Abstract
Five class II (B-L) B genes are encoded in the major histocompatibility complex (MHC) of chickens of the B 12 haplotype. We report here the nucleotide sequence of one of these genes, B-LBII, as well as the primary structure of a corresponding cDNA. The organization of B-LBII, its 5' flanking region including the promotor region, and the amino acid sequence of its product are compared to mammalian class II B genes and to the previously described B-LBIII gene, which probably is a pseudogene since no B-LBIII transcript could be identified. The 5' flanking oegion of B-LBII exhibits homologs of transcription-controlling sequence motifs, namely S, X, X2, and Y boxes, of class II A and B genes of rodents and man. However, the promotor region of B-LBIII lacks an equivalent of the S box, displays two nucleic acid substitutions in the core sequence of the Y box, exhibits a 16 base pair (bp) deletion upstream of the site of initiation of transcription. Therefore, an aberrant promotor region is likely to account for the pseudogene-like nature of B-LBIII, which displays open-reading frames in all exons. The data obtained with the functional B-LBII gene are in line with our previous interpretation that both genomic organization and tertiary structure of class II β molecules are remarkably conserved between birds and mammals.
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References
Auffray, C. and Rougeon, F.: Purification of mouse immunoglobulin heavy chain messenger RNAs from total myeloma tumor RNA. Eur J Biochem 107: 303–314, 1980
Auffray, C. and Strominger, J. L.: Molecular genetics of the human major histocompatibility complex. Adv Hum Genet 15: 197–247, 1986
Auffray, C., Lillie, J. W., Korman, A. J., Boss, J. M., Fréchin, N., Guillemot, F., Cooper, J., Mullingn, R. C., and Strominger, J. L.: Structure and expression of HLA-DQ α and HLA-DX α genes: interallelic alternate splicing of the HLA-DQ α gene and functional splicing of the HLA-DX α gene using a retroviral vector. Immunogenetics 26: 63–73, 1987
Basta, P. V., Scherman, P. A., and Ting, J. P. Y.: Detailed delineation of an interferon λ responsive element important in human HLA-DRA gene expression in a glioblastoma multiform line. Proc Natl Acad Sci USA 85: 8618–8622, 1988
Benoist, C. and Mathis, D. : Regulation of major histocompatibility complex class II genes: X, Y and other letters of the alphabet. Annu Rev Immunol, in press, 1990
Berk, C. and Scharp, P. A.: Sizing and mapping of early adenovirus mRNA by gel electrophoresis of S1 endonuclease-digested hybrids. Cell 12: 721–732, 1977
Boss, J. M. and Strominger, J. L.: Cloning snd sequence analysis of the human major histocompatibility complex gene DC-3B. Proc Natl Acad Sci USA 81: 5199–5203, 1984
Bourlet, Y., Béhar, G., Guillemot, F., Fréchin, N., Billault, A., Chaussé, A.-M., Zoorob, R. and Auffray, C.: Isolation of chicken major histocompatibility complex class II (B-L) β chain sequences: comparison with mammalian β chains and expression in lymphoid organs. EMBO J 7: 1031–1039, 1988
Breathnach, R. and Chambon, P.: Organization andexpression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50: 349–383, 1981
Briles, W. E., Bumstead, N., Ewert, D. L., Golmour, D. G., Gogusev, J., Hála, K., Koch, C., Longenecker, B. M., Nordskog, A. W., Pink, J. R. L., Schierman, L. W., Simonsen, M., Toivanen, A., Vainio, O., and Wick, G.: Nomenclature for chicken major histocompatibility (B) complex. Immunogenetics 16: 441–447, 1982
Brown, J. H., Jardetzky, T., Saper, M. A., Samraoui, B., Bjorkman, P. J., and Wiley, D. C.: A hypothetical model of the foreign antigen binding site of class II histocompatibility molecules. Nature 332: 845–850, 1988
Crone, M. and Simonsen, M.: Avian major histocompatibility complex. In A. Toivanen and P. Toivanen (eds.): Avian Immunology: Basis and Practice, Vol 2, pp. 25–41, CRC, Boca Raton, Florida 1987
Crone, M., Jenesius, J. and Koch, C.: B-L antigens (Ia-like antigens) of the chicken major histocompatibility complex. Scand J Immunol 14: 591–597, 1981
Dorn, A., Bolleken, J., Staub, A., Benoist, C., and Mathis, D.: A multiplicity of CCAAT box-binding proteins. Cell 50: 863–872, 1987
Eccles, S. J. and McMaster, W. R.: DNA sequence analysis of a rat RT1 class II A β gene. Immunogenetics 22: 653–663, 1985
Falkner, F. G. and Zachau, H. G.: Correct transcription of an immunoglobulin gene requires an upstream fragment containing conserved sequences elements. Nature 310: 71–74, 1984
Guillemot, F. and Auffray, C.: Molecular biology of the chicken MHC. In J. McGovernaud and J. R. Mandel (eds.): CRC Review in Poultry Science, IRL, in press, 1989
Guillemot, F., Turmel, P., Charron, D., Le Douarin, N., and Auffray, C.: Structure, polymorphism and biosynthesis of chicken MHC class II (B-L) antigens and associated molecules. J Immunol 137: 1251–1257, 1986
Guillemot, F., Billault, A., Pourquié, O., Béhar, G., Chaussé, A.-M., Zoorob, R., Kreibich, G., and Auffray, C.: A molecular map of the chicken major histocompatibility complex: the class II β genes are closely linked to the class I genes and to the nucleolar organizer. EMBO J 7: 2775–2785, 1988a
Guillemot, F., Auffray, C., Orr, H. T.,and Strominger, J. L.: MHC antigen genes. In B. D. Hames and D. M. Glover (eds.): Frontiers in Molecular Immunology, pp. 81–143, IRL, Oxford, 1988b
Hála, K., Boyd, R., and Wick, G.: Chicken major histocompatibility complex and disease. Scand J Immunol 14: 607–617, 1981
Kaufman, J. F., Auffray, C., Korman, A. J. Shackelford, D. A., and Strominger, J. L.: The class II molecules of the human and murine major histocompatibility complex. Cell 36: 1–13, 1984
Klein, J.: Natural History of the Major Histocompatibility Complex. Wiley, London, 1986
Kroemer, G., Guillemot, F., and Auffray, C.: Genetic organization of the chicken MHC. Immunol Res, in press 1989
Larhammar, D., Schenning, L., Gustafson, K., Wiman, K., Claesson, L., Rask, L., and Peterson, P. A.: Complete amino acid sequence of an HLA-DR antigen-like beta chain as predicted from the nucleotide sequence: similarities with immunoglobulin and HLA-A, B, c antigens. Proc Natl Acad Sci USA 79: 3687–3691, 1982
Larhammar, D., Hammerling, U., Rask, L., and Peterson, P. A.: Sequence of gene and cDNA encoding murine major histocompatibility class II gene Aβ2. J Biol Chem 260: 14111–14119,1985
Malissen, M., Hunkapiller, T., and Hood, L.: Nucleotide sequence of light chain gene of the mouse I-A subregion: Aβd. Science 221: 750–754, 1983
Maniatis, T., Fritsch, E. F., and Sambrook, L.: Molecular Cloning. A Laboratory Manual, Cold Spring Harbor, New York, 1982
Mazerolles, F., Durandy, A., Piatier-Tonneau, D., Charron, D., Montagnier, L., Auffray, C., and Fischer, A.: Immunosuppressive properties of synthetic peptides derived from HLA-DR and CD4 antigens. Cell 55: 497–504, 1988
Mazerolles, F., Amblard, F., Lumbroso, C., Van de Moortele, P. F., Lecomte, O., Barbat, C., Piatier-Tonneau, D., Auffray, C., and Fisher, A.: Regulation of T helper-B lymphocyte adhesion through CD4-HLA class II interaction. Eur J Immunol, in press, 1990
Mengle-Gaw, L. and McDevitt, H. O.: Predicted protein sequence of the murine I-Eβ polypeptide chain from cDNA and genomic clones. Proc Natl Acad Sci USA 82: 2910–2914, 1985
Miwa, K. and Strominger, J. L.: The HLA-DQβ gene upstream region contains an immunoglobulin-like octamer motif that binds cell-type specific nuclear factors. Nucleic Acids Res 15: 8057–8067, 1987
Tonnelle, C., DeMars, R., and Long, E. O.: DOβ: beta chain in HLA-D with a distinct regulation of expression. EMBO J 4: 2839–2847, 1985
Vainio, O., Koch, C., and Toivanen, A.: B-L antigens (class II) of the chicken major histocompatibility complex control T-B cell interaction. Immunogenetics 19: 131–140, 1984
Vainio, O., Veromaa, T., Eerol, E., Toivanen, P., and Ratcliffe, M.: Antigen-presenting cell-T cell interaction in the chickensis MHC class II antigen restricted. J Immunol 140: 2864–2869, 1988
Wick, G., Kroemer, G., Neu, N., Fasseler, R., Ziemiecki, A., Mueller, R. G., Ginzel, M., Béladi, J., Kuer, T., and Hála, K.: The nultifactorial pathogenesis of autoimmune disease. Immunol Lett 16: 249–258, 1987
Xu, Y., Pitcovski, J., Peterson, L., Auffray, C., Bourlet, Y., Gerndt, B.., Nordskog, A. W., Lamont, S. J., and Warner, C. M.: Isolation and characterization of three class II major histocompatibility complex genomic clones from the chicken. J Immunol 142: 2122–2158, 1989
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Address correspondence and offprint tequests to: C. Auffray. The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers M29763 and M29764.
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Zoorob, R., Béhar, G., Kroemer, G. et al. Organization of a functional chicken class II B gene. Immunogenetics 31, 179–187 (1990). https://doi.org/10.1007/BF00211553
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DOI: https://doi.org/10.1007/BF00211553