Anti-melanoma cytotoxic T lymphocytes (CTL) recognize numerous antigenic peptides having 'self' sequences: Autoimmune nature of the anti-melanoma CTL response

International Immunology

Volumn 9, Issue 2, 1997, Pages 327-338

  Tsomides, Theodore J ^a   Reilly, Edward B ^b   Eisen, Herman N ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b ABBOTT LABORATORIES   (United States)

Author keywords

HPLC; Immunotherapy; Melanoma; Natural peptides; Tumor infiltrating lymphocytes

Indexed keywords

ARTICLE; AUTOIMMUNITY; CYTOTOXIC T LYMPHOCYTE; FLOW RATE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; IMMUNOTHERAPY; LYSIS; MELANOMA CELL; MOLECULAR RECOGNITION; PRIORITY JOURNAL; T LYMPHOCYTE; TARGET CELL;

ANTIGEN PRESENTATION; ANTIGENS, NEOPLASM; AUTOANTIGENS; AUTOIMMUNITY; CONSENSUS SEQUENCE; CYTOTOXICITY TESTS, IMMUNOLOGIC; CYTOTOXICITY, IMMUNOLOGIC; HUMANS; IMMUNODOMINANT EPITOPES; LYMPHOCYTES, TUMOR-INFILTRATING; MELANOMA; NEOPLASM PROTEINS; PEPTIDES; T-LYMPHOCYTES, CYTOTOXIC; TUMOR CELLS, CULTURED; TUMOR MARKERS, BIOLOGICAL;

EID: 0031051901     PISSN: 09538178     EISSN: None     Source Type: Journal    
DOI: 10.1093/intimm/9.2.327     Document Type: Article

References (75)

1. Wölfel, T., Klehmann, E., Müller, C., Schütt, K.-H., Meyer zum Büschenfelde, K.-H, and Knuth, A. 1989. Lysis of human melanoma cells by autologous cytolytic T cell clones. Identification of human histocompatibility leukocyte antigen A2 as a restriction element for three different antigens. J. Exp. Med. 170:797.
2. Darrow, T. L., Slingluff, C. L., Jr and Seigler, H. F. 1989. The role of HLA class I antigens in recognition of melanoma cells by tumor-specific cytotoxic T lymphocytes. Evidence for shared tumor antigens. J. Immunol. 142:3329.
3. Horn, S. S., Topalian, S. L., Simonis, T., Mancini, M. and Rosenberg, S. A. 1991. Common expression of melanoma tumorassociated antigens recognized by human tumor infiltrating lymphocytes: analysis by human lymphocyte antigen restriction. J. Immunotherapy 10:153.
4. Kawakami, Y, Zakut, R., Topalian, S. L., Stötter, H. and Rosenberg, S. A. 1992. Shared human melanoma antigens. Recognition by tumor-infiltrating lymphocytes in HLA-A2.1-transfected melanomas. J. Immunol. 148:638.
5. Viret, C., Davodeau, F., Guilloux, Y., Bignon, J.-D., Semana, G., Breathnach, R. and Jotereau, F. 1993. Recognition of shared melanoma antigen by HLA-A2-restricted cytolytic T cell clones derived from human tumor-infiltrating lymphocytes. Eur. J. Immunol. 23:141.
6. Townsend, A. and Bodmer, H. 1989. Antigen recognition by class I-restricted T lymphocytes. Annu. Rev. Immunol 7:601.
7. Tsomides, T. J. and Eisen, H. N. 1994. T-cell antigens in cancer (commentary). Proc. Natl Acad. Sci. USA 91:3487.
8. Mukherji, B., Chakraborty, N. G., Yamasaki, S., Okino, T., Yamase, H., Sporn, J. R., Kurtzman, S. K., Ergin, M. T., Ozols, J., Meehan, J. and Mauri, F. 1995. Induction of antigen-specific cytolytic T cells in situ in human melanoma by immunization with synthetic peptide-pulsed autologous antigen presenting cells. Proc. Natl Acad. Sci. USA 92:8078.
9. Marchand, M., Weynants, P., Rankin, E., Arienti, F., Belli, F., Parmiani, G., Cascinelli, N., Bourlond, A., Vanwijck, R., Humblet, Y., Canon, J.-L., Laurent, C., Naeyaert, J.-M., Plagne, R., Deraemaeker, R., Knuth, A., Jäger, E., Brasseur, F., Herman, J., Coulie, P G, and Boon, T. 1995 Tumor regression in melanoma patients treated with a peptide encoded by gene MAGE-3. Int. J. Cancer 63:883.
10. Zhai, Y., Yang, J. C., Kawakami, Y., Spiess, P., Wadsworth, S. C., Cardoza, L. M., Couture, L A., Smith, A. E. and Rosenberg, S. A. 1996. Antigen-specific tumor vaccines. Development and characterization of recombinant adenoviruses encoding MART 1 or gp 100 for cancer therapy. J. Immunol. 156:700.
11. Tsomides, T. J., Aldovini, A., Johnson, R. P., Walker, B. D., Young, R. A. and Eisen, H. N. 1994. Naturally processed viral peptides recognized by cytotoxic T lymphocytes on cells chronically infected by human immunodeficiency virus type 1. J. Exp. Med. 180:1283.
12. Tsomides, T. J. 1996. Role of ligand density in T cell reactions. In Urban, R. G. and Chicz, R. M., eds, MHC Molecules: Expression, Assembly and Function, p. 191. R. G. Landes, Austin, TX.
13. b molecule. Nature 348:213.
14. Rötzschke, O., Falk. K., Deres, K., Schild, H., Norda, M., Metzger, J., Jung, G. and Rammensee, H.-G. 1990. Isolation and analysis of naturally processed viral peptides as recognized by cytotoxic T cells. Nature 348:252.
15. + cytotoxic T lymphocytes in association with a class I MHC protein. Cell 69:989.
16. + T-cell clone. Proc. Natl Acad. Sci. USA 90:11272.
17. Wu, M. X., Tsomides, T. J. and Eisen, H. N. 1995. Tissue distribution of natural peptides derived from a ubiquitous dehydrogenase, including a novel liver-specific peptide that demonstrates the pronounced specificity of low affinity T cell reactions. J Immunol. 154:4495.
18. Kawakami, Y., Eliyahu, S., Delgado, C. H., Robbins, P. F., Rivoltini, L., Topalian, S. L., Miki, T. and Rosenberg, S., A. 1994. Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl Acad. Sci. USA 91:3515.
19. Coulie, P G., Brichard, V., Van Pel, A., Wölfel, T., Schneider, J., Traversari, C., Mattei, S., De Plaen, E., Lurquin, C., Szikora, J.-P., Renauld, J.-C. and Boon, T. 1994. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 180:35.
20. Falk, K., Rötzschke, O., Stevanovic, S., Jung, G. and Rammensee, H.-G. 1991. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 351:290.
21. Topalian, S. L., Muul, L. M., Solomon, D. and Rosenberg, S. A. 1987. Expansion of human tumor infiltrating lymphocytes for use in immunotherapy trials. J. Immunol. Methods 102:127-141
22. Reilly, E. B. and Antognetti, G. 1991. Increased tumor-specific CTL activity in human tumor-infiltrating lymphocytes stimulated with autologous tumor lines. Cell. Immunol. 135:526.
23. Brichard, V., Van Pel, A., Wölfel, T., Wölfel, C., De Plaen, E., Lethé, B., Coulie, P. and Boon, T. 1993. The tyrosinase gene codes for an antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 178:489.
24. 2m gene expression. J. Clin. Invest. 87:284.
25. Kawakami, Y., Eliyahu, S., Sakaguchi, K., Robbins, P. F., Rivoltini, L., Yannelli, J. R., Appella, E. and Rosenberg, S. A. 1994. Identification of the immunodominant peptides of the MART-1 human melanoma antigen recognized by the majority of HLA-A2-restricted tumor infiltrating lymphocytes. J. Exp. Med. 180:347.
26. Kageyama, S., Tsomides, T. J., Sykulev, Y. and Eisen, H. N. 1995. Variations in the number of peptide-MHC class I complexes required to activate cytotoxic T cell responses. J. Immunol. 154:567.
27. + T cells binds very tightly to the restricting class I major histocompatibility complex protein on intact cells but not to the purified class I protein. Proc. Natl Acad. Sci. USA 88:11276.
28. Tsomides, T. J. and Eisen, H. N. 1993. Identification of naturally occurring peptides associated with MHC molecules. Chem. Immunol. 57:166.
29. Bodmer, H., Ogg, G., Gotch, F. and McMichael, A. 1989. AntiHLA-A2 antibody-enhancement of peptide association with HLA-A2 as detected by cytotoxic T lymphocytes. Nature 342:443.
30. Wölfel, T., Van Pel, A., Brichard, V., Schneider, J., Seliger, B., Meyer zum Büschenfelde, K.-H. and Boon, T. 1994. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur. J. Immunol. 24:759.
31. + cytotoxic T lymphocytes. J. Exp Med. 181:363.
32. Weidmann, E., Elder, E. M., Trucco, M., Lotze, M. T. and Whiteside, T. L. 1993. Usage of T-cell receptor Vβ chain genes in fresh and cultured tumor-infiltrating lymphocytes from human melanoma, Int. J. Cancer 54:383.
33. Shilyansky, J., Nishimura, M. I., Yannelli, J. R., Kawakami, Y., Jacknin, L. S., Charmley, P. and Rosenberg, S. A. 1994. T-cell receptor usage by melanoma-specific clonal and highly oligoclonal tumor-infiltrating lymphocyte lines. Proc. Natl Acad. Sci. USA 91:2829.
34. Puisieux, I., Even, J., Pannetier, C., Jotereau, F., Favrot, M. and Kourilsky, P. 1994. Oligoclonality of tumor-infiltrating lymphocytes from human melanomas. J. Immunol. 153:2807.
35. Sensi, M. and Parmiani, G. 1995. Analysis of TCR usage in human tumors: a new tool for assessing tumor-specific immune responses, Immunol. Today 16:588.
36. Slingluff, C. L., Jr, Cox, A. L., Henderson, R. A., Hunt, D. F. and Engelhard, V. H. 1993. Recognition of human melanoma cells by HLA-A2.1-restricted cytotoxic T lymphocytes is mediated by at least six shared peptide epitopes. J. Immunol. 150:2955.
37. Storkus, W. J., Zeh, H. J., III, Maeurer, M. J., Salter, R. D. and Lotze, M. T. 1993. Identification of human melanoma peptides recognized by class I restricted tumor infiltrating T lymphocytes. J. Immunol. 151:3719.
38. Wölfel, T., Schneider, J., Meyer Zum Büschenfelde, K.-H., Rammensee, H.-G., Rötzschke, O. and Falk, K. 1994. Isolation of naturally processed peptides recognized by cytolytic T lymphocytes (CTL) on human melanoma cells in association with HLA-A2.1. Int. J. Cancer 57:413.
39. Falk, K., Rötzschke, O., Deres, K., Metzger, J., Jung, G. and Rammensee, H.-G. 1991. Identification of naturally processed viral nonapeptides allows their quantification in infected cells and suggests an allele-specific T cell epitope forecast. J. Exp. Med. 174:425.
40. Cox, A L., Skipper, J., Chen, Y., Henderson, R. A., Darrow, T. L., Shabanowitz, J., Engelhard, V. H., Hunt, D. F. and Slingluff, C., L., Jr. 1994. Identification of a peptide recognized by five melanomaspecific human cytotoxic T cell lines. Science 264:716.
41. Wallny, H.-J., Deres, K., Faath, S., Jung, G., Van Pel, A., Boon, T. and Rammensee, H.-G. 1992. Identification and quantification of a naturally presented peptide as recognized by cytotoxic T lymphocytes specific for an immunogenic tumor variant, Int. Immunol. 4;1085.
42. Kawakami, Y., Eliyahu, S., Jennings, C., Sakaguchi, K., Kang, X., Southwood, S., Robbins, P. F., Sette, A., Appella, E. and Rosenberg, S. A. 1995. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol. 154:3961.
43. b cytotoxic T lymphocytes. J. Exp. Med. 168:559.
44. Reddehase, M. J., Rothbard, J. B. and Koszinowski, U. H. 1989. A pentapeptide as minimal antigenic determinant for MHC class I-restricted T lymphocytes. Nature 337:651.
45. Mandelboim, O., Berke, G., Fridkin, M., Feldman, M., Eisenstein, M. and Eisenbach, L. 1994. CTL induction by a tumour-associated antigen octapeptide derived from a murine lung carcinoma. Nature 369:67.
46. Coggin, J. H., Jr, Adkinson, L. and Anderson, N. G. 1980. Fetal antigens shared as transplantation rejection antigens on chemically induced mouse and hamster sarcomas. Cancer Res. 40:1568.
47. Parmiani, G. 1993. Tumor immunity as autoimmunity: tumor antigens include normal self proteins which stimulate anergic peripheral T cells, Immunol. Today 14:536.
48. Houghton, A. N. 1994. Cancer antigens: immune recognition of self and altered self. J. Exp. Med. 180:1.
49. André, I., Gonzalez, A., Wang, B., Katz, J., Benoist, C. and Mathis, D. 1996. Checkpoints in the progression of autoimmune disease: lessons from diabetes models. Proc. Natl Acad. Sci. USA 93:2260.
50. Zamvil, S. S and Steinman, L. 1990. The T lymphocyte in experimental allergic encephalomyelitis. Annu. Rev Immunol. 8:579.
51. Ohashi, P. S., Oehen, S., Buerki, K., Pircher, H., Ohashi, C. T., Odermatt, B., Malissen, B., Zinkernagel, R. M. and Hengartner, H. 1991. Ablation of 'tolerance' and induction of diabetes by virus infection in viral antigen transgenic mice. Cell 65:305.
52. Rivoltini, L., Kawakami, Y., Sakaguchi, K., Southwood, S., Sette, A., Robbins, P. F., Marincola, F. M., Salgaller, M. L., Yannelli, J. R., Appella, E. and Rosenberg, S.A. 1995. Induction of tumor-reactive CTL from peripheral blood and tumor-infiltrating lymphocytes of melanoma patients by in vitro stimulation with an immunodominant peptide of the human melanoma antigen MART-1. J. Immunol. 154:2257.
53. Visseren, M. J. W., van Elsas, A., van der voort, E. I. H., Ressing, M. E., Kast, W. M., Schrier, P. I. and Melief, C. J. M. 1995. CTL specific for the tyrosinase autoantigen can be induced from healthy donor blood to lyse melanoma cells. J. Immunol 154:3991.
54. Rosenberg, S. A., Packard, B. S., Aebersold, P. M., Solomon, D., Topalian, S. L., Toy, S. T., Simon, P., Lotze, M. T., Yang, J. C., Seipp, C. A., Simpson, C., Carter, C., Bock, S., Schwartzentruber, D., Wei, J. P. and White, D. E. 1988. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report. New Engl. J. Med. 319:1676.
55. Anichini, A., Maccalli, C., Mortarini, R., Salvi, S., Mazzocchi, A., Squarcina, P., Herlyn, M. and Parmiani, G. 1993. Melanoma cells and normal melanocytes share antigens recognized by HLA-A2-restricted cytotoxic T cell clones from melanoma patients. J. Exp. Med. 177:989.
56. Bakker, A. B. H., Schreurs, M. W. J., de Boer, A. J., Kawakami, Y., Rosenberg, S. A., Adema, G. J. and Figdor, C. G. 1994. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J. Exp. Med. 179:1005.
57. Mukherji, B. and Chakraborty, N. G. 1995. Immunobiology and immunotherapy of melanoma. Curr. Opin. Oncol. 7:175.
58. Boon, T., Cerottini, J.-C., Van den Eynde, B., van der Bruggen, P. and Van Pel, A. 1994. Tumor antigens recognized by T lymphocytes. Annu. Rev. Immunol. 12:337.
59. van der Bruggen, P., Traversai, C., Chomez, P., Lurquin, C., De Plaen, E., Van den Eynde, B., Knuth, A. and Boon, T. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science 254:1643.
60. Traversari, C., van der Bruggen, P., Luescher, I. R., Lurquin, C., Chomez, P., Van Pel, A., De Plaen, E., Amar-Costesec, A. and Boon, T. 1992. A nonapeptide encoded by human gene MAGE-1 is recognized on HLA-A1 by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J. Exp. Med. 176:1453.
61. De Smet, C., Lurquin, C., van der Bruggen, P., De Plaen, E., Brasseur, F. and Boon, T. 1994. Sequence and expression pattern of the human MAGE2 gene. Immunogenetics 39:121.
62. Gaugler, B., Van den Eynde, B., van der Bruggen, P., Romero, P., Gaforio, J. J., De Plaen, E., Lethé, B., Brasseur, F. and Boon, T. 1994. Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes. J. Exp. Med. 179:921.
63. van der Bruggen, P., Bastin, J., Gajewski, T., Coulie, P. G., Boël, P., De Smet, C., Traversari, C., Townsend, A. and Boon, T. 1994. A peptide encoded by human gene MAGE-3 and presented by HLA-A2 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE-3. Eur. J. Immunol. 24:3038.
64. Kawakami, Y., Eliyahu, S., Delgado, C., H., Bobbins, P. F., Sakaguchi, K., Appella, E., Yannelli, J. R., Adema, G. J., Miki, T. and Rosenberg, S. A. 1994. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl Acad. Sci. USA 91:6458.
65. Bakker, A. B. H., Schreurs, M. W. J., Tafazzul, G., de Boer, A. J., Kawakami, Y., Adema, G. J. and Figdor, C. G. 1995. Identification of a novel peptide derived from the melanocyte-specific gp100 antigen as the dominant epitope recognized by an HLA-A2.1-restricted anti-melanoma CTL line. Int. J. Cancer 62:97.
66. Salgaller, M. L., Afshar, A., Marincola, F. M., Rivoltini, L., Kawakami, Y. and Rosenberg, S. A. 1995. Recognition of multiple epitopes in the human melanoma antigen gp100 by peripheral blood lymphocytes stimulated in vitro with synthetic peptides. Cancer Res. 55:4972.
67. INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269:1281.
68. Robbins, P. F., El-Gamil, M., Li, Y F., Topalian, S. L., Rivoltini, L., Sakaguchi, K., Appella, E., Kawakami, Y. and Rosenberg, S. A. 1995. Cloning of a new gene encoding an antigen recognized by melanoma-specific HLA-A24-restricted tumor-infiltrating lymphocytes. J. Immunol. 154:5944.
69. Kang, X., Kawakami, Y., El-Gamil, M., Wang, R., Sakaguchi, K. Yannelli, J. R., Appella, E., Rosenberg, S. A. and Robbins, P. F 1995. Identification of a tyrosinase epitope recognized by HLA-A24-restricted, tumor-infiltrating lymphocytes. J. Immunol. 155:1343.
70. Van den Eynde, B. and Brichard, V. G. 1995. New tumor antigens recognized by T cells. Curr. Opin. Immunol. 7:674.
71. Coulie, P. G., Lehmann, F., Lethé, B., Herman, J., Lurquin, C., Andrawiss, M. and Boon, T. 1995. A mutated intron sequence codes for an antigenic peptide recognized by cytolytic T lymphocytes on a human melanoma. Proc. Natl Acad. Sci. USA 92:7976.
72. Van den Eynde, B., Peeters, O., De Backer, O., Gaugler, B., Lucas, S. and Boon, T. 1995. A new family of genes coding for an antigen recognized by autologous cytolytic T lymphocytes on a human melanoma. J. Exp. Med. 182:689.
73. van der Bruggen, P., Szikora, J.-P., Boël, P., Wildmann, C., Somville, M., Sensi, M. and Boon, T. 1994. Autologous cytolytic T lymphocytes recognize a MAGE-1 nonapeptide on melanomas expressing HLA-Cw* 1601. Eur J. Immunol. 24:2134.
74. Boël, P., Wildmann, C., Sensi, M. L., Brasseur, R., Renauld, J.-C., Coulie, P., Boon, T. and van der Bruggen, P. 1995. BAGE: a new gene encoding an antigen recognized on human melanomas by cytolytic T lymphocytes. Immunity 2:167.
75. Skipper, J. C. A., Hendrickson, R. C., Gulden, P. H., Brichard, V., Van Pel, A., Chen, Y., Shabanowitz, J., Wölfel, T., Slingluff, C. L., Boon, T., Hunt, D. F. and Engelhard, V. H. 1996. An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins. J. Exp. Med. 183:527.