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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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O. L. Sierra, S.-L. Cheng, A. P. Loewy, N. Charlton-Kachigian, and D. A. Towler (2004)
J. Biol. Chem. 279, 32913-32923
   Abstract »    Full Text »    PDF »
Inhibition of RNA Polymerase II Phosphorylation by a Viral Interferon Antagonist.
D. Thomas, G. Blakqori, V. Wagner, M. Banholzer, N. Kessler, R. M. Elliott, O. Haller, and F. Weber (2004)
J. Biol. Chem. 279, 31471-31477
   Abstract »    Full Text »    PDF »
CtBP Contributes Quantitatively to Knirps Repression Activity in an NAD Binding-Dependent Manner.
M. Sutrias-Grau and D. N. Arnosti (2004)
Mol. Cell. Biol. 24, 5953-5966
   Abstract »    Full Text »    PDF »
Glucocorticoids and Tumor Necrosis Factor Alpha Cooperatively Regulate Toll-Like Receptor 2 Gene Expression.
M. A. Hermoso, T. Matsuguchi, K. Smoak, and J. A. Cidlowski (2004)
Mol. Cell. Biol. 24, 4743-4756
   Abstract »    Full Text »    PDF »
Conjugated Linoleic Acid Blocks Estrogen Signaling in Human Breast Cancer Cells.
P. Tanmahasamut, J. Liu, L. B. Hendry, and N. Sidell (2004)
J. Nutr. 134, 674-680
   Abstract »    Full Text »    PDF »
Transcriptional Regulation of Limulus Factor C: REPRESSION OF AN NF{kappa}B MOTIF MODULATES ITS RESPONSIVENESS TO BACTERIAL LIPOPOLYSACCHARIDE.
L. Wang, B. Ho, and J. L. Ding (2003)
J. Biol. Chem. 278, 49428-49437
   Abstract »    Full Text »    PDF »
Interactions between the Aryl Hydrocarbon Receptor and P-TEFb: SEQUENTIAL RECRUITMENT OF TRANSCRIPTION FACTORS AND DIFFERENTIAL PHOSPHORYLATION OF C-TERMINAL DOMAIN OF RNA POLYMERASE II AT cyp1a1 PROMOTER.
Y. Tian, S. Ke, M. Chen, and T. Sheng (2003)
J. Biol. Chem. 278, 44041-44048
   Abstract »    Full Text »    PDF »
Dexamethasone Enhances Osteoclast Formation Synergistically with Transforming Growth Factor-{beta} by Stimulating the Priming of Osteoclast Progenitors for Differentiation into Osteoclasts.
A. Takuma, T. Kaneda, T. Sato, S. Ninomiya, M. Kumegawa, and Y. Hakeda (2003)
J. Biol. Chem. 278, 44667-44674
   Abstract »    Full Text »    PDF »
Agonist and Chemopreventative Ligands Induce Differential Transcriptional Cofactor Recruitment by Aryl Hydrocarbon Receptor.
E. V. Hestermann and M. Brown (2003)
Mol. Cell. Biol. 23, 7920-7925
   Abstract »    Full Text »    PDF »
Identification of Glucocorticoid Receptor Domains Involved in Transrepression of Transforming Growth Factor-{beta} Action.
G. Li, S. Wang, and T. D. Gelehrter (2003)
J. Biol. Chem. 278, 41779-41788
   Abstract »    Full Text »    PDF »
CIITA regulates transcription onset via Ser5-phosphorylation of RNA Pol II.
C. Spilianakis, A. Kretsovali, T. Agalioti, T. Makatounakis, D. Thanos, and J. Papamatheakis (2003)
EMBO J. 22, 5125-5136
   Abstract »    Full Text »    PDF »
Functional Analysis of Three Genetic Polymorphisms in the Glucocorticoid Receptor Gene.
S. Koyano, Y. Saito, M. Nagano, K. Maekawa, Y. Kikuchi, N. Murayama, T. Fujino, S. Ozawa, T. Nakajima, K. Matsumoto, et al. (2003)
J. Pharmacol. Exp. Ther. 307, 110-116
   Abstract »    Full Text »    PDF »
Dexamethasone suppresses iNOS yet induces GTPCH and CAT-2 mRNA expression in rat lungs.
J. W. Skimming, O. Nasiroglu, C.-J. Huang, C. E. Wood, B. R. Stevens, I. U. L. Haque, P. O. Scumpia, and P. J. Sarcia (2003)
Am J Physiol Lung Cell Mol Physiol 285, L484-L491
   Abstract »    Full Text »    PDF »
The thyroid hormone receptor antagonizes CREB-mediated transcription.
M. Mendez-Pertuz, A. Sanchez-Pacheco, and A. Aranda (2003)
EMBO J. 22, 3102-3112
   Abstract »    Full Text »    PDF »
NF-{kappa}B signalling is inhibited by glucocorticoid receptor and STAT6 via distinct mechanisms.
G. Nelson, G. J. C. Wilde, D. G. Spiller, S. M. Kennedy, D. W. Ray, E. Sullivan, J. F. Unitt, and M. R. H. White (2003)
J. Cell Sci. 116, 2495-2503
   Abstract »    Full Text »    PDF »
Modulation of the folate receptor type {beta} gene by coordinate actions of retinoic acid receptors at activator Sp1/ets and repressor AP-1 sites.
H. Hao, H. Qi, and M. Ratnam (2003)
Blood 101, 4551-4560
   Abstract »    Full Text »    PDF »

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