Abstract
The human ABO blood group system is controlled by alleles at a single locus on chromosome 9. The alleles encode glycosyltransferases, which add different sugar residues to the terminal part of the oligosaccharide core, thus generating the A or B antigens; an allele encoding enzymatically inactive protein is responsible for the blood group O. The A and B antigens are present not only in humans, but also in many other primate species and it has been proposed that the AB polymorphism was established long before these species diverged. Here we provide molecular evidence for the trans-species evolution of the AB polymorphism. Polymerase-chain reaction (PCR) amplification and sequencing has revealed that the critical substitutions differentiating the A and B genes occurred before the divergence of the lineages leading to humans, chimpanzees, gorillas, and orangutans. This polymorphism is therefore at least 13 million years old and is most likely maintained by selection. Comparison of the sequences derived from different species indicates that the difference in enzymatic activities between the A and B transferases is caused by two single nucleotide substitutions responsible for Leu-Met and Gly-Ala replacement at positions 265 and 267 in the polypeptide chains, respectively.
Similar content being viewed by others
References
Clausen, H. and Hakomori, S.: ABH and related histo-blood group antigens; immunochemical differences in carrier isotypes and their distribution. Vox Sang 56: 1–20, 1989
Figueroa, F., Günther, E., and Klein, J.: MHC polymorphism predating speciation. Nature 335: 265–267, 1988
Hakomori, S.: Blood group ABH and Ii antigens of human erythrocytes: chemistry, polymorphism, and their developmental change. Semin Hematol 18: 39–62, 1981
Horton, R. M., Hildebrand, W. H., Martinko, J. M., and Pease, L. R.: Structural analysis of H-2Kf and H-2Kfm1 by using H-2K locus-specific sequences. J Immunol 145: 1782–1787, 1990
Hughes, A. L. and Nei, M.: Pattern of nucleotide substitutions at major histocompatibility complex class I loci reveals overdominant selection. Nature 335: 167–170, 1988
Iorger, 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
Klein, J.: Generation of diversity at MHC loci: Implications for T-cell receptor repertoires. In M. Fougereau and J. Dausset (eds.): Immunology 80: Progress in Immunology IV, pp. 239–253. Academic Press, London, 1990
Klitz, W., Thomson, G., and Baur, M. P.: Contrasting evolutionary histories among tightly-linked HLA loci. Am J Hum Genet 30: 340–349, 1986
Landsteiner, K.: Über Agglutinationserscheinungen normalen menschlichen Blutes. Wein klin Wschr 14: 1132–1134, 1901
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
Maniatis, T., Fritsch, E. F., and Sambrook, J.: Molecular Cloning: A Laboratory Manual. 2nd. Edit., Cold Spring Harbor Laboratory, Cold Spring Harbor, 1989
Martin, R. D.: Primate Origins and Evolution: A Phylogenetic Reconstruction. Chapman and Hall, London, 1990
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 transpecies mode of evolution. EMBO J 7: 2765–2774, 1988
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
Muschel, L. H.: Blood groups, disease, and selection. Bacteriol Rev 30: 427–441, 1966
Oriol, R.: Genetic control of the fucosylation of ABH precursor chains. Evidence for new epistatic interactions in different cells and tissues. J Immunogenet 17: 235–245, 1990
Prokop, O. and Uhlenbruck, G.: Human Blood and Serum Groups. Wiley, New York, 1969
Ruffie, J.: Les donnés de l'immunogénétique et le processus de spéciation chez les primates. C R Acad Sci Paris D 276: 2101–2104, 1973
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
Saitou, N. and Nei, M.: The neighbor-joining method. A new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425, 1987
Socha, W. W. and Ruffie, J.: Blood Groups of Primates: Theory, Practice, Evolutionary Meaning. Alan R. Liss, New York, 1983
Taylor, W. R.: The classification of amino acid conservation. J Theoret Biol 119: 205–218, 1986
Yamamoto, F. and Hakamori, S.: Sugar-nucleotide donor specificity of histo-blood group A and B transferases is based on amino acid substitutions. J Biol Chem 265: 19257–19262, 1990
Yamamoto, F., Clausen, H., White, T., Marken, J., and Hakamori, S.: Molecular genetic basis of the histo-blood group ABO system. Nature 345: 229–233, 1990a
Yamamoto, F., Marken, J., Tsuji, T., White, T., Clausen, H., and Hakamori, S.: Cloning and characterization of DNA complementary to human DUP-GalNAc: Fucα1 →2Galα →3Gal-NAc transferase (histo-blood group A transferase) mRNA. J Biol Chem 265: 1146–1141, 1990b
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Martinko, J.M., Vincek, V., Klein, D. et al. Primate ABO glycosyltransferases: Evidence for trans-species evolution. Immunogenetics 37, 274–278 (1993). https://doi.org/10.1007/BF00187453
Received:
Issue Date:
DOI: https://doi.org/10.1007/BF00187453