Genetic ablation of CaV3.2 channels enhances the arterial myogenic response by modulating the RyR-BKCa axis

Arterioscler Thromb Vasc Biol. 2015 Aug;35(8):1843-51. doi: 10.1161/ATVBAHA.115.305736. Epub 2015 Jun 11.

Abstract

Objective: In resistance arteries, there is an emerging view that smooth muscle CaV3.2 channels restrain arterial constriction through a feedback response involving the large-conductance Ca(2+)-activated K(+) channel (BKCa). Here, we used wild-type and CaV3.2 knockout (CaV3.2(-/-)) mice to definitively test whether CaV3.2 moderates myogenic tone in mesenteric arteries via the CaV3.2-ryanodine receptor-BKCa axis and whether this regulatory mechanism influences blood pressure regulation.

Approach and results: Using pressurized vessel myography, CaV3.2(-/-) mesenteric arteries displayed enhanced myogenic constriction to pressure but similar K(+)-induced vasoconstriction compared with wild-type C57BL/6 arteries. Electrophysiological and myography experiments subsequently confirmed the inability of micromolar Ni(2+), a CaV3.2 blocker, to either constrict arteries or suppress T-type currents in CaV3.2(-/-) smooth muscle cells. The frequency of BKCa-induced spontaneous transient outward K(+) currents dropped in wild-type but not in knockout arterial smooth muscle cells upon the pharmacological suppression of CaV3.2 channel. Line scan analysis performed on en face arteries loaded with Fluo-4 revealed the presence of Ca(2+) sparks in all arteries, with the subsequent application of Ni(2+) only affecting wild-type arteries. Although CaV3.2 channel moderated myogenic constriction of resistance arteries, the blood pressure measurements of CaV3.2(-/-) and wild-type animals were similar.

Conclusions: Overall, our findings establish a negative feedback mechanism of the myogenic response in which CaV3.2 channel modulates downstream ryanodine receptor-BKCa to hyperpolarize and relax arteries.

Keywords: T-type calcium channels; arteries; calcium channels; calcium signaling; calcium-activated potassium channels; ryanodine receptors; vascular smooth muscle.

Publication types

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

MeSH terms

  • Animals
  • Arterial Pressure
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, T-Type / deficiency*
  • Calcium Channels, T-Type / drug effects
  • Calcium Channels, T-Type / genetics
  • Calcium Signaling
  • Feedback, Physiological
  • Female
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits / metabolism*
  • Male
  • Mesenteric Arteries / metabolism
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism*
  • Myocytes, Smooth Muscle / metabolism
  • Ryanodine Receptor Calcium Release Channel / metabolism*
  • Vasoconstriction* / drug effects
  • Vasodilation* / drug effects

Substances

  • BKCa protein, mouse
  • Cacna1h protein, mouse
  • Calcium Channel Blockers
  • Calcium Channels, T-Type
  • Kcnma1 protein, mouse
  • Large-Conductance Calcium-Activated Potassium Channel alpha Subunits
  • Ryanodine Receptor Calcium Release Channel