Synaptotagmin-7 Functions to Replenish Insulin Granules for Exocytosis in Human Islet β-Cells

Diabetes. 2016 Jul;65(7):1962-76. doi: 10.2337/db15-1436. Epub 2016 Apr 26.

Abstract

Synaptotagmin (Syt)-7, a major component of the exocytotic machinery in neurons, is also the major Syt in rodent pancreatic β-cells shown to mediate glucose-stimulated insulin secretion (GSIS). However, Syt-7's precise exocytotic actions in β-cells remain unknown. We show that Syt-7 is abundant in human β-cells. Adenovirus-short hairpin RNA knockdown (KD) of Syt-7 in human islets reduced first- and second-phase GSIS attributed to the reduction of exocytosis of predocked and newcomer insulin secretory granules (SGs). Glucose stimulation expectedly induced Syt-7 association in a Ca(2+)-dependent manner with syntaxin-3 and syntaxin-1A soluble N-ethylmaleimide-sensitive factor attachment protein receptor (SNARE) complexes known to mediate exocytosis of newcomer and predocked SGs, respectively. However, Syt-7-KD did not disrupt SNARE complex assembly. Instead, electron microscopy analysis showed that Syt-7-KD reduced the recruitment of SGs to the plasma membrane after glucose-stimulated depletion, which could not be rescued by glucagon-like peptide 1 pretreatment. To assess the possibility that this new action of Syt-7 on SG recruitment may involve calmodulin (CaM), pretreatment of islets with CaM blocker calmidazolium showed effects very similar to those of Syt-7-KD. Syt-7 therefore plays a novel more dominant function in the replenishment of releasable SG pools in human β-cells than its previously purported role in exocytotic fusion per se.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Animals
  • Calcium / metabolism
  • Exocytosis / drug effects
  • Exocytosis / physiology*
  • Female
  • Glucagon-Like Peptide 1 / pharmacology
  • Glucose / pharmacology
  • Humans
  • Imidazoles / pharmacology
  • Insulin / metabolism*
  • Insulin-Secreting Cells / drug effects
  • Insulin-Secreting Cells / metabolism*
  • Male
  • Middle Aged
  • Qa-SNARE Proteins / metabolism
  • Rats
  • Rats, Sprague-Dawley
  • SNARE Proteins / metabolism
  • Secretory Vesicles / metabolism*
  • Synaptotagmins / metabolism*

Substances

  • Imidazoles
  • Insulin
  • Qa-SNARE Proteins
  • SNARE Proteins
  • Synaptotagmins
  • calmidazolium
  • Glucagon-Like Peptide 1
  • Glucose
  • Calcium