Biomolecular condensates mediate bending and scission of endosome membranes

Yanning Wang, Shulin Li, Marcel Mokbel, Alexander I. May, Zizhen Liang, Yonglun Zeng, Weiqi Wang, Honghong Zhang, Feifei Yu, Katharina Sporbeck, Liwen Jiang, Sebastian Aland, Jaime Agudo-Canalejo, Roland L. Knorr () and Xiaofeng Fang ()
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Yanning Wang: Tsinghua University
Shulin Li: Tsinghua University
Marcel Mokbel: Technical University Freiberg
Alexander I. May: Humboldt-Universität zu Berlin
Zizhen Liang: The Chinese University of Hong Kong
Yonglun Zeng: Chinese Academy of Sciences
Weiqi Wang: The Chinese University of Hong Kong
Honghong Zhang: Tsinghua University
Feifei Yu: China Agricultural University
Katharina Sporbeck: Humboldt-Universität zu Berlin
Liwen Jiang: The Chinese University of Hong Kong
Sebastian Aland: Technical University Freiberg
Jaime Agudo-Canalejo: Max Planck Institute for Dynamics and Self-Organization
Roland L. Knorr: Humboldt-Universität zu Berlin
Xiaofeng Fang: Tsinghua University

Nature, 2024, vol. 634, issue 8036, 1204-1210

Abstract: Abstract Multivesicular bodies are key endosomal compartments implicated in cellular quality control through their degradation of membrane-bound cargo proteins1–3. The ATP-consuming ESCRT protein machinery mediates the capture and engulfment of membrane-bound cargo proteins through invagination and scission of multivesicular-body membranes to form intraluminal vesicles4,5. Here we report that the plant ESCRT component FREE16 forms liquid-like condensates that associate with membranes to drive intraluminal vesicle formation. We use a minimal physical model, reconstitution experiments and in silico simulations to identify the dynamics of this process and describe intermediate morphologies of nascent intraluminal vesicles. Furthermore, we find that condensate-wetting-induced line tension forces and membrane asymmetries are sufficient to mediate scission of the membrane neck without the ESCRT protein machinery or ATP consumption. Genetic manipulation of the ESCRT pathway in several eukaryotes provides additional evidence for condensate-mediated membrane scission in vivo. We find that the interplay between condensate and machinery-mediated scission mechanisms is indispensable for osmotic stress tolerance in plants. We propose that condensate-mediated scission represents a previously undescribed scission mechanism that depends on the physicomolecular properties of the condensate and is involved in a range of trafficking processes. More generally, FREE1 condensate-mediated membrane scission in multivesicular-body biogenesis highlights the fundamental role of wetting in intracellular dynamics and organization.

Date: 2024
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DOI: 10.1038/s41586-024-07990-0

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