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Characterization of a Vϰ family in Mus musculus castaneus: expansion at the subset level

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Abstract

We have examined the same kappa chain variable (Vϰ) region family in several mouse species in order to observe short-term, incremental change at immunoglobun (Ig) multigene loci. In the present study, the Igk-V24 family has been characterized in a Mus m. castaneus colony derived from individuals originating in Thailand and compared to the same family in Mus m. domesticus (BALB/c) and Mus pahari, representing about 1 – 2 and about 5 – 9 million years of evolution, respectively. Southern hybridization of genomic DNA with a probe encoding the prototype Igk-V24 coding region reveals restriction fragment patterns indicative of two distinct M. m. castaneus haplotypes. These haplotypes appear to result from an unequal recombination between similar gene arrays, as their restriction patterns are unique but contain many common fragments. The complexity of these patterns indicates a marked expansion in the Igk-V24 family of M. m. castaneus relative to BALB/c and M. pahari. Additional analyses using probes specific for individual subsets demonstate that the expansion is not general throughout the entire family, but is restricted to particular subsets and therefore to relatively short chromosomal segments. One subset alone accounts for most of the expansion and comprises over 40% of the entire M. m. castaneus family. The wide range of Igk-V24 family complexity seen among M. m. castaneus, M. m. domesticus, and M. pahari, as well as among the different M. m. castaneus family subsets, suggests a model of random evolution in Vϰ family copy number rather than one which is selective.

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References

  • Bonhomme, F., Iskandar, D., Thaler, L., and Petter, F. Electromorphs and phylogeny in murid rodents. In W. P. Luckett and J. L. Hartenberger (eds.): Evolutionary Relationships among Rodents: A Multidisciplinary Analysis, pp. 671–684, Plenum Publishing Corp., New York, 1984

    Google Scholar 

  • Brodeur, P. H. Genes encoding immunoglobulin variable regions. In M. Neuberger and F. Calabi (eds.) Molecular Genetics of Immunoglobulin, pp. 81–109, Elsevier Sciences Publishers, Amsterdam, 1987

    Google Scholar 

  • Caton, A. J. A single pre-B cell can give rise to antigen-specific B cells that utilize distinct immunoglobulin gene rearrangements. J Exp Med 172: 815–825, 1990

    Google Scholar 

  • Caton, A. J., Brownlee, G. G., Staudt, L. M., and Gerhard, W. Structural and functional implications of a restricted antibody response to a defined antigenic region on the influenza virus hemagglutinin. EMBO J 5: 1577–1587, 1986

    Google Scholar 

  • Cory, S., Tyler, B. M., and Adams, J. M. Sets of immunoglobulin V κ genes homologous to ten cloned V ϰ sequences: implications for the number of germline V κ genes. J Mol Appl Genet 1: 103–116, 1981

    Google Scholar 

  • D'Hoostelaere, L. A. and Gibson, D. M. The organization of immunoglobulin variable kappa chain genes on mouse chromosome 6. Immunogenetics 23: 260–265, 1986

    Google Scholar 

  • D'Hoostelaere, L. A., Huppi, K., Mock, B., Mallett, C., Gibson, D., Hilgers, J., and Potter, M. The organization of the immunoglobulin kappa locus in mice. Curr Top Microbiol Immunol 137: 116–129, 1988a

    Google Scholar 

  • D'Hoostelaere, L. A., Huppi, K., Mock, B., Mallett, C., and Potter, M. The Igκ chain allelic groups among the Igϰ haplotypes and Igκ crossover populations suggest a gene order. J Immunol 141: 652–661, 1988b

    Google Scholar 

  • Feinberg, A. P. and Vogelstein, B. A technique for radiolabelling DNA restriction endonuclease fragments to high specific activity. Anal Biochem 132: 6–13, 1983

    CAS  PubMed  Google Scholar 

  • Ferris, S. D., Sage, R. D., Prager, E. M., Ritte, U., and Wilson, A. C. Mitochondrial DNA evolution in mice. Genetics 105: 681–721, 1983

    Google Scholar 

  • Gearhart, P. J. and Bogenhagen, D. F. Clusters of point mutations are found exclusively around rearranged antibody genes. Proc Natl Acad Sci USA 80: 3439–3443, 1983

    Google Scholar 

  • Gearhart, P. J., Johnson, N. D., Douglas, R., and Hood, L. IgG antibodies to phosphorylcholine exhibit more diversity than their IgM counterparts. Nature 291: 29–34, 1981

    Google Scholar 

  • Gershenfeld, H. L., Tsukamoto, A., Weissman, I. L., and Joho, R. Somatic diversification is required to generate the Vκ genes of MOPC 511 and MOPC 167 myeloma proteins. Proc Natl Acad Sci USA 78: 7674–7678, 1981

    Google Scholar 

  • Hood, L., Campbell, J. H., and Elgin, S. C. R. The organization, expression, and evolution of antibody genes and other multigene families. Annu Rev Genet 9: 305–353, 1975

    Google Scholar 

  • Huppi, K., Jouvin-Marche, E., Scott, C. L., Potter, M., and Weigert, M. Genetic polymorphism at the kappa chain locus in mice: comparisons of restriction enzyme hybridization fragments of variable and constant region genes. Immunogenetics 21: 445–457, 1985

    Google Scholar 

  • Jacobs, L. L. and Pilbeam, D. Of mice and men: fossil-based divergence dates and molecular clocks. J Hum Evol 9: 551–555, 1980

    Google Scholar 

  • Joho, R., Weissman, I. L., Early, P., Cole, J., and Hood, L. Organization of κ light chain genes in germ-line and somatic tissue. Proc Natl Acad Sci USA 77: 1106–1110, 1980

    Google Scholar 

  • Joho, R., Gershenfeld, H. L., and Weissman, I. L. Evolution of a multigene family of V κ line genes. EMBO J 3: 185–191, 1984

    Google Scholar 

  • Jouvin-Marche, E. and Rudikoff, S. Evolution of a V κ gene family. Immunogenetics 24: 191–201, 1986

    Google Scholar 

  • Jouvin-Marche, E., Cuddihy, A., Heller, M., Butler, S., Hansen, J. N., and Rudikoff, S. Evolution of immunologically important genes in the genus Mus. Curr Top Microbiol Immunol 127: 149–156, 1986

    Google Scholar 

  • Jouvin-Marche, E., Cuddihy, A., Butler, S., Hansen, J. N., Fitch, W. M., and Rudikoff, S. Modern evolution of a single copy gene: the immunoglobulin C κ locus in wild mice. Mol Biol Evol 5: 500–511, 1988

    Google Scholar 

  • Klein, J., Figueroa, F., and David, C. S. H-2 haplotypes, genes and antigens: second listing. II. the H-2 complex. Immunogenetics 17: 553–596, 11983a

    Google Scholar 

  • Klein, J., Figueroa, F., and Nagy, Z. A. Genetics of the major histocompatibility complex: the final act. Annu Rev Immunol 1: 119–142, 1983b

    Google Scholar 

  • Kodaira, M., Kinashi, T., Umemura, I., Matsuda, F., Noma, T., Ono, Y., and Hojno, T. Organization and evolution of variable region genes of the human immunoglobulin heavy chain. J Mol Biol 190: 529–541, 1986

    Google Scholar 

  • Kofler, R., Duchosal, M. A., and Dixon, F. J. Complexity, polymorphism and connectivity of mouse V κ gene families. Immunogenetics 29: 65–74, 1989

    Google Scholar 

  • Lutz, C. T. and Davie, J. M. Genetics and primary structure of V κ gene segments encoding antibody to streptococcal group A carbohydrate. J Immunol 140: 641–645, 1988

    Google Scholar 

  • Maeda, N. and Smithies, O. The evolution of multigene families: human haptoglobin genes. Annu Rev Genet 20: 81–108, 1986

    Google Scholar 

  • Marshall, J. T. and Sage, R. D. Taxonomy of the house mouse. Symp Zool Soc Lond 47: 15–25, 1981

    Google Scholar 

  • Potter, M., Newell, J. B., Rudikoff, S., and Haber, E. Classification of mouse V κ groups based on the partial amino acid sequence to the first invariant tryptophan: impact of 14 new sequences from IgG myeloma proteins. Mol Immunol 19: 1619–1630, 1982

    Google Scholar 

  • Selsing, E. and Storb, U. Somatic mutation of immunoglobulin light-chain variable region genes. Cell 25: 47–58, 1981

    Google Scholar 

  • Singh, S. K., Wakeland, E. K., Vučak, I., Nagy, Z. A., and Klein, J. An H-2 haplotype possibly derived by crossing-over between (AαAβ) duplex and the Eβ locus. Immunogenetics 14: 273–281, 1981

    Google Scholar 

  • Steinmetz, M., Minard, K., Horvath, S., McNicholas, J., Frelinger, J., Wake, C., Long, E., Mach, B., and Hood, L. A molecular map of the immune response region from the major histocompatibility complex of the mouse. Nature 300: 35–42, 1982

    Google Scholar 

  • Strohal, R., Helmberg, A., Kroemer, G., and Kofler, R. Mouse V κ gene classification by nucleic acid sequence similarity. Immunogenetics 30: 475–493, 1989

    Google Scholar 

  • Tutter, A. and Riblet, R. Duplication and deletions of V H genes in inbred strains of mice. Immunogenetics 28: 125–135, 1988a

    Google Scholar 

  • Tutter, A. and Riblet, R. Selective and neutral evolution in the murine Igh-V locus. Curr Top Microbiol Immunol 137: 107–115, 1988b

    Google Scholar 

  • Tutter, A. and Riblet, R. Evolution of the immunoglobulin heavy chain variable region (Igh-V) locus in the genus Mus. Immunogenetics 30: 315–329, 1989

    Google Scholar 

  • Wakeland, E.K. and Darby, B. R. Recombination and mutation of class II histocompatibility genes in wild mice. J Immunol 131: 3052–3057, 1983

    Google Scholar 

  • Yonekawa, H., Moriwaki, K., Gotoh, O., Hayashi, J. I., Watanabe, J., Miyashita, N., Petras, M. L., and Tagashira, Y. Evolutionary relationship among five subspecies of Mus musculus based on restriction enzyme cleavage patterns of mitochondrial DNA. Genetics 98: 801–816, 1981

    Google Scholar 

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  1. Terry J. Henderson

    Present address: Biophysics Laboratory, Center for Biologics Evaluation and Research, Food and Drug Administration, 8800 Rockville Pike, 20 892, Bethesda, MD, USA

Authors and Affiliations

  1. Laboratory of Genetics, National Cancer Institute, National Institute of Health, 20 892, Bethesda, MD, USA

    Terry J. Henderson & Stuart Rudikoff

  2. Department of Chemistry and Biochemistry, University of Maryland, 20 742, College Park, MD, USA

    Terry J. Henderson

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  1. Terry J. Henderson
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  2. Stuart Rudikoff
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Henderson, T.J., Rudikoff, S. Characterization of a Vϰ family in Mus musculus castaneus: expansion at the subset level. Immunogenetics 37, 415–425 (1993). https://doi.org/10.1007/BF00222465

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