 64: 152-161 [Abstract] [Full Text]  
• Dobrzanski, M. J., Reome, J. B., Hollenbaugh, J. A., Hylind, J. C., Dutton, R. W. (2004). Effector Cell-Derived Lymphotoxin {alpha} and Fas Ligand, but not Perforin, Promote Tc1 and Tc2 Effector Cell-Mediated Tumor Therapy in Established Pulmonary Metastases. Cancer Res. 64: 406-414 [Abstract] [Full Text]  
• Della Bella, S., Nicola, S., Riva, A., Biasin, M., Clerici, M., Villa, M. L. (2004). Functional repertoire of dendritic cells generated in granulocyte macrophage-colony stimulating factor and interferon-{alpha}. J. Leukoc. Biol. 75: 106-116 [Abstract] [Full Text]  
• Cuenca, A., Cheng, F., Wang, H., Brayer, J., Horna, P., Gu, L., Bien, H., Borrello, I. M., Levitsky, H. I., Sotomayor, E. M. (2003). Extra-Lymphatic Solid Tumor Growth Is Not Immunologically Ignored and Results in Early Induction of Antigen-Specific T-Cell Anergy: Dominant Role of Cross-Tolerance to Tumor Antigens. Cancer Res. 63: 9007-9015 [Abstract] [Full Text]  
• Casares, N., Arribillaga, L., Sarobe, P., Dotor, J., Lopez-Diaz de Cerio, A., Melero, I., Prieto, J., Borras-Cuesta, F., Lasarte, J. J. (2003). CD4+/CD25+ Regulatory Cells Inhibit Activation of Tumor-Primed CD4+ T Cells with IFN-{gamma}-Dependent Antiangiogenic Activity, as well as Long-Lasting Tumor Immunity Elicited by Peptide Vaccination. J. Immunol. 171: 5931-5939 [Abstract] [Full Text]  
• Goldszmid, R. S., Idoyaga, J., Bravo, A. I., Steinman, R., Mordoh, J., Wainstok, R. (2003). Dendritic Cells Charged with Apoptotic Tumor Cells Induce Long-Lived Protective CD4+ and CD8+ T Cell Immunity against B16 Melanoma. J. Immunol. 171: 5940-5947 [Abstract] [Full Text]  
• Zhao, Y., Boczkowski, D., Nair, S. K., Gilboa, E. (2003). Inhibition of invariant chain expression in dendritic cells presenting endogenous antigens stimulates CD4+ T-cell responses and tumor immunity. Blood 102: 4137-4142 [Abstract] [Full Text]  
• Rodolfo, M., Luksch, R., Stockert, E., Chen, Y.-T., Collini, P., Ranzani, T., Lombardo, C., Dalerba, P., Rivoltini, L., Arienti, F., Fossati-Bellani, F., Old, L. J., Parmiani, G., Castelli, C. (2003). Antigen-Specific Immunity in Neuroblastoma Patients: Antibody and T-Cell Recognition of NY-ESO-1 Tumor Antigen. Cancer Res. 63: 6948-6955 [Abstract] [Full Text]  

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