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SNARE-complex disassembly by NSF follows synaptic-vesicle fusion
Open accessAbstract
Soluble N- ethylmaleimide-sensitive fusion attachment protein receptor (SNARE)-mediated fusion of synaptic vesicles with the presynaptic-plasma membrane is essential for communication between neurons. Disassembly of the SNARE complex requires the ATPase N -ethylmaleimide-sensitive fusion protein (NSF). To determine where in the synaptic-vesicle cycle NSF functions, we have undertaken a genetic analysis of comatose (dNSF-1) in Drosophila . Characterization of 16 comatose mutations demonstrates that NSF mediates disassembly of SNARE complexes after synaptic-vesicle fusion. Hypomorphic mutations in NSF cause temperature-sensitive paralysis, whereas null mutations result in lethality. Genetic-interaction studies with para demonstrate that blocking evoked fusion delays the accumulation of assembled SNARE complexes and behavioral paralysis that normally occurs in comatose mutants, indicating NSF activity is not required in the absence of vesicle fusion. In addition, the entire vesicle pool can be depleted in shibire comatose double mutants, demonstrating that NSF activity is not required for the fusion step itself. Multiple rounds of vesicle fusion in the absence of NSF activity poisons neurotransmission by trapping SNAREs into cis-complexes. These data indicate that NSF normally dissociates and recycles SNARE proteins during the interval between exocytosis and endocytosis. In the absence of NSF activity, there are sufficient fusion-competent SNAREs to exocytose both the readily released and the reserve pool of synaptic vesicles.
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“Finally, the SNARE complex is disassembled in an ATP-dependent reaction catalyzed by NSF, allowing recycling of the SNARE proteins (398).”
From Pancreatic β-Cell Electrical Activity and Insulin Secretion: Of Mice and Men (2018) · cites this paper as [398]
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Cites
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
Mirnics, K., Middleton, F. A., Marquez, A., Lewis, D. A., & Levitt, P. (2000) · Neuron · doi:10.1016/s0896-6273(00)00085-4 · Cited by 882
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
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
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
Molecular analysis of the para locus, a sodium channel gene in Drosophila
Loughney, K., Kreber, R. A., & Ganetzky, B. (1989) · Cell · doi:10.1016/0092-8674(89)90512-6 · Cited by 507
Self-citationKoenig, J. H., & Ikeda, K. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-11-03844.1989 · Cited by 448
SNARE Complex Formation Is Triggered by Ca 2+ and Drives Membrane Fusion
Chen, Y. A., Scales, S. J., Patel, S. M., Doung, Y.-C., & Scheller, R. H. (1999) · Cell · doi:10.1016/s0092-8674(00)80727-8 · Cited by 417
Structure of the AAA ATPase p97
Zhang, X., Shaw, A., Bates, P. A., Newman, R., Gowen, B. E., Orlova, E. V., Gorman, M. A., Kondo, H., Dokurno, P., Lally, J., et al. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00143-x · Cited by 416
Whiteheart, S. W., Rossnagel, K., Buhrow, S. A., Brunner, M., Jaenicke, R., & Rothman, J. E. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.126.4.945 · Cited by 393
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Sorted by citations
AAA+ proteins: have engine, will work
Hanson, P. I., & Whiteheart, S. W. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1684 · Cited by 1,210
Burgoyne, R. D., & Morgan, A. (2003) · Physiological Reviews · doi:10.1152/physrev.00031.2002 · Cited by 934
“Analysis of comatose mutants has proven controversial, with different groups concluding both pre- and postfusion actions of NSF (376, 435, 436, 771).”
BackgroundPancreatic 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
Snares and Munc18 in synaptic vesicle fusion
Rizo, J., & Südhof, T. C. (2002) · Nature Reviews Neuroscience · doi:10.1038/nrn898 · Cited by 539
“, and indicated that this activity follows synaptic vesicle fusio”
BackgroundSynaptic vesicle recycling: steps and principles
Rizzoli, S. O. (2014) · The EMBO Journal · doi:10.1002/embj.201386357 · Cited by 317
“Blocking NSF activity, as in the Drosophila comatose mutant (Kawasaki et al , 1998; Littleton et al , 2001), results in a relatively rapid inhibition of synaptic release.”
Lipid Rafts and the Regulation of Exocytosis
Salaün, C., James, D. J., & Chamberlain, L. H. (2004) · Traffic · doi:10.1111/j.1600-0854.2004.0162.x · Cited by 301
“Following membrane fusion, the ATPase NSF is recruited to the cis-SNARE complex by the adapter protein a/bSNAP (21).”
BackgroundLRRK2 Controls Synaptic Vesicle Storage and Mobilization within the Recycling Pool
Piccoli, G., Condliffe, S. B., Bauer, M., Giesert, F., Boldt, K., Astis, S. D., Meixner, A., Sarioglu, H., Weisenhorn, D. M. V., Wurst, W., et al. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3730-10.2011 · Cited by 282
The schizophrenia risk gene product miR-137 alters presynaptic plasticity
Siegert, S., Seo, J., Kwon, E. J., Rudenko, A., Cho, S., Wang, W., Flood, Z., Martorell, A. J., Ericsson, M., Mungenast, A. E., et al. (2015) · Nature Neuroscience · doi:10.1038/nn.4023 · Cited by 221
“Syt1 and Nsf were reported to be involved in vesicle recycling 39–41 .”
BackgroundFraldi, A., Annunziata, F., Lombardi, A., Kaiser, H., Medina, D. L., Spampanato, C., Fedele, A. O., Polishchuk, R., Sorrentino, N. C., Simons, K., et al. (2010) · The EMBO Journal · doi:10.1038/emboj.2010.237 · Cited by 225
Membrane traffic in the secretory pathway
Malsam, J., Kreye, S., & Söllner, T. H. (2008) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-008-8352-3 · Cited by 216
Transmission, Development, and Plasticity of Synapses
Harris, K. P., & Littleton, J. T. (2015) · Genetics · doi:10.1534/genetics.115.176529 · Cited by 201
“Genetic interaction experiments support the idea that the BLOC-1 components Snapin and Blos-1 cooperate with Dysb to mediate homeostatic plasticity in Drosophila (Dickman et al. 2012; Mullin et al. 2015), and like Dysb, Snapin localizes to SVs (Dickman et al. 2012).”
BackgroundInfluentialSelf-citationFUSION PORES AND FUSION MACHINES IN CA2+-TRIGGERED EXOCYTOSIS
Jackson, M. B., & Chapman, E. R. (2006) · Annual Review of Biophysics and Biomolecular Structure · doi:10.1146/annurev.biophys.35.040405.101958 · Cited by 182
Self-citationFormation, stabilisation and fusion of the readily releasable pool of secretory vesicles
S∅rensen, J. C. (2004) · Pflügers Archiv - European Journal of Physiology · doi:10.1007/s00424-004-1247-8 · Cited by 177
“A role for NSF/α-SNAP in dissociating cis-SNARE complexes after but not before fusion has been indicated by studies in Drosophila[ 66 ].”
ResultRegulated exocytosis and SNARE function (Review)
Söllner, T. H. (2003) · Molecular Membrane Biology · doi:10.1080/0968768031000104953 · Cited by 169
Distinct Initial SNARE Configurations Underlying the Diversity of Exocytosis
Kasai, H., Takahashi, N., & Tokumaru, H. (2012) · Physiological Reviews · doi:10.1152/physrev.00007.2012 · Cited by 150
“Munc13 proteins contain multiple domains including C2 domains Mouse synaptotagmin-1 (1-421)”
BackgroundPhagosome Maturation: A Few Bugs in the System
Scott, C. C., Botelho, R. J., & Grinstein, S. (2003) · The Journal of Membrane Biology · doi:10.1007/s00232-002-2008-2 · Cited by 138
“After fusion, SNAREpins are disassembled by NSF, a hexameric chaperone ATPase, and can then be recycled for another round of fusion (Sollner et al., 1993; Swanton et al., 2000; Littleton et al., 2001).”
Functions of SNAREs in intracellular membrane fusion and lipid bilayer mixing
Ungermann, C., & Langosch, D. (2005) · Journal of Cell Science · doi:10.1242/jcs.02561 · Cited by 139
“Interestingly, blocking the disassembly of SNAREs also interferes with vesicle budding, which suggests that the fusion and fission reactions are coupled (Littleton et al., 2001; Deak et al., 2004).”
The molecular machinery of synaptic vesicle exocytosis
Li, L., & Chin, L. (2003) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-003-2240-7 · Cited by 129
The Neuroproteomics of Schizophrenia
English, J. A., Pennington, K., Dunn, M. J., & Cotter, D. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.031 · Cited by 127
Phosphorylation of SNAP-23 Regulates Exocytosis from Mast Cells
Hepp, R., Puri, N., Hohenstein, A. C., Crawford, G. L., Whiteheart, S. W., & Roche, P. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m412126200 · Cited by 125
Transcellular spreading of huntingtin aggregates in the Drosophila brain
Babcock, D. T., & Ganetzky, B. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1516217112 · Cited by 129
Self-citationCalmodulin and lipid binding to synaptobrevin regulates calcium‐dependent exocytosis
Quetglas, S., Iborra, C., Sasakawa, N., Haro, L. D., Kumakura, K., Sato, K., Leveque, C., & SEAGAR, M. J. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf404 · Cited by 120
SNARE regulators: matchmakers and matchbreakers
Gerst, J. E. (2003) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(03)00096-x · Cited by 116
“This is typified by the Drosophila NSF mutant, comatose, which shows a reduction in neurotransmitter release and an accumulation of synaptic vesicles and SNARE complexes at restrictive temperatures [88].”
BackgroundRancour, D. M., Dickey-Sims, C., Park, S., & Bednarek, S. Y. (2002) · PLANT PHYSIOLOGY · doi:10.1104/pp.011742 · Cited by 116
“KNOLLE is a cell plate-associated t-SNARE required for cell plate formation (Lukowitz et al., 1996; Lauber et al., 1997).”
BackgroundResultConflicting Views on the Membrane Fusion Machinery and the Fusion Pore
Sørensen, J. B. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.24.110707.175239 · Cited by 113
The synaptic vesicle cycle: exocytosis and endocytosis in Drosophila and C. elegans
Richmond, J. E., & Broadie, K. S. (2002) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(02)00360-4 · Cited by 108
Roles of ATP in Depletion and Replenishment of the Releasable Pool of Synaptic Vesicles
Heidelberger, R., Sterling, P., & Matthews, G. (2002) · Journal of Neurophysiology · doi:10.1152/jn.2002.88.1.98 · Cited by 99
Presynaptic N-type Calcium Channels Regulate Synaptic Growth
Rieckhof, G. E., Yoshihara, M., Guan, Z., & Littleton, J. T. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m306417200 · Cited by 89
Self-citationSNAP-29-mediated Modulation of Synaptic Transmission in CulturedHippocampalNeurons
Pan, P., Cai, Q., Lin, L., Lu, P., Duan, S., & Sheng, Z. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m502356200 · Cited by 89
SNARE Protein Recycling by αSNAP and βSNAP Supports Synaptic Vesicle Priming
Burgalossi, A., Jung, S., Meyer, G., Jockusch, W. J., Jahn, O., Taschenberger, H., O'Connor, V. M., Nishiki, T., Takahashi, M., Brose, N., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.09.019 · Cited by 89
Bademosi, A. T., Lauwers, E., Padmanabhan, P., Odierna, G. L., Chai, Y. J., Papadopulos, A., Goodhill, G. J., Verstreken, P., van Swinderen, B., & Meunier, F. A. (2016) · Nature Communications · doi:10.1038/ncomms13660 · Cited by 87
Bayless, A. M., Zapotocny, R. W., Grunwald, D. J., Amundson, K. K., Diers, B. W., & Bent, A. F. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1717070115 · Cited by 73
“Such conditionally functional NSF mutants are known in the laboratoryderived Drosophila NSF comatose mutants, whereby the NSF-1 protein encoded by the comatose allele supports SNARE complex disassembly at room temperature but is nonfunctional at elevated temperatures, leading to failure of synaptic vesicle transport a…”
BackgroundSNARE Regulatory Proteins in Synaptic Vesicle Fusion and Recycling
Sauvola, C. W., & Littleton, J. T. (2021) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2021.733138 · Cited by 69
Self-citationThe nature of the phagosomal membrane: endoplasmic reticulum versus plasmalemma
Touret, N., Paroutis, P., & Grinstein, S. (2005) · Journal of Leukocyte Biology · doi:10.1189/jlb.1104630 · Cited by 67
“After fusion, NSF, a hexameric chaperone ATPase, disassembles SNAREpins so that the individual components can be recycled for another round of fusion [19–21].”
BackgroundLoss of SNAP29 Impairs Endocytic Recycling and Cell Motility
Rapaport, D., Lugassy, Y., Sprecher, E., & Horowitz, M. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009759 · Cited by 65
“. The stable cis-SNARE core complex is subsequently dissociated by the action of α-SNAP and the ATPase N-ethylmaleimide-sensitive factor (NSF)”
BackgroundCholesterol, regulated exocytosis and the physiological fusion machine
Churchward, M. A., & Coorssen, J. R. (2009) · Biochemical Journal · doi:10.1042/bj20090969 · Cited by 62
Randhawa, V. K., Thong, F. S. L., Lim, D. Y., Li, D., Garg, R. R., Rudge, R. E., Galli, T., Rudich, A., & Klip, A. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-03-0266 · Cited by 63
“Cis-SNARE complexes (i.e., on the same membrane) also exist and must be disassembled to allow for trans-SNARE complex formation (Littleton et al., 2001).”
α-SNAP and NSF are required in a priming step during the human sperm acrosome reaction
Tomes, C. N., Blas, G. A. D., Michaut, M. A., Farré, E. V., Cherhitin, O., Visconti, P. E., & Mayorga, L. S. (2004) · Molecular Human Reproduction · doi:10.1093/molehr/gah126 · Cited by 62
Requirements for the catalytic cycle of the N-ethylmaleimide-Sensitive Factor (NSF)
Zhao, C., Smith, E. C., & Whiteheart, S. W. (2011) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2011.06.003 · Cited by 64
Bombardier, J. P., & Munson, M. (2015) · Current Opinion in Chemical Biology · doi:10.1016/j.cbpa.2015.10.003 · Cited by 62
“Disassembly regulation and moonlighting functions of the machinery The requirement for a-SNAP/NSF in SNARE disassembly has been known for decades [46,47], but recent evidence suggests that their involvement in membrane fusion might be more complicated than originally proposed.”
Lagow, R. D., Bao, H., Cohen, E. N., Daniels, R. W., Zuzek, A., Williams, W. H., Macleod, G. T., Sutton, R. B., & Zhang, B. (2007) · PLoS Biology · doi:10.1371/journal.pbio.0050072 · Cited by 61
“dysfunction of NSF at restrictive temperatures [10–12].”
BackgroundWang, P., Saraswati, S., Guan, Z., Watkins, C. J., Wurtman, R. J., & Littleton, J. T. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0542-04.2004 · Cited by 59
“In contrast, SNARE com- plexes normally found in wild-type animals are reduced in shi mutants, in which the block in vesicle endocytosis eliminates vesicle fusion and subsequent SNARE complex formation (Littleton et al., 2001).”
BackgroundResultInfluentialSelf-citationResolving kinetic intermediates during the regulated assembly and disassembly of fusion pores
Das, D., Bao, H., Courtney, K. C., Wu, L., & Chapman, E. R. (2020) · Nature Communications · doi:10.1038/s41467-019-14072-7 · Cited by 57
Self-citationPresynaptic Frequency- and Pattern-Dependent Filtering
Thomson, A. M. (2003) · Journal of Computational Neuroscience · doi:10.1023/a:1025812808362 · Cited by 56
“However, a study of NSF mutations in Drosophila suggests that hydrolysis of ATP by NSF, disassembly of the core complex and release of the monomers may only be required once per release cycle, after fusion (Littleton et al., 2001).”
InfluentialThe presynaptic CaV2.2 channel–transmitter release site core complex
Khanna, R., Li, Q., Bewersdorf, J., & Stanley, E. F. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05680.x · Cited by 56
“Both of these proteins play important roles in the vesicular fusion cycle: NSF is essential for SNARE complex disassembly (Barnard et al., 1997; Littleton et al., 2001) while the syntaxin 1-binding protein Munc18 is critical for normal transmitter secretion (Verhage et al., 2000).”
BackgroundWang, Y., Vachon, E., Zhang, J., Cherepanov, V., Kruger, J., Li, J., Saito, K., Shannon, P. T., Bottini, N., Huynh, H., et al. (2005) · The Journal of Experimental Medicine · doi:10.1084/jem.20051108 · Cited by 54
γ-Oryzanol Improves Cognitive Function and Modulates Hippocampal Proteome in Mice
Rungratanawanich, W., Cenini, G., Mastinu, A., Sylvester, M., Wilkening, A., Abate, G., Bonini, S. A., Aria, F., Marziano, M., Maccarinelli, G., et al. (2019) · Nutrients · doi:10.3390/nu11040753 · Cited by 52
t‐SNAREs bind the Rhg1 α‐SNAP and mediate soybean cyst nematode resistance
Jia, D., Zielinski, R. E., & Hudson, M. E. (2020) · The Plant Journal · doi:10.1111/tpj.14923 · Cited by 53
A Novel Site of Action for α-SNAP in the SNARE Conformational Cycle Controlling Membrane Fusion
Barszczewski, M. M., Chua, J. J. E., Stein, A., Winter, U., Heintzmann, R., Zilly, F. E., Fasshauer, D., Lang, T., & Jahn, R. (2007) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-05-0498 · Cited by 51
“Impairment or loss of either protein leads to a general inhibition of membrane traffic, which is associated with an accumulation of SNARE complexes and ultimately leads to cell death (Novick et al., 1980; Barnard et al., 1997; Ungermann et al., 1998; Littleton et al., 2001; Hanley et al., 2002).”
BackgroundKuner, T., Li, Y., Gee, K. R., Bonewald, L. F., & Augustine, G. J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0707197105 · Cited by 46
Pongrac, J. L., Slack, P., & Innis, S. M. (2007) · Journal of Nutrition · doi:10.1093/jn/137.8.1852 · Cited by 45
Cellular bases of activity‐dependent paralysis in Drosophila stress‐sensitive mutants
Trotta, N., Rodesch, C. K., Fergestad, T., & Broadie, K. S. (2004) · Journal of Neurobiology · doi:10.1002/neu.20017 · Cited by 42
Kubista, H., Edelbauer, H., & Boehm, S. (2004) · Journal of Cell Science · doi:10.1242/jcs.00941 · Cited by 40
“Bulk chemicals were from Sigma (Vienna, Austria) and BIOMOL (Plymouth Meeting, PA).”
BackgroundMethodInfluentialMembrane repair and immunological danger
Andrews, N. W. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400505 · Cited by 38
“ATP depletion inhibits Ca2+-triggered lysosomal exocytosis (Rodriguez et al, 1997), which is expected given the requirement for the hexameric ATPase N-ethylmaleimide-sensitive factor (NSF) in all intracellular membrane-fusion events (Littleton et al, 2001).”
BackgroundMembrane Trafficking in Protozoa
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Mohrmann, R., & Sørensen, J. B. (2012) · Journal of Molecular Neuroscience · doi:10.1007/s12031-012-9744-2 · Cited by 36
Rikhy, R., Ramaswami, M., & Krishnan, K. S. (2003) · Genetics · doi:10.1093/genetics/165.3.1243 · Cited by 35
Dominant‐negative NSF2 disrupts the structure and function of drosophila neuromuscular synapses
Stewart, B. A., Mohtashami, M., Rivlin, P. K., Deitcher, D. L., Trimble, W. S., & Boulianne, G. L. (2002) · Journal of Neurobiology · doi:10.1002/neu.10059 · Cited by 33
Sangwan, V., Abella, J. V., Lai, A. Z., Bertos, N., Stuible, M., Tremblay, M. L., & Park, M. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.270934 · Cited by 37
Wu, K., Li, S., Bodhinathan, K., Meyers, C., Chen, W., Campbell‐Thompson, M., McIntyre, L. M., Foster, T. C., Muzyczka, N., & Kumar, A. (2011) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2011.09.006 · Cited by 32
Synchronous intra-Golgi transport induces the release of Ca2+ from the Golgi apparatus
Micaroni, M., Perinetti, G., Giandomenico, D. D., Bianchi, K., Spaar, A., & Aa, M. (2010) · Experimental Cell Research · doi:10.1016/j.yexcr.2010.04.024 · Cited by 32
Molecular Aspects of Membrane Trafficking in Paramecium
Plattner, H., & Kissmehl, R. (2003) · International review of cytology · doi:10.1016/s0074-7696(03)32005-4 · Cited by 32
“NSF is an AAA-type ATPase (Neuwald et al., 1999), which is released upon ATP hydrolysis (Littleton et al., 2001).”
BackgroundInherited Isolated Dystonia: Clinical Genetics and Gene Function
Dauer, W. T. (2014) · Neurotherapeutics · doi:10.1007/s13311-014-0297-7 · Cited by 28
Wu, Z., & Chao, C. C. ‐. (2010) · Biochemical Pharmacology · doi:10.1016/j.bcp.2010.05.026 · Cited by 28
Wu, Z., Sun, N., Chien, K., & Chao, C. C. ‐. (2011) · Biochemical Pharmacology · doi:10.1016/j.bcp.2011.08.018 · Cited by 27
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Self-citationNguyen, T. H., Vicidomini, R., Choudhury, S. D., Han, T. H., Maric, D., Brody, T., & Serpe, M. (2024) · Developmental Cell · doi:10.1016/j.devcel.2024.03.016 · Cited by 24
de Paola, M., Bello, O. D., & Michaut, M. A. (2015) · PLoS ONE · doi:10.1371/journal.pone.0135679 · Cited by 25
Kerr, D. J., Marsillo, A., Guariglia, S. R., Budylin, T., Sadek, R., Menkes, S., Chauhan, A., Wen, G. Y., McCloskey, D. P., Wieraszko, A., et al. (2016) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2016.06.005 · Cited by 27
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BackgroundMendes, A. K. B., Sulis, P. M., Cavalari, F. C., Rey, D. P., Aragón, M., Gaspar, J. M., & Silva, F. R. M. B. (2021) · The Journal of Nutritional Biochemistry · doi:10.1016/j.jnutbio.2021.108864 · Cited by 27
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Yu, W., Kawasaki, F., & Ordway, R. W. (2011) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2011.02.002 · Cited by 23
“…role in synaptic vesicle trafficking and neurotransmitter release (Kawasaki et al., 1998; Kawasaki and Ordway, 1999; Kawasaki and Ordway, 2009; Littleton et al., 2001; Pallanck et al., 1995; Tolar and Pallanck, 1998). dNSF1 is thought to disassemble plasma membrane SNARE complexes (presumably…”
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Somasundaram, A., & Taraska, J. W. (2018) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-12-0716 · Cited by 23
Li, T., Tian, Y., Li, Q., Chen, H., Lv, H., Xie, W., & Han, J. (2015) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.644583 · Cited by 24
“NSF is known to mediate SNARE complex disassembly (42, 43).”
BackgroundActivation of Store-operated Calcium Channels
Scott, C. C., Furuya, W., Trimble, W. S., & Grinstein, S. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m304718200 · Cited by 22
Expression of the exocytotic protein syntaxin in mouse oocytes
Iwahashi, K., Kuji, N., Fujiwara, T., Tanaka, H., Takahashi, J., Inagaki, N., Komatsu, S., Yamamoto, A., Yoshimura, Y., & Akagawa, K. (2003) · Reproduction · doi:10.1530/rep.0.1260073 · Cited by 20
Molecular cross-talk in a unique parasitoid manipulation strategy
Kaiser, M., Arvidson, R. S., Zarivach, R., Adams, M. E., & Libersat, F. (2018) · Insect Biochemistry and Molecular Biology · doi:10.1016/j.ibmb.2018.11.009 · Cited by 18
Candidate pathway association study in cocaine dependence: The control of neurotransmitter release
Noèlia Fernàndez-castillo, A., Cormand, B., Roncero, C., Sánchez‐Mora, C., Grau‐López, L., Gonzalvo, B., Miquel, L., Corominas, R., Ramos‐Quiroga, J. A., Casas, M., et al. (2011) · The World Journal of Biological Psychiatry · doi:10.3109/15622975.2010.551406 · Cited by 18
A Neuroprotective Function of NSF1 Sustains Autophagy and Lysosomal Trafficking inDrosophila
Babcock, D. T., Shen, W., & Ganetzky, B. (2014) · Genetics · doi:10.1534/genetics.114.172403 · Cited by 18
Self-citationTemperature-sensitive paralytic mutants: insights into the synaptic vesicle cycle
Vijayakrishnan, N., & Broadie, K. S. (2006) · Biochemical Society Transactions · doi:10.1042/bst0340081 · Cited by 18
Plattner, H. (2010) · Protist · doi:10.1016/j.protis.2010.05.001 · Cited by 17
“2001) engaged in disentangling SNAREs after fusion (Littleton et al. 2001) and/or in arranging them into a fusogenic complex (Ungermann and Langosch 2005).”
BackgroundBar-On, D., Gutman, M., Mezer, A., Ashery, U., Lang, T., & Nachliel, E. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.0710-09.2009 · Cited by 17
“The availability of the SNARE proteins for trans-SNARE complex formation depends on keeping the SNARE proteins in a reactive state (Littleton et al., 2001; Sanyal et al., 2001) and therefore might be impeded by the accumulation of cis-SNARE complex on the PM.”
BackgroundAnalysis of NSF Mutants Reveals Residues Involved in SNAP Binding and ATPase Stimulation
Horsnell, W. G. C., Steel, G. J., & Morgan, A. (2002) · Biochemistry · doi:10.1021/bi0160359 · Cited by 17
Qin, R., Ma, J., He, F., & Qin, W. (2025) · Cell Discovery · doi:10.1038/s41421-024-00764-y · Cited by 17
“For another example, vesicle-fusing ATPase (NSF) and alpha-soluble NSF attachment protein (NAPA) were reported to form a functional protein complex involved in intracellular vesicle traf fi cking processes, particularly membrane fusion events 46 .”
The Amyloid Precursor Protein—A Novel Player within the Molecular Array of Presynaptic Nanomachines
Laßek, M., Weingarten, J., Wegner, M., & Volknandt, W. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2015.00021 · Cited by 15
“After neurotransmitter release, the assembler NSF mediates the hydrolysis of ATP and triggers the disassembling of the SNARE nanomachine (Littleton et al., 2001).”
BackgroundMinimum Essential Factors Required for Vesicle Mobilization at Hippocampal Synapses
Mozhayeva, M. G., Matos, M. F., Liu, X., & Kavalali, E. T. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3801-03.2004 · Cited by 15
The role of synaptic protein NSF in the development and progression of neurological diseases
Yang, J., Kong, L., Zou, L. B., & Liu, Y. (2024) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1395294 · Cited by 15
“Moreover, NSF’s ATPase activity is pivotal for the disassembly of SNARE complexes post-fusion, allowing for their recycling and the continuation of vesicular transport (Littleton et al., 2001).”
BackgroundA Highly Polymorphic Copy Number Variant in the NSF Gene is Associated with Cocaine Dependence
Cabana‐Domínguez, J., Roncero, C., Grau‐López, L., Rodríguez-Cintas, L., Barral, C., Abad, A. C., Erikson, G. A., Wineinger, N. E., Torrico, B., Arenas, C., et al. (2016) · Scientific Reports · doi:10.1038/srep31033 · Cited by 14
Mécanisme de la fusion membranaire
Galli, T., Martı́nez-Arca, S., & Paumet, F. (2002) · Érudit (Université de Montréal) · doi:10.7202/000468ar · Cited by 14
Mécanisme de la fusion membranaire
Galli, T., Martínez-Arca, S., & Paumet, F. (2002) · médecine/sciences · doi:10.1051/medsci/200218111113 · Cited by 18
The ubiquitin ligase Ariadne-1 regulates neurotransmitter release via ubiquitination of NSF
Ramírez, J., Morales, M., Osinalde, N., Martínez-Padrón, I., Mayor, U., & Ferrús, A. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.100408 · Cited by 12
“Opposite to the role of NSF mutant com, which impairs SNARE complex disassembly (55), a change that enhances NSF functionality due to the lack of its ubiquitination would favor the dissociation of the so-called trans-SNARE complex.”
BackgroundTechniques to Dissect Cellular and Subcellular Function in the Drosophila Nervous System
Matthies, H. J. G., & Broadie, K. S. (2003) · Methods in cell biology · doi:10.1016/s0091-679x(03)01011-2 · Cited by 11
SNARE Proteins in Synaptic Vesicle Fusion
Palfreyman, M. T., West, S. E., & Jørgensen, E. M. (2023) · Advances in neurobiology · doi:10.1007/978-3-031-34229-5_4 · Cited by 10
Mechanism of Ethanol-Induced Insulin Secretion from INS-1 and INS-1E Tumor Cell Lines
Hafko, R., Orečná, M., Bačová, Z., Kolláriková, G., Lacı́k, I., & Štrbák, V. (2009) · Cellular Physiology and Biochemistry · doi:10.1159/000257482 · Cited by 9
Gray, L. J., Scarr, E., & Dean, B. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.08.051 · Cited by 9
Fan, J., Zhou, X., Wang, Y., Kuang, C., Sun, Y., Liu, X., Toomre, D. K., & Xu, Y. (2016) · FEBS Letters · doi:10.1002/1873-3468.12532 · Cited by 8
SNARE Protein Recycling by αSNAP and βSNAP Supports Synaptic Vesicle Priming
Burgalossi, A., Jung, S., Meyer, G., Jockusch, W. J., Jahn, O., Taschenberger, H., O'Connor, V. M., Nishiki, T., Takahashi, M., Brose, N., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.01.015 · Cited by 8
Bačová, Z., Orečná, M., Hafko, R., & Štrbák, V. (2007) · Cellular Physiology and Biochemistry · doi:10.1159/000107523 · Cited by 8
Patel, A. O., Caldwell, A. B., Ramachandran, S., & Subramaniam, S. (2023) · Journal of Alzheimer s Disease Reports · doi:10.3233/adr-220098 · Cited by 7
“Notsurprisingly,M1,M3,andM4 werefoundtobeassociatedwithneuronfunction ( NSF , NELL2 , SNAP91 ), dedifferentiation or neuronal precursor-like cell state ( NOTCH2 , ZIC2 ), and energetics ( TOMM20 , ATP5MC3 , ATP5F1A ) (Sup-A plementary Figure 2A, C, D) [45–51].”
Metadata
- Authors
- Littleton, J. T., Barnard, R. J. O., Titus, S. A., Slind, J., Chapman, E. R., & Ganetzky, B.
- Affiliations
- University of Wisconsin–Madison (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-10-02
- Volume
- 98
- Issue
- 21
- Pages
- 12233-12238
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC59797
- OpenAlex
- W2050959850
- Semantic Scholar
- 3803066e22350667cb97543a655caa7de6fa97c4
- Cited by
- 140
- References
- 43
- Citations by year
- 2026: 4 · 2025: 3 · 2024: 2 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 3 · 2019: 3 · 2018: 3 · 2017: 2 · 2016: 6 · 2015: 11 · 2014: 7 · 2012: 4
- FWCI
- 3.63
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (5r01gm043100-07, NS40296)
- National Institute of General Medical Sciences (R01GM056827, GM56827-01, GM43100)
- National Institute of Neurological Disorders and Stroke (NS15390, R01NS040296, NS40296-01, R01NS015390)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
- Keywords
- NSF, SNARE complex disassembly, synaptic vesicle fusion, synaptic vesicle recycling, Pará, shibire, neurotransmission, exocytosis, endocytosis, reserve pool, Drosophila
- MeSH terms
- Alleles, Animals, Carrier Proteins, Drosophila melanogaster, Female, Male, Membrane Fusion, Membrane Proteins, Synaptic Vesicles, Mutagenesis, Vesicular Transport Proteins, SNARE Proteins, N-Ethylmaleimide-Sensitive Proteins
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