The Synaptic Vesicle Cycle Revisited: New Insights into the Modes and Mechanisms

Natali L. Chanaday, Michael A. Cousin, Ira Milosevic, Shigeki Watanabe, Jennifer R. Morgan

Research output: Contribution to journalArticle

Abstract

Neurotransmission is sustained by endocytosis and refilling of synaptic vesicles (SVs) locally within the presynapse. Until recently, a consensus formed that after exocytosis, SVs are recovered by either fusion pore closure (kiss-and-run) or clathrin-mediated endocytosis directly from the plasma membrane. However, recent data have revealed that SV formation is more complex than previously envisaged. For example, two additional recycling pathways have been discovered, ultrafast endocytosis and activity-dependent bulk endocytosis, in which SVs are regenerated from the internalized membrane and synaptic endosomes. Furthermore, these diverse modes of endocytosis appear to influence both the molecular composition and subsequent physiological role of individual SVs. In addition, previously unknown complexity in SV refilling and reclustering has been revealed. This review presents a modern view of the SV life cycle and discusses how neuronal subtype, physiological temperature, and individual activity patterns can recruit different endocytic modes to generate new SVs and sculpt subsequent presynaptic performance.

Original languageEnglish (US)
Pages (from-to)8209-8216
Number of pages8
JournalThe Journal of neuroscience : the official journal of the Society for Neuroscience
Volume39
Issue number42
DOIs
StatePublished - Oct 16 2019

Fingerprint

Synaptic Vesicles
Endocytosis
Synaptic Membranes
Clathrin
Endosomes
Exocytosis
Life Cycle Stages
Synaptic Transmission
Cell Membrane
Temperature

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

The Synaptic Vesicle Cycle Revisited : New Insights into the Modes and Mechanisms. / Chanaday, Natali L.; Cousin, Michael A.; Milosevic, Ira; Watanabe, Shigeki; Morgan, Jennifer R.

In: The Journal of neuroscience : the official journal of the Society for Neuroscience, Vol. 39, No. 42, 16.10.2019, p. 8209-8216.

Research output: Contribution to journalArticle

Chanaday, Natali L. ; Cousin, Michael A. ; Milosevic, Ira ; Watanabe, Shigeki ; Morgan, Jennifer R. / The Synaptic Vesicle Cycle Revisited : New Insights into the Modes and Mechanisms. In: The Journal of neuroscience : the official journal of the Society for Neuroscience. 2019 ; Vol. 39, No. 42. pp. 8209-8216.
@article{ae93fabf18b342a19c7914c17d05f907,
title = "The Synaptic Vesicle Cycle Revisited: New Insights into the Modes and Mechanisms",
abstract = "Neurotransmission is sustained by endocytosis and refilling of synaptic vesicles (SVs) locally within the presynapse. Until recently, a consensus formed that after exocytosis, SVs are recovered by either fusion pore closure (kiss-and-run) or clathrin-mediated endocytosis directly from the plasma membrane. However, recent data have revealed that SV formation is more complex than previously envisaged. For example, two additional recycling pathways have been discovered, ultrafast endocytosis and activity-dependent bulk endocytosis, in which SVs are regenerated from the internalized membrane and synaptic endosomes. Furthermore, these diverse modes of endocytosis appear to influence both the molecular composition and subsequent physiological role of individual SVs. In addition, previously unknown complexity in SV refilling and reclustering has been revealed. This review presents a modern view of the SV life cycle and discusses how neuronal subtype, physiological temperature, and individual activity patterns can recruit different endocytic modes to generate new SVs and sculpt subsequent presynaptic performance.",
author = "Chanaday, {Natali L.} and Cousin, {Michael A.} and Ira Milosevic and Shigeki Watanabe and Morgan, {Jennifer R.}",
year = "2019",
month = "10",
day = "16",
doi = "10.1523/JNEUROSCI.1158-19.2019",
language = "English (US)",
volume = "39",
pages = "8209--8216",
journal = "Journal of Neuroscience",
issn = "0270-6474",
publisher = "Society for Neuroscience",
number = "42",

}

TY - JOUR

T1 - The Synaptic Vesicle Cycle Revisited

T2 - New Insights into the Modes and Mechanisms

AU - Chanaday, Natali L.

AU - Cousin, Michael A.

AU - Milosevic, Ira

AU - Watanabe, Shigeki

AU - Morgan, Jennifer R.

PY - 2019/10/16

Y1 - 2019/10/16

N2 - Neurotransmission is sustained by endocytosis and refilling of synaptic vesicles (SVs) locally within the presynapse. Until recently, a consensus formed that after exocytosis, SVs are recovered by either fusion pore closure (kiss-and-run) or clathrin-mediated endocytosis directly from the plasma membrane. However, recent data have revealed that SV formation is more complex than previously envisaged. For example, two additional recycling pathways have been discovered, ultrafast endocytosis and activity-dependent bulk endocytosis, in which SVs are regenerated from the internalized membrane and synaptic endosomes. Furthermore, these diverse modes of endocytosis appear to influence both the molecular composition and subsequent physiological role of individual SVs. In addition, previously unknown complexity in SV refilling and reclustering has been revealed. This review presents a modern view of the SV life cycle and discusses how neuronal subtype, physiological temperature, and individual activity patterns can recruit different endocytic modes to generate new SVs and sculpt subsequent presynaptic performance.

AB - Neurotransmission is sustained by endocytosis and refilling of synaptic vesicles (SVs) locally within the presynapse. Until recently, a consensus formed that after exocytosis, SVs are recovered by either fusion pore closure (kiss-and-run) or clathrin-mediated endocytosis directly from the plasma membrane. However, recent data have revealed that SV formation is more complex than previously envisaged. For example, two additional recycling pathways have been discovered, ultrafast endocytosis and activity-dependent bulk endocytosis, in which SVs are regenerated from the internalized membrane and synaptic endosomes. Furthermore, these diverse modes of endocytosis appear to influence both the molecular composition and subsequent physiological role of individual SVs. In addition, previously unknown complexity in SV refilling and reclustering has been revealed. This review presents a modern view of the SV life cycle and discusses how neuronal subtype, physiological temperature, and individual activity patterns can recruit different endocytic modes to generate new SVs and sculpt subsequent presynaptic performance.

UR - http://www.scopus.com/inward/record.url?scp=85073459874&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=85073459874&partnerID=8YFLogxK

U2 - 10.1523/JNEUROSCI.1158-19.2019

DO - 10.1523/JNEUROSCI.1158-19.2019

M3 - Article

C2 - 31619489

AN - SCOPUS:85073459874

VL - 39

SP - 8209

EP - 8216

JO - Journal of Neuroscience

JF - Journal of Neuroscience

SN - 0270-6474

IS - 42

ER -