The DOI matches its Crossref record; 43 of the 43 references it cites were found in a registry or an index.
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.
Overview
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
Verification
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?
The cited source says what the claim attributes to it.
In the citing paper
“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]
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
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
Rapid Reuse of Readily Releasable Pool Vesicles at Hippocampal Synapses
Pyle, J. L., Kavalali, E. T., Piedras-Renterı́a, E. S., & Tsien, R. W. (2000) · Neuron · doi:10.1016/s0896-6273(00)00098-2 · Cited by 345
Inhibition of SNARE Complex Assembly Differentially Affects Kinetic Components of Exocytosis
Xu, T., Rammner, B., Margittai, M., Artalejo, A. R., Neher, E., & Jahn, R. (1999) · Cell · doi:10.1016/s0092-8674(00)81669-4 · Cited by 320
Crystal Structure of the Hexamerization Domain of N-ethylmaleimide–Sensitive Fusion Protein
Lenzen, C. U., Steinmann, D., Whiteheart, S. W., & Weis, W. I. (1998) · Cell · doi:10.1016/s0092-8674(00)81593-7 · Cited by 312
Beckers, C. J., Block, M. R., Glick, B. S., Rothman, J. E., & Balch, W. E. (1989) · Nature · doi:10.1038/339397a0 · Cited by 291
Littleton, J. T., Chapman, E. R., Kreber, R. A., Garment, M. B., Carlson, S. D., & Ganetzky, B. (1998) · Neuron · doi:10.1016/s0896-6273(00)80549-8 · Cited by 211
Self-citationBanerjee, A., Barry, V. A., DasGupta, B. R., & Martin, T. F. J. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.34.20223 · Cited by 205
Ordering the Final Events in Yeast Exocytosis
Grote, E., Carr, C. M., & Novick, P. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.151.2.439 · Cited by 181
Barnard, R. J. O., Morgan, A., & Burgoyne, R. D. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.4.875 · Cited by 178
Self-citationDomain structure of an N-ethylmaleimide-sensitive fusion protein involved in vesicular transport.
Tagaya, M., Wilson, D. W., Brunner, M., Arango, N., & Rothman, J. E. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53825-4 · Cited by 177
A Major Conformational Change in p97 AAA ATPase upon ATP Binding
Rouiller, I., Butel, V. M., Latterich, M., Milligan, R. A., & Kubalek, E. W. (2000) · Molecular Cell · doi:10.1016/s1097-2765(00)00144-1 · Cited by 153
Synaptic function modulated by changes in the ratio of synaptotagmin I and IV
Littleton, J. T., Serano, T. L., Rubin, G. M., Ganetzky, B., & Chapman, E. R. (1999) · Nature · doi:10.1038/23462 · Cited by 151
Self-citationSNAP-mediated protein–protein interactions essential for neurotransmitter release
DeBello, W. M., O'Connor, V. M., Dresbach, T., Whiteheart, S. W., Wang, S. S. ‐., Schweizer, F. E., Bertz, H., Rothman, J. E., & Augustine, G. J. (1995) · Nature · doi:10.1038/373626a0 · Cited by 143
Each Domain of the N-Ethylmaleimide-sensitive Fusion Protein Contributes to Its Transport Activity
Nagiec, E. E., Bernstein, A. M., & Whiteheart, S. W. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.49.29182 · Cited by 138
Arrangement of Subunits in 20 S Particles Consisting of NSF, SNAPs, and SNARE Complexes
Hohl, T. M., Parlati, F., Wimmer, C., Rothman, J. E., Söllner, T. H., & Engelhardt, H. (1998) · Molecular Cell · doi:10.1016/s1097-2765(00)80153-7 · Cited by 130
A six-stranded double-psi β barrel is shared by several protein superfamilies
Castillo, R. M., Mizuguchi, K., Dhanaraj, V., Albert, A., Blundell, T. L., & Murzin, A. G. (1999) · Structure · doi:10.1016/s0969-2126(99)80028-8 · Cited by 126
Tolar, L. A., & Pallanck, L. J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10250.1998 · Cited by 118
NSF N-Terminal Domain Crystal Structure
Yu, R. C., Jahn, R., & Brünger, A. T. (1999) · Molecular Cell · doi:10.1016/s1097-2765(00)80191-4 · Cited by 116
Synaptic transmission reversibly conditioned by single-gene mutation in Drosophila melanogaster
Ikeda, K., Ozawa, S., & Hagiwara, S. (1976) · Nature · doi:10.1038/259489a0 · Cited by 112
Pallanck, L. J., Ordway, R. W., & Ganetzky, B. (1995) · Nature · doi:10.1038/376025a0 · Cited by 111
Self-citationKawasaki, F., Mattiuz, A. M., & Ordway, R. W. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-24-10241.1998 · Cited by 96
Crystal structure of the amino-terminal domain of N-ethylmaleimide-sensitive fusion protein
May, A. P., Misura, K. M. S., Whiteheart, S. W., & Weis, W. I. (1999) · Nature Cell Biology · doi:10.1038/11097 · Cited by 92
Matveeva, E. A., He, P., & Whiteheart, S. W. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.42.26413 · Cited by 73
van de Goor, J., Ramaswami, M., & Kelly, R. B. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.12.5739 · Cited by 70
Neurally expressed Drosophila genes encoding homologs of the NSF and SNAP secretory proteins.
Ordway, R. W., Pallanck, L. J., & Ganetzky, B. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.12.5715 · Cited by 66
Self-citationBarnard, R. J., Morgan, A., & Burgoyne, R. D. (1996) · Molecular Biology of the Cell · doi:10.1091/mbc.7.5.693 · Cited by 56
Self-citationMüller, J. M. M., Rabouille, C., Newman, R., Shorter, J., Freemont, P. S., Schiavo, G., Warren, G., & Shima, D. T. (1999) · Nature Cell Biology · doi:10.1038/14025 · Cited by 56
Role of α-SNAP in Promoting Efficient Neurotransmission at the Crayfish Neuromuscular Junction
He, P., Southard, R. C., Chen, D., Whiteheart, S. W., & Cooper, R. L. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.6.3406 · Cited by 50
Crystal structure of the Sec18p N-terminal domain
Babor, S. M., & Fass, D. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.26.14759 · Cited by 39
Boulianne, G. L., & Trimble, W. S. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.15.7095 · Cited by 38
Golby, J. A., Tolar, L. A., & Pallanck, L. J. (2001) · Genetics · doi:10.1093/genetics/158.1.265 · Cited by 37
Steel, G. J., & Morgan, A. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)00072-6 · Cited by 29
TheDrosophilaNSF Protein, dNSF1, Plays a Similar Role at Neuromuscular and Some Central Synapses
Kawasaki, F., & Ordway, R. W. (1999) · Journal of Neurophysiology · doi:10.1152/jn.1999.82.1.123 · Cited by 23
Sanyal, S., Basole, A., & Krishnan, K. S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-24-j0005.1999 · Cited by 20
Flagged first, then by citations
Cited by
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.”
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
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
