Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses

Eggermann, Emmanuel; Bucurenciu, Iancu; Goswami, Sarit Pati; Jonas, Peter

doi:10.1038/nrn3125

Cited by 500Neuroscience and Neuropharmacology ResearchCellular transport and secretionIon channel regulation and function

Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses

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Eggermann, Emmanuel, Bucurenciu, Iancu, Goswami, Sarit Pati, Jonas, Peter·2012·Nature Reviews Neuroscience

DOI 10.1038/nrn3125PMC PMC3617475

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Abstract

The physical distance between presynaptic Ca(2+) channels and the Ca(2+) sensors that trigger exocytosis of neurotransmitter-containing vesicles is a key determinant of the signalling properties of synapses in the nervous system. Recent functional analysis indicates that in some fast central synapses, transmitter release is triggered by a small number of Ca(2+) channels that are coupled to Ca(2+) sensors at the nanometre scale. Molecular analysis suggests that this tight coupling is generated by protein-protein interactions involving Ca(2+) channels, Ca(2+) sensors and various other synaptic proteins. Nanodomain coupling has several functional advantages, as it increases the efficacy, speed and energy efficiency of synaptic transmission.

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The increase in Pr after chemical potentiation might be related to a tightening of the coupling configuration.
“These results suggest that the increase in Pr after induction of chemical potentiation might be related to a tightening of the coupling configuration [8].”
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 [8]
In “Specification and regulation of coupling” (page unavailable), the review suggests that channel–sensor coupling may change during presynaptic potentiation. It does not say that potentiation tightens the coupling, or address the cited sentence’s specific chemical-potentiation condition; the reported increase in Pr is the citing authors’ own result. (LLM, conf=0.83)
Experimental — accuracy not yet measured
Biophysical measurements report the coupling distance between Ca2+ channels and release sensors, but the physical correlate of this measure remains undefined.
“Furthermore, biophysical measurements report the coupling distance between Ca2+ channels and release sensors [7,8] but the physical correlate of this measure remains undefined.”
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 [8]
The “Tight coupling at fast central synapses” section describes chelator experiments and modelling used to estimate channel–sensor coupling distance. The paper does not say that the physical correlate of that measurement remains undefined; its “From nanodomains to protein complexes” section instead discusses protein–protein interactions as a possible basis for tight coupling. No page numbers are available in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measured
Ca2+ entry through P/Q-type voltage-gated Ca2+ channels is tightly coupled to the exocytotic release machinery via formation of specialized nanodomains.
“Ca2+ entry through P/Q channels is tightly coupled to the exocytotic release machinery via formation of specialized “nanodomains” (296).”
From Hippocampal GABAergic Inhibitory Interneurons (2017) · cites this paper as [296]

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[68]Collin T Developmental changes in parvalbumin regulate presynaptic Ca2+ signaling J. Neurosci 2005 25 96 107 15634771 PMC6725212
[73]Lee A Zhou H Scheuer T Catterall WA Molecular determinants of Ca2+/calmodulin-dependent regulation of Ca2.1 channels Proc. Natl Acad. Sci. USA 2003 100 16059 16064 14673106 PMC307692
[100]Kittel RJ Bruchpilot promotes active zone assembly, Ca2+ channel clustering, and vesicle release Science 2006 312 1051 1054 16614170

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Authors: Eggermann, E., Bucurenciu, I., Goswami, S. P., & Jonas, P.
Affiliations: Institute of Science and Technology Austria (AT)
ORCID: Bucurenciu, Iancu
Venue: Nature Reviews Neuroscience
Publisher: Springer Science and Business Media LLC
Published: 2011-12-20
Volume: 13
Issue: 1
Pages: 7-21
ISSN: 1471-003X (ISSN-L)
1471-0048
DOI: 10.1038/nrn3125
PMC: PMC3617475
OpenAlex: W2091694654
Cited by: 500
References: 143
Citations by year: 2026: 16 · 2025: 25 · 2024: 50 · 2023: 32 · 2022: 36 · 2021: 22 · 2020: 37 · 2019: 40 · 2018: 40 · 2017: 33 · 2016: 30 · 2015: 48 · 2014: 35 · 2013: 33 · 2012: 23
FWCI: 2.70
Type: journal article
Language: en
Open access: green
europepmc.org
Licence: www.springer.com/tdm (tdm)
Locations: Nature reviews. Neuroscience (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Institute of Science and Technology Austria (submittedVersion, other-oa)
Funders: Deutsche Forschungsgemeinschaft
Leibniz-Gemeinschaft
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 › Ion channel regulation and function
Keywords: presynaptic calcium channels, calcium sensor, exocytosis, neurotransmitter release, synaptic transmission, protein-protein interaction, synaptic proteins, calcium influx
MeSH terms: Animals, Calcium, Chelating Agents, Exocytosis, Mammals, Models, Biological, Synaptic Transmission, Synapses, Calcium Channels, Signal Transduction

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Nanodomain coupling between Ca2+ channels and sensors of exocytosis at fast mammalian synapses

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