Document Type
Article
Publication Date
5-20-2023
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.
Recommended Citation
Ogunmowo, Tyler H; Jing, Haoyuan; Raychaudhuri, Sumana; Kusick, Grant F; Imoto, Yuuta; Li, Shuo; Itoh, Kie; Ma, Ye; Jafri, Haani; Dalva, Matthew B.; Chapman, Edwin R; Ha, Taekjip; Watanabe, Shigeki; and Liu, Jian, "Membrane Compression by Synaptic Vesicle Exocytosis Triggers Ultrafast Endocytosis" (2023). Department of Neuroscience Faculty Papers. Paper 77.
https://jdc.jefferson.edu/department_neuroscience/77
Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 License.
Additional Supplementary Files.pdf (48 kB)
Supplementary Movie 1.mov (756 kB)
Supplementary Movie 2.mov (801 kB)
Supplementary Movie 3.mov (606 kB)
Supplementary Movie 4.mov (398 kB)
Supplementary Movie 5.mov (393 kB)
Supplementary Movie 6.mov (80 kB)
Reporting Summary.pdf (2658 kB)
Language
English
Comments
This article is the author's final published version in Nature Communications, Volume 14, Issue 1, May 2023, Article number 2888.
The published version is available at https://doi.org/10.1038/s41467-023-38595-2.
Copyright © The Author(s) 2023
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.