J. Exp. Med., Volume 187, Number 8, April 20, 1998 1349-1354

BRIEF DEFINITIVE REPORT:
A Survey of the Humoral Immune Response of Cancer Patients to a Panel of Human Tumor Antigens

By Elisabeth Stockert,^* Elke Jäger, Yao-Tseng Chen,^*§ Matthew J. Scanlan,^* Ivan Gout, Julia Karbach, Michael Arand,^¶ Alexander Knuth, and Lloyd J. Old^*

From the ^* Ludwig Institute for Cancer Research, New York Branch at Memorial Sloan-Kettering Cancer Center, New York 10021;  II. Medizinische Klinik, Hämatologie-Onkologie, Krankenhaus Nordwest, 60488 Frankfurt, Germany; the ^§ Cornell University Medical College, New York 10021;  Ludwig Institute for Cancer Research, London Branch at University College London School of Medicine, W1P 8BT London, United Kingdom; and the ^¶ Institut für Toxikologie, Johannes Gutenberg Universität, 55131 Mainz, Germany

Evidence is growing for both humoral and cellular immune recognition of human tumor antigens. Antibodies with specificity for antigens initially recognized by cytotoxic T lymphocytes (CTLs), e.g., MAGE and tyrosinase, have been detected in melanoma patient sera, and CTLs with specificity for NY-ESO-1, a cancer-testis (CT) antigen initially identified by autologous antibody, have recently been identified. To establish a screening system for the humoral response to autoimmunogenic tumor antigens, an enzyme-linked immunosorbent assay (ELISA) was developed using recombinant NY-ESO-1, MAGE-1, MAGE-3, SSX2, Melan-A, and tyrosinase proteins. A survey of sera from 234 cancer patients showed antibodies to NY-ESO-1 in 19 patients, to MAGE-1 in 3, to MAGE-3 in 2, and to SSX2 in 1 patient. No reactivity to these antigens was found in sera from 70 normal individuals. The frequency of NY-ESO-1 antibody was 9.4% in melanoma patients and 12.5% in ovarian cancer patients. Comparison of tumor NY-ESO-1 phenotype and NY-ESO-1 antibody response in 62 stage IV melanoma patients showed that all patients with NY-ESO-1⁺ antibody had NY-ESO-1⁺ tumors, and no patients with NY-ESO-1 tumors had NY-ESO-1 antibody. As the proportion of melanomas expressing NY-ESO-1 is 20-40% and only patients with NY-ESO-1⁺ tumors have antibody, this would suggest that a high percentage of patients with NY-ESO-1⁺ tumors develop an antibody response to NY-ESO-1.

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• Sugita, Y., Wada, H., Fujita, S., Nakata, T., Sato, S., Noguchi, Y., Jungbluth, A. A., Yamaguchi, M., Chen, Y.-T., Stockert, E., Gnjatic, S., Williamson, B., Scanlan, M. J., Ono, T., Sakita, I., Yasui, M., Miyoshi, Y., Tamaki, Y., Matsuura, N., Noguchi, S., Old, L. J., Nakayama, E., Monden, M. (2004). NY-ESO-1 Expression and Immunogenicity in Malignant and Benign Breast Tumors. Cancer Res. 64: 2199-2204 [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]  
• 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]  
• Yamaguchi, H., Tanaka, F., Ohta, M., Inoue, H., Mori, M. (2004). Identification of HLA-A24-Restricted CTL Epitope from Cancer-Testis Antigen, NY-ESO-1, and Induction of a Specific Antitumor Immune Response. Clin. Cancer Res. 10: 890-896 [Abstract] [Full Text]  
• Miklos, D. B., Kim, H. T., Zorn, E., Hochberg, E. P., Guo, L., Mattes-Ritz, A., Viatte, S., Soiffer, R. J., Antin, J. H., Ritz, J. (2004). Antibody response to DBY minor histocompatibility antigen is induced after allogeneic stem cell transplantation and in healthy female donors. Blood 103: 353-359 [Abstract] [Full Text]  
• Yakirevich, E., Sabo, E., Lavie, O., Mazareb, S., Spagnoli, G. C., Resnick, M. B. (2003). Expression of the MAGE-A4 and NY-ESO-1 Cancer-Testis Antigens in Serous Ovarian Neoplasms. Clin. Cancer Res. 9: 6453-6460 [Abstract] [Full Text]  
• Koziol, J. A., Zhang, J.-Y., Casiano, C. A., Peng, X.-X., Shi, F.-D., Feng, A. C., Chan, E. K. L., Tan, E. M. (2003). Recursive Partitioning as an Approach to Selection of Immune Markers for Tumor Diagnosis. Clin. Cancer Res. 9: 5120-5126 [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]  
• Mandic, M., Almunia, C., Vicel, S., Gillet, D., Janjic, B., Coval, K., Maillere, B., Kirkwood, J. M., Zarour, H. M. (2003). The Alternative Open Reading Frame of LAGE-1 Gives Rise to Multiple Promiscuous HLA-DR-restricted Epitopes Recognized by T-helper 1-type Tumor-reactive CD4+ T Cells. Cancer Res. 63: 6506-6515 [Abstract] [Full Text]  
• Odunsi, K., Jungbluth, A. A., Stockert, E., Qian, F., Gnjatic, S., Tammela, J., Intengan, M., Beck, A., Keitz, B., Santiago, D., Williamson, B., Scanlan, M. J., Ritter, G., Chen, Y.-T., Driscoll, D., Sood, A., Lele, S., Old, L. J. (2003). NY-ESO-1 and LAGE-1 Cancer-Testis Antigens Are Potential Targets for Immunotherapy in Epithelial Ovarian Cancer. Cancer Res. 63: 6076-6083 [Abstract] [Full Text]  
• Li, J., Li, W., Liang, S., Cai, D., Kieny, M. P., Jacob, L., Linnenbach, A., Abramczuk, J. W., Bender, H., Sproesser, K., Swoboda, R., Somasundaram, R., Guerry, D., Herlyn, D. (2003). Recombinant CD63/ME491/Neuroglandular/NKI/C-3 Antigen Inhibits Growth of Established Tumors in Transgenic Mice. J. Immunol. 171: 2922-2929 [Abstract] [Full Text]  
• Gnjatic, S., Atanackovic, D., Jager, E., Matsuo, M., Selvakumar, A., Altorki, N. K., Maki, R. G., Dupont, B., Ritter, G., Chen, Y.-T., Knuth, A., Old, L. J. (2003). Survey of naturally occurring CD4+ T cell responses against NY-ESO-1 in cancer patients: Correlation with antibody responses. Proc. Natl. Acad. Sci. USA 100: 8862-8867 [Abstract] [Full Text]  
• Matsui, K., O'Mara, L. A., Allen, P. M. (2003). Successful elimination of large established tumors and avoidance of antigen-loss variants by aggressive adoptive T cell immunotherapy. Int Immunol 15: 797-805 [Abstract] [Full Text]  
• Lee, S.-Y., Obata, Y., Yoshida, M., Stockert, E., Williamson, B., Jungbluth, A. A., Chen, Y.-T., Old, L. J., Scanlan, M. J. (2003). Immunomic analysis of human sarcoma. Proc. Natl. Acad. Sci. USA 100: 2651-2656 [Abstract] [Full Text]  
• Zhang, J.-Y., Casiano, C. A., Peng, X.-X., Koziol, J. A., Chan, E. K. L., Tan, E. M. (2003). Enhancement of Antibody Detection in Cancer Using Panel of Recombinant Tumor-associated Antigens. Cancer Epidemiol. Biomarkers Prev. 12: 136-143 [Abstract] [Full Text]  
• Maio, M., Coral, S., Sigalotti, L., Elisei, R., Romei, C., Rossi, G., Cortini, E., Colizzi, F., Fenzi, G., Altomonte, M., Pinchera, A., Vitale, M. (2003). Analysis of Cancer/Testis Antigens in Sporadic Medullary Thyroid Carcinoma: Expression and Humoral Response to NY-ESO-1. J. Clin. Endocrinol. Metab. 88: 748-754 [Abstract] [Full Text]  
• Gnjatic, S., Atanackovic, D., Matsuo, M., Jager, E., Lee, S. Y., Valmori, D., Chen, Y.-T., Ritter, G., Knuth, A., Old, L. J. (2003). Cross-Presentation of HLA Class I Epitopes from Exogenous NY-ESO-1 Polypeptides by Nonprofessional APCs. J. Immunol. 170: 1191-1196 [Abstract] [Full Text]  
• Slager, E. H., Borghi, M., van der Minne, C. E., Aarnoudse, C. A., Havenga, M. J. E., Schrier, P. I., Osanto, S., Griffioen, M. (2003). CD4+ Th2 Cell Recognition of HLA-DR-Restricted Epitopes Derived from CAMEL: A Tumor Antigen Translated in an Alternative Open Reading Frame. J. Immunol. 170: 1490-1497 [Abstract] [Full Text]  
• Yang, X.-F., Wu, C. J., Chen, L., Alyea, E. P., Canning, C., Kantoff, P., Soiffer, R. J., Dranoff, G., Ritz, J. (2002). CML28 Is a Broadly Immunogenic Antigen, Which Is Overexpressed in Tumor Cells. Cancer Res. 62: 5517-5522 [Abstract] [Full Text]  
• Gnjatic, S., Jager, E., Chen, W., Altorki, N. K., Matsuo, M., Lee, S.-Y., Chen, Q., Nagata, Y., Atanackovic, D., Chen, Y.-T., Ritter, G., Cebon, J., Knuth, A., Old, L. J. (2002). CD8+ T cell responses against a dominant cryptic HLA-A2 epitope after NY-ESO-1 peptide immunization of cancer patients. Proc. Natl. Acad. Sci. USA 99: 11813-11818 [Abstract] [Full Text]  
• Somers, V. A., Brandwijk, R. J., Joosten, B., Moerkerk, P. T., Arends, J.-W., Menheere, P., Pieterse, W. O., Claessen, A., Scheper, R. J., Hoogenboom, H. R., Hufton, S. E. (2002). A Panel of Candidate Tumor Antigens in Colorectal Cancer Revealed by the Serological Selection of a Phage Displayed cDNA Expression Library. J. Immunol. 169: 2772-2780 [Abstract] [Full Text]  
• Krackhardt, A. M., Witzens, M., Harig, S., Hodi, F. S., Zauls, A. J., Chessia, M., Barrett, P., Gribben, J. G. (2002). Identification of tumor-associated antigens in chronic lymphocytic leukemia by SEREX. Blood 100: 2123-2131 [Abstract] [Full Text]  
• Nagata, Y., Ono, S., Matsuo, M., Gnjatic, S., Valmori, D., Ritter, G., Garrett, W., Old, L. J., Mellman, I. (2002). Differential presentation of a soluble exogenous tumor antigen, NY-ESO-1, by distinct human dendritic cell populations. Proc. Natl. Acad. Sci. USA 99: 10629-10634 [Abstract] [Full Text]  
• Scanlan, M. J., Welt, S., Gordon, C. M., Chen, Y.-T., Gure, A. O., Stockert, E., Jungbluth, A. A., Ritter, G., Jager, D., Jager, E., Knuth, A., Old, L. J. (2002). Cancer-related Serological Recognition of Human Colon Cancer: Identification of Potential Diagnostic and Immunotherapeutic Targets. Cancer Res. 62: 4041-4047 [Abstract] [Full Text]  
• Wang, Y., Han, K.-J., Pang, X.-W., Vaughan, H. A., Qu, W., Dong, X.-Y., Peng, J.-R., Zhao, H.-T., Rui, J.-A., Leng, X.-S., Cebon, J., Burgess, A. W., Chen, W.-F. (2002). Large Scale Identification of Human Hepatocellular Carcinoma-Associated Antigens by Autoantibodies. J. Immunol. 169: 1102-1109 [Abstract] [Full Text]  
• Schuler-Thurner, B., Schultz, E. S., Berger, T. G., Weinlich, G., Ebner, S., Woerl, P., Bender, A., Feuerstein, B., Fritsch, P. O., Romani, N., Schuler, G. (2002). Rapid Induction of Tumor-specific Type 1 T Helper Cells in Metastatic Melanoma Patients by Vaccination with Mature, Cryopreserved, Peptide-loaded Monocyte-derived Dendritic Cells. JEM 195: 1279-1288 [Abstract] [Full Text]  
• Valmori, D., Dutoit, V., Schnuriger, V., Quiquerez, A.-L., Pittet, M. J., Guillaume, P., Rubio-Godoy, V., Walker, P. R., Rimoldi, D., Lienard, D., Cerottini, J.-C., Romero, P., Dietrich, P.-Y. (2002). Vaccination with a Melan-A Peptide Selects an Oligoclonal T Cell Population with Increased Functional Avidity and Tumor Reactivity. J. Immunol. 168: 4231-4240 [Abstract] [Full Text]  
• Valmori, D., Scheibenbogen, C., Dutoit, V., Nagorsen, D., Asemissen, A. M., Rubio-Godoy, V., Rimoldi, D., Guillaume, P., Romero, P., Schadendorf, D., Lipp, M., Dietrich, P.-Y., Thiel, E., Cerottini, J.-C., Lienard, D., Keilholz, U. (2002). Circulating Tumor-reactive CD8+ T Cells in Melanoma Patients Contain a CD45RA+CCR7- Effector Subset Exerting ex Vivo Tumor-specific Cytolytic Activity. Cancer Res. 62: 1743-1750 [Abstract] [Full Text]  
• Le Naour, F., Brichory, F., Misek, D. E., Brechot, C., Hanash, S. M., Beretta, L. (2002). A Distinct Repertoire of Autoantibodies in Hepatocellular Carcinoma Identified by Proteomic Analysis. Mol. Cell. Proteomics 1: 197-203 [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]  
• 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]  
• Lu, M., Nakamura, R. M., Dent, E. D., Zhang, J.-Y., Nielsen, F. C., Christiansen, J., Chan, E. K. L., Tan, E. M. (2001). Aberrant Expression of Fetal RNA-Binding Protein p62 in Liver Cancer and Liver Cirrhosis. Am. J. Pathol. 159: 945-953 [Abstract] [Full Text]  
• Brichory, F. M., Misek, D. E., Yim, A.-M., Krause, M. C., Giordano, T. J., Beer, D. G., Hanash, S. M. (2001). An immune response manifested by the common occurrence of annexins I and II autoantibodies and high circulating levels of IL-6 in lung cancer. Proc. Natl. Acad. Sci. USA 98: 9824-9829 [Abstract] [Full Text]  
• Dutoit, V., Rubio-Godoy, V., Dietrich, P.-Y., Quiqueres, A.-L., Schnuriger, V., Rimoldi, D., Lienard, D., Speiser, D., Guillaume, P., Batard, P., Cerottini, J.-C., Romero, P., Valmori, D. (2001). Heterogeneous T-Cell Response to MAGE-A10254-262: High Avidity-specific Cytolytic T Lymphocytes Show Superior Antitumor Activity. Cancer Res. 61: 5850-5856 [Abstract] [Full Text]  
• Yang, X.-F., Wu, C. J., McLaughlin, S., Chillemi, A., Wang, K. S., Canning, C., Alyea, E. P., Kantoff, P., Soiffer, R. J., Dranoff, G., Ritz, J. (2001). CML66, a broadly immunogenic tumor antigen, elicits a humoral immune response associated with remission of chronic myelogenous leukemia. Proc. Natl. Acad. Sci. USA 98: 7492-7497 [Abstract] [Full Text]  
• Kurashige, T., Noguchi, Y., Saika, T., Ono, T., Nagata, Y., Jungbluth, A., Ritter, G., Chen, Y.-T., Stockert, E., Tsushima, T., Kumon, H., Old, L. J., Nakayama, E. (2001). NY-ESO-1 Expression and Immunogenicity Associated with Transitional Cell Carcinoma: Correlation with Tumor Grade. Cancer Res. 61: 4671-4674 [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]  

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