Crucial role of transient receptor potential ankyrin 1 and mast cells in induction of nonallergic airway hyperreactivity in mice

Am J Respir Crit Care Med. 2013 Mar 1;187(5):486-93. doi: 10.1164/rccm.201208-1358OC. Epub 2012 Dec 21.

Abstract

Rationale: Airway hyperreactivity (AHR) is a key feature of bronchial asthma, and inhalation of irritants may facilitate development of nonallergic AHR. Swimmers exposed to hypochlorite (ClO(-))-containing water show a higher risk of developing AHR. We developed a mouse model in which instillation of ClO(-) before ovalbumin (OVA) induces AHR without bronchial inflammatory cells.

Objectives: To investigate the mechanisms of ClO(-)-OVA-induced nonallergic AHR.

Methods: The involvement of the transient receptor potential ankyrin (TRPA)1 channel was checked in vivo by the use of TRPA1(-/-) mice and in vitro by Ca(2+) imaging experiments. The role of substance P (SP) was investigated by pretreating animals with the receptor antagonist RP67580, by replacing ClO(-) with SP in vivo, and by immunofluorescent staining of large airways of exposed mice. The role of mast cells was evaluated by exposing mast cell-deficient Kit(Wh)/Kit(Wsh) mice to ClO(-)-OVA with or without mast cell reconstitution.

Measurements and main results: ClO(-)-OVA did not induce AHR in TRPA1(-/-) mice, and ClO(-) generates a Ca(2+) influx in TRPA1-transfected cells. Pretreatment with RP67580 reduces ClO(-)-OVA-induced AHR, although no increased SP expression was shown in the airways. SP-OVA exposure resulted in the same AHR as induced by ClO(-)-OVA. Kit(Wsh)/Kit(Wsh) mice did not develop AHR in response to ClO(-)-OVA unless they were reconstituted with bone marrow-derived mast cells.

Conclusions: Induction of AHR by exposure to ClO(-)-OVA depends on a neuroimmune interaction that involves TRPA1-dependent stimulation of sensory neurons and mast cell activation.

Publication types

  • Evaluation Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bronchial Hyperreactivity / etiology
  • Bronchial Hyperreactivity / physiopathology*
  • Cells, Cultured
  • Hypochlorous Acid / adverse effects*
  • Irritants / adverse effects*
  • Mast Cells / immunology*
  • Mice
  • Mice, Inbred BALB C
  • Mice, Knockout
  • Neuroimmunomodulation
  • Nociceptors / immunology
  • Ovalbumin / adverse effects
  • Substance P / metabolism
  • TRPA1 Cation Channel
  • Transient Receptor Potential Channels / immunology*

Substances

  • Irritants
  • TRPA1 Cation Channel
  • Transient Receptor Potential Channels
  • Trpa1 protein, mouse
  • Substance P
  • Hypochlorous Acid
  • Ovalbumin