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Trans-species origin of Mhc-DRB polymorphism in the chimpanzee

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Abstract

Trans-specific evolution of allelic polymorphism at the major histocompatibility complex loci has been demonstrated in a number of species. Estimating the substitution rates and the age of trans-specifically evolving alleles requires detailed information about the alleles in related species. We provide such information for the chimpanzee DRB genes. DNA fragments encompassing exon 2 were amplified in vitro from genomic DNA of ten chimpanzees. The nucleotide sequences were determined and their relationship to the human DRB alleles was evaluated. The alleles were classified according to their positioni in dendrograms and the presence of lineage-specific motifs. Twenty alleles were found at the expressed loci Patr-DRB1,-DRB3, -DRB4, -DRB5, and at the pseudogenes Patr-DRB6, -DRB7; of these, 13 are new alleles. Two other chimpanzee sequences were classified as members of a new lineage tentatively designated DRBX. Chimpanzee counterparts of HLA-DRB1 * 01 and * 04 were not detected. The number of alleles found at individual loci indicates asymmetrical distribution of polymorphism between humans and chimpanzees. Estimations of intra-lineage divergence times suggest that the lineages are more than 30 million year old. Predictions of major chimpanzee DRB haplotypes are made.

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References

  • Andersson, G., Larhammer, D., Widmark, E., Servenius, B., Peterson, P. A., and Rask, L.: Class II genes of the human major histocompatibility complex: Organization and evolutionary relationship of the DRβ genes. J Biol Chem 262: 8748–8758, 1987

    Google Scholar 

  • Arden, B. and Klein, J.: Biochemical comparison of major histocompatibility complex molecules from different subspecies of Mus musculus: Evidence for trans-specific evolution of alleles. Proc Natl Acad Sci USA 79: 2342–2346, 1982

    Google Scholar 

  • Arden, B., Wakeland, E. K., and Klein, J.: Structural comparisons of serologically indistinguishable H-2K-encoded antigen from inbred and wild mice. J Immunol 125: 2424–2428, 1980

    Google Scholar 

  • Biraben, J.-N.: Essai sur l'evolution du nombre des hommes. Population 1: 13–25, 1979

    Google Scholar 

  • Böhme, J., Andersson, G., Möller, E., Peterson, P. A., and Rask, L.: HLA-DRβ genes vary in number between different DR specificities, whereas the number of DQ β genes is constant. J Immunol 135: 2149–2155, 1985

    Google Scholar 

  • Brändle, U., Ono, H., Vincek, V., Klein, D., Golubic, M., Grahovac, B., and Klein, J.: Trans-specific evolution of Mhc-DRB haplotype polymorphism in primates: Organization of DRB genes in the chimpanzee. Immunogenetics 36: 39–48, 1992

    Google Scholar 

  • Breathnach, R. and Chambon, P.: Organization and expression of eucaryotic split genes coding for proteins. Annu Rev Biochem 50: 349–383, 1981

    Article  CAS  PubMed  Google Scholar 

  • Brown, J. H., Jerdetzky, 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

    Article  CAS  PubMed  Google Scholar 

  • Corell, A., Martin-Villa, J.-M., Morales, P., de Juan, M. D., Varela, P., Vicario, J. L., Martinez-Laso, J., and Arnaiz-Villena, A.: Exon-2 nucleotide sequences, polymorphism, and haplotype distribution of a new LA-DRB gene: HLA-DRB6. Mol Immunol 28: 533–543, 1991

    Google Scholar 

  • Corell, A., Morales, P., Varela, Paz-Artal, E., Martin-Villa, J. M., Martinez-Laso, J., and Arnaiz-Villena, A.: Allelic diversity at the primate major histocompatibility complex DRB6 locus. Immunogenetics 36: 33–38, 1992

    Google Scholar 

  • Fan, W., Kasahara, M., Gutnecht, J., Klein, D., Mayer, W. E., Jonker, M., and Klein, J.: Shared class II Mhc polymorphism between human and chimpanzees. Hum Immunol 26: 107–121, 1989

    Google Scholar 

  • Figueroa, F. and Klein, J.: Origins of H-2 polymorphism. In C. S. David (ed.): Antigens, Genes, Molecules, Function, pp. 61–76. Plenum Publishing Corporation, New York 1987

    Google Scholar 

  • Figueroa, F., Günther, E., and Klein, J.: Mhc polymorphism pre-dating speciation. Nature 336: 265–267, 1988

    Google Scholar 

  • Figueroa, F., O'hUigin, C., Inoki, H., and Klein, J.: Primate DRB pseudogenes: clue to the evolutionary origin of the HLA-DR2 haplotype. Immunogenetics 34: 324–337, 1991

    Google Scholar 

  • Gorski, J.: The HLA-DRw8 lineage was generated by a deletion in the DRB region followed by first domain diversification. J Immunol 142: 4041–4045, 1989

    Google Scholar 

  • Gustafsson, K., Brunsberg, U., Sigurdardottir, S., and Andersson, L.: A phylogenetic investigation of MHC class II DRB genes reveals convergent evolution in the antigen binding site. In J. Klein and D. Klein (eds.): Molecular Evolution of the Major Histocompatibility Complex, pp. 119–130. Springer-Verlag, Heidelberg, 1991

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Hughes, A. L. and Nei, M.: Nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Ioerger, T. R., Clark, A. G., and Kao, T.-H.: Polymorphism at the self-incompatibility locus in Solanaceae predates speciation. Proc Natl Acad Sci USA 87: 9732–9735, 1990

    Google Scholar 

  • Jonsson, A.-K., Andersson, L., and Rask, L.: A cellar and functional split in the DRw8 haplotype is due to a single amino acid replacement (DRβ ser57-asp57). Immunogenetics 29: 308–316, 1989

    Google Scholar 

  • Kasahara, M., Klein, D., Vincek, V., Sarapata, D. E., and Klein, J.: The DR subregion of the gorilla major histocompatibility complex: Evidence for linkage disequilibrium conserved across species. Genomics, in press, 1992

  • Kawai, J., Ando, A., Sato, T., Nakatsuji, T., Tsuji, K., and Inoko, H.: Analysis of gene structure and antigen determinants of DR2 antigens using DR gene transfer into mouse L cells. J Immunol 142: 312–317, 1989

    Google Scholar 

  • Kenter, M., Otting, N., Anholts, J., Jonker, M., Schipper, R., and Bontrop, R. E.: Mhc-DRB diversity of the chimpanzee (Pan troglodytes). Immunogenetics 37: 17–27, this issue

  • 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

    CAS  PubMed  Google Scholar 

  • Kimura, M.: The length of time required for a selectively neutral mutant to reach fixation through random frequency drift in a finite population. Genet Res 15: 131–133, 1970

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Klein, J. and Klein, D. (s.): Molecular Evolution of the Major Histocompatibility Complex. NATA ASI Series. Springer-Verlag, Heidelberg, 1991

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Klein, D., Vincek, V., Kasahara, M., Schönbach, C., O'hUigin, C., and Klein, J.: Gorilla major histocompatibility complex-DRB pseudogene orthologous to HLA-DRBVIII. Hum Immunol 32: 211–220, 1991b

    Google Scholar 

  • Klein, J., Satta, Y., O'hUigin, C., Mayer, W. E., and Takahata, N.: Evolution of the primate DRB region. In T. Sasazuki et al. (eds.): HLA 1991, Vol 2. Proceedings of the 11th International Histocompatibility Workshop, Yokohama, Japan. Oxford University Press, Oxford, in press, 1992

    CAS  PubMed  Google Scholar 

  • Larhammer, D., Servenius, B., Rask, L., and Peterson, P. A.: Characterization of an HLA-DR β pseudogene. Proc Natl Acad Sci USA 82: 1475–1479, 1985

    Google Scholar 

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

    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

    Google Scholar 

  • Macdonald, D. (ed.): The Encyclopedia of Mammals, Vol 1, p. 426. George Allen & Unwin, London, 1984

    Google Scholar 

  • Marsh, S. G. E. and Bodmer, J. G.: HLA class II nucleotide sequences, 1991. Immunogenetics 33: 321–334, 1991

    Google Scholar 

  • Martin, R. D.: Primate Origins and Evolution: A Phylogenetic Reconstruction. Chapman and Hall, London, 1990

    Google Scholar 

  • Martinko, J. M., Vincek, V., Klein, D., and Klein, J.: Primate ABO glycosyltransferase: Evidence for trans-species evolution, submitted, 1992

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

    CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Rollini, P., Mach, B., and Gorski, J.: Linkage map of three HLA-DRβ-chain genes: Evidence for a recent duplication event. Proc Natl Acad Sci USA 82: 7197–7201, 1985

    Google Scholar 

  • Saiki, R. K., Gelfand, D. h., Stoffel, S., Scharf, S. J., Higuchi, R., Horn, G. T., Mullis, K. B., and Erlich, H. A.: Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. Science 239: 487–491, 1988

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Sambrook, J., Maniatis, T., and Fritsch, E. F.: Molecular Cloning: A Laboratory Manual. Cold Spring Harbor Press, Cold Spring Harbor, 1989

    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

    CAS  PubMed  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-Verlag, Heidelberg, 1991

    Google Scholar 

  • Satta, Y.: Balancing selection at HLA loci. In N. Takahata and A. G. Clark (eds.): Molecular Paleo-population Biology. Japan Science Society Press/Springer-Verlag, Tokyo, in press, 1992

    Google Scholar 

  • Spies, T., Sorrentino, R., Boss, J. M., Okada, K., and Strominger, J. L.: Structural organization of the DR subregion of the human major histocompatibility complex. Proc Natl Acad Sci USA 82: 5165–5169, 1985

    Google Scholar 

  • Takahata, N., Satta, Y., and Klein, J.: Polymorphism and balancing selection at major histocompatibility loci. Genetics 130: 925–938, 1992

    Google Scholar 

  • Weiss, K. M.: On the number of members of the genus Homo who have ever lived, and some evolutionary implications. Human Biol 56: 637–649, 1984

    Google Scholar 

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Authors and Affiliations

  1. Max-Planck-Institut für Biologie, Abteilung Immungenetik, W-7400, Tübingen, Germany

    Werner E. Mayer, Colm O'hUigin, Zofia Zaleska-Rutczynska & Jan Klein

  2. Department of Microbiology and Immunology, University of Miami School of Medicine, 33101, Miami, FL, USA

    Jan Klein

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  1. Werner E. Mayer
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  2. Colm O'hUigin
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  3. Zofia Zaleska-Rutczynska
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  4. Jan Klein
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Additional information

The nucleotide sequence data reported in this paper have been submitted to the GenBank nucleotide sequence database and have been assigned the accession numbers M94937-M94954.

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Mayer, W.E., O'hUigin, C., Zaleska-Rutczynska, Z. et al. Trans-species origin of Mhc-DRB polymorphism in the chimpanzee. Immunogenetics 37, 12–23 (1992). https://doi.org/10.1007/BF00223540

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