Membrane cholesterol depletion with beta-cyclodextrin impairs pressure-induced contraction and calcium signalling in isolated skeletal muscle arterioles

J Vasc Res. 2007;44(4):292-302. doi: 10.1159/000101451. Epub 2007 Mar 30.

Abstract

Objective: Given evidence for clustering of signalling molecules and ion channels in cholesterol-rich membrane domains, the involvement of such structures in arteriolar smooth muscle mechanotransduction was examined.

Method: To determine the contribution of smooth muscle cholesterol-rich membrane domains to the myogenic response, isolated arterioles were exposed to the cholesterol-depleting agent beta-cyclodextrin (1-10 mM) in the absence and presence of excess exogenous cholesterol.

Results: beta-Cyclodextrin significantly impaired pressure-induced vasoconstriction, while excess cholesterol attenuated this effect. Impaired myogenic constriction was evident in de-endothelialized vessels, indicating an action at the level of smooth muscle. beta-Cyclodextrin treatment uncoupled increases in intracellular Ca(2+) from myogenic constriction and depleted intracellular Ca(2+) stores consistent with a loss of connectivity between plasma membrane and sarcoplasmic reticulum signalling. However, beta-cyclodextrin-treated arterioles showed unaltered constrictor responses to KCl and phenylephrine. Electron microscopy verified that beta-cyclodextrin caused a decrease in caveolae, while confirmation of smooth muscle containing caveolae was obtained by immunostaining for caveolin-1. Viability of beta-cyclodextrin-treated arterioles was confirmed by agonist sensitivity and propidium iodide nuclear staining.

Conclusion: The data suggest that smooth muscle cholesterol-rich membrane domains contribute to the myogenic response. Further studies are required to determine whether this relates to specific mechanosensory events or generalized alterations in membrane function.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arterioles / drug effects
  • Arterioles / physiology*
  • Arterioles / ultrastructure
  • Calcium / metabolism
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Carcinogens / pharmacology
  • Cell Membrane / drug effects
  • Cell Membrane / metabolism
  • Cell Membrane / ultrastructure
  • Cholesterol / metabolism*
  • In Vitro Techniques
  • Male
  • Microscopy, Electron
  • Muscle Contraction / drug effects
  • Muscle Contraction / physiology*
  • Muscle, Skeletal / blood supply
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / physiology*
  • Muscle, Smooth, Vascular / ultrastructure
  • Pressure
  • Rats
  • Rats, Sprague-Dawley
  • Vasoconstriction / drug effects
  • Vasoconstriction / physiology
  • beta-Cyclodextrins / pharmacology

Substances

  • Carcinogens
  • beta-Cyclodextrins
  • Cholesterol
  • betadex
  • Calcium