J. Exp. Med., Volume 187, Number 5, March 2, 1998 693-702

Specific T Helper Cell Requirement for Optimal Induction of Cytotoxic T Lymphocytes against Major Histocompatibility Complex Class II Negative Tumors

By Ferry Ossendorp, Erica Mengedé, Marcel Camps, Rian Filius, and Cornelis J.M. Melief

From the Department of Immunohematology and Bloodbank, Leiden University Medical Center, 2300 RC Leiden, The Netherlands

This study shows that induction of tumor-specific CD4⁺ T cells by vaccination with a specific viral T helper epitope, contained within a synthetic peptide, results in protective immunity against major histocompatibility complex (MHC) class II negative, virus-induced tumor cells. Protection was also induced against sarcoma induction by acutely transforming retrovirus. In contrast, no protective immunity was induced by vaccination with an unrelated T helper epitope. By cytokine pattern analysis, the induced CD4⁺ T cells were of the T helper cell 1 type. The peptide-specific CD4⁺ T cells did not directly recognize the tumor cells, indicating involvement of cross-priming by tumor-associated antigen-presenting cells. The main effector cells responsible for tumor eradication were identified as CD8⁺ cytotoxic T cells that were found to recognize a recently described immunodominant viral gag-encoded cytotoxic T lymphocyte (CTL) epitope, which is unrelated to the viral env-encoded T helper peptide sequence. Simultaneous vaccination with the tumor-specific T helper and CTL epitopes resulted in strong synergistic protection. These results indicate the crucial role of T helper cells for optimal induction of protective immunity against MHC class II negative tumor cells. Protection is dependent on tumor-specific CTLs in this model system and requires cross-priming of tumor antigens by specialized antigen-presenting cells. Thus, tumor-specific T helper epitopes have to be included in the design of epitope-based vaccines.

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• Tham, E. L., Shrikant, P., Mescher, M. F. (2002). Activation-Induced Nonresponsiveness: A Th-Dependent Regulatory Checkpoint in the CTL Response. J. Immunol. 168: 1190-1197 [Abstract] [Full Text]  
• Segal, B. M., Glass, D. D., Shevach, E. M. (2002). Cutting Edge: IL-10-Producing CD4+ T Cells Mediate Tumor Rejection. J. Immunol. 168: 1-4 [Abstract] [Full Text]  
• Ribas, A., Butterfield, L. H., Amarnani, S. N., Dissette, V. B., Kim, D., Meng, W. S., Miranda, G. A., Wang, H.-J., McBride, W. H., Glaspy, J. A., Economou, J. S. (2001). CD40 Cross-Linking Bypasses the Absolute Requirement for CD4 T Cells during Immunization with Melanoma Antigen Gene-modified Dendritic Cells. Cancer Res. 61: 8787-8793 [Abstract] [Full Text]  
• Meyer zum Buschenfelde, C., Metzger, J., Hermann, C., Nicklisch, N., Peschel, C., Bernhard, H. (2001). The Generation of Both T Killer and Th Cell Clones Specific for the Tumor-Associated Antigen HER2 Using Retrovirally Transduced Dendritic Cells. J. Immunol. 167: 1712-1719 [Abstract] [Full Text]  
• Motta, I., Andre, F., Lim, A., Tartaglia, J., Cox, W. I., Zitvogel, L., Angevin, E., Kourilsky, P. (2001). Cross-Presentation by Dendritic Cells of Tumor Antigen Expressed in Apoptotic Recombinant Canarypox Virus-Infected Dendritic Cells. J. Immunol. 167: 1795-1802 [Abstract] [Full Text]  
• Reali, E., Greiner, J. W., Corti, A., Gould, H. J., Bottazzoli, F., Paganelli, G., Schlom, J., Siccardi, A. G. (2001). IgEs Targeted on Tumor Cells: Therapeutic Activity and Potential in the Design of Tumor Vaccines. Cancer Res. 61: 5517-5522 [Abstract] [Full Text]  
• Golgher, D., Korangy, F., Gao, B., Gorski, K., Jaffee, E., Edidin, M., Pardoll, D. M., Elliott, T. (2001). An Immunodominant MHC Class II-Restricted Tumor Antigen Is Conformation Dependent and Binds to the Endoplasmic Reticulum Chaperone, Calreticulin. J. Immunol. 167: 147-155 [Abstract] [Full Text]  
• Kobayashi, H., Song, Y., Hoon, D. S. B., Appella, E., Celis, E. (2001). Tumor-reactive T Helper Lymphocytes Recognize a Promiscuous MAGE-A3 Epitope Presented by Various Major Histocompatibility Complex Class II Alleles. Cancer Res. 61: 4773-4778 [Abstract] [Full Text]  
• Ju, D. W., Tao, Q., Lou, G., Bai, M., He, L., Yang, Y., Cao, X. (2001). Interleukin 18 Transfection Enhances Antitumor Immunity Induced by Dendritic Cell-Tumor Cell Conjugates. Cancer Res. 61: 3735-3740 [Abstract] [Full Text]  
• Christ, O., Matzku, S., Burger, C., Zöller, M. (2001). Interleukin 2-Antibody and Tumor Necrosis Factor-Antibody Fusion Proteins Induce Different Antitumor Immune Responses in Vivo. Clin. Cancer Res. 7: 1385-1397 [Abstract] [Full Text]  
• Eck, S. C., Turka, L. A. (2001). Adoptive Transfer Enables Tumor Rejection Targeted against a Self-Antigen without the Induction of Autoimmunity. Cancer Res. 61: 3077-3083 [Abstract] [Full Text]  
• Okada, H., Attanucci, J., Giezeman-Smits, K. M., Brissette-Storkus, C., Fellows, W. K., Gambotto, A., Pollack, I. F., Pogue-Geile, K., Lotze, M. T., Bozik, M. E., Chambers, W. H. (2001). Immunization with an Antigen Identified by Cytokine Tumor Vaccine-assisted SEREX (CAS) Suppressed Growth of the Rat 9L Glioma in Vivo. Cancer Res. 61: 2625-2631 [Abstract] [Full Text]  
• Zoller, M., Christ, O. (2001). Prophylactic Tumor Vaccination: Comparison of Effector Mechanisms Initiated by Protein Versus DNA Vaccination. J. Immunol. 166: 3440-3450 [Abstract] [Full Text]  
• You, Z., Hester, J., Rollins, L., Spagnoli, G. C., van der Bruggen, P., Chen, S.-Y. (2001). A Retrogen Strategy for Presentation of an Intracellular Tumor Antigen as an Exogenous Antigen by Dendritic Cells Induces Potent Antitumor T Helper and CTL Responses. Cancer Res. 61: 197-205 [Abstract] [Full Text]  
• Marzo, A. L., Kinnear, B. F., Lake, R. A., Frelinger, J. J., Collins, E. J., Robinson, B. W. S., Scott, B. (2000). Tumor-Specific CD4+ T Cells Have a Major ""Post-Licensing"" Role in CTL Mediated Anti-Tumor Immunity. J. Immunol. 165: 6047-6055 [Abstract] [Full Text]  
• Qi, L., Rojas, J.-M., Ostrand-Rosenberg, S. (2000). Tumor Cells Present MHC Class II-Restricted Nuclear and Mitochondrial Antigens and Are the Predominant Antigen Presenting Cells In Vivo. J. Immunol. 165: 5451-5461 [Abstract] [Full Text]  
• Fallarino, F., Grohmann, U., Bianchi, R., Vacca, C., Fioretti, M. C., Puccetti, P. (2000). Th1 and Th2 Cell Clones to a Poorly Immunogenic Tumor Antigen Initiate CD8+ T Cell-Dependent Tumor Eradication In Vivo. J. Immunol. 165: 5495-5501 [Abstract] [Full Text]  
• Riemersma, S. A., Jordanova, E. S., Schop, R. F. J., Philippo, K., Looijenga, L. H. J., Schuuring, E., Kluin, P. M. (2000). Extensive genetic alterations of the HLA region, including homozygous deletions of HLA class II genes in B-cell lymphomas arising in immune-privileged sites. Blood 96: 3569-3577 [Abstract] [Full Text]  
• Schultz, E. S., Lethé, B., Cambiaso, C. L., Van Snick, J., Chaux, P., Corthals, J., Heirman, C., Thielemans, K., Boon, T., van der Bruggen, P. (2000). A MAGE-A3 Peptide Presented by HLA-DP4 Is Recognized on Tumor Cells by CD4+ Cytolytic T Lymphocytes. Cancer Res. 60: 6272-6275 [Abstract] [Full Text]  
• van Bergen, J., Camps, M., Offringa, R., Melief, C. J. M., Ossendorp, F., Koning, F. (2000). Superior Tumor Protection Induced by a Cellular Vaccine Carrying a Tumor-specific T Helper Epitope by Genetic Exchange of the Class II-associated Invariant Chain Peptide. Cancer Res. 60: 6427-6433 [Abstract] [Full Text]  

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