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Trans-species polymorphism of class IIMhc loci in danio fishes

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Abstract

A characteristic feature of the major histocompatibility complex (Mhc) polymorphism in mammals is the existence of allelic lineages shared by related species. This trans-species polymorphism has thus far been documented only in primates, rodents, and artiodactyls. In this communication we provide evidence that it also exists in cyprinid (bony) fishes at the class IIA andB loci coding for the α and β polypeptide chains of the class II α: β heterodimers. The study has focused on three species of the family Cyprinidae, subfamily Rasborinae: the zebrafish (Danio rerio), the giant danio (D. malabaricus), and the pearl danio (D. albolineatus). The polymerase chain reaction was used to amplify and then sequence intron 1 and exon 2 of the class IIB loci and exon 2 of the class IIA loci in these species. Phylogenetic analysis of the sequences revealed the existence of allelic lineages whose divergence predates the divergence of the three species at both theA andB loci. The lineages at theB locus in particular are separated by large genetic distances. The polymorphism is concentrated in the peptide-binding region sites and is apparently maintained by balancing selection. Sharing of this uniqueMhc feature by both bony fishes and mammals suggests that the main function of theMhc (presentation of peptides to T lymphocytes) has not changed during the last 400 million years of its evolution.

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References

  • Arden, B. and Klein, J. Biochemical comparison of major histocom-patibility complex molecules from different subspecies ofMus musculus: evidence for trans-spefific evolution of alleles.Proc Natl Acad Sci USA 79: 2342–2346, 1982

    Article  PubMed  CAS  Google Scholar 

  • Barman, R. P. A taxonomic revision of the Indo-Burmese species ofDanio Hamilton Buchanan (Pisces: Cyprinidae).Rec Zool Surv India 137: 1–91, 1991

    Google Scholar 

  • Brown, J. H., Jardetzky, T. S., 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.

    Article  PubMed  CAS  Google Scholar 

  • 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, 1993

    Article  PubMed  CAS  Google Scholar 

  • Fan, W., Kasahara, M., Gutknecht, J., Klein, D., Mayer, W. E., Jonker, M., and Klein, J. Shared class IIMhc polymorphisms between human and chimpanzees.Hum Immunol 26: 107–121, 1989

    Article  PubMed  CAS  Google Scholar 

  • Figueroa, F. and Klein, J. Origin of H-2 polymorphism.In C. S. David (ed.):H-2 Antigens, Genes, Molecules, Function. Series A: Life Sciences 144, pp. 61–76, Plenum Publishing Corporation, 1987

  • Figueroa, F., Günther, E., and Klein, J. MHC polymorphism pre-dating speciation.Nature 335: 265–267, 1988

    Article  PubMed  CAS  Google Scholar 

  • Grimholt, U., Olsaker, I., De Vries Linstroem, C., and Lie, Ø. A study of variability in the MHC class II β1 and the MHC class I α2 domain exons of Atlantic salmon (Salmo salar).Anim Genet 25: 147–153, 1994.

    Article  PubMed  CAS  Google Scholar 

  • Gyllensten, U., Sundvall, M., Ezcurra, I., and Erlich, H. A. Genetic diversity at class II DRB loci of primate Mhc.J Immunol 146: 4368–4376, 1991

    PubMed  CAS  Google Scholar 

  • Gyllensten, U. B. and Erlich, H. A. Ancient roots for polymorphism at the HLA-DQα locus in primates.Proc Natl Acad Sci USA 86: 9986–9990, 1989

    Article  PubMed  CAS  Google Scholar 

  • Hamilton-Buchanan, F.An Account of the Fishes Found in the River Ganges and its Branches, Archibald Constable, Edinburgh 1822.

    Google Scholar 

  • Hardee, J. J., Godwin, U., Benedetto, R., and McConnell, T. J. Major histocompatibility complex class IIA gene polymorphism in the striped bass.Immunogenetics 41: 229–238, 1995

    Article  PubMed  CAS  Google Scholar 

  • Higgins, D. G., Bleasby, A. J., and Fuchs, R. CLUSTAL V: improved software for multiple sequences aligment.Cabios 8: 189–191, 1992.

    PubMed  CAS  Google Scholar 

  • Hughes, A. L. and Nei, M. Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.Nature 355: 167–170, 1988

    Article  Google Scholar 

  • Hughes, A. L. and Nei, M. Nucleotide substitution at major histocompability complex class II loci: evidence for overdominant selection.Proc Natl Acad Sci USA 86: 958–962, 1989

    Article  PubMed  CAS  Google Scholar 

  • Kenter, M., Otting, N., Anholts, J., Jonker, M., Schipper, R., and Bontrop, R. E.Mhc-DRB diversity of the chimpanzee.Immunogentics 37: 1–11, 1992

    CAS  Google Scholar 

  • Kimura, M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences.J Mol Evol 16: 111–120, 1980

    Article  PubMed  CAS  Google Scholar 

  • Klein, D., Ono, H., O'hUigin, C., Vincek, V., Goldschmidt, T., and Klein, J. Extensive MHC variability in cichlid fishes of Lake Malawi.Nature 364: 330–334, 1993

    Article  PubMed  CAS  Google Scholar 

  • Klein, J. Generation of diversity at MHC loci: implications for T-cell receptor repertoires.In M. Fougereau and L. Dausset (eds.):Immunology 80, pp. 239–253. Academic Press, London, 1980

    Google Scholar 

  • Klein, J.Natural History of the Major Histocompatibility Complex, John Wiley, New York, 1986

    Google Scholar 

  • Klein, J. Origin of major histocompatibility complex polymorphism: the trans-species hypothesis.Hum Immunol 19: 155–162, 1987

    Article  PubMed  CAS  Google Scholar 

  • Klein, J. and Figueroa, F. Evolution of the major histocompatibility complex.CRC Crit Rev Immunol 6: 295–386, 1986

    CAS  Google Scholar 

  • Klein, J. and O'hUigin, C. Class II BMhc motifs in an evolutionary perspective.Immunol Rev 143: 89–111, 1995

    Article  PubMed  CAS  Google Scholar 

  • Klein, J. and Takahata, N. The major histocompatibility complex and the quest for origins.Immunol Rev 113: 5–25, 1990

    Article  PubMed  CAS  Google Scholar 

  • Klein, J., Bontrop, R. E., Dawkins, R. L., Erlich, H. A., Gyllensten, E. B., Heise, E. R., Jones, P. P., Parham, P., Wakeland, E. K., and Watkins, D. I. Nomenclature for the major histocompatibility complexes of different species: a proposal.Immunogenetics 31: 217–219, 1990a

    PubMed  CAS  Google Scholar 

  • Klein, J., Kasahara, M., Gutknecht J., and Figueroa, F. Origin and function ofMhc polymorphism.Chem Immunol 49: 35–50, 1990b

    Article  PubMed  CAS  Google Scholar 

  • Klein, J., Satta, Y., O'hUigin, C., and Takahata, N. The molecular descent of the major histocompatibility complex.Annu Rev Immunol 11: 269–295, 1993

    Article  PubMed  CAS  Google Scholar 

  • Kumar, S., Tamura, K., and Nei, M.MEGA: Molecular Evolutionary Genetic Analysis Version 1.0 The Pennsylvania State University, University Park, PA, 1993

    Google Scholar 

  • Kupfermann, H., Mayer, W. E., O'hUigin, C., Klein, D., and Klein, J. Shared polymorphism between gorilla and human major histocompatibility complexDRB loci.Hum Immunol 34: 267–278, 1992

    Article  PubMed  CAS  Google Scholar 

  • Laird, P. W., Zijderveld, A., Linders, K., Rudnicki, M. A., Jaenisch, R., and Berns, A. Simplified mammalian DNA isolation procedure.Nucleic Acids Res 19: 4293, 1991

    Article  PubMed  CAS  Google Scholar 

  • Lawlor, D. A., Ward, F. E., Ennis, P. D., Jackson, A. P., and Parham, P.HLA-A and-B polymorphism predate the divergence of humans and chimpanzees.Nature 335: 268–271, 1988

    Article  PubMed  CAS  Google Scholar 

  • Li, W.-H., Wu, C.-I., and Luo, C.-C. A new method for estimating synonymous and nonsynonymous rates of nucleotide substitution considering the relative likelihood of nucleotide and codon changes.Mol Biol Evol 2: 150–174, 1985

    PubMed  Google Scholar 

  • Maniatis, T., Fritsch, E. F., and Sambrook, J.,Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, 1991

    Google Scholar 

  • Mayer, W. E., Jonker, M., Klein, D., Ivanyi, P., van Seventer, G., and Klein, J. Nucleotide sequences of chimpanzeeMhc, class I alleles: evidence for trans-species mode of evolution.EMBO J 7: 2765–2774, 1988

    PubMed  CAS  Google Scholar 

  • Mayer, W. E., O'hUigin, C., Zaleska-Rutczynska, Z., and Klein, J. Trans-species origin ofMhc-DRB polymorphism in the chimpanzee.Immunogenetics 37: 12–23, 1992

    Article  PubMed  CAS  Google Scholar 

  • McConnell, T. J., Talbot, W. S., McIndoe, R. A., and Wakeland, E. K. The origin ofMhc class II gene polymorphism within the genusMus.Nature 332: 651–654, 1988

    Article  PubMed  CAS  Google Scholar 

  • Meyer, A., Biermann, C. H., and Ortí, G. The phylogenetic position of the zebrafish (Danio rerio), a model system in developmental biology: an invitation to the comparative method.Proc R Soc Lond (Biol) 252: 231–236, 1993

    Article  CAS  Google Scholar 

  • Meyer, A., Ritchie, P. A., and Witte, K.-E. Predicting developmental processes from evolutionary patterns: a molecular phylogeny of the zebrafish (Danio rerio) and its relatives.Phil Trans R Soc Lond (Biol) 349: 103–111, 1995

    Article  Google Scholar 

  • Nelson, J. S.Fishes of the World, John Wiley, New York, 1984

    Google Scholar 

  • O'hUigin, C. Quantifying the degree of convergence in primate Mhc-DRB genes.Immunol Rev 143: 123–140, 1995

    Article  PubMed  Google Scholar 

  • Ono, H., Klein, D., Vincek, V., Figueroa, F., O'hUigin, C., Tichy, H., and Klein, J. Major histocompatibility complex class II genes of zebrafish.Proc Natl Acad Sci USA 89: 11886–11890, 1992

    Article  PubMed  CAS  Google Scholar 

  • Ono, H., O'hUigin, C., Tichy, H., and Klein, J. Major-histocompatibility-complex variation in two species of cichlid fishes from Lake Malawi.Mol Biol Evol 10: 1060–1072, 1993

    PubMed  CAS  Google Scholar 

  • Ono, H., O'hUigin, C., Vincek, V., and Klein, J. Exon-intron organization of fish major histocompatibility complex class IIB genes.Immunogenetics 38: 223–234, 1993b

    PubMed  CAS  Google Scholar 

  • Ono, H., O'hUigin, C., Vincek, V., Stet, R. J. M., Figueroa, F., and Klein, J. New β chain-encodingMhc class II genes in the carp.Immunogenetics 38: 146–169, 1993c

    PubMed  CAS  Google Scholar 

  • Saitou, N. and Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees.Mol Biol Evol 4: 406–425, 1987

    PubMed  CAS  Google Scholar 

  • Sanger, F., Nicklen, S., and Coulson, A. R. DNA sequencing with chain-terminating inhibitors.Proc Natl Acad Sci USA 74: 5463–5467, 1977

    Article  PubMed  CAS  Google Scholar 

  • Sato, A., Figueroa, F., O'hUigin, C., Reznick, D. N., and Klein, J. Major histocompatibility complex genes of the guppy,Poecilia reticulata: identification and cloning.Immunogenetics 43: 38–49, 1996

    PubMed  CAS  Google Scholar 

  • Satta, Y., Takahata, N., Schönbach, C., Gutknecht, J., and Klein, J. Calibrating evolutionary rates at major histocompatibility complex loci.In J. Klein and D. Klein (eds.):Molecular Evolution of the Major Histocompatibility Complex, pp. 51–62, Springer, Heidelberg, 1991

    Google Scholar 

  • Satta, Y., O'hUigin, C., Takahata, N., and Klein, J. The synonymous substitution rate of the major histocompatibility complex loci in primates.Proc Natl Acad Sci USA 90: 7480–7484, 1993

    Article  PubMed  CAS  Google Scholar 

  • Slierendregt, B. L., van Noort, J., Bakas, R. M., Otting, N., Jonker, M., and Bontrop, R. E. Evolutionary stability of trans-species major histocompatibility complex class IIDRB lineages in man and rhesus monkey.Hum Immunol 35: 29–39, 1992

    Article  PubMed  CAS  Google Scholar 

  • Stanley, S. M. A theory of evolution above the species level.Proc Natl Acad Sci USA 72: 646–650, 1975

    Article  PubMed  CAS  Google Scholar 

  • Sültmann, H., Mayer, W. E., Figueroa, F., O'hUigin, C., and Klein, J. ZebrafishMhc class II α chain-encoding genes: polymorphism, expression, and function.Immunogenetics 38: 408–420, 1993

    Article  PubMed  Google Scholar 

  • Sültmann, H., Mayer, W. E., Figueroa, F., O'hUigin, C., and Klein, J. Organization ofMhc class IIB genes in the zebrafish (Brachydanio rerio).Genomics 23: 1–14, 1994a

    Article  PubMed  Google Scholar 

  • Sültmann, H. Organisation and Charakterisierung vonMhc Klasse IIA undB Genen des Zebrabärblings (Brachydanio rerio). Universität Tübingen, 1994b

  • Wakeland, E. K., Tarruzzee, R. W., Lu, C.-C., Potts, W., McIndoe, R. A., Talbot, W. S., and McConnell, T. J.In C. S. David (ed.):H-2 Antigens, Genes, Molecules, Function, pp. 139–153, Plenum Press, New York, 1987

    Google Scholar 

  • Walker, R. B. and McConnell, T. J. Variability in anMhcMosa class II β chain-encoding gene in the striped bass (Morone saxatilis).Dev Comp Immunol 18: 325–342, 1994

    Article  PubMed  CAS  Google Scholar 

  • 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, 1970

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Abteilung Immuingenetik, Max-Planck Institut für Biologie, Corrensstr. 42, D-72076, Tübingen, Germany

    Colm O'hUigin & Jan Klein

  2. Department of Microbiology and Immunology, University of Miami School of Medicine, 33106, Miami, FL, USA

    Robert Graser, Vladimir Vincek & Jan Klein

  3. Department of Ecology and Evolution, State University of New York at Stony Brook, 11794-6246, Stony Brook, NY, USA

    Axel Meyer

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  1. Robert Graser
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  4. Axel Meyer
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  5. Jan Klein
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Graser, R., O'hUigin, C., Vincek, V. et al. Trans-species polymorphism of class IIMhc loci in danio fishes. Immunogenetics 44, 36–48 (1996). https://doi.org/10.1007/BF02602655

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