Developmentally Regulated Switch in Alternatively Spliced SNAP-25 Isoforms Alters Facilitation of Synaptic Transmission
Open accessAbstract
Although the basic molecular components that promote regulated neurotransmitter release are well established, the contribution of these proteins as regulators of the plasticity of neurotransmission and refinement of synaptic connectivity during development is elaborated less fully. For example, during the period of synaptic growth and maturation in brain, the expression of synaptosomal protein 25 kDa (SNAP-25), a neuronal t-SNARE (soluble N-ethylmaleimide-sensitive factor attachment protein receptor) essential for action potential-dependent neuroexocytosis, is altered through alternative splicing of pre-mRNA transcripts. We addressed the role of the two splice-variant isoforms of SNAP-25 with a targeted mouse mutation that impairs the shift from SNAP-25a to SNAP-25b. Most of these mutant mice die between 3 and 5 weeks of age, which coincides with the time when SNAP-25b expression normally reaches mature levels in brain and synapse formation is essentially completed. The altered expression of these SNAP-25 isoforms influences short-term synaptic function by affecting facilitation but not the initial probability of release. This suggests that mechanisms controlling alternative splicing between SNAP-25 isoforms contribute to a molecular switch important for survival that helps to guide the transition from immature to mature synaptic connections, as well as synapse regrowth and remodeling after neural injury.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
SNAP25 isoforms show differences in the kinetics of synaptic vesicle release.
“that show differences in the kinetics of synaptic vesicle release138,139.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [139]
The SNAP25 gene uses mutually exclusive exons 5a and 5b to produce two alternative isoforms.
“the gene for the SNARE protein SNAP25 uses a pair of mutually exclusive exons (5a and 5b) to produce two alternative isoforms”
From The neurogenetics of alternative splicing (2016) · cites this paper as [139]
Cites
Short-Term Synaptic Plasticity
Zucker, R. S., & Regehr, W. G. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.092501.114547 · Cited by 5,068 · 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
Mansour, S. L., Thomas, K. R., & Capecchi, M. R. (1988) · Nature · doi:10.1038/336348a0 · Cited by 1,683 · see citing works
The role of calcium in neuromuscular facilitation
Katz, B., & Miledi, R. (1968) · The Journal of Physiology · doi:10.1113/jphysiol.1968.sp008469 · Cited by 1,347 · see citing works
Heterogeneity of release probability, facilitation, and depletion at central synapses
Dobrunz, L. E., & Stevens, C. F. (1997) · Neuron · doi:10.1016/s0896-6273(00)80338-4 · Cited by 1,183 · see citing works
SNARE-mediated membrane fusion
Chen, Y. A., & Scheller, R. H. (2001) · Nature Reviews Molecular Cell Biology · doi:10.1038/35052017 · Cited by 1,133 · see citing works
The release of neural transmitter substances
Katz, B. (1969) · Medical Entomology and Zoology · Cited by 1,114 · see citing works
Fasshauer, D., Sutton, R. B., Brünger, A. T., & Jahn, R. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.26.15781 · Cited by 1,055 · see citing works
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 · 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
Self-citationA genomic perspective on membrane compartment organization
Bock, J. B., Matern, H. T., Peden, A. A., & Scheller, R. H. (2001) · Nature · doi:10.1038/35057024 · Cited by 696 · 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
The probability of transmitter release at a mammalian central synapse
Hessler, N. A., Shirke, A. M., & Malinow, R. (1993) · Nature · doi:10.1038/366569a0 · Cited by 617 · see citing works
Nonuniform probability of glutamate release at a hippocampal synapse.
Rosenmund, C., Clements, J., & Westbrook, G. (1993) · Science · doi:10.1126/science.7901909 · Cited by 616 · see citing works
Functions of FGF signalling from the apical ectodermal ridge in limb development
Sun, X., Mariani, F. V., & Martin, G. (2002) · Nature · doi:10.1038/nature00902 · Cited by 581 · see citing works
Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis
Washbourne, P., Thompson, P. M., Carta, M., da Costa, E. T., Mathews, J. R., López‐Bendito, G., Molnár, Z., Bêcher, M. W., Valenzuela, C. F., Partridge, L. D., et al. (2001) · Nature Neuroscience · doi:10.1038/nn783 · Cited by 535 · see citing works
Self-citationTrumpp, A., Depew, M. J., Rubenstein, J. L. R., Bishop, J. M., & Martin, G. R. (1999) · Genes & Development · doi:10.1101/gad.13.23.3136 · Cited by 515 · see citing works
Facilitation and depression at single central synapses
Stevens, C. F., & Wang, Y. (1995) · Neuron · doi:10.1016/0896-6273(95)90223-6 · Cited by 502 · see citing works
Fgf8 signalling from the AER is essential for normal limb development
Lewandoski, M., Sun, X., & Martin, G. R. (2000) · Nature Genetics · doi:10.1038/82609 · Cited by 451 · see citing works
Conditional control of gene expression in the mouse
Lewandoski, M. (2001) · Nature reviews genetics · doi:10.1038/35093537 · Cited by 442 · see citing works
Inhibition of axonal growth by SNAP-25 antisense oligonucleotides in vitro and in vivo
Osen‐Sand, A., Catsicas, M., Staple, J. K., Jones, K. A., Ayala, G., Knowles, J., Grenningloh, G., & Catsicas, S. (1993) · Nature · doi:10.1038/364445a0 · Cited by 442 · see citing works
O’Gorman, S., Dagenais, N., Qian, M., & Marchuk, Y. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.26.14602 · Cited by 436 · see citing works
The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion
Geppert, M., Goda, Y., Stevens, C., & Südhof, T. (1997) · Nature · doi:10.1038/42954 · Cited by 422 · see citing works
Synapse elimination and indelible memory
Lichtman, J. W., & Colman, H. (2000) · Neuron · doi:10.1016/s0896-6273(00)80893-4 · Cited by 380 · see citing works
Differential Control of the Releasable Vesicle Pools by SNAP-25 Splice Variants and SNAP-23
Sørensen, J. B., Nagy, G., Varoqueaux, F., Nehring, R. B., Brose, N., Wilson, M. C., & Neher, E. (2003) · Cell · doi:10.1016/s0092-8674(03)00477-x · Cited by 364 · see citing works
Self-citationRavichandran, V., Chawla, A., & Roche, P. A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.23.13300 · Cited by 354 · see citing works
Mixed and Non-cognate SNARE Complexes
Fasshauer, D., Antonin, W., Margittai, M., Pabst, S., & Jahn, R. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.22.15440 · Cited by 316 · see citing works
SNARE Interactions Are Not Selective
Yang, B., Gonzalez, L. C., Prekeris, R., Steegmaier, M., Advani, R. J., & Scheller, R. H. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.9.5649 · Cited by 315 · see citing works
A conserved domain is present in different families of vesicular fusion proteins: A new superfamily
Weimbs, T., Low, S. H., Chapin, S. J., Mostov, K. E., Bücher, P., & Hofmann, K. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.7.3046 · Cited by 315 · see citing works
Hess, D. T., Slater, T., Wilson, M. C., & Skene, J. H. P. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-12-04634.1992 · Cited by 309 · see citing works
Self-citationDifferences in Left-Right Axis Pathways in Mouse and Chick: Functions of FGF8 and SHH
Meyers, E. N., & Martin, G. R. (1999) · Science · doi:10.1126/science.285.5426.403 · Cited by 304 · see citing works
Multiple palmitoylation of synaptotagmin and the t‐SNARE SNAP‐25
Veit, M., Söllner, T. H., & Rothman, J. E. (1996) · FEBS Letters · doi:10.1016/0014-5793(96)00362-6 · Cited by 251 · see citing works
Estradiol protects mesencephalic dopaminergic neurons from oxidative stress-induced neuronal death
Sawada, H., Ibi, M., Kihara, T., Urushitani, M., Akaike, A., & Shimohama, S. (1998) · Journal of Neuroscience Research · doi:10.1002/(sici)1097-4547(19981201)54:5 · Cited by 246 · see citing works
Bark, C., Hahn, K. M., Ryabinin, A. E., & Wilson, M. C. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.5.1510 · Cited by 236 · see citing works
Self-citationCommon and distinct fusion proteins in axonal growth and transmitter release
Osen‐Sand, A., Staple, J. K., Naldi, E., Schiavo, G., Rossetto, O., Petitpierre, S., Malgaroli, A., Montecucco, C., & Catsicas, S. (1996) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19960401)367:2 · Cited by 206 · see citing works
SNAP-25 Palmitoylation and Plasma Membrane Targeting Require a Functional Secretory Pathway
Gonzalo, S., & Linder, M. E. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.3.585 · Cited by 196 · see citing works
CaMKII?-cre transgene expression and recombination patterns in the mouse brain
Dragatsis, I., & Zeitlin, S. O. (2000) · genesis · doi:10.1002/(sici)1526-968x(200002)26:2 · Cited by 171 · see citing works
A Common Exocytotic Mechanism Mediates Axonal and Dendritic Outgrowth
Martı́nez-Arca, S., Coco, S., Mainguy, G., Schenk, U., Alberts, P., Bouillé, P., Mezzina, M., Prochiantz, A., Matteoli, M., Louvard, D., et al. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-11-03830.2001 · Cited by 164 · see citing works
Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25
Bark, C., & Wilson, M. C. (1994) · Gene · doi:10.1016/0378-1119(94)90773-0 · Cited by 146 · see citing works
Self-citationCharacterization of the Palmitoylation Domain of SNAP‐25
Lane, S. R., & Liu, Y. (1997) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1997.69051864.x · Cited by 124 · see citing works
SNAP-25 Is Targeted to the Plasma Membrane through a Novel Membrane-binding Domain
Gonzalo, S., Greentree, W. K., & Linder, M. E. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.30.21313 · Cited by 123 · see citing works
Bark, C. (1993) · Journal of Molecular Biology · doi:10.1006/jmbi.1993.1485 · Cited by 117 · see citing works
Self-citationSyndet is a novel SNAP-25 related protein expressed in many tissues
Wang, G., Witkin, J. W., Hao, G., Bankaitis, V. A., Scherer, P. E., & Baldini, G. (1997) · Journal of Cell Science · doi:10.1242/jcs.110.4.505 · Cited by 107 · see citing works
Washbourne, P., Cansino, V. V., MATHEWS, J. R., Graham, M. E., Burgoyne, R. D., & Wilson, M. C. (2001) · Biochemical Journal · doi:10.1042/0264-6021:3570625 · Cited by 102 · see citing works
Self-citationOlfactory receptor neurons express D2 dopamine receptors
Koster, N. L., Norman, A. B., Richtand, N. M., Nickell, W. T., Puché, A. C., Pixley, S. K., & Shipley, M. T. (1999) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(19990906)411:4 · Cited by 95 · see citing works
Self-citationGeddes, J. W., Hess, E., Hart, R. A., Kesslak, J. P., Cotman, C. W., & Wilson, M. C. (1990) · Neuroscience · doi:10.1016/0306-4522(90)90047-8 · Cited by 91 · see citing works
Self-citationMolnár, Z., López‐Bendito, G., Small, J. E., Partridge, L. D., Blakemore, C. B., & Wilson, M. C. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-23-10313.2002 · Cited by 90 · see citing works
Self-citationDifferential Expression of SNAP‐25 Isoforms and SNAP‐23 in the Adrenal Gland
Grant, N. J., Hepp, R., Krause, W., Aunis, D., OEHME, P., & Langley, K. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0720363.x · Cited by 56 · see citing works
Patanow, C. M., Day, J. R., & Billingsley, M. L. (1996) · Neuroscience · doi:10.1016/s0306-4522(96)00335-1 · Cited by 55 · see citing works
Gonelle‐Gispert, C., Halban, P. A., Niemann, H., PALMER, M., Catsicas, S., & Sadoul, K. (1999) · Biochemical Journal · doi:10.1042/bj3390159 · Cited by 45 · see citing works
Koticha, D. K., Huddleston, S. J., Witkin, J. W., & Baldini, G. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.13.9053 · Cited by 44 · see citing works
Morihara, T., Mizoguchi, A., Takahashi, M., Kozaki, S., Tsujihara, T., Kawano, S., Shirasu, M., Ohmukai, T., Kitada, M., Kimura, K., et al. (1999) · Neuroscience · doi:10.1016/s0306-4522(98)00671-x · Cited by 36 · see citing works
Complex gene organization of synaptic protein SNAP-25 in Drosophila melanogaster
Risinger, C., Deitcher, D. L., Lundell, I., Schwarz, T. L., & Larhammar, D. (1997) · Gene · doi:10.1016/s0378-1119(97)00106-6 · Cited by 27 · see citing works
Jacobsson, G., Piehl, F., Bark, C., Zhang, X., & Meister, B. (1996) · Molecular Brain Research · doi:10.1016/0169-328x(95)00272-t · Cited by 24 · see citing works
Self-citation
Flagged first, then by citations
1 of the 55 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
Pancreatic 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
Neuronal regulation of alternative pre-mRNA splicing
Li, Q., Lee, J.-A., & Black, D. L. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2237 · Cited by 376 · see citing works
Spine architecture and synaptic plasticity
Carlisle, H. J., & Kennedy, M. B. (2005) · Trends in Neurosciences · doi:10.1016/j.tins.2005.01.008 · Cited by 351 · see citing works
The neurogenetics of alternative splicing
Vuong, C. K., Black, D. L., & Zheng, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.27 · Cited by 340 · see citing works
Integrative Modeling Defines the Nova Splicing-Regulatory Network and Its Combinatorial Controls
Zhang, C., Frias, M. A., Mele, A., Ruggiu, M., Eom, T., Marney, C. B., Wang, H., Licatalosi, D. D., Fak, J. J., & Darnell, R. B. (2010) · Science · doi:10.1126/science.1191150 · Cited by 294 · see citing works
A spatially resolved brain region- and cell type-specific isoform atlas of the postnatal mouse brain
Joglekar, A., Prjibelski, A., Mahfouz, A., Collier, P., Lin, S., Schlusche, A. K., Marrocco, J., Williams, S. R., Haase, B., Hayes, A., et al. (2021) · Nature Communications · doi:10.1038/s41467-020-20343-5 · Cited by 229 · see citing works
Licatalosi, D. D., Yano, M., Fak, J. J., Mele, A., Grabinski, S. E., Zhang, C., & Darnell, R. B. (2012) · Genes & Development · doi:10.1101/gad.191338.112 · Cited by 193 · see citing works
Giudice, J., Xia, Z., Wang, E. T., Scavuzzo, M. A., Ward, A. J., Kalsotra, A., Wang, W., Wehrens, X. H. T., Burge, C. B., Li, W., et al. (2014) · Nature Communications · doi:10.1038/ncomms4603 · Cited by 161 · see citing works
Neuronal proteins custom designed by alternative splicing
Lipscombe, D. (2005) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2005.04.002 · Cited by 145 · see citing works
Lipid Raft Association of SNARE Proteins Regulates Exocytosis in PC12 Cells
Salaün, C., Gould, G. W., & Chamberlain, L. H. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m501923200 · Cited by 143 · see citing works
Differential Abilities of SNAP-25 Homologs to Support Neuronal Function
Delgado-Martínez, I., Nehring, R. B., & Sørensen, J. B. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.5092-06.2007 · Cited by 142 · see citing works
Jeans, A. F., Oliver, P. L., Johnson, R., Capogna, M., Vikman, J., Molnár, Z., Babbs, A., Partridge, C. J., Salehi, A. A., Bengtsson, M., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610222104 · Cited by 121 · see citing works
Expression and Function of SNAP-25 as a Universal SNARE Component in GABAergic Neurons
Tafoya, L. C. R., Mameli, M., Miyashita, T., Guzowski, J. F., Valenzuela, C. F., & Wilson, M. C. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.1866-06.2006 · Cited by 115 · see citing works
Self-citationPozzi, D., Condliffe, S. B., Bozzi, Y., Chikhladze, M., Grumelli, C., Proux‐Gillardeaux, V., Takahashi, M., Franceschetti, S., Verderio, C., & Matteoli, M. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706211105 · Cited by 111 · see citing works
Chen, L., Yamada, K., Nabeshima, T., & Sokabe, M. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2005.09.018 · Cited by 109 · see citing works
Étain, B., Dumaine, A., Mathieu, F., Chevalier, F., Henry, C., Kahn, J., Deshommes, J., Bellivier, F., Leboyer, M., & Jamain, S. (2010) · Molecular Psychiatry · doi:10.1038/mp.2008.148 · Cited by 88 · see citing works
Johansson, J. U., Ericsson, J., Janson, J., Beraki, S., Stanić, D., Mandic, S. A., Wikström, M. A., Hökfelt, T., Ögren, S. O., Rozell, B., et al. (2008) · PLoS Genetics · doi:10.1371/journal.pgen.1000278 · Cited by 83 · see citing works
Self-citationNova1 is a master regulator of alternative splicing in pancreatic beta cells
Villate, O., Turatsinze, J., Mascali, L. G., Grieco, F. A., Nogueira, T. C., Cunha, D. A., Nardelli, T. R., Sammeth, M., Salunkhe, V. A., Esguerra, J. L. S., et al. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku861 · Cited by 79 · 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
Nagy, G., Milošević, I., Fasshauer, D., Müller, E. M., de Groot, B. L., Lang, T., Wilson, M. C., & Sørensen, J. B. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e05-07-0595 · Cited by 80 · see citing works
Self-citationShimada, M., Yanai, Y., Okazaki, T., Yamashita, Y., Sriraman, V., Wilson, M. C., & Richards, J. S. (2007) · Molecular Endocrinology · doi:10.1210/me.2007-0042 · Cited by 69 · see citing works
Self-citationDisorders of synaptic vesicle fusion machinery
Melland, H., Arvell, E. H., & Gordon, S. L. (2020) · Journal of Neurochemistry · doi:10.1111/jnc.15181 · Cited by 65 · see citing works
miR-153 Regulates SNAP-25, Synaptic Transmission, and Neuronal Development
Wei, C., Thatcher, E. J., Olena, A. F., Cha, D. J., Perdigoto, A. L., Marshall, A. F., Carter, B. D., Broadie, K. S., & Patton, J. G. (2013) · PLoS ONE · doi:10.1371/journal.pone.0057080 · Cited by 63 · see citing works
Irfan, M., Gopaul, K. R., Miry, O., Hökfelt, T. G. M., Stanton, P. K., & Bark, C. (2019) · Scientific Reports · doi:10.1038/s41598-019-42833-3 · Cited by 63 · see citing works
Self-citationDevelopmental alterations in the functional properties of excitatory neocortical synapses
Feldmeyer, D., & Radnikow, G. (2009) · The Journal of Physiology · doi:10.1113/jphysiol.2009.169458 · Cited by 59 · see citing works
Control of alternative splicing by forskolin through hnRNP K during neuronal differentiation
Cao, W., Razanau, A., Feng, D., Lobo, V. G., & Xie, J. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks504 · Cited by 61 · see citing works
Understanding the molecular diversity of synapses
van Oostrum, M., & Schuman, E. M. (2025) · Nature Reviews Neuroscience · doi:10.1038/s41583-024-00888-w · Cited by 49 · see citing works
Liu, Y.-S., Dai, X., Wu, W., Yuan, F.-F., Gu, X., Chen, J.-G., Zhu, L.-Q., & Wu, J. (2017) · Molecular Neurobiology · doi:10.1007/s12035-016-9810-9 · Cited by 38 · see citing works
Control of alternative pre-mRNA splicing by Ca++ signals
Xie, J. (2008) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2008.01.003 · Cited by 44 · see citing works
Synaptic Vesicle Proteins: Targets and Routes for Botulinum Neurotoxins
Ahnert‐Hilger, G., Münster‐Wandowski, A., & Höltje, M. (2012) · Current topics in microbiology and immunology · doi:10.1007/978-3-642-33570-9_8 · Cited by 41 · see citing works
Regulation of SNARE fusion machinery by fatty acids
Davletov, B., Connell, E., & Darios, F. (2007) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-007-6557-5 · Cited by 50 · see citing works
Schiess, A., & Partridge, L. D. (2005) · European Journal of Pharmacology · doi:10.1016/j.ejphar.2005.06.007 · Cited by 40 · see citing works
Self-citationA Multilevel Functional Study of aSNAP25At-Risk Variant for Bipolar Disorder and Schizophrenia
Houenou, J., Boisgontier, J., Henrion, A., d’Albis, M.-A., Dumaine, A., Linke, J. O., Wessa, M., Daban, C., Hamdani, N., Delavest, M., et al. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.1040-17.2017 · Cited by 36 · see citing works
SIP30 Is Regulated by ERK in Peripheral Nerve Injury-induced Neuropathic Pain
Peng, G., Han, M., Du, Y., Lin, A., Yu, L., Zhang, Y., & Jing, N. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.036756 · Cited by 35 · see citing works
Regulation of Ca2+channels by SNAP-25 via recruitment of syntaxin-1 from plasma membrane clusters
Toft‐Bertelsen, T. L., Ziomkiewicz, I., Houy, S., Pinheiro, P. S., & Sørensen, J. B. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e16-03-0184 · Cited by 33 · see citing works
Yun, Y.-Y., Zurawski, Z., & Hamm, H. (2018) · Pharmacology and Therapeutics · doi:10.1016/j.pharmthera.2018.07.005 · Cited by 25 · see citing works
Membrane Trafficking in Neuronal Development: Ins and Outs of Neural Connectivity
Winkle, C. C., & Gupton, S. L. (2016) · International review of cytology · doi:10.1016/bs.ircmb.2015.10.003 · Cited by 31 · see citing works
How alternative splicing affects membrane-trafficking dynamics
Blue, R. E., Curry, E. G., Engels, N. M., Lee, E. Y., & Giudice, J. (2018) · Journal of Cell Science · doi:10.1242/jcs.216465 · Cited by 32 · see citing works
SNAP25 Ameliorates Sensory Deficit in Rats with Spinal Cord Transection
Wang, W., Wang, F., Liu, J., Zhao, W., Zhao, Q., He, M., Qian, B., Yang, X., Liu, R., Liu, S., et al. (2014) · Molecular Neurobiology · doi:10.1007/s12035-014-8642-8 · Cited by 32 · see citing works
Subgroup-specific alternative splicing in medulloblastoma
Dubuc, A. M., Morrissy, A. S., Kloosterhof, N. K., Northcott, P. A., Yu, E. P. Y., Shih, D. J. H., Peacock, J., Grajkowska, W., Meter, T. E. V., Eberhart, C. G., et al. (2012) · Acta Neuropathologica · doi:10.1007/s00401-012-0959-7 · Cited by 31 · see citing works
Targeting Synaptic Pathology with a Novel Affinity Mass Spectrometry Approach
Brinkmalm, A., Brinkmalm, G., Honer, W. G., Moreno, J. A., Jakobsson, J., Mallucci, G. R., Zetterberg, H., Blennow, K., & Öhrfelt, A. (2014) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.040113 · Cited by 31 · see citing works
Replacing SNAP-25b with SNAP-25a expression results in metabolic disease
Valladolid‐Acebes, I., Daraio, T., Brismar, K., Harkany, T., Ögren, S. O., Hökfelt, T. G. M., & Bark, C. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1511951112 · Cited by 30 · see citing works
Self-citationMandolesi, G., Vanni, V., Cesa, R., Grasselli, G., Puglisi, F., Cesare, P., & Strata, P. (2009) · Neuroscience · doi:10.1016/j.neuroscience.2009.08.067 · Cited by 27 · see citing works
The expanding roles and mechanisms of G protein–mediated presynaptic inhibition
Zurawski, Z., Yim, Y. Y., Alford, S. T., & Hamm, H. E. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.tm118.004163 · Cited by 27 · see citing works
Li, N., Yu, Z., Wang, L., Zheng, Y., Jia, J. X., Wang, Q., Zhu, M., Liu, X. H., Xia, X., & Li, W. J. (2009) · Biological Trace Element Research · doi:10.1007/s12011-009-8551-2 · Cited by 26 · see citing works
Patterns of sequence conservation in presynaptic neural genes
Hadley, D., Murphy, T., Valladares, O., Hannenhalli, S. S., Ungar, L., Kim, J., & Bućan, M. (2006) · Genome biology · doi:10.1186/gb-2006-7-11-r105 · Cited by 26 · see citing works
Wang, Y., Dong, Y., Song, H., Liu, Y., Liu, M., Yuan, Y., Ding, F., Gu, X., & Wang, Y. (2012) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/j.biocel.2012.09.011 · Cited by 25 · see citing works
Tafoya, L. C. R., Shuttleworth, C. W., Yanagawa, Y., Obata, K., & Wilson, M. C. (2008) · BMC Neuroscience · doi:10.1186/1471-2202-9-105 · Cited by 25 · see citing works
Self-citationThe Control of Neuronal Calcium Homeostasis by SNAP-25 and its Impact on Neurotransmitter Release
Pozzi, D., Corradini, I., & Matteoli, M. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.11.009 · Cited by 24 · see citing works
Chemomechanical Regulation of SNARE Proteins Studied with Molecular Dynamics Simulations
Bock, L. V., Hutchings, B., Grubmüller, H., & Woodbury, D. J. (2010) · Biophysical Journal · doi:10.1016/j.bpj.2010.06.019 · Cited by 23 · see citing works
Kroeze, Y., Oti, M., van Beusekom, E., Cooijmans, R. H. M., van Bokhoven, H., Kolk, S. M., Homberg, J. R., & Zhou, H. (2017) · Cerebral Cortex · doi:10.1093/cercor/bhw407 · Cited by 21 · see citing works
Selenoprotein P Regulates Synaptic Zinc and Reduces Tau Phosphorylation
Kiyohara, A. C. P., Torres, D. J., Hagiwara, A., Pak, J., Rueli, R. H., Shuttleworth, C. W., & Bellinger, F. P. (2021) · Frontiers in Nutrition · doi:10.3389/fnut.2021.683154 · Cited by 21 · see citing works
Self-citationQuantitative mass spectrometry reveals changes in SNAP-25 isoforms in schizophrenia
Barakauskas, V., Moradian, A., Barr, A. M., Beasley, C. L., Rosoklija, G. B., Mann, J. J., Ilievski, B., Stankov, A., Dwork, A. J., Falkai, P., et al. (2016) · Schizophrenia Research · doi:10.1016/j.schres.2016.03.002 · Cited by 20 · see citing works
Schiess, A., Scullin, C. S., & Partridge, L. D. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2006.118505 · Cited by 20 · see citing works
Self-citationThomas, M. J., Mameli, M., Carta, M., Valenzuela, C. F., Li, P., & Partridge, L. D. (2005) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.11.014 · Cited by 18 · see citing works
Self-citationScullin, C. S., Tafoya, L. C. R., Wilson, M. C., & Partridge, L. (2011) · Brain Research · doi:10.1016/j.brainres.2011.10.035 · Cited by 17 · see citing works
Self-citationSNAP-25a and SNAP-25b differently mediate interactions with Munc18-1 and Gβγ subunits
Daraio, T., Valladolid‐Acebes, I., Brismar, K., & Bark, C. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.03.024 · Cited by 16 · see citing works
Self-citationGopaul, K. R., Irfan, M., Miry, O., Vose, L. R., Moghadam, A. A., Subah, G., Hökfelt, T. G. M., Bark, C., & Stanton, P. K. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21041448 · Cited by 15 · see citing works
Self-citationSNAP-25 Puts SNAREs at Center Stage in Metabolic Disease
Irfan, M., Daraio, T., & Bark, C. (2018) · Neuroscience · doi:10.1016/j.neuroscience.2018.07.035 · Cited by 14 · see citing works
Self-citationXie, J. (2014) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-014-1688-y · Cited by 13 · see citing works
mRNA isoform balance in neuronal development and disease
LaForce, G. R., Philippidou, P., & Schaffer, A. E. (2022) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1762 · Cited by 14 · see citing works
Vasoactive intestinal peptide-induced neuritogenesis in neuroblastoma SH-SY5Y cells involves SNAP-25
Héraud, C., Chevrier, L., Meunier, A.-C., Jm, M., & Chadéneau, C. (2008) · Neuropeptides · doi:10.1016/j.npep.2008.05.005 · Cited by 12 · see citing works
Gene expression profile during functional maturation of a central mammalian synapse
Körber, C., Dondzillo, A., Eisenhardt, G., Herrmannsdörfer, F., Wafzig, O., & Kuner, T. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12661 · Cited by 13 · see citing works
Blakey, D., Wilson, M. C., & Molnár, Z. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08120.x · Cited by 12 · see citing works
Self-citationSNAP25 mutation disrupts metabolic homeostasis, steroid hormone production and central neurobehavior
Xiao, H., Zhu, B. D., Yang, P., Dong, D., Sahbaie, P., Oliver, P. L., Shen, W., Azhar, S., & Kraemer, F. B. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2021.166304 · Cited by 11 · see citing works
Scullin, C. S., Wilson, M. C., & Partridge, L. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07137.x · Cited by 11 · see citing works
Self-citationWang, J., & Hessler, N. A. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05173.x · Cited by 10 · see citing works
SNAP‐25 and Gene‐targeted Mouse Mutants
Bark, C. (2009) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2008.04009.x · Cited by 12 · see citing works
Self-citationRest mutant zebrafish swim erratically and display atypical spatial preferences
Moravec, C. E., Li, E., Maaswinkel, H., Kritzer, M. F., Weng, W., & Sirotkin, H. I. (2015) · Behavioural Brain Research · doi:10.1016/j.bbr.2015.02.026 · Cited by 8 · see citing works
Transcriptomic analysis of spinal cord regeneration after injury in Cynops orientalis
Wang, D., Man, Z., Tang, X., Gao, M., Liu, W., Xiang, M., Jian, R., Chen, J., Long, B., & Li, J. (2023) · Neural Regeneration Research · doi:10.4103/1673-5374.373717 · Cited by 7 · see citing works
Guan, M., Xie, Y., Wang, Z., Miao, Y., Li, X., Yu, S.-F., & Wang, H. (2025) · Translational Psychiatry · doi:10.1038/s41398-025-03376-6 · Cited by 8 · see citing works
Schatton, A., Mendoza, E., Grube, K., & Scharff, C. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24430 · Cited by 7 · see citing works
Valladolid‐Acebes, I., Daraio, T., Brismar, K., Hökfelt, T. G. M., & Bark, C. (2016) · Adipocyte · doi:10.1080/21623945.2015.1137689 · Cited by 6 · see citing works
Self-citationMultiple structural states in an intrinsically disordered protein, SNAP-25, using circular dichroism
Sumsion, J. S., Shumway, S. W., Blocker, T. M., Weed, T. D., Chambers, T. M., Poland, R. J., & Woodbury, D. J. (2025) · Biophysical Journal · doi:10.1016/j.bpj.2025.02.003 · Cited by 5 · see citing works
A dual role of SNAP‐25 as carrier and guardian of synaptic transmission
Kochlamazashvili, G., & Haucke, V. (2013) · EMBO Reports · doi:10.1038/embor.2013.74 · Cited by 4 · see citing works
Walz, C., Elßner-Beyer, B., Schubert, D., & Gottmann, K. (2009) · Experimental Brain Research · doi:10.1007/s00221-009-2051-7 · Cited by 4 · see citing works
Reduction in hippocampal GABAergic transmission in a low birth weight rat model of depression
Dosa, Z. J., Nieto-González, J. L., Elfving, B., Hougaard, K. S., Holm, M. M., Wegener, G., & Jensen, K. (2023) · Acta Neuropsychiatrica · doi:10.1017/neu.2023.18 · Cited by 3 · see citing works
The Role of the Postsynaptic Density and the Spine Cytoskeleton in Synaptic Plasticity
Marcora, E. M., Carlisle, H. J., & Kennedy, M. B. (2008) · Elsevier eBooks · doi:10.1016/b978-012370509-9.00036-x · Cited by 4 · see citing works
Scaffold Proteins in the Postsynaptic Density
Kennedy, M. B., Marcora, E. M., & Carlisle, H. J. (2008) · Springer eBooks · doi:10.1007/978-0-387-77232-5_14 · Cited by 2 · see citing works
Fusion Machinery: SNARE Protein Complex
Milošević, I., & Sørensen, J. B. (2014) · Springer eBooks · doi:10.1007/978-4-431-55166-9_4 · Cited by 2 · see citing works
Alternative Splicing of Neuronal Cav2 Calcium Channels
Lipscombe, D., Allen, S. E., Gray, A. C., Marangoudakis, S., & Raingo, J. (2008) · doi:10.1002/9780470429907.ch8 · Cited by 2 · see citing works
Chu, C., Pan, G.-Z., Tsai, C., Yu, C.-H. A., Lin, H.-N., Chiang, H., Chen, C., Chen, L.-C., Pham, X.-D. T., Lin, C., et al. (2025) · The EMBO Journal · doi:10.1038/s44318-025-00560-8 · Cited by 1 · see citing works
Cognitive Functions, Attention- Defi cit Hyperactivity Disorders, and Alzheimer's Disease
Passani, M. B., Blandina, P., Browman, K. E., & Fox, G. B. (2008) · CRC Press eBooks · doi:10.1201/9781420053937.secc · Cited by 1 · see citing works
Synaptic NMDA-Receptor Signaling Complex
Kennedy, M. B. (2010) · Elsevier eBooks · doi:10.1016/b978-0-12-374145-5.00158-3 · Cited by 1 · see citing works
Novel schizophrenia risk genesand gene expression
Knight, D. A. (2012) · ORCA Online Research @Cardiff (Cardiff University) · Cited by 1 · see citing works
SNAP-25 and Cdk5 as exocytotic regulators : Consequences for synaptic function and insulin release
Johansson, J. U. (2007) · Figshare
Functional Studies of SNAP-25 using a knock-out and rescue approach
Delgado-Martínez, I. (2006) · doi:10.53846/goediss-3299
Cognitive Functions, Attention- Defi cit Hyperactivity Disorders, and Alzheimer's Disease
Passani, M. B., Blandina, P., Browman, K. E., & Fox, G. B. (2008) · CRC Press eBooks · doi:10.1201/9781420053937-7 · Cited by 1 · see citing works
Attention Deficit Hyperactivity Disorder
Browman, K. E., & Fox, G. B. (2007) · Elsevier eBooks · doi:10.1016/b0-08-045044-x/00165-6
The Role of HuD in Alternative Splicing and Alternative Polyadenylation in the Brain
Sena, R. M. (2020) · UNM’s Digital Repository (University of New Mexico)
Dynamics and Driving Forces of Macromolecular Complexes
Bock, L. V. (2013) · MPG.PuRe (Max Planck Society) · doi:10.53846/goediss-3864
Isoswitching in human brain development and agingPreprint
Erdogdu, B., Ji, H. J., Rudnick, Z., Pertea, M., & Salzberg, S. L. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.05.652255
Development of presynaptic calcium dynamics and short-term plasticity in the SC-Ca1 synapse
Scullin, C. S. (2010) · UNM’s Digital Repository (University of New Mexico)
Tafoya, L. C. R. (2011) · UNM’s Digital Repository (University of New Mexico)
- Authors
- Bark, C., Bellinger, F. P., Kaushal, A., Mathews, J. R., Partridge, L. D., & Wilson, M. C.
- Affiliations
- Karolinska University Hospital (SE)
- University of New Mexico (US)
- Corresponding author
- Wilson, Michael C.
- ORCID
- Bark, Christina
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2004-10-06
- Volume
- 24
- Issue
- 40
- Pages
- 8796-8805
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6729955
- OpenAlex
- W1967517418
- Cited by
- 101
- References
- 55
- Citations by year
- 2025: 4 · 2024: 1 · 2023: 2 · 2022: 1 · 2021: 3 · 2020: 3 · 2019: 2 · 2018: 6 · 2017: 3 · 2016: 6 · 2015: 2 · 2014: 7 · 2013: 6 · 2012: 8
- FWCI
- 2.80
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Karolinska Institutet
- National Institutes of Health
- National Institute of Mental Health (MH 4-8989, R01MH048989)
- 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 › RNA Research and Splicing
- Keywords
- SNAP-25, alternative splicing, synaptic facilitation, neurotransmitter release, synapse maturation, t-SNARE, short-term plasticity, synaptogenesis, mouse mutants
- MeSH terms
- Animals, Hippocampus, Membrane Proteins, Mice, Mutant Strains, Nerve Tissue Proteins, Synaptic Transmission, Neuronal Plasticity, Neurons, Phenotype, Alternative Splicing, Gene Targeting, Patch-Clamp Techniques, Gene Expression Regulation, Developmental, Integrases, Protein Isoforms, Synaptosomal-Associated Protein 25, Mice
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