Involvement of calmodulin in glucagon-like peptide 1(7-36) amide-induced inhibition of the ATP-sensitive K+ channel in mouse pancreatic beta-cells

Exp Physiol. 2001 May;86(3):331-9. doi: 10.1113/eph8602173.

Abstract

The present investigation was designed to examine whether calmodulin is involved in the inhibition of the ATP-sensitive K+ (K(ATP)) channel by glucagon-like peptide 1(7-36) amide (GLP-1) in mouse pancreatic beta-cells. Membrane potential, single channel and whole-cell currents through the K(ATP) channels, and intracellular free Ca2+ concentration ([Ca2+]i) were measured in single mouse pancreatic beta-cells. Whole-cell patch-clamp experiments with amphotericin-perforated patches revealed that membrane conductance at around the resting potential is predominantly supplied by the K(ATP) channels in mouse pancreatic beta-cells. The addition of 20 nM GLP-1 in the presence of 5 mM glucose significantly reduced the membrane K(ATP) conductance, accompanied by membrane depolarization and the generation of electrical activity. A calmodulin inhibitor N-(6-aminohexyl)-5-chloro-1-naphthalenesulphonamide (W-7, 20 microM) completely reversed the inhibitory actions of GLP-1 on the membrane K(ATP) conductance and resultant membrane depolarization. Cell-attached patch recordings confirmed the inhibition of the K(ATP) channel activity by 20 nM GLP-1 and its restoration by 20 microM W-7 or 10 microM calmidazolium at the single channel level. Bath application of 20 microM W-7 also consistently abolished the GLP-1-evoked increase in [Ca2+]i in the presence of 5 mM glucose. These results strongly suggest that the mechanisms by which GLP-1 inhibits the K(ATP) channel activity accompanied by the initiation of electrical activity in mouse pancreatic beta-cells include a calmodulin-dependent mechanism in addition to the well-documented activation of the cyclic AMP-protein kinase A system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • Calcium / metabolism
  • Calmodulin / antagonists & inhibitors
  • Calmodulin / metabolism*
  • Electrophysiology
  • Enzyme Inhibitors / pharmacology
  • Glucagon
  • Glucagon-Like Peptide 1
  • Glucagon-Like Peptides
  • Hypoglycemic Agents / pharmacology
  • Imidazoles / pharmacology
  • Islets of Langerhans / drug effects
  • Islets of Langerhans / metabolism*
  • Male
  • Membrane Potentials / drug effects
  • Membrane Potentials / physiology
  • Mice
  • Mice, Inbred ICR
  • Peptide Fragments / pharmacology*
  • Potassium Channels / metabolism*
  • Sulfonamides / pharmacology
  • Tolbutamide / pharmacology

Substances

  • Calmodulin
  • Enzyme Inhibitors
  • Hypoglycemic Agents
  • Imidazoles
  • Peptide Fragments
  • Potassium Channels
  • Sulfonamides
  • glucagon-like peptide 1 (7-36)
  • calmidazolium
  • Glucagon-Like Peptides
  • W 7
  • Glucagon-Like Peptide 1
  • Adenosine Triphosphate
  • Glucagon
  • Tolbutamide
  • Calcium