Skip to main content
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1981 Mar 25;9(6):1365–1381. doi: 10.1093/nar/9.6.1365

The complete nucleotide sequence of mouse immunoglobin gamma 2a gene and evolution of heavy chain genes: further evidence for intervening sequence-mediated domain transfer.

Y Yamawaki-Kataoka, T Miyata, T Honjo
PMCID: PMC326763  PMID: 6262729

Abstract

We have determined the complete nucleotide sequence (1990 base pairs) of mouse immunoglobulin gamma 2a gene, and compared it with the sequences of other gamma subclass genes so far sequenced, i.e. gamma 1 and gamma 2b genes. Divergence of the nucleotide sequence between a compared pair of the gamma genes varies extensively among different segments of the gene. For example, comparison of the gamma 2a and gamma 2b genes has revealed a remarkable homology in a long continuous segment (about 900 bases) that covers from the 3' portion of the first intervening sequence to the third intervening sequence. However, there is no particular segment of the gamma gene that is conserved universally among the three gamma genes. These findings suggest that, during their evolution, segments of the gamma genes had been scrambled between different subclass genes through recombinations within intervening sequences, thus providing further evidence for the intervening sequence-mediated domain transfer hypothesis. We have discussed several possible phylogenic trees which can explain the difference of divergence in various segments of the gamma genes.

Full text

PDF
1369

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Adetugbo K. Evolution of immunoglobulin subclasses. Primary structure of a murine myeloma gamma1 chain. J Biol Chem. 1978 Sep 10;253(17):6068–6075. [PubMed] [Google Scholar]
  2. Calame K., Rogers J., Early P., Davis M., Livant D., Wall R., Hood L. Mouse Cmu heavy chain immunoglobulin gene segment contains three intervening sequences separating domains. Nature. 1980 Apr 3;284(5755):452–455. doi: 10.1038/284452a0. [DOI] [PubMed] [Google Scholar]
  3. Darnell J. E., Jr Implications of RNA-RNA splicing in evolution of eukaryotic cells. Science. 1978 Dec 22;202(4374):1257–1260. doi: 10.1126/science.364651. [DOI] [PubMed] [Google Scholar]
  4. Dunnick W., Rabbitts T. H., Milstein C. An immunoglobulin deletion mutant with implications for the heavy-chain switch and RNA splicing. Nature. 1980 Aug 14;286(5774):669–675. doi: 10.1038/286669a0. [DOI] [PubMed] [Google Scholar]
  5. Early P. W., Davis M. M., Kaback D. B., Davidson N., Hood L. Immunoglobulin heavy chain gene organization in mice: analysis of a myeloma genomic clone containing variable and alpha constant regions. Proc Natl Acad Sci U S A. 1979 Feb;76(2):857–861. doi: 10.1073/pnas.76.2.857. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Edelman G. M., Cunningham B. A., Gall W. E., Gottlieb P. D., Rutishauser U., Waxdal M. J. The covalent structure of an entire gammaG immunoglobulin molecule. Proc Natl Acad Sci U S A. 1969 May;63(1):78–85. doi: 10.1073/pnas.63.1.78. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Fougereau M., Bourgois A., de Preval C., Rocca-Serra J., Schiff C. The complete sequence of the murine monoclonal immunoglobulin MOPC 173 (IgG2a): genetic implications. Ann Immunol (Paris) 1976 Sep-Oct;127(5):607–631. [PubMed] [Google Scholar]
  8. Francus T., Birshtein B. K. An IgG2a-producing variant of an IgG2b-producing mouse myeloma cell line. Structural studies on the Fc region of parent and variant heavy chains. Biochemistry. 1978 Oct 3;17(20):4324–4331. doi: 10.1021/bi00613a033. [DOI] [PubMed] [Google Scholar]
  9. Gough N. M., Kemp D. J., Tyler B. M., Adams J. M., Cory S. Intervening sequences divide the gene for the constant region of mouse immunoglobulin mu chains into segments, each encoding a domain. Proc Natl Acad Sci U S A. 1980 Jan;77(1):554–558. doi: 10.1073/pnas.77.1.554. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Honjo T., Obata M., Yamawaki-Katoaka Y., Kataoka T., Kawakami T., Takahashi N., Mano Y. Cloning and complete nucleotide sequence of mouse immunoglobulin gamma 1 chain gene. Cell. 1979 Oct;18(2):559–568. doi: 10.1016/0092-8674(79)90072-2. [DOI] [PubMed] [Google Scholar]
  11. Kataoka T., Yamawaki-Kataoka Y., Yamagishi H., Honjo T. Cloning immunoglobulin gamma 2b chain gene of mouse: characterization and partial sequence determination. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4240–4244. doi: 10.1073/pnas.76.9.4240. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Kawakami T., Takahashi N., Honjo T. Complete nucleotide sequence of mouse immunoglobulin mu gene and comparison with other immunoglobulin heavy chain genes. Nucleic Acids Res. 1980 Sep 11;8(17):3933–3945. doi: 10.1093/nar/8.17.3933. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kemp D. J., Cory S., Adams J. M. Cloned pairs of variable region genes for immunoglobulin heavy chains isolated from a clone library of the entire mouse genome. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4627–4631. doi: 10.1073/pnas.76.9.4627. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Konkel D. A., Maizel J. V., Jr, Leder P. The evolution and sequence comparison of two recently diverged mouse chromosomal beta--globin genes. Cell. 1979 Nov;18(3):865–873. doi: 10.1016/0092-8674(79)90138-7. [DOI] [PubMed] [Google Scholar]
  15. Lauer J., Shen C. K., Maniatis T. The chromosomal arrangement of human alpha-like globin genes: sequence homology and alpha-globin gene deletions. Cell. 1980 May;20(1):119–130. doi: 10.1016/0092-8674(80)90240-8. [DOI] [PubMed] [Google Scholar]
  16. Liu C. P., Tucker P. W., Mushinski J. F., Blattner F. R. Mapping of heavy chain genes for mouse immunoglobulins M and D. Science. 1980 Sep 19;209(4463):1348–1353. doi: 10.1126/science.6774414. [DOI] [PubMed] [Google Scholar]
  17. MacDonald R. J., Crerar M. M., Swain W. F., Pictet R. L., Thomas G., Rutter W. J. Structure of a family of rat amylase genes. Nature. 1980 Sep 11;287(5778):117–122. doi: 10.1038/287117a0. [DOI] [PubMed] [Google Scholar]
  18. Miyata T., Yasunaga T. Molecular evolution of mRNA: a method for estimating evolutionary rates of synonymous and amino acid substitutions from homologous nucleotide sequences and its application. J Mol Evol. 1980 Sep;16(1):23–36. doi: 10.1007/BF01732067. [DOI] [PubMed] [Google Scholar]
  19. Miyata T., Yasunaga T., Yamawaki-Kataoka Y., Obata M., Honjo T. Nucleotide sequence divergence of mouse immunoglobulin gamma 1 and gamma 2b chain genes and the hypothesis of intervening sequence-mediated domain transfer. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2143–2147. doi: 10.1073/pnas.77.4.2143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Nagata S., Mantei N., Weissmann C. The structure of one of the eight or more distinct chromosomal genes for human interferon-alpha. Nature. 1980 Oct 2;287(5781):401–408. doi: 10.1038/287401a0. [DOI] [PubMed] [Google Scholar]
  21. Obata M., Yamawaki-Kataoka Y., Takahashi N., Kataoka T., Shimizu A., Mano Y., Seidman J. G., Peterlin B. M., Leder P., Honjo T. Immunoglobulin gamma 1 heavy chain gene: structural gene sequences cloned in a bacterial plasmid. Gene. 1980 Apr;9(1-2):87–97. doi: 10.1016/0378-1119(80)90168-7. [DOI] [PubMed] [Google Scholar]
  22. Pink J. R., Buttery S. H., De Vries G. M., Milstein C. Human immunoglobulin subclasses. Partial amino acid sequence of the constant region of a gamma 4 chain. Biochem J. 1970 Mar;117(1):33–47. doi: 10.1042/bj1170033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Royal A., Garapin A., Cami B., Perrin F., Mandel J. L., LeMeur M., Brégégègre F., Gannon F., LePennec J. P., Chambon P. The ovalbumin gene region: common features in the organisation of three genes expressed in chicken oviduct under hormonal control. Nature. 1979 May 10;279(5709):125–132. doi: 10.1038/279125a0. [DOI] [PubMed] [Google Scholar]
  24. Sakano H., Rogers J. H., Hüppi K., Brack C., Traunecker A., Maki R., Wall R., Tonegawa S. Domains and the hinge region of an immunoglobulin heavy chain are encoded in separate DNA segments. Nature. 1979 Feb 22;277(5698):627–633. doi: 10.1038/277627a0. [DOI] [PubMed] [Google Scholar]
  25. Sikorav J. L., Auffray C., Rougeon F. Structure of the constant and 3' untranslated regions of the murine Balb/c gamma 2a heavy chain messenger RNA. Nucleic Acids Res. 1980 Jul 25;8(14):3143–3155. doi: 10.1093/nar/8.14.3143. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Slightom J. L., Blechl A. E., Smithies O. Human fetal G gamma- and A gamma-globin genes: complete nucleotide sequences suggest that DNA can be exchanged between these duplicated genes. Cell. 1980 Oct;21(3):627–638. doi: 10.1016/0092-8674(80)90426-2. [DOI] [PubMed] [Google Scholar]
  27. Southern E. M. Detection of specific sequences among DNA fragments separated by gel electrophoresis. J Mol Biol. 1975 Nov 5;98(3):503–517. doi: 10.1016/s0022-2836(75)80083-0. [DOI] [PubMed] [Google Scholar]
  28. Tucker P. W., Marcu K. B., Newell N., Richards J., Blattner F. R. Sequence of the cloned gene for the constant region of murine gamma 2b immunoglobulin heavy chain. Science. 1979 Dec 14;206(4424):1303–1306. doi: 10.1126/science.117549. [DOI] [PubMed] [Google Scholar]
  29. Wahli W., Dawid I. B., Wyler T., Weber R., Ryffel G. U. Comparative analysis of the structural organization of two closely related vitellogenin genes in X. laevis. Cell. 1980 May;20(1):107–117. doi: 10.1016/0092-8674(80)90239-1. [DOI] [PubMed] [Google Scholar]
  30. Yamawaki-Kataoka Y., Kataoka T., Takahashi N., Obata M., Honjo T. Complete nucleotide sequence of immunoglobulin gamma2b chain gene cloned from newborn nouse DNA. Nature. 1980 Feb 21;283(5749):786–789. doi: 10.1038/283786a0. [DOI] [PubMed] [Google Scholar]
  31. Yamawaki-Kataoka Y., Sato K., Shimizu A., Kataoka T., Mano Y., Ono M., Kawakami M., Honjo T. Mutual homology of mouse immunoglobulin gamma-chain gene sequences. Biochemistry. 1979 Feb 6;18(3):490–494. doi: 10.1021/bi00570a018. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES