The primed SNARE–complexin–synaptotagmin complex for neuronal exocytosis

Zhou, Qiangjun; Zhou, Peng; Wang, Austin L.; Wu, Dick; Zhao, Minglei; Südhof, Thomas C.; Brunger, Axel T.

doi:10.1038/nature23484

Title: The primed SNARE–complexin–synaptotagmin complex for neuronal exocytosis

Journal Article · Wed Aug 16 00:00:00 EDT 2017 · Nature (London)

DOI:https://doi.org/10.1038/nature23484· OSTI ID:1390868

Zhou, Qiangjun; Zhou, Peng; Wang, Austin L.; Wu, Dick; Zhao, Minglei; Südhof, Thomas C.; Brunger, Axel T.

Synaptotagmin, complexin, and neuronal SNARE (soluble N-ethylmaleimide sensitive factor attachment protein receptor) proteins mediate evoked synchronous neurotransmitter release, but the molecular mechanisms mediating the cooperation between these molecules remain unclear. Here we determine crystal structures of the primed pre-fusion SNARE–complexin–synaptotagmin-1 complex. These structures reveal an unexpected tripartite interface between synaptotagmin-1 and both the SNARE complex and complexin. Simultaneously, a second synaptotagmin-1 molecule interacts with the other side of the SNARE complex via the previously identified primary interface. Mutations that disrupt either interface in solution also severely impair evoked synchronous release in neurons, suggesting that both interfaces are essential for the primed pre-fusion state. Ca2+ binding to the synaptotagmin-1 molecules unlocks the complex, allows full zippering of the SNARE complex, and triggers membrane fusion. The tripartite SNARE–complexin–synaptotagmin-1 complex at a synaptic vesicle docking site has to be unlocked for triggered fusion to start, explaining the cooperation between complexin and synaptotagmin-1 in synchronizing evoked release on the sub-millisecond timescale.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: National Institutes of Health (NIH)

OSTI ID:: 1390868

Journal Information:: Nature (London), Vol. 548, Issue 7668; ISSN 0028-0836

Publisher:: Nature Publishing Group

Country of Publication:: United States

Language:: ENGLISH

References (57)

Synaptotagmin: a calcium sensor on the synaptic vesicle surface Brose, N.; Petrenko, A.; Sudhof, T. Science, Vol. 256, Issue 5059 https://doi.org/10.1126/science.1589771	journal	May 1992
Complexin Clamps Asynchronous Release by Blocking a Secondary Ca2+ Sensor via Its Accessory α Helix Yang, Xiaofei; Kaeser-Woo, Yea Jin; Pang, Zhiping P. Neuron, Vol. 68, Issue 5 https://doi.org/10.1016/j.neuron.2010.11.001	journal	December 2010
A Complexin/Synaptotagmin 1 Switch Controls Fast Synaptic Vesicle Exocytosis Tang, Jiong; Maximov, Anton; Shin, Ok-Ho Cell, Vol. 126, Issue 6 https://doi.org/10.1016/j.cell.2006.08.030	journal	September 2006
Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution Sutton, R. Bryan; Fasshauer, Dirk; Jahn, Reinhard Nature, Vol. 395, Issue 6700 https://doi.org/10.1038/26412	journal	September 1998
Architecture of the synaptotagmin–SNARE machinery for neuronal exocytosis Zhou, Qiangjun; Lai, Ying; Bacaj, Taulant Nature, Vol. 525, Issue 7567 https://doi.org/10.1038/nature14975	journal	August 2015
Complexin Controls Spontaneous and Evoked Neurotransmitter Release by Regulating the Timing and Properties of Synaptotagmin Activity Jorquera, R. A.; Huntwork-Rodriguez, S.; Akbergenova, Y. Journal of Neuroscience, Vol. 32, Issue 50 https://doi.org/10.1523/JNEUROSCI.3212-12.2012	journal	December 2012
Complexin Controls the Force Transfer from SNARE Complexes to Membranes in Fusion Maximov, A.; Tang, J.; Yang, X. Science, Vol. 323, Issue 5913 https://doi.org/10.1126/science.1166505	journal	January 2009
X-ray Structure of a Neuronal Complexin-SNARE Complex from Squid Bracher, Andreas; Kadlec, Jan; Betz, Heinrich Journal of Biological Chemistry, Vol. 277, Issue 29 https://doi.org/10.1074/jbc.M203460200	journal	May 2002
High Resolution Structure, Stability, and Synaptotagmin Binding of a Truncated Neuronal SNARE Complex Ernst, James A.; Brunger, Axel T. Journal of Biological Chemistry, Vol. 278, Issue 10 https://doi.org/10.1074/jbc.M211889200	journal	December 2002
Exploring the gas access routes in a [NiFeSe] hydrogenase using crystals pressurized with krypton and oxygen Zacarias, Sónia; Temporão, Adriana; Carpentier, Philippe JBIC Journal of Biological Inorganic Chemistry, Vol. 25, Issue 6 https://doi.org/10.1007/s00775-020-01814-y	journal	August 2020
PtdInsP2 and PtdSer cooperate to trap synaptotagmin-1 to the plasma membrane in the presence of calcium Pérez-Lara, Ángel; Thapa, Anusa; Nyenhuis, Sarah B. eLife, Vol. 5 https://doi.org/10.7554/eLife.15886	journal	October 2016
Monitoring synaptic transmission in primary neuronal cultures using local extracellular stimulation Maximov, Anton; Pang, Zhiping P.; Tervo, Dougal G. R. Journal of Neuroscience Methods, Vol. 161, Issue 1 https://doi.org/10.1016/j.jneumeth.2006.10.009	journal	March 2007
PHENIX : building new software for automated crystallographic structure determination Adams, Paul D.; Grosse-Kunstleve, Ralf W.; Hung, Li-Wei Acta Crystallographica Section D Biological Crystallography, Vol. 58, Issue 11 https://doi.org/10.1107/S0907444902016657	journal	October 2002
Complexins: small but capable Mohrmann, Ralf; Dhara, Madhurima; Bruns, Dieter Cellular and Molecular Life Sciences, Vol. 72, Issue 22 https://doi.org/10.1007/s00018-015-1998-8	journal	August 2015
Processive ATP-driven Substrate Disassembly by the N -Ethylmaleimide-sensitive Factor (NSF) Molecular Machine Cipriano, Daniel J.; Jung, Jaemyeong; Vivona, Sandro Journal of Biological Chemistry, Vol. 288, Issue 32 https://doi.org/10.1074/jbc.M113.476705	journal	June 2013
Syntaxin-1 N-peptide and Habc-domain perform distinct essential functions in synaptic vesicle fusion Zhou, Peng; Pang, Zhiping P.; Yang, Xiaofei The EMBO Journal, Vol. 32, Issue 1 https://doi.org/10.1038/emboj.2012.307	journal	November 2012
Synaptotagmin I functions as a calcium regulator of release probability Fernández-Chacón, Rafael; Königstorfer, Andreas; Gerber, Stefan H. Nature, Vol. 410, Issue 6824 https://doi.org/10.1038/35065004	journal	March 2001
Single-molecule FRET–derived model of the synaptotagmin 1–SNARE fusion complex Choi, Ucheor B.; Strop, Pavel; Vrljic, Marija Nature Structural & Molecular Biology, Vol. 17, Issue 3 https://doi.org/10.1038/nsmb.1763	journal	February 2010
Cell biology of Ca2+-triggered exocytosis Pang, Zhiping P.; Südhof, Thomas C. Current Opinion in Cell Biology, Vol. 22, Issue 4 https://doi.org/10.1016/j.ceb.2010.05.001	journal	August 2010
Morphologies of synaptic protein membrane fusion interfaces Gipson, Preeti; Fukuda, Yoshiyuki; Danev, Radostin Proceedings of the National Academy of Sciences, Vol. 114, Issue 34 https://doi.org/10.1073/pnas.1708492114	journal	July 2017
Complexin synchronizes primed vesicle exocytosis and regulates fusion pore dynamics Dhara, Madhurima; Yarzagaray, Antonio; Schwarz, Yvonne The Journal of Cell Biology, Vol. 204, Issue 7 https://doi.org/10.1083/jcb.201311085	journal	March 2014
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
An optimized growth medium for increased recombinant protein secretion titer via the type III secretion system Burdette, Lisa Ann; Wong, Han Teng; Tullman-Ercek, Danielle Microbial Cell Factories, Vol. 20, Issue 1 https://doi.org/10.1186/s12934-021-01536-z	journal	February 2021
Synaptotagmin-1 functions as a Ca2+ sensor for spontaneous release Xu, Jun; Pang, Zhiping P.; Shin, Ok-Ho Nature Neuroscience, Vol. 12, Issue 6 https://doi.org/10.1038/nn.2320	journal	May 2009
The Principle of Membrane Fusion in the Cell (Nobel Lecture) Rothman, James Edward Angewandte Chemie International Edition, Vol. 53, Issue 47 https://doi.org/10.1002/anie.201402380	journal	August 2014
Distinct roles for two synaptotagmin isoforms in synchronous and asynchronous transmitter release at zebrafish neuromuscular junction Wen, H.; Linhoff, M. W.; McGinley, M. J. Proceedings of the National Academy of Sciences, Vol. 107, Issue 31 https://doi.org/10.1073/pnas.1008598107	journal	July 2010
Complexin induces a conformational change at the membrane-proximal C-terminal end of the SNARE complex Choi, Ucheor B.; Zhao, Minglei; Zhang, Yunxiang eLife, Vol. 5 https://doi.org/10.7554/eLife.16886	journal	June 2016
Neurotransmitter Release: The Last Millisecond in the Life of a Synaptic Vesicle Südhof, Thomas C. Neuron, Vol. 80, Issue 3 https://doi.org/10.1016/j.neuron.2013.10.022	journal	October 2013
Direct Interaction of a Ca ²⁺ -binding Loop of Synaptotagmin with Lipid Bilayers Chapman, Edwin R.; Davis, Anson F. Journal of Biological Chemistry, Vol. 273, Issue 22 https://doi.org/10.1074/jbc.273.22.13995	journal	May 1998
E-catenin is an autoinhibited molecule that coactivates vinculin Choi, H. -J.; Pokutta, S.; Cadwell, G. W. Proceedings of the National Academy of Sciences, Vol. 109, Issue 22 https://doi.org/10.1073/pnas.1203906109	journal	May 2012
Functional analysis of the interface between the tandem C2 domains of synaptotagmin-1 Evans, Chantell S.; He, Zixuan; Bai, Hua Molecular Biology of the Cell, Vol. 27, Issue 6 https://doi.org/10.1091/mbc.E15-07-0503	journal	March 2016
SNAREpins: Minimal Machinery for Membrane Fusion Weber, Thomas; Zemelman, Boris V.; McNew, James A. Cell, Vol. 92, Issue 6 https://doi.org/10.1016/S0092-8674(00)81404-X	journal	March 1998
Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse Geppert, Martin; Goda, Yukiko; Hammer, Robert E. Cell, Vol. 79, Issue 4 https://doi.org/10.1016/0092-8674(94)90556-8	journal	November 1994
Differential but convergent functions of Ca2+ binding to synaptotagmin-1 C2 domains mediate neurotransmitter release Shin, O. -H.; Xu, J.; Rizo, J. Proceedings of the National Academy of Sciences, Vol. 106, Issue 38 https://doi.org/10.1073/pnas.0908798106	journal	September 2009
N-terminal domain of complexin independently activates calcium-triggered fusion Lai, Ying; Choi, Ucheor B.; Zhang, Yunxiang Proceedings of the National Academy of Sciences, Vol. 113, Issue 32 https://doi.org/10.1073/pnas.1604348113	journal	July 2016
Dynamic binding mode of a Synaptotagmin-1–SNARE complex in solution Brewer, Kyle D.; Bacaj, Taulant; Cavalli, Andrea Nature Structural & Molecular Biology, Vol. 22, Issue 7 https://doi.org/10.1038/nsmb.3035	journal	June 2015
Synaptotagmin-1 and Synaptotagmin-7 Trigger Synchronous and Asynchronous Phases of Neurotransmitter Release Bacaj, Taulant; Wu, Dick; Yang, Xiaofei Neuron, Vol. 80, Issue 4 https://doi.org/10.1016/j.neuron.2013.10.026	journal	November 2013
Complexin cross-links prefusion SNAREs into a zigzag array Kümmel, Daniel; Krishnakumar, Shyam S.; Radoff, Daniel T. Nature Structural & Molecular Biology, Vol. 18, Issue 8 https://doi.org/10.1038/nsmb.2101	journal	July 2011
Synaptotagmin-1 and -7 are functionally overlapping Ca2+ sensors for exocytosis in adrenal chromaffin cells Schonn, J. -S.; Maximov, A.; Lao, Y. Proceedings of the National Academy of Sciences, Vol. 105, Issue 10 https://doi.org/10.1073/pnas.0712373105	journal	February 2008
The Ca ²⁺ Affinity of Synaptotagmin 1 Is Markedly Increased by a Specific Interaction of Its C2B Domain with Phosphatidylinositol 4,5-Bisphosphate Radhakrishnan, Anand; Stein, Alexander; Jahn, Reinhard Journal of Biological Chemistry, Vol. 284, Issue 38 https://doi.org/10.1074/jbc.M109.042499	journal	July 2009
Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C Perin, Mark S.; Fried, Victor A.; Mignery, Gregory A. Nature, Vol. 345, Issue 6272 https://doi.org/10.1038/345260a0	journal	May 1990
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Synaptotagmin Increases the Dynamic Range of Synapses by Driving Ca2+-Evoked Release and by Clamping a Near-Linear Remaining Ca2+ Sensor Kochubey, Olexiy; Schneggenburger, Ralf Neuron, Vol. 69, Issue 4 https://doi.org/10.1016/j.neuron.2011.01.013	journal	February 2011
Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP Wu, Dick; Bacaj, Taulant; Morishita, Wade Nature, Vol. 544, Issue 7650 https://doi.org/10.1038/nature21720	journal	March 2017
Overview of the CCP4 suite and current developments. Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.52322	text	January 2011
The Calcium-Dependent and Calcium-Independent Membrane Binding of Synaptotagmin 1: Two Modes of C2B Binding Kuo, Weiwei; Herrick, Dawn Z.; Ellena, Jeffrey F. Journal of Molecular Biology, Vol. 387, Issue 2 https://doi.org/10.1016/j.jmb.2009.01.064	journal	March 2009
Complexin Activates Exocytosis of Distinct Secretory Vesicles Controlled by Different Synaptotagmins Cao, P.; Yang, X.; Sudhof, T. C. Journal of Neuroscience, Vol. 33, Issue 4 https://doi.org/10.1523/JNEUROSCI.4087-12.2013	journal	January 2013
Post-Translational Modifications and Lipid Binding Profile of Insect Cell-Expressed Full-Length Mammalian Synaptotagmin 1 Vrljic, Marija; Strop, Pavel; Hill, Ryan C. Biochemistry, Vol. 50, Issue 46 https://doi.org/10.1021/bi200998y	journal	November 2011
Calcium-sensing beyond neurotransmitters: functions of synaptotagmins in neuroendocrine and endocrine secretion Gustavsson, Natalia; Han, Weiping Bioscience Reports, Vol. 29, Issue 4 https://doi.org/10.1042/BSR20090031	journal	June 2009
Three-Dimensional Structure of the Complexin/SNARE Complex Chen, Xiaocheng; Tomchick, Diana R.; Kovrigin, Evguenii Neuron, Vol. 33, Issue 3 https://doi.org/10.1016/S0896-6273(02)00583-4	journal	January 2002
Synaptotagmin-1, -2, and -9: Ca2+ Sensors for Fast Release that Specify Distinct Presynaptic Properties in Subsets of Neurons Xu, Jun; Mashimo, Tomoyuki; Südhof, Thomas C. Neuron, Vol. 54, Issue 4 https://doi.org/10.1016/j.neuron.2007.05.004	journal	May 2007
Three-dimensional structure of the complexin/snare complex Tomchick, D. R.; Chen, X.; Kovrigin, E. Acta Crystallographica Section A Foundations of Crystallography, Vol. 58, Issue s1 https://doi.org/10.1107/s0108767302094813	journal	August 2002
Three-Dimensional Structure of the Synaptotagmin 1 C2B-Domain Fernandez, Imma; Araç, Demet; Ubach, Josep Neuron, Vol. 32, Issue 6 https://doi.org/10.1016/S0896-6273(01)00548-7	journal	December 2001
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Genetic Analysis of Synaptotagmin C2 Domain Specificity in Regulating Spontaneous and Evoked Neurotransmitter Release Lee, J.; Guan, Z.; Akbergenova, Y. Journal of Neuroscience, Vol. 33, Issue 1 https://doi.org/10.1523/JNEUROSCI.3214-12.2013	journal	January 2013
Structural and functional conservation of synaptotagmin (p65) in Drosophila and humans. Perin, M. S.; Johnston, P. A.; Ozcelik, T. Journal of Biological Chemistry, Vol. 266, Issue 1 https://doi.org/10.1016/S0021-9258(18)52479-0	journal	January 1991
A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. Davletov, B. A.; Südhof, T. C. Journal of Biological Chemistry, Vol. 268, Issue 35 https://doi.org/10.1016/S0021-9258(19)74326-9	journal	December 1993

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