Abstract
Little is known about the major histocompatibility (Mhc) genes of birds in different taxonomic groups or about how Mhc genes may be organized in avian species divergent by evolution or habitat. Yet it seems likely that much might be learned from birds about the evolution, organization, and function of this intricate complex of polymorphic genes. In this study a close relative of the chicken, the ring-necked pheasant (Phasianus colchicus), was examined for the presence and organization of Mhc B-G genes. The patterns of restriction fragments revealed by chicken B-G probes in Southern hybridizations and the patterns of pheasant erythrocyte polypeptides revealed in immunoblots by antisera raised against chicken B-G polypeptides provide genetic, molecular, and biochemical data confirming earlier serological evidence for the presence of B-G genes in the pheasant, and hence, the presence of a family of B-G genes in at least a second species of birds. The high polymorphism exhibited by the pheasant B-G gene family allowed genetic differences among individuals within the small experimental population in this study to be detected easily by restriction fragment patterns. Further evidence was found for the organization of the pheasant Mhc class I and class II genes into genetically independent clusters. Whether these gene clusters are fully comparable to the B and Rfp-Y systems in the chicken or whether yet another organization of Mhc genes has been encountered in the pheasant remains to be determined.
Similar content being viewed by others
References
Alberts, C. and Ober, S. Genetic variability in the major histocompatibility complex: a review of non-pathogen mediated selective mechanisms. Yearbook of Physical Anthropology 36: 71–89, 1993
Bacon, L. D. Influence of the major histocompatibility complex on disease resistance and productivity. Poult Sci 66: 802–811, 1987
Bloom, S. E., Delany, M. E., and Muscarella, D. E. Constant and variable features of avian chromosomes. In R. J. Etches and A. M. V. Gibbons (eds.): Manipulation of the Avian Genome, pp. 39–59, CRC Press, Boca Raton, 1993
Briles, W. E. and Briles, R. W. Identification of haplotypes of the chicken major histocompatibility complex (B). Immunogenetics 15: 449–459, 1982
Briles, W. E., Briles, R. W., Toffs, R. E., and Stone, H. A. Resistance to a malignant lymphoma in chickens is mapped to subregion of major histocompatibility (B) complex. Science 219: 977–979, 1983
Briles, W. E., Goto, R. M., Auffray, C., and Miller, M. M. A polymorphic system related to but genetically independent of the chicken major histocompatibility complex. Immunogenetics 37: 408–414, 1993
Briles, W. E., Stone, H. A., and Cole, R. K. Marek's disease: Effects of B histocompatibility alloalleles in resistant and susceptible chicken lines. Science 195: 193–195, 1977
Dominquez-Steglich, M., Auffray, C., and Schmid, M. Linkage of the chicken MHC to the nucleolus organizer region visualized using non-isotopic in situ hybridization. J Hered 82: 503–505, 1991
Feinberg, A. P. and Vogelstein, B. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13, 1983
Gardinier, M. V., Amiquet, P., Linington, C., and Matthieu, J.-M. Myelin/oligodendrocyte glycoprotein is a unique member of the immunoglobulin superfamily. J Neuroscience Res 33: 177–187, 1992
Golemboski, K. A., Taylor, Jr., R. L., Briles, R. W., and Dietert, R. R. Inflammatory function of macrophages from chickens with B-recombinant haplotypes. Avian Pathol 24: 347–352, 1995
Goto, R., Miyada, C. G., Young, S., Wallace, R. B., Abplanalp, H., Bloom, S. E., Briles, W. E., and Miller, M. M. Isolation of a cDNA clone from the B-G subregion of the chicken histocompatibility (B) complex. Immunogenetics 27: 102–109, 1988
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 IIB genes are closely linked to the class I genes and the nucleolar organizer. EMBO J 7: 2775–2785, 1988
Helm-Bychowski, K. M. and Wilson, A. C. Rates of nuclear DNA evolution in pheasant-like birds: evidence from restriction maps. Proc Natl Acad Sci USA 83: 688–692, 1986
Hepkema, B. G., Blankert, J. J., Albers, G. A. A., Tilanus, M. G. J., Egberts, E., van der Zijpp, A. J., and Hensen, E. J. Mapping of susceptibility to Marek's disease within the major histocompatibility (B) complex by refined typing of white leghorn chickens. Anim Genetics 24: 283–287, 1994
Holton, T. A. and Graham, M. W. A simple and efficient method for direct cloning of PCR products using ddT-tailed vectors. Nucleic Acids Res 19: 1156, 1991
Hughes, A. L. and Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988
Hughes, A. L. and Nei, M. Nucleotide substitution at major histocompatibility complex class II loci: evidence for overdominant selection. Proc Natl Acad Sci USA 86: 958–962, 1989
Jack, L. J. W. and Mather, I. H. Cloning and analysis of cDNA encoding bovine butyrophilin, an apical glycoprotein expressed in mammary tissue and secreted in association with the milk-fat globule membrane during lactation. J Biol Chem 265: 14481–14486, 1990
Jarvi, S. I. and Briles, W. E. Identification of the major histocompatibility complex in the ring-necked pheasant, Phasianus colchicus. Anim Genet 23: 211–220, 1992
Jarvi, J. I., Goto, R. M., Gee, G. F., Briles, W. E., and Miller, M. M. Approaches to the study of the major histocompatibility complex in birds. In F. Coudert (ed.): Avian Immunology in Progress, pp. 160–164, Institut National de la Recherche Agronomique, Paris, 1993
Kaufman, J., Salomonsen, J., Skjødt, K., and Thorpe, D. Size polymorphism of chicken major histocompatibility complex-encoded B-G molecules is due to length variation in the cytoplasmic heptad repeat region. Proc Natl Acad Sci USA 87: 8277–8281, 1990
Kronenberg, M., Brines, R., and Kaufman, J. MHC evolution: a long term investment in defense. Immunol Today 15: 4–6, 1994
L'Abbe, D., Belmaaza, A. B., Decary, F., and Chartrand, P. Elimination of heteroduplex artifacts when sequencing HLA genes amplified by polymerase chain reaction (PCR). Immunogenetics 35: 395–397, 1992
Miller, M. M., Abplanalp, H., and Goto, R. Genotyping chickens for the B-G subregion of the major histocompatibility complex using restriction fragment length polymorphisms. Immunogenetics 28: 374–379, 1988
Miller, M. M. and Goto, R. PCR-SSCP: A method for studying the polymorphism of the B-G antigens of the chicken major histocompatibility complex. In F. Coudert (ed.): Avian Immunology in Progress, pp. 160–164, Institut National de la Recherche Agronomique, Paris, 1993
Miller, M. M., Goto, R., and Abplanalp, H. Analysis of the B-G antigens of the chicken MHC by two-dimensional gel electrophoresis. Immunogenetics 20: 373–385, 1984
Miller, M. M., Goto, R., Young, S., Liu, J., and Hardy, J. Antigens similar to major histocompatibility complex B-G are expressed in the intestinal epithelium in the chicken. Immunogenetics 32: 45–50, 1990
Miller, M. M., Goto, R., Young, S., Chirivella, J., Hawke, D., and Miyada, C. G. Immunoglobulin variable-region-like domains of diverse sequence within the major histocompatibility complex of the chicken. Proc Natl Acad Sci USA 88: 4377–4381, 1991
Miller, M. M., Goto, R., Zoorob, R., Auffray, C., and Briles, W. E. Southern hybridizations reveal regions of homology shared by Rfp-Y and major histocompatibility B complex class I (B-F) and class II (B-L) genes. Immunogenetics 39: 71–73, 1994a
Miller, M. M., Goto, R., Bernot, A., Zoorob, R., Auffray, C., Bumstead, N., and Briles, W. E. Two Mhc class I and two Mhc class II genes map to the chicken Rfp-Y system outside the B complex. Proc Natl Acad Sci USA 91: 4397–4401, 1994b
Orita, M., Suzuki, Y., Sekiiya, T., and Hayashi, K. Rapid and sensitive detection of point mutations and DNA polymorphisms using the polymerase chain reaction. Genomics 5: 874–879, 1989
Oto, M., Miyake, S., and Yuasa, Y. Optimization of nonradioisotopic single strand conformation polymorphism analysis with a conventional minislab gel electrophoresis apparatus. Anal Biochem 213: 19–22, 1993
Pham-Dinh, D., Mattei, M. G., Nussbaum, J.-L., Roussel, G., Pontarotti, P., Roeckel, N., Mather, I. H., Artzt, K., Lindahl, K. F., and Dautigny, A. Myelin/oligodendrocyte glycoprotein is a member of a subset of the immunoglobulin superfamily encoded within the major histocompatibility complex. Proc Natl Acad Sci USA 90: 7990–7994, 1993
Plachý, J., Pink, J. R., and Halá, K. Biology of the chicken MHC (B complex). Crit Rev Immunol 12: 47–79, 1992
Salomonsen, J., Dunon, D., Skjødt, K., Thorpe, D., Vainio, O., and Kaufman, J. Chicken major histocompatibility complex-encoded B-G antigens are found on many cell types that are important for the immune response. Proc Natl Acad Sci USA 88: 1359–1363, 1991
Schat, K. A., Taylor, Jr., R. L., and Briles, W. E. Resistance of Marek's disease in chickens with recombinant haplotypes of the major histocompatibility (B) complex. Poult Sci 73: 502–508, 1994
Shamansky, L., Long, X., and Miller, M. M. Isolation and characterization of reticuloendotheliosis virus transformed bone marrow cells from congenic lines of chickens differing at the MHC. FASEB J 2: A482, 1988
Shiina, T., Ando, A., Imanishi, T., Kawata, H., Hanzawa, K., Gojobori, T., Inoko, H., and Watanabe, S. Isolation and characterization of cDNA clones for Japanese quail (Coturnix japonica) major histocompatibility complex (MhcCoja) class I molecules. Immunogenetics 42: 213–216, 1995
Tegelstrom, H. and Ryttman, H. Chromosomes in birds (Aves): evolutionary implications of macro- and micro-chromosome numbers and lengths. Hereditas 94: 225–233, 1981
Trowsdale, J. “Both man & bird & breast”: comparative organization of MHC genes. Immunogenetics 41: 1–17, 1995
Vernet, C., Boretto, J., Mattéi, M.-G., Takahashi, M., Jack, L. J. W., Mather, I. H., Rouquier, S., and Pontarotti, P. Evolutionary study of multigenic families mapping close to the human MHC class I region. J Mol Evol 37: 600–612, 1993
Vincek, V., Klein, D., Glaser, R. T., Figueroa, F., O'hUigin, C., and Klein, J. Molecular cloning of major histocompatibility complex class II B gene cDNA from the Bengalese finch Lonchura striata. Immunogenetics 42: 262–267, 1995
Wedekind, C., Seebeck, T., Bettens, F., and Paepke, A. J. MHC-dependent mate preferences in humans. Proc R Soc Lond (Biol) 260: 245–249, 1995
Witzell, H., von Schantz, T., Zoorob, R., and Auffray, C. Molecular characterization of three Mhc class II B haplotypes in the ring-necked pheasant. Immunogenetics 39: 395–403, 1994
Witzell, H., von Schantz, T., Zoorob, R., and Auffray, C. Rfp-Y-like sequences assort independently of pheasant Mhc genes. Immunogenetics 42: 68–71, 1995
Zoorob, R., Béhar, G., Kroemer, G., and Auffray, C. Organization of a functional chicken class II B gene. Immunogenetics 31: 179–187, 1990
Zoorob, R., Bernot, A., Renoir, D., Choukri, F., and Auffray, C. Chicken MHC class II B genes: analysis of interallelic and interlocus sequence variance. Eur J Immunol 23: 1139–1145, 1993
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Jarvi, S.I., Goto, R.M., Briles, W.E. et al. Characterization of Mhc genes in a multigenerational family of ring-necked pheasants. Immunogenetics 43, 125–135 (1996). https://doi.org/10.1007/BF00176673
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00176673