Glucose-stimulated insulin secretion is coupled to the interaction of actin with the t-SNARE (target membrane soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein) complex

Mol Endocrinol. 2003 Apr;17(4):732-42. doi: 10.1210/me.2002-0333. Epub 2003 Jan 16.

Abstract

The actin monomer sequestering agent latrunculin B depolymerized beta-cell cortical actin, which resulted in increased glucose-stimulated insulin secretion in both cultured MIN6 beta-cells and isolated rat islet cells. In perifused islets, latrunculin B treatment increased both first- and second-phase glucose-stimulated insulin secretion without any significant effect on total insulin content. This increase in secretion was independent of calcium regulation because latrunculin B also potentiated calcium-stimulated insulin secretion in permeabilized MIN6 cells. Confocal immunofluorescent microscopy revealed a redistribution of insulin granules to the cell periphery in response to glucose or latrunculin B, which correlated with a reduction in phalloidin staining of cortical actin. Moreover, the t-SNARE [target membrane soluble N-ethylmaleimide-sensitive factor attachment protein (SNAP) receptor] proteins Syntaxin 1 and SNAP-25 coimmunoprecipitated polymerized actin from unstimulated MIN6 cells. Glucose stimulation transiently decreased the amount of actin coimmunoprecipitated with Syntaxin 1 and SNAP-25, and latrunculin B treatment fully ablated the coimmunoprecipitation. In contrast, the actin stabilizing agent jasplakinolide increased the amount of actin coimmunoprecipitated with the t-SNARE complex and prevented its dissociation upon glucose stimulation. These data suggest a mechanism whereby glucose modulates beta-cell cortical actin organization and disrupts the interaction of polymerized actin with the plasma membrane t-SNARE complex at a distal regulatory step in the exocytosis of insulin granules.

Publication types

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

MeSH terms

  • Actins / drug effects
  • Actins / metabolism*
  • Animals
  • Antigens, Surface / metabolism
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Calcium / metabolism
  • Calcium Channels / metabolism
  • Cells, Cultured
  • Cytoplasmic Granules / metabolism
  • Glucose / metabolism*
  • Glucose / pharmacology
  • In Vitro Techniques
  • Insulin / metabolism*
  • Insulin Secretion
  • Islets of Langerhans / drug effects
  • Islets of Langerhans / metabolism
  • Membrane Proteins / metabolism*
  • Nerve Tissue Proteins / metabolism
  • Perfusion
  • Precipitin Tests
  • R-SNARE Proteins
  • Rats
  • SNARE Proteins
  • Synaptosomal-Associated Protein 25
  • Syntaxin 1
  • Thiazoles / pharmacology
  • Thiazolidines
  • Vesicular Transport Proteins*

Substances

  • Actins
  • Antigens, Surface
  • Bridged Bicyclo Compounds, Heterocyclic
  • Calcium Channels
  • Insulin
  • Membrane Proteins
  • Nerve Tissue Proteins
  • R-SNARE Proteins
  • SNARE Proteins
  • Snap25 protein, rat
  • Stx1a protein, rat
  • Synaptosomal-Associated Protein 25
  • Syntaxin 1
  • Thiazoles
  • Thiazolidines
  • Vesicular Transport Proteins
  • Glucose
  • latrunculin B
  • Calcium