Single-molecule studies of the neuronal SNARE fusion machinery.

SNAREs are essential components of the machinery for Ca(2+)-triggered fusion of synaptic vesicles with the plasma membrane, resulting in neurotransmitter release into the synaptic cleft. Although much is known about their biophysical and structural properties and their interactions with accessory proteins such as the Ca(2+) sensor synaptotagmin, their precise role in membrane fusion remains an enigma. Ensemble studies of liposomes with reconstituted SNAREs have demonstrated that SNAREs and accessory proteins can trigger lipid mixing/fusion, but the inability to study individual fusion events has precluded molecular insights into the fusion process. Thus, this field is ripe for studies with single-molecule methodology. In this review, we discuss applications of single-molecule approaches to observe reconstituted SNAREs, their complexes, associated proteins, and their effect on biological membranes. Some of the findings are provocative, such as the possibility of parallel and antiparallel SNARE complexes or of vesicle docking with only syntaxin and synaptobrevin, but have been confirmed by other experiments.

[1]  T. Reese,et al.  Structure of the Synapse , 2011 .

[2]  Daniel G Nocera,et al.  Proton-coupled electron transfer in biology: results from synergistic studies in natural and model systems. , 2009, Annual review of biochemistry.

[3]  D. Finley,et al.  Recognition and processing of ubiquitin-protein conjugates by the proteasome. , 2009, Annual review of biochemistry.

[4]  Thomas Walz,et al.  The advent of near-atomic resolution in single-particle electron microscopy. , 2009, Annual review of biochemistry.

[5]  A. Becker,et al.  Differential mRNA expression patterns of the synaptotagmin gene family in the rodent brain , 2009, The Journal of comparative neurology.

[6]  J. Rothman,et al.  Alternative Zippering as an On-Off Switch for SNARE-Mediated Fusion , 2009, Science.

[7]  T. Südhof,et al.  Complexin Controls the Force Transfer from SNARE Complexes to Membranes in Fusion , 2009, Science.

[8]  Helmut Grubmüller,et al.  Single-molecule FRET measures bends and kinks in DNA , 2008, Proceedings of the National Academy of Sciences.

[9]  Alexander M. Walter,et al.  The SNAP-25 linker as an adaptation toward fast exocytosis. , 2008, Molecular biology of the cell.

[10]  Christopher M Hickey,et al.  Reconstituted membrane fusion requires regulatory lipids, SNAREs and synergistic SNARE chaperones , 2008, The EMBO journal.

[11]  E. Chapman,et al.  Synaptotagmin arrests the SNARE complex before triggering fast, efficient membrane fusion in response to Ca2+ , 2008, Nature Structural &Molecular Biology.

[12]  Vladimir Parpura,et al.  Comparative energy measurements in single molecule interactions. , 2008, Biophysical journal.

[13]  T. Ha,et al.  Complexin and Ca2+ stimulate SNARE-mediated membrane fusion , 2008, Nature Structural &Molecular Biology.

[14]  Alessandro Borgia,et al.  Single-molecule studies of protein folding. , 2008, Annual review of biochemistry.

[15]  Colin Echeverría Aitken,et al.  Translation at the single-molecule level. , 2008, Annual review of biochemistry.

[16]  W. Greenleaf,et al.  Single-molecule studies of RNA polymerase: motoring along. , 2008, Annual review of biochemistry.

[17]  C. Joo,et al.  Advances in single-molecule fluorescence methods for molecular biology. , 2008, Annual review of biochemistry.

[18]  Rahul Roy,et al.  A practical guide to single-molecule FRET , 2008, Nature Methods.

[19]  R. Jahn,et al.  Synaptic Vesicles Are Constitutively Active Fusion Machines that Function Independently of Ca2+ , 2008, Current Biology.

[20]  Nam Ki Lee,et al.  Single-molecule approach to molecular biology in living bacterial cells. , 2008, Annual review of biophysics.

[21]  I. Dulubova,et al.  NMR analysis of the closed conformation of syntaxin-1 , 2008, Journal of biomolecular NMR.

[22]  Dirk Fasshauer,et al.  Munc18a controls SNARE assembly through its interaction with the syntaxin N‐peptide , 2008, The EMBO journal.

[23]  Tingting Wang,et al.  Productive hemifusion intermediates in fast vesicle fusion driven by neuronal SNAREs. , 2008, Biophysical journal.

[24]  A. Brunger,et al.  Accessory proteins stabilize the acceptor complex for synaptobrevin, the 1:1 syntaxin/SNAP-25 complex. , 2008, Structure.

[25]  J. Rizo,et al.  Binding of the Munc13-1 MUN domain to membrane-anchored SNARE complexes. , 2008, Biochemistry.

[26]  M. Vrljic,et al.  The Structure of the Yeast Plasma Membrane SNARE Complex Reveals Destabilizing Water-filled Cavities* , 2008, Journal of Biological Chemistry.

[27]  Josep Rizo,et al.  Dual Modes of Munc18-1/SNARE Interactions Are Coupled by Functionally Critical Binding to Syntaxin-1 N Terminus , 2007, The Journal of Neuroscience.

[28]  R B Sutton,et al.  Structure of human synaptotagmin 1 C2AB in the absence of Ca2+ reveals a novel domain association. , 2007, Biochemistry.

[29]  J. Rothman,et al.  Energetics and dynamics of SNAREpin folding across lipid bilayers , 2007, Nature Structural &Molecular Biology.

[30]  Peter M. Kasson,et al.  Control of Membrane Fusion Mechanism by Lipid Composition: Predictions from Ensemble Molecular Dynamics , 2007, PLoS Comput. Biol..

[31]  R. Jahn,et al.  Synaptotagmin activates membrane fusion through a Ca2+-dependent trans interaction with phospholipids , 2007, Nature Structural &Molecular Biology.

[32]  George J Augustine,et al.  Kinetics of complexin binding to the SNARE complex: correcting single molecule FRET measurements for hidden events. , 2007, Biophysical journal.

[33]  Nils Brose,et al.  Distinct domains of Complexin I differentially regulate neurotransmitter release , 2007, Nature Structural &Molecular Biology.

[34]  B. Lentz,et al.  Analysis of membrane fusion as a two-state sequential process: evaluation of the stalk model. , 2007, Biophysical journal.

[35]  M. Kozlov,et al.  How Synaptotagmin Promotes Membrane Fusion , 2007, Science.

[36]  W. Greenleaf,et al.  High-resolution, single-molecule measurements of biomolecular motion. , 2007, Annual review of biophysics and biomolecular structure.

[37]  J. Rizo,et al.  A quaternary SNARE-synaptotagmin-Ca2+-phospholipid complex in neurotransmitter release. , 2007, Journal of molecular biology.

[38]  Sotaro Uemura,et al.  Peptide bond formation destabilizes Shine–Dalgarno interaction on the ribosome , 2007, Nature.

[39]  T. Südhof,et al.  Munc18-1 binds directly to the neuronal SNARE complex , 2007, Proceedings of the National Academy of Sciences.

[40]  R. Jahn,et al.  Early endosomal SNAREs form a structurally conserved SNARE complex and fuse liposomes with multiple topologies , 2007, The EMBO journal.

[41]  T. Ha,et al.  Multiple intermediates in SNARE-induced membrane fusion , 2006, Proceedings of the National Academy of Sciences.

[42]  Helmut Grubmüller,et al.  Molecular Anatomy of a Trafficking Organelle , 2006, Cell.

[43]  M. Kozlov,et al.  Membranes of the world unite! , 2006, The Journal of cell biology.

[44]  R. Jahn,et al.  Munc18-Bound Syntaxin Readily Forms SNARE Complexes with Synaptobrevin in Native Plasma Membranes , 2006, PLoS biology.

[45]  Thomas C. Südhof,et al.  A Complexin/Synaptotagmin 1 Switch Controls Fast Synaptic Vesicle Exocytosis , 2006, Cell.

[46]  Reinhard Jahn,et al.  SNAREs — engines for membrane fusion , 2006, Nature Reviews Molecular Cell Biology.

[47]  Peter M. Kasson,et al.  Ensemble molecular dynamics yields submillisecond kinetics and intermediates of membrane fusion , 2006, Proceedings of the National Academy of Sciences.

[48]  Alexander Stein,et al.  N- to C-Terminal SNARE Complex Assembly Promotes Rapid Membrane Fusion , 2006, Science.

[49]  Y. Shin,et al.  Hemifusion arrest by complexin is relieved by Ca2+–synaptotagmin I , 2006, Nature Structural &Molecular Biology.

[50]  V. Parpura,et al.  Single molecule mechanical probing of the SNARE protein interactions. , 2006, Biophysical journal.

[51]  Demet Araç,et al.  Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release. , 2006, Trends in cell biology.

[52]  A. Brunger,et al.  Conformation of the synaptobrevin transmembrane domain. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[53]  S. Weiss,et al.  Single-molecule fluorescence studies of protein folding and conformational dynamics. , 2006, Chemical reviews.

[54]  Haw Yang,et al.  Quantitative single-molecule conformational distributions: a case study with poly-(L-proline). , 2006, The journal of physical chemistry. A.

[55]  J. Rizo,et al.  SNARE-mediated lipid mixing depends on the physical state of the vesicles. , 2006, Biophysical journal.

[56]  Suren Felekyan,et al.  Separating structural heterogeneities from stochastic variations in fluorescence resonance energy transfer distributions via photon distribution analysis. , 2006, The journal of physical chemistry. B.

[57]  A. Brunger,et al.  Neuronal SNAREs do not trigger fusion between synthetic membranes but do promote PEG-mediated membrane fusion. , 2006, Biophysical journal.

[58]  T. Südhof,et al.  Close membrane-membrane proximity induced by Ca2+-dependent multivalent binding of synaptotagmin-1 to phospholipids , 2006, Nature Structural &Molecular Biology.

[59]  T. Laurence,et al.  Retention of transcription initiation factor sigma70 in transcription elongation: single-molecule analysis. , 2005, Molecular cell.

[60]  N. Grishin,et al.  A minimal domain responsible for Munc13 activity , 2005, Nature Structural &Molecular Biology.

[61]  Edwin R Chapman,et al.  SNARE-driven, 25-millisecond vesicle fusion in vitro. , 2005, Biophysical journal.

[62]  L. Mayorga,et al.  Dynamics of SNARE Assembly and Disassembly during Sperm Acrosomal Exocytosis , 2005, PLoS biology.

[63]  Takeshi Sakaba,et al.  Distinct Kinetic Changes in Neurotransmitter Release After SNARE Protein Cleavage , 2005, Science.

[64]  Axel T Brunger,et al.  Single-molecule studies of synaptotagmin and complexin binding to the SNARE complex. , 2005, Biophysical journal.

[65]  B. Davletov,et al.  Self-assembly of SNARE fusion proteins into star-shaped oligomers. , 2005, The Biochemical journal.

[66]  Y. Shin,et al.  A Partially Zipped SNARE Complex Stabilized by the Membrane* , 2005, Journal of Biological Chemistry.

[67]  Fan Zhang,et al.  Hemifusion in SNARE-mediated membrane fusion , 2005, Nature Structural &Molecular Biology.

[68]  Nam Ki Lee,et al.  Accurate FRET measurements within single diffusing biomolecules using alternating-laser excitation. , 2005, Biophysical journal.

[69]  W. Eaton,et al.  Polyproline and the "spectroscopic ruler" revisited with single-molecule fluorescence. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[70]  Axel T Brunger,et al.  Structure and function of SNARE and SNARE-interacting proteins , 2005, Quarterly Reviews of Biophysics.

[71]  A. Brunger,et al.  Single molecule observation of liposome-bilayer fusion thermally induced by soluble N-ethyl maleimide sensitive-factor attachment protein receptors (SNAREs). , 2004, Biophysical journal.

[72]  G. Augustine,et al.  Dual Roles of the C2B Domain of Synaptotagmin I in Synchronizing Ca2+-Dependent Neurotransmitter Release , 2004, The Journal of Neuroscience.

[73]  Christian Rosenmund,et al.  Calmodulin and Munc13 Form a Ca2+ Sensor/Effector Complex that Controls Short-Term Synaptic Plasticity , 2004, Cell.

[74]  T. Südhof The synaptic vesicle cycle , 2004 .

[75]  Nancy R Forde,et al.  Mechanical processes in biochemistry. , 2004, Annual review of biochemistry.

[76]  B. Lentz,et al.  Energetics of vesicle fusion intermediates: comparison of calculations with observed effects of osmotic and curvature stresses. , 2004, Biophysical journal.

[77]  T. Weber,et al.  Reconstitution of Ca2+-Regulated Membrane Fusion by Synaptotagmin and SNAREs , 2004, Science.

[78]  M. Jackson,et al.  Transmembrane Segments of Syntaxin Line the Fusion Pore of Ca2+-Triggered Exocytosis , 2004, Science.

[79]  M. Jackson,et al.  Fusion Pore Dynamics Are Regulated by Synaptotagmin•t-SNARE Interactions , 2004, Neuron.

[80]  C. Seidel,et al.  Determinants of liposome fusion mediated by synaptic SNARE proteins. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[81]  E. Chapman,et al.  The C2 domains of synaptotagmin--partners in exocytosis. , 2004, Trends in biochemical sciences.

[82]  H. Grubmüller,et al.  Single-molecule fluorescence resonance energy transfer reveals a dynamic equilibrium between closed and open conformations of syntaxin 1 , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[83]  Axel T. Brunger,et al.  Single-molecule studies of SNARE complex assembly reveal parallel and antiparallel configurations , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[84]  Christian Rosenmund,et al.  Molecular mechanisms of active zone function , 2003, Current Opinion in Neurobiology.

[85]  E. Jorgensen,et al.  Controversies in synaptic vesicle exocytosis , 2003, Journal of Cell Science.

[86]  T. Martin Tuning exocytosis for speed: fast and slow modes. , 2003, Biochimica et biophysica acta.

[87]  R. Schneggenburger,et al.  Presynaptic Capacitance Measurements and Ca2+ Uncaging Reveal Submillisecond Exocytosis Kinetics and Characterize the Ca2+ Sensitivity of Vesicle Pool Depletion at a Fast CNS Synapse , 2003, The Journal of Neuroscience.

[88]  C. Stevens,et al.  The Synaptotagmin C2A Domain Is Part of the Calcium Sensor Controlling Fast Synaptic Transmission , 2003, Neuron.

[89]  E. Neher,et al.  Differential Control of the Releasable Vesicle Pools by SNAP-25 Splice Variants and SNAP-23 , 2003, Cell.

[90]  J. Rizo,et al.  Facile detection of protein-protein interactions by one-dimensional NMR spectroscopy. , 2003, Biochemistry.

[91]  A. Brunger,et al.  High Resolution Structure, Stability, and Synaptotagmin Binding of a Truncated Neuronal SNARE Complex* , 2003, The Journal of Biological Chemistry.

[92]  L. Tamm,et al.  FTIR and Fluorescence Studies of Interactions of Synaptic Fusion Proteins in Polymer-Supported Bilayers† , 2003 .

[93]  T. Südhof,et al.  Sr2+ Binding to the Ca2+ Binding Site of the Synaptotagmin 1 C2B Domain Triggers Fast Exocytosis without Stimulating SNARE Interactions , 2003, Neuron.

[94]  M. Müller,et al.  A new mechanism of model membrane fusion determined from Monte Carlo simulation. , 2002, Biophysical journal.

[95]  Lin Yang,et al.  Observation of a Membrane Fusion Intermediate Structure , 2002, Science.

[96]  J. Rothman,et al.  Regulation of membrane fusion by the membrane-proximal coil of the t-SNARE during zippering of SNAREpins , 2002, The Journal of cell biology.

[97]  P. Hanson,et al.  Sealed with a twist: complexin and the synaptic SNARE complex , 2002, Trends in Neurosciences.

[98]  Jodi Gureasko,et al.  Calcium-independent stimulation of membrane fusion and SNAREpin formation by synaptotagmin I , 2002, The Journal of cell biology.

[99]  W. Weissenhorn,et al.  X-ray Structure of a Neuronal Complexin-SNARE Complex from Squid* , 2002, The Journal of Biological Chemistry.

[100]  I. Robinson,et al.  The C2B Ca2+-binding motif of synaptotagmin is required for synaptic transmission in vivo , 2002, Nature.

[101]  T. Schwarz,et al.  Synaptotagmins I and IV promote transmitter release independently of Ca2+ binding in the C2A domain , 2002, Nature.

[102]  Christian Rosenmund,et al.  Total arrest of spontaneous and evoked synaptic transmission but normal synaptogenesis in the absence of Munc13-mediated vesicle priming , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[103]  J. Rothman,et al.  Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[104]  R. Jahn,et al.  Rapid and Selective Binding to the Synaptic SNARE Complex Suggests a Modulatory Role of Complexins in Neuroexocytosis* , 2002, The Journal of Biological Chemistry.

[105]  E. Neher,et al.  The SNARE protein SNAP-25 is linked to fast calcium triggering of exocytosis , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[106]  W. Antonin,et al.  Crystal structure of the endosomal SNARE complex reveals common structural principles of all SNAREs , 2002, Nature Structural Biology.

[107]  T. Südhof,et al.  Three-Dimensional Structure of the Complexin/SNARE Complex , 2002, Neuron.

[108]  Nils Brose,et al.  Differential Control of Vesicle Priming and Short-Term Plasticity by Munc13 Isoforms , 2002, Neuron.

[109]  Thomas C. Südhof,et al.  β Phorbol Ester- and Diacylglycerol-Induced Augmentation of Transmitter Release Is Mediated by Munc13s and Not by PKCs , 2002, Cell.

[110]  L. Donald Partridge,et al.  Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis , 2002, Nature Neuroscience.

[111]  E. Jorgensen,et al.  An open form of syntaxin bypasses the requirement for UNC-13 in vesicle priming , 2001, Nature.

[112]  M. L. Wagner,et al.  Reconstituted syntaxin1a/SNAP25 interacts with negatively charged lipids as measured by lateral diffusion in planar supported bilayers. , 2001, Biophysical journal.

[113]  R. Scheller,et al.  Three SNARE complexes cooperate to mediate membrane fusion , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[114]  R. Jahn,et al.  Homo- and Heterooligomeric SNARE Complexes Studied by Site-directed Spin Labeling* , 2001, The Journal of Biological Chemistry.

[115]  W. Xiao,et al.  The neuronal t-SNARE complex is a parallel four-helix bundle , 2001, Nature Structural Biology.

[116]  R. Scheller,et al.  Sequential SNARE Assembly Underlies Priming and Triggering of Exocytosis , 2001, Neuron.

[117]  T. Südhof,et al.  Synaptotagmin I functions as a calcium regulator of release probability , 2001, Nature.

[118]  Toru Ishizuka,et al.  SNARE Complex Oligomerization by Synaphin/Complexin Is Essential for Synaptic Vesicle Exocytosis , 2001, Cell.

[119]  Arne Stoschek,et al.  The architecture of active zone material at the frog's neuromuscular junction , 2001, Nature.

[120]  T Centner,et al.  Fluorescence quenching: A tool for single-molecule protein-folding study. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[121]  D. Woodbury,et al.  THE t‐SNARE SYNTAXIN IS SUFFICIENT FOR SPONTANEOUS FUSION OF SYNAPTIC VESICLES TO PLANAR MEMBRANES , 2000, Cell biology international.

[122]  Thomas C. Südhof,et al.  The Synaptic VesicleCycle Revisited , 2000, Neuron.

[123]  J. Rothman,et al.  Compartmental specificity of cellular membrane fusion encoded in SNARE proteins , 2000, Nature.

[124]  J. Rothman,et al.  Topological restriction of SNARE-dependent membrane fusion , 2000, Nature.

[125]  J. Littleton,et al.  The C2b Domain of Synaptotagmin Is a Ca2+–Sensing Module Essential for Exocytosis , 2000, The Journal of cell biology.

[126]  J. Rothman,et al.  Close Is Not Enough , 2000, The Journal of cell biology.

[127]  T. Südhof,et al.  Selective Interaction of Complexin with the Neuronal SNARE Complex , 2000, The Journal of Biological Chemistry.

[128]  Richard H. Scheller,et al.  Three-dimensional structure of the neuronal-Sec1–syntaxin 1a complex , 2000, Nature.

[129]  T. Martin,et al.  The C Terminus of SNAP25 Is Essential for Ca2+-dependent Binding of Synaptotagmin to SNARE Complexes* , 2000, The Journal of Biological Chemistry.

[130]  T. Südhof,et al.  The synaptic vesicle cycle revisited. , 2000, Neuron.

[131]  E. Neher,et al.  Inhibition of SNARE Complex Assembly Differentially Affects Kinetic Components of Exocytosis , 1999, Cell.

[132]  M. Charlton,et al.  Activity-dependent changes in partial VAMP complexes during neurotransmitter release , 1999, Nature Neuroscience.

[133]  A. Brunger,et al.  Crystal Structure of the Cytosolic C2a-C2b Domains of Synaptotagmin III , 1999, The Journal of cell biology.

[134]  J. Rothman,et al.  Rapid and efficient fusion of phospholipid vesicles by the alpha-helical core of a SNARE complex in the absence of an N-terminal regulatory domain. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[135]  J. Rothman,et al.  Content mixing and membrane integrity during membrane fusion driven by pairing of isolated v-SNAREs and t-SNAREs. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[136]  D. Fasshauer,et al.  Kinetics of Synaptotagmin Responses to Ca2+ and Assembly with the Core SNARE Complex onto Membranes , 1999, Neuron.

[137]  J. Rothman,et al.  The length of the flexible SNAREpin juxtamembrane region is a critical determinant of SNARE-dependent fusion. , 1999, Molecular cell.

[138]  T. Südhof,et al.  A conformational switch in syntaxin during exocytosis: role of munc18 , 1999, The EMBO journal.

[139]  T. Südhof,et al.  NMR analysis of the structure of synaptobrevin and of its interaction with syntaxin , 1999, Journal of biomolecular NMR.

[140]  W. Antonin,et al.  Mixed and Non-cognate SNARE Complexes , 1999, The Journal of Biological Chemistry.

[141]  R. Scheller,et al.  SNARE Interactions Are Not Selective , 1999, The Journal of Biological Chemistry.

[142]  K. Fiebig,et al.  Folding intermediates of SNARE complex assembly , 1999, Nature Structural Biology.

[143]  A. Brunger,et al.  Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[144]  J. Rothman,et al.  Arrangement of subunits in 20 S particles consisting of NSF, SNAPs, and SNARE complexes. , 1998, Molecular cell.

[145]  Reinhard Jahn,et al.  Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution , 1998, Nature.

[146]  Tao Xu,et al.  Multiple kinetic components of exocytosis distinguished by neurotoxin sensitivity , 1998, Nature Neuroscience.

[147]  D. Hoekstra,et al.  Probe transfer with and without membrane fusion in a fluorescence fusion assay. , 1998, Biochemistry.

[148]  Benedikt Westermann,et al.  SNAREpins: Minimal Machinery for Membrane Fusion , 1998, Cell.

[149]  R. Scheller,et al.  Structural Organization of the Synaptic Exocytosis Core Complex , 1997, Neuron.

[150]  A T Brünger,et al.  Structural Changes Are Associated with Soluble N-Ethylmaleimide-sensitive Fusion Protein Attachment Protein Receptor Complex Formation* , 1997, The Journal of Biological Chemistry.

[151]  T. Schikorski,et al.  Quantitative Ultrastructural Analysis of Hippocampal Excitatory Synapses Materials and Methods Terminology Fixation and Embedding , 2022 .

[152]  R. Pagano,et al.  Measurement of spontaneous transfer and transbilayer movement of BODIPY-labeled lipids in lipid vesicles. , 1997, Biochemistry.

[153]  P. Hanson,et al.  Assembly and disassembly of a ternary complex of synaptobrevin, syntaxin, and SNAP-25 in the membrane of synaptic vesicles. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[154]  P. Hanson,et al.  Neurotransmitter release — four years of SNARE complexes , 1997, Current Opinion in Neurobiology.

[155]  C. Stevens,et al.  Heterogeneity of Release Probability, Facilitation, and Depletion at Central Synapses , 1997, Neuron.

[156]  A. Brünger,et al.  A Structural Change Occurs upon Binding of Syntaxin to SNAP-25* , 1997, The Journal of Biological Chemistry.

[157]  J. Rothman,et al.  Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-treated synapses. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[158]  T. Südhof,et al.  Synaptotagmin–Syntaxin Interaction: The C2 Domain as a Ca2+-Dependent Electrostatic Switch , 1997, Neuron.

[159]  R. Scheller,et al.  Localization of synaptotagmin-binding domains on syntaxin , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[160]  P. Hanson,et al.  Ca2+ Regulates the Interaction between Synaptotagmin and Syntaxin 1 (*) , 1995, The Journal of Biological Chemistry.

[161]  Thomas C. Südhof,et al.  Complexins: Cytosolic proteins that regulate SNAP receptor function , 1995, Cell.

[162]  Thomas C. Südhof,et al.  Ca2+-dependent and -independent activities of neural and non-neural synaptotagmins , 1995, Nature.

[163]  S. Sprang,et al.  Structure of the first C2 domain of synaptotagmin I: A novel Ca2+/phospholipid-binding fold , 1995, Cell.

[164]  J. Dolly,et al.  Differences in the protease activities of tetanus and botulinum B toxins revealed by the cleavage of vesicle-associated membrane protein and various sized fragments. , 1994, Biochemistry.

[165]  J. Rothman,et al.  Mechanisms of intracellular protein transport , 1994, Nature.

[166]  Reinhard Jahn,et al.  Vesicle fusion from yeast to man , 1994, Nature.

[167]  H. V. Gersdorff,et al.  Dynamics of synaptic vesicle fusion and membrane retrieval in synaptic terminals , 1994, Nature.

[168]  T. Südhof,et al.  Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin , 1993, Nature.

[169]  T. Südhof,et al.  Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C , 1990, Nature.