Thioredoxin-mediated denitrosylation regulates cytokine-induced nuclear factor κB (NF-κB) activation

J Biol Chem. 2014 Jan 31;289(5):3066-72. doi: 10.1074/jbc.M113.503938. Epub 2013 Dec 12.

Abstract

S-nitrosylation of nuclear factor κB (NF-κB) on the p65 subunit of the p50/p65 heterodimer inhibits NF-κB DNA binding activity. We have recently shown that p65 is constitutively S-nitrosylated in the lung and that LPS-induced injury elicits a decrease in SNO-p65 levels concomitant with NF-κB activation in the respiratory epithelium and initiation of the inflammatory response. Here, we demonstrate that TNFα-mediated activation of NF-κB in the respiratory epithelium similarly induces p65 denitrosylation. This process is mediated by the denitrosylase thioredoxin (Trx), which becomes activated upon cytokine-induced degradation of thioredoxin-interacting protein (Txnip). Similarly, inhibition of Trx activity in the lung attenuates LPS-induced SNO-p65 denitrosylation, NF-κB activation, and airway inflammation, supporting a pathophysiological role for this mechanism in lung injury. These data thus link stimulus-coupled activation of NF-κB to a specific, protein-targeted denitrosylation mechanism and further highlight the importance of S-nitrosylation in the regulation of the immune response.

Keywords: Lung Injury; NF-κB; Nitric Oxide; S-nitrosylation; Thioredoxin.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Adenocarcinoma
  • Animals
  • Cell Line, Tumor
  • Cytokines / metabolism
  • Disease Models, Animal
  • HEK293 Cells
  • Humans
  • Lipopolysaccharides / toxicity
  • Lung Injury / immunology
  • Lung Injury / metabolism*
  • Lung Injury / pathology
  • Lung Neoplasms
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-kappa B p50 Subunit / metabolism
  • Nitric Oxide / metabolism
  • Reactive Nitrogen Species / metabolism
  • Respiratory Mucosa / immunology
  • Respiratory Mucosa / metabolism
  • Respiratory Mucosa / pathology
  • Signal Transduction / immunology*
  • Thioredoxins / genetics
  • Thioredoxins / immunology
  • Thioredoxins / metabolism*
  • Transcription Factor RelA / metabolism*

Substances

  • Cytokines
  • Lipopolysaccharides
  • NF-kappa B p50 Subunit
  • Reactive Nitrogen Species
  • TXN protein, human
  • Transcription Factor RelA
  • Txn1 protein, mouse
  • Nitric Oxide
  • Thioredoxins