Airway Surface Dehydration by Transforming Growth Factor β (TGF-β) in Cystic Fibrosis Is Due to Decreased Function of a Voltage-dependent Potassium Channel and Can Be Rescued by the Drug Pirfenidone

J Biol Chem. 2015 Oct 16;290(42):25710-6. doi: 10.1074/jbc.M115.670885. Epub 2015 Sep 3.

Abstract

Transforming growth factor β1 (TGF-β1) is not only elevated in airways of cystic fibrosis (CF) patients, whose airways are characterized by abnormal ion transport and mucociliary clearance, but TGF-β1 is also associated with worse clinical outcomes. Effective mucociliary clearance depends on adequate airway hydration, governed by ion transport. Apically expressed, large-conductance, Ca(2+)- and voltage-dependent K(+) (BK) channels play an important role in this process. In this study, TGF-β1 decreased airway surface liquid volume, ciliary beat frequency, and BK activity in fully differentiated CF bronchial epithelial cells by reducing mRNA expression of the BK γ subunit leucine-rich repeat-containing protein 26 (LRRC26) and its function. Although LRRC26 knockdown itself reduced BK activity, LRRC26 overexpression partially reversed TGF-β1-induced BK dysfunction. TGF-β1-induced airway surface liquid volume hyper-absorption was reversed by the BK opener mallotoxin and the clinically useful TGF-β signaling inhibitor pirfenidone. The latter increased BK activity via rescue of LRRC26. Therefore, we propose that TGF-β1-induced mucociliary dysfunction in CF airways is associated with BK inactivation related to a LRRC26 decrease and is amenable to treatment with clinically useful TGF-β1 inhibitors.

Keywords: BK; LRRC26; airway surface liquid; cilia; cystic fibrosis; epithelium; mallotoxin; pirfenidone; potassium channel; transforming growth factor beta (TGF-B).

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Bronchi / drug effects
  • Bronchi / pathology*
  • Cystic Fibrosis / drug therapy
  • Cystic Fibrosis / metabolism*
  • Cystic Fibrosis / pathology
  • Gene Knockdown Techniques
  • Humans
  • Mucociliary Clearance / drug effects
  • Neoplasm Proteins / genetics
  • Potassium Channels, Voltage-Gated / physiology*
  • Pyridones / pharmacology*
  • Pyridones / therapeutic use
  • Transforming Growth Factor beta1 / antagonists & inhibitors
  • Transforming Growth Factor beta1 / physiology*

Substances

  • LRRC26 protein, human
  • Neoplasm Proteins
  • Potassium Channels, Voltage-Gated
  • Pyridones
  • Transforming Growth Factor beta1
  • Adenosine Triphosphate
  • pirfenidone