Triggered Ca2+ influx is required for extended synaptotagmin 1-induced ER-plasma membrane tethering

EMBO J. 2015 Sep 2;34(17):2291-305. doi: 10.15252/embj.201591565. Epub 2015 Jul 22.

Abstract

The extended synaptotagmins (E-Syts) are ER proteins that act as Ca(2+)-regulated tethers between the ER and the plasma membrane (PM) and have a putative role in lipid transport between the two membranes. Ca(2+) regulation of their tethering function, as well as the interplay of their different domains in such function, remains poorly understood. By exposing semi-intact cells to buffers of variable Ca(2+) concentrations, we found that binding of E-Syt1 to the PI(4,5)P2-rich PM critically requires its C2C and C2E domains and that the EC50 of such binding is in the low micromolar Ca(2+) range. Accordingly, E-Syt1 accumulation at ER-PM contact sites occurred only upon experimental manipulations known to achieve these levels of Ca(2+) via its influx from the extracellular medium, such as store-operated Ca(2+) entry in fibroblasts and membrane depolarization in β-cells. We also show that in spite of their very different physiological functions, membrane tethering by E-Syt1 (ER to PM) and by synaptotagmin (secretory vesicles to PM) undergo a similar regulation by plasma membrane lipids and cytosolic Ca(2+).

Keywords: Orai1; PLC; STIM1; membrane contact sites; tricalbin.

Publication types

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

MeSH terms

  • Animals
  • COS Cells
  • Calcium / metabolism*
  • Calcium Signaling / physiology*
  • Cell Membrane / genetics
  • Cell Membrane / metabolism*
  • Chlorocebus aethiops
  • Endoplasmic Reticulum / genetics
  • Endoplasmic Reticulum / metabolism*
  • Fibroblasts / cytology
  • Fibroblasts / metabolism
  • HeLa Cells
  • Humans
  • Insulin-Secreting Cells / cytology
  • Insulin-Secreting Cells / metabolism
  • Membrane Potentials / physiology
  • Phosphatidylinositol 4,5-Diphosphate / genetics
  • Phosphatidylinositol 4,5-Diphosphate / metabolism
  • Protein Structure, Tertiary
  • Synaptotagmin I / genetics
  • Synaptotagmin I / metabolism*

Substances

  • Phosphatidylinositol 4,5-Diphosphate
  • Synaptotagmin I
  • Calcium