RIM-BPs Mediate Tight Coupling of Action Potentials to Ca(2+)-Triggered Neurotransmitter Release

Neuron. 2015 Sep 23;87(6):1234-1247. doi: 10.1016/j.neuron.2015.08.027.

Abstract

Ultrafast neurotransmitter release requires tight colocalization of voltage-gated Ca(2+) channels with primed, release-ready synaptic vesicles at the presynaptic active zone. RIM-binding proteins (RIM-BPs) are multidomain active zone proteins that bind to RIMs and to Ca(2+) channels. In Drosophila, deletion of RIM-BPs dramatically reduces neurotransmitter release, but little is known about RIM-BP function in mammalian synapses. Here, we generated double conditional knockout mice for RIM-BP1 and RIM-BP2, and analyzed RIM-BP-deficient synapses in cultured hippocampal neurons and the calyx of Held. Surprisingly, we find that in murine synapses, RIM-BPs are not essential for neurotransmitter release as such, but are selectively required for high-fidelity coupling of action potential-induced Ca(2+) influx to Ca(2+)-stimulated synaptic vesicle exocytosis. Deletion of RIM-BPs decelerated action-potential-triggered neurotransmitter release and rendered it unreliable, thereby impairing the fidelity of synaptic transmission. Thus, RIM-BPs ensure optimal organization of the machinery for fast release in mammalian synapses without being a central component of the machinery itself.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • ATP-Binding Cassette Transporters / physiology*
  • Action Potentials / drug effects
  • Action Potentials / physiology*
  • Animals
  • Calcium / metabolism*
  • Calcium / pharmacology
  • Calcium Channels, N-Type / metabolism
  • Cells, Cultured
  • Excitatory Postsynaptic Potentials / drug effects
  • Excitatory Postsynaptic Potentials / physiology
  • HEK293 Cells
  • Hippocampus / drug effects
  • Hippocampus / metabolism
  • Humans
  • Inhibitory Postsynaptic Potentials / drug effects
  • Inhibitory Postsynaptic Potentials / physiology
  • Mice
  • Mice, Knockout
  • Neurotransmitter Agents / metabolism*
  • rab3 GTP-Binding Proteins / physiology*

Substances

  • ATP-Binding Cassette Transporters
  • Abca4 protein, mouse
  • CACNA1B protein, human
  • Calcium Channels, N-Type
  • Neurotransmitter Agents
  • voltage-dependent calcium channel (P-Q type)
  • Rim2 protein, mouse
  • rab3 GTP-Binding Proteins
  • Calcium