Electronic Cigarette Vapor with Nicotine Causes Airway Mucociliary Dysfunction Preferentially via TRPA1 Receptors

Am J Respir Crit Care Med. 2019 Nov 1;200(9):1134-1145. doi: 10.1164/rccm.201811-2087OC.

Abstract

Rationale: Electronic cigarette (e-cig) use has been widely adopted under the perception of safety. However, possibly adverse effects of e-cig vapor in never-smokers are not well understood.Objectives: To test the effects of nicotine-containing e-cig vapors on airway mucociliary function in differentiated human bronchial epithelial cells isolated from never-smokers and in the airways of a novel, ovine large animal model.Methods: Mucociliary parameters were measured in human bronchial epithelial cells and in sheep. Systemic nicotine delivery to sheep was quantified using plasma cotinine levels, measured by ELISA.Measurements and Main Results:In vitro, exposure to e-cig vapor reduced airway surface liquid hydration and increased mucus viscosity of human bronchial epithelial cells in a nicotine-dependent manner. Acute nicotine exposure increased intracellular calcium levels, an effect primarily dependent on TRPA1 (transient receptor potential ankyrin 1). TRPA1 inhibition with A967079 restored nicotine-mediated impairment of mucociliary parameters including mucus transport in vitro. Sheep tracheal mucus velocity, an in vivo measure of mucociliary clearance, was also reduced by e-cig vapor. Nebulized e-cig liquid containing nicotine also reduced tracheal mucus velocity in a dose-dependent manner and elevated plasma cotinine levels. Importantly, nebulized A967079 reversed the effects of e-cig liquid on sheep tracheal mucus velocity.Conclusions: Our findings show that inhalation of e-cig vapor causes airway mucociliary dysfunction in vitro and in vivo. Furthermore, they suggest that the main nicotine effect on mucociliary function is mediated by TRPA1 and not nicotinic acetylcholine receptors.

Keywords: TRPA1; airway epithelium; electronic nicotine delivery systems; mucociliary transport; mucus.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Culture Techniques
  • Cotinine
  • E-Cigarette Vapor / pharmacology*
  • Electronic Nicotine Delivery Systems
  • Epithelial Cells / drug effects*
  • Epithelial Cells / metabolism
  • Ganglionic Stimulants / pharmacology*
  • Humans
  • Mucociliary Clearance / drug effects*
  • Nicotine / pharmacology*
  • Sheep
  • TRPA1 Cation Channel / metabolism*
  • Vaping

Substances

  • E-Cigarette Vapor
  • Ganglionic Stimulants
  • TRPA1 Cation Channel
  • TRPA1 protein, human
  • Nicotine
  • Cotinine