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Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution
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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“Indeed modeling the four SNARE proteins (Ufe1, Use1, Sec20, and Sec22) that are known to mediate the fusion between Golgi-derived retrograde transport vesicles with ER (87), together resulted in a complex that resembles a typical SNARE complex (84) (fig. S26B, C).”
From Computed structures of core eukaryotic protein complexes (2021) · cites this paper as [84]
In the citing paper
“Membrane fusion requires the formation of a 4-helix bundle (called the SNARE complex) between the vesicle SNARE and the target membrane SNAREs (84,85).”
From Computed structures of core eukaryotic protein complexes (2021) · cites this paper as [84]
Citations
Cites
[20] Processing of X-ray diffraction data collected in oscillation mode
Otwinowski, Z., & Minor, W. (1997) · Methods in Enzymology · doi:10.1016/s0076-6879(97)76066-x · Cited by 33,475
Crystallography & NMR System: A New Software Suite for Macromolecular Structure Determination
Brünger, A. T., Adams, P. D., Clore, G. M., DeLano, W. L., Gros, P., Grosse‐Kunstleve, R. W., Jiang, J., Kuszewski, J. J., Nilges, M., Pannu, N., et al. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998003254 · Cited by 15,723
Jones, T. A., Zou, J.-Y., Cowan, S. W., & Kjeldgaard, M. (1991) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767390010224 · Cited by 12,616
Nicholls, A. O., Sharp, K. A., & Honig, B. H. (1991) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340110407 · Cited by 5,230
Jorgensen, W. L., & Tirado‐Rives, J. (1988) · Journal of the American Chemical Society · doi:10.1021/ja00214a001 · Cited by 5,060
Predicting coiled coils from protein sequences.
Lupas, A., Van Dyke, M., & Stock, J. (1991) · Science · doi:10.1126/science.252.5009.1162 · Cited by 3,953
Free R value: a novel statistical quantity for assessing the accuracy of crystal structures
Brünger, A. T. (1992) · Nature · doi:10.1038/355472a0 · Cited by 3,877
Structure of the haemagglutinin membrane glycoprotein of influenza virus at 3 Å resolution
Wilson, I. A., Skehel, J. J., & Wiley, D. C. (1981) · Nature · doi:10.1038/289366a0 · Cited by 2,537
Core Structure of gp41 from the HIV Envelope Glycoprotein
Chan, D. C., Fass, D., Berger, J. M., & Kim, P. S. (1997) · Cell · doi:10.1016/s0092-8674(00)80205-6 · Cited by 2,000
The synaptic vesicle cycle: a cascade of protein–protein interactions
Südhof, T. C. (1995) · Nature · doi:10.1038/375645a0 · Cited by 1,991
Söllner, T. H., Bennett, M., Whiteheart, S., Scheller, R., & Rothman, J. (1993) · Cell · doi:10.1016/0092-8674(93)90376-2 · Cited by 1,922
Improved Fourier coefficients for maps using phases from partial structures with errors
Read, R. J. (1986) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767386099622 · Cited by 1,870
An extensively modified version of MolScript that includes greatly enhanced coloring capabilities
Esnouf, R. M. (1997) · Journal of Molecular Graphics and Modelling · doi:10.1016/s1093-3263(97)00021-1 · Cited by 1,703
Experimentally determined hydrophobicity scale for proteins at membrane interfaces
Wimley, W. C., & White, S. H. (1996) · Nature Structural & Molecular Biology · doi:10.1038/nsb1096-842 · Cited by 1,691
Atomic structure of the ectodomain from HIV-1 gp41
Weissenhorn, W., Dessen, A., Harrison, S. C., Skehel, J. J., & Wiley, D. C. (1997) · Nature · doi:10.1038/387426a0 · Cited by 1,625
The packing of α-helices: simple coiled-coils
Crick, F. H. C. (1953) · Acta Crystallographica · doi:10.1107/s0365110x53001964 · Cited by 1,578
A Switch Between Two-, Three-, and Four-stranded Coiled Coils in GCN4 Leucine Zipper Mutants
Harbury, P. B., Zhang, T., Kim, P. S., & Alber, T. (1993) · Science · doi:10.1126/science.8248779 · Cited by 1,490 · cited 1×
“2a ) superficially resembles the tetrameric GCN4 four-helix-bundle structur”
BackgroundChan, D. C., & Kim, P. S. (1998) · Cell · doi:10.1016/s0092-8674(00)81430-0 · Cited by 1,296
Determination of Macromolecular Structures from Anomalous Diffraction of Synchrotron Radiation
Hendrickson, W. A. (1991) · Science · doi:10.1126/science.1925561 · Cited by 1,131
Resolution of phase ambiguity in macromolecular crystallography
Wang, B. (1985) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(85)15009-3 · Cited by 1,030
Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E. L. F., Billingsley, M. L., Bloom, F. E., & Wilson, M. C. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.3039 · Cited by 809
Synaptic vesicle membrane fusion complex: action of clostridial neurotoxins on assembly.
Hayashi, T., McMahon, H. T., Yamasaki, S., Binz, T., Hata, Y., Südhof, T. C., & Niemann, H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06834.x · Cited by 798
Hanson, P. I., Roth, R. A., Morisaki, H., Jahn, R., & Heuser, J. E. (1997) · Cell · doi:10.1016/s0092-8674(00)80512-7 · Cited by 797
Self-citationMultiCoil: A program for predicting two‐and three‐stranded coiled coils
Wolf, E., Kim, P. S., & Berger, B. (1997) · Protein Science · doi:10.1002/pro.5560060606 · Cited by 720
Stereochemically restrained refinement of macromolecular structures
Hendrickson, W. A. (1985) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(85)15021-4 · Cited by 606
Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport.
Block, M. R., Glick, B. S., Wilcox, C. A., Wieland, F., & Rothman, J. E. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.21.7852 · Cited by 523
Homotypic vacuolar fusion mediated by t- and v-SNAREs
Nichols, B. J., Ungermann, C., Pelham, H. R. B., Wickner, W. T., & Haas, A. (1997) · Nature · doi:10.1038/387199a0 · Cited by 455
Three‐dimensional solution structure of the 44 kDa ectodomain of SIV gp41
Caffrey, M. S., Cai, M., Kaufman, J. D., Stahl, S. J., Wingfield, P. T., Covell, D. G., Gronenborn, A. M., & Clore, G. M. (1998) · The EMBO Journal · doi:10.1093/emboj/17.16.4572 · Cited by 410
Neurotransmitter release — four years of SNARE complexes
Hanson, P. I., Heuser, J. E., & Jahn, R. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80057-8 · Cited by 394
Self-citationFasshauer, D., Otto, H., Eliason, W. K., Jahn, R., & Brünger, A. T. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.44.28036 · Cited by 378
Self-citationRice, L. M., & Brünger, A. T. (1994) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340190403 · Cited by 369
Fasshauer, D., Eliason, W. K., Brünger, A. T., & Jahn, R. (1998) · Biochemistry · doi:10.1021/bi980542h · Cited by 270
Self-citationOtto, H., Hanson, P. I., & Jahn, R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.12.6197 · Cited by 269
Self-citationDisassembly of the reconstituted synaptic vesicle membrane fusion complex in vitro.
Hayashi, T., Yamasaki, S., Nauenburg, S., Binz, T., & Niemann, H. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb07226.x · Cited by 262
Burling, F. T., Weis, W. I., Flaherty, K. M., & Brünger, A. T. (1996) · Science · doi:10.1126/science.271.5245.72 · Cited by 241
Saifee, O., Wei, L., & Nonet, M. L. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.6.1235 · Cited by 221
A Structural Change Occurs upon Binding of Syntaxin to SNAP-25
Fasshauer, D., Bruns, D., Shen, B. W., Jahn, R., & Brünger, A. T. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.7.4582 · Cited by 218
Self-citationThe N-Ethylmaleimide-sensitive Fusion Protein and α-SNAP Induce a Conformational Change in Syntaxin
Hanson, P. I., Otto, H., Barton, N. R., & Jahn, R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.28.16955 · Cited by 209
Self-citationKee, Y., Lin, R. C.-S., Hsu, S.-C., & Scheller, R. H. (1995) · Neuron · doi:10.1016/0896-6273(95)90337-2 · Cited by 199
Incorporation of Prior Phase Information Strengthens Maximum-Likelihood Structure Refinement
Pannu, N. S., Murshudov, G. N., Dodson, E. J., & Read, R. J. (1998) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444998004119 · Cited by 194
Malashkevich, V. N., Chan, D. C., Chutkowski, C. T., et al. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.16.9134 · Cited by 188
Zhang, K. Y. J., & Main, P. (1990) · Acta Crystallographica Section A Foundations of Crystallography · doi:10.1107/s0108767389009311 · Cited by 171
A model for structural similarity between different SNARE complexes based on sequence relationships
Weimbs, T., Mostov, K. E., Low, S. H., & Hofmann, K. (1998) · Trends in Cell Biology · doi:10.1016/s0962-8924(98)01285-9 · Cited by 153
[23] Bayesian statistical viewpoint on structure determination: Basic concepts and examples
Bricogne, G. (1997) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(97)76069-5 · Cited by 114
[7] Model phases: Probabilities and bias
Read, R. J. (1997) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(97)77009-5 · Cited by 90
Leahy, D. J., Erickson, H., Aukhil, I., et al. (1994) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340190107 · Cited by 89
Molecular Mechanisms of Clostridial Neurotoxins
Jahn, R., & Niemann, H. (1994) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1994.tb17274.x · Cited by 89
Self-citationFormation of a yeast SNARE complex is accompanied by significant structural changes
Rice, L. M., Brennwald, P., & Brünger, A. T. (1997) · FEBS Letters · doi:10.1016/s0014-5793(97)01091-0 · Cited by 73
The use of anomalous scattering effects to phase diffraction patterns from macromolecules
Phillips, J. C., & Hodgson, K. O. (1980) · Acta Crystallographica Section A · doi:10.1107/s0567739480001817 · Cited by 72
Hao, J. C., Salem, N., Peng, X., Kelly, R. B., & Bennett, M. K. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-05-01596.1997 · Cited by 58
Fermentation and Growth ofEscherichia colifor Optimal Protein Production
Bernard, A., & Payton, M. A. (1995) · Current Protocols in Protein Science · doi:10.1002/0471140864.ps0503s00 · Cited by 25
Research works printed but not linked: 1
- Bernard, A. & Payton, M. Fermentation and growth of Escherichia coli for optimal protein production. Curr. Protocol. Protein Sci. 5.3, 1–18 (1995).
Cited by
Sorted by citations
Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm
Wright, P. E., & Dyson, H. J. (1999) · Journal of Molecular Biology · doi:10.1006/jmbi.1999.3110 · Cited by 2,968
“An X-ray structure has been determined for the core synaptic SNARE complex formed by syntaxin-1A, synaptobrevin-II, and SNAP-25B; the ternary complex consists of a twisted four-helix bundle 120 AÊ in length (Sutton et al., 1998).”
BackgroundReceptor Binding and Membrane Fusion in Virus Entry: The Influenza Hemagglutinin
Skehel, J. J., & Wiley, D. C. (2000) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.69.1.531 · Cited by 2,706
SNAREs — engines for membrane fusion
Jahn, R., & Scheller, R. H. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2002 · Cited by 2,635
Self-citationMembrane Fusion: Grappling with SNARE and SM Proteins
Südhof, T. C., & Rothman, J. E. (2009) · Science · doi:10.1126/science.1161748 · Cited by 2,027
The Mechanisms of Vesicle Budding and Fusion
Bonifacino, J. S., & Glick, B. S. (2004) · Cell · doi:10.1016/s0092-8674(03)01079-1 · Cited by 1,908
Metadata
- Authors
- Sutton, R. B., Fasshauer, D., Jahn, R., & Brunger, A. T.
- Affiliations
- Howard Hughes Medical Institute (US)
- Max Planck Society (DE)
- Venue
- Nature
- Published
- 1998-09
- Volume
- 395
- Issue
- 6700
- Pages
- 347-353
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- 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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