Two Members Of The Human Mageb Gene Family Located In Xp21.3 Are Expressed In Tumors Of Various Histological Origins

[en] Genes of the MAGE family direct the expression of tumor antigens recognized on a human melanoma by autologous cytolytic T lymphocytes. Twelve closely related MAGE genes are located in the Xq28 region. These genes share 60-98% nucleotide identity in their coding region. The presence of homologous genes in a region of Xp21.3 has been reported previously. We obtained the complete sequence of a 42-kb stretch of this region. It contains four MAGE-related genes, which we propose to name MAGE-B1, B2, B3, and B4 (HGMW-approved symbols MAGEB1, MAGEB2, MAGEB3, and MAGEB4). The coding regions of these genes share 66-81% nucleotide identity and show 45-63% identity with those of the MAGE genes located in Xq28. Like the MAGE genes located in Xq28, the MAGE-B genes are silent in normal tissues with the exception of testis. Like MAGE-1, 2, 3, 4, 6 and 12 (HGMW-approved symbols MAGEA1, 2, 3, 4, 6, and 12), genes MAGE-B1 and MAGE-B2 are expressed in a significant fraction of tumors of various histological types. The transcription of MAGE-B1 and MAGE-B2 can be induced by 5-aza-2'-deoxycytidine, suggesting that the activation of these genes in tumors results from a demethylation process.

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Lurquin, C.

De Smet, C.

Brasseur, F.

Muscatelli, F.

Martelange, V.

De Plaen, E.

Brasseur, Robert ; Université de Liège - ULiège > Gembloux Agro-Bio Tech

Monaco, Ap.

Boon, T.

Language :

English

Title :

Two Members Of The Human Mageb Gene Family Located In Xp21.3 Are Expressed In Tumors Of Various Histological Origins

Publication date :

1997

Journal title :

Genomics

ISSN :

0888-7543

eISSN :

1089-8646

Publisher :

Elsevier, Atlanta, Georgia

Volume :

Issue :

Pages :

397-408
397-408

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 25 June 2010

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Bibliography

Bardoni, B., Zanaria, E., Guioli, S., Floridia, G., Worley, K. C., Tonini, G., Ferrante, E., Chiumello, G., McCabe, E. R. B., Fraccaro, M. L., Zuffardi, O., and Camerino, G. (1994). A dosage sensitive locus at chromosome Xp21 is involved in male to female sex reversal. Nature Genet. 7: 497-501.
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: 337-365.
Boon, T., Coulie, P. G., Brichard, V., and, Marchand, M. (1995). T-Lymphocyte responses. In "Clinical Oncology" (M. D. Abeloff, J. O. Armitage, A. S. Lichter, and J. E. Niederhuber, Eds.), pp. 90-99, Churchill Livingstone, New York.
Brasseur, F., Marchand, M., Vanwijck, R., Hérin, M., Lethé, B., Chomez, P., and Boon, T. (1992). Human gene MAGE-1, which codes for a tumor rejection antigen, is expressed by some breast tumors. Int. J. Cancer 52: 839-841.
Brasseur, F., Rimoldi, D., Liénard, D., Lethé, B., Carrel, S., Arienti, F., Suter, L., Vanwijck, R., Bourlond, A., Humblet, Y., Vacca, A., Conese, M., Lahaye, T., Degiovanni, G., Deraemaecker, R., Beauduin, M., Sastre, X., Salamon, E., Dréno, B., Jäger, E., Knuth, A., Chevreau, C., Suciu, S., Lachapelle, M., Pouillart, P., Parmiani, G., Lejeune, F., Cerottini, J.-C., Boon, T., and Marchand, M. (1995). Expression of MAGE genes in primary and metastatic cutaneous melanoma. Int. J. Cancer 63: 375-380.
Counts, J. L., and Goodman, J. I. (1995). Alterations in DNA methylation may play a variety of roles in carcinogenesis. Cell 83: 13-15.
Dabovic, B., Zanaria, E., Bardoni, B., Lisa, A., Bordignon, C., Russo, V., Matessi, C., Traversari, C., and Camerino, G. (1995). A family of rapidly evolving genes from the sex reversal critical region in Xp21. Mamm. Genome 6: 571-580.
Davis, L. G., Dibner, M. D., and Battey, J. F. (1986). "Basic Methods in Molecular Biology", pp. 130-135, Elsevier Science Publishing, New York.
De Backer, O., Verheyden, A.-M., Martin, B., Godelaine, D., De Plaen, E., Brasseur, R., Avner, P., and Boon, T. (1995). Structure, chromosomal location, and expression pattern of three mouse genes homologous to the human MAGE genes. Genomics 28: 74-83.
De Loof, H., Rosseneu, M., Brasseur, R., and Ruysschaert, J. M. (1986). Use of hydrophobicity profiles to predict receptor binding domains on apolipoprotein E and the low density lipoprotein apolipoprotein B-E receptor. Proc. Natl. Acad. Sci. USA 83:2295-2299.
De Plaen, E., Arden, K., Traversari, C., Gaforio, J. J., Szikora, J.-P., De Smet, C., Brasseur, F., van der Bruggen, P., Lethé, B., Lurquin, C., Brasseur, R., Chomez, P., De Backer, O., Cavenee, W., and Boon, T. (1994). Structure, chromosomal localization and expression of twelve genes of the MAGE family. Immunogenetics 40:360-369.
De Plaen, E., Lurquin, C., Brichard, V., van der Bruggen, P., Renauld, J. C., Coulie, P., Szikora, J. P., Wölfel, T., Van Pel, A., and Boon, T. (1996). Cloning of genes coding for antigens recognized by cytolytic T lymphocytes. In "The Immunology Methods Manual" (I. Lefkovits, Ed.), pp. 691-718, Academic Press Ltd., London.
De Plaen, E., Lurquin, C., Lethé, B., van der Bruggen, P., Brichard, V., Renauld, J. C., Coulie, P., Van Pel, A., and Boon, T. (1997a). Identification of genes coding for tumor antigens recognized by cytolytic T lymphocytes. Methods: Companion Methods Enzymol. 12: 125-142.
De Plaen, E., Naerhuyzen, B., De Smet, C., Szikora, J. P., and Boon, T. (1997b). Alternative promoters of gene MAGE4a. Genomics 40: 305-313.
De Smet, C., Courtois, S. J., Faraoni, I., Lurquin, C., Szikora, J.-P., De Backer, O., and Boon, T. (1995). Involvement of two Ets binding sites in the transcriptional activation of the MAGE1 gene. Immunogenetics 42: 282-290.
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.
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: 121-129.
Fleischhauer, K., Fruci, D., Van Endert, P., Herman, J., Tanzarella, S., Wallny, H. J., Coulie, P., Bordignon, C., and Traversari, C. (1996). Characterization of antigenic peptides presented by HLA-B44 molecules on tumor cells expressing the gene MAGE-3. Int. J. Cancer 68: 622-628.
Gaboriaud, C., Bissery, V., Benchetrit, T., and Mornon, J. P. (1987). Hydrophobic cluster analysis: An efficient new way to compare and analyse amino acid sequences. FEBS Lett. 224: 149-155.
Gaugler, B., Van den Eynde, B., van der Bruggen, P., Romero, P., Gaforio, J. J., De Plaen, E., Lethe, 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.
Henikoff, S. (1984). Unidirectional digestion with exonuclease III creates targeted breakpoints for DNA sequencing. Gene 28: 351-359.
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.
Inoue, H., Mori, M., Honda, M., Li, J., Shibuta, K., Mimori, K., Ueo, H., and Akiyoshi, T. (1995a). The expression of tumor-rejection antigen "MAGE" genes in human gastric carcinoma. Gastroenterology 109: 1522-1525.
Inoue, H., Mori, M., Li, J., Mimori, K., Honda, M., Nakashima, H., Mafune, K.-i., Tanaka, Y., and Akiyoshi, T. (1995b). Human esophageal carcinomas frequently express the tumor-rejection antigens of MAGE genes. Int. J. Cancer 63: 523-526.
Jassim, A., Oilier, W., Payne, A., Biro, A., Oliver, R. T. D., and Festenstein, H. (1989). Analysis of HLA antigens on germ cells in human semen. Eur. J. Immunol. 19: 1215-1220.
Le, L., Brasseur, R., Werners, C., Meulemans, G., and Burny, A. (1988). Fusion (F) protein gene of Newcastle disease virus: Sequence and hydrophobicity comparative analysis between virulent and avirulent strains. Virus Genes 1: 333-350.
Lurquin, C., Van Pel, A., Mariamé, B., De Plaen, E., Szikora, J.-P., Janssens, C., Reddehase, M., Lejeune, J., and Boon, T. (1989). Structure of the gene coding for turn-transplantation antigen P91A. A peptide encoded by the mutated exon is recognized with Ld by cytolytic T cells. Cell 58: 293-303.
Maeurer, M. J., Storkus, W. J., Kirkwood, J. M., and Lotze, M. T. (1996). New treatment options for patients with melanoma: Review of melanoma-derived T-cell epitope-based peptide vaccines. Melanoma Res. 6: 11-24.
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 responses in melanoma patients treated with a peptide encoded by gene MAGE-3. Int. J. Cancer 63: 883-885.
Mulcahy, K. A., Rimoldi, D., Brasseur, F., Rodgers, S., Liénard, D., Marchand, M., Rennie, I. G., Murray, A. K., McIntyre, C. A., Platts, K. E., Leyvraz, S., Boon, T., and Ree, R. C. (1996). Infrequent expression of the MAGE gene family in uveal melanomas. Int. J. Cancer 66: 738-742.
Muscatelli, F., Strom, T. M., Walker, A. P., Zanaria, E., Recan, D., Meindl, A., Bardoni, B., Guioli, S., Zehetner, G., Rabl, W., Schwarz, H. P., Kaplan, J. C., Camerino, G., Meitinger, T., and Monaco, A. (1994). Mutations in the DAX-1 gene give rise to both X-linked adrenal hypoplasia congenita and hypogonadotropic hypogonadism. Nature 372: 672-676.
Muscatelli, F., Walker, A. P., De Plaen, E., Stafford, A. N., and Monaco, A. P. (1995). Isolation and characterization of a new MAGE gene family in the Xp21.3 region. Proc. Natl. Acad. Sci. USA 92: 4987-4991.
Patard, J.-J., Brasseur, F., Gil-Diez, S., Radvanyi, F., Marchand, M., Francois, P., Abi Aad, A., Van Cangh, P., Abbou, C. C., Chopin, D., and Boon, T. (1995). Expression of MAGE genes in transitional-cell carcinomas of the urinary bladder. Int. J. Cancer 64: 60-64.
Rogner, U. C., Wilke, K., Steck, E., Korn, B., and Poustka, A. (1995). The melanoma antigen gene (MAGE) family is clustered in the chromosomal band Xq28. Genomics 29: 725-731.
Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989). "Molecular Cloning: A Laboratory Manual," Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
Shah, M. B., Guan, X., Einstein, J. R., Matis, S., Xu, Y., Mural, R. J., and Uberbacher, E. C. (1994). "User's Guide to GRAIL and GENQUEST (Sequence Analysis, Gene Assembly And Sequence Comparison Systems) E-mail Servers and XGRAIL (Version 1.2) and XGENQUEST (Version 1.1) Client-Server Systems," http://avalon. epm.ornl.gov/manuals/grail-genquest.9407.html, Oak Ridge National Laboratory, Tennessee.
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.
Swain, A., Zanaria, E., Hacker, A., Lovell-Badge, R., and Camerino, G. (1996). Mouse Dax1 expression is consistent with a role in sex determination as well as in adrenal and hypothalamus function. Nature Genet. 12: 404-409.
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.
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. (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: 1453-1457.
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.
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.
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.
Van Pel, A., van der Bruggen, P., Coulie, P. G., Brichard, V. G., Lethé, B., Van den Eynde, B., Uyttenhove, C., Renauld, J.-C., and Boon, T. (1995). Genes coding for tumor antigens recognized by cytolytic T lymphocytes. Immunol. Rev. 145: 229-250.
Weber, J., Salgaller, M., Samid, D., Johnson, B., Herlyn, M., Lassam, N., Treisman, J., and Rosenberg, S. A. (1994). Expression of the MAGE1 tumor antigen is upregulated by the demethylating agent 5-aza-2′-deoxycytidine. Cancer Res. 54: 1766-1771.
Weynants, P., Lethe, B., Brasseur, F., Marchand, M., and Boon, T. (1994). Expression of MAGE genes by non-small-cell lung carcinomas. Int. J. Cancer 56: 826-829.
Zanaria, E., Muscatelli, F., Bardoni, B., Strom, T. M., Guioli, S., Guo, W., Lalli, E., Moser, C., Walker, A. P., McCabe, E. R. B., Meitinger, T., Monaco, A. P., Sassone-Corsi, P., and Camerino, G. (1994). An unusual member of the nuclear hormone receptor superfamily responsible for X-linked adrenal hypoplasia congenita. Nature 372: 635-641.