Upregulation of 5-hydroxytryptamine receptor signaling in coronary arteries after organ culture

PLoS One. 2014 Sep 9;9(9):e107128. doi: 10.1371/journal.pone.0107128. eCollection 2014.

Abstract

Background: 5-Hydroxytryptamine (5-HT) is a powerful constrictor of coronary arteries and is considered to be involved in the pathophysiological mechanisms of coronary-artery spasm. However, the mechanism of enhancement of coronary-artery constriction to 5-HT during the development of coronary artery disease remains to be elucidated. Organ culture of intact blood-vessel segments has been suggested as a model for the phenotypic changes of smooth muscle cells in cardiovascular disease.

Methodology/principal findings: We wished to characterize 5-HT receptor-induced vasoconstriction and quantify expression of 5-HT receptor signaling in cultured rat coronary arteries. Cumulative application of 5-HT produced a concentration-dependent vasoconstriction in fresh and 24 h-cultured rat coronary arteries without endothelia. 5-HT induced greater constriction in cultured coronary arteries than in fresh coronary arteries. U46619- and CaCl2-induced constriction in the two groups was comparable. 5-HT stimulates the 5-HT2A receptor and cascade of phospholipase C to induce coronary vasoconstriction. Calcium influx through L-type calcium channels and non-L-type calcium channels contributed to the coronary-artery constrictions induced by 5-HT. The contractions mediated by non-L-type calcium channels were significantly enhanced in cultured coronary arteries compared with fresh coronary arteries. The vasoconstriction induced by thapsigargin was also augmented in cultured coronary arteries. The decrease in Orai1 expression significantly inhibited 5-HT-evoked entry of Ca2+ in coronary artery cells. Expression of the 5-HT2A receptor, Orai1 and STIM1 were augmented in cultured coronary arteries compared with fresh coronary arteries.

Conclusions: An increased contraction in response to 5-HT was mediated by the upregulation of 5-HT2A receptors and downstream signaling in cultured coronary arteries.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 15-Hydroxy-11 alpha,9 alpha-(epoxymethano)prosta-5,13-dienoic Acid / pharmacology
  • Animals
  • Calcium / metabolism
  • Calcium Channels / genetics
  • Calcium Channels / metabolism
  • Calcium Channels, L-Type / genetics
  • Calcium Channels, L-Type / metabolism
  • Coronary Vessels / drug effects
  • Coronary Vessels / metabolism*
  • Male
  • Membrane Glycoproteins / genetics
  • Membrane Glycoproteins / metabolism
  • Muscle, Smooth, Vascular / drug effects
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Smooth Muscle / drug effects
  • Myocytes, Smooth Muscle / metabolism
  • ORAI1 Protein
  • Organ Culture Techniques / methods
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Serotonin, 5-HT2A / genetics*
  • Receptor, Serotonin, 5-HT2A / metabolism
  • Serotonin / genetics
  • Serotonin / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Stromal Interaction Molecule 1
  • Thapsigargin / pharmacology
  • Up-Regulation / drug effects
  • Up-Regulation / genetics*
  • Vasoconstriction / drug effects
  • Vasoconstriction / genetics

Substances

  • Calcium Channels
  • Calcium Channels, L-Type
  • Membrane Glycoproteins
  • ORAI1 Protein
  • Orai1 protein, rat
  • Receptor, Serotonin, 5-HT2A
  • Stim1 protein, rat
  • Stromal Interaction Molecule 1
  • Serotonin
  • Thapsigargin
  • 15-Hydroxy-11 alpha,9 alpha-(epoxymethano)prosta-5,13-dienoic Acid
  • Calcium

Grants and funding

This work was supported by the National Natural Science Foundation of China (No. 81273516, No. 81270222, No. 81330007, No. 81302779), by Guangdong Provincial Natural Science Foundation (No. S2013010014762, No. S2013040014689), National Key Basic Research Program of China (No. 2012CB526600) and by Guangdong Provincial Medical Science Foundation (No. A2012006). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.