An HLA-A2-restricted tyrosinase antigen on melanoma cells results from posttranslational modification and suggests a novel pathway for processing of membrane proteins

Journal of Experimental Medicine

Volumn 183, Issue 2, 1996, Pages 527-534

  Skipper, Jonathan C A ^a   Hendrickson, Ronald C ^a   Gulden, Pamela H ^a   Brichard, Vincent ^c   Van Pel, Ailene ^c   Chen, Ye ^a   Shabanowitz, Jeffrey ^a   Wolfel, Thomas ^d   Slingluff Jr , Craig L ^a   Boon, Thierry ^c   Hunt, Donald F ^b   Engelhard, Victor H ^a  

^a UNIVERSITY OF VIRGINIA   (United States)

^b UNIVERSITY OF VIRGINIA   (United States)

^c UNIVERSITÉ CATHOLIQUE DE LOUVAIN   (Belgium)

^d JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

HLA A2 ANTIGEN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 1; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MEMBRANE PROTEIN; MONOPHENOL MONOOXYGENASE;

ANTIGEN DETECTION; ANTIGEN RECOGNITION; ARTICLE; ENDOPLASMIC RETICULUM; HLA SYSTEM; HUMAN; HUMAN CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MELANOMA CELL; MOLECULAR CLONING; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN MODIFICATION; PROTEIN PROCESSING;

AMINO ACID SEQUENCE; ANTIGENS, NEOPLASM; ASPARAGINE; ASPARTIC ACID; CLONE CELLS; EPITOPES; HLA-A2 ANTIGEN; HUMANS; MELANOMA; MEMBRANE PROTEINS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MONOPHENOL MONOOXYGENASE; PEPTIDE FRAGMENTS; PROTEIN PROCESSING, POST-TRANSLATIONAL; TUMOR CELLS, CULTURED;

EID: 0001433072     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.183.2.527     Document Type: Article

References (48)

1. Townsend, A., and H. Bodiner. 1989. Antigen recognition by class I-restricted T lymphocytes. Annu Rev. Immunol. 7: 601-624.
2. Morrison, L.A., A.E. Lukacher, V.L. Braciale, O.P. Fan, and T.J. Braciale. 1986. Differences in antigen presentation to MHC class I- and class II-restricted influenza virus specific cytolytic T lymphocyte clones. J. Exp. Med. 163:903-921.
3. Moore, M.W., F.R. Carbone, and M.J. Bevan. 1988. Introduction of soluble protein into the class I pathway of antigen processing and presentation. Cell 54:777-785.
4. van der Bruggen, P., C. Traversari, P. Chomez, C. Lurquin, E. De Plaen, B. Van den Eynde, A. Knuth, and T. Boon. 1991. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science (Wash. DC). 254:1643-1647.
5. Traversari, C., P. van der Bruggen, I.F. Luescher, C. Lurquin, P. Chornez, A. Van Pel, E. De Plaen, A. AmarCostesec, and T. Boon. 1992. A nonapeptide encoded by human MAGE-1 is recognized on HLA-Al by cytolytic T lymphocytes directed against tumor antigen MZ2-E. J Exp. Med. 176:1453-1457.
6. Gaugler, B., B. Van den Eynde, P. van der Bruggen, P Romero, J.J. Gaforio, E. De Plaen, B Lethe, F. Brasseur, and T. Boon. 1994. Human gene MAGE-3 codes for an antigen recognized on melanoma by autologous cytolync T lymphocytes. J. Exp. Med. 179:921-930.
7. Boon, T., J.C. Cerottini, A. Van Pel, and P. van der Bruggen. 1994. Tumor antigens recognized by T lymphocytes. Annu. Rev. Immunol. 12:337-365.
8. Bakker, A.B.H., W.J. Schreurs, A.J. de Boer, Y. Kawakami. S.A. Rosenberg, G.J. Adema, and G.G. Figdor. 1994. Melanocyte lineage-specific antigen gp100 is recognized by melanoma-derived tumor-infiltrating lymphocytes. J. Exp. Med. 179:1005-1009.
9. Kawakami, Y., S. Eliyahu, C.H. Delgado, P.P. Robbins, K. Sakaguchi, E. Appella, J.R. Yannelli, G.J. Adema, T. Miki, and S.A. Rosenberg. 1994. Identification of a human melanoma antigen recognized by tumor infiltrating lymphocytes associated with in vivo tumor rejection. Proc. Natl. Acad. Sci. USA. 91:6458-6462.
10. Kawakami, Y., S. Eliyahu, C H. Delgado, P.P. Robbins, L. Rivoltini, S.L. Topalian, T. Miki, and S.A. Rosenberg. 1994. Cloning of the gene for a shared melanoma antigen recognized by autologous T cells infiltrating into tumor. Proc. Natl. Acad. Sci. USA. 91:3515-3519.
11. Coulie, P.G., V. Brichard, A. Van Pel, T. Wolfel, J. Schneider, C. Traversari, S. Mattei, E. De Plaen, C. Lurquin, J.-P Szikora, J.C. Renauld, and T. Boon. 1994. A new gene coding for a differentiation antigen recognized by autologous cytolytic T lymphocytes on HLA-A2 melanomas. J. Exp. Md.180:35-42.
12. Kawakami Y., S. Eliyahu, K. Sakaguchi, P.P. Robbins, L. Rivoltini. J.R. Yannelli, E. Appella, and S.A. Rosenberg. 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. 180:347-352.
13. Brichard, V., A. Van Pel. T. Wolfel, C. Wolfel, E. De Plaen, B. Lethe, P. Coulie, and T. Boon. 1993. The tyrosinase gene encodes for an antigen recognized by autologous cytotoxic T lymphocytes on HLA-A2 melanomas. J. Exp. Med. 178:489-495
14. Wolfel, T., A. Van Pel, V. Brichard, J. Schneider, B. Seliger, K.H.M. zum Buschenfelde, and T. Boon. 1994. Two tyrosinase nonapeptides recognized on HLA-A2 melanomas by autologous cytolytic T lymphocytes. Eur. J. Immunol. 24:759-764
15. Slingluff, C.L., Jr., A.L. Cox, R.A. Henderson, D.F. Hunt, and V.H. Engelhard. 1993. Recognition of human melanoma cells by HLA-A2.1-restricted CTL is mediated by at least six shared pepnde epitopes. J. Immunol. 150:2955-2963.
16. Hunt, D.F., R.A. Henderson, J. Shabanowitz, K. Sakaguchi, H. Michel, N. Sevihr, A. Cox, E. Appella. and V.H. Engelhard 1992. Characterization of peptides bound to the class I MHC molecule HLA-A2.1 by mass spectrometry. Science (Wash. DC). 255:1261-1263.
17. Henderson, R.A., A.L. Cox, K. Sakaguchi, E Appella, J. Shabanowitz, D.F. Hunt, and V.H. Engelhard. 1993. Direct identification of an endogenous peptide recognized by multiple HLA-A2.1 specific cytotoxic T cells. Proc. Natl. Acad. Sci. USA 90:10275-10279.
18. Cox. A.L., J. Skipper, Y. Chen, R.A. Henderson, T.L. Darrow, J. Shabanowitz, V.H. Engelhard, D.F. Hunt, and C.L. Slingluff. 1994. Identification of a peptide recognized by five melanoma-specific human cytotoxic T cell lines. Science (Wash. DC). 264:716-719.
19. Engelhard, V.H., E. Appella, D.C. Benjamin, W.M. Bodnar, A.L. Cox, Y. Chen, R.A. Henderson, E.L. Huczko, H. Michel. K. Sakaguchi, et al. 1993. Mass spectrometric analysis of peptides associated with the human class I MHC molecules HLA-A2.1 and HLA-B7 and identification of structural features that determine binding. Chem. Immunol. 57:39-62.
20. Salter, R.D., D.N. Howell, and P. Cresswell. 1985. Genes regulating HLA class I antigen expression in T-B lymphoblast hybrids. Immunogenettcs. 21:235-246.
21. Henderson, R.A., H. Michel, K. Sakaguchi, J. Shabanowitz, E. Appella, D.F. Hunt, and V.H. Engelhard. 1992. HLA-A2.1 associated peptides from a mutant cell line: a second pathway of antigen presentation. Science (Wash. DC). 255: 1264-1266.
22. Bodmer, H., G. Ogg, F. Gotch, and A. McMichael. 1989. Anti-HLA-A2 antibody-enhancement of peptide association with HLA-A2 as detected by cytotoxic T lymphocytes. Nature (Lond.). 342:443-446.
23. Chen, Y., J. Sidney, S. Southwood, A.L. Cox, K. Sakaguchi, R. Henderson, E. Appella, D.F. Hunt, A. Sette, and V.H. Engelhard. 1994. Naturally processed peptides longer than nine amino acid residues bind to the class I MHC molecule HLA-A2.1 with high affinity and in different conformations. J. Immunol 152:2874-2881.
24. Ruppert, J., J. Sidney, E. Celis, R.T. Kubo, H.M. Grey, and A. Sette. 1993. Prominent role of secondary anchor residues in peptide binding to A2.1 molecules. Cell. 74:929-937.
25. den Haan, J.H.H., N.E. Sherman, E. Blokland, E.L. Huczko, F. Korung, J.W. Drijfhout, J. Skipper, J. Shabanowitz, D.F. Hunt, V.H. Engelhard, and E. Goulmy. 1995. Identification of a graft-versus-host disease associated human minor histocompatibility antigen. Science (Wash. DC). 268:1476-1480.
26. Bertoletti, A., F.V. Chisari, A. Penna, S. Guilhot, L. Galati, G. Missale, P. Fowler, H. Schlicht, A. Vitiello, R.C. Chesnut, et al. 1993. Definition of a minimal optimal cytotoxic T-cell epitope within the hepatitis B virus nucleocapsid protein. J. Virol. 67:2376-2380.
27. Utz, U., S. Koenig, J.E. Coligan, and W.E. Biddison. 1992. Presentation of three different viral peptides, HTLV-1 Tax, HCMV gB, and influenza virus M1, is determined by common structural features of the HLA-A2.1 molecule. J. Immunol 149:214-221.
28. Bednarek, M.A., S.Y. Sauma, M.C. Gammon, G. Porter, S. Tamhankar, A.R. Williamson, and H.J. Zweerink. 1991. The minimum peptide epitope from the influenza virus matrix protein. Extracellular and intracellular loading of HLA-A2.J. Immunol. 147:4047-4053.
29. Kwon, B.S., A.K. Haq, S.H. Pomerantz, and R. Halaban. 1987. Isolation and sequence of a cDNA for human tyrosinase that maps at the mouse c-albino locus. Proc. Natl. Acad. Sci. USA. 84:7473-7477.
30. Bouchard, B., B.B. Fuller, S. Vijayasaradhi, and A.N. Houghton. 1989. Induction of pigrnentation in mouse fibroblasts by expression of human tyrosinase cDNA. J. Exp. Med. 169:2029-2042.
31. Oetting, W.S., H.Y. Handoko, M.M. Mentink, A.S. Palier, J.G. White, and R.A. King. 1991. Molecular analysis of an extended family with type IA (tyrosinase negative) oculocutaneous albinism.J. Invest. Dermatol. 97:15-19.
32. Wright, H.T. 1991. Nonenzymatic deamidation of asparaginyl and glutaminyl residues in proteins. Crit. Rev. Biochem. Mol. Biol. 26:1-52.
33. Suzuki, T., A. Seko, K. Kitajima, Y. Inoue, and S. Inoue. 1993. Identification of peptide:N-glycanase activity in mammalian-derived cultured cells. Biochem. Biophys. Res. Commun. 194:1124-1130.
34. Suzuki, T., A. Seko, K. Kitajima, Y. Inoue, and S. Inoue. 1994. Purification and enzymatic properties of peptide:N-glycanase from C3H mouse-derived L-929 fibroblast cells. J. Biol. Chem. 269:17611-17618.
35. Aronson, N.N., and M.J. Kuranda. 1989. Lysosomal degradation of Asn-linked glycoproteins. FASEB (Fed. Am. Soc. Exp. Biol.). 3:2615-2622.
36. Kaartinen, V., T. Mononen, R. Laatkainen, and I. Mononen. 1992. Substrate speciocity and reaction mechanism of human glycoasparaginase. J. Biol. Chem. 267:6855-6858.
37. Mononen, I., K.J. Fisher, V. Kaartinen, and N.N. Aronson. 1993. Aspartylglycosaminuria: protein, chemistry and molecular biology of the most common lysosomal storage disorder of glycoprotein degradation. FASEB (Fed. Am. Soc. Exp. Biol.). 7:1247-1256.
38. Hearing, V.J., and M. Jimenez. 1987. The critical regulatory control point in melanocyte pigmentation. Int. J. Biochem. 19: 1141-1147.
39. Hearing, V.J., and M. Jimenez. 1989. Analysis of mammalian pigmentation at the molecular level. Pigm. Cell Res. 2:75-85.
40. Ohkura, T., K. Yamashita, Y. Mishima, and A. Kobata. 1984. Purification of hamster melanoma tyrosinase and structural studies of their asparagine-linked sugar chains. Arch. Biochem. Biophys. 235:63-77.
41. Yewdell, J.W., and J.R. Bennink. 1992. Cell biology of antigen processing and presentation to MHC class I molecule restricted T lymphocytes. Adv. Immunol. 52:1-123.
42. Germain, R.N., and D.H. Margulies. 1993. The biochemistry and cell biology of antigen processing and presentation. Annu. Rev. Immunol. 11:403-450.
43. + T cells. Nature (Lond.). 364:158-161.
44. van Binnendijk, R.S., C.A. van Baalen, M.C. Poelen, P. de Vries, J. Boes, V. Cerundolo, A.D. Osterhaus, and F.G. UytdeHaag. 1992. Measles virus transmembrane fusion protein synthesized de novo or presented in immunostimulating complexes is endogenously processed for HLA class I- and class II-restricted cytotoxic T cell recognition. J. Exp. Med. 176:119-128.
45. Chicz, R.M., R.G. Urban, J.C. Gorga, D.A. Vignali, W.S. Lane, and J.L. Strominger. 1993. Specificity and promiscuity among naturally processed peptides bound to HLA-DR alleles. J. Exp. Med. 178:27-47.
46. Michaelsson, E., V. Malmstrom, S. Reis, A. Engstrom. H. Burkhardt, and R. Holmdahl. 1994. T cell recognition of carbohydrates on type II collagen. J. Exp. Med. 180:745-749.
47. Jerome, K.R., N. Domenech, and O.J. Finn. 1993. Tumorspecific cytotoxic T cell clones from patients with breast and pancreatic adenocarcinoma recognize EBV-immortalized B cells transfected with polymorphic epithelial mucin complementary DNA. J. Immunol. 151:1654-1662.
48. Huczko, E.L., W.M. Bodnar, D. Benjamin, K. Sakaguchi, N.Z. Zhu, J. Shabanowitz, R.A. Henderson. E. Appella, D.F. Hunt, and V.H. Engelhard. 1993. Characteristics of endogenous peptides eluted from the class I MHC molecule HLA-B7 determined by mass spectrometry and computer modeling. J. Immunol. 151:2572-2587.