J. Exp. Med., Volume 187, Number 2, January 19, 1998 265-270

BRIEF DEFINITIVE REPORT:
Simultaneous Humoral and Cellular Immune Response against Cancer-Testis Antigen NY-ESO-1: Definition of Human Histocompatibility Leukocyte Antigen (HLA)-A2-binding Peptide Epitopes

By Elke Jäger,^* Yao-Tseng Chen,^§ Jan W. Drijfhout, Julia Karbach,^* Mark Ringhoffer,^* Dirk Jäger,^* Michael Arand,^¶ Hisashi Wada,^§ Yuji Noguchi,^§ Elisabeth Stockert,^§ Lloyd J. Old,^§ and Alexander Knuth^*

From the ^* II. Medizinische Klinik, Hämatologie-Onkologie, Krankenhaus Nordwest, 60488 Frankfurt, Germany;  Cornell University Medical College, New York 10021; ^§ Ludwig Institute for Cancer Research, New York Branch at Memorial Sloan-Kettering Cancer Center, New York 10021;  Department of Immunohaematology and Blood Bank, Leiden University Hospital, 2300 Leiden, The Netherlands; and ^¶ Institut für Toxikologie, Johannes Gutenberg Universität, 55131 Mainz, Germany

A growing number of human tumor antigens have been described that can be recognized by cytotoxic T lymphocytes (CTLs) in a major histocompatibility complex (MHC) class I-restricted fashion. Serological screening of cDNA expression libraries, SEREX, has recently been shown to provide another route for defining immunogenic human tumor antigens. The detection of antibody responses against known CTL-defined tumor antigens, e.g., MAGE-1 and tyrosinase, raised the question whether antibody and CTL responses against a defined tumor antigen can occur simultaneously in a single patient. In this paper, we report on a melanoma patient with a high-titer antibody response against the "cancer-testis" antigen NY-ESO-1. Concurrently, a strong MHC class I-restricted CTL reactivity against the autologous NY-ESO-1-positive tumor cell line was found. A stable CTL line (NW38-IVS-1) was established from this patient that reacted with autologous melanoma cells and with allogeneic human histocompatibility leukocyte antigen (HLA)-A2, NY-ESO-1-positive, but not NY-ESO-1-negative, melanoma cells. Screening of NY-ESO-1 transfectants with NW38-IVS-1 revealed NY-ESO-1 as the relevant CTL target presented by HLA-A2. Computer calculation identified 26 peptides with HLA-A2-binding motifs encoded by NY-ESO-1. Of these, three peptides were efficiently recognized by NW38-IVS-1. Thus, we show that antigen-specific humoral and cellular immune responses against human tumor antigens may occur simultaneously. In addition, our analysis provides a general strategy for identifying the CTL-recognizing peptides of tumor antigens initially defined by autologous antibody.

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• Wen, Y.-J., Min, R., Tricot, G., Barlogie, B., Yi, Q. (2002). Tumor lysate-specific cytotoxic T lymphocytes in multiple myeloma: promising effector cells for immunotherapy. Blood 99: 3280-3285 [Abstract] [Full Text]  
• Rubio-Godoy, V., Pinilla, C., Dutoit, V., Borras, E., Simon, R., Zhao, Y., Cerottini, J.-C., Romero, P., Houghten, R., Valmori, D. (2002). Toward Synthetic Combinatorial Peptide Libraries in Positional Scanning Format (PS-SCL)-based Identification of CD8+ Tumor-reactive T-Cell Ligands: A Comparative Analysis of PS-SCL Recognition by a Single Tumor-reactive CD8+ Cytolytic T-Lymphocyte Clone. Cancer Res. 62: 2058-2063 [Abstract] [Full Text]  
• Rosenberg, S. A., Tong-On, P., Li, Y., Riley, J. P., El-Gamil, M., Parkhurst, M. R., Robbins, P. F. (2002). Identification of BING-4 Cancer Antigen Translated From an Alternative Open Reading Frame of a Gene in the Extended MHC Class II Region Using Lymphocytes From a Patient With a Durable Complete Regression Following Immunotherapy. J. Immunol. 168: 2402-2407 [Abstract] [Full Text]  
• Ayyoub, M., Stevanovic, S., Sahin, U., Guillaume, P., Servis, C., Rimoldi, D., Valmori, D., Romero, P., Cerottini, J.-C., Rammensee, H.-G., Pfreundschuh, M., Speiser, D., Levy, F. (2002). Proteasome-Assisted Identification of a SSX-2-Derived Epitope Recognized by Tumor-Reactive CTL Infiltrating Metastatic Melanoma. J. Immunol. 168: 1717-1722 [Abstract] [Full Text]  
• Miconnet, I., Koenig, S., Speiser, D., Krieg, A., Guillaume, P., Cerottini, J.-C., Romero, P. (2002). CpG Are Efficient Adjuvants for Specific CTL Induction Against Tumor Antigen-Derived Peptide. J. Immunol. 168: 1212-1218 [Abstract] [Full Text]  
• Khong, H. T., Rosenberg, S. A. (2002). Pre-Existing Immunity to Tyrosinase-Related Protein (TRP)-2, a New TRP-2 Isoform, and the NY-ESO-1 Melanoma Antigen in a Patient with a Dramatic Response to Immunotherapy. J. Immunol. 168: 951-956 [Abstract] [Full Text]  
• Zarour, H. M., Maillere, B., Brusic, V., Coval, K., Williams, E., Pouvelle-Moratille, S., Castelli, F., Land, S., Bennouna, J., Logan, T., Kirkwood, J. M. (2002). NY-ESO-1 119-143 Is a Promiscuous Major Histocompatibility Complex Class II T-Helper Epitope Recognized by Th1- and Th2-Type Tumor-reactive CD4+ T Cells. Cancer Res. 62: 213-218 [Abstract] [Full Text]  
• Kiniwa, Y., Fujita, T., Akada, M., Ito, K., Shofuda, T., Suzuki, Y., Yamamoto, A., Saida, T., Kawakami, Y. (2001). Tumor Antigens Isolated from a Patient with Vitiligo and T-Cell-infiltrated Melanoma. Cancer Res. 61: 7900-7907 [Abstract] [Full Text]  
• Jager, D, Jager, E, Knuth, A (2001). Immune responses to tumour antigens: implications for antigen specific immunotherapy of cancer. J. Clin. Pathol. 54: 669-674 [Abstract] [Full Text]  
• Rubio-Godoy, V., Dutoit, V., Rimoldi, D., Lienard, D., Lejeune, F., Speiser, D., Guillaume, P., Cerottini, J.-C., Romero, P., Valmori, D. (2001). Discrepancy between ELISPOT IFN-gamma secretion and binding of A2/peptide multimers to TCR reveals interclonal dissociation of CTL effector function from TCR-peptide/MHC complexes half-life. Proc. Natl. Acad. Sci. USA 10.1073/pnas.181348898v1 [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]  
• Abu-Shakra, M, Buskila, D, Ehrenfeld, M, Conrad, K, Shoenfeld, Y (2001). Cancer and autoimmunity: autoimmune and rheumatic features in patients with malignancies. Ann Rheum Dis 60: 433-441 [Abstract] [Full Text]  
• Zeng, G., Wang, X., Robbins, P. F., Rosenberg, S. A., Wang, R.-F. (2001). CD4+ T cell recognition of MHC class II-restricted epitopes from NY-ESO-1 presented by a prevalent HLA DP4 allele: Association with NY-ESO-1 antibody production. Proc. Natl. Acad. Sci. USA 10.1073/pnas.061507398v1 [Abstract] [Full Text]  
• Wen, Y.-J., Barlogie, B., Yi, Q. (2001). Idiotype-specific cytotoxic T lymphocytes in multiple myeloma: evidence for their capacity to lyse autologous primary tumor cells. Blood 97: 1750-1755 [Abstract] [Full Text]  
• Ono, T., Kurashige, T., Harada, N., Noguchi, Y., Saika, T., Niikawa, N., Aoe, M., Nakamura, S., Higashi, T., Hiraki, A., Wada, H., Kumon, H., Old, L. J., Nakayama, E. (2001). Identification of proacrosin binding protein sp32 precursor as a human cancer/testis antigen. Proc. Natl. Acad. Sci. USA 98: 3282-3287 [Abstract] [Full Text]  
• Jäger, D., Stockert, E., Güre, A. O., Scanlan, M. J., Karbach, J., Jäger, E., Knuth, A., Old, L. J., Chen, Y.-T. (2001). Identification of a Tissue-specific Putative Transcription Factor in Breast Tissue by Serological Screening of a Breast Cancer Library. Cancer Res. 61: 2055-2061 [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]  
• Eichmüller, S., Usener, D., Dummer, R., Stein, A., Thiel, D., Schadendorf, D. (2001). Serological detection of cutaneous T-cell lymphoma-associated antigens. Proc. Natl. Acad. Sci. USA 10.1073/pnas.021386498v1 [Abstract] [Full Text]  
• Rimoldi, D., Rubio-Godoy, V., Dutoit, V., Lienard, D., Salvi, S., Guillaume, P., Speiser, D., Stockert, E., Spagnoli, G., Servis, C., Cerottini, J.-C., Lejeune, F., Romero, P., Valmori, D. (2000). Efficient Simultaneous Presentation of NY-ESO-1/LAGE-1 Primary and Nonprimary Open Reading Frame-Derived CTL Epitopes in Melanoma. J. Immunol. 165: 7253-7261 [Abstract] [Full Text]  
• Jäger, E., Gnjatic, S., Nagata, Y., Stockert, E., Jäger, D., Karbach, J., Neumann, A., Rieckenberg, J., Chen, Y.-T., Ritter, G., Hoffman, E., Arand, M., Old, L. J., Knuth, A. (2000). Induction of primary NY-ESO-1 immunity: CD8+ T lymphocyte and antibody responses in peptide-vaccinated patients with NY-ESO-1+ cancers. Proc. Natl. Acad. Sci. USA 10.1073/pnas.220413497v1 [Abstract] [Full Text]  
• Gnjatic, S., Nagata, Y., Jager, E., Stockert, E., Shankara, S., Roberts, B. L., Mazzara, G. P., Lee, S. Y., Dunbar, P. R., Dupont, B., Cerundolo, V., Ritter, G., Chen, Y.-T., Knuth, A., Old, L. J. (2000). Strategy for monitoring T cell responses to NY-ESO-1 in patients with any HLA class I allele. Proc. Natl. Acad. Sci. USA 97: 10917-10922 [Abstract] [Full Text]  
• Pulford, K., Falini, B., Banham, A. H., Codrington, D., Roberton, H., Hatton, C., Mason, D. Y. (2000). Immune response to the ALK oncogenic tyrosine kinase in patients with anaplastic large-cell lymphoma. Blood 96: 1605-1607 [Abstract] [Full Text]  
• Valmori, D., Dutoit, V., Liénard, D., Rimoldi, D., Pittet, M. J., Champagne, P., Ellefsen, K., Sahin, U., Speiser, D., Lejeune, F., Cerottini, J.-C., Romero, P. (2000). Naturally Occurring Human Lymphocyte Antigen-A2 Restricted CD8+ T-Cell Response to the Cancer Testis Antigen NY-ESO-1 in Melanoma Patients. Cancer Res. 60: 4499-4506 [Abstract] [Full Text]  
• Chen, J.-L., Dunbar, P. R., Gileadi, U., Jager, E., Gnjatic, S., Nagata, Y., Stockert, E., Panicali, D. L., Chen, Y.-T., Knuth, A., Old, L. J., Cerundolo, V. (2000). Identification of NY-ESO-1 Peptide Analogues Capable of Improved Stimulation of Tumor-Reactive CTL. J. Immunol. 165: 948-955 [Abstract] [Full Text]  
• Zeng, G., Touloukian, C. E., Wang, X., Restifo, N. P., Rosenberg, S. A., Wang, R.-F. (2000). Identification of CD4+ T Cell Epitopes from NY-ESO-1 Presented by HLA-DR Molecules. J. Immunol. 165: 1153-1159 [Abstract] [Full Text]  
• Jäger, D., Stockert, E., Jäger, E., Güre, A. O., Scanlan, M. J., Knuth, A., Old, L. J., Chen, Y.-T. (2000). Serological Cloning of a Melanocyte rab Guanosine 5'-Triphosphate-binding Protein and a Chromosome Condensation Protein from a Melanoma Complementary DNA Library. Cancer Res. 60: 3584-3591 [Abstract] [Full Text]  
• Valmori, D., Dutoit, V., Lienard, D., Lejeune, F., Speiser, D., Rimoldi, D., Cerundolo, V., Dietrich, P.-Y., Cerottini, J.-C., Romero, P. (2000). Tetramer-Guided Analysis of TCR {beta}-Chain Usage Reveals a Large Repertoire of Melan-A-Specific CD8+ T Cells in Melanoma Patients. J. Immunol. 165: 533-538 [Abstract] [Full Text]  
• Jager, E., Nagata, Y., Gnjatic, S., Wada, H., Stockert, E., Karbach, J., Dunbar, P. R., Lee, S. Y., Jungbluth, A., Jager, D., Arand, M., Ritter, G., Cerundolo, V., Dupont, B., Chen, Y.-T., Old, L. J., Knuth, A. (2000). Monitoring CD8 T cell responses to NY-ESO-1: Correlation of humoral and cellular immune responses. Proc. Natl. Acad. Sci. USA 97: 4760-4765 [Abstract] [Full Text]  
• Stenner-Liewen, F., Luo, G., Sahin, U., Tureci, O., Koslovski, M., Kautz, I., Liewen, H., Pfreundschuh, M. (2000). Definition of Tumor-associated Antigens in Hepatocellular Carcinoma. Cancer Epidemiol. Biomarkers Prev. 9: 285-290 [Abstract] [Full Text]  
• Nakao, M., Shichijo, S., Imaizumi, T., Inoue, Y., Matsunaga, K., Yamada, A., Kikuchi, M., Tsuda, N., Ohta, K., Takamori, S., Yamana, H., Fujita, H., Itoh, K. (2000). Identification of a Gene Coding for a New Squamous Cell Carcinoma Antigen Recognized by the CTL. J. Immunol. 164: 2565-2574 [Abstract] [Full Text]  
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• Wang, F., Bade, E., Kuniyoshi, C., Spears, L., Jeffery, G., Marty, V., Groshen, S., Weber, J. (1999). Phase I Trial of a MART-1 Peptide Vaccine with Incomplete Freund's Adjuvant for Resected High-Risk Melanoma. Clin. Cancer Res. 5: 2756-2765 [Abstract] [Full Text]  
• van Baren, N., Brasseur, F., Godelaine, D., Hames, G., Ferrant, A., Lehmann, F., Andre, M., Ravoet, C., Doyen, C., Spagnoli, G. C., Bakkus, M., Thielemans, K., Boon, T. (1999). Genes Encoding Tumor-Specific Antigens Are Expressed in Human Myeloma Cells. Blood 94: 1156-1164 [Abstract] [Full Text]  
• Fernandez-Madrid, F., VandeVord, P. J., Yang, X., Karvonen, R. L., Simpson, P. M., Kraut, M. J., Granda, J. L., Tomkiel, J. E. (1999). Antinuclear Antibodies as Potential Markers of Lung Cancer. Clin. Cancer Res. 5: 1393-1400 [Abstract] [Full Text]  
• Huang, L.-Q., Brasseur, F., Serrano, A., De Plaen, E., van der Bruggen, P., Boon, T., Van Pel, A. (1999). Cytolytic T Lymphocytes Recognize an Antigen Encoded by MAGE-A10 on a Human Melanoma. J. Immunol. 162: 6849-6854 [Abstract] [Full Text]  

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