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. 1980 Nov;77(11):6793–6796. doi: 10.1073/pnas.77.11.6793

Simultaneous expression of mouse immunoglobulins M and D is determined by the same homolog of chromosome 12.

M R Wabl, J P Johnson, I G Haas, M Tenkhoff, T Meo, R Inan
PMCID: PMC350375  PMID: 6779283

Abstract

A hamster-mouse hybrid cell line expressiong both murine IgM and murine IgD on the membrane was shown to have only one copy of mouse chromosome 12. This chromosome is known to carry the structural genes for the immunoglobulin heavy chains. Cloning of populations selected for loss of mouse membrane IgM yielded cells that had also lost expression of membrane IgD, but not the expression of hamster immunoglobulin heavy chain. Karyotype analysis of these subclones demonstrated the concurrent loss of the chromosome 12 present in the parental hybrid. Absence of this chromosome was confirmed by use of the isozyme acid phosphatase 1. The results of the genetic analysis prove that the coexpression of mu and delta immunoglobulin heavy chains is not due to long-lived immunoglobulin mRNA nor to the transcription of genes on homologous chromosomes. We conclude that the genetic information for IgM and IgD expressed by a single cell lies on the same chromosome.

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Selected References

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

  1. Abney E. R., Parkhouse R. M. Candidate for immunoglobulin D present on murine B lymphocytes. Nature. 1974 Dec 13;252(5484):600–602. doi: 10.1038/252600a0. [DOI] [PubMed] [Google Scholar]
  2. Buckland R. A., Fletcher J. M., Chandley C. Characterization of the domestic horse (Equus caballus) karyotype using G- and C-banding techniques. Experientia. 1976 Sep 15;32(9):1146–1149. doi: 10.1007/BF01927593. [DOI] [PubMed] [Google Scholar]
  3. Coe J. E., Green I. B-cell origin of hamster lymphoid tumors induced by simian virus 40. J Natl Cancer Inst. 1975 Jan;54(1):269–270. doi: 10.1093/jnci/54.1.269. [DOI] [PubMed] [Google Scholar]
  4. Coleclough C., Cooper D., Perry R. P. Rearrangement of immunoglobulin heavy chain genes during B-lymphocyte development as revealed by studies of mouse plasmacytoma cells. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1422–1426. doi: 10.1073/pnas.77.3.1422. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Cory S., Adams J. M. Deletions are associated with somatic rearrangement of immunoglobulin heavy chain genes. Cell. 1980 Jan;19(1):37–51. doi: 10.1016/0092-8674(80)90386-4. [DOI] [PubMed] [Google Scholar]
  6. Davis M. M., Calame K., Early P. W., Livant D. L., Joho R., Weissman I. L., Hood L. An immunoglobulin heavy-chain gene is formed by at least two recombinational events. Nature. 1980 Feb 21;283(5749):733–739. doi: 10.1038/283733a0. [DOI] [PubMed] [Google Scholar]
  7. Diamandopoulos G. T. Induction of lymphocytic leukemia, lymphosarcoma, reticulum cell sarcoma, and osteogenic sarcoma in the Syrian golden hamster by oncogenic DNA simian virus 40. J Natl Cancer Inst. 1973 May;50(5):1347–1365. doi: 10.1093/jnci/50.5.1347. [DOI] [PubMed] [Google Scholar]
  8. Ferrarini M., Corte G., Viale G., Durante M. L., Bargellesi A. Membrane Ig on human lymphocytes: rate of turnover of IgD and IgM on the surface of human tonsil cells. Eur J Immunol. 1976 May;6(5):372–378. doi: 10.1002/eji.1830060513. [DOI] [PubMed] [Google Scholar]
  9. Francke U., Lalley P. A., Moss W., Ivy J., Minna J. D. Gene mapping in Mus musculus by interspecific cell hybridization: assignment of the genes for tripeptidase-1 to chromosome 10, dipeptidase-2 to chromosome 18, acid phosphatase-1 to chromosome 12, and adenylate kinase-1 to chromosome 2. Cytogenet Cell Genet. 1977;19(2-3):57–84. doi: 10.1159/000130799. [DOI] [PubMed] [Google Scholar]
  10. Fu S. M., Winchester R. J., Feizi T., Walzer P. D., Kunkel H. G. Idiotypic specificity of surface immunoglobulin and the maturation of leukemic bone-marrow-derived lymphocytes. Proc Natl Acad Sci U S A. 1974 Nov;71(11):4487–4490. doi: 10.1073/pnas.71.11.4487. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Haustein D. Effective radioiodination by lactoperoxidase and solubilisation of cell-surface proteins of cultured murine T lymphoma cells. J Immunol Methods. 1975 Apr;7(1):25–38. doi: 10.1016/0022-1759(75)90127-1. [DOI] [PubMed] [Google Scholar]
  12. Hengartner H., Meo T., Müller E. Assignment of genes for immunoglobulin kappa and heavy chains to chromosomes 6 and 12 in mouse. Proc Natl Acad Sci U S A. 1978 Sep;75(9):4494–4498. doi: 10.1073/pnas.75.9.4494. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Herzenberg L. A., Herzenberg L. A., Black S. J., Loken M. R., Okumura K., van der Loo W., Osborne B. A., Hewgill D., Goding J. W., Gutman G. Surface markers and functional relationships of cells involved in murine B-lymphocyte differentiation. Cold Spring Harb Symp Quant Biol. 1977;41(Pt 1):33–45. doi: 10.1101/sqb.1977.041.01.007. [DOI] [PubMed] [Google Scholar]
  14. Honjo T., Kataoka T. Organization of immunoglobulin heavy chain genes and allelic deletion model. Proc Natl Acad Sci U S A. 1978 May;75(5):2140–2144. doi: 10.1073/pnas.75.5.2140. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kabat D. Gene selection in hemoglobin and in antibody-synthesizing cells. Science. 1972 Jan 14;175(4018):134–140. doi: 10.1126/science.175.4018.134. [DOI] [PubMed] [Google Scholar]
  16. Kearney J. F., Lawton A. R. B lymphocyte differentiation induced by lipopolysaccharide. I. Generation of cells synthesizing four major immunoglobulin classes. J Immunol. 1975 Sep;115(3):671–676. [PubMed] [Google Scholar]
  17. Kessler S. W. Rapid isolation of antigens from cells with a staphylococcal protein A-antibody adsorbent: parameters of the interaction of antibody-antigen complexes with protein A. J Immunol. 1975 Dec;115(6):1617–1624. [PubMed] [Google Scholar]
  18. Knapp W., Bolhuis R. L., Rádl J., Hijmans W. Independent movement of IgD and IgM molecules on the surface of individual lymphocytes. J Immunol. 1973 Oct;111(4):1295–1298. [PubMed] [Google Scholar]
  19. 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]
  20. Maki R., Traunecker A., Sakano H., Roeder W., Tonegawa S. Exon shuffling generates an immunoglobulin heavy chain gene. Proc Natl Acad Sci U S A. 1980 Apr;77(4):2138–2142. doi: 10.1073/pnas.77.4.2138. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Marshall C. J. A method for analysis of chromosomes in hybrid cells employing sequential G-banding and mouse specific D-banding. Exp Cell Res. 1975 Mar 15;91(2):464–469. doi: 10.1016/0014-4827(75)90130-5. [DOI] [PubMed] [Google Scholar]
  22. Melcher U., Vitetta E. S., McWilliams M., Lamm M. E., Phillips-Quagliata J. M., Uhr J. W. Cell surface immunoglobulin. X. Identification of an IgD-like molecule on the surface of murine splenocytes. J Exp Med. 1974 Nov 1;140(5):1427–1431. doi: 10.1084/jem.140.5.1427. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Meo T., Johnson J., Beechey C. V., Andrews S. J., Peters J., Searle A. G. Linkage analyses of murine immunoglobulin heavy chain and serum prealbumin genes establish their location on chromosome 12 proximal to the T (5;12) 31H breakpoint in band 12F1. Proc Natl Acad Sci U S A. 1980 Jan;77(1):550–553. doi: 10.1073/pnas.77.1.550. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Nesbitt M. N., Francke U. A system of nomenclature for band patterns of mouse chromosomes. Chromosoma. 1973;41(2):145–158. doi: 10.1007/BF00319691. [DOI] [PubMed] [Google Scholar]
  25. Pernis B., Brouet J. C., Seligmann M. IgD and IgM on the membrane of lymphoid cells in macroglobulinemia. Evidence for identity of membrane IgD and IgM antibody activity in a case with anti-IgG receptors. Eur J Immunol. 1974 Nov;4(11):776–778. doi: 10.1002/eji.1830041114. [DOI] [PubMed] [Google Scholar]
  26. Rabbitts T. H., Forster A., Dunnick W., Bentley D. L. The role of gene deletion in the immunoglobulin heavy chain switch. Nature. 1980 Jan 24;283(5745):351–356. doi: 10.1038/283351a0. [DOI] [PubMed] [Google Scholar]
  27. Rowe D. S., Hug K., Forni L., Pernis B. Immunoglobulin D as a lymphocyte receptor. J Exp Med. 1973 Oct 1;138(4):965–972. doi: 10.1084/jem.138.4.965. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Swallow D. M., Povey S., Harris H. Activity of the "red cell" acid phosphatase locus in other tissues. Ann Hum Genet. 1973 Jul;37(1):31–38. doi: 10.1111/j.1469-1809.1973.tb01812.x. [DOI] [PubMed] [Google Scholar]

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