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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.

This study was financed by the Netherlands Cancer Foundation grants 93-560 and 97-1451.

Address correspondence to F. Ossendorp, Department of Immunohematology and Bloodbank, University Hospital Leiden, Bldg. 1, E3-Q, PO Box 9600, 2300 RC Leiden, The Netherlands. Phone: 31-71-5263800; Fax: 31-71-5216751; E-mail: ossendorp{at}rullf2.medfac.leidenuniv.nl

¹ Abbreviations used in this paper: FMR, Friend, Moloney, Rauscher; gag-L, gag-leader; gp, glycoprotein; MoMSV, Moloney murine sarcoma and leukemia virus complex; MuLV, murine leukemia virus; n.s., not significant.

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• Mulryan, K., Ryan, M. G., Myers, K. A., Shaw, D., Wang, W., Kingsman, S. M., Stern, P. L., Carroll, M. W. (2002). Attenuated Recombinant Vaccinia Virus Expressing Oncofetal Antigen (Tumor-associated Antigen) 5T4 Induces Active Therapy of Established Tumors. Molecular Cancer Therapeutics 1: 1129-1137 [Abstract] [Full Text]  
• Schepers, K., Toebes, M., Sotthewes, G., Vyth-Dreese, F. A., Dellemijn, T. A. M., Melief, C. J. M., Ossendorp, F., Schumacher, T. N. M. (2002). Differential Kinetics of Antigen-Specific CD4+ and CD8+ T Cell Responses in the Regression of Retrovirus-Induced Sarcomas. J. Immunol. 169: 3191-3199 [Abstract] [Full Text]  
• Su, Z., Vieweg, J., Weizer, A. Z., Dahm, P., Yancey, D., Turaga, V., Higgins, J., Boczkowski, D., Gilboa, E., Dannull, J. (2002). Enhanced Induction of Telomerase-specific CD4+ T Cells Using Dendritic Cells Transfected with RNA Encoding a Chimeric Gene Product. Cancer Res. 62: 5041-5048 [Abstract] [Full Text]  
• Zeng, G., Li, Y., El-Gamil, M., Sidney, J., Sette, A., Wang, R.-f., Rosenberg, S. A., Robbins, P. F. (2002). Generation of NY-ESO-1-specific CD4+ and CD8+ T Cells by a Single Peptide with Dual MHC Class I and Class II Specificities: A New Strategy for Vaccine Design. Cancer Res. 62: 3630-3635 [Abstract] [Full Text]  
• Zwaveling, S., Mota, S. C. F., Nouta, J., Johnson, M., Lipford, G. B., Offringa, R., van der Burg, S. H., Melief, C. J. M. (2002). Established Human Papillomavirus Type 16-Expressing Tumors Are Effectively Eradicated Following Vaccination with Long Peptides. J. Immunol. 169: 350-358 [Abstract] [Full Text]  
• Stern, B. V., Boehm, B. O., Tary-Lehmann, M. (2002). Vaccination with Tumor Peptide in CpG Adjuvant Protects Via IFN-{gamma}-Dependent CD4 Cell Immunity. J. Immunol. 168: 6099-6105 [Abstract] [Full Text]  
• Wang, H. Y., Zhou, J., Zhu, K., Riker, A. I., Marincola, F. M., Wang, R.-F. (2002). Identification of a Mutated Fibronectin As a Tumor Antigen Recognized by CD4+T Cells: Its Role in Extracellular Matrix Formation and Tumor Metastasis. JEM 195: 1397-1406 [Abstract] [Full Text]  
• Schroers, R., Huang, X. F., Hammer, J., Zhang, J., Chen, S.-Y. (2002). Identification of HLA DR7-restricted Epitopes from Human Telomerase Reverse Transcriptase Recognized by CD4+ T-Helper Cells. Cancer Res. 62: 2600-2605 [Abstract] [Full Text]  
• Kelly, J. M., Takeda, K., Darcy, P. K., Yagita, H., Smyth, M. J. (2002). A Role for IFN-{gamma} in Primary and Secondary Immunity Generated by NK Cell-Sensitive Tumor-Expressing CD80 In Vivo. J. Immunol. 168: 4472-4479 [Abstract] [Full Text]  
• Haupt, K., Roggendorf, M., Mann, K. (2002). The Potential of DNA Vaccination against Tumor-Associated Antigens for Antitumor Therapy. Exp. Biol. Med. 227: 227-237 [Abstract] [Full Text]  
• Huang, H., Li, F., Gordon, J. R., Xiang, J. (2002). Synergistic Enhancement of Antitumor Immunity with Adoptively Transferred Tumor-specific CD4+ and CD8+ T Cells and Intratumoral Lymphotactin Transgene Expression. Cancer Res. 62: 2043-2051 [Abstract] [Full Text]  
• Tutt, A. L., O'Brien, L., Hussain, A., Crowther, G. R., French, R. R., Glennie, M. J. (2002). T Cell Immunity to Lymphoma Following Treatment with Anti-CD40 Monoclonal Antibody. J. Immunol. 168: 2720-2728 [Abstract] [Full Text]  
• Machy, P., Serre, K., Baillet, M., Leserman, L. (2002). Induction of MHC Class I Presentation of Exogenous Antigen by Dendritic Cells Is Controlled by CD4+ T Cells Engaging Class II Molecules in Cholesterol-Rich Domains. J. Immunol. 168: 1172-1180 [Abstract] [Full Text]  
• 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]  

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