Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis

Tyler H. Ogunmowo, Haoyuan Jing, Sumana Raychaudhuri, Grant F. Kusick, Yuuta Imoto, Shuo Li, Kie Itoh, Ye Ma, Haani Jafri, Matthew B. Dalva, Edwin R. Chapman, Taekjip Ha, Shigeki Watanabe () and Jian Liu ()
Additional contact information
Tyler H. Ogunmowo: Johns Hopkins University
Haoyuan Jing: Johns Hopkins University
Sumana Raychaudhuri: Johns Hopkins University
Grant F. Kusick: Johns Hopkins University
Yuuta Imoto: Johns Hopkins University
Shuo Li: Johns Hopkins University
Kie Itoh: Johns Hopkins University
Ye Ma: Johns Hopkins University
Haani Jafri: Thomas Jefferson University
Matthew B. Dalva: Thomas Jefferson University
Edwin R. Chapman: University of Wisconsin-Madison
Taekjip Ha: Johns Hopkins University
Shigeki Watanabe: Johns Hopkins University
Jian Liu: Johns Hopkins University

Nature Communications, 2023, vol. 14, issue 1, 1-16

Abstract: Abstract 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.

Date: 2023
References: View references in EconPapers View complete reference list from CitEc
Citations:

Downloads: (external link)
https://www.nature.com/articles/s41467-023-38595-2 Abstract (text/html)

Related works:
This item may be available elsewhere in EconPapers: Search for items with the same title.

Export reference: BibTeX RIS (EndNote, ProCite, RefMan) HTML/Text

Persistent link: https://EconPapers.repec.org/RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38595-2

Ordering information: This journal article can be ordered from
https://www.nature.com/ncomms/

DOI: 10.1038/s41467-023-38595-2

Access Statistics for this article

Nature Communications is currently edited by Nathalie Le Bot, Enda Bergin and Fiona Gillespie

More articles in Nature Communications from Nature
Bibliographic data for series maintained by Sonal Shukla () and Springer Nature Abstracting and Indexing ().