Molecular underpinnings of synaptic vesicle pool heterogeneity

Devon C. Crawford, Ege T. Kavalali

Research output: Contribution to journalArticle

27 Citations (Scopus)

Abstract

Neuronal communication relies on chemical synaptic transmission for information transfer and processing. Chemical neurotransmission is initiated by synaptic vesicle fusion with the presynaptic active zone resulting in release of neurotransmitters. Classical models have assumed that all synaptic vesicles within a synapse have the same potential to fuse under different functional contexts. In this model, functional differences among synaptic vesicle populations are ascribed to their spatial distribution in the synapse with respect to the active zone. Emerging evidence suggests, however, that synaptic vesicles are not a homogenous population of organelles, and they possess intrinsic molecular differences and differential interaction partners. Recent studies have reported a diverse array of synaptic molecules that selectively regulate synaptic vesicles' ability to fuse synchronously and asynchronously in response to action potentials or spontaneously irrespective of action potentials. Here we discuss these molecular mediators of vesicle pool heterogeneity that are found on the synaptic vesicle membrane, on the presynaptic plasma membrane, or within the cytosol and consider some of the functional consequences of this diversity. This emerging molecular framework presents novel avenues to probe synaptic function and uncover how synaptic vesicle pools impact neuronal signaling.

Original languageEnglish (US)
Pages (from-to)338-364
Number of pages27
JournalTraffic
Volume16
Issue number4
DOIs
StatePublished - Apr 1 2015

Fingerprint

Synaptic Vesicles
Electric fuses
Cell membranes
Spatial distribution
Neurotransmitter Agents
Fusion reactions
Membranes
Molecules
Communication
Synaptic Transmission
Synapses
Action Potentials
Processing
Synaptic Membranes
Automatic Data Processing
Organelles
Cytosol
Population
Cell Membrane

Keywords

  • Asynchronous neurotransmission
  • Neurotransmitter release
  • SNARE proteins
  • Spontaneous neurotransmission
  • Synaptic transmission
  • Synaptic vesicle
  • Synchronous neurotransmission
  • Vesicle exocytosis
  • Vesicle pools

ASJC Scopus subject areas

  • Biochemistry
  • Cell Biology
  • Structural Biology
  • Molecular Biology
  • Genetics

Cite this

Molecular underpinnings of synaptic vesicle pool heterogeneity. / Crawford, Devon C.; Kavalali, Ege T.

In: Traffic, Vol. 16, No. 4, 01.04.2015, p. 338-364.

Research output: Contribution to journalArticle

Crawford, Devon C. ; Kavalali, Ege T. / Molecular underpinnings of synaptic vesicle pool heterogeneity. In: Traffic. 2015 ; Vol. 16, No. 4. pp. 338-364.
@article{71befe30553149dca7dd258008d72e0a,
title = "Molecular underpinnings of synaptic vesicle pool heterogeneity",
abstract = "Neuronal communication relies on chemical synaptic transmission for information transfer and processing. Chemical neurotransmission is initiated by synaptic vesicle fusion with the presynaptic active zone resulting in release of neurotransmitters. Classical models have assumed that all synaptic vesicles within a synapse have the same potential to fuse under different functional contexts. In this model, functional differences among synaptic vesicle populations are ascribed to their spatial distribution in the synapse with respect to the active zone. Emerging evidence suggests, however, that synaptic vesicles are not a homogenous population of organelles, and they possess intrinsic molecular differences and differential interaction partners. Recent studies have reported a diverse array of synaptic molecules that selectively regulate synaptic vesicles' ability to fuse synchronously and asynchronously in response to action potentials or spontaneously irrespective of action potentials. Here we discuss these molecular mediators of vesicle pool heterogeneity that are found on the synaptic vesicle membrane, on the presynaptic plasma membrane, or within the cytosol and consider some of the functional consequences of this diversity. This emerging molecular framework presents novel avenues to probe synaptic function and uncover how synaptic vesicle pools impact neuronal signaling.",
keywords = "Asynchronous neurotransmission, Neurotransmitter release, SNARE proteins, Spontaneous neurotransmission, Synaptic transmission, Synaptic vesicle, Synchronous neurotransmission, Vesicle exocytosis, Vesicle pools",
author = "Crawford, {Devon C.} and Kavalali, {Ege T.}",
year = "2015",
month = "4",
day = "1",
doi = "10.1111/tra.12262",
language = "English (US)",
volume = "16",
pages = "338--364",
journal = "Traffic",
issn = "1398-9219",
publisher = "Blackwell Munksgaard",
number = "4",

}

TY - JOUR

T1 - Molecular underpinnings of synaptic vesicle pool heterogeneity

AU - Crawford, Devon C.

AU - Kavalali, Ege T.

PY - 2015/4/1

Y1 - 2015/4/1

N2 - Neuronal communication relies on chemical synaptic transmission for information transfer and processing. Chemical neurotransmission is initiated by synaptic vesicle fusion with the presynaptic active zone resulting in release of neurotransmitters. Classical models have assumed that all synaptic vesicles within a synapse have the same potential to fuse under different functional contexts. In this model, functional differences among synaptic vesicle populations are ascribed to their spatial distribution in the synapse with respect to the active zone. Emerging evidence suggests, however, that synaptic vesicles are not a homogenous population of organelles, and they possess intrinsic molecular differences and differential interaction partners. Recent studies have reported a diverse array of synaptic molecules that selectively regulate synaptic vesicles' ability to fuse synchronously and asynchronously in response to action potentials or spontaneously irrespective of action potentials. Here we discuss these molecular mediators of vesicle pool heterogeneity that are found on the synaptic vesicle membrane, on the presynaptic plasma membrane, or within the cytosol and consider some of the functional consequences of this diversity. This emerging molecular framework presents novel avenues to probe synaptic function and uncover how synaptic vesicle pools impact neuronal signaling.

AB - Neuronal communication relies on chemical synaptic transmission for information transfer and processing. Chemical neurotransmission is initiated by synaptic vesicle fusion with the presynaptic active zone resulting in release of neurotransmitters. Classical models have assumed that all synaptic vesicles within a synapse have the same potential to fuse under different functional contexts. In this model, functional differences among synaptic vesicle populations are ascribed to their spatial distribution in the synapse with respect to the active zone. Emerging evidence suggests, however, that synaptic vesicles are not a homogenous population of organelles, and they possess intrinsic molecular differences and differential interaction partners. Recent studies have reported a diverse array of synaptic molecules that selectively regulate synaptic vesicles' ability to fuse synchronously and asynchronously in response to action potentials or spontaneously irrespective of action potentials. Here we discuss these molecular mediators of vesicle pool heterogeneity that are found on the synaptic vesicle membrane, on the presynaptic plasma membrane, or within the cytosol and consider some of the functional consequences of this diversity. This emerging molecular framework presents novel avenues to probe synaptic function and uncover how synaptic vesicle pools impact neuronal signaling.

KW - Asynchronous neurotransmission

KW - Neurotransmitter release

KW - SNARE proteins

KW - Spontaneous neurotransmission

KW - Synaptic transmission

KW - Synaptic vesicle

KW - Synchronous neurotransmission

KW - Vesicle exocytosis

KW - Vesicle pools

UR - http://www.scopus.com/inward/record.url?scp=84925943313&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=84925943313&partnerID=8YFLogxK

U2 - 10.1111/tra.12262

DO - 10.1111/tra.12262

M3 - Article

VL - 16

SP - 338

EP - 364

JO - Traffic

JF - Traffic

SN - 1398-9219

IS - 4

ER -