CaV2.2 Gates Calcium-Independent but Voltage-Dependent Secretion in Mammalian Sensory Neurons

Neuron. 2017 Dec 20;96(6):1317-1326.e4. doi: 10.1016/j.neuron.2017.10.028. Epub 2017 Nov 30.

Abstract

Action potential induces membrane depolarization and triggers intracellular free Ca2+ concentration (Ca2+)-dependent secretion (CDS) via Ca2+ influx through voltage-gated Ca2+ channels. We report a new type of somatic exocytosis triggered by the action potential per se-Ca2+-independent but voltage-dependent secretion (CiVDS)-in dorsal root ganglion neurons. Here we uncovered the molecular mechanism of CiVDS, comprising a voltage sensor, fusion machinery, and their linker. Specifically, the voltage-gated N-type Ca2+ channel (CaV2.2) is the voltage sensor triggering CiVDS, the SNARE complex functions as the vesicle fusion machinery, the "synprint" of CaV2.2 serves as a linker between the voltage sensor and the fusion machinery, and ATP is a cargo of CiVDS vesicles. Thus, CiVDS releases ATP from the soma while CDS releases glutamate from presynaptic terminals, establishing the CaV2.2-SNARE "voltage-gating fusion pore" as a novel pathway co-existing with the canonical "Ca2+-gating fusion pore" pathway for neurotransmitter release following action potentials in primary sensory neurons.

Keywords: ATP release; CA dependent secretion; CaV2.2; CiVDS; DRG; N-type calcium channel; SNAP25; TIRF; quantal; synprint.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Action Potentials / drug effects
  • Animals
  • Caffeine / pharmacology
  • Calcium / metabolism*
  • Calcium Channel Blockers / pharmacology
  • Calcium Channels, N-Type / genetics*
  • Calcium Channels, N-Type / metabolism*
  • Cells, Cultured
  • Endoplasmic Reticulum / drug effects
  • Endoplasmic Reticulum / ultrastructure
  • Exocytosis / drug effects
  • Exocytosis / genetics
  • Ganglia, Spinal / cytology
  • Ganglia, Spinal / ultrastructure
  • Humans
  • Ion Channel Gating / drug effects
  • Ion Channel Gating / genetics*
  • Male
  • Membrane Fusion / drug effects
  • Membrane Fusion / genetics
  • Models, Molecular
  • Phosphodiesterase Inhibitors / pharmacology
  • Presynaptic Terminals / drug effects
  • Presynaptic Terminals / physiology
  • Rats
  • Rats, Sprague-Dawley
  • Rats, Wistar
  • SNARE Proteins / genetics
  • SNARE Proteins / metabolism
  • Sensory Receptor Cells / physiology*
  • Sensory Receptor Cells / ultrastructure
  • Synaptic Transmission / drug effects
  • Synaptic Transmission / genetics
  • Transduction, Genetic
  • omega-Conotoxin GVIA / pharmacology

Substances

  • Cacna1b protein, rat
  • Calcium Channel Blockers
  • Calcium Channels, N-Type
  • Phosphodiesterase Inhibitors
  • SNARE Proteins
  • Caffeine
  • omega-Conotoxin GVIA
  • Calcium