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Independent gene duplications, not concerted evolution, explain relationships among class I MHC genes of murine rodents

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Abstract

It has been claimed that class I MHC loci are homogenized within species by frequent events of interlocus genetic exchange (“concerted evolution”). Evidence for this process includes the fact that certain rat class I loci (including RT1.A) located centromeric to class II and class III are more similar to each other than to the mouse K locus (also centromeric to class II/class III). However, a phylogenetic analysis showed that the rat RT1.A locus is in fact orthologous to the mouse K1 pseudogene (also centromeric to class II/class III). Thus, two independent events of translocation of genes centromeric to class II/class III have occurred in the history of the murine rodents, at least one of which (involving the ancestor of RT1.A and K1) occurred prior to the divergence of rat and mouse. It was also found that the rat nonclassical class I gene RT.BM1 is orthologous to the mouse nonclassical gene 37 d. These results argue that intelocus genetic exchange does not occur at a rate sufficient to cause within-species homogenization of class I MHC loci.

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References

  • Baltimore, D.: Gene conversion: some implications for immunoglobulin genes. Cell 24: 592–594, 1981

    Google Scholar 

  • Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, W. S., Stromigner, J. L., and Wiley, D. C.: Structure of the human class I histocompatibility antigen, HLA-A2. Nature 329: 506–512, 1987a

    Google Scholar 

  • Bjorkman, P. J., Saper, M. A., Samraoui, B., Bennett, 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

    Google Scholar 

  • Devlin, J. J., Weiss, E. H., Paulson, M., and Flavell, R. A.: Duplicated gene pairs and alleles of class I genes in the Qa2 region of the murine major histocompatibility complex: a comparison. EMBO J 4: 3203–3207, 1985

    Google Scholar 

  • Fisher, D. A., Hunt, S. W. III, and Hood, L.: Structure of a gene encoding a murine thymus leukemia antigen and organization of Tla genes in the BALB/c mouse. J Exp Med 162: 528–545, 1985

    Google Scholar 

  • Hedley, M. L., Hunt, S. W. III, Brorson, K. A., Andris, J. S., Hood, L., Forman, J., and Tucker, P. W.: Analysis of D2 d: A D-region class I gene. Immunogenetics 29: 359–365, 1989

    Google Scholar 

  • Howard, J. G.: MHC organization in the rat: evolutionary considerations. In G. Kelsoe and D. H. Schulze (eds.): Evolution and Vertebrate Immunity, pp. 397–427, University of Texas Press, Austin, 1987

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Hughes, A. L. and Nei, M.: Evolution of the major histocompatibility complex: independent origin of nonclassical class I genes in different groups of mammals. Mol Biol Evol 6: 559–579, 1989a

    Google Scholar 

  • Hughes, A. L. and Nei, M.: Ancient interlocus exon exchange in the history of the HLA-A locus. Genetics 122: 681–686, 1989b

    Google Scholar 

  • Hughes, A. L. and Nei, M.: Evolutionary relationships of class II major-histocompatibility-complex genes in mammals. Mol Biol Evol 7: 491–514, 1990

    Google Scholar 

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

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Koller, B. H. and Orr, H. T.: Cloning and complete sequence of an HLA-A2 gene: analysis of the HLA-A alleles at the nucleotide level. J Immunol 134: 2727–2733, 1985

    Google Scholar 

  • Koop, B. F., Siemieniak, D., Slightom, J. L., Goodman, M., Dunbar, J., Wright, P. C., and Simons, E. L.: Tarsius δ- and β-globin genes: conversion, evolution, and systematic implications. J Biol Chem 264: 68–79, 1989

    Google Scholar 

  • Kottman, A. H., Seeman, G. H. A., Guessow, H. D., and Roos, M. H.: DNA sequence of the coding region of the HLA-B44 gene. Immunogenetics 23: 396–400, 1986

    Google Scholar 

  • Kuhner, M. K. and Goodenow, R. S.: DNA sequences of mouse H-2 and Qa genes. Immunogenetics 30: 458–464, 1989

    CAS  PubMed  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 

  • Liskay, R. M., Letson, A., and Stacheleck, J. L.: Homology requirement for efficient gene conversion between duplicated chromosomal sequences in mammalian cells. Genetics 115: 161–167, 1987

    Google Scholar 

  • McGuire, K. L., Duncan, W. R., and Tucker, P. W.: Structure of a class I gene from Syrian hamster. J Immunol 137: 366–371, 1986

    Google Scholar 

  • Mauxion, F., Sobczak, J., and Kress, M.: Characterization of five distinct cDNA clones encoding for class I RT1 antigens. Immunogenetics 29: 397–401, 1989

    Google Scholar 

  • 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

    Google Scholar 

  • Mellor, A. L., Weiss, E. H., Kress, M., Jay, G., and Flavell, R. A.: A nonpolymorphic class I gene in the murine major histocompatibility complex. Cell 36: 139–144, 1984

    Google Scholar 

  • Morita, T., Delarbre, C., Kress, M., Kourlisky, P., and Gachelin, G.: An H-2K gene of the t w32 mutant at the T/t complex is a close parent of an H-2k qgene. Immunogenetics 21: 367–383, 1985

    Google Scholar 

  • Nei, M. and Gojobori, T.: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418–426, 1986

    CAS  PubMed  Google Scholar 

  • 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

    Google Scholar 

  • Parker, K. E., Carter, C. A., and Fabre, J. W.: A rat class I cDNA clone with an Alu-like sequence and mapping to two genes in RT1.C/E. Immunogenetics 21: 211–214, 1990

    Google Scholar 

  • 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

    Google Scholar 

  • Radojcic, A., Kunz, H. W., and Gill, T. J. III.: Expression and analysis of the rat placental class I cDNA clone encoding the Pa antigen. Immunogenetics 31: 326–332, 1990

    Google Scholar 

  • Robinson, P. J., Bevec, D., Mellor, A. L., and Weiss, E. H.: Sequences of the mouse Q4 class I gene and characterization of the gene product. Immunogenetics 27: 79–86, 1988

    Google Scholar 

  • Rubocki, R. J., Lee, D. R., Lie, W.-R., Myers, N. B., and Hansen, T. H.: Molecular evidence that the H-2D and H-2L genes arose by duplication: Differences between the evolution of the class I genes in mice and humans. J Exp Med 171: 2043–2061, 1990

    Google Scholar 

  • Rogers, J. H.: Mouse histocompatibility-related genes not conserved in other mammals. EMBO J 4: 749–753, 1985

    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 

  • Transy, C., Nash, S. R., David-Watine, B., Cochet, M., Hunt, S. W. III, Hood, L. E., and Kourlisky, P.: A low polymorphic mouse H-2 class I gene from the Tla complex is expressed in a broad variety of cell types. J Exp Med 166: 341–361, 1988

    Google Scholar 

  • Walsh, J. B.: Sequence-dependent gene conversion: Can duplicated genes diverge fast enough to escape conversion? Genetics 117: 543–557, 1987

    Google Scholar 

  • Watkins, D. I., Chen, Z. W., Hughes, A. L., Evans, M. G., 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

    Google Scholar 

  • Watts, S. J., Vogel, J. M., Harriman, W. D., Itoh, T., Stauss, H. J., and Goodenow, R. S.: DNA sequence analysis of the C3H H-2K k and H-2D k loci: Evolutionary relationship to H-2 genes from four other mouse strains. J Immunol 139: 3878–3885, 1987

    Google Scholar 

  • Watts, S., Davis, A. C., and Goodenow, R. S.: Sequence analysis of the C3H H-2K1 k gene: relationship to the H-2 loci: Immunogenetics 29: 355–357, 1989a

    Google Scholar 

  • Watts, S., Davis, A. C., Gant, B., Wheeler, C., Hill, L., and Goodenow, R. S.: Organization and structure of the Qa genes of the major histocompatibility complex of the C3H mouse: implications for Qa function and class I evolution. EMBO J 8: 1749–1759, 1989b

    Google Scholar 

  • Weiss, E. H., Golden, L., Zakut, R., Mellor, A., Fahrner, K., Kvist, S., and Flavell, R. A.: The DNA sequence of the H-2K bgene: Evidence for gene conversion as a mechanism for the generation of polymorphism in histocompatibility antigens. EMBO J 2: 453–462, 1983

    Google Scholar 

  • Wolfe, K. H., Sharp, P. M., and Li, W.-H: Mutation rates vary among regions of the mammalian genome. Nature 337: 283–285, 1989

    Article  CAS  PubMed  Google Scholar 

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  1. Department of Biology and Institute of Molecular Evolutionary Genetics, Mueller Laboratory, The Pennsylvania State University, 16802, University Park, PA, USA

    Austin L. Hughes

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Hughes, A.L. Independent gene duplications, not concerted evolution, explain relationships among class I MHC genes of murine rodents. Immunogenetics 33, 367–373 (1991). https://doi.org/10.1007/BF00216696

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