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Molecular Endocrinology, Vol 9, 401-412, Copyright © 1995 by Endocrine Society

ARTICLES

Negative cross-talk between RelA and the glucocorticoid receptor: a possible mechanism for the antiinflammatory action of glucocorticoids

E Caldenhoven, J Liden, S Wissink, A Van de Stolpe, J Raaijmakers, L Koenderman, S Okret, JA Gustafsson and PT Van der Saag
Hubrecht Laboratory, Netherlands Institute for Developmental Biology, Utrecht.

Glucocorticoids are efficient antiinflammatory agents, and their effects include transcriptional repression of several cytokines and adhesion molecules. Whereas glucocorticoids down-regulate the expression of genes relevant during inflammation, nuclear factor (NF)- kappa B/Rel proteins function as important positive regulators of these genes. The expression of intercellular adhesion molecule-1 (ICAM-1), which plays an essential role in recruitment and migration of leukocytes to sites of inflammation, is also down-regulated by glucocorticoids. We found that a functional NF-kappa B site in the ICAM- 1 promoter, which can be activated by either 12-O-tetradecanoylphorbol- 13-acetate or tumor necrosis factor-alpha (TNF alpha), is also the target for glucocorticoids. In this report we present evidence that the ligand-activated glucocorticoid receptor (GR) is able to repress RelA- mediated activation of the ICAM-1 NF-kappa B site. Conversely, transcriptional activation by GR via a glucocorticoid response element is specifically repressed by RelA, but not by other NF-kappa B/Rel family members. Mutational analysis of GR demonstrates that the DNA binding domain and the ligand binding domain are required for the functional repression of NF-kappa B activation. Despite the importance of the DNA binding domain, we found that the transcriptional repression of NF-kappa B, mediated by GR, is not caused by binding of GR to the ICAM-1 NF-kappa B element, but by a physical interaction between the GR and RelA protein. The repressive effect of GR on NF-kappa B-mediated activation was not shared by other steroid/thyroid receptors. Only the progesterone receptor, which belongs to the same subfamily as GR and which possesses high homology with GR, was able to repress NF-kappa B- mediated transcription. These studies highlight a possible molecular mechanism that can explain the antiinflammatory effects of glucocorticoid treatment during inflammation.


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 EndocrinologyHome page
J. Chung, E. S. Park, D. Kim, J. M. Suh, H. K. Chung, J. Kim, H. Kim, S. J. Park, O-Y. Kwon, H. K. Ro, et al.
Thyrotropin Modulates Interferon-{gamma}-Mediated Intercellular Adhesion Molecule-1 Gene Expression by Inhibiting Janus Kinase-1 and Signal Transducer and Activator of Transcription-1 Activation in Thyroid Cells
Endocrinology, June 1, 2000; 141(6): 2090 - 2097.
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R. Dimri, Y. Sharabi, and J. Shoham
Specific Inhibition of Glucocorticoid-Induced Thymocyte Apoptosis by Substance P
J. Immunol., March 1, 2000; 164(5): 2479 - 2486.
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R. M. Sapolsky, L. M. Romero, and A. U. Munck
How Do Glucocorticoids Influence Stress Responses? Integrating Permissive, Suppressive, Stimulatory, and Preparative Actions
Endocr. Rev., February 1, 2000; 21(1): 55 - 89.
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S. Wissink, O. Meijer, D. Pearce, B. van der Burg, and P. T. van der Saag
Regulation of the Rat Serotonin-1A Receptor Gene by Corticosteroids
J. Biol. Chem., January 14, 2000; 275(2): 1321 - 1326.
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 Plant CellHome page
H.-H. Woo, M. J. Orbach, A. M. Hirsch, and M. C. Hawes
Meristem-Localized Inducible Expression of a UDP-Glycosyltransferase Gene Is Essential for Growth and Development in Pea and Alfalfa
PLANT CELL, December 1, 1999; 11(12): 2303 - 2316.
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 GutHome page
K Thiele, A Bierhaus, F Autschbach, M Hofmann, W Stremmel, H Thiele, R Ziegler, and P P Nawroth
Cell specific effects of glucocorticoid treatment on the NF-kappa Bp65/Ikappa Balpha system in patients with Crohn's disease
Gut, November 1, 1999; 45(5): 693 - 704.
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A Tailor, A Tomlinson, A Salas, J Panes, D N Granger, R J Flower, and M Perretti
Dexamethasone inhibition of leucocyte adhesion to rat mesenteric postcapillary venules: role of intercellular adhesion molecule 1 and KC
Gut, November 1, 1999; 45(5): 705 - 712.
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D. W. Ray, C.-S. Suen, A. Brass, J. Soden, and A. White
Structure/Function of the Human Glucocorticoid Receptor: Tyrosine 735 Is Important for Transactivation
Mol. Endocrinol., November 1, 1999; 13(11): 1855 - 1863.
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S. P. Malkoski and R. I. Dorin
Composite Glucocorticoid Regulation at a Functionally Defined Negative Glucocorticoid Response Element of the Human Corticotropin-Releasing Hormone Gene
Mol. Endocrinol., October 1, 1999; 13(10): 1629 - 1644.
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H. A. Kester, C. Blanchetot, J. den Hertog, P. T. van der Saag, and B. van der Burg
Transforming Growth Factor-beta -stimulated Clone-22 Is a Member of a Family of Leucine Zipper Proteins That Can Homo- and Heterodimerize and Has Transcriptional Repressor Activity
J. Biol. Chem., September 24, 1999; 274(39): 27439 - 27447.
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R. H. Oakley, C. M. Jewell, M. R. Yudt, D. M. Bofetiado, and J. A. Cidlowski
The Dominant Negative Activity of the Human Glucocorticoid Receptor beta Isoform. SPECIFICITY AND MECHANISMS OF ACTION
J. Biol. Chem., September 24, 1999; 274(39): 27857 - 27866.
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L. I. McKay and J. A. Cidlowski
Molecular Control of Immune/Inflammatory Responses: Interactions Between Nuclear Factor-{kappa}B and Steroid Receptor-Signaling Pathways
Endocr. Rev., August 1, 1999; 20(4): 435 - 459.
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 EndocrinologyHome page
P. Aarnisalo, H. Santti, H. Poukka, J. J. Palvimo, and O. A. Jänne
Transcription Activating and Repressing Functions of the Androgen Receptor Are Differentially Influenced by Mutations in the Deoxyribonucleic Acid-Binding Domain
Endocrinology, July 1, 1999; 140(7): 3097 - 3105.
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N. Subramaniam, E. Treuter, and S. Okret
Receptor Interacting Protein RIP140 Inhibits Both Positive and Negative Gene Regulation by Glucocorticoids
J. Biol. Chem., June 18, 1999; 274(25): 18121 - 18127.
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 CarcinogenesisHome page
B. Glinghammar, K. Holmberg, and J. Rafter
Effects of colonic lumenal components on AP-1-dependent gene transcription in cultured human colon carcinoma cells
Carcinogenesis, June 1, 1999; 20(6): 969 - 976.
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J. Anrather, V. Csizmadia, M. P. Soares, and H. Winkler
Regulation of NF-kappa B RelA Phosphorylation and Transcriptional Activity by p21ras and Protein Kinase Czeta in Primary Endothelial Cells
J. Biol. Chem., May 7, 1999; 274(19): 13594 - 13603.
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Z. F. Cheema, S. B. Wade, M. Sata, K. Walsh, F. Sohrabji, and R. C. Miranda
Fas/Apo [Apoptosis]-1 and Associated Proteins in the Differentiating Cerebral Cortex: Induction of Caspase-Dependent Cell Death and Activation of NF-kappa B
J. Neurosci., March 1, 1999; 19(5): 1754 - 1770.
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Y. Tian, S. Ke, Michael. S. Denison, A. B. Rabson, and M. A. Gallo
Ah Receptor and NF-kappa B Interactions, a Potential Mechanism for Dioxin Toxicity
J. Biol. Chem., January 1, 1999; 274(1): 510 - 515.
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S.-Y. Na, H.-S. Choi, J. W. Kim, D. S. Na, and J. W. Lee
Bcl3, an Ikappa B Protein, as a Novel Transcription Coactivator of the Retinoid X Receptor
J. Biol. Chem., November 20, 1998; 273(47): 30933 - 30938.
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 J. Biol. Chem.Home page
K.-A. Sheppard, K. M. Phelps, A. J. Williams, D. Thanos, C. K. Glass, M. G. Rosenfeld, M. E. Gerritsen, and T. Collins
Nuclear Integration of Glucocorticoid Receptor and Nuclear Factor-kappa B Signaling by CREB-binding Protein and Steroid Receptor Coactivator-1
J. Biol. Chem., November 6, 1998; 273(45): 29291 - 29294.
[Abstract] [Full Text] [PDF]

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 GutHome page
R M SCHMID, G ADLER, S LIPTAY, S SCHREIBER, S NIKOLAUS, and J HAMPE
Activation of NFkappa B in inflammatory bowel disease • Reply
Gut, October 1, 1998; 43(4): 586c - 586.
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N. Subramaniam, W. Cairns, and S. Okret
Glucocorticoids Repress Transcription from a Negative Glucocorticoid Response Element Recognized by Two Homeodomain-containing Proteins, Pbx and Oct-1
J. Biol. Chem., September 4, 1998; 273(36): 23567 - 23574.
[Abstract] [Full Text] [PDF]

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 EndocrinologyHome page
J. Ramdas and J. M. Harmon
Glucocorticoid-Induced Apoptosis and Regulation of NF-{kappa}B Activity in Human Leukemic T Cells
Endocrinology, September 1, 1998; 139(9): 3813 - 3821.
[Abstract] [Full Text] [PDF]

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 BloodHome page
M. Lansink, P. Koolwijk, V. van Hinsbergh, and T. Kooistra
Effect of Steroid Hormones and Retinoids on the Formation of Capillary-Like Tubular Structures of Human Microvascular Endothelial Cells in Fibrin Matrices Is Related to Urokinase Expression
Blood, August 1, 1998; 92(3): 927 - 938.
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F. Lezoualc'h, Y. Sagara, F. Holsboer, and C. Behl
High Constitutive NF-kappa B Activity Mediates Resistance to Oxidative Stress in Neuronal Cells
J. Neurosci., May 1, 1998; 18(9): 3224 - 3232.
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 Mol. Endocrinol.Home page
S. Wissink, E. C. van Heerde, B. van der Burg, and P. T. van der Saag
A Dual Mechanism Mediates Repression of NF-{kappa}B Activity by Glucocorticoids
Mol. Endocrinol., March 1, 1998; 12(3): 355 - 363.
[Abstract] [Full Text]

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 Am. J. Respir. Crit. Care Med.Home page
P. J. BARNES, S. PEDERSEN, and W. W. BUSSE
Efficacy and Safety of Inhaled Corticosteroids . New Developments
Am. J. Respir. Crit. Care Med., March 1, 1998; 157(3): S1 - 53.
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 Mol. Endocrinol.Home page
L. I. McKay and J. A. Cidlowski
Cross-Talk between Nuclear Factor-{kappa}B and the Steroid Hormone Receptors: Mechanisms of Mutual Antagonism
Mol. Endocrinol., January 1, 1998; 12(1): 45 - 56.
[Abstract] [Full Text]

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 Proc. Natl. Acad. Sci. USAHome page
K. De Bosscher, M. L. Schmitz, W. Vanden Berghe, S. Plaisance, W. Fiers, and G. Haegeman
Glucocorticoid-mediated repression of nuclear factor-kappa Bdependent transcription involves direct interference with transactivation
PNAS, December 9, 1997; 94(25): 13504 - 13509.
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Z. Zhang, S. Jones, J. S. Hagood, N. L. Fuentes, and G. M. Fuller
STAT3 Acts as a Co-activator of Glucocorticoid Receptor Signaling
J. Biol. Chem., December 5, 1997; 272(49): 30607 - 30610.
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 J. Biol. Chem.Home page
H. Chen, G. Srinivasan, and E. B. Thompson
Protein-Protein Interactions Are Implied in Glucocorticoid Receptor Mutant 465*-mediated Cell Death
J. Biol. Chem., October 10, 1997; 272(41): 25873 - 25880.
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 J. Biol. Chem.Home page
S. Wissink, E. C. van Heerde, M. L. Schmitz, E. Kalkhoven, B. van der Burg, P. A. Baeuerle, and P. T. van der Saag
Distinct Domains of the RelA NF-kappa B Subunit Are Required for Negative Cross-talk and Direct Interaction with the Glucocorticoid Receptor
J. Biol. Chem., August 29, 1997; 272(35): 22278 - 22284.
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 J. Biol. Chem.Home page
T. Meyer, D. B. Starr, and J. Carlstedt-Duke
The Rat Glucocorticoid Receptor Mutant K461A Differentiates between Two Different Mechanisms of Transrepression
J. Biol. Chem., August 22, 1997; 272(34): 21090 - 21095.
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 J. Biol. Chem.Home page
J. Liden, F. Delaunay, I. Rafter, J.-A. Gustafsson, and S. Okret
A New Function for the C-terminal Zinc Finger of the Glucocorticoid Receptor. REPRESSION OF RelA TRANSACTIVATION
J. Biol. Chem., August 22, 1997; 272(34): 21467 - 21472.
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 Mol. Endocrinol.Home page
B. M. Vayssière, S. Dupont, A. Choquart, F. Petit, T. Garcia, C. Marchandeau, H. Gronemeyer, and M. Resche-Rigon
Synthetic Glucocorticoids That Dissociate Transactivation and AP-1 Transrepression Exhibit Antiinflammatory Activity in Vivo
Mol. Endocrinol., August 1, 1997; 11(9): 1245 - 1255.
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 J. Pharmacol. Exp. Ther.Home page
J. J. Breton and M. C. Chabot-Fletcher
The Natural Product Hymenialdisine Inhibits Interleukin-8 Production in U937 Cells by Inhibition of Nuclear Factor-kappa B
J. Pharmacol. Exp. Ther., July 1, 1997; 282(1): 459 - 466.
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 Mol. Endocrinol.Home page
P. de Lange, J. W. Koper, N. A. T. M. Huizenga, A. O. Brinkmann, F. H. de Jong, M. Karl, G. P. Chrousos, and S. W. J. Lamberts
Differential Hormone-Dependent Transcriptional Activation and -Repression by Naturally Occurring Human Glucocorticoid Receptor Variants
Mol. Endocrinol., July 1, 1997; 11(8): 1156 - 1164.
[Abstract] [Full Text]

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 Endocr. Rev.Home page
D. Ray and S. Melmed
Pituitary Cytokine and Growth Factor Expression and Action
Endocr. Rev., April 1, 1997; 18(2): 206 - 228.
[Abstract] [Full Text]

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 EndocrinologyHome page
T. Bui, C. Kuo, P. Rotwein, and D. S. Straus
Prostaglandin A2 Specifically Represses Insulin-Like Growth Factor-I Gene Expression in C6 Rat Glioma Cells
Endocrinology, March 1, 1997; 138(3): 985 - 993.
[Abstract] [Full Text] [PDF]

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 ScienceHome page
C.-Y. Wang, M. W. Mayo, and A. S. Baldwin Jr.
TNF- and Cancer Therapy-Induced Apoptosis: Potentiation by Inhibition of NF-kappa B
Science, November 1, 1996; 274(5288): 784 - 787.
[Abstract] [Full Text]


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