Bartholomé, Odile ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Van Den Ackerveken, Priscilla ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Sanchez Gil, Judit ; Université de Liège - ULiège > Master bioch. & biol. mol. & cel., à fin.
Franzen, Rachelle ; Université de Liège > Département des sciences biomédicales et précliniques > Neuro-anatomie
Rogister, Bernard ; Université de Liège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, et biochimie humaine
Language :
English
Title :
Puzzling Out Synaptic Vesicle 2 Family Members Functions
Alvarez de Toledo, G., Fernández-Chacón, R., and Fernández, J. (1993). Release of secretory products during transient vesicle fusion. Nature 363, 554–558. doi: 10.1038/363554a0
Bai, J., Wang, P., and Chapman, E. R. (2002). C2A activates a cryptic Ca2+ -triggered membrane penetration activity within the C2B domain of synaptotagmin I. Proc. Natl. Acad. Sci. U S A 99, 1665–1670. doi: 10.1073/pnas. 032541099
Bajjalieh, S. M., Frantz, G. D., Weimann, J. M., McConnell, S. K., and Scheller, R. H. (1994). Differential expression of synaptic vesicle protein 2 (SV2) isoforms. J. Neurosci. 14, 5223–5235.
Bajjalieh, S. M., Peterson, K., Shinghal, R., and Scheller, R. H. (1992). SV2, a brain synaptic vesicle protein homologous to bacterial transporters. Science 257, 1271–1273. doi: 10.1126/science.15 19064
Bakker, A., Krauss, G. L., Albert, M. S., Speck, C. L., Jones, L. R., Stark, C. E., et al. (2012). Reduction of hippocampal hyperactivity improves cognition in amnestic mild cognitive impairment. Neuron 74, 467–474. doi: 10.1016/j.neuron.2012.03.023
Bennett, M. K., Calakos, N., Kreiner, T., and Scheller, R. H. (1992). Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116, 761–775. doi: 10.1083/jcb.116.3.761
Bookheimer, S. Y., Strojwas, M. H., Cohen, M. S., Saunders, A. M., Pericak-Vance, M. A., Mazziotta, J. C., et al. (2000). Patterns of brain activation in people at risk for Alzheimer’s disease. N. Engl. J. Med. 343, 450–456. doi: 10.1056/NEJM200008173430701
Bragina, L., Fattorini, G., Giovedí, S., Melone, M., Bosco, F., Benfenati, F., et al. (2012). Analysis of synaptotagmin, SV2, and Rab3 expression in cortical glutamatergic and GABAergic axon terminals. Front. Cell. Neurosci. 5:32. doi: 10.3389/fncel.2011.00032
Brose, N., Petrenko, A. G., Südhof, T. C., and Jahn, R. (1992). Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 256, 1021–1025. doi: 10.1126/science.1589771
Buckley, K., and Kelly, R. B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 100, 1284–1294. doi: 10.1083/jcb.100.4.1284
Budzinski, K. L., Allen, R. W., Fujimoto, B. S., Kensel-Hammes, P., Belnap, D. M., Bajjalieh, S. M., et al. (2009). Large structural change in isolated synaptic vesicles upon loading with neurotransmitter. Biophys. J. 97, 2577–2584. doi: 10.1016/j.bpj.2009.08.032
Chang, W.-P., and Sudhof, T. C. (2009). SV2 renders primed synaptic vesicles competent for Ca2+ -induced exocytosis. J. Neurosci. 29, 883–897. doi: 10.1523/JNEUROSCI.4521-08.2009
Chapman, E. R., Desai, R. C., Davis, A. F., and Tornehl, C. K. (1998). Delineation of the oligomerization, AP-2 binding, and synprint binding region of the C2B domain of synaptotagmin. J. Biol. Chem. 273, 32966–32972. doi: 10.1074/jbc. 273.49.32966
Cohen, J. E., Lee, P. R., Chen, S., Li, W., and Fields, R. D. (2011). MicroRNA regulation of homeostatic synaptic plasticity. Proc. Natl. Acad. Sci. U S A 108, 11650–11655. doi: 10.1073/pnas.1017576108
Crèvecœur, J., Foerch, P., Doupagne, M., Thielen, C., Vandenplas, C., Moonen, G., et al. (2013). Expression of SV2 isoforms during rodent brain development. BMC Neurosci. 14:87. doi: 10.1186/1471-2202-14-87
Crèvecœur, J., Kaminski, R. M., Rogister, B., Foerch, P., Vandenplas, C., Neveux, M., et al. (2014). Expression pattern of synaptic vesicle protein 2 (SV2) isoforms in patients with temporal lobe epilepsy and hippocampal sclerosis. Neuropathol. Appl. Neurobiol. 40, 191–204. doi: 10.1111/nan. 12054
Crowder, K. M., Gunther, J. M., Jones, T. A., Hale, B. D., Zhang, H. Z., Peterson, M. R., et al. (1999). Abnormal neurotransmission in mice lacking synaptic vesicle protein 2A (SV2A). Proc. Natl. Acad. Sci. U S A 96, 15268–15273. doi: 10.1073/pnas.96.26.15268
Custer, K. L., Austin, N. S., Sullivan, J. M., and Bajjalieh, S. M. (2006). Synaptic vesicle protein 2 enhances release probability at quiescent synapses. J. Neurosci. 26, 1303–1313. doi: 10.1523/JNEUROSCI.2699-05.2006
Dardou, D., Dassesse, D., Cuvelier, L., Deprez, T., De Ryck, M., and Schiffmann, S. N. (2011). Distribution of SV2C mRNA and protein expression in the mouse brain with a particular emphasis on the basal ganglia system. Brain Res. 1367, 130–145. doi: 10.1016/j.brainres.2010.09.063
Dardou, D., Monlezun, S., Foerch, P., Courade, J. P., Cuvelier, L., De Ryck, M., et al. (2013). A role for Sv2c in basal ganglia functions. Brain Res. 1507, 61–73. doi: 10.1016/j.brainres.2013.02.041
Darstein, M., Petralia, R. S., Swanson, G. T., Wenthold, R. J., and Heinemann, S. F. (2003). Distribution of kainate receptor subunits at hippocampal mossy fiber synapses. J. Neurosci. 23, 8013–8019.
Dennis, N. A., Browndyke, J. N., Stokes, J., Need, A., Burke, J. R., Welsh-Bohmer, K. A., et al. (2010). Temporal lobe functional activity and connectivity in young adult APOE ε4 carriers. Alzheimers Dement. 6, 303–311. doi: 10.1016/j.jalz.2009.07.003
Detrait, E., Maurice, T., Hanon, E., Leclercq, K., and Lamberty, Y. (2014). Lack of synaptic vesicle protein SV2B protects against amyloid-β25–35 -induced oxidative stress, cholinergic deficit and cognitive impairment in mice. Behav. Brain Res. 271, 277–285. doi: 10.1016/j.bbr.2014.06.013
de Groot, M., Toering, S. T., Boer, K., Spliet, W. G., Heimans, J. J., Aronica, E., et al. (2010). Expression of synaptic vesicle protein 2A in epilepsy-associated brain tumors and in the peritumoral cortex. Neuro Oncol. 12, 265–273. doi: 10.1093/neuonc/nop028
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
Dong, M., Liu, H., Tepp, W. H., Johnson, E. A., Janz, R., and Chapman, E. R. (2008). Glycosylated SV2A and SV2B mediate the entry of botulinum neurotoxin e into neurons. Mol. Biol. Cell 19, 5226–5237. doi: 10.1091/mbc. E08-07-0765
Dong, M., Yeh, F., Tepp, W. H., Dean, C., Johnson, E. A., Janz, R., et al. (2006). SV2 is the protein receptor for botulinum neurotoxin A. Science 312, 592–596. doi: 10.1126/science.1123654
Dunn, A. R., Stout, K. A., Ozawa, M., Lohr, K. M., Hoffman, C. A., Bernstein, A. I., et al. (2017). Synaptic vesicle glycoprotein 2C (SV2C) modulates dopamine release and is disrupted in Parkinsons disease. Proc. Natl. Acad. Sci. U S A 114, E2253–E2262. doi: 10.1073/pnas.1616892114
Edvinsson, J., Warfvinge, K., and Edvinsson, L. (2015). Modulation of inflammatory mediators in the trigeminal ganglion by botulinum neurotoxin type A: an organ culture study. J. Headache Pain 16:555. doi: 10.1186/s10194-015-0555-z
Feany, M. B., Lee, S., Edwards, R. H., and Buckley, K. M. (1992). The synaptic vesicle protein SV2 is a novel type of transmembrane transporter. Cell 70, 861–867. doi: 10.1016/0092-8674(92)90319-8
Feng, G., Xiao, F., Lu, Y., Huang, Z., Yuan, J., Xiao, Z., et al. (2009). Down-regulation synaptic vesicle protein 2A in the anterior temporal neocortex of patients with intractable epilepsy. J. Mol. Neurosci. 39, 354–359. doi: 10.1007/s12031-009-9288-2
Fergestad, T., Davis, W. S., and Broadie, K. (1999). The stoned proteins regulate synaptic vesicle recycling in the presynaptic terminal. J. Neurosci. 19, 5847–5860.
Gassmann, M., Shaban, H., Vigot, R., Sansig, G., Haller, C., Barbieri, S., et al. (2004). Redistribution of GABAB(1) protein and atypical GABAB responses in GABAB(2) -deficient mice. J. Neurosci. 24, 6086–6097. doi: 10.1523/JNEUROSCI.5635-03.2004
Geppert, M., Archer, B. T. III., and Sudhof, T. C. (1991). Synaptotagmin II. A novel differentially distributed form of synaptotagmin. J. Biol. Chem. 266, 13548–13552.
Gillard, M., Fuks, B., Leclercq, K., and Matagne, A. (2011). Binding characteristics of brivaracetam, a selective, high affinity SV2A ligand in rat, mouse and human brain: relationship to anti-convulsant properties. Eur. J. Pharmacol. 664, 36–44. doi: 10.1016/j.ejphar.2011. 04.064
Gómez Ravetti, M., Rosso, O. A., Berretta, R., and Moscato, P. (2010). Uncovering molecular biomarkers that correlate cognitive decline with the changes of hippocampus’ gene expression profiles in Alzheimer’s disease. PLoS One 5:e10153. doi: 10.1371/journal.pone.0010153
Gordon, S. L., and Cousin, M. A. (2016). The iTRAPs: guardians of synaptic vesicle cargo retrieval during endocytosis. Front. Synaptic Neurosci. 8:1. doi: 10.3389/fnsyn.2016.00001
Grønborg, M., Pavlos, N. J., Brunk, I., Chua, J. J., Münster-Wandowski, A., Riedel, D., et al. (2010). Quantitative comparison of glutamatergic and GABAergic synaptic vesicles unveils selectivity for few proteins including MAL2, a novel synaptic vesicle protein. J. Neurosci. 30, 2–12. doi: 10.1523/JNEUROSCI.4074-09.2010
Gulyás, A. I., Megías, M., Emri, Z., and Freund, T. F. (1999). Total number and ratio of excitatory and inhibitory synapses converging onto single interneurons of different types in the CA1 area of the rat hippocampus. J. Neurosci. 19, 10082–10097.
Hanaya, R., Hosoyama, H., Sugata, S., Tokudome, M., Hirano, H., Tokimura, H., et al. (2012). Low distribution of synaptic vesicle protein 2A and synaptotagimin-1 in the cerebral cortex and hippocampus of spontaneously epileptic rats exhibiting both tonic convulsion and absence seizure. Neuroscience 221, 12–20. doi: 10.1016/j.neuroscience.2012.06.058
Haucke, V., and De Camilli, P. (1999). AP-2 recruitment to synaptotagmin stimulated by tyrosine-based endocytic motifs. Science 285, 1268–1271. doi: 10.1126/science.285.5431.1268
Haucke, V., Wenk, M. R., Chapman, E. R., Farsad, K., and De Camilli, P. (2000). Dual interaction of synaptotagmin with mu2- and alpha-adaptin facilitates clathrin-coated pit nucleation. EMBO J. 19, 6011–6019. doi: 10.1093/emboj/19. 22.6011
Heese, K., Nagai, Y., and Sawada, T. (2001). Identification of a new synaptic vesicle protein 2B mRNA transcript which is up-regulated in neurons by amyloid beta peptide fragment (1–42). Biochem. Biophys. Res. Commun. 289, 924–928. doi: 10.1006/bbrc.2001.5932
Hill-Burns, E. M., Singh, N., Ganguly, P., Hamza, T. H., Montimurro, J., Kay, D. M., et al. (2013). A genetic basis for the variable effect of smoking/nicotine on Parkinson’s disease. Pharmacogenomics J. 13, 530–537. doi: 10.1038/tpj.2012.38
Hovinga, C. A. (2001). Levetiracetam: a novel antiepileptic drug. Pharmacotherapy 21, 1375–1388. doi: 10.1592/phco.21.17.1375.34432
Hui, E., Johnson, C. P., Yao, J., Dunning, F. M., and Chapman, E. R. (2009). Synaptotagmin-mediated bending of the target membrane is a critical step in Ca2+ -regulated fusion. Cell 138, 709–721. doi: 10.1016/j.cell.2009.05.049
Iezzi, M., Theander, S., Janz, R., Loze, C., and Wollheim, C. B. (2005). SV2A and SV2C are not vesicular Ca2+ transporters but control glucose-evoked granule recruitment. J. Cell Sci. 118, 5647–5660. doi: 10.1242/jcs.02658
Ito, I., Futai, K., Katagiri, H., Watanabe, M., Sakimura, K., Mishina, M., et al. (1997). Synapse-selective impairment of NMDA receptor functions in mice lacking NMDA receptor epsilon 1 or epsilon 2 subunit. J. Physiol. 500, 401–408. doi: 10.1113/jphysiol.1997.sp022030
Jaffe, D. B., and Carnevale, N. T. (1999). Passive normalization of synaptic integration influenced by dendritic architecture. J. Neurophysiol. 82, 3268–3285.
Janz, R., Goda, Y., Geppert, M., Missler, M., and Südhof, T. C. (1999). SV2A and SV2B function as redundant Ca2+ regulators in neurotransmitter release. Neuron 24, 1003–1016. doi: 10.1016/s0896-6273(00)81046-6
Janz, R., Hofmann, K., and Sudhof, T. C. (1998). SVOP, an evolutionarily conserved synaptic vesicle protein, suggests novel transport functions of synaptic vesicles. J. Neurosci. 18, 9269–9281.
Janz, R., and Sudhof, T. C. (1999). Sv2C is a synaptic vesicle protein with an unusually restricted localization: anatomy of a synaptic vesicle protein family. Neuroscience 94, 1279–1290. doi: 10.1016/s0306-4522(99)00370-x
Jung, N., Wienisch, M., Gu, M., Rand, J. B., Müller, S. L., Krause, G., et al. (2007). Molecular basis of synaptic vesicle cargo recognition by the endocytic sorting adaptor stonin 2. J. Cell Biol. 179, 1497–1510. doi: 10.1083/jcb.200708107
Kaempf, N., Kochlamazashvili, G., Puchkov, D., Maritzen, T., Bajjalieh, S. M., Kononenko, N. L., et al. (2015). Overlapping functions of stonin 2 and SV2 in sorting of the calcium sensor synaptotagmin 1 to synaptic vesicles. Proc. Natl. Acad. Sci. U S A 112, 7297–7302. doi: 10.1073/pnas.1501627112
Kawakami, R., Shinohara, Y., Kato, Y., Sugiyama, H., Shigemoto, R., and Ito, I. (2003). Asymmetrical allocation of NMDA receptor epsilon2 subunits in hippocampal circuitry. Science 300, 990–994. doi: 10.1126/science.10 82609
Kislinger, T., Cox, B., Kannan, A., Chung, C., Hu, P., Ignatchenko, A., et al. (2006). Global survey of organ and organelle protein expression in mouse: combined proteomic and transcriptomic profiling. Cell 125, 173–186. doi: 10.1016/j.cell. 2006.01.044
Kononenko, N. L., Diril, M. K., Puchkov, D., Kintscher, M., Koo, S. J., Pfuhl, G., et al. (2013). Compromised fidelity of endocytic synaptic vesicle protein sorting in the absence of stonin 2. Proc. Natl. Acad. Sci. U S A 110, E526–E535. doi: 10.1073/pnas.1218432110
Kulik, A., Vida, I., Luján, R., Haas, C. A., López-Bendito, G., Shigemoto, R., et al. (2003). Subcellular localization of metabotropic GABAB receptor subunits GABAB1a/b and GABAB2 in the rat hippocampus. J. Neurosci. 23, 11026–11035.
Kwon, S. E., and Chapman, E. R. (2012). Glycosylation is dispensable for sorting of synaptotagmin 1 but is critical for targeting of SV2 and synaptophysin to recycling synaptic vesicles. J. Biol. Chem. 287, 35658–35668. doi: 10.1074/jbc. M112.398883
Laruelle, M., Detrait, E., Lamberty, Y., Leclercq, K., Jnoff, E., Wood, M., et al. (2014). Negative modulation of the synaptic vesicle protein (Sv2a): a new pharmacological target for cognitive deficit associated with schizophrenia. Schizophr. Res. 153:S66. doi: 10.1016/s0920-9964(14)70213-0
Lazzell, D. R., Belizaire, R., Thakur, P., Sherry, D. M., and Janz, R. (2004). SV2B regulates synaptotagmin 1 by direct interaction. J. Biol. Chem. 279, 52124–52131. doi: 10.1074/jbc.M407502200
Lee, J., Daniels, V., Sands, Z. A., Lebon, F., Shi, J., and Biggin, P. C. (2015). Exploring the interaction of SV2A with racetams using homology modelling, molecular dynamics and site-directed mutagenesis. PLoS One 10:e0116589. doi: 10.1371/journal.pone.0116589
Levine, K. B., Cloherty, E. K., Fidyk, N. J., and Carruthers, A. (1998). Structural and physiologic determinants of human erythrocyte sugar transport regulation by adenosine triphosphate. Biochemistry 37, 12221–12232. doi: 10.1021/bi98 0585y
Levine, K. B., Cloherty, E. K., Hamill, S., and Carruthers, A. (2002). Molecular determinants of sugar transport regulation by ATP. Biochemistry 41, 12629–12638. doi: 10.1021/bi0258997
Littleton, J. T., Serano, T. L., Rubin, G. M., Ganetzky, B., and Chapman, E. R. (1999). Synaptic function modulated by changes in the ratio of synaptotagmin I and IV. Nature 400, 757–760. doi: 10.1038/23462
Löscher, W., Gillard, M., Sands, Z. A., Kaminski, R. M., and Klitgaard, H. (2016). Synaptic vesicle glycoprotein 2A ligands in the treatment of epilepsy and beyond. CNS Drugs 30, 1055–1077. doi: 10.1007/s40263-016-0384-x
Lynch, B. A., Lambeng, N., Nocka, K., Kensel-Hammes, P., Bajjalieh, S. M., Matagne, A., et al. (2004). The synaptic vesicle protein SV2A is the binding site for the antiepileptic drug levetiracetam. Proc. Natl. Acad. Sci. U S A 101, 9861–9866. doi: 10.1073/pnas.0308208101
Lynch, B. A., Matagne, A., Brännström, A., von Euler, A., Jansson, M., Hauzenberger, E., et al. (2008). Visualization of SV2A conformations in situ by the use of protein tomography. Biochem. Biophys. Res. Commun. 375, 491–495. doi: 10.1016/j.bbrc.2008.07.145
Madeo, M., Kovács, A. D., and Pearce, D. A. (2014). The human synaptic vesicle protein, SV2A, functions as a galactose transporter in Saccharomyces cerevisiae. J. Biol. Chem. 289, 33066–33071. doi: 10.1074/jbc.C114.584516
Magee, J. C., and Cook, E. P. (2000). Somatic EPSP amplitude is independent of synapse location in hippocampal pyramidal neurons. Nat. Neurosci. 3, 895–903. doi: 10.1038/78800
Mahrhold, S., Bergström, T., Stern, D., Dorner, B. G., stot, C., and Rummel, A. (2016). Only the complex N559-glycan in the synaptic vesicle glycoprotein 2C mediates high affinity binding to botulinum neurotoxin serotype A1. Biochem. J. 473, 2645–2654. doi: 10.1042/BCJ20160439
Marszalek, P. E., Farrell, B., Verdugo, P., and Fernandez, J. M. (1997). Kinetics of release of serotonin from isolated secretory granules. I. Amperometric detection of serotonin from electroporated granules. Biophys. J. 73, 1160–1168. doi: 10.1016/s0006-3495(97)78148-7
Martens, S., Kozlov, M. M., and McMahon, H. T. (2007). How synaptotagmin promotes membrane fusion. Science 316, 1205–1209. doi: 10.1126/science. 1142614
Mattheisen, M., Mühleisen, T. W., Strohmaier, J., Treutlein, J., Nenadic, I., Alblas, M., et al. (2012). Genetic variation at the synaptic vesicle gene SV2A is associated with schizophrenia. Schizophr. Res. 141, 262–265. doi: 10.1016/j. schres.2012.08.027
Matveeva, E. A., Vanaman, T. C., Whiteheart, S. W., and Slevin, J. T. (2007). Asymmetric accumulation of hippocampal 7S SNARE complexes occurs regardless of kindling paradigm. Epilepsy Res. 73, 266–274. doi: 10.1016/j. eplepsyres.2006.11.003
Matveeva, E. A., Vanaman, T. C., Whiteheart, S. W., and Slevin, J. T. (2008). Levetiracetam prevents kindling-induced asymmetric accumulation of hippocampal 7S SNARE complexes. Epilepsia 49, 1749–1758. doi: 10.1111/j. 1528-1167.2008.01687.x
Megías, M., Emri, Z., Freund, T. F., and Gulyás, A. I. (2001). Total number and distribution of inhibitory and excitatory synapses on hippocampal CA1 pyramidal cells. Neuroscience 102, 527–540. doi: 10.1016/s0306-4522(00)00496-6
Menten-Dedoyart, C., Serrano Navacerrada, M. E., Bartholome, O., Sánchez Gil, J., Neirinckx, V., Wislet, S., et al. (2016). Development and validation of a new mouse model to investigate the role of SV2A in epilepsy. PLoS One 11:e0166525. doi: 10.1371/journal.pone.0166525
Miles, R., and Wong, R. K. (1984). Unitary inhibitory synaptic potentials in the guinea-pig hippocampus in vitro. J. Physiol. 356, 97–113. doi: 10.1113/jphysiol. 1984.sp015455
Miles, R., and Wong, R. K. (1986). Excitatory synaptic interactions between CA3 neurones in the guinea-pig hippocampus. J. Physiol. 373, 397–418. doi: 10.1113/jphysiol.1986.sp016055
Morgans, C. W., Kensel-Hammes, P., Hurley, J. B., Burton, K., Idzerda, R., McKnight, G. S., et al. (2009). Loss of the synaptic vesicle protein SV2B results in reduced neurotransmission and altered synaptic vesicle protein expression in the retina. PLoS One 4:e5230. doi: 10.1371/journal.pone.0005230
Mudge, J., Miller, N. A., Khrebtukova, I., Lindquist, I. E., May, G. D., Huntley, J. J., et al. (2008). Genomic convergence analysis of schizoprenia: mRNA sequencing reveals altered synaptic vesicular transport in post-mortem cerebellum. PLoS One 3:e3625. doi: 10.1371/journal.pone.0003625
Mullen, G. P., Grundahl, K. M., Gu, M., Watanabe, S., Hobson, R. J., Crowell, J. A., et al. (2012). UNC-41/stonin functions with AP2 to recycle synaptic vesicles in Caenorhabditis elegans. PLoS One 7:e40095. doi: 10.1371/journal.pone.0040095
Nanavati, C., and Fernandez, J. M. (1993). The secretory granule matrix: a fast-acting smart polymer. Science 259, 963–965. doi: 10.1126/science.8438154
Nensa, F. M., Neumann, M. H., Schrötter, A., Przyborski, A., Mastalski, T., Susdalzew, S., et al. (2014). Amyloid betaA4 precursor protein-binding family B member 1 (FE65) interactomics revealed synaptic vesicle glycoprotein 2A (SV2A) and sarcoplasmic/endoplasmic reticulum calcium ATPase 2 (SERCA2) as new binding proteins in the human brain. Mol. Cell. Proteomics 13, 475–488. doi: 10.1074/mcp.M113.029280
Nowack, A., Malarkey, E. B., Yao, J., Bleckert, A., Hill, J., and Bajjalieh, S. M. (2011). Levetiracetam reverses synaptic deficits produced by overexpression of SV2A. PLoS One 6:e29560. doi: 10.1371/journal.pone.0029560
Nowack, A., Yao, J., Custer, K. L., and Bajjalieh, S. M. (2010). SV2 regulates neurotransmitter release via multiple mechanisms. Am. J. Physiol. Cell Physiol. 299, C960–C967. doi: 10.1152/ajpcell.00259.2010
Ohno, Y., Ishihara, S., Terada, R., Kikuta, M., Sofue, N., Kawai, Y., et al. (2009). Preferential increase in the hippocampal synaptic vesicle protein 2A (SV2A) by pentylenetetrazole kindling. Biochem. Biophys. Res. Commun. 390, 415–420. doi: 10.1016/j.bbrc.2009.09.035
Ohno, Y., Okumura, T., Terada, R., Ishihara, S., Serikawa, T., and Sasa, M. (2012). Kindling-associated SV2A expression in hilar GABAergic interneurons of the mouse dentate gyrus. Neurosci. Lett. 510, 93–98. doi: 10.1016/j.neulet.2012. 01.009
Peng, L., Tepp, W. H., Johnson, E. A., and Dong, M. (2011). Botulinum neurotoxin D uses synaptic vesicle protein SV2 and gangliosides as receptors. PLoS Pathog. 7:e1002008. doi: 10.1371/journal.ppat.1002008
Pyle, R. A., Schivell, A. E., Hidaka, H., and Bajjalieh, S. M. (2000). Phosphorylation of synaptic vesicle protein 2 modulates binding to synaptotagmin. J. Biol. Chem. 275, 17195–17200. doi: 10.1074/jbc.M000674200
Quiroz, Y. T., Budson, A. E., Celone, K., Ruiz, A., Newmark, R., Castrillón, G., et al. (2010). Hippocampal hyperactivation in presymptomatic familial Alzheimer’s disease. Ann. Neurol. 68, 865–875. doi: 10.1002/ana.22105
Reigada, D., Díez-Pérez, I., Gorostiza, P., Verdaguer, A., Gómez de Aranda, I., Pineda, O., et al. (2003). Control of neurotransmitter release by an internal gel matrix in synaptic vesicles. Proc. Natl. Acad. Sci. U S A 100, 3485–3490. doi: 10.1073/pnas.0336914100
Rogawski, M. A. (2016). A new SV2A ligand for epilepsy. Cell 167:587. doi: 10.1016/j.cell.2016.09.057
Schivell, A. E., Batchelor, R. H., and Bajjalieh, S. M. (1996). Isoform-specific, calcium-regulated interaction of the synaptic vesicle proteins SV2 and synaptotagmin. J. Biol. Chem. 271, 27770–27775. doi: 10.1074/jbc.271.44. 27770
Schivell, A. E., Mochida, S., Kensel-Hammes, P., Custer, K. L., and Bajjalieh, S. M. (2005). SV2A and SV2C contain a unique synaptotagmin-binding site. Mol. Cell. Neurosci. 29, 56–64. doi: 10.1016/j.mcn.2004.12.011
Scranton, T. W., Iwata, M., and Carlson, S. S. (1993). The SV2 protein of synaptic vesicles is a keratan sulfate proteoglycan. J. Neurochem. 61, 29–44. doi: 10.1111/j.1471-4159.1993.tb03535.x
Serajee, F. J., and Huq, A. M. (2015). Homozygous mutation in synaptic vesicle glycoprotein 2A gene results in intractable epilepsy, involuntary movements, microcephaly and developmental and growth retardation. Pediatr. Neurol. 52, 642–646. doi: 10.1016/j.pediatrneurol.2015.02.011
Sharma, A. K., Reams, R. Y., Jordan, W. H., Miller, M. A., Thacker, H. L., and Snyder, P. W. (2007). Mesial temporal lobe epilepsy: pathogenesis, induced rodent models and lesions. Toxicol. Pathol. 35, 984–999. doi: 10.1080/01926230701748305
Shi, J., Anderson, D., Lynch, B. A., Castaigne, J. G., Foerch, P., and Lebon, F. (2011). Combining modelling and mutagenesis studies of synaptic vesicle protein 2A to identify a series of residues involved in racetam binding. Biochem. Soc. Trans. 39, 1341–1347. doi: 10.1042/BST0391341
Silver, D. J., and Silver, J. (2014). Contributions of chondroitin sulfate proteoglycans to neurodevelopment, injury and cancer. Curr. Opin. Neurobiol. 27, 171–178. doi: 10.1016/j.conb.2014.03.016
Smith, P. D., Coulson-Thomas, V. J., Foscarin, S., Kwok, J. C., and Fawcett, J. W. (2015). ‘‘GAG-ing with the neuron’’: the role of glycosaminoglycan patterning in the central nervous system. Exp. Neurol. 274, 100–114. doi: 10.1016/j. expneurol.2015.08.004
Snow, A. D., Nochlin, D., Sekiguichi, R., and Carlson, S. S. (1996). Identification and immunolocalization of a new class of proteoglycan (keratan sulfate) to the neuritic plaques of alzheimers disease. Exp. Neurol. 138, 305–317. doi: 10.1006/exnr.1996.0069
Steinberg, A., Frederiksen, S. D., Blixt, F. W., Warfvinge, K., and Edvinsson, L. (2016). Expression of messenger molecules and receptors in rat and human sphenopalatine ganglion indicating therapeutic targets. J. Headache Pain 17:78. doi: 10.1186/s10194-016-0664-3
Stockburger, C., Miano, D., Baeumlisberger, M., Pallas, T., Arrey, T. N., Karas, M., et al. (2016). A mitochondrial role of SV2a protein in aging and Alzheimer’s disease: studies with levetiracetam. J. Alzheimers Dis. 50, 201–215. doi: 10.3233/JAD-150687
Swerdlow, R. H. (2012). Mitochondria and cell bioenergetics: increasingly recognized components and a possible etiologic cause of Alzheimer’s disease. Antioxid. Redox Signal. 16, 1434–1455. doi: 10.1089/ars.2011.4149
Takeda-Uchimura, Y., Uchimura, K., Sugimura, T., Yanagawa, Y., Kawasaki, T., Komatsu, Y., et al. (2015). Requirement of keratan sulfate proteoglycan phosphacan with a specific sulfation pattern for critical period plasticity in the visual cortex. Exp. Neurol. 274, 145–155. doi: 10.1016/j.expneurol.2015. 08.005
Tan, M. G., Chua, W. T., Esiri, M. M., Smith, A. D., Vinters, H. V., and Lai, M. K. (2010). Genome wide profiling of altered gene expression in the neocortex of Alzheimer’s disease. J. Neurosci. Res. 88, 1157–1169. doi: 10.1002/jnr.22290
Tighe, A. P., and Schiavo, G. (2013). Botulinum neurotoxins: mechanism of action. Toxicon 67, 87–93. doi: 10.1016/j.toxicon.2012.11.011
Toering, S. T., Boer, K., de Groot, M., Troost, D., Heimans, J. J., Spliet, W. G., et al. (2009). Expression patterns of synaptic vesicle protein 2A in focal cortical dysplasia and TSC-cortical tubers. Epilepsia 50, 1409–1418. doi: 10.1111/j.1528-1167.2008.01955.x
Tokudome, K., Okumura, T., Shimizu, S., Mashimo, T., Takizawa, A., Serikawa, T., et al. (2016a). Synaptic vesicle glycoprotein 2A (SV2A) regulates kindling epileptogenesis via GABAergic neurotransmission. Sci. Re. 6:27420. doi: 10.1038/srep27420
Tokudome, K., Okumura, T., Terada, R., Shimizu, S., Kunisawa, N., Mashimo, T., et al. (2016b). A missense mutation of the gene encoding synaptic vesicle glycoprotein 2A (SV2A) confers seizure susceptibility by disrupting amygdalar synaptic GABA release. Front. Pharmacol. 7:210. doi: 10.3389/fphar.2016.00210
Um, J. W., and Ko, J. (2013). LAR-RPTPs: synaptic adhesion molecules that shape synapse development. Trends Cell Biol. 23, 465–475. doi: 10.1016/j.tcb.2013. 07.004
Venkatesan, K., Alix, P., Marquet, A., Doupagne, M., Niespodziany, I., Rogister, B., et al. (2012). Altered balance between excitatory and inhibitory inputs onto CA1 pyramidal neurons from SV2A-deficient but not SV2B-deficient mice. J. Neurosci. Res. 90, 2317–2327. doi: 10.1002/jnr.23111
Verderio, C., Rossetto, O., Grumelli, C., Frassoni, C., Montecucco, C., and Matteoli, M. (2006). Entering neurons: botulinum toxins and synaptic vesicle recycling. EMBO Rep. 7, 995–999. doi: 10.1038/sj.embor.7400796
van Vliet, E. A., Aronica, E., Redeker, S., Boer, K., and Gorter, J. A. (2009). Decreased expression of synaptic vesicle protein 2A, the binding site for levetiracetam, during epileptogenesis and chronic epilepsy. Epilepsia 50, 422–433. doi: 10.1111/j.1528-1167.2008.01727.x
Walther, K., Diril, M. K., Jung, N., and Haucke, V. (2004). Functional dissection of the interactions of stonin 2 with the adaptor complex AP-2 and synaptotagmin.
Walther, K., Krauss, M., Diril, M. K., Lemke, S., Ricotta, D., Honing, S., et al. (2001). Human stoned B interacts with AP-2 and synaptotagmin and facilitates clathrin-coated vesicle uncoating. EMBO Rep. 2, 634–640. doi: 10.1093/embo-reports/kve134
Wan, Q. F., Zhou, Z. Y., Thakur, P., Vila, A., Sherry, D. M., Janz, R., et al. (2010). SV2 acts via presynaptic calcium to regulate neurotransmitter release. Neuron 66, 884–895. doi: 10.1016/j.neuron.2010.05.010
Wang, M. M., Janz, R., Belizaire, R., Frishman, L. J., and Sherry, D. M. (2003). Differential distribution and developmental expression of synaptic vesicle protein 2 isoforms in the mouse retina. J. Comp. Neurol. 460, 106–122. doi: 10.1002/cne.10636
Weisemann, J., Stern, D., Mahrhold, S., Dorner, B. G., and Rummel, A. (2016). Botulinum neurotoxin serotype a recognizes its protein receptor SV2 by a different mechanism than botulinum neurotoxin B synaptotagmin. Toxins 8:e154. doi: 10.3390/toxins8050154
Xu, T., and Bajjalieh, S. M. (2001). SV2 modulates the size of the readily releasable pool of secretory vesicles. Nat. Cell Biol. 3, 691–698. doi: 10.1038/35087000
Xu, P. T., Li, Y. J., Qin, X. J., Scherzer, C. R., Xu, H., Schmechel, D. E., et al. (2006). Differences in apolipoprotein E3/3 and E4/4 allele-specific gene expression in hippocampus in Alzheimer disease. Neurobiol. Dis. 21, 256–275. doi: 10.1016/j. nbd.2005.07.004
Xu, J., Mashimo, T., and Südhof, T. C. (2007). Synaptotagmin-1, -2, and -9: Ca2+ sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron 54, 567–581. doi: 10.1016/j.neuron.2007.05.004
Yao, J., and Bajjalieh, S. M. (2008). Synaptic vesicle protein 2 binds adenine nucleotides. J. Biol. Chem. 283, 20628–20634. doi: 10.1074/jbc.M800738200
Yao, J., and Bajjalieh, S. M. (2009). SVOP is a nucleotide binding protein. PLoS One 4:e5315. doi: 10.1371/journal.pone.0005315
Yao, J., de la Iglesia, H. O., and Bajjalieh, S. M. (2013). Loss of the SV2-like protein SVOP produces no apparent deficits in laboratory mice. PLoS One 8:e68215. doi: 10.1371/journal.pone.0068215
Yao, J., Nowack, A., Kensel-Hammes, P., Gardner, R. G., and Bajjalieh, S. M. (2010). Co-trafficking of SV2 and synaptotagmin at the synapse. J. Neurosci. 30, 5569–5578. doi: 10.1523/JNEUROSCI.4781-09.2010
Yao, G., Zhang, S., Mahrhold, S., Lam, K. H., Stern, D., Bagramyan, K., et al. (2016). N-linked glycosylation of SV2 is required for binding and uptake of botulinum neurotoxin A. Nat. Struct. Mol. Biol. 23, 656–662. doi: 10.1038/ns mb.3245
Zhang, N., Gordon, S. L., Fritsch, M. J., Esoof, N., Campbell, D. G., Gourlay, R., et al. (2015). Phosphorylation of synaptic vesicle protein 2A at Thr84 by casein kinase 1 family kinases controls the specific retrieval of synaptotagmin-1. J. Neurosci. 35, 2492–2507. doi: 10.1523/JNEUROSCI.4248-14.2015
Zhang, H., Uchimura, K., and Kadomatsu, K. (2006). Brain keratan sulfate and glial scar formation. Ann. N Y Acad. Sci. 1086, 81–90. doi: 10.1093/glycob/cwj115