Skip to main content
NCBI home page
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1982 Mar;79(6):2008–2012. doi: 10.1073/pnas.79.6.2008

mRNA for surface immunoglobulin gamma chains encodes a highly conserved transmembrane sequence and a 28-residue intracellular domain.

B M Tyler, A F Cowman, S D Gerondakis, J M Adams, O Bernard
PMCID: PMC346111  PMID: 6804950

Abstract

To probe the structure of the gamma heavy chain of membrane IgG and the mRNA and gene segments that encode it, we have analyzed cDNA clones derived from a gamma 1 membrane RNA of B lymphoma 2PK-3. The nucleotide sequence of the clones indicated that membrane gamma 1 chains bear a COOH-terminal 71-residue segment that is absent from secretory gamma 1 chains. This terminus includes a 26-residue hydrophobic transmembrane region homologous to that of membrane mu chains and, significantly, a 28-residue intracellular domain found only on gamma chains. The extra domain suggests that receptor IgG, on memory B cells, may generate a different signal on binding antigen than does receptor IgM, on virgin B cells. The gamma 1 membrane terminus is encoded by two gene segments 1.5 and 2.4 kilobase pairs downstream from the C gamma 1 gene, and homologous segments occur 3' to the C gamma 2a and C gamma 3 genes. Small amounts of membrane gamma mRNAs persist in plasmacytomas secreting IgG1, IgG2a, or IgG2b, suggesting that competition between alternative RNA processing pathways governs the synthesis of membrane and secretory gamma chain mRNAs.

Full text

PDF
2008

Images in this article

2010Image
on p.2010
2010Image
on p.2010
2011Image
on p.2011

Selected References

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

  1. Adams J. M., Webb E., Gerondakis S., Cory S. Cloned embryonic DNA sequences flanking the mouse immunoglobulin C gamma 3 and C gamma 1 genes. Nucleic Acids Res. 1980 Dec 20;8(24):6019–6032. doi: 10.1093/nar/8.24.6019. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Alt F. W., Bothwell A. L., Knapp M., Siden E., Mather E., Koshland M., Baltimore D. Synthesis of secreted and membrane-bound immunoglobulin mu heavy chains is directed by mRNAs that differ at their 3' ends. Cell. 1980 Jun;20(2):293–301. doi: 10.1016/0092-8674(80)90615-7. [DOI] [PubMed] [Google Scholar]
  3. Alwine J. C., Kemp D. J., Stark G. R. Method for detection of specific RNAs in agarose gels by transfer to diazobenzyloxymethyl-paper and hybridization with DNA probes. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5350–5354. doi: 10.1073/pnas.74.12.5350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Berk A. J., Sharp P. A. Sizing and mapping of early adenovirus mRNAs by gel electrophoresis of S1 endonuclease-digested hybrids. Cell. 1977 Nov;12(3):721–732. doi: 10.1016/0092-8674(77)90272-0. [DOI] [PubMed] [Google Scholar]
  5. Burstein Y., Schechter I. Primary structures of N-terminal extra peptide segments linked to the variable and constant regions of immunoglobulin light chain precursors: implications on the organization and controlled expression of immunoglobulin genes. Biochemistry. 1978 Jun 13;17(12):2392–2400. doi: 10.1021/bi00605a022. [DOI] [PubMed] [Google Scholar]
  6. Early P., Rogers J., Davis M., Calame K., Bond M., Wall R., Hood L. Two mRNAs can be produced from a single immunoglobulin mu gene by alternative RNA processing pathways. Cell. 1980 Jun;20(2):313–319. doi: 10.1016/0092-8674(80)90617-0. [DOI] [PubMed] [Google Scholar]
  7. Gething M. J., Bye J., Skehel J., Waterfield M. Cloning and DNA sequence of double-stranded copies of haemagglutinin genes from H2 and H3 strains elucidates antigenic shift and drift in human influenza virus. Nature. 1980 Sep 25;287(5780):301–306. doi: 10.1038/287301a0. [DOI] [PubMed] [Google Scholar]
  8. Goding J. W., Scott D. W., Layton J. E. Genetics, cellular expression and function of IgD and IgM receptors. Immunol Rev. 1977;37:152–186. doi: 10.1111/j.1600-065x.1977.tb00249.x. [DOI] [PubMed] [Google Scholar]
  9. Gough N. M., Webb E. A., Cory S., Adams J. M. Molecular cloning of seven mouse immunoglobulin kappa chain messenger ribonucleic acids. Biochemistry. 1980 Jun 10;19(12):2702–2710. doi: 10.1021/bi00553a026. [DOI] [PubMed] [Google Scholar]
  10. Greenblatt J. Regulation of transcription termination by the N gene protein of bacteriophage lambda. Cell. 1981 Apr;24(1):8–9. doi: 10.1016/0092-8674(81)90495-5. [DOI] [PubMed] [Google Scholar]
  11. Grunstein M., Hogness D. S. Colony hybridization: a method for the isolation of cloned DNAs that contain a specific gene. Proc Natl Acad Sci U S A. 1975 Oct;72(10):3961–3965. doi: 10.1073/pnas.72.10.3961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Karn J., Brenner S., Barnett L., Cesareni G. Novel bacteriophage lambda cloning vector. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5172–5176. doi: 10.1073/pnas.77.9.5172. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kehry M., Ewald S., Douglas R., Sibley C., Raschke W., Fambrough D., Hood L. The immunoglobulin mu chains of membrane-bound and secreted IgM molecules differ in their C-terminal segments. Cell. 1980 Sep;21(2):393–406. doi: 10.1016/0092-8674(80)90476-6. [DOI] [PubMed] [Google Scholar]
  14. Kemp D. J., Harris A. W., Cory S., Adams J. M. Expression of the immunoglobulin C mu gene in mouse T and B lymphoid and myeloid cell lines. Proc Natl Acad Sci U S A. 1980 May;77(5):2876–2880. doi: 10.1073/pnas.77.5.2876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. 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]
  16. Maki R., Roeder W., Traunecker A., Sidman C., Wabl M., Raschke W., Tonegawa S. The role of DNA rearrangement and alternative RNA processing in the expression of immunoglobulin delta genes. Cell. 1981 May;24(2):353–365. doi: 10.1016/0092-8674(81)90325-1. [DOI] [PubMed] [Google Scholar]
  17. Mason D. W. The class of surface immunoglobulin on cells carrying IgG memory in rat thoracic duct lymph: the size of the subpopulation mediating IgG memory. J Exp Med. 1976 May 1;143(5):1122–1130. doi: 10.1084/jem.143.5.1122. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Maxam A. M., Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 1980;65(1):499–560. doi: 10.1016/s0076-6879(80)65059-9. [DOI] [PubMed] [Google Scholar]
  19. Nevins J. R., Darnell J. E., Jr Steps in the processing of Ad2 mRNA: poly(A)+ nuclear sequences are conserved and poly(A) addition precedes splicing. Cell. 1978 Dec;15(4):1477–1493. doi: 10.1016/0092-8674(78)90071-5. [DOI] [PubMed] [Google Scholar]
  20. Oi V. T., Bryan V. M., Herzenberg L. A., Herzenberg L. A. Lymphocyte membrane IgG and secreted IgG are structurally and allotypically distinct. J Exp Med. 1980 May 1;151(5):1260–1274. doi: 10.1084/jem.151.5.1260. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Okumura K., Julius M. H., Tsu T., Herzenberg L. A., Herzenberg L. A. Demonstration that IgG memory is carried by IgG-bearing cells. Eur J Immunol. 1976 Jul;6(7):467–472. doi: 10.1002/eji.1830060704. [DOI] [PubMed] [Google Scholar]
  22. Parkhouse R. M., Lifter J., Choi Y. S. Chemical characterisation of the Fab and Fc fragments from surface immunoglobulin. Nature. 1980 Mar 20;284(5753):280–281. doi: 10.1038/284280a0. [DOI] [PubMed] [Google Scholar]
  23. Princler G. L., McIntire K. R. Surface immunoglobulins on mouse myeloma cells. Cell Immunol. 1975 Jan;15(1):197–207. doi: 10.1016/0008-8749(75)90175-6. [DOI] [PubMed] [Google Scholar]
  24. Rigby P. W., Dieckmann M., Rhodes C., Berg P. Labeling deoxyribonucleic acid to high specific activity in vitro by nick translation with DNA polymerase I. J Mol Biol. 1977 Jun 15;113(1):237–251. doi: 10.1016/0022-2836(77)90052-3. [DOI] [PubMed] [Google Scholar]
  25. Rogers J., Choi E., Souza L., Carter C., Word C., Kuehl M., Eisenberg D., Wall R. Gene segments encoding transmembrane carboxyl termini of immunoglobulin gamma chains. Cell. 1981 Oct;26(1 Pt 1):19–27. doi: 10.1016/0092-8674(81)90029-5. [DOI] [PubMed] [Google Scholar]
  26. Rogers J., Clarke P., Salser W. Sequence analysis of cloned cDNA encoding part of an immunoglobulin heavy chain. Nucleic Acids Res. 1979 Jul 25;6(10):3305–3321. doi: 10.1093/nar/6.10.3305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Rogers J., Early P., Carter C., Calame K., Bond M., Hood L., Wall R. Two mRNAs with different 3' ends encode membrane-bound and secreted forms of immunoglobulin mu chain. Cell. 1980 Jun;20(2):303–312. doi: 10.1016/0092-8674(80)90616-9. [DOI] [PubMed] [Google Scholar]
  28. Sanger F., Coulson A. R., Barrell B. G., Smith A. J., Roe B. A. Cloning in single-stranded bacteriophage as an aid to rapid DNA sequencing. J Mol Biol. 1980 Oct 25;143(2):161–178. doi: 10.1016/0022-2836(80)90196-5. [DOI] [PubMed] [Google Scholar]
  29. Sidman C. L., Bercovici T., Gitler C. Membrane insertion of lymphocyte surface molecules. Mol Immunol. 1980 Dec;17(12):1575–1583. doi: 10.1016/0161-5890(80)90183-2. [DOI] [PubMed] [Google Scholar]
  30. Tomita M., Marchesi V. T. Amino-acid sequence and oligosaccharide attachment sites of human erythrocyte glycophorin. Proc Natl Acad Sci U S A. 1975 Aug;72(8):2964–2968. doi: 10.1073/pnas.72.8.2964. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Tyler B. M., Adams J. M. Organization of the sequences flanking immunoglobulin heavy chain genes and their role in class switching. Nucleic Acids Res. 1980 Dec 11;8(23):5579–5598. doi: 10.1093/nar/8.23.5579. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Tyler B. M., Cowman A. F., Adams J. M., Harris A. W. Generation of long mRNA for membrane immunoglobulin gamma 2a chains by differential splicing. Nature. 1981 Oct 1;293(5831):406–408. doi: 10.1038/293406a0. [DOI] [PubMed] [Google Scholar]
  33. Walters C. S., Wigzell H. Demonstration of heavy and light chain antigenic determinants on the cell-bound receptor for antigen. Similarities between membrane-attached and humoral antibodies produced by the same cell. J Exp Med. 1970 Dec 1;132(6):1233–1249. doi: 10.1084/jem.132.6.1233. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Word C. J., Kuehl W. M. Expression of surface and secreted IgG2a by a murine B-lymphoma before and after hybridization to myeloma cells. Mol Immunol. 1981 Apr;18(4):311–322. doi: 10.1016/0161-5890(81)90055-9. [DOI] [PubMed] [Google Scholar]
  35. 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]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES