Identification of a shared HLA-A*0201-restricted T-cell epitope from the melanoma antigen tyrosinase-related protein 2 (TRP2)

Cancer Research

Volumn 58, Issue 21, 1998, Pages 4895-4901

  Parkhurst, Maria R ^a   Fitzgerald, Ellen B ^a   Southwood, Scott ^b   Sette, Alessandro ^b   Rosenberg, Steven A ^a   Kawakami, Yutaka ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b Epimmune   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MELANOMA ANTIGEN; MONOPHENOL MONOOXYGENASE; TUMOR ANTIGEN; TYROSINASE RELATED PROTEIN 2; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANTIGEN EXPRESSION; ARTICLE; CANCER IMMUNOTHERAPY; CYTOKINE RELEASE; CYTOTOXIC T LYMPHOCYTE; GENE EXPRESSION; GENE FREQUENCY; HUMAN; HUMAN CELL; MELANOCYTE; MELANOMA; MELANOSOME; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; TUMOR REGRESSION;

ANTIGENS, NEOPLASM; EPITOPES, T-LYMPHOCYTE; HLA-A ANTIGENS; HUMANS; INTRAMOLECULAR OXIDOREDUCTASES; MELANOMA; PEPTIDE FRAGMENTS; T-LYMPHOCYTES, CYTOTOXIC; TUMOR CELLS, CULTURED;

EID: 0032212445     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (68)

1. 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., and Seipp, C. A. Use of tumor-infiltrating lymphocytes and interleukin-2 in the immunotherapy of patients with metastatic melanoma. A preliminary report [see comments]. N. Engl. J. Med., 319: 1676-1680, 1988.
2. Rosenberg, S. A., Yannelli, J. R., Yang, J. C., Topalian, S. L., Schwartzentruber, D. J., Weber, J. S., Parkinson, D. R., Seipp, C. A., Einhorn, J. H., and White, D. E. Treatment of patients with metastatic melanoma with autologous tumor-infiltrating lymphocytes and interleukin 2 [see comments]. J. Natl. Cancer Inst., 86: 1159-1166, 1994.
3. Kawakami, Y., and Rosenberg, S. A. Human tumor antigens recognized by T-cells. Immunol. Res., 16: 313-339, 1997.
4. Salazar-Onfray, F., Nakazawa, T., Chhajlani, V., Petersson, M., Karre, K., Masucci, G., Celis, E., Sette, A., Southwood, S., Appella, E., and Kiessling, R. Synthetic peptides derived from the melanocyte-stimulating hormone receptor MC1R can stimulate HLA-A2-restricted cytotoxic T lymphocytes that recognize naturally processed peptides on human melanoma cells. Cancer Res., 57: 4348-4355, 1997.
5. Jager, E., Chen, Y. T., Drijfhout, J. W., Karbach, J., Ringhoffer, M., Jager, D., Arand, M., Wada, H., Noguchi, Y., Stockert, E., Old, L. J., and Knuth, A. Simultaneous humoral and cellular immune response against cancer-testis antigen NY-ESO-1: definition of human histocompatibility leukocyte antigen (HLA)-A2-binding peptide epitopes. J. Exp. Med., 187: 265-270, 1998.
6. Kawakami, Y., Eliyahu, S., Delgado, C. H., Robbins, P. F., Sakaguchi, K., Appella, E., Yannelli, J. R., Adema, G. J., Miki, T., and Rosenberg, S. A. Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. USA, 91: 6458-6462, 1994.
7. Kawakami, Y., Eliyahu, S., Jennings, C., Sakaguchi, K., Kang, X., Southwood, S., Robbins, P. F., Sette, A., Appella, E., and Rosenberg, S. A. Recognition of multiple epitopes in the human melanoma antigen gp100 by tumor-infiltrating T lymphocytes associated with in vivo tumor regression. J. Immunol., 154: 3961-3968, 1995.
8. Jager, E., Ringhoffer, M., Karbach, J., Arand, M., Oesch, F., and Knuth, A. Inverse relationship of melanocyte differentiation antigen expression in melanoma tissues and CD8+ cytotoxic-T-cell responses: evidence for immunoselection of antigen-loss variants in vivo. Int. J. Cancer, 66: 470-476, 1996.
9. Rosenberg, S. A., Yang, J. C., Schwartzentruber, D. J., Hwu, P., Marincola, F. M., Topalian, S. L., Restifo, N. P., Dudley, M. E., Schwarz, S. L., Spiess, P. J., Wunderlich, J. R., Parkhurst, M. R., Kawakami, Y., Seipp, C. A., Einhorn, J. H., and White, D. E. Immunologic and therapeutic evaluation of a synthetic peptide vaccine for the treatment of patients with metastatic melanoma. Nat. Med., 4: 321-327, 1998.
10. Kameyama, K., Sakai, C., Kuge, S., Nishiyama, S., Tomita, Y., Ito, S., Wakamatsu, K., and Hearing, V. J. The expression of tyrosinase, tyrosinase-related proteins 1 and 2 (TRP1 and TRP2), the silver protein, and a melanogenic inhibitor in human melanoma cells of differing melanogenic activities. Pigment Cell Res., 8: 97-104, 1995.
11. Martinez-Esparza, M., Jimenez-Cervantes, C., Garcia-Borron, J. C., Lozano, J. A., del Marmol, V., Ghanem, G., and Solano, F. Comparison of TRPs from murine and human malignant melanocytes. Pigment Cell Res., 10: 229-235, 1997.
12. Bloom, M. B., Perry-Lalley, D., Robbins, P. F., Li, Y., el-Gamil, M., Rosenberg, S. A., and Yang, J. C. Identification of tyrosinase-related protein 2 as a tumor rejection antigen for the B16 melanoma. J. Exp. Med., 185: 453-459, 1997.
13. Wang, R. F., Appella, E., Kawakami, Y., Kang, X., and Rosenberg, S. A. Identification of TRP-2 as a human tumor antigen recognized by cytotoxic T lymphocytes. J. Exp. Med., 184: 2207-2216, 1996.
14. Wang, R. F., Johnston, S. L., Southwood, S., Sette, A., and Rosenberg, S. A. Recognition of an antigenic peptide derived from tyrosinase-related protein-2 by CTL in the context of HLA-A31 and -A33. J. Immunol., 160: 890-897, 1998.
15. Marincola, F. M., Shamamian, P., Rivoltini, L., Salgaller, M., Cormier, J., Restifo, N. P., Simonis, T. B., Venzon, D., White, D. E., and Parkinson, D. R. HLA associations in the antitumor response against malignant melanoma [see comments]. J. Immunother. Emphasis Tumor Immunol., 18: 242-252, 1995.
16. Player, M. A., Barracchini, K. C., Simonis, T. B., Rivoltini, L., Arienti, F., Castelli, C., Mazzocchi, A., Belli, F., Parmiani, G., and Marincola, F. M. Differences in frequency distribution of HLA-A2 subtypes between North American and Italian white melanoma patients: relevance for epitope specific vaccination protocols. J. Immunother. Emphasis Tumor Immunol., 19: 357-363, 1996.
17. Kawakami, Y., Eliyahu, S., Sakaguchi, K., Robbins, P. F., Rivoltini, L., Yannelli, J. R., Appella, E., and Rosenberg, S. A. 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: 347-352, 1994.
18. 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. J. Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines. Science (Washington DC), 264: 716-719, 1994.
19. Bakker, A. B., Schreurs, M. W., Tafazzul, G., de Boer, A. J., Kawakami, Y., Adema, G. J., and Figdor, C. G. 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: 97-102, 1995.
20. Tsai, V., Southwood, S., Sidney, J., Sakaguchi, K., Kawakami, Y., Appella, E., Sette, A., and Celis, E. Identification of subdominant CTL epitopes of the GP100 melanoma-associated tumor antigen by primary in vitro immunization with peptide-pulsed dendritic cells. J. Immunol., 158: 1796-1802, 1997.
21. Wolfel, T., Van Pel, A., Brichard, V., Schneider, J., Seliger, B., Meyer, Z. B. K., and Boon, T. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur. J. Immunol., 24: 759-764, 1994.
22. van der Bruggen, P., Bastin, J., Gajewski, T., Coulie, P. G., Boel, P., De Smet, C., Traversari, C., Townsend, A., and Boon, T. 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: 3038-3043, 1994.
23. Celis, E., Tsai, V., Crimi, C., DeMars, R., Wentworth, P. A., Chesnut, R. W., Grey, H. M., Sette, A., and Serra, H. M. Induction of anti-tumor cytotoxic T lymphocytes in normal humans using primary cultures and synthetic peptide epitopes. Proc. Natl. Acad. Sci. USA, 91: 2105-2109, 1994.
24. Guilloux, Y., Lucas, S., Brichard, V. G., Van Pel, A., Viret, C., De Plaen, E., Brasseur, F., Lethe, B., Jotereau, F., and Boon, T. A peptide recognized by human cytolytic T lymphocytes on HLA-A2 melanomas is encoded by an intron sequence of the N-acetylglucosaminyltransferase V gene. J. Exp. Med., 183: 1173-1183, 1996.
25. Parker, K. C., Bednarek, M. A., Hull, L. K., Utz, U., Cunningham, B., Zweerink, H. J., Biddison, W. E., and Coligan, J. E. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J. Immunol., 149: 3580-3587, 1992.
26. Falk, K., Rotzschke, O., Stevanovic, S., Jung, G., and Rammensee, H. G. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature (Lond.), 351: 290-296, 1991.
27. Kubo, R. T., Sette, A., Grey, H. M., Appella, E., Sakaguchi, K., Zhu, N. Z., Arnott, D., Sherman, N., Shabanowitz, J., and Michel, H. Definition of specific peptide motifs for four major HLA-A alleles. J. Immunol., 152: 3913-3924, 1994.
28. Ruppert, J., Sidney, J., Celis, E., Kubo, R. T., Grey, H. M., and Sette, A. Prominent role of secondary anchor residues in peptide binding to HLA-A2.1 molecules. Cell, 74: 929-937, 1993.
29. Parker, K. C., Shields, M., DiBrino, M., Brooks, A., and Coligan, J. E. Peptide binding to MHC class I molecules: implications for antigenic peptide prediction. Immunol. Res., 14: 34-57, 1995.
30. Rammensee, H. G., Friede, T., and Stevanovic, S. MHC ligands and peptide motifs: first listing, Immunogenetics, 41: 178-228, 1995.
31. Topalian, S. L., Solomon, D., and Rosenberg, S. A. Tumor-specific cytolysis by lymphocytes infiltrating human melanomas. J. Immunol., 142: 3714-3725, 1989.
32. Salter, R. D., Howell, D. N., and Cresswell, P. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenetics, 21: 235-246, 1985.
33. Sette, A., Sidney, J., del Guercio, M. F., Southwood, S., Ruppert, J., Dahlberg, C., Grey, H. M., and Kubo, R. T. Peptide binding to the most frequent HLA-A class I alleles measured by quantitative molecular binding assays. Mol. Immunol., 31: 813-822, 1994.
34. Romani, N., Gruner, S., Brang, D., Kampgen, E., Lenz, A., Trockenbacher, B., Konwalinka, G., Fritsch, P. O., Steinman, R. M., and Schuler, G. Proliferating dendritic cell progenitors in human blood. J. Exp. Med., 180: 83-93, 1994.
35. Parkhurst, M. R., Salgaller, M. L., Southwood, S., Robbins, P. F., Sette, A., Rosenberg, S. A., and Kawakami, Y, Improved induction of melanoma-reactive CTL with peptides from the melanoma antigen gp100 modified at HLA-A *0201-binding residues. J. Immunol., 157: 2539-2548, 1996.
36. Kawakami, Y., Eliyahu, S., Delgado, C. H., Robbins, P. F., Rivoltini, L., Topalian, S. L., Miki, T., and Rosenberg, S. A. 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: 3515-3519, 1994.
37. Kawakami, Y., and Rosenberg, S. A. Immunobiology of human melanoma antigens MART-1 and gp100 and their use for immuno-gene therapy. Int. Rev. Immunol., 14: 173-192, 1997.
38. Kawakami, Y., and Rosenberg, S. A. T-cell recognition of self peptides as tumor rejection antigens. Immunol. Res., 15: 179-190, 1996.
39. Sette, A., Vitiello, A., Reherman, B., Fowler, P., Nayersina, R., Kast, W. M., Melief, C. J., Oseroff, C., Yuan, L., and Ruppert, J. The relationship between class I binding affinity and immunogenicity of potential cytotoxic T cell epitopes. J. Immunol., 153: 5586-5592, 1994.
40. Rivoltini, L., Kawakami, Y., Sakaguchi, K., Southwood, S., Sette, A., Robbins, P. F., Marincola, F. M., Salgaller, M. L., Yannelli, J. R., and Appella, E. 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: 2257-2265, 1995.
41. Salgaller, M. L., Afshar, A., Marincola, F. M., Rivoltini, L., Kawakami, Y., and Rosenberg, S. A. Recognition of multiple epitopes in the human melanoma antigen gp100 by peripheral blood lymphocytes stimulated in vitro with synthetic peptides. Cancer Res., 55: 4972-4979, 1995.
42. Skipper, J. C., Kittlesen, D. J., Hendrickson, R. C., Deacon, D. D., Harthun, N. L., Wagner, S. N., Hunt, D. F., Engelhard, V. H., and Slingluff, C. L. J. Shared epitopes for HLA-A3-restricted melanoma-reactive human CTL include a naturally processed epitope from Pmel-17/gp100. J. Immunol., 157: 5027-5033, 1996.
43. Kang, X., Kawakami, Y., el-Gamil, M., Wang, R., Sakaguchi, K., Yannelli, J. R., Appella, E., Rosenberg, S. A., and Robbins, P. F. Identification of a tyrosinase epitope recognized by HLA-A24-restricted, tumor-infiltrating lymphocytes. J. Immunol., 155: 1343-1348, 1995.
44. Wang, R. F., Parkhurst, M. R., Kawakami, Y., Robbins, P. F., and Rosenberg, S. A. Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen. J. Exp. Med., 183: 1131-1140, 1996.
45. Traversari, C., van der Bruggen, P., Luescher, I. F., Lurquin, C., Chomez, P., Van Pel, A., De Plaen, E., Amar-Costesec, A., and Boon, T. 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: 1453-1457, 1992.
46. van der Bruggen, P., Szikora, J. P., Boel, P., Wildmann, C., Somville, M., Sensi, M., and Boon, T. Autologous cytolytic T lymphocytes recognize a MAGE-1 nonapeptide on melanomas expressing HLA-Cw*1601. Eur. J. Immunol., 24: 2134-2140, 1994.
47. Alexander-Miller, M. A., Leggatt, G. R., and Berzofsky, J. A. Selective expansion of high-or low-avidity cytotoxic T lymphocytes and efficacy for adoptive immunotherapy. Proc. Natl. Acad. Sci. USA, 93: 4102-4107, 1996.
48. Tanaka, F., Fujie, T., Tahara, K., Mori, M., Takesako, K., Sette, A., Celis, E., and Akiyoshi, T. Induction of antitumor cytotoxic T lymphocytes with a MAGE-3-encoded synthetic peptide presented by human leukocytes antigen-A24. Cancer Res., 57: 4465-4468, 1997.
49. Nijman, H. W., Van der Burg, S. H., Vierboom, M. P., Houbiers, J. G., Kast, W. M., and Melief, C. J. p53, a potential target for tumor-directed T cells. Immunol. Lett., 40: 171-178, 1994.
50. Fisk, B., Blevins, T. L., Wharton, J. T., and Ioannides, C. G. Identification of an immunodominant peptide of HER-2/neu protooncogene recognized by ovarian tumor-specific cytotoxic T lymphocyte lines. J. Exp. Med., 181: 2109-2117, 1995.
51. Cerny, A., McHutchison, J. G., Pasquinelli, C., Brown, M. E., Brothers, M. A., Grabscheid, B., Fowler, P., Houghton, M., and Chisari, F. V. Cytotoxic T lymphocyte response to hepatitis C virus-derived peptides containing the HLA A2.1 binding motif. J. Clin. Invest., 95: 521-530, 1995.
52. Chen, Y. T., Scanlan, M. J., Sahin, U., Tureci, O., Gure, A. O., Tsang, S., Williamson, B., Stocken, E., Pfreundschuh, M., and Old, L. J. A testicular antigen aberrantly expressed in human cancers detected by autologous antibody screening. Proc. Natl. Acad. Sci. USA, 94: 1914-1918, 1997.
53. Tureci, O., Sahin, U., Schobert, I., Koslowski, M., Scmitt, H., Schild, H. J., Stenner, F., Seitz, G., Rammensee, H. G., and Pfreundschuh, M. The SSX-2 gene, which is involved in the t(X;18) translocation of synovial sarcomas, codes for the human tumor antigen HOM-MEL-40. Cancer Res., 56: 4766-4772, 1996.
54. Velculescu, V. E., Zhang, L., Vogelstein, B., and Kinzler, K. W. Serial analysis of gene expression [see comments]. Science (Washington DC), 270: 484-487, 1995.
55. Ronde, M., Hummel, R., Pallisgaard, N., Podstufka, T., Riedel, H., Letters, H., and Strauss, M. Identification and cloning of differentially expressed genes by DDRT-PCR. Methods Mol. Biol., 67: 419-430, 1997.
56. Bonaldo, M. F., Lennon, G., and Soares, M. B. Normalization and subtraction: two approaches to facilitate gene discovery. Genome Res., 6: 791-806, 1996.
57. Diatchenko, L., Lau, Y. F., Campbell, A. P., Chenchik, A., Moqadam, F., Huang, B., Lukyanov, S., Lukyanov, K., Gurskaya, N., Sverdlov, E. D., and Siebert, P. D. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proc. Natl. Acad. Sci. USA, 93: 6025-6030, 1996.
58. Schweinfest, C. W., Nelson, P. S., Graber, M. W., Demopoulos, R. I., and Papas, T. S. Subtraction hybridization cDNA libraries. Methods Mol. Biol., 37: 13-30, 1995.
59. Dadaglio, G., Leroux, A., Langlade-Demoyen, P., Bahraoui, E. M., Traincard, F., Fisher, R., and Plata, F. Epitope recognition of conserved HIV envelope sequences by human cytotoxic T lymphocytes. J. Immunol., 147: 2302-2309, 1991.
60. Achour, A., Picard, O., Mbika, J. P., Willer, A., Snart, R., Bizzini, B., Carelli, C., Burny, A., and Zagury, D. Envelope protein and p18(IIIB) peptide recognized by cytotoxic T lymphocytes from humans immunized with human immunodeficiency virus envelope. Vaccine, 11: 609-701, 1993.
61. Achour, A., Lemhammedi, S., Picard, O., M'Bika, J. P., Zagury, J. F., Moukrim, Z., Willer, A., Beix, F., Burny, A., and Zagury, D. Cytotoxic T lymphocytes specific for HIV-1 gp160 antigen and synthetic P18IIIB peptide in an HLA-A11-immunized individual. AIDS Res. Hum. Retroviruses, 10: 19-25, 1994.
62. Shirai, M., Pendleton, C. D., and Berzofsky, J. A. Broad recognition of cytotoxic T cell epitopes from the HIV-1 envelope protein with multiple class I histocompatibility molecules. J. Immunol., 148: 1657-1667, 1992.
63. Bertoni, R., Sidney, J., Fowler, P., Chesnut, R. W., Chisari, F. V., and Sette, A. Human histocompatibility leukocyte antigen-binding supermotifs predict broadly cross-reactive cytotoxic T lymphocyte responses in patients with acute hepatitis. J. Clin. Invest., 100: 503-513, 1997.
64. Apostolopoulos, V., Xing, P. X., and McKenzie, I. F. Murine immune response to cells transfected with human MUCI: immunization with cellular and synthetic antigens. Cancer Res., 54: 5186-5193, 1994.
65. Domenech, N., Henderson, R. A., and Finn, O. J. Identification of an HLA-A11-restricted epitope from the tandem repeat domain of the epithelial tumor antigen mucin. J. Immunol., 155: 4766-4774, 1995.
66. Apostolopoulos, V., Karanikas, V., Haurum, J. S., and McKenzie, I. F. C. Induction of HLA-A2-Restricted CTLs to the mucin 1 human breast cancer antigen. J. Immunol., 159: 5211-5218, 1998.
67. del Guercio, M. F., Sidney, J., Hermanson, G., Perez, C., Grey, H. M., Kubo, R. T., and Sette, A. Binding of a peptide antigen to multiple HLA alleles allows definition of an A2-like supertype. J. Immunol., 154: 685-693, 1995.
68. Parker, K. C., Bednarek, M. A., and Coligan, J. E. Scheme for ranking potential HLA-A2 binding peptides based on independent binding of individual peptide side-chains. J. Immunol., 152: 163-175, 1994.