Actin dynamics provides membrane tension to merge fusing vesicles into the plasma membrane

Peter J Wen, Staffan Grenklo, Gianvito Arpino, Xinyu Tan, Hsien-Shun Liao, Johanna Heureaux, Shi-Yong Peng, Hsueh-Cheng Chiang, Edaeni Hamid, Wei-Dong Zhao, Wonchul Shin, Tuomas Näreoja, Emma Evergren, Yinghui Jin, Roger Karlsson, Steven N Ebert, Albert Jin, Allen P Liu, Oleg Shupliakov, Ling-Gang Wu

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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.

Original languageEnglish
Article number12604
JournalNature Communications
Volume7
DOIs
Publication statusPublished - 31 Aug 2016

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