Cited by 2,417Cellular transport and secretionLipid Membrane Structure and BehaviorNeuroscience and Neuropharmacology Research

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Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution

Sutton, R. Bryan, Fasshauer, Dirk, Jahn, Reinhard, Brunger, Axel T.·1998·Nature

DOI 10.1038/26412

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Abstract

The evolutionarily conserved SNARE proteins and their complexes are involved in the fusion of vesicles with their target membranes; however, the overall organization and structural details of these complexes are unknown. Here we report the X-ray crystal structure at 2.4 A resolution of a core synaptic fusion complex containing syntaxin-1 A, synaptobrevin-II and SNAP-25B. The structure reveals a highly twisted and parallel four-helix bundle that differs from the bundles described for the haemagglutinin and HIV/SIV gp41 membrane-fusion proteins. Conserved leucine-zipper-like layers are found at the centre of the synaptic fusion complex. Embedded within these leucine-zipper layers is an ionic layer consisting of an arginine and three glutamine residues contributed from each of the four alpha-helices. These residues are highly conserved across the entire SNARE family. The regions flanking the leucine-zipper-like layers contain a hydrophobic core similar to that of more general four-helix-bundle proteins. The surface of the synaptic fusion complex is highly grooved and possesses distinct hydrophilic, hydrophobic and charged regions. These characteristics may be important for membrane fusion and for the binding of regulatory factors affecting neurotransmission.

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Background
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Background
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Background
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Background
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Background
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Background
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Background
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“Synaptobrevin and syntaxin contribute one helix and SNAP-25 two helices to a parallel four-helix bundle ( Sutton et al., 1998 ).”
Background
α-Synuclein Can Inhibit SNARE-Mediated Vesicle Fusion through Direct Interactions with Lipid Bilayers
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Munc18-1 prevents the formation of ectopic SNARE complexes in living cells
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“Membrane fusion requires the assembly of all three proteins into a trimeric, four-helical complex to promote fusion of the two opposing bilayers in living cells (Sutton et al., 1998; Burgoyne and Morgan, 2003; Sudhof, 1995).”
Background
Apical targeting of syntaxin 3 is essential for epithelial cell polarity
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“Structural domains of syntaxin 3 were identifi ed by sequence alignment with the highly homologous syntaxin 1 whose structure has been previously reported (Fernandez et al., 1998; Sutton et al., 1998; Lerman et al., 2000; Misura et al., 2000).”
Background
ArabidopsisSec1/Munc18 Protein SEC11 Is a Competitive and Dynamic Modulator of SNARE Binding and SYP121-Dependent Vesicle Traffic
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Syntaphilin
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“JCB • Volume 210 • NumBer 1 • 2015 136 four-helical bundle that catalyzes membrane fusion (Sutton et al., 1998).”
BackgroundInfluential
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Role of the synaptobrevin C terminus in fusion pore formation
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SYNCRIP, a Cytoplasmic Counterpart of Heterogeneous Nuclear Ribonucleoprotein R, Interacts with Ubiquitous Synaptotagmin Isoforms
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“This is in contrast to SNAREs tethering complexes, which are formed by parallel coiled-coil interactions, oriented parallel to the membrane surface and allowing closer membrane contacts (Sutton et al., 1998).”
Result
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“…to the unprimed state, when the secretory apparatus is in the primed state (Figure 4e), the a helices of these three proteins are arranged as four intertwined tails, with SNAP-25 contributing two helices, the other two SNAREs contributing one helix each (see inset from Sutton et al., 1998).”
Background
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Self-citation
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“The Q-SNARE motif of Syntaxin and SNAP-25 family proteins contains conserved layers of interacting amino acid side chains.”
BackgroundInfluential
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Exocytosis requires asymmetry in the central layer of the SNARE complex
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Self-citation
A single amino acid near the C terminus of the synaptosomeassociated protein of 25 kDa (SNAP-25) is essential for exocytosis in chromaffin cells
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The Identification of a Novel Endoplasmic Reticulum to Golgi SNARE Complex Used by the Prechylomicron Transport Vesicle
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“The priming of vesicular release is regulated by a multi-protein complex sequentially recruiting Ca2+ sensors, SNARE proteins and the docking machinery embedded in the presynaptic terminal (Hata et al, 1993; Sollner et al, 1993; Sutton et al, 1998; Pang & Sudhof, 2010).”
Background
The SNAP-25 Protein Family
Kádková, A., Radecke, J., & Sørensen, J. B. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.09.020 · Cited by 97
Rab22a affects the morphology and function of the endocytic pathway
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Comparative studies of Munc18c and Munc18-1 reveal conserved and divergent mechanisms of Sec1/Munc18 proteins
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“…available, but based on structural studies of the neuronal plasma membrane SNARE complex (Hanson et al., 1997; Lin and Scheller, 1997; Poirier et al., 1998; Sutton et al., 1998), it is likely to consist of a parallel four -helix bundle with all the SNARE transmembrane domains situated at one end.”
Background
MARCH-II Is a Syntaxin-6–binding Protein Involved in Endosomal Trafficking
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“Only cognate pairs of SNAREs on transport vesicles (v-SNARE) and on target membranes (t-SNARE) form the SNARE complex through their conserved amphipathic helices (SNARE motifs) and draw two membranes into apposition, allowing membrane fusion to occur (Fasshauer et al., 1998; Sutton et al., 1998).”
Background

Authors: Sutton, R. B., Fasshauer, D., Jahn, R., & Brunger, A. T.
Affiliations: Howard Hughes Medical Institute (US)
Max Planck Society (DE)
ORCID: Sutton, R. Bryan
Fasshauer, Dirk
Jahn, Reinhard
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 1998-09
Volume: 395
Issue: 6700
Pages: 347-353
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/26412
OpenAlex: W1822252127
Semantic Scholar: f0ea2581b47bed29546d2d208a47cff4312eb1fe
Cited by: 2,417
References: 52
Citations by year: 2026: 25 · 2025: 44 · 2024: 45 · 2023: 55 · 2022: 63 · 2021: 60 · 2020: 59 · 2019: 51 · 2018: 80 · 2017: 70 · 2016: 67 · 2015: 91 · 2014: 93 · 2013: 89 · 2012: 93
FWCI: 44.62
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords: SNARE complex, synaptic vesicle exocytosis, syntaxin 1A, membrane fusion, four-helix bundle, hydrophobic core, neurotransmitter release, vesicle fusion
MeSH terms: Antigens, Surface, Escherichia coli, Exocytosis, Membrane Fusion, Membrane Proteins, Models, Molecular, Nerve Tissue Proteins, Neurotoxins, Protein Binding, Protein Conformation, Recombinant Proteins, Synaptic Vesicles, Crystallography, X-Ray, Vesicular Transport Proteins, Macromolecular Substances, SNARE Proteins, R-SNARE Proteins, Synaptosomal-Associated Protein 25, Syntaxin 1

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Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution

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