Feedback regulation of receptor-induced Ca2+ signaling mediated by E-Syt1 and Nir2 at endoplasmic reticulum-plasma membrane junctions

Cell Rep. 2013 Nov 14;5(3):813-25. doi: 10.1016/j.celrep.2013.09.038. Epub 2013 Oct 31.

Abstract

Endoplasmic reticulum (ER)-plasma membrane (PM) junctions are highly conserved subcellular structures. Despite their importance in Ca(2+) signaling and lipid trafficking, the molecular mechanisms underlying the regulation and functions of ER-PM junctions remain unclear. By developing a genetically encoded marker that selectively monitors ER-PM junctions, we found that the connection between ER and PM was dynamically regulated by Ca(2+) signaling. Elevation of cytosolic Ca(2+) triggered translocation of E-Syt1 to ER-PM junctions to enhance ER-to-PM connection. This subsequently facilitated the recruitment of Nir2, a phosphatidylinositol transfer protein (PITP), to ER-PM junctions following receptor stimulation. Nir2 promoted the replenishment of PM phosphatidylinositol 4,5-bisphosphate (PIP2) after receptor-induced hydrolysis via its PITP activity. Disruption of the enhanced ER-to-PM connection resulted in reduced PM PIP2 replenishment and defective Ca(2+) signaling. Altogether, our results suggest a feedback mechanism that replenishes PM PIP2 during receptor-induced Ca(2+) signaling via the Ca(2+) effector E-Syt1 and the PITP Nir2 at ER-PM junctions.

Publication types

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

MeSH terms

  • Calcium / metabolism*
  • Calcium Signaling*
  • Calcium-Binding Proteins / genetics*
  • Calcium-Binding Proteins / metabolism
  • Cell Culture Techniques
  • Endoplasmic Reticulum / metabolism*
  • Eye Proteins / genetics*
  • Eye Proteins / metabolism
  • HeLa Cells
  • Humans
  • Jurkat Cells
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Microscopy, Electron
  • Signal Transduction
  • Synaptotagmins / genetics*
  • Synaptotagmins / metabolism
  • Transfection

Substances

  • Calcium-Binding Proteins
  • ESYT1 protein, human
  • Eye Proteins
  • Membrane Proteins
  • PITPNM1 protein, human
  • Synaptotagmins
  • Calcium