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Cited by 248Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions

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Watanabe, Shigeki, Liu, Qiang, Davis, M Wayne, Hollopeter, Gunther, Thomas, Nikita, Jorgensen, Nels B, Jorgensen, Erik M·2013·eLife
DOI 10.7554/elife.00723PMC PMC3762212
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Abstract

Synaptic vesicles can be released at extremely high rates, which places an extraordinary demand on the recycling machinery. Previous ultrastructural studies of vesicle recycling were conducted in dissected preparations using an intense stimulation to maximize the probability of release. Here, a single light stimulus was applied to motor neurons in intact Caenorhabditis elegans nematodes expressing channelrhodopsin, and the animals rapidly frozen. We found that docked vesicles fuse along a broad active zone in response to a single stimulus, and are replenished with a time constant of about 2 s. Endocytosis occurs within 50 ms adjacent to the dense projection and after 1 s adjacent to adherens junctions. These studies suggest that synaptic vesicle endocytosis may occur on a millisecond time scale following a single physiological stimulus in the intact nervous system and is unlikely to conform to current models of endocytosis.

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  • In ultrafast endocytosis, endocytic invaginations always form at the edge of the active zone.

    “In this pathway, endocytic invaginations always form at the edge of the active zone5–7.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [6]

    The Results describe invaginations next to the dense projection 20 ms after stimulation and others at flanking adherens junctions later. The Discussion (‘Two endocytic sites?’) explicitly identifies both as endocytic sites, contrary to ‘always’ at the edge of the active zone. No page numbers are available in our copy. (LLM, conf=0.87)

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  • Synaptic vesicle endocytosis at mammalian central synapses is mediated by clathrin-independent ultrafast endocytosis.

    “Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [6]

    The Discussion reports ultrafast endocytosis after stimulation at C. elegans neuromuscular junctions, not at mammalian central synapses. In “Clathrin-mediated or kiss-and run?” (page unavailable), it says the observed pits lack clathrin coats but explicitly does not exclude a role for clathrin. The source therefore supports the ultrafast aspect, but not the claimed setting or an established clathrin-independent mechanism there. (LLM, conf=0.90)

    Experimental — accuracy not yet measured

  • Ultrafast endocytosis is tightly coupled to exocytosis in time and space.

    “Several recent studies suggest that synaptic vesicle endocytosis is mediated by clathrin-independent ultrafast endocytosis at mammalian central synapses and is tightly coupled to exocytosis in time and space5–9.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [6]

  • The timing and location of endocytic pit formation in simulations quantitatively recapitulates endocytic events observed by ultrastructural analysis.

    “Importantly, the timing and the location of endocytic pit formation quantitatively recapitulates endocytic events observed by ultrastructural analysis5,6.”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [6]

  • Ultrafast endocytosis is compensatory: the membrane area of endocytic vesicles is roughly equal to the total surface area of synaptic vesicles exocytosed.

    “Interestingly, ultrafast endocytosis is compensatory - the membrane area of endocytic vesicles is roughly equal to the total surface area of synaptic vesicles exocytosed5,6”

    From Membrane compression by synaptic vesicle exocytosis triggers ultrafast endocytosis (2023) · cites this paper as [6]

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Cited by

Sorted by citations

Authors
Watanabe, S., Liu, Q., Davis, M. W., Hollopeter, G., Thomas, N., Jorgensen, N. B., & Jorgensen, E. M.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Department of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United States
ORCID
Venue
eLife
Publisher
eLife Sciences Publications, Ltd
Published
2013-09-03
Volume
2
Pages
e00723-e00723
ISSN
2050-084X (ISSN-L)
DOI
10.7554/elife.00723
PMC
PMC3762212
OpenAlex
W2081406232
Cited by
248
References
5
Citations by year
2026: 6 · 2025: 14 · 2024: 18 · 2023: 17 · 2022: 26 · 2021: 15 · 2020: 26 · 2019: 23 · 2018: 17 · 2017: 21 · 2016: 19 · 2015: 20 · 2014: 23 · 2013: 3
FWCI
12.57
Type
journal article
Language
en
Open access
Licence
Locations
  • eLife (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Funders
  • National Institutes of Health (NS034307)
  • National Science Foundation (0920069)
  • Howard Hughes Medical Institute
  • Marine Biological Laboratory (The Dart Scholars Program)
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
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords
synaptic vesicle endocytosis, vesicle recycling, neuromuscular junction, Caenorhabditis elegans, motor neurons, active zone, adherens junctions
MeSH terms
Animals, Endocytosis, Neuromuscular Junction, Caenorhabditis elegans

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