Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
20 05 2023
20 05 2023
Historique:
received:
17
07
2022
accepted:
09
05
2023
medline:
22
5
2023
pubmed:
21
5
2023
entrez:
20
5
2023
Statut:
epublish
Résumé
Compensatory endocytosis keeps the membrane surface area of secretory cells constant following exocytosis. At chemical synapses, clathrin-independent ultrafast endocytosis maintains such homeostasis. This endocytic pathway is temporally and spatially coupled to exocytosis; it initiates within 50 ms at the region immediately next to the active zone where vesicles fuse. However, the coupling mechanism is unknown. Here, we demonstrate that filamentous actin is organized as a ring, surrounding the active zone at mouse hippocampal synapses. Assuming the membrane area conservation is due to this actin ring, our theoretical model suggests that flattening of fused vesicles exerts lateral compression in the plasma membrane, resulting in rapid formation of endocytic pits at the border between the active zone and the surrounding actin-enriched region. Consistent with model predictions, our data show that ultrafast endocytosis requires sufficient compression by exocytosis of multiple vesicles and does not initiate when actin organization is disrupted, either pharmacologically or by ablation of the actin-binding protein Epsin1. Our work suggests that membrane mechanics underlie the rapid coupling of exocytosis to endocytosis at synapses.
Identifiants
pubmed: 37210439
doi: 10.1038/s41467-023-38595-2
pii: 10.1038/s41467-023-38595-2
pmc: PMC10199930
doi:
Substances chimiques
Actins
0
Types de publication
Journal Article
Research Support, U.S. Gov't, Non-P.H.S.
Research Support, Non-U.S. Gov't
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Pagination
2888Subventions
Organisme : NIDA NIH HHS
ID : R01 DA022727
Pays : United States
Organisme : NINDS NIH HHS
ID : DP2 NS111133
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS105810
Pays : United States
Organisme : NIMH NIH HHS
ID : R01 MH061876
Pays : United States
Organisme : NINDS NIH HHS
ID : R35 NS097362
Pays : United States
Organisme : Howard Hughes Medical Institute
Pays : United States
Organisme : NINDS NIH HHS
ID : R01 NS106906
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM148459
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM007445
Pays : United States
Informations de copyright
© 2023. The Author(s).
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