The Morphological and Molecular Nature of Synaptic Vesicle Priming at Presynaptic Active Zones
Open accessAbstract
Synaptic vesicle docking, priming, and fusion at active zones are orchestrated by a complex molecular machinery. We employed hippocampal organotypic slice cultures from mice lacking key presynaptic proteins, cryofixation, and three-dimensional electron tomography to study the mechanism of synaptic vesicle docking in the same experimental setting, with high precision, and in a near-native state. We dissected previously indistinguishable, sequential steps in synaptic vesicle active zone recruitment (tethering) and membrane attachment (docking) and found that vesicle docking requires Munc13/CAPS family priming proteins and all three neuronal SNAREs, but not Synaptotagmin-1 or Complexins. Our data indicate that membrane-attached vesicles comprise the readily releasable pool of fusion-competent vesicles and that synaptic vesicle docking, priming, and trans-SNARE complex assembly are the respective morphological, functional, and molecular manifestations of the same process, which operates downstream of vesicle tethering by active zone components.
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The readily releasable pool often closely correlates with the pool of docked vesicles, but exceptions to this correlation have been observed.
“For example, the readily releasable pool (RRP) often closely correlates with the pool of docked vesicles (i.e., vesicles in the direct contact with AZ plasma membrane) [14] but exceptions to this correlation have been also observed [15–17].”
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 [14]
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 [14]
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 [14]
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Self-citationFunctions of Rab Proteins at Presynaptic Sites
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RIM C2B Domains Target Presynaptic Active Zone Functions to PIP2-Containing Membranes
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Munc13- and SNAP25-dependent molecular bridges play a key role in synaptic vesicle priming
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Self-citation
- Authors
- Imig, C., Min, S.-W., Krinner, S., Arancillo, M., Rosenmund, C., Südhof, T. C., Rhee, J., Brose, N., & Cooper, B. H.
- Affiliations
- Max Planck Institute of Experimental Medicine (DE)
- NeuroCure Cluster of Excellence (DE)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Brose, Nils
- Cooper, Benjamin H.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2014-10
- Volume
- 84
- Issue
- 2
- Pages
- 416-431
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W1996414800
- Cited by
- 389
- References
- 104
- Citations by year
- 2026: 18 · 2025: 24 · 2024: 33 · 2023: 28 · 2022: 42 · 2021: 44 · 2020: 35 · 2019: 39 · 2018: 32 · 2017: 40 · 2016: 27 · 2015: 26 · 2014: 1
- FWCI
- 15.60
- Type
- journal article
- Language
- en
- Update notices
- erratum (2014-11-19)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- GRO (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- 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 priming, synaptic vesicle docking, active zone, Munc13, synaptotagmin-1, complexin, vesicle tethering, membrane adhesion, readily releasable pool, hippocampal synapses
- MeSH terms
- Animals, Hippocampus, Membrane Fusion, Synaptic Transmission, Neurons, Synapses, Synaptic Vesicles, SNARE Proteins, Mice
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