IκBα-independent downregulation of NF-κB activity by glucocorticoid receptor

EMBO Journal

Volumn 16, Issue 15, 1997, Pages 4698-4707

  Heck, Stefanie ^a   Bender, Klaus ^a   Kullmann, Michael ^a   Göttlicher, Martin ^a   Herrlich, Peter ^a   Cato, Andrew C B ^a  

^a KARLSRUHE INSTITUTE OF TECHNOLOGY   (Germany)

Author keywords

Androgen receptor; Anti inflammation; Dissociating glucocorticoids; Glucocorticoid receptor dimerization; Oestrogen receptor

Indexed keywords

CHEMOKINE; CYTOKINE; GLUCOCORTICOID RECEPTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INHIBITOR PROTEIN; TRANSCRIPTION FACTOR; ANDROSTANOLONE; DNA BINDING PROTEIN; ESTRADIOL; GLUCOCORTICOID; I KAPPA B; NF KAPPAB INHIBITOR ALPHA; NF-KAPPAB INHIBITOR ALPHA; PRIMER DNA;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RAT; ANIMAL; CELL LINE; CHEMISTRY; DIMERIZATION; DOWN REGULATION; DRUG ANTAGONISM; DRUG EFFECT; GENETIC TRANSFECTION; GENETICS; HELA CELL; METABOLISM; MUTATION; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PROMOTER REGION;

ANIMALIA;

ANIMALS; BASE SEQUENCE; CELL LINE; DIHYDROTESTOSTERONE; DIMERIZATION; DNA PRIMERS; DNA-BINDING PROTEINS; DOWN-REGULATION; ESTRADIOL; GLUCOCORTICOIDS; HELA CELLS; HUMANS; I-KAPPA B PROTEINS; INFLAMMATION; MICE; MUTATION; NF-KAPPA B; POLYMERASE CHAIN REACTION; PROMOTER REGIONS (GENETICS); RECEPTORS, GLUCOCORTICOID; TRANSFECTION;

EID: 0030789420     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.15.4698     Document Type: Article

References (66)

1. Adler, A.J., Scheller, A., Hoffman, Y. and Robins, D.M. (1991) Multiple components of a complex androgen-dependent enhancer. Mol. Endocrinol. 5, 1587-1596.
2. Adler, A.J., Danielsen, M. and Robins, D.M. (1992) Androgen-specific gene activation via a consensus glucocorticoid response element is determined by interaction with nonreceptor factors. Proc. Natl. Acad. Sci. USA, 89, 11660-11663.
3. Alkalay, I., Yaron, A., Hatzubai, A., Jung, S., Avraham, A., Gerlitz, O., Pashut-Lavon, I. and Ben-Neriah, Y. (1995) In vivo stimulation of IκB phosphorylation is not sufficient to activate NF-κB. Mol. Cell. Biol., 15, 1294-1301.
4. Angel, P., Baumann, I., Stein, B., Delius, H., Rahmsdorf, H.J. and Herrlich, P. (1987) 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. 7, 2256-2266.
5. Auphan, N., Di Donato, J.A., Rosette, C. Helmberg, A. and Karin, M. (1995) Immunosuppression by glucocorticoids: inhibition of NF-κB activity through induction of IκB synthesis. Science, 270, 286-290.
6. Baeuerle, P.A. and Baltimore, D. (1996) NF-κB: ten years after. Cell, 87, 13-20.
7. Barnes, P.J. and Adcock, I. (1993) Anti-inflammatory actions of steroids: molecular mechanisms. Trends Pharmacol. Sci., 14, 436-441.
8. Beato, M. (1989) Gene regulation by steroid hormones. Cell, 56, 335-344.
9. Beg, A.A. and Baldwin, A.S., Jr (1993) The IκB proteins: multifunctional regulators of Rel/NF-κB transcription factors. Genes Dev., 7, 2064-2070.
10. Beg, A.A., Ruben, S.M., Scheinman, R.I., Haskill, S., Rosen, C.A. and Baldwin, A.S., Jr (1992) IκB interacts with the nuclear localization sequences of the subunits of NF-κB: a mechanism for cytoplasmic retention. Genes Dev., 6, 1899-1913.
11. Beg, A.A., Finco, T.S., Nantermet, P.V. and Baldwin, A.S., Jr (1993) Tumor necrosis factor and interleukin-1 lead to phosphorylation and loss of IκB-α: a mechanism for NF-κB activation. Mol. Cell. Biol., 13, 3301-3310.
12. Beg, A.A., Sha, W.C., Bronson, R.T. and Baltimore, D. (1995) Constitutive NF-κB activation, enhanced granulopoiesis and neonatal lethality in IκBα-delicient mice. Genes Dev., 9, 2736-2746.
13. Brown, K., Park, S., Kanno, T., Franzoso, G. and Siebenlist, U. (1993) Mutual regulation of the transcriptional activator NF-κB and its inhibitor, IκB-α. Proc. Natl Acad. Sci. USA, 90, 2532-2536.
14. Caldenhoven, E., Liden, J., Wissink, S., van de Stolpe, A., Raaijmakers, J., Koenderman, L., Okret, S., Gustafsson, J.-Å. and van der Saag, P.T. (1995) Negative cross-talk between Rel A and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids. Mol. Endocrinol., 9, 401-412.
15. Cato, A.C.B. and Wade, E. (1996) Molecular mechanisms of anti-inflammatory action of glucocorticoids. BioEssays, 18, 371-378.
16. Cato, A.C.B., Skroch, P., Weinmann, J., Butkeraitis, P. and Ponta, H. (1988) DNA sequences outside the receptor-binding sites differently modulate the responsiveness of the mouse mammary tumour virus promoter to various steroid hormones. EMBO J., 7, 1403-1410.
17. Claessens, F., Alen, P., Devos, A., Peeters, B., Verhoeven, G. and Rombauts, W. (1996) The androgen-specific probasin response element 2 interacts differently with androgen and glucocorticoid receptors. J. Biol. Chem., 712, 19013-19016.
18. Davis, N., Ghosh, S., Simmons, D.L., Tempst, P., Liou, H.-C., Baltimore, D. and Bose, H.R., Jr (1991) Rel-associated pp40: an inhibitor of the rel family of transcription factors. Science, 253, 1268-1271.
19. Finco, T.S., Beg, A.A. and Baldwin, A.S., Jr (1994) Inducible phosphorylation of IκB-α is not sufficient for its dissociation from NF-κB and is inhibited by protease inhibitors. Proc. Natl Acad. Sci. USA, 91, 11884-11888.
20. Fort, P., Marty, L., Piechaczyk, M., el Sabrouty, S., Dani, C., Jeanteur, P. and Blanchard, J.M. (1985) Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res., 13, 1431-1442.
21. Grimm, S. and Baeuerle, P.A. (1993) The inducible transcription factor NF-κB: structure-function relationship of its protein subunits. Biochem. J., 290, 297-308.
22. Heck, S., Kullmann M., Gast, A., Ponta, H., Rahmsdorf, H.J., Herrlich, P. and Cato, A.C.B. (1994) A distinct modulating domain in glucocorticoid receptor monomers in the repression of activity of the transcription factor AP-1. EMBO J., 13, 4087-4095.
23. Helmberg, A., Auphan, N., Caelles, C. and Karin, M. (1995) Glucocorticoid-induced apoptosis of human leukemic cells is caused by the repressive function of the glucocorticoid receptor. EMBO J., 14, 452-460.
24. Israël, N., Gougerot-Pocidalo, M.-A., Aillet, F. and Virelizier, J.-L. (1992) Redox status of cells influences constitutive or induced NF-κB translocation and HIV long terminal repeat activity in human T and monocytic cell lines. J. Immunol. 149, 3386-3393.
25. Ito, C.Y., Kazantsev, A.G. and Baldwin, A.S., Jr (1994) Three NF-κB sites in the IκB-α promoter are required for induction of gene expression by TNFα. Nucleic Acids Res., 22, 3787-3792.
26. Jonat, C. (1990) Glucocorticoid-induzierte Repression der Kollagenase-1 Synthese: Vermittlung durch den Transkriptionsfaktor AP-1. PhD Thesis, University of Karlsruhe, Germany.
27. Jonat, C., Rahmsdorf, H.J., Park, K.K., Cato, A.C.B., Gebel, S., Ponta, H. and Herrlich, P. (1990) Antitumor promotion and antiinflammation: down-modulation of AP-1 (Fos/Jun) activity by glucocorticoid hormone. Cell, 62, 1189-1204.
28. Kalkhoven, E., Wissink, S., van der Saag, P.T. and van der Burg, B. (1996) Negative interaction between the Rel(p65) subunit of NF-κB and the progesterone receptor. J. Biol.Chem., 271, 6217-6224.
29. Karin, M. and Richards, R.I. (1982) Human metallothionein genes: molecular cloning and sequence analysis of the mRNA. Nucleic Acids Res., 10, 3165-3173.
30. Karin, M., Haslinger, A., Holtgreve, H., Richards, R.I., Krauter, P., Westphal, H.M. and Beato, M. (1984) Characterization of DNA sequences through which cadium and glucocorticoid hormones induce human metallothionein-IIa gene. Nature, 308, 513-519.
31. Keller, E.T., Chang, C. and Ershler, W.B. (1996) Inhibition of NF-κB activity through maintenance of IκBα levels contributes to dihydrotesterone-mediated repression of the Interleukin-6 promoter. J. Biol. Chem., 271, 26267-26275.
32. Kerr, L.D., Inoue, J., Davis, N., Link, E., Baeuerle, P.A., Bose, H.R., Jr and Verma, I.M. (1991) The rel-associated pp40 protein prevents DNA binding of Rel and NF-κB: relationship with IκB-β and regulation by phosphorylation. Genes Dev., 5, 1464-1476.
33. Le Bail, O., Schmidt-Ullrich, R. and Israël, A. (1993) Promoter analysis of the gene encoding the IκB-α/MAD3 inhibitor of NF-κB: positive regulation by members of the rel/NF-κB family. EMBO J., 12, 5043-5049.
34. Lee, S.W., Tsou, A.-P., Chan, H., Thomas, J., Petrie, K., Eugui, E.M. and Allison, A.C. (1988) Glucocorticoids selectively inhibit the transcription of the interleukin 1β gene and decrease the stability of interleukin 1β mRNA. Proc. Natl Acad. Sci. USA, 85, 1204-1208.
35. Lin, Y.-C., Brown, K. and Siebenlist, U. (1995) Activation of NF-κB requires proteolysis of the inhibitor IκB-α: signal induced phosphorylation of IκB-α alone does not release active NF-κB. Proc. Natl Acad. Sci. USA, 92, 552-556.
36. Liou, H.C. and Baltimore, D. (1993). Regulation of the NF-κB/Rel transcription factor and IκB inhibitor system. Curr. Opin. Cell Biol., 5, 477-487.
37. Liou, H.C., Nolan, G.P., Ghosh, S., Fujita, T. and Baltimore, D. (1992) The NF-κB p50 precursor, p105, contains an internal IκB like inhibitor that preferentially inhibits p50. EMBO J., 11, 3003-3009.
38. Morgenstern, J.P. and Land, H. (1990) Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res., 18, 3587-3596.
39. Nebl, G., Mermod, N. and Cato, A.C.B. (1994) Post-transcriptional down-regulation of expression of transcription factor NF1 by Ha-ras oncogene. J. Biol. Chem., 269, 7371-7378.
40. Neurath, M.F., Pettersson, S., Meyer zum Büschenfelde, K.-H. and Stober, W. (1996) Local administration of antisense phosphorothioate oligonucleotides to the p65 subunit of NF-κB abrogates established experimental colitis in mice. Nature Med., 2, 998-1004.
41. Nordeen, S.K. (1988) Luciferase reporter gene vectors for analysis of promoters and enhancers. Biotechniques, 6, 454-458.
42. Ray, A. and Prefontaine, K.E. (1994) Physical association and antagonism between the p65 subunit of transcription factor NF-κB and the glucocorticoid receptor. Proc. Natl Acad. Sci. USA, 91, 752-756.
43. Scheidereit C., von der Ahe, D., Cato, A.C.B., Wenz, M., Suske, G., Carlson, C., Bosshard, H., Westphal, H.M. and Beato, M. (1989) Protein-DNA interactions at steroid hormone regulated genes. Endocrine Res., 15, 417-440.
44. Scheinman, R.L. Cogswell, P.C., Lofquist, A.K. and Baldwin, A.S., Jr (1995a) Role of transcriptional activation of IκB-α in mediation of immunosuppression by glucocorticoids. Science, 270, 283-286.
45. Scheinman, R.I., Gualberto, A., Jewell, C.M., Cidlowsky, J.A. and Baldwin, A.S., Jr (1995b) Characterization of mechanisms involved in transrepression of NF-κB by activated glucocorticoid receptors. Mol. Cell. Biol. 15, 943-953.
46. Schena, M., Freedman, L.P. and Yamamoto, K.R. (1989) Mutations in the glucocorticoid receptor zinc finger region that distinguish interdigitated DNA binding and transcriptional enhancement activities. Genes Dev., 3, 1590-1601.
47. Schneikert, J., Peterziel, H., Defossez, P.-A., Klocker, H., de Lauroit, Y. and Cato, A.C.B. (1996) Androgen receptor-Ets protein interaction is a novel mechanism for steroid hormone-mediated down-modulation of matrix metalloproteinase expression. J. Biol. Chem., 271, 23907-23913.
48. Schüle, R., Müller, M., Kaltschmidt, C. and Renkawitz, R. (1988) Many transcription factors interact synergistically with steroid receptors. Science, 242, 1418-1420.
49. Schüle, R., Umesono, K., Mangelsdorf, D.J., Bolado, J., Pike, J.W. and Evans, R.M. (1990) Jun-Fos and receptors for vitamins A and D recognize a common response element in the human osteocalcin gene. Cell, 61, 497-504.
50. Shirakawa, F., Saito, K., Bonagura, C.A., Galson, D.L., Fenton, M.J., Webb, A.C. and Auron, P.E. (1993) The human prointerleukin 1β gene requires DNA sequences both proximal and distal to the transcription start site for tissue specific induction. Mol Cell. Biol. 13, 1332-1344.
51. Stein, B. and Yang, M.X. (1995) Repression of the interleukin-6 promoter by estrogen receptor is mediated by NF-κB and C/EBPβ. Mol. Cell. Biol., 15, 4971-4979.
52. Strähle, U., Schmid, W. and Schütz, G. (1988) Synergistic action of the glucocorticoid receptor with transcription factors. EMBO J., 7, 3389-3395.
53. Sun, S.-C., Ganchi, P.A., Ballard, D.W. and Greene, W.C. (1993) NF-κB controls expression of inhibitor IκBα: evidence for an inducible autoregulatory pathway. Science, 259, 1912-1915.
54. Thanos, D. and Maniatis, T. (1995) NF-κB: a lesson in family values. Cell, 80, 529-532.
55. Traenckner, E.B.-M., Wilk, S. and Baeuerle, P.A. (1994) A proteasome inhibitor prevents activation of NF-κB and stabilizes a newly phosphorylated form of IκB-α that is still bound to NF-κB. EMBO J., 13, 5433-5441.
56. Tsukada, J., Saito, K., Waterman, W.R., Webb, A.C. and Auron, P.E. (1994) Transcription factor NF-IL6 and CREB recognize a common essential site in the human prointerleukin 1β gene. Mol. Cell. Biol., 14, 7285-7297.
57. Urban, M.B. and Baeuerle, P.A. (1990) The 65-kD subunit of NF-κB is a receptor for IκB and a modulator of DNA-binding specificity. Genes Dev., 4, 1975-1984.
58. Verma, I.M., Stevenson, J.-K., Schwarz, E.M., van Antwerp, D. and Miyamoto, S. (1995) Rel/NF-κB/IκB family: intimate tales of association and dissociation. Genes Dev., 9, 2723-2735.
59. von der Ahe, D., Janich, S., Scheidereit, C. Renkawitz, R., Schütz, G. and Beato, M. (1985) Glucocorticoid and progesterone receptors bind to the same sites in two hormonally regulated promoters. Nature, 313, 706-709.
60. Wade, E.J., Heck, S. and Cato, A.C.B. (1995) Glucocorticoid receptor-activator protein-I interactions in drug design. Biochem. Soc. Trans., 23, 946-952.
61. Wehle, H., Moll, J. and Cato, A.C.B. (1995) Molecular identification of steroid analogs with dissociated antiprogestin activities. Steroids, 60, 368-374.
62. Wulczyn, F.G., Naumann, M. and Scheidereit, C. (1992) Candidate protooncogene bcl-3 encodes a subunit-specific inhibitor of transcription factor NF-κB. Nature, 358, 597-599.
63. Yang-Yen, H.-F., Chambard, J.-C., Sun, Y.-L., Smeal, T., Schmidt, T.J., Drouin, J. and Karin, M. (1990). Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell. 62, 1205-1215.
64. Zabel, U. and Baeuerle, P.A. (1990) Purified human IκB can rapidly dissociate the complex of the NF-κB transcription factor with its cognate DNA. Cell, 61, 255-265.
65. Zentel, H.J. and Töpert, M. (1994) Preclinical evaluation of a new topical corticosteroid methylprednisolone aceponate. J. Eur. Acad. Dermatol. Venereol., 3(Suppl. 1), 32-38.
66. Zhang, X.-K., Wills, K.N., Husmann, T. and Pfahl, M. (1991) Novel pathway for thyroid hormone receptor action through interaction with jun and fos oncogene activities. Mol. Cell. Biol., 11, 6016-6025.