Skip to main content
NCBI home page
The Journal of Experimental Medicine logoLink to The Journal of Experimental Medicine
. 1982 Oct 1;156(4):962–974. doi: 10.1084/jem.156.4.962

Effect of lipopolysaccharide stimulation on the transcription and translation of messenger RNA for cell surface immunoglobulin M

PMCID: PMC2186812  PMID: 6818319

Abstract

Analysis of mu-specific mRNA in the B cell tumor line, BCL1, shows that the cells contain predominantly mRNA for mu chain of membrane-bound immunoglobulin M (IgM) (2.7 kb, mu m mRNA). Stimulation of the cells to Ig secretion by lipopolysaccharide (LPS) results in a 6-12 fold increase in amount of mRNA for the mu chain of secreted IgM (2.4 kb mu s mRNA). The increase in mu s mRNA is accompanied by a 3-4-fold increase in mu m mRNA. The rate of mu chain synthesis of membrane IgM in LPS-stimulated cells is, however, reduced by at least twofold, suggesting that both transcriptional and translational regulatory events are involved in the induction of B lymphocytes to secretion.

Full Text

The Full Text of this article is available as a PDF (1.1 MB).

Selected References

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

  1. 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]
  2. Alt F. W., Rosenberg N., Enea V., Siden E., Baltimore D. Multiple immunoglobulin heavy-chain gene transcripts in Abelson murine leukemia virus-transformed lymphoid cell lines. Mol Cell Biol. 1982 Apr;2(4):386–400. doi: 10.1128/mcb.2.4.386. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Bourgois A., Kitajima K., Hunter I. R., Askonas B. A. Surface immunoglobulins of lipopolysaccharide-stimulated spleen cells. The behavior of IgM, IgD and IgG. Eur J Immunol. 1977 Mar;7(3):151–153. doi: 10.1002/eji.1830070307. [DOI] [PubMed] [Google Scholar]
  4. Boyd A. W., Goding J. W., Schrader J. W. The regulation of growth and differentiation of a murine B cell lymphoma. I. Lipopolysaccharide-induced differentiation. J Immunol. 1981 Jun;126(6):2461–2465. [PubMed] [Google Scholar]
  5. DePhilip R. M., Rudert W. A., Lieberman I. Preferential stimulation of ribosomal protein synthesis by insulin and in the absence of ribosomal and messenger ribonucleic acid formation. Biochemistry. 1980 Apr 15;19(8):1662–1669. doi: 10.1021/bi00549a022. [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. Gronowicz E. S., Doss C. A., Howard F. D., Morrison D. C., Strober S. An in vitro line of the B cell tumor BCL1 can be activated by LPS to secrete IgM1. J Immunol. 1980 Sep;125(3):976–980. [PubMed] [Google Scholar]
  8. Honjo T., Shimizu A., Tsuda M., Natori S., Katatoka T., Dohmoto C., Mano Y. Accumulation of immunoglobulin messenger ribonucleic acid in immunized mouse spleen. Biochemistry. 1977 Dec 27;16(26):5764–5769. doi: 10.1021/bi00645a018. [DOI] [PubMed] [Google Scholar]
  9. Isakson P. C., Krolick K. A., Uhr J. W., Vitetta E. S. The effect of anti-immunoglobulin antibodies on the in vitro proliferation and differentiation of normal and neoplastic murineB cells. J Immunol. 1980 Aug;125(2):886–892. [PubMed] [Google Scholar]
  10. 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]
  11. Kessler S. W. Cell membrane antigen isolation with the staphylococcal protein A-antibody adsorbent. J Immunol. 1976 Nov;117(5 Pt 1):1482–1490. [PubMed] [Google Scholar]
  12. Krolick K. A., Isakson P. C., Uhr J. W., Vitetta E. S. Murine B cell leukemia (BCL1): organ distribution and kinetics of growth as determined by fluorescence analysis with an anti-idiotypic antibody. J Immunol. 1979 Nov;123(5):1928–1935. [PubMed] [Google Scholar]
  13. Krüger C., Benecke B. J. In vitro translation of Drosophila heat-shock and non--heat-shock mRNAs in heterologous and homologous cell-free systems. Cell. 1981 Feb;23(2):595–603. doi: 10.1016/0092-8674(81)90155-0. [DOI] [PubMed] [Google Scholar]
  14. Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
  15. Lodish H. F. Model for the regulation of mRNA translation applied to haemoglobin synthesis. Nature. 1974 Oct 4;251(5474):385–388. doi: 10.1038/251385a0. [DOI] [PubMed] [Google Scholar]
  16. Marcu K. B., Banerji J., Penncavage N. A., Lang R., Arnheim N. 5' flanking region of immunoglobulin heavy chain constant region genes displays length heterogeneity in germlines of inbred mouse strains. Cell. 1980 Nov;22(1 Pt 1):187–196. doi: 10.1016/0092-8674(80)90167-1. [DOI] [PubMed] [Google Scholar]
  17. McCune J. M., Lingappa V. R., Fu S. M., Blobel G., Kunkel H. G. Biogenesis of membrane-bound and secreted immunoglobulins. I. Two distinct translation products of human mu-chain, with identical N-termini and different C-termini. J Exp Med. 1980 Aug 1;152(2):463–468. doi: 10.1084/jem.152.2.463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Melcher U., Eidels L., Uhr J. W. Are immunoglobulins integral membrane proteins? Nature. 1975 Dec 4;258(5534):434–435. doi: 10.1038/258434a0. [DOI] [PubMed] [Google Scholar]
  19. Melchers F., Andersson J. The kinectics of proliferation and maturation of mitogen-activated bone marrow-derived lymphocytes. Eur J Immunol. 1974 Oct;4(10):687–691. doi: 10.1002/eji.1830041010. [DOI] [PubMed] [Google Scholar]
  20. Olsson M. O., Gausing K. Post-transciptional control of coordinated ribosomal protein synthesis in Escherichia coli. Nature. 1980 Feb 7;283(5747):599–600. doi: 10.1038/283599a0. [DOI] [PubMed] [Google Scholar]
  21. Perry R. P., Kelley D. E., Coleclough C., Kearney J. F. Organization and expression of immunoglobulin genes in fetal liver hybridomas. Proc Natl Acad Sci U S A. 1981 Jan;78(1):247–251. doi: 10.1073/pnas.78.1.247. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Perry R. P., Kelley D. E. Immunoglobulin messenger RNAs in murine cell lines that have characteristics of immature B lymphocytes. Cell. 1979 Dec;18(4):1333–1339. doi: 10.1016/0092-8674(79)90243-5. [DOI] [PubMed] [Google Scholar]
  23. 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]
  24. 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]
  25. Sidman C. B lymphocyte differentiation and the control of IgM mu chain expression. Cell. 1981 Feb;23(2):379–389. doi: 10.1016/0092-8674(81)90133-1. [DOI] [PubMed] [Google Scholar]
  26. Singer P. A., Singer H. H., Williamson A. R. Different species of messenger RNA encode receptor and secretory IgM mu chains differing at their carboxy termini. Nature. 1980 May 29;285(5763):294–300. doi: 10.1038/285294a0. [DOI] [PubMed] [Google Scholar]
  27. Slavin S., Strober S. Spontaneous murine B-cell leukaemia. Nature. 1978 Apr 13;272(5654):624–626. doi: 10.1038/272624a0. [DOI] [PubMed] [Google Scholar]
  28. Tartakoff A., Vassalli P. Plasma cell immunoglobulin M molecules. Their biosynthesis, assembly, and intracellular transport. J Cell Biol. 1979 Nov;83(2 Pt 1):284–299. doi: 10.1083/jcb.83.2.284. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Thomas P. S. Hybridization of denatured RNA and small DNA fragments transferred to nitrocellulose. Proc Natl Acad Sci U S A. 1980 Sep;77(9):5201–5205. doi: 10.1073/pnas.77.9.5201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Tsuda M., Honjo T., Shimizu A., Mizuno D., Natori S. Induced synthesis of immunoglobulin messenger RNA accompanies induction of immunoglobulin production in cultured mouse spleen cells. J Biochem. 1978 Nov;84(5):1285–1290. doi: 10.1093/oxfordjournals.jbchem.a132247. [DOI] [PubMed] [Google Scholar]
  31. Vassalli P., Tartakoff A., Pink J. R., Jaton J. C. Biosynthesis of two forms of IgM heavy chains by normal mouse B lymphocytes. Membrane and secretory IgM. J Biol Chem. 1980 Dec 25;255(24):11822–11827. [PubMed] [Google Scholar]
  32. Vassalli P., Tedghi R., Lisowska-Bernstein B., Tartakoff A., Jaton J. C. Evidence for hydrophobic region within heavy chains of mouse B lymphocyte membrane-bound IgM. Proc Natl Acad Sci U S A. 1979 Nov;76(11):5515–5519. doi: 10.1073/pnas.76.11.5515. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. Vitetta E. S., Baur S., Uhr J. W. Cell surface immunoglobulin. II. Isolation and characterization of immunoglobulin from mouse splenic lymphocytes. J Exp Med. 1971 Jul 1;134(1):242–264. doi: 10.1084/jem.134.1.242. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Vitetta E. S., Yuan D., Krolick K., Isakson P., Knapp M., Slavin S., Strober S. Characterization of the spontaneous murine B cell leukemia (BCL1). III. Evidence for monoclonality by using an anti-idiotype antibody. J Immunol. 1979 May;122(5):1649–1654. [PubMed] [Google Scholar]
  35. Williams P. B., Kubo R. T., Grey H. M. mu-Chains from a nonsecretor B cell line differ from secreted mu-chains at the C-terminal end. J Immunol. 1978 Dec;121(6):2435–2439. [PubMed] [Google Scholar]
  36. Yuan D., Uhr J. W., Vitetta E. S. A peptide difference between the mu-chains from cell-associated and secreted IgM of the BCL1 tumor. J Immunol. 1980 Jul;125(1):40–46. [PubMed] [Google Scholar]
  37. Yuan D., Vitetta E. S., Kettman J. R. Cell surface immunoglobulin. XX. Antibody responsiveness of subpopulations of B lymphocytes bearing different isotypes. J Exp Med. 1977 Jun 1;145(6):1421–1435. doi: 10.1084/jem.145.6.1421. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Experimental Medicine are provided here courtesy of The Rockefeller University Press

RESOURCES