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Restriction fragment length polymorphism and evolution of the mouse immunoglobulin constant region gamma loci

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Abstract

Genomic DNA from twelve laboratory mouse strains, in addition to 21 wild-derived strains belonging to different taxa (Mus musculus domesticus, Mus musculus musculus, Mus spretus, Mus macedonicus, a and Mus spicilegus) and four mouse strains that are evolutionarily more distant, were analyzed by Southern blot for polymorphism of the Ig heavy chain constant region γ isotype (Igh-Cγ) and for the distribution of the duplicated Igh-1 (Cγ2α) haplotype. Distinct allelic forms of each Igh-C locus could be defined by restriction fragment length polymorphism (RFLP). In laboratory mouse strains RFLP proved to be more sensitive in the detection of Igh-4 (Cγ1) alleles than serological methods. Taq I digestion allowed the definition of two alleles in the Igh-8 (Cγ3) locus, which is absolutely conserved at the protein levels. More extensive RFLP could be found in wild strains belonging to the subgenus Mus and in the evolutionarily more distant Mus species belonging to other subgenera. In previous studies we have shown that the Igh-1 locus is duplicated in M. m. musculus subspecies. We now extend this observations to the wild mouse strains belonging to M. spicilegus and M. macedonicus species and to the evolutionarily more distant wild mouse strain Mus pahari (subgenus coelomys), which is thought to have diverged from domestic mice about 5 million years ago. In addition, we found a similar RFLP pattern in ten of 18 wild mice trapped in India, suggesting that the haplotype containing the two Igh-1-like genes, organized in tandem as distinct isotypes, is widely spread in natural populations. The evolution of murine Igh-Cγ-encoded isotypes is also discussed.

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References

  • Amor, M., Bonhomme, F., Guénet, J. L., Petter, F., and Cazenave, P.-A. Polymorphism of heavy chain immunoglobulin isotypes in the Mus subgenus. I. Limited γ3 polymorphism revealed by antibodies raised in SPE wild-derived inbred strain. Immunogenetics 20: 577–581, 1984

    Google Scholar 

  • Auffray, J.-C., Vanlerberghe, F., and Britton-Davidian, J. The house mouse progression in Eurasia: a palaeontological and archaeozoological approach. Biol J Linn Soc London 41: 13–25, 1990

    Google Scholar 

  • Bishop, C. E., Boursot, P., Baron, B., Bonhomme, F., and Hatat, D. Most classical M. m. domesticus laboratory strains carry a M. m musculus Y chromosome. Nature 315: 70–72, 1985

    Google Scholar 

  • Bonhomme, F. Evolutionary relationships in the genus Mus. In M. Potter, J. H. NNadeau, and M. P. Cancro (eds.): The Wild Mouse in Immunology. Curr Top Microbiol Immunol 127: 19–34, 1986

  • Bonhomme, F., Guénet, J. L., Dod, B., Moriwaki, K., and Bulfield, G. The polyphyletic origin of laboratory inbred mice and their rate of evolution. Biol J Linn Soc London 30: 51–58, 1987

    Google Scholar 

  • Bruggemann, M. Evolution of the rat immunoglobulin gamma heavy-chain gene family. Gene 74: 473–482, 1988

    Google Scholar 

  • Cazenave, P.-A., Bonhomme, F., Guénet, J. L., and Kindt, T. J. Correlation of CTβ phenotype with origins of laboratory mouse strains. In M. Potter, J. H. Nadeau, and M. P. Cancro (eds.): The Wild Mouse in Immunology. Curr Top Microbiol Immunol 127: 300–306, 1986

  • Din, W., Anand, R., Boursot, P., Darviche, D., Jouvin-Marche, E., Orth, A., Talwar, G. P., Cazenave, P.-A., and Bonhomme, F. The house mouse as a ring species: I. Nuclear genes. Evolution, in press, 1993

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

    CAS  PubMed  Google Scholar 

  • Fukui, K., Hamagushi, Y., Shimizu, A., Nakai, S., Moriwaki, K., Wang, C. H., and Honjo, T. Duplicated immunoglobulin gamma genes in wild mice. J Mol Cell Immunol 1: 321–330, 1984

    Google Scholar 

  • Green, M. C. Genetic nomenclature for the immunoglobulin loci of the mouse. Immunogenetics 8: 89–99, 1979

    Google Scholar 

  • Hayashida, H., Miyata, T., Yamawaki-Kataoka, Y., Honjo, T., Weis, J., and Blattner, F. Concerted evolution of the mouse immunoglobulin gamma chain genes. EMBO J 3: 2047–2053, 1984

    Google Scholar 

  • Honjo, T., Obata, M., Yamawaki-Kataoka, Y., Kataoka, T., Kawakami, T., Takahashi, N., and Mano, T. Cloning and complete nucleotide sequence of mouse immunoglobulin γ1 chain gene. Cell 18: 559–568, 1979

    Google Scholar 

  • Huang, C.-M., Huang, H.-J. S., and Lee, S.-C. Detection of immunoglobulin heavy chain IgG3 polymorphism in wild mice with xenogeneic monoclonal antibodies. Immunogenetics 20: 565–575, 1984

    Google Scholar 

  • Huang, C.-M., Parsons, M., Oi, V. T., Huang, H.-J. S., and Herzenberg, L. A.: Genetic characterization of mouse immunoglobulin allotypic determinants (allotopes) defined by monoclonal antibodies. Immunogenetics 18: 311–321, 1983

    Google Scholar 

  • Huang, C.-M., Parsons, M., Wakeland, E. K., Moriwaki, K., and Herzenberg, L. A. New immunoglobulin IgG allotypes and haplotypes found in wild mice with monoclonal anti-allotype antibodies. J Immunol 128: 661–667, 1982

    Google Scholar 

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

    Google Scholar 

  • Jouvin-Marche, E., Morgado, M. G., Le Guern, C., Voegtlé, D., Bonhomme, F., and Cazenave, P.-A. The mouse Igh-1 aand Igh-1 bH chain constant regions are derived from two distinct isotypic genes. Immunogenetics 29: 92–97, 1989

    Google Scholar 

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

    Google Scholar 

  • Lieberman, R. Genetics of IgCH (allotype) locus in the mouse. Springer Semin Immunopathol 1: 7–30, 1978

    Google Scholar 

  • Lieberman, R. and Potter, M. Crossing-over between genes in the immunoglobulin heavy chain linkage group of the mouse. J Exp Med 130: 519–541, 1969

    Google Scholar 

  • Mami, F., Cazenave, P.-A., and Kindt, T. J. Conservation of the immunoglobulin Cγ5 gene in the Mus genus. EMBO J 7: 117–122, 1988

    Google Scholar 

  • Masmoudi, H., Bonhomme, F., and Cazenave, P.-A. “New” allotypes of the murine γ1 immunoglobulins. Mol Immunol 26: 551–555, 1989

    Google Scholar 

  • Morgado, M. G., Cam, P., Gris-Liebe, C., Cazenave, P.-A., and Jouvin-Marche, E. Further evidence that BALB/c and C57BL/6 g2a genes originate from two distinct isotypes. EMBO J 8: 3245–3252, 1989

    Google Scholar 

  • Ollo, R., Auffray, C., Morchamps, C., and Rougeon, F. Comparison of mouse immunoglobulin γ2a and γ2b chain genes suggests that exons can be exchanged between genes in a multigenic family. Proc Natl Acad Sci USA 78: 2442–2446, 1981

    Google Scholar 

  • Ollo, R. and Rougeon, F. Mouse immunoglobulin allotypes: post-duplication divergence of γ2a and γ2b chain genes. Nature 296: 761–763, 1982

    Google Scholar 

  • Parsons, M., Herzenberg, L. A., Stall, A. M., and Herzenberg, L. A. Mouse immunoglobulin allotypes. In D. M. Wier (ed.): Immunochemistry, 97.1–97.17, 1986

  • Riblet, R., Tutter, A., and Brodeur, P. Polymorphism and evolution of Igh-V gene families. In M. Potter, J. H. Nadeau and M. P. Cancro (eds.): The Wild Mouse in Immunology. Curr Top Microbial Immunol 127: 167–172, 1986

  • Scott, C. and Potter, M. Polymorphism of genes and units of duplication in the genus Mus. J Immunol 132: 2630–2637, 1984

    Google Scholar 

  • She, J. X., Bonhomme, F., Boursot, P., Thaler, L., and Catzeflis, F. Molecular phylogenies in genus Mus: comparative analysis of electrophoretic, scnDNA hybridization and mtDNA RFLP data. Biol J Linn Soc London 41: 83–103, 1990

    Google Scholar 

  • Shimizu, A., Hamaguchi, Y., Yaoita, Y., Moriwaki, K., Kondo, K., and Honjo, T. Japanese wild mouse, Mus musculus molossinus, had duplicated immunoglobulin γ2a genes. Nature 298: 82–84, 1982a

    Google Scholar 

  • Shimizu, A., Takahashi, N., Yaoita, Y., and Honjo, T. Organization of the constant-region gene family of the mouse immunoglobulin heavy chain. Cell 28: 499–506, 1982b

    Google Scholar 

  • Southern, E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol 98: 503–517, 1975

    CAS  PubMed  Google Scholar 

  • Takahashi, N., Ueda, S., Obata, M., Nikaido, T., Nakai, S., and Honjo, T. Structure of human immunoglobulin gamma genes: implications for evolution of a gene family. Cell 29: 671–679, 1982

    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 

  • Wels, J. A., Word, C. J., Rimm, D., Der-Balan, G. P., Martinez, H. M., Tucker, P. W., and Blattner, F. R. Structural analysis of the murine IgG3 constant region gene. EMBO J 3: 2041–2046, 1984

    Google Scholar 

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Correspondence to: P.-A. Cazenave.

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Morgado, M.G., Jouvin-Marche, E., Gris-Liebe, C. et al. Restriction fragment length polymorphism and evolution of the mouse immunoglobulin constant region gamma loci. Immunogenetics 38, 184–192 (1993). https://doi.org/10.1007/BF00211518

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  • DOI: https://doi.org/10.1007/BF00211518

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