Bitter taste receptor agonists regulate epithelial two-pore potassium channels via cAMP signaling

Respir Res. 2021 Jan 28;22(1):31. doi: 10.1186/s12931-021-01631-0.

Abstract

Background: Epithelial solitary chemosensory cell (tuft cell) bitter taste signal transduction occurs through G protein coupled receptors and calcium-dependent signaling pathways. Type II taste cells, which utilize the same bitter taste signal transduction pathways, may also utilize cyclic adenosine monophosphate (cAMP) as an independent signaling messenger in addition to calcium.

Methods: In this work we utilized specific pharmacologic inhibitors to interrogate the short circuit current (Isc) of polarized nasal epithelial cells mounted in Ussing chambers to assess the electrophysiologic changes associated with bitter agonist (denatonium) treatment. We also assessed release of human β-defensin-2 from polarized nasal epithelial cultures following treatment with denatonium benzoate and/or potassium channel inhibitors.

Results: We demonstrate that the bitter taste receptor agonist, denatonium, decreases human respiratory epithelial two-pore potassium (K2P) current in polarized nasal epithelial cells mounted in Ussing chambers. Our data further suggest that this occurs via a cAMP-dependent signaling pathway. We also demonstrate that this decrease in potassium current lowers the threshold for denatonium to stimulate human β-defensin-2 release.

Conclusions: These data thus demonstrate that, in addition to taste transducing calcium-dependent signaling, bitter taste receptor agonists can also activate cAMP-dependent respiratory epithelial signaling pathways to modulate K2P currents. Bitter-agonist regulation of potassium currents may therefore serve as a means of rapid regional epithelial signaling, and further study of these pathways may provide new insights into regulation of mucosal ionic composition and innate mechanisms of epithelial defense.

Keywords: Antimicrobial peptide; Chronic rhinosinusitis; Defensin; Denatonium; K2P; Potassium channel; SCC; Tuft cell.

MeSH terms

  • Aversive Agents / pharmacology
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology
  • Cyclic AMP / metabolism*
  • Humans
  • Nasal Mucosa / drug effects
  • Nasal Mucosa / metabolism
  • Potassium Channels / metabolism*
  • Quaternary Ammonium Compounds / pharmacology*
  • Respiratory Mucosa / drug effects
  • Respiratory Mucosa / metabolism*
  • Signal Transduction / drug effects
  • Signal Transduction / physiology
  • Taste / drug effects
  • Taste / physiology*
  • Taste Buds / drug effects
  • Taste Buds / metabolism*

Substances

  • Aversive Agents
  • Potassium Channels
  • Quaternary Ammonium Compounds
  • denatonium
  • Cyclic AMP