Membrane Fusion: Grappling with SNARE and SM Proteins
Open accessAbstract
The two universally required components of the intracellular membrane fusion machinery, SNARE and SM (Sec1/Munc18-like) proteins, play complementary roles in fusion. Vesicular and target membrane–localized SNARE proteins zipper up into an α-helical bundle that pulls the two membranes tightly together to exert the force required for fusion. SM proteins, shaped like clasps, bind to trans-SNARE complexes to direct their fusogenic action. Individual fusion reactions are executed by distinct combinations of SNARE and SM proteins to ensure specificity, and are controlled by regulators that embed the SM-SNARE fusion machinery into a physiological context. This regulation is spectacularly apparent in the exquisite speed and precision of synaptic exocytosis, where synaptotagmin (the calcium-ion sensor for fusion) cooperates with complexin (the clamp activator) to control the precisely timed release of neurotransmitters that initiates synaptic transmission and underlies brain function.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Plasma membrane SNARE proteins syntaxin and SNAP-25 and the SM protein Munc18 are not enriched in active zones but distributed all over the plasma membrane.
“Furthermore, as noted above, the plasma membrane SNARE proteins syntaxin and SNAP-25 and the SM protein Munc18 that are components of the synaptic vesicle fusion machinery for exocytosis (Südhof and Rothman, 2009) are not enriched in active zones but distributed all over the plasma membrane.”
From The Presynaptic Active Zone (2012) · cites this paper as Südhof and Rothman, 2009
SNARE proteins drive intracellular membrane fusion between transport vesicles and organelles.
“SNARE proteins drive intracellular membrane fusion between transport vesicles and organelles (82).”
From Computed structures of core eukaryotic protein complexes (2021) · cites this paper as [82]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 14,984 · see citing works
SNAP receptors implicated in vesicle targeting and fusion
Söllner, T. H., Whiteheart, S. W., Brunner, M., Erdjument‐Bromage, H., Geromanos, S. J., Tempst, P., & Rothman, J. E. (1993) · Nature · doi:10.1038/362318a0 · Cited by 3,239 · see citing works
Self-citationSNAREpins: Minimal Machinery for Membrane Fusion
Weber, T., Zemelman, B. V., McNew, J. A., Westermann, B., Gmachl, M., Parlati, F., Söllner, T. H., & Rothman, J. E. (1998) · Cell · doi:10.1016/s0092-8674(00)81404-x · Cited by 2,481 · see citing works
Self-citationCrystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 Å resolution
Sutton, R. B., Fasshauer, D., Jahn, R., & Brunger, A. T. (1998) · Nature · doi:10.1038/26412 · Cited by 2,417 · see citing works
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 · see citing works
Self-citationNovick, P., Field, C., & Schekman, R. W. (1980) · Cell · doi:10.1016/0092-8674(80)90128-2 · Cited by 1,807 · see citing works
Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., de Laureto, P. P., DasGupta, B. R., & Montecucco, C. (1992) · Nature · doi:10.1038/359832a0 · Cited by 1,803 · see citing works
Synaptotagmin I: A major Ca2+ sensor for transmitter release at a central synapse
Geppert, M., Goda, Y., Hammer, R. E., Li, C., Rosahl, T. W., Stevens, C. F., & Südhof, T. C. (1994) · Cell · doi:10.1016/0092-8674(94)90556-8 · Cited by 1,483 · see citing works
Self-citationSynaptic Assembly of the Brain in the Absence of Neurotransmitter Secretion
Verhage, M., Maia, A. S., Plomp, J. J., Brussaard, A. B., Heeroma, J. H., Vermeer, H., Toonen, R. F. G., Hammer, R. E., van den Berg, T. K., Berg, et al. (2000) · Science · doi:10.1126/science.287.5454.864 · Cited by 1,431 · see citing works
Syntaxin: A Synaptic Protein Implicated in Docking of Synaptic Vesicles at Presynaptic Active Zones
Bennett, M. K., Calakos, N., & Scheller, R. H. (1992) · Science · doi:10.1126/science.1321498 · Cited by 1,263 · see citing works
Botulinum neurotoxin A selectively cleaves the synaptic protein SNAP-25
Blasi, J., Chapman, E. R., Link, E., Binz, T., Yamasaki, S., Camilli, P. V. D., Südhof, T. C., Niemann, H., & Jahn, R. (1993) · Nature · doi:10.1038/365160a0 · Cited by 1,221 · see citing works
Synaptotagmin: a Calcium Sensor on the Synaptic Vesicle Surface
Brose, N., Petrenko, A. G., Südhof, T. C., & Jahn, R. (1992) · Science · doi:10.1126/science.1589771 · Cited by 979 · see citing works
Synaptotagmin I functions as a calcium regulator of release probability
Fernández-Chacón, R., Königstorfer, A., Gerber, S. H., García, J., Matos, M. F., Stevens, C. F., Brose, N., Rizo, J., Rosenmund, C., & Südhof, T. C. (2001) · Nature · doi:10.1038/35065004 · Cited by 961 · see citing works
Perin, M. S., Fried, V. A., Mignery, G. A., Jahn, R., & Südhof, T. C. (1990) · Nature · doi:10.1038/345260a0 · Cited by 813 · see citing works
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 · see citing works
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 · see citing works
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 · see citing works
Three-dimensional structure of the neuronal-Sec1–syntaxin 1a complex
Misura, K. M. S., Scheller, R. H., & Weis, W. I. (2000) · Nature · doi:10.1038/35006120 · Cited by 786 · see citing works
A conformational switch in syntaxin during exocytosis: role of munc18
Dulubova, I., Sugita, S., Hill, S., Hosaka, M., Fernández, I., Südhof, T., & Rizo, J. (1999) · EMBO Journal · doi:10.1093/emboj/18.16.4372 · Cited by 772 · see citing works
Synaptic vesicle fusion complex contains unc-18 homologue bound to syntaxin
Hata, Y., Slaughter, C., & Südhof, T. (1993) · Nature · doi:10.1038/366347a0 · Cited by 751 · see citing works
Compartmental specificity of cellular membrane fusion encoded in SNARE proteins
McNew, J. A., Parlati, F., Fukuda, R., Johnston, R. J., Paz, K., Paumet, F., Söllner, T. H., & Rothman, J. E. (2000) · Nature · doi:10.1038/35025000 · Cited by 691 · see citing works
Self-citationStructure of the first C2 domain of synaptotagmin I: a novel Ca2+/phospholipid-binding fold.
Sutton, R., Davletov, B., Berghuis, A., Südhof, T., & Sprang, S. R. (1995) · Cell · doi:10.1016/0092-8674(95)90296-1 · Cited by 689 · see citing works
SNARE Function Analyzed in Synaptobrevin/VAMP Knockout Mice
Schoch, S., Deák, F., Königstorfer, A., Mozhayeva, M. G., Sara, Y., Südhof, T. C., & Kavalali, E. T. (2001) · Science · doi:10.1126/science.1064335 · Cited by 664 · see citing works
Ca2+-dependent and -independent activities of neural and non-neural synaptotagmins
Li, C., Ullrich, B., Zhang, J. Z., Anderson, R. G. W., Brose, N., & Südhof, T. C. (1995) · Nature · doi:10.1038/375594a0 · Cited by 599 · see citing works
Clary, D. O., Griff, I. C., & Rothman, J. E. (1990) · Cell · doi:10.1016/0092-8674(90)90482-t · Cited by 588 · see citing works
Self-citationSec18p (NSF)-Driven Release of Sec17p (α-SNAP) Can Precede Docking and Fusion of Yeast Vacuoles
Mayer, A., Wickner, W. T., & Haas, A. (1996) · Cell · doi:10.1016/s0092-8674(00)81084-3 · Cited by 580 · see citing works
VAMP-1: a synaptic vesicle-associated integral membrane protein.
Trimble, W. S., Cowan, D. M., & Scheller, R. H. (1988) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.85.12.4538 · Cited by 575 · see citing works
A fusion protein required for vesicle-mediated transport in both mammalian cells and yeast
Wilson, D. W., Wilcox, C. A., Flynn, G. C., Chen, E., Kuang, W.-J., Henzel, W. J., Block, M. R., Ullrich, A., & Rothman, J. E. (1989) · Nature · doi:10.1038/339355a0 · Cited by 574 · see citing works
Self-citationBotulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC‐1/syntaxin.
Blasi, J., Chapman, E. R., Yamasaki, S., Binz, T., Niemann, H., & Jahn, R. (1993) · The EMBO Journal · doi:10.1002/j.1460-2075.1993.tb06171.x · Cited by 546 · see citing works
Rizo, J., & Rosenmund, C. (2008) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.1450 · Cited by 538 · see citing works
Complexins Regulate a Late Step in Ca2+-Dependent Neurotransmitter Release
Reim, K., Mansour, M., Varoqueaux, F., McMahon, H. T., Südhof, T. C., Brose, N., & Rosenmund, C. (2001) · Cell · doi:10.1016/s0092-8674(01)00192-1 · Cited by 500 · see citing works
Selective Activation of Cognate SNAREpins by Sec1/Munc18 Proteins
Shen, J., Tareste, D. C., Paumet, F., Rothman, J. E., & Melia, T. J. (2007) · Cell · doi:10.1016/j.cell.2006.12.016 · Cited by 484 · see citing works
Self-citationA single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding.
Davletov, B. A., & Südhof, T. C. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)74326-9 · Cited by 480 · see citing works
Self-citationA complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis.
Tang, J., Maximov, A., Shin, O., Dai, H., Rizo, J., & Südhof, T. (2006) · Cell · doi:10.1016/j.cell.2006.08.030 · Cited by 467 · see citing works
Three-Dimensional Structure of the Complexin/SNARE Complex
Chen, X., Tomchick, D. R., Kovrigin, E., Araç, D., Machius, M., Südhof, T. C., & Rizo, J. (2002) · Neuron · doi:10.1016/s0896-6273(02)00583-4 · Cited by 451 · see citing works
Timing of neurotransmission at fast synapses in the mammalian brain
Sabatini, B. L., & Regehr, W. G. (1996) · Nature · doi:10.1038/384170a0 · Cited by 442 · see citing works
Identification of the nerve terminal targets of botulinum neurotoxin serotypes A, D, and E.
Schiavo, G., Rossetto, O., Catsicas, S., et al. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)80452-9 · Cited by 426 · see citing works
Malhotra, V. (1988) · Cell · doi:10.1016/0092-8674(88)90554-5 · Cited by 391 · see citing works
Fernández, I., Araç, D., Ubach, J., Gerber, S. H., Shin, O., Gao, Y., Anderson, R. G. W., Südhof, T., & Rizo, J. (2001) · Neuron · doi:10.1016/s0896-6273(01)00548-7 · Cited by 387 · see citing works
A Clamping Mechanism Involved in SNARE-Dependent Exocytosis
Giraudo, C. G., Eng, W. S., Melia, T. J., & Rothman, J. E. (2006) · Science · doi:10.1126/science.1129450 · Cited by 368 · see citing works
Self-citationCa2+ Regulates the Interaction between Synaptotagmin and Syntaxin 1 (*)
Chapman, E., Hanson, P., An, S. J., & Jahn, R. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.40.23667 · Cited by 363 · see citing works
Tetanus toxin action: Inhibition of neurotransmitter release linked to synaptobrevin proteolysis
Link, E., Edelmann, L., Chou, J. H., Binz, T., Yamasaki, S., Eisel, U., Baumert, M., Südhof, T. C., Niemann, H., & Jahn, R. (1992) · Biochemical and Biophysical Research Communications · doi:10.1016/0006-291x(92)92305-h · Cited by 349 · see citing works
Munc18-1 binds directly to the neuronal SNARE complex
Dulubova, I., Khvotchev, M. V., Liu, S., Huryeva, I., Südhof, T. C., & Rizo, J. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611318104 · Cited by 348 · see citing works
Dascher, C., Ossig, R., Gallwitz, D., & Schmitt, H. D. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.2.872 · Cited by 345 · see citing works
Complexin Controls the Force Transfer from SNARE Complexes to Membranes in Fusion
Maximov, A., Tang, J., Yang, X., Pang, Z. P., & Südhof, T. C. (2009) · Science · doi:10.1126/science.1166505 · Cited by 339 · see citing works
Three-dimensional structure of an evolutionarily conserved N-terminal domain of syntaxin 1A.
Fernández, I., Ubach, J., Dulubova, I., Zhang, X., Südhof, T., & Rizo, J. (1998) · Cell · doi:10.1016/s0092-8674(00)81742-0 · Cited by 324 · see citing works
Cohen, F., & Melikyan, G. B. (2004) · The Journal of Membrane Biology · doi:10.1007/s00232-004-0669-8 · Cited by 321 · see citing works
Hardwick, K., & Pelham, H. R. B. (1992) · The Journal of Cell Biology · doi:10.1083/jcb.119.3.513 · Cited by 306 · see citing works
McNew, J. A., Weber, T., Parlati, F., et al. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.1.105 · Cited by 302 · see citing works
Conformational switch of syntaxin-1 controls synaptic vesicle fusion
Gerber, S. H., Rah, J.-C., Min, S.-W., Liu, X., de Wit, H., Dulubova, I., Meyer, A. C., Rizo, J., Arancillo, M., Hammer, R. E., et al. (2008) · Science · doi:10.1126/science.1163174 · Cited by 294 · see citing works
A complexin fusion clamp regulates spontaneous neurotransmitter release and synaptic growth
Huntwork, S., & Littleton, J. T. (2007) · Nature Neuroscience · doi:10.1038/nn1980 · Cited by 292 · see citing works
Topological restriction of SNARE-dependent membrane fusion
Parlati, F., McNew, J. A., Fukuda, R., Miller, R. B., Söllner, T. H., & Rothman, J. E. (2000) · Nature · doi:10.1038/35025076 · Cited by 287 · see citing works
Self-citationEnergetics and dynamics of SNAREpin folding across lipid bilayers
Li, F., Pincet, F., Perez, É., Eng, W. S., Melia, T. J., Rothman, J. E., & Tareste, D. C. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1310 · Cited by 278 · see citing works
Self-citationCloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1.
Inoue, A., Obata, K., & Akagawa, K. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)50061-8 · Cited by 274 · see citing works
A synaptic vesicle membrane protein is conserved from mammals to Drosophila
Südhof, T. C., Baumert, M., Perin, M. S., & Jahn, R. (1989) · Neuron · doi:10.1016/0896-6273(89)90193-1 · Cited by 269 · see citing works
Unraveling the mechanisms of synaptotagmin and SNARE function in neurotransmitter release.
Rizo, J., Chen, X., & Araç, D. (2006) · Trends in Cell Biology · doi:10.1016/j.tcb.2006.04.006 · Cited by 255 · see citing works
Kloepper, T. H., Kienle, C. N., & Fasshauer, D. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-03-0193 · Cited by 247 · see citing works
Functional architecture of an intracellular membrane t-SNARE
Fukuda, R., McNew, J. A., Weber, T., Parlati, F., Engel, T., Nickel, W., Rothman, J. E., & Söllner, T. H. (2000) · Nature · doi:10.1038/35025084 · Cited by 245 · see citing works
Self-citationPurification of active HOPS complex reveals its affinities for phosphoinositides and the SNARE Vam7p
Stroupe, C., Collins, K. M., Fratti, R. A., & Wickner, W. T. (2006) · The EMBO Journal · doi:10.1038/sj.emboj.7601051 · Cited by 244 · see citing works
Sly1 binds to Golgi and ER syntaxins via a conserved N-terminal peptide motif.
Yamaguchi, T., Dulubova, I., Min, S.-W., Chen, X., Rizo, J., & Südhof, T. (2002) · Developmental Cell · doi:10.1016/s1534-5807(02)00125-9 · Cited by 223 · see citing works
Multiple intermediates in SNARE-induced membrane fusion
Yoon, T., Okumuş, B., Zhang, F., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0606032103 · Cited by 221 · see citing works
Hemifusion arrest by complexin is relieved by Ca2+–synaptotagmin I
Schaub, J. R., Lu, X., Doneske, B., Shin, Y., & McNew, J. A. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1124 · Cited by 219 · see citing works
Three SNARE complexes cooperate to mediate membrane fusion
Hua, Y., & Scheller, R. H. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.131214798 · Cited by 206 · see citing works
How Tlg2p/syntaxin 16 'snares’ Vps45
Dulubova, I., Yamaguchi, T., Gao, Y., Min, S., Huryeva, I., Südhof, T. C., & Rizo, J. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf381 · Cited by 204 · see citing works
McNew, J. A., Weber, T., Engelman, D. M., et al. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80343-3 · Cited by 172 · see citing works
Alternative Zippering as an On-Off Switch for SNARE-Mediated Fusion
Giraudo, C. G., Garcia-Diaz, A., Eng, W. S., Chen, Y., Hendrickson, W. A., Melia, T. J., & Rothman, J. E. (2009) · Science · doi:10.1126/science.1166500 · Cited by 167 · see citing works
Self-citationBowen, M. E., Weninger, K., Brünger, A. T., & Chu, S. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.048637 · Cited by 164 · see citing works
Structural Determinants of Synaptobrevin 2 Function in Synaptic Vesicle Fusion
Deák, F., Shin, O., Kavalali, E. T., & Südhof, T. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5272-05.2006 · Cited by 150 · see citing works
SNAREpin/Munc18 promotes adhesion and fusion of large vesicles to giant membranes
Tareste, D. C., Shen, J., Melia, T. J., & Rothman, J. E. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0712125105 · Cited by 116 · see citing works
Self-citationPang, Z. P., Shin, O.-H., Meyer, A. C., Rosenmund, C., & Südhof, T. C. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3804-06.2006 · Cited by 113 · see citing works
Self-citationShim, J., Newman, A. P., & Ferro‐Novick, S. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.113.1.55 · Cited by 98 · see citing works
Dascher, C., Ossig, R., Gallwitz, D., et al. (1991) · Molecular and Cellular Biology · doi:10.1128/mcb.11.2.872-885.1991 · Cited by 98 · see citing works
Distinct Targeting and Fusion Functions of the PX and SNARE Domains of Yeast Vacuolar Vam7p
Fratti, R. A., & Wickner, W. T. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m700584200 · Cited by 46 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The stressed synapse: the impact of stress and glucocorticoids on glutamate transmission
Popoli, M., Yan, Z., McEwen, B. S., & Sanacora, G. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3138 · Cited by 1,393 · see citing works
Platelet α-granules: Basic biology and clinical correlates
Blair, P., & Flaumenhaft, R. (2009) · Blood Reviews · doi:10.1016/j.blre.2009.04.001 · Cited by 1,157 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Self-citationPancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men
Rorsman, P., & Ashcroft, F. M. (2018) · Physiological Reviews · doi:10.1152/physrev.00008.2017 · Cited by 793 · see citing works
Computed structures of core eukaryotic protein complexes
Humphreys, I. R., Pei, J., Baek, M., Krishnakumar, A., Anishchenko, I., Ovchinnikov, S., Zhang, J., Ness, T. J., Banjade, S., Bagde, S. R., et al. (2021) · Science · doi:10.1126/science.abm4805 · Cited by 542 · see citing works
The mechanisms and functions of spontaneous neurotransmitter release
Kavalali, E. T. (2015) · Nature Reviews Neuroscience · doi:10.1038/nrn3875 · Cited by 486 · see citing works
Short-Term Presynaptic Plasticity
Regehr, W. G. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005702 · Cited by 482 · see citing works
Munc13 mediates the transition from the closed syntaxin–Munc18 complex to the SNARE complex
Ma, C., Li, W., Xu, Y., & Rizo, J. (2011) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2047 · Cited by 363 · see citing works
Lőrincz, P., & Juhász, G. (2020) · Journal of Molecular Biology · doi:10.1016/j.jmb.2019.10.028 · Cited by 328 · see citing works
Apical–basal polarity and the control of epithelial form and function
Buckley, C. E., & St Johnston, D. (2022) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-022-00465-y · Cited by 295 · see citing works
Wang, Z., Miao, G., Xue, X., Guo, X., Yuan, C., Wang, Z., Zhang, G., Chen, Y., Feng, D., Hu, J., et al. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.08.021 · Cited by 321 · see citing works
Brinkmalm, A., Brinkmalm, G., Honer, W. G., Frölich, L., Hausner, L., Minthon, L., Hansson, O., Wallin, A., Zetterberg, H., Blennow, K., et al. (2014) · Molecular Neurodegeneration · doi:10.1186/1750-1326-9-53 · Cited by 293 · see citing works
Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L)
Fan, W., Nassiri, A., & Zhong, Q. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1016472108 · Cited by 285 · see citing works
Phosphoinositides in Control of Membrane Dynamics
Schink, K. O., Tan, K.-W., & Stenmark, H. (2016) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-111315-125349 · Cited by 283 · see citing works
Current Knowledge on Exosome Biogenesis, Cargo-Sorting Mechanism and Therapeutic Implications
Xie, S., Zhang, Q., & Jiang, L. (2022) · Membranes · doi:10.3390/membranes12050498 · Cited by 262 · see citing works
Synaptic markers of cognitive decline in neurodegenerative diseases: a proteomic approach
Bereczki, E., Branca, R. M., Francis, P. T., Pereira, J. B., Baek, J.-H., Hortobágyi, T., Winblad, B., Ballard, C., Lehtiö, J., & Aarsland, D. (2018) · Brain · doi:10.1093/brain/awx352 · Cited by 220 · see citing works
Astrocyte lipid metabolism is critical for synapse development and function in vivo
van Deijk, A. F., Camargo, N., Timmerman, J., Heistek, T., Brouwers, J. F., Mogavero, F., Mansvelder, H. D., Smit, A. B., & Verheijen, M. H. G. (2017) · Glia · doi:10.1002/glia.23120 · Cited by 201 · see citing works
Mechanism of neurotransmitter release coming into focus
Rizo, J. (2018) · Protein Science · doi:10.1002/pro.3445 · Cited by 210 · see citing works
Zhang, G., Bai, H., Zhang, H., Dean, C., Wu, Q., Li, J., Guariglia, S., Meng, Q., & Cai, D. (2011) · Neuron · doi:10.1016/j.neuron.2010.12.036 · Cited by 208 · see citing works
Disorders in the initial steps of steroid hormone synthesis
Miller, W. L. (2017) · The Journal of Steroid Biochemistry and Molecular Biology · doi:10.1016/j.jsbmb.2016.03.009 · Cited by 205 · see citing works
Endocytosis and Autophagy: Exploitation or Cooperation?
Tooze, S. A., Abada, A., & Elazar, Z. (2014) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a018358 · Cited by 202 · see citing works
From the stochasticity of molecular processes to the variability of synaptic transmission
Ribrault, C., Sekimoto, K., & Triller, A. (2011) · Nature Reviews Neuroscience · doi:10.1038/nrn3025 · Cited by 198 · see citing works
Biesemann, C., Grønborg, M., Luquet, E., Wichert, S. P., Bernard, V., Bungers, S. R., Cooper, B., Varoqueaux, F., Li, L., Byrne, J. A., et al. (2014) · The EMBO Journal · doi:10.1002/embj.201386120 · Cited by 156 · see citing works
Regulation of NMDA glutamate receptor functions by the GluN2 subunits
Vieira, M., Yong, X. L. H., Roche, K. W., & Anggono, V. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.14970 · Cited by 151 · see citing works
“In general, vesicular fusion to the plasma membrane is mediated by the assembly soluble N-ethylmaleimide-sensitive factor attachment protein receptors (SNAREs) protein family, including the target SNARE (t-SNARE) syntaxin, synaptosome-associated protein (SNAP) and the vesicular SNARE (v-SNARE) vesicle-associated membr…”
BackgroundInfluentialIzumo is part of a multiprotein family whose members form large complexes on mammalian sperm
Ellerman, D. A., Pei, J., Gupta, S., Snell, W. J., Myles, D., & Primakoff, P. (2009) · Molecular Reproduction and Development · doi:10.1002/mrd.21092 · Cited by 143 · see citing works
Fusion Competent Synaptic Vesicles Persist upon Active Zone Disruption and Loss of Vesicle Docking
Wang, S. S. H., Held, R. G., Wong, M. Y., Liu, C., Karakhanyan, A., & Kaeser, P. S. (2016) · Neuron · doi:10.1016/j.neuron.2016.07.005 · Cited by 143 · see citing works
SNAREopathies: Diversity in Mechanisms and Symptoms
Verhage, M., & Sørensen, J. B. (2020) · Neuron · doi:10.1016/j.neuron.2020.05.036 · Cited by 121 · see citing works
Salpietro, V., Malintan, N. T., Llano-Rivas, I., Spaeth, C. G., Efthymiou, S., Striano, P., Vandrovcova, J., Cutrupi, M. C., Chimenz, R., David, E., et al. (2019) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2019.02.016 · Cited by 134 · see citing works
Self-citationAssessing the landscape of <i>STXBP1</i> -related disorders in 534 individuals
Xian, J., Parthasarathy, S., Ruggiero, S. M., Balagura, G., Fitch, E., Helbig, K., Gan, J., Ganesan, S., Kaufman, M. C., Ellis, C. A., et al. (2022) · Brain · doi:10.1093/brain/awab327 · Cited by 130 · see citing works
Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M. O., Durakoglugil, M., Herz, J., Monteggia, L. M., & Kavalali, E. T. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.024 · Cited by 131 · see citing works
Quantitative proteomics reveals distinct composition of amyloid plaques in Alzheimer’s disease
Xiong, F., Ge, W., & Ma, C. (2019) · Alzheimer's & Dementia · doi:10.1016/j.jalz.2018.10.006 · Cited by 133 · see citing works
Postsynaptic Complexin Controls AMPA Receptor Exocytosis during LTP
Ahmad, M., Polepalli, J. S., Goswami, D., Yang, X., Kaeser-Woo, Y. J., Südhof, T. C., & Malenka, R. C. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.020 · Cited by 133 · see citing works
Self-citationIntracellular trafficking and secretion of inflammatory cytokines
Stow, J. L., & Murray, R. Z. (2013) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2013.04.001 · Cited by 128 · see citing works
SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking
Lau, C. G., Takayasu, Y., Rodenas-Ruano, A., Paternain, A. V., Lerma, J., Bennett, M. V. L., & Zukin, R. S. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4933-08.2010 · Cited by 120 · see citing works
Lai, Y., Diao, J., Cipriano, D. J., Zhang, Y., Pfuetzner, R. A., Padolina, M. S., & Brunger, A. T. (2014) · eLife · doi:10.7554/elife.03756 · Cited by 107 · see citing works
Understanding a protein fold: The physics, chemistry, and biology of α-helical coiled coils
Woolfson, D. N. (2023) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2023.104579 · Cited by 106 · see citing works
Amyloid-β Oligomers May Impair SNARE-Mediated Exocytosis by Direct Binding to Syntaxin 1a
Yang, Y., Kim, J., Kim, H. Y., Ryoo, N., Lee, S., Kim, Y., Rhim, H., & Shin, Y.-K. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.07.044 · Cited by 88 · see citing works
A secretagogin locus of the mammalian hypothalamus controls stress hormone release
Romanov, R. A., Alpár, A., Zhang, M., Zeisel, A., Calas, A., Landry, M., Fuszard, M., Shirran, S. L., Schnell, R., Dobolyi, Á., et al. (2015) · The EMBO Journal · doi:10.15252/embj.201488977 · Cited by 85 · see citing works
Dual Role of VAMP8 in Regulating Insulin Exocytosis and Islet β Cell Growth
Zhu, D., Zhang, Y., Lam, P. P. L., Dolai, S., Liu, Y., Cai, E. P., Choi, D., Schroer, S. A., Kang, Y., Allister, E. M., et al. (2012) · Cell Metabolism · doi:10.1016/j.cmet.2012.07.001 · Cited by 87 · see citing works
Zhu, D., Koo, E., Kwan, E., Kang, Y., Park, S., Xie, H., Sugita, S., & Gaisano, H. Y. (2013) · Diabetologia · doi:10.1007/s00125-012-2757-0 · Cited by 81 · see citing works
Reduced SNAP‐25 alters short‐term plasticity at developing glutamatergic synapses
Antonucci, F., Corradini, I., Morini, R., Fossati, G., Menna, E., Pozzi, D., Pacioni, S., Verderio, C., Bacci, A., & Matteoli, M. (2013) · The EMBO Reports · doi:10.1038/embor.2013.75 · Cited by 71 · see citing works
The Journey of the Synaptic Autophagosome: A Cell Biological Perspective
Kargbo-Hill, S. E., & Colón-Ramos, D. A. (2020) · Neuron · doi:10.1016/j.neuron.2020.01.018 · Cited by 72 · see citing works
The origin and evolution of synaptic proteins – choanoflagellates lead the way
Burkhardt, P. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110247 · Cited by 59 · see citing works
Different regions of synaptic vesicle membrane regulate VAMP2 conformation for the SNARE assembly
Wang, C., Tu, J., Zhang, S., Cai, B., Liu, Z., Hou, S., Zhong, Q., Hu, X., Liu, W., Li, G., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-15270-4 · Cited by 55 · see citing works
Richter, E. A., Bilan, P. J., & Klip, A. (2025) · Physiological Reviews · doi:10.1152/physrev.00033.2024 · Cited by 64 · see citing works
Impaired neurotransmission in ether lipid-deficient nerve terminals
Brodde, A., Teigler, A., Brugger, B., Lehmann, W. D., Wieland, F., Berger, J., & Just, W. W. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds097 · Cited by 57 · see citing works
Synaptotagmin-7 Functions to Replenish Insulin Granules for Exocytosis in Human Islet β-Cells
Dolai, S., Xie, L., Zhu, D., Liang, T., Qin, T., Xie, H., Kang, Y., Chapman, E. R., & Gaisano, H. Y. (2016) · Diabetes · doi:10.2337/db15-1436 · Cited by 55 · see citing works
Central presynaptic terminals are enriched in ATP but the majority lack mitochondria
Chavan, V., Willis, J., Walker, S. K., Clark, H. R., Liu, X., Fox, M. A., Srivastava, S., & Mukherjee, K. (2015) · PLoS ONE · doi:10.1371/journal.pone.0125185 · Cited by 52 · see citing works
Munc18b Is a Major Mediator of Insulin Exocytosis in Rat Pancreatic β-Cells
Lam, P. P. L., Ohno, M., Dolai, S., He, Y., Qin, T., Liang, T., Zhu, D., Kang, Y., Liu, Y., Kauppi, M., et al. (2013) · Diabetes · doi:10.2337/db12-1380 · Cited by 44 · see citing works
“Assembly of distinct SNARE complexes is regulated by cognate SM proteins to ensure subcellular compartmental specificity, and that fusion only occurs in response to cellular needs and demand (3,9).”
BackgroundBeta-amyloid short- and long-term synaptic entanglement
Lanni, C., Fagiani, F., Racchi, M., Preda, S., Pascale, A., Grilli, M., Allegri, N., & Govoni, S. (2019) · Pharmacological Research · doi:10.1016/j.phrs.2018.11.018 · Cited by 29 · see citing works
EHD1 is a synaptic protein that modulates exocytosis through binding to snapin
Wei, S., Xu, Y., Shi, H., Wong, S.-H., Han, W., Talbot, K., Hong, W., & Ong, W.-Y. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.07.014 · Cited by 22 · see citing works
Troup, M., Zalucki, O. H., Kottler, B. D., Karunanithi, S., Anggono, V., & van Swinderen, B. (2019) · Anesthesiology · doi:10.1097/aln.0000000000002850 · Cited by 21 · see citing works
Perić, I., Costina, V., Gass, P., Findeisen, P., & Filipović, D. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.11.013 · Cited by 18 · see citing works
Small, C., Harper, C., Jiang, A., Kontaxi, C., Pronot, M., Yak, N., Malapaka, A., Davenport, E. C., Wallis, T. P., Gormal, R. S., et al. (2024) · Journal of Neurochemistry · doi:10.1111/jnc.16186 · Cited by 14 · see citing works
Small, C., Harper, C., Jiang, A., Kontaxi, C., Yak, N., Malapaka, A., Davenport, E. C., Wallis, T. P., Gormal, R. S., Joensuu, M., et al. (2022) · doi:10.1101/2022.12.12.520075 · Cited by 4 · see citing works
- Authors
- Südhof, T. C., & Rothman, J. E.
- Affiliations
- Department of Cellular and Molecular Physiology, Stanford University, Palo Alto, CA 94304, USA.
- Yale University (US)
- ORCID
- Rothman, James E.
- Venue
- Science
- Published
- 2009-01-23
- Volume
- 323
- Issue
- 5913
- Pages
- 474-477
- ISSN
- 0036-8075 (ISSN-L)
- 1095-9203
- PMC
- PMC3736821
- OpenAlex
- W2024136850
- Cited by
- 2,027
- References
- 73
- Citations by year
- 2026: 64 · 2025: 64 · 2024: 76 · 2023: 115 · 2022: 114 · 2021: 105 · 2020: 107 · 2019: 112 · 2018: 113 · 2017: 129 · 2016: 112 · 2015: 140 · 2014: 121 · 2013: 160 · 2012: 150
- FWCI
- 12.50
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Science (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- National Institute of General Medical Sciences (R01GM071458)
- 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 › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- membrane fusion, SNARE proteins, Sm proteins, trans-SNARE complex, synaptic vesicle exocytosis, synaptotagmin, complexin, calcium sensor, neurotransmitter release, vesicle targeting
- MeSH terms
- Animals, Membrane Fusion, Nerve Tissue Proteins, Synaptic Transmission, Protein Binding, Protein Conformation, Synapses, Synaptic Vesicles, Protein Structure, Tertiary, Amino Acid Motifs, Protein Structure, Quaternary, Vesicular Transport Proteins, SNARE Proteins, Qa-SNARE Proteins, Synaptotagmins, Munc18 Proteins
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review