Gap junctions and other mechanisms of cell-cell communication regulate basal insulin secretion in the pancreatic islet

J Physiol. 2011 Nov 15;589(Pt 22):5453-66. doi: 10.1113/jphysiol.2011.218909. Epub 2011 Sep 19.

Abstract

Cell-cell communication in the islet of Langerhans is important for the regulation of insulin secretion. Gap-junctions coordinate oscillations in intracellular free-calcium ([Ca(2+)](i)) and insulin secretion in the islet following elevated glucose. Gap-junctions can also ensure that oscillatory [Ca(2+)](i) ceases when glucose is at a basal levels. We determine the roles of gap-junctions and other cell-cell communication pathways in the suppression of insulin secretion under basal conditions. Metabolic, electrical and insulin secretion levels were measured from islets lacking gap-junction coupling following deletion of connexion36 (Cx36(-/-)), and these results were compared to those obtained using fully isolated β-cells. K(ATP) loss-of-function islets provide a further experimental model to specifically study gap-junction mediated suppression of electrical activity. In isolated β-cells or Cx36(-/-) islets, elevations in [Ca(2+)](i) persisted in a subset of cells even at basal glucose. Isolated β-cells showed elevated insulin secretion at basal glucose; however, insulin secretion from Cx36(-/-) islets was minimally altered. [Ca(2+)](i) was further elevated under basal conditions, but insulin release still suppressed in K(ATP) loss-of-function islets. Forced elevation of cAMP led to PKA-mediated increases in insulin secretion from islets lacking gap-junctions, but not from islets expressing Cx36 gap junctions. We conclude there is a redundancy in how cell-cell communication in the islet suppresses insulin release. Gap junctions suppress cellular heterogeneity and spontaneous [Ca(2+)](i) signals, while other juxtacrine mechanisms, regulated by PKA and glucose, suppress more distal steps in exocytosis. Each mechanism is sufficiently robust to compensate for a loss of the other and still suppress basal insulin secretion.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Calcium / physiology
  • Cell Communication / physiology*
  • Cells, Cultured
  • Connexins / deficiency
  • Connexins / physiology
  • Cyclic AMP / physiology
  • Cyclic AMP-Dependent Protein Kinases / physiology
  • Gap Junction delta-2 Protein
  • Gap Junctions / physiology*
  • Glucose / pharmacology
  • In Vitro Techniques
  • Insulin / metabolism*
  • Insulin Secretion
  • Insulin-Secreting Cells / physiology*
  • Islets of Langerhans / physiology*
  • Membrane Potentials
  • Mice
  • Mice, Knockout

Substances

  • Connexins
  • Insulin
  • Cyclic AMP
  • Cyclic AMP-Dependent Protein Kinases
  • Glucose
  • Calcium