Phosphatidylinositol 4,5-bisphosphate optical uncaging potentiates exocytosis

Elife. 2017 Oct 25:6:e30203. doi: 10.7554/eLife.30203.

Abstract

Phosphatidylinositol-4,5-bisphosphate [PI(4,5)P2] is essential for exocytosis. Classical ways of manipulating PI(4,5)P2 levels are slower than its metabolism, making it difficult to distinguish effects of PI(4,5)P2 from those of its metabolites. We developed a membrane-permeant, photoactivatable PI(4,5)P2, which is loaded into cells in an inactive form and activated by light, allowing sub-second increases in PI(4,5)P2 levels. By combining this compound with electrophysiological measurements in mouse adrenal chromaffin cells, we show that PI(4,5)P2 uncaging potentiates exocytosis and identify synaptotagmin-1 (the Ca2+ sensor for exocytosis) and Munc13-2 (a vesicle priming protein) as the relevant effector proteins. PI(4,5)P2 activation of exocytosis did not depend on the PI(4,5)P2-binding CAPS-proteins, suggesting that PI(4,5)P2 uncaging may bypass CAPS-function. Finally, PI(4,5)P2 uncaging triggered the rapid fusion of a subset of readily-releasable vesicles, revealing a rapid role of PI(4,5)P2 in fusion triggering. Thus, optical uncaging of signaling lipids can uncover their rapid effects on cellular processes and identify lipid effectors.

Keywords: Munc13; adrenal chromaffin cell; cell biology; exocytosis; mouse; neuroscience; optical uncaging; phosphatidylinositols; synaptotagmin.

Publication types

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

MeSH terms

  • Animals
  • Carrier Proteins / metabolism
  • Cell Line
  • Chromaffin Cells / metabolism
  • Cytological Techniques / methods
  • Exocytosis*
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Membrane Proteins / metabolism
  • Mice
  • Nerve Tissue Proteins / metabolism
  • Phosphatidylinositol 4,5-Diphosphate / metabolism*
  • Synaptotagmin I / metabolism

Substances

  • Carrier Proteins
  • Cybr protein, mouse
  • Intracellular Signaling Peptides and Proteins
  • Membrane Proteins
  • Nerve Tissue Proteins
  • Phosphatidylinositol 4,5-Diphosphate
  • Synaptotagmin I
  • Syt1 protein, mouse
  • Unc13b protein, mouse