Unitary TRPV3 channel Ca2+ influx events elicit endothelium-dependent dilation of cerebral parenchymal arterioles

Am J Physiol Heart Circ Physiol. 2015 Dec 15;309(12):H2031-41. doi: 10.1152/ajpheart.00140.2015. Epub 2015 Oct 9.

Abstract

Cerebral parenchymal arterioles (PA) regulate blood flow between pial arteries on the surface of the brain and the deeper microcirculation. Regulation of PA contractility differs from that of pial arteries and is not completely understood. Here, we investigated the hypothesis that the Ca(2+) permeable vanilloid transient receptor potential (TRPV) channel TRPV3 can mediate endothelium-dependent dilation of cerebral PA. Using total internal reflection fluorescence microscopy (TIRFM), we found that carvacrol, a monoterpenoid compound derived from oregano, increased the frequency of unitary Ca(2+) influx events through TRPV3 channels (TRPV3 sparklets) in endothelial cells from pial arteries and PAs. Carvacrol-induced TRPV3 sparklets were inhibited by the selective TRPV3 blocker isopentenyl pyrophosphate (IPP). TRPV3 sparklets have a greater unitary amplitude (ΔF/F0 = 0.20) than previously characterized TRPV4 (ΔF/F0 = 0.06) or TRPA1 (ΔF/F0 = 0.13) sparklets, suggesting that TRPV3-mediated Ca(2+) influx could have a robust influence on cerebrovascular tone. In pressure myography experiments, carvacrol caused dilation of cerebral PA that was blocked by IPP. Carvacrol-induced dilation was nearly abolished by removal of the endothelium and block of intermediate (IK) and small-conductance Ca(2+)-activated K(+) (SK) channels. Together, these data suggest that TRPV3 sparklets cause dilation of cerebral parenchymal arterioles by activating IK and SK channels in the endothelium.

Keywords: endothelium-dependent hyperpolarization; parenchymal arterioles; transient receptor potential channel; transient receptor potential sparklet; vanilloid transient receptor potential 3.

Publication types

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

MeSH terms

  • Animals
  • Arterioles / physiology*
  • Calcium / metabolism*
  • Calcium Signaling / drug effects
  • Calcium Signaling / genetics*
  • Calcium Signaling / physiology*
  • Cerebrovascular Circulation / genetics*
  • Cerebrovascular Circulation / physiology*
  • Cymenes
  • Electromyography
  • Endothelium, Vascular / physiology*
  • Hemiterpenes / pharmacology
  • Intermediate-Conductance Calcium-Activated Potassium Channels / drug effects
  • Male
  • Monoterpenes / pharmacology
  • Muscle Tonus / drug effects
  • Muscle Tonus / genetics
  • Muscle Tonus / physiology
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / physiology
  • Organophosphorus Compounds / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Small-Conductance Calcium-Activated Potassium Channels / drug effects
  • TRPV Cation Channels / antagonists & inhibitors
  • TRPV Cation Channels / genetics*
  • TRPV Cation Channels / physiology*
  • Vasodilation / drug effects
  • Vasodilation / physiology
  • Vasodilator Agents / pharmacology

Substances

  • Cymenes
  • Hemiterpenes
  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Monoterpenes
  • Organophosphorus Compounds
  • Small-Conductance Calcium-Activated Potassium Channels
  • TRPV Cation Channels
  • TRPV3 protein, rat
  • Vasodilator Agents
  • isopentenyl pyrophosphate
  • carvacrol
  • Calcium