Actin dynamics provides membrane tension to merge fusing vesicles into the plasma membrane
Journal
Nature communications
Journal Volume
7
Journal Issue
1
Date Issued
2016
Author(s)
Wen, Peter J
Grenklo, Staffan
Arpino, Gianvito
Tan, Xinyu
Heureaux, Johanna
Peng, Shi-Yong
Chiang, Hsueh-Cheng
Hamid, Edaeni
Zhao, Wei-Dong
Shin, Wonchul
Näreoja, Tuomas
Evergren, Emma
Jin, Yinghui
Karlsson, Roger
Ebert, Steven N
Jin, Albert
Liu, Allen P
Shupliakov, Oleg
Wu, Ling-Gang
Abstract
Vesicle fusion is executed via formation of an Ω-shaped structure (Ω-profile), followed by closure (kiss-and-run) or merging of the Ω-profile into the plasma membrane (full fusion). Although Ω-profile closure limits release but recycles vesicles economically, Ω-profile merging facilitates release but couples to classical endocytosis for recycling. Despite its crucial role in determining exocytosis/endocytosis modes, how Ω-profile merging is mediated is poorly understood in endocrine cells and neurons containing small ∼30-300 nm vesicles. Here, using confocal and super-resolution STED imaging, force measurements, pharmacology and gene knockout, we show that dynamic assembly of filamentous actin, involving ATP hydrolysis, N-WASP and formin, mediates Ω-profile merging by providing sufficient plasma membrane tension to shrink the Ω-profile in neuroendocrine chromaffin cells containing ∼300 nm vesicles. Actin-directed compounds also induce Ω-profile accumulation at lamprey synaptic active zones, suggesting that actin may mediate Ω-profile merging at synapses. These results uncover molecular and biophysical mechanisms underlying Ω-profile merging.
Other Subjects
adenosine triphosphate; beta actin; F actin; neural Wiskott Aldrich syndrome protein; phospholipase C delta; actin; biochemistry; biophysics; cells and cell components; hydrolysis; membrane; physiology; protein; actin filament; actin polymerization; animal cell; Article; cell membrane; cell membrane depolarization; chromaffin cell; confocal microscopy; controlled study; electron microscopy; endocytosis; exocytosis; gene inactivation; lamprey; membrane vesicle; microtubule assembly; molecular dynamics; molecular imaging; mouse; neurosecretory cell; nonhuman; protein hydrolysis; super resolution stimulated emission depletion imaging; tension; animal; biological model; bovine; C57BL mouse; cell membrane; female; gene knockout; genetics; image processing; knockout mouse; male; membrane fusion; metabolism; microscopy; nerve cell; patch clamp technique; primary cell culture; procedures; secretory vesicle; synapse; synapse vesicle; Petromyzontidae; Actins; Animals; Cattle; Cell Membrane; Chromaffin Cells; Endocytosis; Exocytosis; Female; Gene Knockout Techniques; Image Processing, Computer-Assisted; Lampreys; Male; Membrane Fusion; Mice; Mice, Inbred C57BL; Mice, Knockout; Microscopy; Models, Biological; Molecular Imaging; Neurons; Patch-Clamp Techniques; Primary Cell Culture; Secretory Vesicles; Synapses; Synaptic Vesicles
Publisher
NATURE PUBLISHING GROUP
Type
journal article