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http://dx.doi.org/10.14348/molcells.2015.0233

Synapsin Isoforms and Synaptic Vesicle Trafficking  

Song, Sang-Ho (Lee Kong Chian School of Medicine)
Augustine, George J. (Lee Kong Chian School of Medicine)
Abstract
Synapsins were the first presynaptic proteins identified and have served as the flagship of the presynaptic protein field. Here we review recent studies demonstrating that different members of the synapsin family play different roles at presynaptic terminals employing different types of synaptic vesicles. The structural underpinnings for these functions are just beginning to be understood and should provide a focus for future efforts.
Keywords
neurotransmitter release; presynaptic terminals; synapsins; synaptic vesicles; vesicle trafficking;
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1 Baldelli, P., Fassio, A., Valtorta, F., and Benfenati, F. (2007). Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses. J. Neurosci. 27, 13520-13531.   DOI
2 Brautigam, C.A., Chelliah, Y., and Deisenhofer, J. (2004). Tetramerization and ATP binding by a protein comprising the A, B, and C domains of rat synapsin I. J. Biol. Chem., 279, 11948-11956.   DOI
3 Cavalleri, G.L., Weale, M.E., Shianna, K.V., Singh, R., Lynch, J.M., Grinton, B., Szoeke, C., Murphy, K., Kinirons, P., O'Rourke, D., et al. (2007). Multicentre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: a case-control study. Lancet Neurol. 6, 970-980.   DOI
4 Cheetham, J.J., Hilfiker, S., Benfenati, F., Weber, T., Greengard, P., and Czernik, A.J. (2001). Identification of synapsin I peptides that insert into lipid membranes. Biochem. J. 354, 57-66.   DOI
5 Chi, P., Greengard, P., and Ryan, T.A. (2003). Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38, 69-78.   DOI
6 Dyck, B.A., Beyaert, M.G., Ferro, M.A., and Mishra, R.K. (2011). Medial prefrontal cortical synapsin II knock-down induces behavioral abnormalities in the rat: examining synapsin II in the pathophysiology of schizophrenia. Schizophr Res. 130, 250-259.   DOI
7 Esser, L., Wang, C.R., Hosaka, M., Smagula, C.S., C.Südhof, T.C., and Deisenhofer, J. (1998). Synapsin I is structurally similar to ATP-utilizing enzymes. EMBO J. 17, 977-984.   DOI
8 Evergren, E., Marcucci, M., Tomilin, N., Low, P., Slepnev, V., Andersson, F., Gad, H., Brodin, L., De Camilli, P., and Shupliakov, O. (2004). Amphiphysin is a component of clathrin coats formed during synaptic vesicle recycling at the lamprey giant synapse. Traffic 5, 514-528.   DOI
9 Feng, J., Chi, P., Blanpied, T.A, Xu, Y., Magarinos, A.M., Ferreira, A., Takahashi, R.H., Kao, H.-T., McEwen, B.S., Ryan, T.A., et al. (2002). Regulation of neurotransmitter release by synapsin III. J. Neurosci. 22, 4372-4380.   DOI
10 Garcia, C.C., Blair, H.J., Seager, M., Coulthard, A., Tennant, S., Buddles, M., Curtis, A., and Goodship, J.A. (2004). Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy. J. Med. Genet. 41,183-186.   DOI
11 Giovedì, S., Darchen, F., Valtorta, F., Greengard, P., and Benfenati, F. (2004). Synapsin is a novel Rab3 effector protein on small synaptic vesicles: II. Functional effects of the Rab3A-synapsin I interaction. J. Biol. Chem. 279, 43769-43779.   DOI
12 Gitler, D., Xu, Y., Kao, H.-T., Lin, D., Lim, S., Feng, J., Greengard, P., and Augustine, G.J. (2004a). Molecular determinants of synapsin targeting to presynaptic terminals. J. Neurosci. 24, 3711-3720.   DOI
13 Gitler, D., Takagishi, Y., Feng, J., Ren, Y., Rodriguiz, R.M., Wetsel, W.C., Greengard, P., and Augustine, G.J. (2004b). Different presynaptic roles of synapsins at excitatory and inhibitory synapses. J. Neurosci. 24, 11368-11380.   DOI
14 Gitler, D., Cheng, Q., Greengard, P., and Augustine, G.J. (2008). Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles. J. Neurosci. 28, 10835-10843.   DOI
15 Hilfiker, S., Schweizer, F.E., Kao, H.T., Czernik, A.J., Greengard, P., and Augustine, G.J. (1998). Two sites of action for synapsin domain E in regulating neurotransmitter release. Nat. Neurosci. 1, 29-35.   DOI
16 Hilfiker, S., Pieribone, V.A., Czernik, A.J., Kao, H.T., Augustine, G.J., and Greengard, P. (1999). Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 354, 269-279.   DOI
17 Jovanovic, J.N., Benfenati, F., Siow, Y.L., Sihra, T.S., Sanghera, J.S., Pelech, S.L., Greengard, P., and Czernik, A.J. (1996). Neurotrophins stimulate phosphorylation of synapsin I by MAP kinase and regulate synapsin I-actin interactions. Proc. Natl. Acad. Sci. USA 93, 3679-3683.   DOI
18 Hilfiker, S., Benfenati, F., Doussau, F., Nairn, A.C., Czernik, A.J., Augustine, G.J., and Greengard, P. (2005). Structural domains involved in the regulation of transmitter release by synapsins. J. Neurosci. 25, 2658-2669.   DOI
19 Hosaka, M., and Südhof, T.C. (1998). Synapsin III, a Novel Synapsin with an Unusual Regulation by $Ca^{2+}$. J. Biol. Chem. 273, 13371-13374.   DOI
20 Hosaka, M., and Südhof, T.C. (1999). Homo- and heterodimerization of synapsins. J. Biol. Chem. 274, 16747-16753.   DOI
21 Kao, H.T., Porton, B., Czernik, A. J., Feng, J., Yiu, G., Haring, M., Benfenati, F., and Greengard, P. (1998). A third member of the synapsin gene family. Proc. Natl. Acad. Sci. USA 95, 4667-4672.   DOI
22 Kile, B.M., Guillot, T.S., Venton, B.J., Wetsel, W.C., Augustine, G.J., and Wightman, R.M. (2010). Synapsins differentially control dopamine and serotonin release. J. Neurosci. 30, 9762-9770.   DOI
23 Li, L., Chin, L.S., Shupliakov, O., Brodin, L., Sihra, T.S., Hvalby, O., Jensen, V., Zheng, D.,McNamara, J.O., Greengard, P., et al., (1995). Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice. Proc. Natl. Acad. Sci. USA 92, 9235-9239.   DOI
24 Llinas, R., Gruner, J.A., Sugimori, M., McGuinness, T.L., Greengard, P. (1991). Regulation by synapsin I and $Ca^{2+}$-calmodulindependent protein kinase II of the transmitter release in squid giant synapse. J. Physiol. 436, 257-282.   DOI
25 Pieribone, V.A., Shupliakov, O., Brodin, L., Hilfiker, S., Czernik, A.J., Greengard, P. (1995) Distinct pools of synaptic vesicles in neurotransmitter release. Nature 375, 493-497.   DOI
26 Medrihan, L., Cesca, F., Raimondi, A., Lignani, G., Baldelli, P., and Benfenati, F. (2013). Synapsin II desynchronizes neurotransmitter release at inhibitory synapses by interacting with presynaptic calcium channels. Nat. Commun. 4, 1512.   DOI
27 Mirnics, K., Middleton, F.A., Marquez, A., Lewis, D.A., Levitt, P. (2000). Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex. Neuron 28, 53-67.   DOI
28 Monaldi, I., Vassalli, M., Bachi, A., Giovedì, S., Millo, E., Valtorta, F., Raiteri, R., Benfenati, F., and Fassio, A. (2010). The highly conserved synapsin domain E mediates synapsin dimerization and phospholipid vesicle clustering. Biochem. J. 426, 55-64.   DOI
29 Porton, B., Ferreira, A., DeLisi, L.E., and Kao, H.T. (2004). A rare polymorphism affects a mitogen-activated protein kinase site in synapsin III: Possible relationship to schizophrenia. Biol. Psychiatry 55, 118-125.   DOI
30 Porton, B., Wetsel, W.C., Kao, H.T. (2011). Synapsin III: role in neuronal plasticity and disease. Semin Cell Dev. Biol. 22, 416-424.   DOI
31 Rosahl, T.W., Spillane, D., Missler, M., Herz, J., Selig, D.K., Wolff, J.R., Hammer, R.E., Malenka, R.C., Sudhof, T.C. (1995). Essential functions of synapsins I and II in synaptic vesicle regulation. Nature 375, 488-493.   DOI
32 Song, SH., and Augustine, J.G. (2014). Synapsin isoforms regulating GABA release from hippocampal interneurons. Annual Meeting of Society for Neuroscience 783,12.
33 Venton, B.J., Seipel, A.T., Phillips, P.E.M., Wetsel, W.C., Gitler, D., Greengard, P., Augustine, G.J., and Wightman, R.M. (2006). Cocaine increases dopamine release by mobilization of a synapsin-dependent reserve pool. J. Neurosci. 26, 3206-3209.   DOI
34 Südhof, T.C., Czernik, A.J., Kao, H.T., Takei, K., Johnston, P.A., Horiuchi, A., Kanazir, S.D., Wagner, M.A., Perin, M.S., and De Camilli, P. (1989). Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. Science 245, 1474-1480.   DOI
35 Tan, M.L., Dyck, B.A., Gabriele, J., Daya, R.P., Thomas, N., Sookram, C., Basu, D., Ferro, M.A., Chong, V.Z., and Mishra, R.K. (2014). Synapsin II gene expression in the dorsolateral prefrontal cortex of brain specimens from patients with schizophrenia and bipolar disorder: effect of lifetime intake of antipsychotic drugs. Pharmacogenomics J.14, 63-69.   DOI
36 Vawter, M.P., Thatcher, L., Usen, N., Hyde, T.M., Kleinman, J.E., and Freed, W.J. (2002). Reduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia. Mol. Psychiatry 7, 571-578.   DOI
37 Villanueva, M., Thornley, K., Augustine, G.J., and Wightman, R.M. (2006). Synapsin II negatively regulates catecholamine release. Brain Cell Biol. 35, 125-136.