Thiopental-induced insulin secretion via activation of IP3-sensitive calcium stores in rat pancreatic β-cells

Am J Physiol Cell Physiol. 2012 Mar 1;302(5):C796-803. doi: 10.1152/ajpcell.00081.2011. Epub 2011 Nov 30.

Abstract

While glucose-stimulated insulin secretion depends on Ca(2+) influx through voltage-gated Ca(2+) channels in the cell membrane of the pancreatic β-cell, there is also ample evidence for an important role of intracellular Ca(2+) stores in insulin secretion, particularly in relation to drug stimuli. We report here that thiopental, a common anesthetic agent, triggers insulin secretion from the intact pancreas and primary cultured rat pancreatic β-cells. We investigated the underlying mechanisms by measurements of whole cell K(+) and Ca(2+) currents, membrane potential, cytoplasmic Ca(2+) concentration ([Ca(2+)](i)), and membrane capacitance. Thiopental-induced insulin secretion was first detected by enzyme-linked immunoassay, then further assessed by membrane capacitance measurement, which revealed kinetics distinct from glucose-induced insulin secretion. The thiopental-induced secretion was independent of cell membrane depolarization and closure of ATP-sensitive potassium (K(ATP)) channels. However, accompanied by the insulin secretion stimulated by thiopental, we recorded a significant intracellular [Ca(2+)] increase that was not from Ca(2+) influx across the cell membrane, but from intracellular Ca(2+) stores. The thiopental-induced [Ca(2+)](i) rise in β-cells was sensitive to thapsigargin, a blocker of the endoplasmic reticulum Ca(2+) pump, as well as to heparin (0.1 mg/ml) and 2-aminoethoxydiphenyl borate (2-APB; 100 μM), drugs that inhibit inositol 1,4,5-trisphosphate (IP(3)) binding to the IP(3) receptor, and to U-73122, a phospholipase C inhibitor, but insensitive to ryanodine. Thapsigargin also diminished thiopental-induced insulin secretion. Thus, we conclude that thiopental-induced insulin secretion is mediated by activation of the intracellular IP(3)-sensitive Ca(2+) store.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Anesthetics, Intravenous
  • Animals
  • Boron Compounds / pharmacology
  • Calcium / metabolism*
  • Estrenes / pharmacology
  • Glucose / metabolism
  • Heparin / pharmacology
  • Inositol 1,4,5-Trisphosphate / antagonists & inhibitors
  • Inositol 1,4,5-Trisphosphate / metabolism*
  • Inositol 1,4,5-Trisphosphate Receptors / antagonists & inhibitors
  • Inositol 1,4,5-Trisphosphate Receptors / metabolism*
  • Insulin / analysis
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulin-Secreting Cells / drug effects*
  • Insulin-Secreting Cells / metabolism
  • Membrane Potentials / drug effects
  • Patch-Clamp Techniques
  • Potassium Channels / drug effects
  • Potassium Channels / metabolism
  • Pyrrolidinones / pharmacology
  • Rats
  • Rats, Wistar
  • Ryanodine / pharmacology
  • Thapsigargin / pharmacology
  • Thiopental / pharmacology*

Substances

  • Anesthetics, Intravenous
  • Boron Compounds
  • Estrenes
  • Inositol 1,4,5-Trisphosphate Receptors
  • Insulin
  • Potassium Channels
  • Pyrrolidinones
  • 1-(6-((3-methoxyestra-1,3,5(10)-trien-17-yl)amino)hexyl)-1H-pyrrole-2,5-dione
  • Ryanodine
  • Thapsigargin
  • Inositol 1,4,5-Trisphosphate
  • Heparin
  • 2-aminoethoxydiphenyl borate
  • Glucose
  • Thiopental
  • Calcium