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Cited by 213Cellular transport and secretionLipid Membrane Structure and BehaviorCaveolin-1 and cellular processes

Membrane tension and peripheral protein density mediate membrane shape transitions

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Shi, Zheng, Baumgart, Tobias·2015·Nature Communications
DOI 10.1038/ncomms6974PMC PMC4353700
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Abstract

Endocytosis is a ubiquitous eukaryotic membrane budding, vesiculation and internalization process fulfilling numerous roles including compensation of membrane area increase after bursts of exocytosis. The mechanism of the coupling between these two processes to enable homeostasis is not well understood. Recently, an ultrafast endocytosis (UFE) pathway was revealed with a speed significantly exceeding classical clathrin-mediated endocytosis (CME). Membrane tension reduction is a potential mechanism by which endocytosis can be rapidly activated at remote sites. Here, we provide experimental evidence for a mechanism whereby membrane tension reduction initiates membrane budding and tubulation mediated by endocytic proteins, such as endophilin A1. We find that shape instabilities occur at well-defined membrane tensions and surface densities of endophilin. From our data, we obtain a membrane shape stability diagram that shows remarkable consistency with a quantitative model. This model applies to all laterally diffusive curvature-coupling proteins and therefore a wide range of endocytic proteins. An ultrafast mechanism of endocytosis was recently discovered, and proposed to be dependent on local reduction in membrane tension. Shi and Baumgart provide experimental support for this hypothesis by quantifying the impact of membrane tension on membrane tubulation by endocytic proteins, such as endophilin A1.

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  • A reduction in membrane tension after exocytosis cannot account for the kinetics and spatial precision of ultrafast endocytosis.

    “Therefore, even if membrane tension alters upon exocytosis, this model cannot account for the kinetics and spatial precision of ultrafast endocytosis.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [10]

    The Discussion (page unavailable) says the opposite about kinetics: lowering membrane tension after exocytic vesicle fusion could trigger endocytosis rapidly enough to be a plausible signal for ultrafast endocytosis. The Abstract also describes tension reduction as a way to activate endocytosis rapidly at remote sites. The paper does not establish the claimed failure of spatial precision. (LLM, conf=0.90)

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  • In the absence of calcium, presynaptic endocytic pits reminiscent of ultrafast endocytosis form when exocytosis is induced with a hyperosmotic shock.

    “Indeed, in the absence of calcium, presynaptic endocytic pits reminiscent of ultrafast endocytosis form when exocytosis is induced with a hyperosmotic shock10.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [10]

    The Discussion (page unavailable) proposes that reduced membrane tension after exocytic vesicle fusion could trigger endocytosis and discusses abortive pits. Neither it nor the passages retrieved for calcium and hyperosmotic shock report presynaptic pits forming without calcium after hyperosmotic-shock-induced exocytosis. (LLM, conf=0.78)

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Research works printed but not linked: 45

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Cited by

Sorted by citations

Authors
Shi, Z., & Baumgart, T.
Affiliations
University of Pennsylvania (US)
Corresponding author
Baumgart, Tobias
ORCID
Venue
Nature Communications
Publisher
Springer Science and Business Media LLC
Published
2015-01-08
Volume
6
Issue
1
Pages
5974-5974
ISSN
2041-1723 (ISSN-L)
DOI
10.1038/ncomms6974
PMC
PMC4353700
OpenAlex
W2055395908
Cited by
213
References
1
Citations by year
2026: 9 · 2025: 12 · 2024: 8 · 2023: 11 · 2022: 18 · 2021: 33 · 2020: 19 · 2019: 25 · 2018: 24 · 2017: 17 · 2016: 24 · 2015: 12
FWCI
13.68
Type
journal article
Language
en
Open access
Licence
Locations
  • Nature Communications (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
Funders
  • National Science Foundation (1053857)
  • National Institutes of Health
  • National Institute of General Medical Sciences (R01GM097552, GM097552)
  • Division of Chemical, Bioengineering, Environmental, and Transport Systems
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Caveolin-1 and cellular processes
Keywords
membrane tension, endophilin A1, membrane tubulation, membrane budding, shape instability, membrane homeostasis, clathrin-mediated endocytosis, membrane curvature
MeSH terms
Biomechanical Phenomena, Biophysics, Cell Membrane, Endocytosis, Exocytosis, Microscopy, Fluorescence, Models, Biological, Cell Shape, Adaptor Proteins, Signal Transducing

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