Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions

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 sing...

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Main Authors: Shigeki Watanabe, Qiang Liu, M Wayne Davis, Gunther Hollopeter, Nikita Thomas, Nels B Jorgensen, Erik M Jorgensen
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2013-09-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/00723
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author Shigeki Watanabe
Qiang Liu
M Wayne Davis
Gunther Hollopeter
Nikita Thomas
Nels B Jorgensen
Erik M Jorgensen
author_facet Shigeki Watanabe
Qiang Liu
M Wayne Davis
Gunther Hollopeter
Nikita Thomas
Nels B Jorgensen
Erik M Jorgensen
author_sort Shigeki Watanabe
collection DOAJ
description 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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spelling doaj.art-3c9b8f7c312a4155964027368d6deb0d2022-12-22T03:33:26ZengeLife Sciences Publications LtdeLife2050-084X2013-09-01210.7554/eLife.00723Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctionsShigeki Watanabe0Qiang Liu1M Wayne Davis2Gunther Hollopeter3Nikita Thomas4Nels B Jorgensen5Erik M Jorgensen6Department of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesDepartment of Biology, Howard Hughes Medical Institute, University of Utah, Salt Lake City, United StatesSynaptic 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.https://elifesciences.org/articles/00723synaptic vesicle endocytosisoptogeneticstime-resolved electron microscopyhigh-pressure freezingsynaptic vesicle exocytosisactive zone
spellingShingle Shigeki Watanabe
Qiang Liu
M Wayne Davis
Gunther Hollopeter
Nikita Thomas
Nels B Jorgensen
Erik M Jorgensen
Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
eLife
synaptic vesicle endocytosis
optogenetics
time-resolved electron microscopy
high-pressure freezing
synaptic vesicle exocytosis
active zone
title Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
title_full Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
title_fullStr Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
title_full_unstemmed Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
title_short Ultrafast endocytosis at Caenorhabditis elegans neuromuscular junctions
title_sort ultrafast endocytosis at caenorhabditis elegans neuromuscular junctions
topic synaptic vesicle endocytosis
optogenetics
time-resolved electron microscopy
high-pressure freezing
synaptic vesicle exocytosis
active zone
url https://elifesciences.org/articles/00723
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