Synaptic weight set by Munc13-1 supramolecular assemblies

Sakamoto, Hirokazu; Ariyoshi, Tetsuroh; Kimpara, Naoya; Sugao, Kohtaroh; Taiko, Isamu; Takikawa, Kenji; Asanuma, Daisuke; Namiki, Shigeyuki; Hirose, Kenzo

doi:10.1038/s41593-017-0041-9

Cited by 235Neuroscience and Neuropharmacology ResearchCellular transport and secretionExtracellular vesicles in disease

Synaptic weight set by Munc13-1 supramolecular assemblies

Sakamoto, Hirokazu, Ariyoshi, Tetsuroh, Kimpara, Naoya, Sugao, Kohtaroh, Taiko, Isamu, Takikawa, Kenji, Asanuma, Daisuke, Namiki, Shigeyuki +1 more·2018·Nature Neuroscience

DOI 10.1038/s41593-017-0041-9

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Abstract

The weight of synaptic connections, which is controlled not only postsynaptically but also presynaptically, is a key determinant in neuronal network dynamics. The mechanisms controlling synaptic weight, especially on the presynaptic side, remain elusive. Using single-synapse imaging of the neurotransmitter glutamate combined with super-resolution imaging of presynaptic proteins, we identify a presynaptic mechanism for setting weight in central glutamatergic synapses. In the presynaptic terminal, Munc13-1 molecules form multiple and discrete supramolecular self-assemblies that serve as independent vesicular release sites by recruiting syntaxin-1, a soluble N-ethylmaleimide-sensitive-factor attachment receptor (SNARE) protein essential for synaptic vesicle exocytosis. The multiplicity of these Munc13-1 assemblies affords multiple stable states conferring presynaptic weight, potentially encoding several bits of information at individual synapses. Supramolecular assembling enables a stable synaptic weight, which confers robustness of synaptic computation on neuronal circuits and may be a general mechanism by which biological processes operate despite the presence of molecular noise.

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Forskolin slightly reduces the distance between CaV2.1 Ca2+ channels and Munc13-1.
“Furthermore, we discovered that forskolin slightly reduced the distance between CaV2.1 (P/Q-type) Ca2+ channels and Munc13-1, an essential vesicle priming protein and putative marker of primed vesicles [14,40–45].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [45]
Munc13-1/2 are putative markers of primed vesicles.
“and Munc13-1/2, putative markers of primed vesicles [14,42–45,60,61].”
From Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons (2024) · cites this paper as [45]

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Authors: Sakamoto, H., Ariyoshi, T., Kimpara, N., Sugao, K., Taiko, I., Takikawa, K., Asanuma, D., Namiki, S., & Hirose, K.
Affiliations: The University of Tokyo (JP)
Corresponding author: Hirose, Kenzo
ORCID: Sakamoto, Hirokazu
Takikawa, Kenji
Asanuma, Daisuke
Namiki, Shigeyuki
Hirose, Kenzo
Venue: Nature Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2017-12-11
Volume: 21
Issue: 1
Pages: 41-49
ISSN: 1097-6256 (ISSN-L)
1546-1726
DOI: 10.1038/s41593-017-0041-9
OpenAlex: W2772190072
Cited by: 235
References: 61
Citations by year: 2026: 21 · 2025: 27 · 2024: 33 · 2023: 26 · 2022: 34 · 2021: 32 · 2020: 31 · 2019: 18 · 2018: 11 · 2017: 2
FWCI: 8.30
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (unspecified)
Locations: Nature Neuroscience (publishedVersion)
PubMed (publishedVersion)
Funders: Japan Society for the Promotion of Science (17K08584, 17H04029)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
Keywords: synaptic weights, Munc13-1, supramolecular self-assembly, presynaptic terminals, glutamate release, syntaxin-1, SNARE proteins, synaptic vesicle exocytosis, glutamatergic synapses, super-resolution imaging
MeSH terms: Animals, Calcium, Cells, Cultured, Cytoskeletal Proteins, Embryo, Mammalian, Exocytosis, Hippocampus, Nerve Tissue Proteins, Synaptic Transmission, Neurons, Neuropeptides, Synapses, Synaptic Vesicles, Rats, Sprague-Dawley, Presynaptic Terminals, Glutamic Acid, GTP-Binding Proteins, RNA, Small Interfering, Adaptor Proteins, Signal Transducing, Vesicular Glutamate Transport Protein 1, Syntaxin 1, Rats

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Synaptic weight set by Munc13-1 supramolecular assemblies

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