Human gene MAGE-3 codes for an antigen recognized on a melanoma by autologous cytolytic T lymphocytes (original) (raw)

• Journal List
• J Exp Med
• v.179(3); 1994 Mar 1
• PMC2191409

J Exp Med. 1994 Mar 1; 179(3): 921–930.

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Abstract

Human melanoma cell line MZ2-MEL expresses several antigens recognized by autologous cytolytic T lymphocyte (CTL) clones. We reported previously the identification of a gene, named MAGE-1, that codes for one of these antigens named MZ2-E. We show here that antigen MZ2-D, which is present on the same tumor, is encoded by another member of the MAGE gene family named MAGE-3. Like MAGE-1, MAGE-3 is composed of three exons and the large open reading frame is entirely located in the third exon. Its sequence shows 73% identity with MAGE-1. Like MZ2-E, antigen MZ2-D is presented by HLA-A1. The antigenic peptide of MZ2-D is a nonapeptide that is encoded by the sequence of MAGE-3 that is homologous to the MAGE-1 sequence coding for the MZ2-E peptide. Competition experiments using single Ala-substituted peptides indicated that amino acid residues Asp in position 3 and Tyr in position 9 were essential for binding of the MAGE-1 peptide to HLA-A1. Gene MAGE-3 is expressed in many tumors of several types, such as melanoma, head and neck squamous cell carcinoma, lung carcinoma and breast carcinoma, but not in normal tissues except for testes. It is expressed in a larger proportion of melanoma samples than MAGE-1. MAGE-3 encoded antigens may therefore have a wide applicability for specific immunotherapy of melanoma patients.

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• Mukherji B, MacAlister TJ. Clonal analysis of cytotoxic T cell response against human melanoma. J Exp Med. 1983 Jul 1;158(1):240–245. [PMC free article] [PubMed] [Google Scholar]
• Knuth A, Danowski B, Oettgen HF, Old LJ. T-cell-mediated cytotoxicity against autologous malignant melanoma: analysis with interleukin 2-dependent T-cell cultures. Proc Natl Acad Sci U S A. 1984 Jun;81(11):3511–3515. [PMC free article] [PubMed] [Google Scholar]
• Hérin M, Lemoine C, Weynants P, Vessière F, Van Pel A, Knuth A, Devos R, Boon T. Production of stable cytolytic T-cell clones directed against autologous human melanoma. Int J Cancer. 1987 Mar 15;39(3):390–396. [PubMed] [Google Scholar]
• Topalian SL, Solomon D, Rosenberg SA. Tumor-specific cytolysis by lymphocytes infiltrating human melanomas. J Immunol. 1989 May 15;142(10):3714–3725. [PubMed] [Google Scholar]
• Van den Eynde B, Hainaut P, Hérin M, Knuth A, Lemoine C, Weynants P, van der Bruggen P, Fauchet R, Boon T. Presence on a human melanoma of multiple antigens recognized by autologous CTL. Int J Cancer. 1989 Oct 15;44(4):634–640. [PubMed] [Google Scholar]
• van der Bruggen P, Traversari C, Chomez P, Lurquin C, De Plaen E, Van den Eynde B, Knuth A, Boon T. A gene encoding an antigen recognized by cytolytic T lymphocytes on a human melanoma. Science. 1991 Dec 13;254(5038):1643–1647. [PubMed] [Google Scholar]
• De Smet C, Lurquin C, van der Bruggen P, De Plaen E, Brasseur F, Boon T. Sequence and expression pattern of the human MAGE2 gene. Immunogenetics. 1994;39(2):121–129. [PubMed] [Google Scholar]
• Traversari C, van der Bruggen P, Luescher IF, Lurquin C, Chomez P, Van Pel A, De Plaen E, Amar-Costesec A, 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. 1992 Nov 1;176(5):1453–1457. [PMC free article] [PubMed] [Google Scholar]
• De Plaen E, Lurquin C, Van Pel A, Mariamé B, Szikora JP, Wölfel T, Sibille C, Chomez P, Boon T. Immunogenic (tum-) variants of mouse tumor P815: cloning of the gene of tum- antigen P91A and identification of the tum- mutation. Proc Natl Acad Sci U S A. 1988 Apr;85(7):2274–2278. [PMC free article] [PubMed] [Google Scholar]
• Lurquin C, Van Pel A, Mariamé B, De Plaen E, Szikora JP, Janssens C, Reddehase MJ, Lejeune J, Boon T. Structure of the gene of tum- transplantation antigen P91A: the mutated exon encodes a peptide recognized with Ld by cytolytic T cells. Cell. 1989 Jul 28;58(2):293–303. [PubMed] [Google Scholar]
• Seed B, Aruffo A. Molecular cloning of the CD2 antigen, the T-cell erythrocyte receptor, by a rapid immunoselection procedure. Proc Natl Acad Sci U S A. 1987 May;84(10):3365–3369. [PMC free article] [PubMed] [Google Scholar]
• Traversari C, van der Bruggen P, Van den Eynde B, Hainaut P, Lemoine C, Ohta N, Old L, Boon T. Transfection and expression of a gene coding for a human melanoma antigen recognized by autologous cytolytic T lymphocytes. Immunogenetics. 1992;35(3):145–152. [PubMed] [Google Scholar]
• Boon T, Van Snick J, Van Pel A, Uyttenhove C, Marchand M. Immunogenic variants obtained by mutagenesis of mouse mastocytoma P815. II. T lymphocyte-mediated cytolysis. J Exp Med. 1980 Nov 1;152(5):1184–1193. [PMC free article] [PubMed] [Google Scholar]
• Brasseur F, Marchand M, Vanwijck R, Hérin M, Lethé B, Chomez P, Boon T. Human gene MAGE-1, which codes for a tumor-rejection antigen, is expressed by some breast tumors. Int J Cancer. 1992 Nov 11;52(5):839–841. [PubMed] [Google Scholar]
• Maryanski JL, Romero P, Van Pel A, Boon T, Salemme FR, Cerottini JC, Corradin G. The identification of tyrosine as a common key residue in unrelated H-2Kd restricted antigenic peptides. Int Immunol. 1991 Oct;3(10):1035–1042. [PubMed] [Google Scholar]
• Falk K, Rötzschke O, Stevanović S, Jung G, Rammensee HG. Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature. 1991 May 23;351(6324):290–296. [PubMed] [Google Scholar]
• Hill AV, Elvin J, Willis AC, Aidoo M, Allsopp CE, Gotch FM, Gao XM, Takiguchi M, Greenwood BM, Townsend AR, et al. Molecular analysis of the association of HLA-B53 and resistance to severe malaria. Nature. 1992 Dec 3;360(6403):434–439. [PubMed] [Google Scholar]
• Townsend AR, Rothbard J, Gotch FM, Bahadur G, Wraith D, McMichael AJ. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell. 1986 Mar 28;44(6):959–968. [PubMed] [Google Scholar]
• McMichael AJ, Gotch FM, Rothbard J. HLA B37 determines an influenza A virus nucleoprotein epitope recognized by cytotoxic T lymphocytes. J Exp Med. 1986 Nov 1;164(5):1397–1406. [PMC free article] [PubMed] [Google Scholar]
• Robbins PA, Lettice LA, Rota P, Santos-Aguado J, Rothbard J, McMichael AJ, Strominger JL. Comparison between two peptide epitopes presented to cytotoxic T lymphocytes by HLA-A2. Evidence for discrete locations within HLA-A2. J Immunol. 1989 Dec 15;143(12):4098–4103. [PubMed] [Google Scholar]
• Pazmany L, Rowland-Jones S, Huet S, Hill A, Sutton J, Murray R, Brooks J, McMichael A. Genetic modulation of antigen presentation by HLA-B27 molecules. J Exp Med. 1992 Feb 1;175(2):361–369. [PMC free article] [PubMed] [Google Scholar]
• Silver ML, Guo HC, Strominger JL, Wiley DC. Atomic structure of a human MHC molecule presenting an influenza virus peptide. Nature. 1992 Nov 26;360(6402):367–369. [PubMed] [Google Scholar]
• Jardetzky TS, Lane WS, Robinson RA, Madden DR, Wiley DC. Identification of self peptides bound to purified HLA-B27. Nature. 1991 Sep 26;353(6342):326–329. [PubMed] [Google Scholar]
• DiBrino M, Parker KC, Shiloach J, Knierman M, Lukszo J, Turner RV, Biddison WE, Coligan JE. Endogenous peptides bound to HLA-A3 possess a specific combination of anchor residues that permit identification of potential antigenic peptides. Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1508–1512. [PMC free article] [PubMed] [Google Scholar]
• Falk K, Rötzschke O, Grahovac B, Schendel D, Stevanović S, Jung G, Rammensee HG. Peptide motifs of HLA-B35 and -B37 molecules. Immunogenetics. 1993;38(2):161–162. [PubMed] [Google Scholar]
• Zhang QJ, Gavioli R, Klein G, Masucci MG. An HLA-A11-specific motif in nonamer peptides derived from viral and cellular proteins. Proc Natl Acad Sci U S A. 1993 Mar 15;90(6):2217–2221. [PMC free article] [PubMed] [Google Scholar]
• Townsend A, Elliott T, Cerundolo V, Foster L, Barber B, Tse A. Assembly of MHC class I molecules analyzed in vitro. Cell. 1990 Jul 27;62(2):285–295. [PubMed] [Google Scholar]
• Elvin J, Cerundolo V, Elliott T, Townsend A. A quantitative assay of peptide-dependent class I assembly. Eur J Immunol. 1991 Sep;21(9):2025–2031. [PubMed] [Google Scholar]
• Parker KC, Bednarek MA, Hull LK, Utz U, Cunningham B, Zweerink HJ, Biddison WE, Coligan JE. Sequence motifs important for peptide binding to the human MHC class I molecule, HLA-A2. J Immunol. 1992 Dec 1;149(11):3580–3587. [PubMed] [Google Scholar]
• Macatonia SE, Taylor PM, Knight SC, Askonas BA. Primary stimulation by dendritic cells induces antiviral proliferative and cytotoxic T cell responses in vitro. J Exp Med. 1989 Apr 1;169(4):1255–1264. [PMC free article] [PubMed] [Google Scholar]
• De Bruijn ML, Nieland JD, Schumacher TN, Ploegh HL, Kast WM, Melief CJ. Mechanisms of induction of primary virus-specific cytotoxic T lymphocyte responses. Eur J Immunol. 1992 Nov;22(11):3013–3020. [PubMed] [Google Scholar]
• Houbiers JG, Nijman HW, van der Burg SH, Drijfhout JW, Kenemans P, van de Velde CJ, Brand A, Momburg F, Kast WM, Melief CJ. In vitro induction of human cytotoxic T lymphocyte responses against peptides of mutant and wild-type p53. Eur J Immunol. 1993 Sep;23(9):2072–2077. [PubMed] [Google Scholar]
• Schild H, Deres K, Wiesmüller KH, Jung G, Rammensee HG. Efficiency of peptides and lipopeptides for in vivo priming of virus-specific cytotoxic T cells. Eur J Immunol. 1991 Nov;21(11):2649–2654. [PubMed] [Google Scholar]
• Romero P, Eberl G, Casanova JL, Cordey AS, Widmann C, Luescher IF, Corradin G, Maryanski JL. Immunization with synthetic peptides containing a defined malaria epitope induces a highly diverse cytotoxic T lymphocyte response. Evidence that two peptide residues are buried in the MHC molecule. J Immunol. 1992 Mar 15;148(6):1871–1878. [PubMed] [Google Scholar]
• Feltkamp MC, Smits HL, Vierboom MP, Minnaar RP, de Jongh BM, Drijfhout JW, ter Schegget J, Melief CJ, Kast WM. Vaccination with cytotoxic T lymphocyte epitope-containing peptide protects against a tumor induced by human papillomavirus type 16-transformed cells. Eur J Immunol. 1993 Sep;23(9):2242–2249. [PubMed] [Google Scholar]
• Rock KL, Fleischacker C, Gamble S. Peptide-priming of cytolytic T cell immunity in vivo using beta 2-microglobulin as an adjuvant. J Immunol. 1993 Feb 15;150(4):1244–1252. [PubMed] [Google Scholar]

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