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. 1993 Aug 1;90(15):7054–7058. doi: 10.1073/pnas.90.15.7054

Interleukin 1 induction of the c-jun promoter.

K Muegge 1, M Vila 1, G L Gusella 1, T Musso 1, P Herrlich 1, B Stein 1, S K Durum 1
PMCID: PMC47074  PMID: 8346217

Abstract

Interleukin 1 (IL-1) induces pleiotropic effects in many cell types during inflammation and immunity. We have recently shown how the IL-1 signal is transmitted to the nucleus: In T cells and in pituitary cells, IL-1 induced genes via activation of the nuclear factor AP-1. We now demonstrate how IL-1 activates the AP-1 factor in liver cells, which are a major target for IL-1 during the acute phase response in vivo. IL-1 induced gene transcription of both AP-1 components, c-jun and c-fos. IL-1 also increased the stability of c-jun mRNA. We define two enhancer sites in the jun promoter that are required for induction by IL-1. Although the binding sites share some similarity with the AP-1 binding site, the nuclear factors binding the jun motifs are not composed of Jun or Fos proteins. Thus these data identify two binding proteins that serve as one of the first nuclear targets for IL-1 signal transduction.

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Selected References

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

  1. Akira S., Isshiki H., Sugita T., Tanabe O., Kinoshita S., Nishio Y., Nakajima T., Hirano T., Kishimoto T. A nuclear factor for IL-6 expression (NF-IL6) is a member of a C/EBP family. EMBO J. 1990 Jun;9(6):1897–1906. doi: 10.1002/j.1460-2075.1990.tb08316.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Angel P., Baumann I., Stein B., Delius H., Rahmsdorf H. J., Herrlich P. 12-O-tetradecanoyl-phorbol-13-acetate induction of the human collagenase gene is mediated by an inducible enhancer element located in the 5'-flanking region. Mol Cell Biol. 1987 Jun;7(6):2256–2266. doi: 10.1128/mcb.7.6.2256. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Angel P., Hattori K., Smeal T., Karin M. The jun proto-oncogene is positively autoregulated by its product, Jun/AP-1. Cell. 1988 Dec 2;55(5):875–885. doi: 10.1016/0092-8674(88)90143-2. [DOI] [PubMed] [Google Scholar]
  4. Angel P., Imagawa M., Chiu R., Stein B., Imbra R. J., Rahmsdorf H. J., Jonat C., Herrlich P., Karin M. Phorbol ester-inducible genes contain a common cis element recognized by a TPA-modulated trans-acting factor. Cell. 1987 Jun 19;49(6):729–739. doi: 10.1016/0092-8674(87)90611-8. [DOI] [PubMed] [Google Scholar]
  5. Bird T. A., Sleath P. R., deRoos P. C., Dower S. K., Virca G. D. Interleukin-1 represents a new modality for the activation of extracellular signal-regulated kinases/microtubule-associated protein-2 kinases. J Biol Chem. 1991 Nov 25;266(33):22661–22670. [PubMed] [Google Scholar]
  6. Brenner D. A., O'Hara M., Angel P., Chojkier M., Karin M. Prolonged activation of jun and collagenase genes by tumour necrosis factor-alpha. Nature. 1989 Feb 16;337(6208):661–663. doi: 10.1038/337661a0. [DOI] [PubMed] [Google Scholar]
  7. Chirgwin J. M., Przybyla A. E., MacDonald R. J., Rutter W. J. Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry. 1979 Nov 27;18(24):5294–5299. doi: 10.1021/bi00591a005. [DOI] [PubMed] [Google Scholar]
  8. Chiu R., Angel P., Karin M. Jun-B differs in its biological properties from, and is a negative regulator of, c-Jun. Cell. 1989 Dec 22;59(6):979–986. doi: 10.1016/0092-8674(89)90754-x. [DOI] [PubMed] [Google Scholar]
  9. Curran T., Franza B. R., Jr Fos and Jun: the AP-1 connection. Cell. 1988 Nov 4;55(3):395–397. doi: 10.1016/0092-8674(88)90024-4. [DOI] [PubMed] [Google Scholar]
  10. Devary Y., Gottlieb R. A., Lau L. F., Karin M. Rapid and preferential activation of the c-jun gene during the mammalian UV response. Mol Cell Biol. 1991 May;11(5):2804–2811. doi: 10.1128/mcb.11.5.2804. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Făgărăsan M. O., Aiello F., Muegge K., Durum S., Axelrod J. Interleukin 1 induces beta-endorphin secretion via Fos and Jun in AtT-20 pituitary cells. Proc Natl Acad Sci U S A. 1990 Oct;87(20):7871–7874. doi: 10.1073/pnas.87.20.7871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Gorman C. M., Moffat L. F., Howard B. H. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol Cell Biol. 1982 Sep;2(9):1044–1051. doi: 10.1128/mcb.2.9.1044. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Greenberg M. E., Ziff E. B. Stimulation of 3T3 cells induces transcription of the c-fos proto-oncogene. Nature. 1984 Oct 4;311(5985):433–438. doi: 10.1038/311433a0. [DOI] [PubMed] [Google Scholar]
  14. Han T. H., Lamph W. W., Prywes R. Mapping of epidermal growth factor-, serum-, and phorbol ester-responsive sequence elements in the c-jun promoter. Mol Cell Biol. 1992 Oct;12(10):4472–4477. doi: 10.1128/mcb.12.10.4472. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Karin M., Imbra R. J., Heguy A., Wong G. Interleukin 1 regulates human metallothionein gene expression. Mol Cell Biol. 1985 Oct;5(10):2866–2869. doi: 10.1128/mcb.5.10.2866. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lafyatis R., Kim S. J., Angel P., Roberts A. B., Sporn M. B., Karin M., Wilder R. L. Interleukin-1 stimulates and all-trans-retinoic acid inhibits collagenase gene expression through its 5' activator protein-1-binding site. Mol Endocrinol. 1990 Jul;4(7):973–980. doi: 10.1210/mend-4-7-973. [DOI] [PubMed] [Google Scholar]
  17. Lee W., Mitchell P., Tjian R. Purified transcription factor AP-1 interacts with TPA-inducible enhancer elements. Cell. 1987 Jun 19;49(6):741–752. doi: 10.1016/0092-8674(87)90612-x. [DOI] [PubMed] [Google Scholar]
  18. McCroskery P. A., Arai S., Amento E. P., Krane S. M. Stimulation of procollagenase synthesis in human rheumatoid synovial fibroblasts by mononuclear cell factor/interleukin 1. FEBS Lett. 1985 Oct 21;191(1):7–12. doi: 10.1016/0014-5793(85)80983-2. [DOI] [PubMed] [Google Scholar]
  19. McIntyre P., Stark G. R. A quantitative method for analyzing specific DNA sequences directly from whole cells. Anal Biochem. 1988 Oct;174(1):209–214. doi: 10.1016/0003-2697(88)90537-4. [DOI] [PubMed] [Google Scholar]
  20. Muegge K., Durum S. K. From cell code to gene code: cytokines and transcription factors. New Biol. 1989 Dec;1(3):239–246. [PubMed] [Google Scholar]
  21. Muegge K., Williams T. M., Kant J., Karin M., Chiu R., Schmidt A., Siebenlist U., Young H. A., Durum S. K. Interleukin-1 costimulatory activity on the interleukin-2 promoter via AP-1. Science. 1989 Oct 13;246(4927):249–251. doi: 10.1126/science.2799385. [DOI] [PubMed] [Google Scholar]
  22. Otani Y., Quinones S., Saus J., Kurkinen M., Harris E. D., Jr Cycloheximide induces stromelysin mRNA in cultured human fibroblasts. Eur J Biochem. 1990 Aug 28;192(1):75–79. doi: 10.1111/j.1432-1033.1990.tb19197.x. [DOI] [PubMed] [Google Scholar]
  23. Pabo C. O., Sauer R. T. Transcription factors: structural families and principles of DNA recognition. Annu Rev Biochem. 1992;61:1053–1095. doi: 10.1146/annurev.bi.61.070192.005201. [DOI] [PubMed] [Google Scholar]
  24. Pulverer B. J., Kyriakis J. M., Avruch J., Nikolakaki E., Woodgett J. R. Phosphorylation of c-jun mediated by MAP kinases. Nature. 1991 Oct 17;353(6345):670–674. doi: 10.1038/353670a0. [DOI] [PubMed] [Google Scholar]
  25. Schönthal A., Feramisco J. R. Different promoter elements are required for the induced expression of c-fos and c-jun proto-oncogenes by the v-mos oncogene product. New Biol. 1990 Feb;2(2):143–150. [PubMed] [Google Scholar]
  26. Shapiro D. J., Sharp P. A., Wahli W. W., Keller M. J. A high-efficiency HeLa cell nuclear transcription extract. DNA. 1988 Jan-Feb;7(1):47–55. doi: 10.1089/dna.1988.7.47. [DOI] [PubMed] [Google Scholar]
  27. Shirakawa F., Chedid M., Suttles J., Pollok B. A., Mizel S. B. Interleukin 1 and cyclic AMP induce kappa immunoglobulin light-chain expression via activation of an NF-kappa B-like DNA-binding protein. Mol Cell Biol. 1989 Mar;9(3):959–964. doi: 10.1128/mcb.9.3.959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Sims J. E., March C. J., Cosman D., Widmer M. B., MacDonald H. R., McMahan C. J., Grubin C. E., Wignall J. M., Jackson J. L., Call S. M. cDNA expression cloning of the IL-1 receptor, a member of the immunoglobulin superfamily. Science. 1988 Jul 29;241(4865):585–589. doi: 10.1126/science.2969618. [DOI] [PubMed] [Google Scholar]
  29. Stein B., Angel P., van Dam H., Ponta H., Herrlich P., van der Eb A., Rahmsdorf H. J. Ultraviolet-radiation induced c-jun gene transcription: two AP-1 like binding sites mediate the response. Photochem Photobiol. 1992 Mar;55(3):409–415. doi: 10.1111/j.1751-1097.1992.tb04255.x. [DOI] [PubMed] [Google Scholar]
  30. Thévenin C., Kim S. J., Kehrl J. H. Inhibition of protein phosphatases by okadaic acid induces AP1 in human T cells. J Biol Chem. 1991 May 25;266(15):9363–9366. [PubMed] [Google Scholar]
  31. Unlap T., Franklin C. C., Wagner F., Kraft A. S. Upstream regions of the c-jun promoter regulate phorbol ester-induced transcription in U937 leukemic cells. Nucleic Acids Res. 1992 Feb 25;20(4):897–902. doi: 10.1093/nar/20.4.897. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. van Dam H., Offringa R., Meijer I., Stein B., Smits A. M., Herrlich P., Bos J. L., van der Eb A. J. Differential effects of the adenovirus E1A oncogene on members of the AP-1 transcription factor family. Mol Cell Biol. 1990 Nov;10(11):5857–5864. doi: 10.1128/mcb.10.11.5857. [DOI] [PMC free article] [PubMed] [Google Scholar]

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