Characterization of an antigen that is recognized on a melanoma showing partial HLA loss by CTL expressing an NK inhibitory receptor

Immunity

Volumn 6, Issue 2, 1997, Pages 199-208

  Ikeda, Hideyuki ^a   Lethé, Bernard ^a   Lehmann, Frédéric ^a   Van Baren, Nicolas ^a   Baurain, Jean François ^a   De Smet, Charles ^a   Chambost, Hervé ^b   Vitale, Massimo ^c   Moretta, Alessandro ^d   Boon, Thierry ^a   Coulie, Pierre G ^a  

^a UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^b INSTITUT PAOLI CALMETTES   (France)

^c CENTRO DI BIOTECNOLOGIE AVANZATE   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

HLA A ANTIGEN; TUMOR ANTIGEN;

ARTICLE; CELL LINE; CYTOTOXIC T LYMPHOCYTE; DNA SEQUENCE; HLA SYSTEM; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX RESTRICTION; MELANOMA; PRIORITY JOURNAL;

EID: 0030962059     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1074-7613(00)80426-4     Document Type: Article

References (60)

1. Atherton, E., Logan, C.J., and Sheppard, R.C. (1981). Peptide synthesis. II. Procedures for solid-phase synthesis using Nα-fluorenylmethysoxycarbamylamino acid on polymide supports: synthesis of substance P and of acyl carrier protein 65-74 decapeptide. J. Chem. Soc. Lond. Perkin Trans. 1, 538-546.
2. Biassoni, R., Falco, M., Cambiaggi, A., Costa, P., Verdiani, S., Pende, D., Conte, R., Di Donato, C., Parham, P., and Moretta, L. (1995). Amino acid substitutions can influence the natural killer (NK)-mediated recognition of HLA-C molecules: role of serine-77 and lysine-80 in the target cell protection from lysis mediated by "group 2" or "group 1" NK clones. J. Exp. Med. 182, 605-609.
3. 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, 167-175.
4. Bottino, C., Sivori, S., Vitale, M., Cantoni, C., Falco, M., Pende, D., Morelli, L., Augugliaro, R., Semenzato, G., Biassoni, R., Moretta, L., and Moretta, A. (1996). A novel surface molecule homologous to the p58/p50 family of receptors is selectively expressed on a subset of human natural killer cells and induces both triggering of cell functions and proliferation. Eur. J. Immunol., in press.
5. Brändle, D., Brasseur, F., Weynants, P., Boon, T., and Van den Eynde, B. (1996). A mutated HLA-A2 molecule recognized by autologous cytotoxic T lymphocytes on a human renal cell carcinoma. J. Exp. Med. 183, 2501-2508.
6. 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, 489-495.
7. Brichard, V.G., Herman, J., Van Pel, A., Wildmann, C., Gaugler, B., Wölfel, T., Boon, T., and Lethé, B. (1996). A tyrosinase nonapeptide presented by HLA-B44 is recognized on a human melanoma by autologous cytolytic T lymphocytes. Eur. J. Immunol. 26, 224-230.
8. Castelli, C., Storkus, W.J., Maeurer, M.J., Martin, D.M., Huang, E.C., Pramanik, B.N., Nagabhushan, T.L., Parmiani, G., and Lotze, M.T. (1995). Mass spectrometric identification of a naturally processed melanoma peptide recognized by CD8+ cytotoxic T lymphocytes. J. Exp. Med. 181, 363-368.
9. Chambost, H., Brasseur, F., Coulie, P., De Plaen, E., Stoppa, A.M., Baume, D., Mannoni, P., Boon, T., Maraninchi, D., and Olive, D. (1993). A tumour-associated antigen expression in human haematological malignancies. Br. J. Haematol. 84, 524-526.
10. Chomez, P., Williams, R., De Backer, O., Boon, T., and Vennström, B. (1995). The SMAGE gene family is expressed in post-meiotic spermatids during mouse germ cell differentiation. Immunogenetics 43, 97-100.
11. Colonna, M. (1996). Natural killer cell receptors specific for MHC class I molecules. Curr. Opin. Immunol. 8, 101-107.
12. Colonna, M., and Samaridis, J. (1995). Cloning of immunoglobulin-superfamily members associated with HLA-C and HLA-B: recognition by human natural killer cells. Science 268, 405-408.
13. Colonna, M., Brooks, E.G., Falco, M., Ferrara, G.B., and Strominger, J.L. (1993). Generation of allospecific natural killer cells by stimulation across a polymorphism of HLA-C. Science 260, 1121-1124.
14. Coulie, P.G., Somville, M., Lehmann, F., Hainaut, P., Brasseur, F., Devos, R., and Boon, T. (1992). Precursor frequency analysis of human cytolytic T lymphocytes directed against autologous melanoma cells. Int. J. Cancer 50, 289-297.
15. 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, 35-42.
16. 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, 7976-7980.
17. 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 melanoma-specific human cytotoxic T cell lines. Science 264, 716-719.
18. D'Andrea, A., Chang, C., Franz-Bacon, K., McClanahan, T., Phillips, J.H., and Lanier, L.L. (1995). Molecular cloning of NKB1: a natural killer cell receptor for HLA-B allotypes. J. Immunol. 155, 2306-2310.
19. De Smet, C., De Backer, O., Faraoni, I., Lurquin, C., Brasseur, F., and Boon, T. (1996). The activation of human gene MAGE-1 in tumor cells is correlated with genome-wide demethylation. Proc. Natl. Acad. Sci. USA 93, 7149-7153.
20. Espevik, T., and Nissen-Meyer, J. (1986). A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J. Immunol. Meth. 95, 99-105.
21. Falk, C.S., Steinle, A., and Schendel, D.J. (1995). Expression of HLA-C molecules confers target cell resistance to some non-major histocompatibility complex-restricted T cells in a manner analogous to allospecific natural killer cells. J. Exp. Med. 182, 1005-1018.
22. Garrido, F., Cabrera, T., Lopez-Nevot, M.A., and Ruiz-Cabello, F. (1995). HLA class I antigens in human tumors. Adv. Cancer Res. 67, 155-195.
23. 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, 921-930.
24. Herman, J., van der Bruggen, P., Luescher, I., Mandruzzato, S., Romero, P., Thonnard, J., Fleischhauer, K., Boon, T., and Coulie, P.G. (1996). A peptide encoded by human gene MAGE-3 and presented by HLA-B44 induces cytolytic T lymphocytes that recognize tumor cells expressing MAGE-3. Immunogenetics 43, 377-383.
25. 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, 1343-1348.
26. Kawakami, Y., Eliyahu, S., Delgado, C.H., Robbins, P.F., Rivoltini, L., Topalian, S.L., Miki, T., and Rosenberg, S.A. (1994a). Cloning of the gene coding for a shared human melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl. Acad. Sci. USA 97, 3515-3519.
27. 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. (1994b). Identification of a human melanoma antigen recognized by tumor-infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. USA 97, 6458-6462.
28. 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, 3961-3968.
29. Kubo, R.T., Sette, A., Grey, H.M., Appella, E., Sakaguchi, K., Zhu, N.-Z., Arnott, D., Sherman, N., Shabanowitz, J., Michel, H., Bodnar, W.M., Davis, T.A., and Hunt, D.F. (1994). Definition of specific peptide motifs for four major HLA-Aalleles. J. Immunol. 152, 3913-3924.
30. Lehmann, F., Marchand, M., Hainaut, P., Pouillart, P., Sastre, X., Ikeda, H., Boon, T., and Coulie, P.G. (1995). Differences in the antigens recognized by cytolytic T cells on two successive metastases of a melanoma patient are consistent with immune selection. Eur. J. Immunol. 25, 340-347.
31. Lemonnier, F.A., Rebai, N., Le Bouteiller, P.P., Malissen, B., Caillol, D.H., and Kourilsky, F.M. (1982). Epitopic analysis of detergent-solubilized HLA molecules by solid-phase radioimmunoassay. J. Immunol. Meth. 54, 9-22.
32. Ljunggren, H.-G., and Karre, K. (1985). Host resistance directed selectively against H-2 deficient lymphoma variants. J. Exp. Med. 162, 1745-1759.
33. Maier, R., Falk, K., Rötzschke, O., Maier, B., Gnau, V., Stevanovic, S., Jung, G., Rammensee, H.-G., and Meyerhans, A. (1994). Peptide motifs of HLA-A3, -A24, and -B7 molecules as determined by pool sequencing. Immunogenetics 40, 306-308.
34. Mingari, M.C., Vitale, C., Cambiaggi, A., Schiavetti, F., Melioli, G., Ferrini, S., and Poggi, A. (1995). Cytolytic T lymphocytes displaying natural killer (NK)-like activity: expression of NK-related functional receptors for HLA class I molecules (p58 and CD94) and inhibitory effect on the TCR-mediated target cell lysis or lymphokine production. Int. Immunol. 7, 697-703.
35. Mingari, M.C., Schiavetti, F., Ponte, M., Vitale, C., Maggi, E., Romagnani, S., Demarest, J., Pantaleo, G., Fauci, A.S., and Moretta, L. (1996). Human CD8+ T lymphocyte subsets that express HLA class I-specific inhibitory receptors represent oligoclonally or monoclonally expanded cell populations. Proc. Natl. Acad. Sci. USA 93, in press.
36. Mizushima, S., and Nagata, S. (1990). pEF-BOS, a powerful mammalian expression vector. Nucl. Acids Res. 18, 5322.
37. + natural killer cells: role in cell activation and regulation of cytolytic function. J. Exp. Med. 171, 695-714.
38. + natural killer (NK) cells by the expression of clonally distributed functional surface molecules: correlation between subset assignment of NK clones and ability to mediate specific alloantigen recognition. J. Exp. Med. 172, 1589-1598.
39. Moretta, A., Vitale, M., Bottino, C., Orengo, A.M., Morelli, L., Augugliaro, R., Barbaresi, M., Ciccone, E., and Moretta, L. (1993). P58 molecules as putative receptors for major histocompatibility complex (MHC) class I molecules in human natural killer (NK) cells: anti-P58 antibodies reconstitute lysis of MHC class I-protected cells in NK clones displaying different specificities. J. Exp. Med. 178, 597-604.
40. Moretta, A., Bottino, C., Vitale, M., Pende, D., Biassoni, R., Mingari, M.C., and Moretta, L. (1996). Receptors for HLA class-I molecules in human natural killer cells. Annu. Rev. Immunol. 14, 619-648.
41. Moretta, L., Ciccone, E., Moretta, A., Höglund, P., Öhlén, C., and Kärre, K. (1992). Allorecognition by NK cells: nonself or no self? Immunol. Today 13, 300-305.
42. Murakawa, K., Matsubara, K., Fukushima, A., Yoshii, J., and Okubo, K. (1994). Chromosomal assignments of 3'-directed partial cDNA sequences representing novel genes expressed in granulocytoid cells. Genomics 23, 379-389.
43. Pawlak, A., Toussaint, C., Lévy, I., Bulle, F., Poyard, M., Barouki, R., and Guellaën, G. (1995). Characterization of a large population of mRNAs from human testis. Genomics 26, 151-158.
44. Phillips, J.H., Gumperz, J.E., Parham, P., and Lanier, L.L. (1995). Superantigen-dependent, cell-mediated cytotoxicity inhibited by MHC class I receptors on T lymphocytes. Science 268, 403-405.
45. Rebai, N., and Malissen, B. (1983). Structural and genetic analyses of HLA class I molecules using monoclonal xenoantibodies. Tissue Antigens 22, 107.
46. Robbins, P.F., El-Gamil, M., Li, Y.F., Kawakami, Y., Loftus, D., Appella, E., and Rosenberg, S.A. (1996). A mutated β-catenin gene encodes a melanoma-specific antigen recognized by tumor infiltrating lymphocytes. J. Exp. Med. 183, 1185-1192.
47. Seed, B., and Aruffo, A. (1987). Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc. Natl. Acad. Sci. USA 84, 3365-3369.
48. Shichijo, S., Sagawa, K., Brasseur, F., Boon, T., and Itoh, K. (1996). MAGE-1 gene is expressed in T-cell leukemia. Int. J. Cancer 65, 709-710.
49. Smith, M.E.F., Bodmer, S.G., Kelly, A.P., Trowsdale, J., Kirkland, S.C., and Bodmer, W.F. (1989). Variation in HLA expression on tumors: an escape from immune response. Cold Spring Harbor Symp. Quant. Biol. 54, 581-586.
50. Takahashi, K., Shichijo, S., Noguchi, M., Hirohata, M., and Itoh, K. (1995). Identification of MAGE-1 and MAGE-4 proteins in spermatogonia and primary spermatocytes of testis. Cancer Res. 55, 3478-3482.
51. 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. (1992a). 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.
52. Traversari, C., van der Bruggen, P., Van den Eynde, B., Hainaut, P., Lemoine, C., Ohta, N., Old, L., and Boon, T. (1992b). Transfection and expression of a gene coding for a human melanoma antigen recognized by autologous cytolyticT lymphocytes. Immunogenetics 35, 145-152.
53. 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, 689-698.
54. van der Bruggen, P., Traversari, 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, 1643-1647.
55. van der Bruggen, P., Bastin, J., Gajewski, T., Coulie, P.G., Boël, P., De Smet, C., Traversari, C., Townsend, A., and Boon, T. (1994a). 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.
56. van der Bruggen, P., Szikora, J.-P., Boël, P., Wildmann, C., Somville, M., Sensi, M., and Boon, T. (1994b). Autologous cytolytic T lymphocytes recognize a MAGE-1 nonapeptide on melanomas expressing HLA-Cw*1601. Eur. J. Immunol. 24, 2134-2140.
57. Wagtmann, N., Biassoni, R., Cantoni, C., Verdiani, S., Malnati, M.S., Vitale, M., Bottino, C., Moretta, L, Moretta, A., and Long, E.O. (1995). Molecular clones of the p58 NK cell receptor reveal immunoglobin-related molecules with diversity in both the extra-and intracellular domains. Immunity 2, 439-449.
58. Wang, R.-F., Parkhurst, M.R., Kawakami, Y., Robbins, P.F., and Rosenberg, S.A. (1996). Utilization of an alternative open reading frame of a normal gene in generating a novel human cancer antigen. J. Exp. Med. 183, 1131-1140.
59. 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, 759-764.
60. INK4a-insensitive CDK4 mutant targeted by cytolytic T lymphocytes in a human melanoma. Science 269, 1281-1284.