The relationship between membrane potential and calcium dynamics in glucose-stimulated beta cell syncytium in acute mouse pancreas tissue slices

PLoS One. 2013 Dec 6;8(12):e82374. doi: 10.1371/journal.pone.0082374. eCollection 2013.

Abstract

Oscillatory electrical activity is regarded as a hallmark of the pancreatic beta cell glucose-dependent excitability pattern. Electrophysiologically recorded membrane potential oscillations in beta cells are associated with in-phase oscillatory cytosolic calcium activity ([Ca(2+)]i) measured with fluorescent probes. Recent high spatial and temporal resolution confocal imaging revealed that glucose stimulation of beta cells in intact islets within acute tissue slices produces a [Ca(2+)]i change with initial transient phase followed by a plateau phase with highly synchronized [Ca(2+)]i oscillations. Here, we aimed to correlate the plateau [Ca(2+)]i oscillations with the oscillations of membrane potential using patch-clamp and for the first time high resolution voltage-sensitive dye based confocal imaging. Our results demonstrated that the glucose-evoked membrane potential oscillations spread over the islet in a wave-like manner, their durations and wave velocities being comparable to the ones for [Ca(2+)]i oscillations and waves. High temporal resolution simultaneous records of membrane potential and [Ca(2+)]i confirmed tight but nevertheless limited coupling of the two processes, with membrane depolarization preceding the [Ca(2+)]i increase. The potassium channel blocker tetraethylammonium increased the velocity at which oscillations advanced over the islet by several-fold while, at the same time, emphasized differences in kinetics of the membrane potential and the [Ca(2+)]i. The combination of both imaging techniques provides a powerful tool that will help us attain deeper knowledge of the beta cell network.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Calcium / metabolism*
  • Calcium Signaling* / drug effects
  • Giant Cells / metabolism
  • Glucose / metabolism*
  • Glucose / pharmacology
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism*
  • Islets of Langerhans / physiology
  • Membrane Potentials / physiology*
  • Mice
  • Microscopy, Confocal
  • Patch-Clamp Techniques
  • Tetraethylammonium / pharmacology

Substances

  • Tetraethylammonium
  • Glucose
  • Calcium