Glucocorticoid receptor represses proinflammatory genes at distinct steps of the transcription cycle
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Widespread anti-inflammatory actions of glucocorticoid hormones are mediated by the glucocorticoid receptor (GR), a ligand-dependent transcription factor of the nuclear receptor superfamily. In conjunction with its corepressor GR-interacting protein-1 (GRIP1), GR tethers to the DNA-bound activator protein-1 and NF-κB and represses transcription of their target proinflammatory cytokine genes. However, these target genes fall into distinct classes depending on the step of the transcription cycle that is rate-limiting for their activation: Some are controlled through RNA polymerase II (PolII) recruitment and initiation, whereas others undergo signal-induced release of paused elongation complexes into productive RNA synthesis. Whether these genes are differentially regulated by GR is unknown. Here we report that, at the initiation-controlled inflammatory genes in primary macrophages, GR inhibited LPS-induced PolII occupancy. In contrast, at the elongation-controlled genes, GR did not affect PolII recruitment or transcription initiation but promoted, in a GRIP1-dependent manner, the accumulation of the pause-inducing negative elongation factor. Consistently, GR-dependent repression of elongation-controlled genes was abolished specifically in negative elongation factor-deficient macrophages. Thus, GR:GRIP1 use distinct mechanisms to repress inflammatory genes at different stages of the transcription cycle.
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GR:GRIP1 complexes prevent recruitment of PolII to initiation-controlled inflammatory genes such as IL-1alpha and IL-1beta, and promote accumulation of pause-inducing negative elongation factor, precluding PolII release from the elongation block of genes like TNF-alpha, CCL2, and CCL3.
“In this line, very recent data point toward a role of GR:GRIP1 complexes in preventing the recruitment of PolII to initiation-controlled inflammatory genes such as IL-1α and IL-1β, and concomitantly promoting the accumulation of pause-inducing negative elongation factor, which precludes the release of PolII from the elongation block of genes like TNF-α, CCL2, and CCL3 (88).”
From The HPA – Immune Axis and the Immunomodulatory Actions of Glucocorticoids in the Brain (2014) · cites this paper as [88]
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- Authors
- Gupte, R., Muse, G. W., Chinenov, Y., Adelman, K., & Rogatsky, I.
- Affiliations
- Hospital for Special Surgery (US)
- National Institutes of Health (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-08-15
- Volume
- 110
- Issue
- 36
- Pages
- 14616-14621
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3767553
- OpenAlex
- W2029181455
- Cited by
- 70
- References
- 42
- Citations by year
- 2026: 6 · 2025: 3 · 2024: 6 · 2023: 2 · 2022: 2 · 2021: 10 · 2020: 4 · 2019: 3 · 2018: 3 · 2017: 8 · 2016: 7 · 2015: 6 · 2014: 9 · 2013: 1
- FWCI
- 5.09
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Environmental Health Sciences (Z01ES101987)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Estrogen and related hormone effects
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › NF-κB Signaling Pathways
- Keywords
- glucocorticoid receptor, GRIP1, transcriptional repression, pro-inflammatory gene expression, NELF, RNA polymerase II, transcriptional pause, transcription elongation, macrophages, lipopolysaccharide-induced inflammation, NF-κB, AP-1
- MeSH terms
- Animals, Bone Marrow Cells, Cells, Cultured, Dexamethasone, Gene Expression Regulation, Lipopolysaccharides, Macrophages, Mice, Inbred C57BL, Nerve Tissue Proteins, Receptors, Glucocorticoid, RNA Polymerase II, Transcription Factors, Transcription, Genetic, Immunoblotting, Cytokines, NF-kappa B, Mice, Knockout, Inflammation Mediators, Reverse Transcriptase Polymerase Chain Reaction, Positive Transcriptional Elongation Factor B, Adaptor Proteins, Signal Transducing, Mice
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