Cited by 348Cellular transport and secretionNeuroscience and Neuropharmacology ResearchExtracellular vesicles in disease

The DOI matches its Crossref record; 92 of the 95 references it cites were found in a registry or an index; 43 of the 77 sources its claims cite were checked for support.

Architecture of the synaptotagmin–SNARE machinery for neuronal exocytosis

Open access

Abstract

Synaptotagmin-1 and neuronal SNARE proteins have central roles in evoked synchronous neurotransmitter release; however, it is unknown how they cooperate to trigger synaptic vesicle fusion. Here we report atomic-resolution crystal structures of Ca2+- and Mg2+-bound complexes between synaptotagmin-1 and the neuronal SNARE complex, one of which was determined with diffraction data from an X-ray free-electron laser, leading to an atomic-resolution structure with accurate rotamer assignments for many side chains. The structures reveal several interfaces, including a large, specific, Ca2+-independent and conserved interface. Tests of this interface by mutagenesis suggest that it is essential for Ca2+-triggered neurotransmitter release in mouse hippocampal neuronal synapses and for Ca2+-triggered vesicle fusion in a reconstituted system. We propose that this interface forms before Ca2+ triggering, moves en bloc as Ca2+ influx promotes the interactions between synaptotagmin-1 and the plasma membrane, and consequently remodels the membrane to promote fusion, possibly in conjunction with other interfaces.

Overview

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Written from the paper’s full text.

TL;DR

The paper reports crystal structures of Ca2+- and Mg2+-bound synaptotagmin-1–neuronal SNARE complexes, including one determined from X-ray free electron laser diffraction data, revealing a large conserved Ca2+-independent primary interface. Mutagenesis and functional assays indicate this interface is required for efficient Syt1–SNARE binding and Ca2+-triggered evoked release/fusion, supporting a model in which the C2B–SNARE unit moves en bloc upon Ca2+ influx to remodel the membrane.

Key findings

  • The structures reveal three Syt1–SNARE interfaces (“primary,” “secondary,” and “tertiary”) plus a C2A–C2B interface; the primary interface is the largest, similar in both crystal forms and in Ca2+- versus Mg2+-bound structures, has relatively low B-factors, and is conserved across synaptotagmins/SNAP-25/syntaxin-1A homologs involved in fast synchronous release.
  • Mutating primary-interface regions reduced Syt1 binding to syntaxin-1A/SNARE complex by ~50% for region I or region II mutants and to ~33% for the Syt1 quintuple mutant; in single-vesicle content-mixing assays, these mutants reduced vesicle association and Ca2+-triggered fusion amplitude/synchronization but did not affect spontaneous fusion, with the Syt1 quintuple reducing Ca2+-triggered synchronization to the no-Syt1 control level.
  • In Syt1 cKO neurons, region I mutants retained some rescue of evoked inhibitory postsynaptic currents, whereas region II mutants were nearly non-functional; triple and quintuple mutants showed more severe phenotypes, and E295A/Y338W rescued spontaneous-release unclamping while region II mutants did not.
  • XFEL data collection used 148 crystals; 113 produced 578 processable images, and the final long-unit-cell dataset used 309 images from 72 crystals. At LCLS, 61 of ~72 long-unit-cell crystals diffracted to at least 3.5 Å, versus 1 of 85 screened long-unit-cell crystals reaching 4.1 Å at APS; refined structures were at 3.50 Å (Ca2+-bound long unit cell), 3.60 Å (Ca2+-bound short unit cell), 4.10 Å (Mg2+-bound short unit cell), and 1.65 Å (Syt1 C2B quintuple mutant).

Methods

  • A Syt1 C2AB–linker–SNAP-25_C chimera plus SNAP-25_N, syntaxin-1A, and synaptobrevin-2 fragments was co-expressed in E. coli, purified, and crystallized as Ca2+- and Mg2+-bound Syt1–SNARE complexes; diffraction data were collected at LCLS XFEL and APS synchrotron beamlines, and structures were determined by molecular replacement and refined with Coot/CNS/phenix.refine.
  • Structure-guided mutations were validated by circular dichroism, size-exclusion chromatography, and a crystal structure of the Syt1 C2B quintuple mutant; functional tests included co-immunoprecipitation from Syt1 cKO neurons, single-vesicle content-mixing assays with full-length Syt1/SNAREs/complexin-1, and electrophysiological recordings in cultured hippocampal neurons.
  • Analyses included crystallographic data/refinement statistics, interface and electrostatic-potential analysis, sequence alignments, comparison with prior smFRET histograms, quantitative immunoblotting, and counting of spontaneous versus Ca2+-triggered fusion events.

Limitations

  • Stated: the XFEL diffraction data had poorer conventional merging statistics than rotation data, and it is difficult to assess their relative quality; lack of available XFEL beamtime prevented collecting a complete dataset beyond 3.5 Å. The authors also note that comparison with a prior NMR study was not possible because covalently attached lanthanide labels would likely disrupt the primary interface.
  • Stated: the minimal reconstituted system lacks other factors, which may explain why the R398Q/R399Q mutant had little effect on synchronization there and why spontaneous release behavior differed between neuronal cultures and the reconstituted assay.
  • Evident from the text: the crystal structures use a Syt1 C2AB fragment and truncated SNARE fragments, and the covalent linker was cleaved during crystallization; functional conclusions rely on designed mutants and may not fully capture full-length protein behavior in native membranes, although the paper argues the linker likely did not affect the final structures.

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Integrity signals

Registry

Crossref · 10.1038/nature14975

Cites

92 of 92 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Verification

Claims the paper makes

43 of 77 cited sources checked · 35 supported · 0 flagged · accuracy not yet measured

Show all 62 claims

  • It may state two separate claims as one. 49
  • Probably not a substantial claim. 20
  • The quote only partly states this claim. 1
66 of 66
  • The authors state this as an assumption.

    Prior to Ca2+ influx, there is a membrane juxtaposed, hemifusion-free state, the likely starting state for fast Ca2+ triggered fusion, and a partially folded trans-SNARE complex.

    “Prior to Ca2+ influx, we assume a membrane juxtaposed, hemifusion-free state (Fig. 5c), the likely starting state for fast Ca2+ triggered fusion37, and a partially folded trans-SNARE complex46.”
  • The authors state this as an assumption.

    The Syt1 C2B-SNARE unit can assemble in the pre-Ca2+ state.

    “We assume that the Syt1 C2B-SNARE unit can assemble in this state since the primary interface involves residues within the folded region of the trans-SNARE complex.”
  • The paper relies on this without support.

    The atomic-resolution structure of the complex between Syt1 and the neuronal SNARE complex has been elusive.

    “However, the atomic-resolution structure of the complex between Syt1 and the neuronal SNARE complex (referred to as Syt1-SNARE complex) has been elusive.”
  • The paper relies on this without support.

    The molecular basis and the significance of the interaction between Syt1 and the SNARE complex remain unknown.

    “but the molecular basis and the significance of the interaction between Syt1 and the SNARE complex remain unknown.”
  • The paper relies on this without support.

    It is unknown how Syt1 and neuronal SNARE proteins cooperate to trigger synaptic vesicle fusion.

    “However, it is unknown how they cooperate to trigger synaptic vesicle fusion.”
  • The paper relies on this without support.

    It is unknown at the atomic level of detail how these factors cooperate with SNAREs to promote synaptic transmission.

    “but it is unknown at the atomic level of detail how these factors cooperate with SNAREs to promote synaptic transmission.”
  • The paper relies on this without support.

    Interactions in region I have not been implicated in any previous studies.

    “Moreover, interactions in region I (Fig. 2a) have not been implicated in any previous studies.”
  • The paper relies on this without support.

    The role of the region II interacting residues was unclear in the absence of structural information.

    “However, the role of these residues was unclear in the absence of structural information, which now reveals that they are part of a larger interface between Syt1 and the SNARE complex.”
8 of 8

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Metadata

Authors
Zhou, Q., Lai, Y., Bacaj, T., Zhao, M., Lyubimov, A. Y., Uervirojnangkoorn, M., Zeldin, O. B., Brewster, A. S., Sauter, N. K., Cohen, A. E., Soltis, S. M., Alonso-Mori, R., Chollet, M., Lemke, H. T., Pfuetzner, R. A., Choi, U. B., Weis, W. I., Diao, J., Südhof, T. C., & Brunger, A. T.
Affiliations
  • Howard Hughes Medical Institute (US)
  • Lawrence Berkeley National Laboratory (US)
  • SLAC National Accelerator Laboratory (US)
  • Stanford University (US)
Corresponding author
Südhof, Thomas C.
Venue
Nature
Published
2015-08-17
Volume
525
Issue
7567
Pages
62-67
ISSN
  • 0028-0836 (ISSN-L)
  • 1476-4687
OpenAlex
W2128007435
Cited by
348
References
95
Citations by year
2026: 20 · 2025: 20 · 2024: 48 · 2023: 27 · 2022: 33 · 2021: 23 · 2020: 29 · 2019: 27 · 2018: 37 · 2017: 42 · 2016: 36 · 2015: 6
FWCI
18.64
Type
journal article
Language
en
Open access
Locations
  • Nature (publishedVersion)
  • PubMed (publishedVersion)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • Europe PMC (PubMed Central) (submittedVersion)
  • PubMed Central (submittedVersion)
  • RePEc: Research Papers in Economics (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion)
Funders
  • Howard Hughes Medical Institute
  • U.S. Department of Energy (76SF00515, DE–AC02–76SF00515, P41 GM103403, P41GM103393, AC02‐76SF00515, DE-AC02-)
  • National Institutes of Health (3p41gm103403-15s1, 8p41gm103393-33, DE-AC02-76SF00515, R37 MH63105, P41 GM103403, P41 GM103393, MH086403, GM103403, GM102520, GM095887)
  • Office of Science (AC02-76SF00515, P41GM103393, DE-AC02-76SF0051 5, DE-AC02, 76SF00515)
  • National Institute of Mental Health (R37 MH063105, MH086403, P50 MH086403, R37MH63105)
  • National Institute of General Medical Sciences (R01-GM095887, R01 GM102520, P41-GM-103393, R01 GM077071, GM095887, DE-AC02-76SF00515, P41GM103403, GM102520, GM-103403)
  • Basic Energy Sciences (DE-AC02, P41GM103393, 76SF00515, AC02-76SF00515, GM103403, DE-AC-02-76SF00515)
  • Biological and Environmental Research (P41 GM103393, DE- AC0276SF00515)
  • SLAC National Accelerator Laboratory (DEAC02−76SF00515, AC02‐76SF00515, P41GM103393)
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
synaptotagmin-1, synaptic vesicle fusion, neurotransmitter release, calcium-triggered exocytosis, protein complex crystal structure, hippocampal synapses, membrane remodeling
MeSH terms
Animals, Binding Sites, Calcium, Cell Membrane, Electrons, Exocytosis, Hippocampus, Lasers, Magnesium, Membrane Fusion, Models, Biological, Models, Molecular, Mutation, Synaptic Transmission, Neurons, Synaptic Vesicles, Crystallography, X-Ray, SNARE Proteins, Synaptotagmins, Mice

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