TNF-α inhibits glucocorticoid receptor-induced gene expression by reshaping the GR nuclear cofactor profile

Proc Natl Acad Sci U S A. 2019 Jun 25;116(26):12942-12951. doi: 10.1073/pnas.1821565116. Epub 2019 Jun 10.

Abstract

Glucocorticoid resistance (GCR) is defined as an unresponsiveness to the therapeutic effects, including the antiinflammatory ones of glucocorticoids (GCs) and their receptor, the glucocorticoid receptor (GR). It is a problem in the management of inflammatory diseases and can be congenital as well as acquired. The strong proinflammatory cytokine TNF-alpha (TNF) induces an acute form of GCR, not only in mice, but also in several cell lines: e.g., in the hepatoma cell line BWTG3, as evidenced by impaired Dexamethasone (Dex)-stimulated direct GR-dependent gene up- and down-regulation. We report that TNF has a significant and broad impact on this transcriptional performance of GR, but no impact on nuclear translocation, dimerization, or DNA binding capacity of GR. Proteome-wide proximity-mapping (BioID), however, revealed that the GR interactome was strongly modulated by TNF. One GR cofactor that interacted significantly less with the receptor under GCR conditions is p300. NFκB activation and p300 knockdown both reduced direct transcriptional output of GR whereas p300 overexpression and NFκB inhibition reverted TNF-induced GCR, which is in support of a cofactor reshuffle model. This hypothesis was supported by FRET studies. This mechanism of GCR opens avenues for therapeutic interventions in GCR diseases.

Keywords: genetics; mechanism; regulation; transcription.

MeSH terms

  • A549 Cells
  • Animals
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism
  • Dexamethasone / pharmacology
  • Dexamethasone / therapeutic use
  • Down-Regulation / drug effects
  • Down-Regulation / immunology
  • Drug Resistance / genetics*
  • E1A-Associated p300 Protein / genetics
  • E1A-Associated p300 Protein / metabolism*
  • Female
  • Gene Knockdown Techniques
  • Glucocorticoids / pharmacology*
  • Glucocorticoids / therapeutic use
  • HEK293 Cells
  • Humans
  • Inflammation / drug therapy*
  • Inflammation / immunology
  • Mice
  • NF-kappa B / metabolism
  • Protein Interaction Mapping
  • Protein Interaction Maps / drug effects
  • Protein Interaction Maps / immunology
  • RNA, Small Interfering / metabolism
  • RNA-Seq
  • Receptors, Glucocorticoid / immunology
  • Receptors, Glucocorticoid / metabolism*
  • Tumor Necrosis Factor-alpha / metabolism*
  • Up-Regulation / drug effects
  • Up-Regulation / immunology

Substances

  • Glucocorticoids
  • NF-kappa B
  • NR3C1 protein, human
  • RNA, Small Interfering
  • Receptors, Glucocorticoid
  • TNF protein, human
  • Tnf protein, mouse
  • Tumor Necrosis Factor-alpha
  • Dexamethasone
  • E1A-Associated p300 Protein
  • EP300 protein, human
  • Ep300 protein, mouse