The TREK-1 potassium channel is a potential pharmacological target for vasorelaxation in pulmonary hypertension

Br J Pharmacol. 2024 Oct;181(19):3576-3593. doi: 10.1111/bph.16426. Epub 2024 May 28.

Abstract

Background and purpose: Pulmonary arterial hypertension (PAH) is a progressive disease in which chronic membrane potential (Em) depolarisation of the pulmonary arterial smooth muscle cells (PASMCs) causes calcium overload, a key pathological alteration. Under resting conditions, the negative Em is mainly set by two pore domain potassium (K2P) channels, of which the TASK-1 has been extensively investigated.

Experimental approach: Ion channel currents and membrane potential of primary cultured human(h) PASMCs were measured using the voltage- and current clamp methods. Intracellular [Ca2+] was monitored using fluorescent microscopy. Pulmonary BP and vascular tone measurements were also performed ex vivo using a rat PAH model.

Key results: TREK-1 was the most abundantly expressed K2P in hPASMCs of healthy donors and idiopathic(I) PAH patients. Background K+-current was similar in hPASMCs for both groups and significantly enhanced by the TREK activator ML-335. In donor hPASMCs, siRNA silencing or pharmacological inhibition of TREK-1 caused depolarisation, reminiscent of the electrophysiological phenotype of idiopathic PAH. ML-335 hyperpolarised donor hPASMCs and normalised the Em of IPAH hPASMCs. A close link was found between TREK-1 activity and intracellular Ca2+-signalling using a channel activator, ML-335, and an inhibitor, spadin. In the rat, ML-335 relaxed isolated pre-constricted pulmonary arteries and significantly decreased pulmonary arterial pressure in the isolated perfused lung.

Conclusions and implications: These data suggest that TREK-1is a key factor in Em setting and Ca2+ homeostasis of hPASMC, and therefore, essential for maintenance of a low resting pulmonary vascular tone. Thus TREK-1 may represent a new therapeutic target for PAH.

Keywords: ML‐335; TREK‐1; pulmonary arterial hypertension (PAH); pulmonary arterial smooth muscle cells (PASMC); spadin.

MeSH terms

  • Animals
  • Calcium / metabolism
  • Cells, Cultured
  • Female
  • Humans
  • Hypertension, Pulmonary* / drug therapy
  • Hypertension, Pulmonary* / metabolism
  • Hypertension, Pulmonary* / physiopathology
  • Male
  • Membrane Potentials / drug effects
  • Middle Aged
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • Potassium Channels, Tandem Pore Domain* / antagonists & inhibitors
  • Potassium Channels, Tandem Pore Domain* / metabolism
  • Pulmonary Artery / drug effects
  • Pulmonary Artery / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Wistar
  • Vasodilation* / drug effects

Substances

  • Potassium Channels, Tandem Pore Domain
  • potassium channel protein TREK-1
  • Calcium