Glucocorticoid and TNF signaling converge at A20 (TNFAIP3) to repress airway smooth muscle cytokine expression

Am J Physiol Lung Cell Mol Physiol. 2016 Aug 1;311(2):L421-32. doi: 10.1152/ajplung.00179.2016. Epub 2016 Jul 1.

Abstract

Airway smooth muscle is a major target tissue for glucocorticoid (GC)-based asthma therapies, however, molecular mechanisms through which the GC receptor (GR) exerts therapeutic effects in this key airway cell type have not been fully elucidated. We previously identified the nuclear factor-κB (NF-κB) inhibitor, A20 (TNFAIP3), as a mediator of cytokine repression by glucocorticoids (GCs) in airway epithelial cells and defined cooperative regulation of anti-inflammatory genes by GR and NF-κB as a key mechanistic underpinning of airway epithelial GR function. Here, we expand on these findings to determine whether a similar mechanism is operational in human airway smooth muscle (HASM). Using HASM cells derived from normal and fatal asthma samples as an in vitro model, we demonstrate that GCs spare or augment TNF-mediated induction of A20 (TNFAIP3), TNIP1, and NFKBIA, all implicated in negative feedback control of NF-κB-driven inflammatory processes. We applied chromatin immunoprecipitation and reporter analysis to show that GR and NF-κB directly regulate A20 expression in HASM through cooperative induction of an intronic enhancer. Using overexpression, we show for the first time that A20 and its interacting partner, TNIP1, repress TNF signaling in HASM cells. Moreover, we applied small interfering RNA-based gene knockdown to demonstrate that A20 is required for maximal cytokine repression by GCs in HASM. Taken together, our data suggest that inductive regulation of A20 by GR and NF-κB contributes to cytokine repression in HASM.

Keywords: NF-κB; airway smooth muscle; cytokine; glucocorticoid; tumor necrosis factor.

MeSH terms

  • Adolescent
  • Asthma / metabolism
  • Binding Sites
  • Cells, Cultured
  • Cytokines / biosynthesis*
  • Cytokines / genetics
  • Cytokines / metabolism
  • Dexamethasone / pharmacology*
  • Enhancer Elements, Genetic
  • Female
  • Gene Silencing
  • Glucocorticoids / pharmacology*
  • Humans
  • Male
  • Middle Aged
  • Muscle, Smooth / drug effects
  • Muscle, Smooth / metabolism*
  • NF-kappa B / metabolism
  • Protein Binding
  • Receptors, Glucocorticoid / metabolism
  • Signal Transduction
  • Transcription, Genetic
  • Transcriptional Activation
  • Tumor Necrosis Factor alpha-Induced Protein 3 / metabolism*
  • Tumor Necrosis Factor-alpha / physiology*
  • Young Adult

Substances

  • Cytokines
  • Glucocorticoids
  • NF-kappa B
  • Receptors, Glucocorticoid
  • TNF protein, human
  • Tumor Necrosis Factor-alpha
  • Dexamethasone
  • TNFAIP3 protein, human
  • Tumor Necrosis Factor alpha-Induced Protein 3