Vaccination with Mage-3A1 Peptide-pulsed Mature, Monocyte-derived Dendritic Cells Expands Specific Cytotoxic T Cells and Induces Regression of Some Metastases in Advanced Stage IV Melanoma

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© The Rockefeller University Press, 0022-1007/1999/12/1669/ $5.00
The Journal of Experimental Medicine, Volume 190, Number 11, December 6, 1999 1669-1678

Original Article

Vaccination with Mage-3A1 Peptide–pulsed Mature, Monocyte-derived Dendritic Cells Expands Specific Cytotoxic T Cells and Induces Regression of Some Metastases in Advanced Stage IV Melanoma

Beatrice Thurner^a, Ina Haendle^a, Claudia Röder^a, Detlef Dieckmann^a, Petra Keikavoussi^b, Helmut Jonuleit^c, Armin Bender^a, Christian Maczek^a, Doris Schreiner^a, Peter von den Driesch^a, Eva B. Bröcker^b, Ralph M. Steinman^d, Alexander Enk^c, Eckhart Kämpgen^b, and Gerold Schuler^a
^a Department of Dermatology, University of Erlangen-Nuremberg, D-91052 Erlangen, Germany
^b Department of Dermatology, University of Würzburg, D-97080 Würzburg, Germany
^c Department of Dermatology, University of Mainz, D-55131 Mainz, Germany
^d Laboratory of Cellular Physiology and Immunology, The Rockefeller University, New York, New York 10021

Correspondence to: Gerold Schuler, Dermatologische Klinik mit Poliklinik, Hartmannstr. 14, D-91052 Erlangen, Germany. Tel:49-9131-85-0, ext. 33661 Fax:49-9131-85-6175 E-mail:schuler{at}derma.med.uni-erlangen.de.

Dendritic cells (DCs) are considered to be promising adjuvantsfor inducing immunity to cancer. We used mature, monocyte-derivedDCs to elicit resistance to malignant melanoma. The DCs werepulsed with Mage-3A1 tumor peptide and a recall antigen, tetanustoxoid or tuberculin. 11 far advanced stage IV melanoma patients,who were progressive despite standard chemotherapy, receivedfive DC vaccinations at 14-d intervals. The first three vaccinationswere administered into the skin, 3 x 10⁶ DCs each subcutaneouslyand intradermally, followed by two intravenous injections of6 x 10⁶ and 12 x 10⁶ DCs, respectively. Only minor (less thanor equal to grade II) side effects were observed. Immunity tothe recall antigen was boosted. Significant expansions of Mage-3A1–specificCD8⁺ cytotoxic T lymphocyte (CTL) precursors were induced in8/11 patients. Curiously, these immune responses often declinedafter the intravenous vaccinations. Regressions of individualmetastases (skin, lymph node, lung, and liver) were evidentin 6/11 patients. Resolution of skin metastases in two of thepatients was accompanied by erythema and CD8⁺ T cell infiltration,whereas nonregressing lesions lacked CD8⁺ T cells as well asMage-3 mRNA expression. This study proves the principle thatDC "vaccines" can frequently expand tumor-specific CTLs andelicit regressions even in advanced cancer and, in addition,provides evidence for an active CD8⁺ CTL–tumor cell interactionin situ as well as escape by lack of tumor antigen expression.

Key Words: dendritic cells, vaccination, active immunotherapy, melanoma,cytotoxic T lymphocytes

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Maraskovsky, E., Sjolander, S., Drane, D. P., Schnurr, M., Le, T. T. T., Mateo, L., Luft, T., Masterman, K.-A., Tai, T.-Y., Chen, Q., Green, S., Sjolander, A., Pearse, M. J., Lemonnier, F. A., Chen, W., Cebon, J., Suhrbier, A. (2004). NY-ESO-1 Protein Formulated in ISCOMATRIX Adjuvant Is a Potent Anticancer Vaccine Inducing Both Humoral and CD8+ T-Cell-Mediated Immunity and Protection against NY-ESO-1+ Tumors. Clin. Cancer Res. 10: 2879-2890 [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]
Yang, S., Haluska, F. G. (2004). Treatment of Melanoma with 5-Fluorouracil or Dacarbazine In Vitro Sensitizes Cells to Antigen-Specific CTL Lysis through Perforin/Granzyme- and Fas-Mediated Pathways. J. Immunol. 172: 4599-4608 [Abstract] [Full Text]
Coughlin, C. M., Vance, B. A., Grupp, S. A., Vonderheide, R. H. (2004). RNA-transfected CD40-activated B cells induce functional T-cell responses against viral and tumor antigen targets: implications for pediatric immunotherapy. Blood 103: 2046-2054 [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]
Breckpot, K., Heirman, C., De Greef, C., van der Bruggen, P., Thielemans, K. (2004). Identification of New Antigenic Peptide Presented by HLA-Cw7 and Encoded by Several MAGE Genes Using Dendritic Cells Transduced with Lentiviruses. J. Immunol. 172: 2232-2237 [Abstract] [Full Text]
Jackson, S. H., Yu, C.-R., Mahdi, R. M., Ebong, S., Egwuagu, C. E. (2004). Dendritic Cell Maturation Requires STAT1 and Is under Feedback Regulation by Suppressors of Cytokine Signaling. J. Immunol. 172: 2307-2315 [Abstract] [Full Text]
Schmidt, S. M., Schag, K., Muller, M. R., Weinschenk, T., Appel, S., Schoor, O., Weck, M. M., Grunebach, F., Kanz, L., Stevanovic, S., Rammensee, H.-G., Brossart, P. (2004). Induction of Adipophilin-Specific Cytotoxic T Lymphocytes Using a Novel HLA-A2-Binding Peptide That Mediates Tumor Cell Lysis. Cancer Res. 64: 1164-1170 [Abstract] [Full Text]
Vonderheide, R. H., Domchek, S. M., Schultze, J. L., George, D. J., Hoar, K. M., Chen, D.-Y., Stephans, K. F., Masutomi, K., Loda, M., Xia, Z., Anderson, K. S., Hahn, W. C., Nadler, L. M. (2004). Vaccination of Cancer Patients Against Telomerase Induces Functional Antitumor CD8+ T Lymphocytes. Clin. Cancer Res. 10: 828-839 [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]
Barlogie, B., Shaughnessy, J., Tricot, G., Jacobson, J., Zangari, M., Anaissie, E., Walker, R., Crowley, J. (2004). Treatment of multiple myeloma. Blood 103: 20-32 [Abstract] [Full Text]
Brown, K., Gao, W., Alber, S., Trichel, A., Murphey-Corb, M., Watkins, S. C., Gambotto, A., Barratt-Boyes, S. M. (2003). Adenovirus-Transduced Dendritic Cells Injected into Skin or Lymph Node Prime Potent Simian Immunodeficiency Virus-Specific T Cell Immunity in Monkeys. J. Immunol. 171: 6875-6882 [Abstract] [Full Text]
Butterfield, L. H., Ribas, A., Meng, W. S., Dissette, V. B., Amarnani, S., Vu, H. T., Seja, E., Todd, K., Glaspy, J. A., McBride, W. H., Economou, J. S. (2003). T-Cell Responses to HLA-A*0201 Immunodominant Peptides Derived from {alpha}-Fetoprotein in Patients with Hepatocellular Cancer. Clin. Cancer Res. 9: 5902-5908 [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]
Godelaine, D., Carrasco, J., Lucas, S., Karanikas, V., Schuler-Thurner, B., Coulie, P. G., Schuler, G., Boon, T., Van Pel, A. (2003). Polyclonal CTL Responses Observed in Melanoma Patients Vaccinated with Dendritic Cells Pulsed with a MAGE-3.A1 Peptide. J. Immunol. 171: 4893-4897 [Abstract] [Full Text]
Karanikas, V., Lurquin, C., Colau, D., van Baren, N., De Smet, C., Lethe, B., Connerotte, T., Corbiere, V., Demoitie, M.-A., Lienard, D., Dreno, B., Velu, T., Boon, T., Coulie, P. G. (2003). Monoclonal Anti-MAGE-3 CTL Responses in Melanoma Patients Displaying Tumor Regression after Vaccination with a Recombinant Canarypox Virus. J. Immunol. 171: 4898-4904 [Abstract] [Full Text]
de Vries, I. J. M., Lesterhuis, W. J., Scharenborg, N. M., Engelen, L. P. H., Ruiter, D. J., Gerritsen, M.-J. P., Croockewit, S., Britten, C. M., Torensma, R., Adema, G. J., Figdor, C. G., Punt, C. J. A. (2003). Maturation of Dendritic Cells Is a Prerequisite for Inducing Immune Responses in Advanced Melanoma Patients. Clin. Cancer Res. 9: 5091-5100 [Abstract] [Full Text]
Bedrosian, I., Mick, R., Xu, S., Nisenbaum, H., Faries, M., Zhang, P., Cohen, P. A., Koski, G., Czerniecki, B. J. (2003). Intranodal Administration of Peptide-Pulsed Mature Dendritic Cell Vaccines Results in Superior CD8+ T-Cell Function in Melanoma Patients. JCO 21: 3826-3835 [Abstract] [Full Text]
de Rijke, B., Fredrix, H., Zoetbrood, A., Scherpen, F., Witteveen, H., de Witte, T., van de Wiel-van Kemenade, E., Dolstra, H. (2003). Generation of autologous cytotoxic and helper T-cell responses against the B-cell leukemia-associated antigen HB-1: relevance for precursor B-ALL-specific immunotherapy. Blood 102: 2885-2891 [Abstract] [Full Text]
Wissniowski, T. T., Hansler, J., Neureiter, D., Frieser, M., Schaber, S., Esslinger, B., Voll, R., Strobel, D., Hahn, E. G., Schuppan, D. (2003). Activation of Tumor-specific T Lymphocytes by Radio-Frequency Ablation of the VX2 Hepatoma in Rabbits. Cancer Res. 63: 6496-6500 [Abstract] [Full Text]
Soiffer, R., Hodi, F. S., Haluska, F., Jung, K., Gillessen, S., Singer, S., Tanabe, K., Duda, R., Mentzer, S., Jaklitsch, M., Bueno, R., Clift, S., Hardy, S., Neuberg, D., Mulligan, R., Webb, I., Mihm, M., Dranoff, G. (2003). Vaccination With Irradiated, Autologous Melanoma Cells Engineered to Secrete Granulocyte-Macrophage Colony-Stimulating Factor by Adenoviral-Mediated Gene Transfer Augments Antitumor Immunity in Patients With Metastatic Melanoma. JCO 21: 3343-3350 [Abstract] [Full Text]
Lindner, I., Kharfan-Dabaja, M. A., Ayala, E., Kolonias, D., Carlson, L. M., Beazer-Barclay, Y., Scherf, U., Hnatyszyn, J. H., Lee, K. P. (2003). Induced Dendritic Cell Differentiation of Chronic Myeloid Leukemia Blasts Is Associated with Down-Regulation of BCR-ABL. J. Immunol. 171: 1780-1791 [Abstract] [Full Text]
Hayashi, T., Hideshima, T., Akiyama, M., Raje, N., Richardson, P., Chauhan, D., Anderson, K. C. (2003). Ex vivo induction of multiple myeloma-specific cytotoxic T lymphocytes. Blood 102: 1435-1442 [Abstract] [Full Text]
Nakahara, S., Tsunoda, T., Baba, T., Asabe, S., Tahara, H. (2003). Dendritic Cells Stimulated with a Bacterial Product, OK-432, Efficiently Induce Cytotoxic T Lymphocytes Specific to Tumor Rejection Peptide. Cancer Res. 63: 4112-4118 [Abstract] [Full Text]
Schmidt, S. M., Schag, K., Muller, M. R., Weck, M. M., Appel, S., Kanz, L., Grunebach, F., Brossart, P. (2003). Survivin is a shared tumor-associated antigen expressed in a broad variety of malignancies and recognized by specific cytotoxic T cells. Blood 102: 571-576 [Abstract] [Full Text]
Sato, M., Chamoto, K., Nishimura, T. (2003). A novel tumor-vaccine cell therapy using bone marrow-derived dendritic cell type 1 and antigen-specific Th1 cells. Int Immunol 15: 837-843 [Abstract] [Full Text]
Tschoep, K., Manning, T. C., Harlin, H., George, C., Johnson, M., Gajewski, T. F. (2003). Disparate functions of immature and mature human myeloid dendritic cells: implications for dendritic cell-based vaccines. J. Leukoc. Biol. 74: 69-80 [Abstract] [Full Text]
Camporeale, A., Boni, A., Iezzi, G., Degl'Innocenti, E., Grioni, M., Mondino, A., Bellone, M. (2003). Critical Impact of the Kinetics of Dendritic Cells Activation on the in Vivo Induction of Tumor-specific T Lymphocytes. Cancer Res. 63: 3688-3694 [Abstract] [Full Text]
Zhang, Y., Chaux, P., Stroobant, V., Eggermont, A. M. M., Corthals, J., Maillere, B., Thielemans, K., Marchand, M., Boon, T., van der Bruggen, P. (2003). A MAGE-3 Peptide Presented by HLA-DR1 to CD4+ T Cells That Were Isolated from a Melanoma Patient Vaccinated with a MAGE-3 Protein. J. Immunol. 171: 219-225 [Abstract] [Full Text]
Gilliet, M., Kleinhans, M., Lantelme, E., Schadendorf, D., Burg, G., Nestle, F. O. (2003). Intranodal injection of semimature monocyte-derived dendritic cells induces T helper type 1 responses to protein neoantigen. Blood 102: 36-42 [Abstract] [Full Text]
Peterson, A. C., Harlin, H., Gajewski, T. F. (2003). Immunization With Melan-A Peptide-Pulsed Peripheral Blood Mononuclear Cells Plus Recombinant Human Interleukin-12 Induces Clinical Activity and T-Cell Responses in Advanced Melanoma. JCO 21: 2342-2348 [Abstract] [Full Text]
Parmiani, G., Pilla, L., Castelli, C., Rivoltini, L. (2003). Vaccination of patients with solid tumours. Ann Oncol 14: 817-824 [Abstract] [Full Text]
Yamada, A., Kawano, K., Koga, M., Takamori, S., Nakagawa, M., Itoh, K. (2003). Gene and Peptide Analyses of Newly Defined Lung Cancer Antigens Recognized by HLA-A2402-restricted Tumor-specific Cytotoxic T Lymphocytes. Cancer Res. 63: 2829-2835 [Abstract] [Full Text]