Upregulation of SK3 and IK1 channels contributes to the enhanced endothelial calcium signaling and the preserved coronary relaxation in obese Zucker rats

PLoS One. 2014 Oct 10;9(10):e109432. doi: 10.1371/journal.pone.0109432. eCollection 2014.

Abstract

Background and aims: Endothelial small- and intermediate-conductance KCa channels, SK3 and IK1, are key mediators in the endothelium-derived hyperpolarization and relaxation of vascular smooth muscle and also in the modulation of endothelial Ca2+ signaling and nitric oxide (NO) release. Obesity is associated with endothelial dysfunction and impaired relaxation, although how obesity influences endothelial SK3/IK1 function is unclear. Therefore we assessed whether the role of these channels in the coronary circulation is altered in obese animals.

Methods and results: In coronary arteries mounted in microvascular myographs, selective blockade of SK3/IK1 channels unmasked an increased contribution of these channels to the ACh- and to the exogenous NO- induced relaxations in arteries of Obese Zucker Rats (OZR) compared to Lean Zucker Rats (LZR). Relaxant responses induced by the SK3/IK1 channel activator NS309 were enhanced in OZR and NO- endothelium-dependent in LZR, whereas an additional endothelium-independent relaxant component was found in OZR. Fura2-AM fluorescence revealed a larger ACh-induced intracellular Ca2+ mobilization in the endothelium of coronary arteries from OZR, which was inhibited by blockade of SK3/IK1 channels in both LZR and OZR. Western blot analysis showed an increased expression of SK3/IK1 channels in coronary arteries of OZR and immunohistochemistry suggested that it takes place predominantly in the endothelial layer.

Conclusions: Obesity may induce activation of adaptive vascular mechanisms to preserve the dilator function in coronary arteries. Increased function and expression of SK3/IK1 channels by influencing endothelial Ca2+ dynamics might contribute to the unaltered endothelium-dependent coronary relaxation in the early stages of obesity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium Signaling / drug effects
  • Calcium Signaling / physiology*
  • Coronary Vessels / drug effects
  • Coronary Vessels / metabolism*
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Indoles / pharmacology
  • Intermediate-Conductance Calcium-Activated Potassium Channels / agonists
  • Intermediate-Conductance Calcium-Activated Potassium Channels / genetics
  • Intermediate-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Male
  • Myography
  • Obesity / genetics
  • Obesity / metabolism*
  • Oximes / pharmacology
  • Rats
  • Rats, Zucker
  • Small-Conductance Calcium-Activated Potassium Channels / agonists
  • Small-Conductance Calcium-Activated Potassium Channels / genetics
  • Small-Conductance Calcium-Activated Potassium Channels / metabolism*
  • Up-Regulation*
  • Vasodilation / drug effects
  • Vasodilation / physiology

Substances

  • 6,7-dichloro-1H-indole-2,3-dione 3-oxime
  • Indoles
  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Kcnn3 protein, rat
  • Oximes
  • Small-Conductance Calcium-Activated Potassium Channels

Grants and funding

This study was supported by: 1. Grant n° SAF2009-10448 from the Spanish Ministry of Science and Innovation (http://www.idi.mineco.gob.es/portal/site/MICINN/). 2. Grant n° SAF2012-31631 of the Spanish Ministry of Economy (http://www.mineco.gob.es/portal/site/mineco/). 3. LM was supported by MS program (http://www.isciii.es/ISCIII/es/contenidos/fd-el-instituto/fd-comunicacion/fd-notas-prensa/15mar011XIIIPromocionMiguelServet.shtml). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.