, Volume 39, Issue 6, pp 395–403

Molecular characterization of three Mhc class II B haplotypes in the ring-necked pheasant

  • Håkan Wittzell
  • Torbjörn von Schantz
  • Rima Zoorob
  • Charles Auffray
Original Articles


We investigated the class II B genes in free-ranging population of the ring-necked pheasant Phasianus colchicus by a combination of restriction fragment length polymorphism (RFLP), polymerase chain reaction (PCR), and DNA sequencing. Special attention was paid to the variation in the second exon, which encodes the peptide-binding β1-domain. The population was introduced, but it still exhibited major histocompatibility complex polymorphism with at least three segregating class II B haplotypes and consequently six genotypes. We found two class II B genes associated with each haplotype. The class II B genes of birds had until then only been molecularly characterized in the domestic chicken. the pheasant genes were highly variable, although one of the amplified sequences was found in two different haplotypes. Taken together, the most polymorphic positions (residues 37 and 38) were not identical in any of the predicted protein sequences, but all except one of the motifs had already been foud in the domestic chicken. Structurally important features in mammalian class II B genes were generally conserved also in the pheasant sequences, but the loss of a potential salt bridge constituent (Arg72) in several sequences may suggest a slightly different structure of the adjacent parts of the peptide-binding groove. The pheasant genes are most closely related to the so called B-LBII family in the chicken, indicating that this represents a major line of development among avian class II B genes.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Bell, J. I., Denney, D. Jr., Foster, L., Belt, T., Todd, J. A., and McDevitt, H. O. Allelic variation in the DR subregion of the human major histocompatibility complex. Proc Natl Acad Sci USA 84: 6234–6238, 1987Google Scholar
  2. 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, 1988PubMedGoogle Scholar
  3. 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, 1993PubMedGoogle Scholar
  4. 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, 1988CrossRefPubMedGoogle Scholar
  5. Brown, J. H., Jardetzky, T. S., Gorga, J. C., Stern, L. J., Urban, R. G., Strominger, J. L., and Wiley, D. C. Three-dimensional structure of the human class II histocompatibility antigen HLA-DR1. Nature 364: 33–39, 1993CrossRefPubMedGoogle Scholar
  6. Cho, S., Attaya, M., and Monaco, J. J. New class II-like genes in the murine MHC. Nature 353: 573–576, 1991Google Scholar
  7. Cramp, S. and Simmons, K. E. L. Handbook of the Birds of Europe, the Middle East and North Africa, Vol. 2, Oxford University Press, Oxford, 1980Google Scholar
  8. Germain, r. N. and Margulies, D. H. The biochemistry and cell biology of antigen processing and presentation. Annu Rev Immunol 11: 403–450, 1993Google Scholar
  9. Göransson, G., von Schantz, T., Fröberg, I., Helgée, A., and Wittzell, H. Male characteristics, viability and harem size in the pheasant, Phasianus colchicus. Anim Behav 40: 89–104, 1990Google Scholar
  10. 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 the nucleolar organizer. EMBO J 7: 2775–2785, 1988PubMedGoogle Scholar
  11. Hamilton, W. D. and Zuk, M. Heritable true fitness and bright birds: a role for parasites? Science 218: 384–387, 1982Google Scholar
  12. Hashimoto, K., Nakanishi, T., and Kurosawa, Y. Isolation of carp genes encoding major histocompatibility complex antigens. Proc natl Acad Sci USA 87: 6863–6867, 1990Google Scholar
  13. 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, 1986Google Scholar
  14. Hughes, A. L. and Nei, M Nucleotide substitution at major histocompatibility complex class II loci: evidence for over-dominant selection. Proc Natl Acad Sci USA 86: 958–962, 1989PubMedGoogle Scholar
  15. 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, 1992Google Scholar
  16. Kasahara, M., Vazquez, M., Sato, K., McKinney, E. C., and Flajnik, M. F. Evolution of the major histocompatibility complex: isolation of class II A cDNA clones from the cartilaginous fish. Proc Natl Acad Sci USA 89: 6688–6692, 1992Google Scholar
  17. Kaufman, J., Skjødt, K., and Salomonsen, J. The B-G multigene family of the chicken major histocompatibility complex. Crit Rev Immunol 11: 113–143, 1991Google Scholar
  18. Kelly, A. P., Monaco, J. J., Cho, S., and Trowsdale, J. A new human HLA class II-related locus, DM. Nature 353: 571–573, 1991Google Scholar
  19. Klein, J. Natural History of the Major Histocompatibility Complex. John Wiley, New York, 1986Google Scholar
  20. Kroemer, G., Bernot, A., Béhar, G., Chaussé, A.-M., Gastinel, L.-N., Guillemot, F., Park, I., Thoraval, P., Zoorob, R., and Auffray, C. Molecular genetics of the chicken MHC: current status and evolutionary aspects. Immunol Rev 113: 119–145, 1990PubMedGoogle Scholar
  21. Nepom, G. T., and Erlich, H. MHC class-II molecules and auto-immunity. Annu Rev Immunol 9: 493–525, 1991Google Scholar
  22. Nevo, E. and Beiles, A. Selection for class II Mhc heterozygosity by parasites in subterranean mole rats. Experentia 48: 512–515, 1992Google Scholar
  23. Pharr, G. T., Bacon, L. D., and Dodgson, J. B. Analysis of B-Lβ-chain expression in two chicken cDNA libraries. Immunogenetics 37: 381–385, 1993Google Scholar
  24. Rudensky, A. Y., Preston-Hurlburt, P., Hong, S.-C., Barlow, A., and Janeway, C. A. Jr. Sequence analysis of peptides bound to MHC class II molecules. Nature 353: 622–627, 1991Google Scholar
  25. Sambrook, J., Fritsch, E. F., and Maniatis, T. Molecular Cloning: A Laboratory Manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor, 1989Google Scholar
  26. Sanger, F., Nicklen, S., and Coulson, A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977PubMedGoogle Scholar
  27. Sato, K., Flajnik, M. F., Du Pasquier, L., Katagiri, M., and Kasahara, M. Evolution of the MHC: isolation of class IIβ-chain cDNA clones from the amphibian Xenopus laevis. J Immunol 150: 2831–2843, 1993Google Scholar
  28. Tiwari, J. L. and Terasaki, P. I. HLA and Disease Associations, Springer, New York Berlin Heidelberg, 1985Google Scholar
  29. Wu, T. T. and Kabat, E. A. An analysis of the sequences of the variable regions of Bence Jones proteins and myeloma light chains and their implications for antibody complementarity. J Exp Med 132: 211–250, 1970Google Scholar
  30. Xu, Y., Pitcovski, J., Peterson, L., Auffray, C., Bourlet, Y., Gerndt, B. M., Nordskog, A. W., Lamont, S. J., and Warner, C. M. Isolation and characterization of three class II Mhc genomic clones from the chicken. J Immunol 142: 2122–2132, 1989Google Scholar
  31. Zoorob, R., Béhar, G., Kroemer, G., and Auffray, C. Organization of a functional chicken class II B gene. Immunogenetics 31: 179–187, 1990PubMedGoogle Scholar
  32. Zoorob, R., Bernot, A., Martel Renoir, D., Choukri, F., and Auffray, C. Chicken major histocompatibility complex class II B genes: analysis of interallelic and interlocus sequence variance. Eur J Immunol 23: 1139–1145, 1993PubMedGoogle Scholar

Copyright information

© Springer-Verlag 1994

Authors and Affiliations

  • Håkan Wittzell
    • 1
    • 2
  • Torbjörn von Schantz
    • 3
    • 4
  • Rima Zoorob
    • 1
  • Charles Auffray
    • 1
  1. 1.Génétique Moléculaire et Biologie du DéveloppementCNRS UPR 420Villejuif CedexFrance
  2. 2.Department of Theoretical EcologyLund UniversityLundSweden
  3. 3.Molecular Population Biology, The Wallenberg LaboratoyLund UniversityLundSweden
  4. 4.Department of Animal EcologyLund UniversityLundSweden

Personalised recommendations