Abstract
To explore genetic mechanisms responsible for major histocompatibility complex (MHC) class I evolution in the artiodactyls, we cloned and sequenced MHC class I cDNAs from a Bos taurus bull heterozygous for cattle MHC (BoLA) class I serological specificities w2 and w30. Four unique cDNAs were found, indicating the presence of at least two MHC class I loci. Analysis of these four cDNAs and all previously published BoLA cDNA sequences suggested that there may be three cattle MHC class I loci. Additionally, comparison of all of the BoLA class I cDNAs to MHC class I cDNAs of other artiodactyls showed that some of the BoLA class I cDNAs were more similar to certain sheep cDNAs than they were to other cattle cDNAs. These data indicate that each BoLA class I locus has evolved independently after an ancestral gene duplication event and that inter-locus segmental exchange o or concerted evolution has not occurred rapidly enough to cause extensive divergence between the orthologous MHC class I loci of sheep and cattle.
Similar content being viewed by others
References
Anonymous. Proceedings of the second international bovine lymphocyte antigen (BoLA) workshop. Anim Blood Groups Biochem Genet 13: 33–53, 1982
Barnstable, C. J., Bodmer, W. F., Brown, G., Galfre, G., Milstein, C., Williams, A. F., and Zeigler, A. Production of monoclonal antibodies to group A erythrocytes, HLA and other human cell surface antigens-new tools for genetic analysis. Cell 14: 9–20, 1978
Bensaid, A. M., Kaushal, A., Baldwin, C. L., Clevers, H., Young, J. R., Kemp, S. J., MacHugh, N. D., Toye, P. G., and Teale, A. J. Identification of expressed bovine class I MHC genes at two loci and demonstration of physical linkage. Immunogenetics 33: 247–254, 1991
Bernoco, D., Lewin, H. A., Andersson, L., Arriens, M. A., Byrns, G., Cwik, S., Davies, C. J., Hines, H. C., Leibold, W., Lie, O., Meggiolaro, D., Oliver, R. A., Ostergard, H., Spooner, R. L., Stewart-Haynes, J. A., Teale, A. J., Templeton, J. W., and Zanotti, M. Joint report of the fourth international bovine lymphocyte antigen (BoLA) workshop. Anim Genet 22: 477–496, 1991
Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennet, W. S., Strominger, J. L., and Wiley, D. C. Structure of human class I histocompatibility antigen, HLA-A2. Nature 329: 506–512, 1987a
Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennet, W. S., Strominger, J. L., and Wiley, D. C. The foreign antigen binding site and T cell recognition regions of class I histocompatibility antigens. Nature 329: 512–518, 1987b
Brown, P., Spooner, R. L., and Clark, A. J. Cloning and characterization of a BoLA class I cDNA clone. Immunogenetics 29: 58–60, 1989
Bull, R. W., Lewin, H. A., Wu, M. C., Peterbaugh, K., Antczak, D., Bernoco, D., Cwik, S., Dam, L., Davies, C., Dawkins, R. L., Dufty, J. H., Gerlach, J., Hines, H. C., Lazary, S., Leibold, W., Leveziel, H., Lie, O., Lindberg, P. G., Meggliolaro, D., Meyer, E., Oliver, R., Ross, M., Simon, M., Spooner, R. L., Stear, M. J., Teale, A. J., and Templeton, J. W. Joint report of the third international bovine lymphocyte antigen (BoLA) workshop, Helsinki, Finland, 27 July 1986. Anim Genet 20: 109–132, 1989
Carroll, R. L. Vertebrate Paleontology and Evolution. Freeman, New York, 1988
Chen, Z. W., McAdam, S. N., Hughes, A. L., Dogan, A. L., Letvin, N. L., and Watkins, D. I. Molecular cloning of orangutan and gibbon MHC class I cDNAs: The HLA-A and -B loci diverged over 30 million years ago. J Immunol 148: 2547–2554, 1992
Chomczynski, P. and Sacchi, N. Single-step method of RNA isolation by acid guanidinium thiocynate-phenol-chloroform extraction. Anal Biochem 162: 156–159, 1987
Dover, G. A. Molecular drive: a cohesive mode of species evolution. Nature 299: 111–117, 1982
Ennis, P. D., Jackson, A. P., and Parham, P. Molecular cloning of bovine class I MHC cDNA. J Immunol 141: 642–651, 1988
Garber, T. L., Hiser, L. M., and Templeton, J. W. Immunochemical and electrophoretic analysis of BoLA class I antigens. Anim Genet 20 (supplement1): 87, 1989
Grossberger, D., Hein, W., and Marcuz, A. Class I major histocompatibility complex cDNA clones from sheep thymus: alternative splicing could make a long cytoplasmic tail. Immunogenetics 32: 77–87, 1990
Guild, B. C. and Strominger, J. L. Human and murine class I MHC antigens share conserved serine 335, the site of HLA phosphorylation in vivo. J Biol Chem 259: 9235–9240, 1984
Gussow, D., Rein, R. S., Meijer, I., de Hoog, W., Seemann, G. H. A., Hochstenbach, F. M., and Ploegh, H. L. Isolation, expression, and the primary structure of HLA-Cw1 and HLA-Cw2 genes: evolutionary aspects. Immunogenetics 25: 313–322, 1987
Hughes, A. L. Independent gene duplications, not concerted evolution, explain relationships among class I MHC genes. Immunogenetics 33: 367–373, 1991
Hughes, A. L. and Nei, M. Pattern of nucleotide substitution at major histocompatibility complex loci reveals overdominant selection. Nature 335: 167–170, 1988
Hughes, A. L. and Nei, M. Evolution of the major histocompatibility complex: independent origins of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6: 559–579, 1989
Joosten, I., Oliver, R. A., Spooner, R. L., Williams, J. L., Hepkema, B. G., Sanders, M. F., and Hensen, E. J. Characterization of class I bovine lymphocyte antigens (BoLA) by one-dimensional isoelectricfocusing. Anim Genet 19: 103–113, 1988
Jukes, T. H. and Cantor, C. R. Evolution of protein molecules. pp. 21–132. In H. N. Munro (ed.): Mammalian Protein metabolism. Academic Press, New York, 1969
Klein, J. The Natural History of the Major Histocompatibility Complex. Wiley, New York, 1987
Klein, J. and Figueroa, G. Evolution of the Major Histocompatibility Complex. CRC Crit Rev Immunol 6: 295–384, 1988
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
Lawlor, D. A., Warren, E., Ward, F. E., and Parham, P. Comparison of class I MHC alleles in humans and apes. Immunol Rev 113: 147–185, 1990
Lawlor, D. A., Warren, E., Taylor, P., and Parham, P. Gorilla class I major histocompatibility complex alleles: Comparison to human and chimpanzee class I. J Exp Med 174: 1491–1509, 1991
Li, W.-H. A statistical test of phylogenies estimated from sequence data. Mol Biol Evol 6: 424–435, 1989
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
Melton, D. A., Krieg, P. A., Rebagliati, M. R., Maniatis, T., Zinn, K., and Green, M. R. Efficient in vitro synthesis of biologically active RNA and RNA hybridization probes from plasmids containing bacteriophage SP6 promotor. Nucleic Acids Res 12: 7035–7056, 1984
Nathenson, S. G., Geliebter, J., Pfaffenbach, G. M., and Zeff, R. A. Murine major histocompatibility complex class-I mutants: molecular analysis and structure-function implications. Annu Rev Immunol 4: 471–502, 1986
Neefjes, J. J., Breur-Vriesendorp, B. S., van Seventer, G. A., Ivanyi, P., and Ploegh, H. L. An improved biochemical method for the analysis of HLA-class I antigens. Definition of new HLA-class I subtypes. Hum Immunol 16: 169–181, 1986
Nei, M. and Gojobori, T. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426, 1986
Nei, M. and Jin, L. Variances of the average numbers of nucleotide substitutions within and between populations. Mol Biol Evol 6: 290–300, 1989
Newman, P. J., Gorski, J., White, G. C., Gidwitz, S., Cretney, C. J., and Aster, R. H. Enzymatic amplification of platelet-specific messenger RNA using the polymerase chain reaction. J Clin Invest 82: 739–743, 1988
Parham, P., Lomen, C. E., Lawlor, D. A., Ways, J. P., Holmes, N., Coppin, H. L., Salter, R. D., Wan, A. M., and Ennis, P. D. The nature of polymorphism in HLA-A,-B, and-C molecules. Proc Natl Acad Sci USA 85: 4005–4009, 1988
Parham, P., Lawlor, D. A., Lomen, C. E., and Ennis, P. D. Diversity and diversification of HLA-A,B,C alleles. J Immunol 142: 3937–3950, 1989
Parker, K. E., Carter, C. A., Murphy, G., and Fabre, J. W. The rat RT.BM1 MHC class I cDNA shows a high level of sequence similarity to the mouse H-2T23 d gene. Immunogenetics 34: 211–213, 1991
Ploegh, H. L., Orr, H. T., and Strominger, J. L. Major histocompatibility antigens: the human (HLA-A,-B,-C) and murine (H2-K, H2-D) class I molecules. Cell 24: 287–299, 1981
Rada, C., Lorenzi, R., Powis, S. J., van den Bogaerde, J., Parham, P., and Howard, J. C. Concerted evolution of class I genes in the major histocompatibility complex of murine rodents. Proc Natl Acad Sci USA 87: 2167–2171, 1990
Saitou, N. and Nei, M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425, 1987
Sanger, F., Nicklen, S., and Coulson, A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74: 5463–5467, 1977
Satz, M. L., Wang, L., Singer, D. S., and Rudikiff, S. Structure and expression of two porcine genomic clones encoding class I MHC antigens. J Immunol 135: 2167–2175, 1985
Savage, D. E. and Russel, D. E. Mammalian Paleofaunas of the World. Addison-Wesley, Reading, Mass., 1983
Spooner, R. L., Oliver, R. A., Sales, D. I., McCoubrey, C. M., Millar, P., Morgan, A. G., Amorena, B., Bailey, E., Bernoco, D., Brandon, M., Bull, R. W., Caldwell, J. S., Cwik, S., van Dam, R. H., Dodd, J., Gahne, B., Grosclaude, F., Hall, J. G., Hines, H., Leveziel, H., Newman, M. J., Stear, M. J., Stone, W. H., and Vaiman, M. Analysis of alloantisera against bovine lymphocytes. Joint report of the 1st international bovine lymphocyte antigen (BoLA) workshop. Anim Blood Groups Biochem Genet 10: 63–86, 1979
Stam, N. J., Spits, H., and Ploegh, H. L. Monoclonal antibodies raised against denatured HLA-B locus heavy chains permit biochemical characterization of certain HLA-C locus products. J Immunol 137: 2299–2306, 1986
Stear, M. J., Newman, M. J., and Nicholas, F. W. Two closely linked loci and one apparently independent locus code for bovine lymphocyte antigens. Tissue Antigens 20: 289–299, 1982
Steinmetz, M., Winoto, A., Minard, K., and Hood, L. Clusters of genes encoding mouse transplantation antigens. Cell 28: 489–498, 1982
Terasaki, P. I., Bernoco, D., Park, M. S., Ozturk, G., and Iwaki, Y. Microdroplet testing for HLA-A,-B,-C and-D antigens. Am J Clin Pathol 69: 103–120, 1978
Townsend, A. R. M., Rothbard, J., Gotch, F. M., Bahadur, G., Wraith, D., and McMichael, A. J. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44: 959–968, 1986
Toye, P. G., MacHugh, N. D., Bensaid, A. M., Alberti, S., Teale, A. J., and Morrison, W. I. Transfection into mouse L cells of genes encoding two serologically and functionally distinct bovine class I MHC molecules from a MHC-homozygous animal: evidence for a second class I locus in cattle. Immunology 70: 20–26, 1990
Wan, A. M., Ennis, P., Parham, P., and Holmes, N. The primary structure of HLA-A32 suggests a region involved in formation of the Bw4/Bw6 epitopes. J Immunol 137: 3671–3674, 1986
Watkins, D. I., Kannagi, M., Stone, M. E., and Letvin, N. L. Major histocompatibility complex class I molecules of nonhuman primates. Eur J Immunol 18: 1425–1432, 1988
Watkins, D. I., Shadduck, J. A., Stone, M. E., Lewin, H. A., and Letvin, N. L. Isoelectric focusing of bovine major histocompatibility complex class I molecules. J Immunogenetics 16: 233–245, 1989
Watkins, D. I., Chen, Z. W., Hughes, A. L., Evans, M. E., Tedder, T. F., and Letvin, N. L. Evolution of the MHC class I genes of a New World primate from ancestral homologues of human nonclassical genes. Nature 346: 60–63, 1990
Watkins, D. I., Garber, T. L., Chen, Z. W., Toukatly, G., Hughes, A. L., and Letvin, N. L. Unusually limited nucleotide sequence variation of the expressed major histocompatibility complex class I genes of a New World primate species (Saguinus oedipus). Immunogenetics 33: 79–89, 1991a
Watkins, D. I., Chen, Z. W., Garber, T. L., Hughes, A. L., and Letvin, N. L. Segmental exchange between MHC class I genes in a higher primate. Recombination in the gorilla between the ancestor of a human non-functional gene and an A locus gene. Immunogenetics 34: 185–191, 1991b
Weiss, E. H., Mellor, A., Golden, L., Fahrner, K., Simpson, E., Hurst, J., and Flavell, R. A. The structure of a mutant H-2 gene suggests that the generation of polymorphism in H-2 genes may occur by gene converion-like agents. Nature 301: 671–674, 1983
Weiss, E. H., Golden, L., Fahrner, K., Mellor, A. L., Devlin, J. J., Bullman, H., Tiddens, H., Bud, H., and Flavell, R. A. Organization and evolution of the class I gene family in the major histocompatibility complex of the C57BL/10 mouse. Nature 310: 650–655, 1984
Wu, C.-I. and Li, W. H. Evidence for higher rates of nucleotide substitution in rodents than in man. Proc Natl Acad Sci USA 82: 1741–1745, 1985
Zemmour, J., Ennis, P. D., Parham, P., and Dupont, B. Comparison of the structure of HLA-Bw47 to HLA-B13 and its relationship to 21-hydroxylase deficiency. Immunogenetics 21: 281–287, 1988
Zinkernagel, R. M. and Doherty, P. C. Restriction of T cell mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semisyngeneic system. Nature 248: 701–702, 1974
Author information
Authors and Affiliations
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 L02832–L02835.
Correspondence to: T. L. Garber at the present address.
Rights and permissions
About this article
Cite this article
Garber, T.L., Hughes, A.L., Letvin, N.L. et al. Sequence and evolution of cattle MHC class I cDNAs: concerted evolution has not taken place in cattle. Immunogenetics 38, 11–20 (1993). https://doi.org/10.1007/BF00216385
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00216385