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Cited by 10Cellular transport and secretionNeuroscience and Neuropharmacology ResearchAutophagy in Disease and Therapy

Beyond Clathrin: Decoding the Mechanism of Ultrafast Endocytosis

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Imoto, Yuuta, Watanabe, Shigeki·2025·Physiology
DOI 10.1152/physiol.00041.2024PMC PMC12244253
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Abstract

Endocytosis in nonneuronal cells requires gradual recruitment of proteins to endocytic sites for inducing membrane curvature and forming scaffolds around the neck of endocytic pits. This recruitment process is thought to be rate-limiting, requiring tens of seconds. In contrast, a form of endocytosis in neurons called ultrafast endocytosis is much faster, requiring only 100 ms. In this review, we compare the mechanisms of protein recruitment during clathrin-mediated endocytosis in nonneuronal cells and ultrafast endocytosis in neurons and discuss how endocytosis can complete within 100 ms. We then discuss the potential clinical relevance of this endocytic pathway.

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Crossref · 10.1152/physiol.00041.2024

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  • Clathrin-mediated endocytosis (CME) is the most prevalent pathway for SV retrieval, involving clathrin-coated pits that bud off within tens of seconds following full-collapse fusion.

    “Clathrin-mediated endocytosis (CME) is the most prevalent pathway for SV retrieval. It involves the formation of clathrin-coated pits that bud off from the plasma membrane, internalizing SV components within tens of seconds following full-collapse fusion [30,31].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [31]

    The ‘Kinetics and molecular mechanisms of clathrin-mediated endocytosis’ section (page not available) describes clathrin-coated pits budding from the plasma membrane and gives a 10–30-second timescale for synaptic-vesicle retrieval via CME. It calls CME the most well-characterized endocytic pathway, not the most prevalent pathway for synaptic-vesicle retrieval, and does not tie that timescale specifically to full-collapse fusion. (LLM, conf=0.87)

    Experimental — accuracy not yet measured

  • The molecular switch shifting retrieval toward ultrafast endocytosis is primarily mechanical, driven by a 'membrane compression model' where fused synaptic vesicles exert lateral pressure against an F-actin-enriched stiff periactive zone, inducing rapid membrane buckling and curvature independent of clathrin recruitment.

    “The molecular switch shifting retrieval toward ultrafast endocytosis is primarily mechanical, driven by a ‘membrane compression model’ where fused synaptic vesicles exert lateral pressure against an F-actin-enriched stiff periactive zone, inducing rapid membrane buckling and curvature independent of clathrin recruitment [31,34].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [31]

    The Introduction’s “Kinetics and molecular mechanisms” section describes the proposed membrane-compression model: fused vesicles laterally compress an F-actin-enriched region, producing curvature akin to buckling. It also says early initiation is likely mechanical and that ultrafast endocytosis is clathrin-independent. But it presents compression as one of two potential models, not an established molecular switch that primarily drives the shift to ultrafast retrieval. The supplied passages have no page numbers. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Bulk endocytosis is triggered by intense or prolonged neuronal stimulation and involves retrieval of large portions of the plasma membrane as large endocytic vacuoles, from which new SVs are regenerated through clathrin-mediated budding.

    “Bulk endocytosis is triggered by intense or prolonged neuronal stimulation. This pathway involves the retrieval of large portions of the plasma membrane in the form of large endocytic vacuoles [30]. New SVs are subsequently regenerated from these larger structures through clathrin-mediated budding [12,31].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [31]

    The Introduction and Conclusion and perspectives identify activity-dependent bulk endocytosis as a pathway involved in synaptic-vesicle recycling. The Introduction describes clathrin-dependent sorting at endosomes for ultrafast endocytosis, not bulk endocytosis. Our copy does not establish intense or prolonged stimulation, retrieval as large vacuoles, or clathrin-mediated budding from those vacuoles for the bulk pathway. No page numbers are available in our copy. (LLM, conf=0.78)

    Experimental — accuracy not yet measured

  • Following exocytosis, synaptic vesicles are recovered through clathrin-mediated, ultrafast, bulk, or kiss-and-run endocytic pathways.

    “Following exocytosis, synaptic vesicles are recovered through clathrin-mediated, ultrafast, bulk, or kiss-and-run endocytic pathways.”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [31]

  • Kiss-and-run is a rapid mechanism involving transient opening of a fusion pore, allowing neurotransmitter release without full collapse of the SV, with retrieval often within approximately one second.

    “Kiss-and-run is a rapid mechanism that involves a transient opening of a fusion pore, allowing for neurotransmitter release without full collapse of the SV into the plasma membrane [30]. The vesicle is then rapidly retrieved, often within approximately one second [31,32].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [31]

    The Introduction lists kiss-and-run as a model but gives no account of its fusion pore or retrieval time. It assigns retrieval within 100 ms to a separate pathway, ultrafast endocytosis. Searches for kiss-and-run retrieval and one-second timing found no passage establishing the attributed claim. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

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200 of 217 shown

Authors
Imoto, Y., & Watanabe, S.
Affiliations
  • St. Jude Children's Research Hospital (US)
  • Johns Hopkins University (US)
Corresponding author
  • Imoto, Yuuta
  • Watanabe, Shigeki
ORCID
Venue
Physiology
Publisher
American Physiological Society
Published
2025-09-01
Volume
40
Issue
5
Pages
454-469
ISSN
  • 0886-1714 (ISSN-L)
  • 1548-9213
  • 1548-9221
DOI
10.1152/physiol.00041.2024
PMC
PMC12244253
OpenAlex
W4408301626
Cited by
10
References
1
Citations by year
2026: 6 · 2025: 4
FWCI
1.19
Type
journal article
Language
en
Open access
Locations
  • Physiology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
Funders
  • HHS | NIH | National Institute of Neurological Disorders and Stroke (NS111133-01, NS105810-01A1, NS132153)
  • Alfred P. Sloan Foundation
  • McKnight Endowment Fund for Neuroscience
  • Esther A. and Joseph Klingenstein Fund
  • Chan Zuckerberg Initiative
  • Brain Research Foundation
  • Vallee Foundation
  • MEXT | Japan Society for the Promotion of Science
  • Kazato Research Foundation
  • American Lebanese Syrian Associated Charities
  • JHU | School of Medicine, Johns Hopkins University
  • Johns Hopkins Discovery funds
  • Johns Hopkins Catalyst award
  • Marine Biological Laboratory Whitman Fellowship
  • Helis Foundation award
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
  • Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
Keywords
clathrin-mediated endocytosis, protein recruitment, membrane curvature, non-neuronal cells
MeSH terms
Animals, Cell Membrane, Clathrin, Endocytosis, Humans, Neurons, Clathrin-Coated Vesicles

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