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Genes & Dev. 14 (18): 2314-2329

Copyright © 2000 by Cold Spring Harbor Laboratory Press.

Vol. 14, No. 18, pp. 2314-2329, September 15, 2000

RESEARCH PAPER
The glucocorticoid receptor inhibits NFkappa B by interfering with serine-2 phosphorylation of the RNA polymerase II carboxy-terminal domain

Robert M. Nissen, and Keith R. Yamamoto1

Departments of Cellular and Molecular Pharmacology, and Biochemistry and Biophysics, PIBS Biochemistry and Molecular Biology Program, University of California, San Francisco, San Francisco, California 94143-0450, USA

Glucocorticoids repress NFkappa B-mediated activation of proinflammatory genes such as interleukin-8 (IL-8) and ICAM-1. Our experiments suggest that the glucocorticoid receptor (GR) confers this effect by associating through protein-protein interactions with NFkappa B bound at each of these genes. That is, we show that the GR zinc binding region (ZBR), which includes the DNA binding and dimerization functions of the receptor, binds directly to the dimerization domain of the RelA subunit of NFkappa B in vitro and that the ZBR is sufficient to associate with RelA bound at NFkappa B response elements in vivo. Moreover, we demonstrate in vivo and in vitro that GR does not disrupt DNA binding by NFkappa B. In transient transfections, we found that the GR ligand binding domain is essential for repression of NFkappa B but not for association with it and that GR can repress an NFkappa B derivative bearing a heterologous activation domain. We used chromatin immunoprecipitation assays in untransfected A549 cells to infer the mechanism by which the tethered GR represses NFkappa B-activated transcription. As expected, we found that the inflammatory signal TNFalpha stimulated preinitiation complex (PIC) assembly at the IL-8 and ICAM-1 promoters and that the largest subunit of RNA polymerase II (pol II) in those complexes became phosphorylated at serines 2 and 5 in its carboxy-terminal domain (CTD) heptapeptide repeats (YSPTSPS); these modifications are required for transcription initiation. Remarkably, GR did not inhibit PIC assembly under repressing conditions, but rather interfered with phosphorylation of serine 2 of the pol II CTD.

[Key Words: Glucocorticoid receptor; transcriptional repression; intracellular receptor; RelA; chromatin; anti-inflammation]

1 Corresponding author.

GENES & DEVELOPMENT 14:2314-2329 © 2000 by Cold Spring Harbor Laboratory Press  ISSN 0890-9369/00 $5.00

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T. Valineva, J. Yang, R. Palovuori, and O. Silvennoinen (2005)
J. Biol. Chem. 280, 14989-14996
   Abstract »    Full Text »    PDF »
Glucocorticoids suppress macrophage migration inhibitory factor (MIF) expression in a cell-type-specific manner.
Z Alourfi, R P Donn, A Stevens, A Berry, A McMaster, and D W Ray (2005)
J. Mol. Endocrinol. 34, 583-595
   Abstract »    Full Text »    PDF »
Protein-Protein Interactions and Transcriptional Antagonism between the Subfamily of NGFI-B/Nur77 Orphan Nuclear Receptors and Glucocorticoid Receptor.
C. Martens, S. Bilodeau, M. Maira, Y. Gauthier, and J. Drouin (2005)
Mol. Endocrinol. 19, 885-897
   Abstract »    Full Text »    PDF »
Chronic Hyperglycemia Enhances PEPCK Gene Expression and Hepatocellular Glucose Production Via Elevated Liver Activating Protein/Liver Inhibitory Protein Ratio.
J. Shao, L. Qiao, R. C. Janssen, M. Pagliassotti, and J. E. Friedman (2005)
Diabetes 54, 976-984
   Abstract »    Full Text »    PDF »
Identification of Endogenous Glucocorticoid Repressed Genes Differentially Regulated by a Glucocorticoid Receptor Mutant Able to Separate between Nuclear Factor-{kappa}B and Activator Protein-1 Repression.
L.-G. Bladh, J. Liden, K. Dahlman-Wright, M. Reimers, S. Nilsson, and S. Okret (2005)
Mol. Pharmacol. 67, 815-826
   Abstract »    Full Text »    PDF »
Cyclin-dependent Kinase 9 Is Required for Tumor Necrosis Factor-{alpha}-stimulated Matrix Metalloproteinase-9 Expression in Human Lung Adenocarcinoma Cells.
B. Shan, Y. Zhuo, D. Chin, C. A. Morris, G. F. Morris, and J. A. Lasky (2005)
J. Biol. Chem. 280, 1103-1111
   Abstract »    Full Text »    PDF »
From Microarray to Bedside: Targeting NF-{kappa}B for Therapy of Lymphomas.
A. B. Rabson and D. Weissmann (2005)
Clin. Cancer Res. 11, 2-6
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Effects of dexamethasone on Muc5ac mucin production by primary airway goblet cells.
W. Lu, E. P. Lillehoj, and K. C. Kim (2005)
Am J Physiol Lung Cell Mol Physiol 288, L52-L60
   Abstract »    Full Text »    PDF »
Transcription Factor Binding and Induced Transcription Alter Chromosomal c-myc Replicator Activity.
M. Ghosh, G. Liu, G. Randall, J. Bevington, and M. Leffak (2004)
Mol. Cell. Biol. 24, 10193-10207
   Abstract »    Full Text »    PDF »
Glucocorticoid Ligands Specify Different Interactions with NF-{kappa}B by Allosteric Effects on the Glucocorticoid Receptor DNA Binding Domain.
H. Garside, A. Stevens, S. Farrow, C. Normand, B. Houle, A. Berry, B. Maschera, and D. Ray (2004)
J. Biol. Chem. 279, 50050-50059
   Abstract »    Full Text »    PDF »
From The Cover: Chromatin immunoprecipitation (ChIP) scanning identifies primary glucocorticoid receptor target genes.
J.-C. Wang, M. K. Derynck, D. F. Nonaka, D. B. Khodabakhsh, C. Haqq, and K. R. Yamamoto (2004)
PNAS 101, 15603-15608
   Abstract »    Full Text »    PDF »
Mechanisms of Glucocorticoid Receptor Action in Noninflammatory and Inflammatory Cells.
B. M. Necela and J. A. Cidlowski (2004)
1, 239-246
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Glucocorticoids: Effects on Gene Transcription.
I. M. Adcock, K. Ito, and P. J. Barnes (2004)
1, 247-254
   Abstract »    Full Text »    PDF »
Brg-1 Is Required for Maximal Transcription of the Human Matrix Metalloproteinase-2 Gene.
Z. Ma, M. J. Chang, R. Shah, J. Adamski, X. Zhao, and E. N. Benveniste (2004)
J. Biol. Chem. 279, 46326-46334
   Abstract »    Full Text »    PDF »
Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors.
P. C. Hollenhorst, D. A. Jones, and B. J. Graves (2004)
Nucleic Acids Res. 32, 5693-5702
   Abstract »    Full Text »    PDF »
A nuclear isoform of the focal adhesion LIM-domain protein Trip6 integrates activating and repressing signals at AP-1- and NF-{kappa}B-regulated promoters.
O. Kassel, S. Schneider, C. Heilbock, M. Litfin, M. Gottlicher, and P. Herrlich (2004)
Genes & Dev. 18, 2518-2528
   Abstract »    Full Text »    PDF »
Transcriptional activation of hTERT through the NF-{kappa}B pathway in HTLV-I-transformed cells.
U. Sinha-Datta, I. Horikawa, E. Michishita, A. Datta, J. C. Sigler-Nicot, M. Brown, M. Kazanji, J. C. Barrett, and C. Nicot (2004)
Blood 104, 2523-2531
   Abstract »    Full Text »    PDF »
Identification of Liver Receptor Homolog-1 as a Novel Regulator of Apolipoprotein AI Gene Transcription.
P. Delerive, C. M. Galardi, J. E. Bisi, E. Nicodeme, and B. Goodwin (2004)
Mol. Endocrinol. 18, 2378-2387
   Abstract »    Full Text »    PDF »

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