TNF-α-induces airway hyperresponsiveness to cholinergic stimulation in guinea pig airways

Br J Pharmacol. 2012 Mar;165(6):1978-1991. doi: 10.1111/j.1476-5381.2011.01675.x.

Abstract

Background and purpose: TNF-α is an inflammatory cytokine implicated in the pathogenesis of asthma and it causes airway inflammation, bronchoconstriction and airway hyperresponsiveness to a number of spasmogens following inhalation.

Experimental approach: We compared contractions of guinea pig isolated trachea incubated with saline or TNF-α for 1, 2 or 4 days to electrical field stimulation (EFS), 5-HT or methacholine. In addition, we compared bronchoconstriction in anaesthetized guinea pigs 6 h after intratracheal instillation of saline or TNF-α to vagal nerve stimulation, i.v. 5-HT or methacholine. Differential counts were performed on the bronchoalvelolar lavage fluid (BALF).

Key results: Maximum contractions to methacholine, 5-HT and EFS were not different between freshly prepared and saline-incubated tissues. Exposure to TNF-α concentration-dependently potentiated contractions to 5-HT and EFS, but not methacholine. All contractions were atropine-sensitive, but not hexamethonium-sensitive. 5-HT-evoked contractions were inhibited by ketanserin or epithelial denudation. Only EFS-evoked contractions were tetrodotoxin-sensitive. Vagal stimulation, i.v. 5-HT or MCh caused a significant atropine-sensitive, frequency- and dose-dependent bronchoconstriction and decreased blood pressure similarly in both saline and TNF-α pre-treated animals. TNF-α potentiated the bronchoconstriction to vagal stimulation and 5-HT, but not MCh. The BALF from saline-treated animals contained predominantly macrophages, whereas that from TNF-α-treated animals contained neutrophils.

Conclusions and implications: TNF-α caused airway hyperresponsiveness to nerve stimulation in vivo and increased contractility in vitro. However, responsiveness to MCh was unchanged, suggesting a pre-synaptic action of TNF-α on parasympathetic nerves. TNF-α-induced airway hyperresponsiveness to 5-HT suggested an increased 5-HT(2A) receptor-mediated acetylcholine release from epithelial cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blood Pressure
  • Bronchial Hyperreactivity / physiopathology*
  • Bronchoalveolar Lavage Fluid / cytology
  • Cell Count
  • Electric Stimulation
  • Guinea Pigs
  • Heart Rate
  • In Vitro Techniques
  • Male
  • Methacholine Chloride / pharmacology
  • Muscarinic Agonists / pharmacology
  • Muscle Contraction / physiology*
  • Muscle, Smooth / physiology
  • Serotonin / pharmacology
  • Serotonin Receptor Agonists / pharmacology
  • Trachea / physiology
  • Tumor Necrosis Factor-alpha / physiology*

Substances

  • Muscarinic Agonists
  • Serotonin Receptor Agonists
  • Tumor Necrosis Factor-alpha
  • Methacholine Chloride
  • Serotonin