SNAP-25, a Known presynaptic protein with emerging postsynaptic functions

Frontiers in Synaptic Neuroscience

Volumn 8, Issue MAR, 2016, Pages

  Antonucci, Flavia ^a   Corradini, Irene ^a,b   Fossati, Giuliana ^c   Tomasoni, Romana ^c   Menna, Elisabetta ^b,c   Matteoli, Michela ^b,c  

^a UNIVERSITY OF MILAN   (Italy)

^b Centro Nazionale Ricerche   (Italy)

^c HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

Author keywords

Brain diseases; Postsynaptic role; Presynaptic role; SNAP 25; Synaptopathies

Indexed keywords

POSTSYNAPTIC RECEPTOR; SYNAPTOSOMAL ASSOCIATED PROTEIN 25;

CELL FUNCTION; ENDOCYTOSIS; EXOCYTOSIS; GENETIC ASSOCIATION; GENETIC POLYMORPHISM; HUMAN; MENTAL DISEASE; MORPHOGENESIS; NERVE CELL PLASTICITY; NERVE ENDING; NEUROMODULATION; NONHUMAN; PRESYNAPTIC NERVE; PROTEIN FUNCTION; SHORT SURVEY; SPINAL CORD NERVE CELL; SYNAPSE; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION;

EID: 84993978491     PISSN: None     EISSN: 16633563     Source Type: Journal    
DOI: 10.3389/fnsyn.2016.00007     Document Type: Short Survey

References (106)

1. Ahnert-Hilger, G., Munster-Wandowski, A., and Höltje, M. (2013). Synaptic vesicle proteins: targets and routes for botulinum neurotoxins. Curr. Top. Microbiol. Immunol. 364, 159-177. doi: 10.1007/978-3-662-45790-0_8
2. Antonucci, F., Corradini, I., Morini, R., Fossati, G., Menna, E., Pozzi, D., et al. (2013). Reduced SNAP-25 alters short-term plasticity at developing glutamatergic synapses. EMBO Rep. 14, 645-651. doi: 10.1038/embor.2013.75
3. Aoki, K. R., and Guyer, B. (2001). Botulinum toxin type A and other botulinum toxin serotypes: a comparative review of biochemical and pharmacological actions. Eur. J. Neurol. 8(Suppl. 5), 21-29. doi: 10.1046/j.1468-1331.2001.00035.x
4. Atlas, D., Wiser, O., and Trus, M. (2001). The voltage-gated Ca2+ channel is the Ca2+ sensor of fast neurotransmitter release. Cell. Mol. Neurobiol. 21, 717-731. doi: 10.1023/A:1015104105262
5. Bark, I. C. (1993). Structure of the chicken gene for SNAP-25 reveals duplicated exon encoding distinct isoforms of the protein. J. Mol. Biol. 233, 67-76. doi: 10.1006/jmbi.1993.1485
6. Bark, I. C., Hahn, K. M., Ryabinin, A. E., and Wilson, M. C. (1995). Differential expression of SNAP-25 protein isoforms during divergent vesicle fusion events of neural development. Proc. Natl. Acad. Sci. U.S.A. 92, 1510-1514. doi: 10.1073/pnas.92.5.1510
7. Bark, I. C., and Wilson, M. C. (1994). Human cDNA clones encoding two different isoforms of the nerve terminal protein SNAP-25. Gene 139, 291-292. doi: 10.1016/0378-1119(94)90773-0
8. Barr, C. L., Feng, Y., Wigg, K., Bloom, S., Roberts, W., Malone, M., et al. (2000). Identification of DNA variants in the SNAP-25 gene and linkage study of these polymorphisms and attention-deficit hyperactivity disorder. Mol. Psychiatry 5, 405-409. doi: 10.1038/sj.mp.4000733
9. Bennett, M. K., Calakos, N., and Scheller, R. H. (1992). Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. Science 257, 255-259. doi: 10.1126/science.1321498
10. Braida, D., Guerini, F. R., Ponzoni, L., Corradini, I., De Astis, S., Pattini, L., et al. (2015). Association between SNAP-25 gene polymorphisms and cognition in autism: functional consequences and potential therapeutic strategies. Transl. Psychiatry 5:e500. doi: 10.1038/tp.2014.136
11. Brophy, K., Hawi, Z., Kirley, A., Fitzgerald, M., and Gill, M. (2002). Synaptosomal-associated protein 25 (SNAP-25) and attention deficit hyperactivity disorder (ADHD): evidence of linkage and association in the Irish population. Mol. Psychiatry 7, 913-917. doi: 10.1038/sj.mp.4001092
12. Cagliani, R., Riva, S., Marino, C., Fumagalli, M., D'Angelo, M. G., Riva, V., et al. (2012). Variants in SNAP25 are targets of natural selection and influence verbal performances in women. Cell. Mol. Life Sci. 69, 1705-1715. doi: 10.1007/s00018-011-0896-y
13. Carroll, L. S., Kendall, K., O'Donovan, M. C., Owen, M. J., and Williams, N. M. (2009). Evidence that putative ADHD low risk alleles at SNAP25 may increase the risk of schizophrenia. Am. J. Med. Genet. B Neuropsychiatr. Genet. 150B, 893-899. doi: 10.1002/ajmg.b.30915
14. Catterall, W. A., and Few, A. P. (2008). Calcium channel regulation and presynaptic plasticity. Neuron 59, 882-901. doi: 10.1016/j.neuron.2008.09.005
15. Chapman, E. R., An, S., Barton, N., and Jahn, R. (1994). SNAP-25, a t-SNARE which binds to both syntaxin and synaptobrevin via domains that may form coiled coils. J. Biol. Chem. 269, 27427-27432.
16. Condliffe, S. B., Corradini, I., Pozzi, D., Verderio, C., and Matteoli, M. (2010). Endogenous SNAP-25 regulates native voltage-gated calcium channels in glutamatergic neurons. J. Biol. Chem. 285, 24968-24976. doi: 10.1074/jbc.M110.145813
17. Condliffe, S. B., and Matteoli, M. (2011). Inactivation kinetics of voltage-gated calcium channels in glutamatergic neurons are influenced by SNAP-25. Channels 5, 304-307. doi: 10.4161/chan.5.4.16228
18. Corradini, I., Donzelli, A., Antonucci, F., Welzl, H., Loos, M., Martucci, R., et al. (2014). Epileptiform activity and cognitive deficits in SNAP-25+/-mice are normalized by antiepileptic drugs. Cereb. Cortex 24, 364-376. doi: 10.1093/cercor/bhs316
19. Dai, D., Wang, Y., Yuan, J., Zhou, X., Jiang, D., Li, J., et al. (2014). Meta-analyses of 10 polymorphisms associated with the risk of schizophrenia. Biomed. Rep. 2, 729-736. doi: 10.3892/br.2014.308
20. Diril, M. K., Wienisch, M., Jung, N., Klingauf, J., and Haucke, V. (2006). Stonin 2 is an AP-2-dependent endocytic sorting adaptor for synaptotagmin internalization and recycling. Dev. Cell 10, 233-244. doi: 10.1016/j.devcel.2005.12.011
21. Etain, B., Dumaine, A., Mathieu, F., Chevalier, F., Henry, C., Kahn, J. P., et al. (2010). A SNAP25 promoter variant is associated with early-onset bipolar disorder and a high expression level in brain. Mol. Psychiatry 15, 748-755. doi: 10.1038/mp.2008.148
22. Faraone, S. V., Perlis, R. H., Doyle, A. E., Smoller, J. W., Goralnick, J. J., Holmgren, M. A., et al. (2005). Molecular genetics of attention-deficit/hyperactivity disorder. Biol. Psychiatry 57, 1313-1323. doi: 10.1016/j.biopsych.2004.11.024
23. Fatemi, S. H., Earle, J. A., Stary, J. M., Lee, S., and Sedgewick, J. (2001). Altered levels of the synaptosomal associated protein SNAP-25 in hippocampus of subjects with mood disorders and schizophrenia. Neuroreport 12, 3257-3262. doi: 10.1097/00001756-200110290-00023
24. Fernández, E., Collins, M. O., Uren, R. T., Kopanitsa, M. V., Komiyama, N. H., Croning, M. D., et al. (2009). Targeted tandem affinity purification of PSD-95 recovers core postsynaptic complexes and schizophrenia susceptibility proteins. Mol. Syst. Biol. 5, 269. doi: 10.1038/msb.2009.27
25. Fossati, G., Morini, R., Corradini, I., Antonucci, F., Trepte, P., Edry, E., et al. (2015). Reduced SNAP-25 increases PSD-95 mobility and impairs spine morphogenesis. Cell Death Differ. 22, 1425-1436. doi: 10.1038/cdd.2014.227
26. Galas, M. C., Chasserot-Golaz, S., Dirrig-Grosch, S., and Bader, M. F. (2000). Presence of dynamin-syntaxin complexes associated with secretory granules in adrenal chromaffin cells. J. Neurochem. 75, 1511-1519. doi: 10.1046/j.1471-4159.2000.0751511.x
27. Genoud, S., Pralong, W., Riederer, B. M., Eder, L., Catsicas, S., and Muller, D. (1999). Activity-dependent phosphorylation of SNAP-25 in hippocampal organotypic cultures. J. Neurochem. 72, 1699-1706. doi: 10.1046/j.1471-4159.1999.721699.x
28. Gosso, M. F., de Geus, E. J., Polderman, T. J., Boomsma, D. I., Heutink, P., and Posthuma, D. (2008). Common variants underlying cognitive ability: further evidence for association between the SNAP-25 gene and cognition using a family-based study in two independent Dutch cohorts. Genes Brain Behav. 7, 355-364. doi: 10.1111/j.1601-183X.2007.00359.x
29. Gosso, M. F., de Geus, E. J., van Belzen, M. J., Polderman, T. J., Heutink, P., Boomsma, D. I., et al. (2006). The SNAP-25 gene is associated with cognitive ability: evidence from a family-based study in two independent Dutch cohorts. Mol. Psychiatry 11, 878-886. doi: 10.1038/sj.mp.4001868
30. Guerini, F. R., Agliardi, C., Sironi, M., Arosio, B., Calabrese, E., Zanzottera, M., et al. (2014). Possible association between SNAP-25 single nucleotide polymorphisms and alterations of categorical fluency and functional MRI parameters in Alzheimer's disease. J. Alzheimers Dis. 42, 1015-1028. doi: 10.3233/JAD-140057
31. Guerini, F. R., Bolognesi, E., Chiappedi, M., Manca, S., Ghezzo, A., Agliardi, C., et al. (2011). SNAP-25 single nucleotide polymorphisms are associated with hyperactivity in autism spectrum disorders. Pharmacol. Res. 64, 283-288. doi: 10.1016/j.phrs.2011.03.015
32. Hawi, Z., Matthews, N., Wagner, J., Wallace, R. H., Butler, T. J., Vance, A., et al. (2013). DNA variation in the SNAP25 gene confers risk to ADHD and is associated with reduced expression in prefrontal cortex. PLoS ONE 8:e60274. doi: 10.1371/journal.pone.0060274
33. Hess, E. J., Jinnah, H. A., Kozak, C. A., and Wilson, M. C. (1992). Spontaneous locomotor hyperactivity in a mouse mutant with a deletion including the Snap gene on chromosome 2. J. Neurosci. 12, 2865-2874.
34. Hess, E. J., Rogan, P. K., Domoto, M., Tinker, D. E., Ladda, R. L., and Ramer, J. C. (1995). Absence of linkage of apparently single gene mediated ADHD with the human syntenic region of the mouse mutant Coloboma. Am. J. Med. Genet. 60, 573-579. doi: 10.1002/ajmg.1320600619
35. Holderith, N., Lorincz, A., Katona, G., Rózsa, B., Kulik, A., Watanabe, M., et al. (2012). Release probability of hippocampal glutamatergic terminals scales with the size of the active zone. Nat. Neurosci. 15, 988-997. doi: 10.1038/nn.3137
36. Houeland, G., Nakhost, A., Sossin, W. S., and Castellucci, V. F. (2007). PKC modulation of transmitter release by SNAP-25 at sensory-to-motor synapses in Aplysia. J. Neurophysiol. 97, 134-143. doi: 10.1152/jn.00122.2006
37. Jahn, R., Lang, T., and Sudhof, T. C. (2003). Membrane fusion. Cell 112, 519-533. doi: 10.1016/S0092-8674(03)00112-0
38. Jarvis, S. E., and Zamponi, G. W. (2001). Distinct molecular determinants govern syntaxin 1A-mediated inactivation and G-protein inhibition of N-type calcium channels. J. Neurosci. 21, 2939-2948.
39. Jaworski, J., Kapitein, L. C., Gouveia, S. M., Dortland, B. R., Wulf, P. S., Grigoriev, I., et al. (2009). Dynamic microtubules regulate dendritic spine morphology and synaptic plasticity. Neuron 61, 85-100. doi: 10.1016/j.neuron.2008.11.013
40. Jeans, A. F., Oliver, P. L., Johnson, R., Capogna, M., Vikman, J., Molnár, Z., et al. (2007). A dominant mutation in Snap25 causes impaired vesicle trafficking, sensorimotor gating, and ataxia in the blind-drunk mouse. Proc. Natl. Acad. Sci. U.S.A. 104, 2431-2436. doi: 10.1073/pnas.0610222104
41. Jurado, S., Goswami, D., Zhang, Y., Molina, A. J., Sudhof, T. C., and Malenka, R. C. (2013). LTP requires a unique postsynaptic SNARE fusion machinery. Neuron 77, 542-558. doi: 10.1016/j.neuron.2012.11.029
42. Kataoka, M., Kuwahara, R., Matsuo, R., Sekiguchi, M., Inokuchi, K., and Takahashi, M. (2006). Development-and activity-dependent regulation of SNAP-25 phosphorylation in rat brain. Neurosci. Lett. 407, 258-262. doi: 10.1016/j.neulet.2006.08.055
43. Kataoka, M., Yamamori, S., Suzuki, E., Watanabe, S., Sato, T., Miyaoka, H., et al. (2011). A single amino acid mutation in SNAP-25 induces anxiety-related behavior in mouse. PLoS ONE 6:e25158. doi: 10.1371/journal.pone.0025158
44. Kerti, K., Lorincz, A., and Nusser, Z. (2012). Unique somato-dendritic distribution pattern of Kv4.2 channels on hippocampal CA1 pyramidal cells. Eur. J. Neurosci. 35, 66-75. doi: 10.1111/j.1460-9568.2011.07907.x
45. Kochlamazashvili, G., and Haucke, V. (2013). A dual role of SNAP-25 as carrier and guardian of synaptic transmission. EMBO Rep. 14, 579-580. doi: 10.1038/embor.2013.74
46. Koo, S. J., Markovic, S., Puchkov, D., Mahrenholz, C. C., Beceren-Braun, F., Maritzen, T., et al. (2011). SNARE motif-mediated sorting of synaptobrevin by the endocytic adaptors clathrin assembly lymphoid myeloid leukemia (CALM) and AP180 at synapses. Proc. Natl. Acad. Sci. U.S.A. 108, 13540-13545. doi: 10.1073/pnas.1107067108
47. Kustanovich, V., Merriman, B., McGough, J., McCracken, J. T., Smalley, S. L., and Nelson, S. F. (2003). Biased paternal transmission of SNAP-25 risk alleles in attention-deficit hyperactivity disorder. Mol. Psychiatry 8, 309-315. doi: 10.1038/sj.mp.4001247
48. Lau, C. G., Takayasu, Y., Rodenas-Ruano, A., Paternain, A. V., Lerma, J., Bennett, M. V., et al. (2010). SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J. Neurosci. 30, 242-254. doi: 10.1523/JNEUROSCI.4933-08.2010
49. Lévêque, C., el Far, O., Martin-Moutot, N., Sato, K., Kato, R., Takahashi, M., et al. (1994). Purification of the N-type calcium channel associated with syntaxin and synaptotagmin. A complex implicated in synaptic vesicle exocytosis. J. Biol. Chem. 269, 6306-6312.
50. Martin-Moutot, N., Charvin, N., Leveque, C., Sato, K., Nishiki, T., Kozaki, S., et al. (1996). Interaction of SNARE complexes with P/Q-type calcium channels in rat cerebellar synaptosomes. J. Biol. Chem. 271, 6567-6570. doi: 10.1074/jbc.271.12.6567
51. Miller, S. E., Sahlender, D. A., Graham, S. C., Höning, S., Robinson, M. S., Peden, A. A., et al. (2011). The molecular basis for the endocytosis of small R-SNAREs by the clathrin adaptor CALM. Cell 147, 1118-1131. doi: 10.1016/j.cell.2011.10.038
52. Milovanovic, D., and Jahn, R. (2015). Organization and dynamics of SNARE proteins in the presynaptic membrane. Front. Physiol. 6:89. doi: 10.3389/fphys.2015.00089
53. Mohrmann, R., de Wit, H., Verhage, M., Neher, E., and Sørensen, J. B. (2010). Fast vesicle fusion in living cells requires at least three SNARE complexes. Science 330, 502-505. doi: 10.1126/science.1193134
54. Montecucco, C., Schiavo, G., and Pantano, S. (2005). SNARE complexes and neuroexocytosis: how many, how close? Trends Biochem. Sci. 30, 367-372. doi: 10.1016/j.tibs.2005.05.002
55. Nagy, G., Matti, U., Nehring, R. B., Binz, T., Rettig, J., Neher, E., et al. (2002). Protein kinase C-dependent phosphorylation of synaptosome-associated protein of 25 kDa at Ser(187) potentiates vesicle recruitment. J. Neurosci. 22, 9278-9286.
56. Németh, N., Kovács-Nagy, R., Székely, A., Sasvári-Székely, M., and Rónai, Z. (2013). Association of impulsivity and polymorphic microRNA-641 target sites in the SNAP-25 gene. PLoS ONE 8:e84207. doi: 10.1371/journal.pone.0084207
57. Ohira, K., Kobayashi, K., Toyama, K., Nakamura, H. K., Shoji, H., Takao, K., et al. (2013). Synaptosomal-associated protein 25 mutation induces immaturity of the dentate granule cells of adult mice. Mol. Brain 6:12. doi: 10.1186/1756-6606-6-12
58. Okamoto, M., Schoch, S., and Sudhof, T. C. (1999). EHSH1/intersectin, a protein that contains EH and SH3 domains and binds to dynamin and SNAP-25. A protein connection between exocytosis and endocytosis? J. Biol. Chem. 274, 18446-18454. doi: 10.1074/jbc.274.26.18446
59. Oliver, P. L., and Davies, K. E. (2009). Interaction between environmental and genetic factors modulates schizophrenic endophenotypes in the Snap-25 mouse mutant blind-drunk. Hum. Mol. Genet. 18, 4576-4589. doi: 10.1093/hmg/ddp425
60. Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E., Billingsley, M., Bloom, F. E., et al. (1989). The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations. J. Cell Biol. 109, 3039-3052. doi: 10.1083/jcb.109.6.3039
61. Pantano, S., and Montecucco, C. (2014). The blockade of the neurotransmitter release apparatus by botulinum neurotoxins. Cell. Mol. Life Sci. 71, 793-811. doi: 10.1007/s00018-013-1380-7
62. Pazvantoglu, O., Günes, S., Karabekiroglu, K., Yegin, Z., Erenkus, Z., Akbas, S., et al. (2013). The relationship between the presence of ADHD and certain candidate gene polymorphisms in a Turkish sample. Gene 528, 320-327. doi: 10.1016/j.gene.2013.07.004
63. Penzes, P., Cahill, M. E., Jones, K. A., VanLeeuwen, J. E., and Woolfrey, K. M. (2011). Dendritic spine pathology in neuropsychiatric disorders. Nat. Neurosci. 14, 285-293. doi: 10.1038/nn.2741
64. Poirier, M. A., Hao, J. C., Malkus, P. N., Chan, C., Moore, M. F., King, D. S., et al. (1998). Protease resistance of syntaxin.SNAP-25.VAMP complexes. Implications for assembly and structure. J. Biol. Chem. 273, 11370-11377. doi: 10.1074/jbc.273.18.11370
65. Pozzi, D., Condliffe, S., Bozzi, Y., Chikhladze, M., Grumelli, C., Proux-Gillardeaux, V., et al. (2008). Activity-dependent phosphorylation of Ser187 is required for SNAP-25-negative modulation of neuronal voltage-gated calcium channels. Proc. Natl. Acad. Sci. U.S.A. 105, 323-328. doi: 10.1073/pnas.0706211105
66. Prescott, G. R., and Chamberlain, L. H. (2011). Regional and developmental brain expression patterns of SNAP25 splice variants. BMC Neurosci. 12:35. doi: 10.1186/1471-2202-12-35
67. Raciborska, D. A., Trimble, W. S., and Charlton, M. P. (1998). Presynaptic protein interactions in vivo: evidence from botulinum A, C, D and E action at frog neuromuscular junction. Eur. J. Neurosci. 10, 2617-2628. doi: 10.1046/j.1460-9568.1998.00270.x
68. Ramos-Miguel, A., Beasley, C. L., Dwork, A. J., Mann, J. J., Rosoklija, G., Barr, A. M., et al. (2015). Increased SNARE protein-protein interactions in orbitofrontal and anterior cingulate cortices in Schizophrenia. Biol. Psychiatry 78, 361-373. doi: 10.1016/j.biopsych.2014.12.012
69. Repetto, D., Camera, P., Melani, R., Morello, N., Russo, I., Calcagno, E., et al. (2014). p140Cap regulates memory and synaptic plasticity through Src-mediated and citron-N-mediated actin reorganization. J. Neurosci. 34, 1542-1553. doi: 10.1523/JNEUROSCI.2341-13.2014
70. Rettig, J., Sheng, Z. H., Kim, D. K., Hodson, C. D., Snutch, T. P., and Catterall, W. A. (1996). Isoform-specific interaction of the alpha1A subunits of brain Ca2+ channels with the presynaptic proteins syntaxin and SNAP-25. Proc. Natl. Acad. Sci. U.S.A. 93, 7363-7368. doi: 10.1073/pnas.93.14.7363
71. Rizzi, T. S., Beunders, G., Rizzu, P., Sistermans, E., Twisk, J. W., van Mechelen, W., et al. (2012). Supporting the generalist genes hypothesis for intellectual ability/disability: the case of SNAP25. Genes Brain Behav. 11, 767-771. doi: 10.1111/j.1601-183X.2012.00819.x
72. Rohena, L., Neidich, J., Truitt Cho, M., Gonzalez, K. D., Tang, S., Devinsky, O., et al. (2013). Mutation in SNAP25 as a novel genetic cause of epilepsy and intellectual disability. Rare Dis. 1:e26314. doi: 10.4161/rdis.26314
73. Russell, V. A. (2007). Neurobiology of animal models of attention-deficit hyperactivity disorder. J. Neurosci. Methods 161, 185-198. doi: 10.1016/j.jneumeth.2006.12.005
74. Scarr, E., Gray, L., Keriakous, D., Robinson, P. J., and Dean, B. (2006). Increased levels of SNAP-25 and synaptophysin in the dorsolateral prefrontal cortex in bipolar I disorder. Bipolar Disord. 8, 133-143. doi: 10.1111/j.1399-5618.2006.00300.x
75. Schiavo, G., Matteoli, M., and Montecucco, C. (2000). Neurotoxins affecting neuroexocytosis. Physiol. Rev. 80, 717-766.
76. Selak, S., Paternain, A. V., Aller, M. I., Picó, E., Rivera, R., and Lerma, J. (2009). A role for SNAP25 in internalization of kainate receptors and synaptic plasticity. Neuron 63, 357-371. doi: 10.1016/j.neuron.2009.07.017
77. Sharma, M., Burré, J., Bronk, P., Zhang, Y., Xu, W., and Südhof, T. C. (2012). CSPalpha knockout causes neurodegeneration by impairing SNAP-25 function. EMBO J. 31, 829-841. doi: 10.1038/emboj.2011.467
78. Shen, X. M., Selcen, D., Brengman, J., and Engel, A. G. (2014). Mutant SNAP25B causes myasthenia, cortical hyperexcitability, ataxia, and intellectual disability. Neurology 83, 2247-2255. doi: 10.1212/WNL.0000000000001079
79. Sheng, Z. H., Rettig, J., Cook, T., and Catterall, W. A. (1996). Calcium-dependent interaction of N-type calcium channels with the synaptic core complex. Nature 379, 451-454. doi: 10.1038/379451a0
80. Söderqvist, S., McNab, F., Peyrard-Janvid, M., Matsson, H., Humphreys, K., Kere, J., et al. (2010). The SNAP25 gene is linked to working memory capacity and maturation of the posterior cingulate cortex during childhood. Biol. Psychiatry 68, 1120-1125. doi: 10.1016/j.biopsych.2010.07.036
81. Söllner, T., Bennett, M. K., Whiteheart, S. W., Scheller, R. H., and Rothman, J. E. (1993a). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418. doi: 10.1016/0092-8674(93)90376-2
82. Söllner, T., Whiteheart, S. W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., et al. (1993b). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324. doi: 10.1038/362318a0
83. Sørensen, J. B., Nagy, G., Varoqueaux, F., Nehring, R. B., Brose, N., Wilson, M. C., et al. (2003). Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23. Cell 114, 75-86. doi: 10.1016/S0092-8674(03)00477-X
84. Spellmann, I., Müller, N., Musil, R., Zill, P., Douhet, A., Dehning, S., et al. (2008). Associations of SNAP-25 polymorphisms with cognitive dysfunctions in Caucasian patients with schizophrenia during a brief trail of treatment with atypical antipsychotics. Eur. Arch. Psychiatry Clin. Neurosci. 258, 335-344. doi: 10.1007/s00406-007-0800-9
85. Sudhof, T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509-547. doi: 10.1146/annurev.neuro.26.041002.131412
86. Sudhof, T. C. (2012). Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol. 4:a011353. doi: 10.1101/cshperspect.a011353
87. Sutton, R. B., Fasshauer, D., Jahn, R., and Brunger, A. T. (1998). Crystal structure of a SNARE complex involved in synaptic exocytosis at 2.4 A resolution. Nature 395, 347-353. doi: 10.1038/26412
88. Tao-Cheng, J. H., Du, J., and McBain, C. J. (2000). Snap-25 is polarized to axons and abundant along the axolemma: an immunogold study of intact neurons. J. Neurocytol. 29, 67-77. doi: 10.1023/A:1007168231323
89. Thompson, P. M., Egbufoama, S., and Vawter, M. P. (2003). SNAP-25 reduction in the hippocampus of patients with schizophrenia. Prog. Neuropsychopharmacol. Biol. Psychiatry 27, 411-417. doi: 10.1016/S0278-5846(03)00027-7
90. Thompson, P. M., Sower, A. C., and Perrone-Bizzozero, N. I. (1998). Altered levels of the synaptosomal associated protein SNAP-25 in schizophrenia. Biol. Psychiatry 43, 239-243. doi: 10.1016/S0006-3223(97)00204-7
91. Tomasoni, R., Repetto, D., Morini, R., Elia, C., Gardoni, F., Di Luca, M., et al. (2013). SNAP-25 regulates spine formation through postsynaptic binding to p140Cap. Nat. Commun. 4, 2136. doi: 10.1038/ncomms3136
92. Verderio, C., Pozzi, D., Pravettoni, E., Inverardi, F., Schenk, U., Coco, S., et al. (2004). SNAP-25 modulation of calcium dynamics underlies differences in GABAergic and glutamatergic responsiveness to depolarization. Neuron 41, 599-610. doi: 10.1016/S0896-6273(04)00077-7
93. Wang, Q., Wang, Y., Ji, W., Zhou, G., He, K., Li, Z., et al. (2015). SNAP25 is associated with schizophrenia and major depressive disorder in the Han Chinese population. J. Clin. Psychiatry 76, e76-82. doi: 10.4088/JCP.13m08962
94. Washbourne, P., Thompson, P. M., Carta, M., Costa, E. T., Mathews, J. R., Lopez-Bendito, G., et al. (2002). Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5, 19-26. doi: 10.1038/nn783
95. Watanabe, S., Yamamori, S., Otsuka, S., Saito, M., Suzuki, E., Kataoka, M., et al. (2015). Epileptogenesis and epileptic maturation in phosphorylation site-specific SNAP-25 mutant mice. Epilepsy Res. 115, 30-44. doi: 10.1016/j.eplepsyres.2015.05.004
96. Weiss, N., Hameed, S., Fernández-Fernández, J. M., Fablet, K., Karmazinova, M., Poillot, C., et al. (2012). A Ca(v)3.2/Syntaxin-1A signaling complex controls T-type channel activity and low-threshold exocytosis. J. Biol. Chem. 287, 2810-2818. doi: 10.1074/jbc.M111.290882
97. Wiser, O., Trus, M., Hernández, A., Renstrom, E., Barg, S., Rorsman, P., et al. (1999). The voltage sensitive Lc-type Ca2+ channel is functionally coupled to the exocytotic machinery. Proc. Natl. Acad. Sci. U.S.A. 96, 248-253. doi: 10.1073/pnas.96.1.248
98. Wu, L. G., Hamid, E., Shin, W., and Chiang, H. C. (2014). Exocytosis and endocytosis: modes, functions, and coupling mechanisms. Annu. Rev. Physiol. 76, 301-331. doi: 10.1146/annurev-physiol-021113-170305
99. Xu, J., Luo, F., Zhang, Z., Xue, L., Wu, X. S., Chiang, H. C., et al. (2013). SNARE proteins synaptobrevin, SNAP-25, and syntaxin are involved in rapid and slow endocytosis at synapses. Cell Rep. 3, 1414-1421. doi: 10.1016/j.celrep.2013.03.010
100. Yoshida, A., Oho, C., Omori, A., Kuwahara, R., Ito, T., and Takahashi, M. (1992). HPC-1 is associated with synaptotagmin and omega-conotoxin receptor. J. Biol. Chem. 267, 24925-24928.
101. Young, C. E., Arima, K., Xie, J., Hu, L., Beach, T. G., Falkai, P., et al. (1998). SNAP-25 deficit and hippocampal connectivity in schizophrenia. Cereb. Cortex 8, 261-268. doi: 10.1093/cercor/8.3.261
102. Zamponi, G. W. (2003). Regulation of presynaptic calcium channels by synaptic proteins. J. Pharmacol. Sci. 92, 79-83. doi: 10.1254/jphs.92.79
103. Zhang, H., Zhu, S., Zhu, Y., Chen, J., Zhang, G., and Chang, H. (2011). An association study between SNAP-25 gene and attention-deficit hyperactivity disorder. Eur. J. Paediatr. Neurol. 15, 48-52. doi: 10.1016/j.ejpn.2010.06.001
104. Zhang, Y., Vilaythong, A. P., Yoshor, D., and Noebels, J. L. (2004). Elevated thalamic low-voltage-activated currents precede the onset of absence epilepsy in the SNAP25-deficient mouse mutant coloboma. J. Neurosci. 24, 5239-5248. doi: 10.1523/JNEUROSCI.0992-04.2004
105. Zhang, Z., Wang, D., Sun, T., Xu, J., Chiang, H. C., Shin, W., et al. (2013). The SNARE proteins SNAP25 and synaptobrevin are involved in endocytosis at hippocampal synapses. J. Neurosci. 33, 9169-9175. doi: 10.1523/JNEUROSCI.0301-13.2013
106. Zhong, H., Yokoyama, C. T., Scheuer, T., and Catterall, W. A. (1999). Reciprocal regulation of P/Q-type Ca2+ channels by SNAP-25, syntaxin and synaptotagmin. Nat. Neurosci. 2, 939-941. doi: 10.1038/14721