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. 1989 Mar;9(3):959–964. doi: 10.1128/mcb.9.3.959

Interleukin 1 and cyclic AMP induce kappa immunoglobulin light-chain expression via activation of an NF-kappa B-like DNA-binding protein.

F Shirakawa 1, M Chedid 1, J Suttles 1, B A Pollok 1, S B Mizel 1
PMCID: PMC362684  PMID: 2542770

Abstract

Interleukin 1 (IL-1) induces the synthesis of kappa immunoglobulin light chains and the expression of surface immunoglobulin in the murine pre-B-cell line 70Z/3 (J. G. Giri, P. W. Kincade, and S. B. Mizel, J. Immunol. 132:223-228, 1984). In the present study, we found that these effects of IL-1 are mimicked by cyclic AMP (cAMP) analogs and cAMP-elevating drugs. The induction of kappa immunoglobulin light-chain gene expression by IL-1 was associated with an increase in intracellular cAMP levels. Incubation of 70Z/3 cells with IL-1 or cAMP resulted in the activation of the kappa immunoglobulin enhancer, as detected by the induction of chloramphenicol acetyltransferase (CAT) in cells transfected with a kappa enhancer-CAT expression plasmid. In contrast, CAT plasmids lacking a kappa immunoglobulin enhancer were inactive in the presence of IL-1 or cAMP. Furthermore, IL-1 and cAMP analogs and inducers were found to induce the activation of a NF-kappa B-like DNA-binding protein that exhibited specificity for the kappa immunoglobulin enhancer. These results suggest that cAMP may play an important role as a second messenger for IL-1 in the induction of kappa immunoglobulin light-chain synthesis in pre-B cells via the activation of a DNA-binding protein that is similar or identical to NF-kappa B.

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Selected References

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  1. Abraham R. T., Ho S. N., Barna T. J., McKean D. J. Transmembrane signaling during interleukin 1-dependent T cell activation. Interactions of signal 1- and signal 2-type mediators with the phosphoinositide-dependent signal transduction mechanism. J Biol Chem. 1987 Feb 25;262(6):2719–2728. [PubMed] [Google Scholar]
  2. Atchison M. L., Perry R. P. The role of the kappa enhancer and its binding factor NF-kappa B in the developmental regulation of kappa gene transcription. Cell. 1987 Jan 16;48(1):121–128. doi: 10.1016/0092-8674(87)90362-x. [DOI] [PubMed] [Google Scholar]
  3. Avissar S., Stenzel K. H., Novogrodsky A. Selective effects of TPA and IL-1 on protein phosphorylation in murine thymocytes. Cell Immunol. 1985 Dec;96(2):462–471. doi: 10.1016/0008-8749(85)90378-8. [DOI] [PubMed] [Google Scholar]
  4. Baeuerle P. A., Baltimore D. Activation of DNA-binding activity in an apparently cytoplasmic precursor of the NF-kappa B transcription factor. Cell. 1988 Apr 22;53(2):211–217. doi: 10.1016/0092-8674(88)90382-0. [DOI] [PubMed] [Google Scholar]
  5. Cambier J. C., Newell M. K., Justement L. B., McGuire J. C., Leach K. L., Chen Z. Z. Ia binding ligands and cAMP stimulate nuclear translocation of PKC in B lymphocytes. Nature. 1987 Jun 18;327(6123):629–632. doi: 10.1038/327629a0. [DOI] [PubMed] [Google Scholar]
  6. Dignam J. D., Lebovitz R. M., Roeder R. G. Accurate transcription initiation by RNA polymerase II in a soluble extract from isolated mammalian nuclei. Nucleic Acids Res. 1983 Mar 11;11(5):1475–1489. doi: 10.1093/nar/11.5.1475. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dinarello C. A. Interleukin-1. Rev Infect Dis. 1984 Jan-Feb;6(1):51–95. doi: 10.1093/clinids/6.1.51. [DOI] [PubMed] [Google Scholar]
  8. Gill D. M., Meren R. ADP-ribosylation of membrane proteins catalyzed by cholera toxin: basis of the activation of adenylate cyclase. Proc Natl Acad Sci U S A. 1978 Jul;75(7):3050–3054. doi: 10.1073/pnas.75.7.3050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Giri J. G., Kincade P. W., Mizel S. B. Interleukin 1-mediated induction of kappa-light chain synthesis and surface immunoglobulin expression on pre-B cells. J Immunol. 1984 Jan;132(1):223–228. [PubMed] [Google Scholar]
  10. Hoffmann M. K. Macrophages and T cells control distinct phases of B cell differentiation in the humoral immune response in vitro. J Immunol. 1980 Nov;125(5):2076–2081. [PubMed] [Google Scholar]
  11. Howard M., Paul W. E. Regulation of B-cell growth and differentiation by soluble factors. Annu Rev Immunol. 1983;1:307–333. doi: 10.1146/annurev.iy.01.040183.001515. [DOI] [PubMed] [Google Scholar]
  12. Kishimoto T., Nishizawa Y., Kikutani H., Yamamura Y. Biphasic effect of cyclic amp on IgG production and on the changes of non-histone nuclear proteins induced with anti-immunoglobulin and enhancing soluble factor. J Immunol. 1977 Jun;118(6):2027–2033. [PubMed] [Google Scholar]
  13. Londos C., Wolff J. Two distinct adenosine-sensitive sites on adenylate cyclase. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5482–5486. doi: 10.1073/pnas.74.12.5482. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Lowenthal J. W., Böhnlein E., Ballard D. W., Greene W. C. Regulation of interleukin 2 receptor alpha subunit (Tac or CD25 antigen) gene expression: binding of inducible nuclear proteins to discrete promoter sequences correlates with transcriptional activation. Proc Natl Acad Sci U S A. 1988 Jun;85(12):4468–4472. doi: 10.1073/pnas.85.12.4468. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Mizel S. B. Interleukin 1 and T cell activation. Immunol Rev. 1982;63:51–72. doi: 10.1111/j.1600-065x.1982.tb00411.x. [DOI] [PubMed] [Google Scholar]
  16. Mukaida N., Kasahara T., Yagisawa H., Shioiri-Nakano K., Kawai T. Signal requirement for interleukin-1-dependent interleukin 2 production by a human leukemia-derived HSB.2 subclone. J Immunol. 1987 Nov 15;139(10):3321–3329. [PubMed] [Google Scholar]
  17. Nelson K. J., Kelley D. E., Perry R. P. Inducible transcription of the unrearranged kappa constant region locus is a common feature of pre-B cells and does not require DNA or protein synthesis. Proc Natl Acad Sci U S A. 1985 Aug;82(16):5305–5309. doi: 10.1073/pnas.82.16.5305. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Ransom J. T., Harris L. K., Cambier J. C. Anti-Ig induces release of inositol 1,4,5-trisphosphate, which mediates mobilization of intracellular Ca++ stores in B lymphocytes. J Immunol. 1986 Jul 15;137(2):708–714. [PubMed] [Google Scholar]
  19. Ribeiro-Neto F. A., Mattera R., Hildebrandt J. D., Codina J., Field J. B., Birnbaumer L., Sekura R. D. ADP-ribosylation of membrane components by pertussis and cholera toxin. Methods Enzymol. 1985;109:566–572. doi: 10.1016/0076-6879(85)09115-7. [DOI] [PubMed] [Google Scholar]
  20. Sakaguchi N., Kishimoto T., Kikutani H., Watanabe T., Yoshida N., Shimizu A., Yamawaki-Kataoka Y., Honjo T., Yamamura Y. Induction and regulation of immunoglobulin expression in a murine pre-B cell line, 70Z/3. I. Cell cycle-associated induction of sIgM expression and kappa-chain synthesis in 70Z/3 cells by LPS stimulation. J Immunol. 1980 Dec;125(6):2654–2659. [PubMed] [Google Scholar]
  21. Sen R., Baltimore D. Inducibility of kappa immunoglobulin enhancer-binding protein Nf-kappa B by a posttranslational mechanism. Cell. 1986 Dec 26;47(6):921–928. doi: 10.1016/0092-8674(86)90807-x. [DOI] [PubMed] [Google Scholar]
  22. Sen R., Baltimore D. Multiple nuclear factors interact with the immunoglobulin enhancer sequences. Cell. 1986 Aug 29;46(5):705–716. doi: 10.1016/0092-8674(86)90346-6. [DOI] [PubMed] [Google Scholar]
  23. Shirakawa F., Tanaka Y., Eto S., Suzuki H., Yamashita U. Requirement of macrophages (monocytes) for the induction of interleukin 2 receptors on B lymphocytes. J Immunol. 1986 May 1;136(9):3288–3291. [PubMed] [Google Scholar]
  24. Shirakawa F., Tanaka Y., Eto S., Suzuki H., Yodoi J., Yamashita U. Effect of interleukin 1 on the expression of interleukin 2 receptor (Tac antigen) on human natural killer cells and natural killer-like cell line (YT cells). J Immunol. 1986 Jul 15;137(2):551–556. [PubMed] [Google Scholar]
  25. Shirakawa F., Yamashita U., Chedid M., Mizel S. B. Cyclic AMP--an intracellular second messenger for interleukin 1. Proc Natl Acad Sci U S A. 1988 Nov;85(21):8201–8205. doi: 10.1073/pnas.85.21.8201. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Stanton T. H., Maynard M., Bomsztyk K. Effect of interleukin-1 on intracellular concentration of sodium, calcium, and potassium in 70Z/3 cells. J Biol Chem. 1986 May 5;261(13):5699–5701. [PubMed] [Google Scholar]

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