The synapsins: Key actors of synapse function and plasticity
Abstract
The synapsins are a family of neuronal phosphoproteins evolutionarily conserved in invertebrate and vertebrate organisms. Their best-characterised function is to modulate neurotransmitter release at the pre-synaptic terminal, by reversibly tethering synaptic vesicles (SVs) to the actin cytoskeleton. However, many recent data have suggested novel functions for synapsins in other aspects of the pre-synaptic physiology, such as SV docking, fusion and recycling. Synapsin activity is tightly regulated by several protein kinases and phosphatases, which modulate the association of synapsins to SVs as well as their interaction with actin filaments and other synaptic proteins. In this context, synapsins act as a link between extracellular stimuli and the intracellular signalling events activated upon neuronal stimulation. Genetic manipulation of synapsins in various in vivo models has revealed that, although not essential for the basic development and functioning of neuronal networks, these proteins are extremely important in the fine-tuning of neuronal plasticity, as shown by the epileptic phenotype and behavioural abnormalities characterising mouse lines lacking one or more synapsin isoforms. In this review, we summarise the current knowledge about how the various members of the synapsin family are involved in the modulation of the pre-synaptic physiology. We give a comprehensive description of the molecular basis of synapsin function, as well as an overview of the more recent evidence linking mutations in the synapsin proteins to the onset of severe central nervous system diseases such as epilepsy and schizophrenia.
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?
Synapsins are critical in synapse function and plasticity.
“These synapsins are critical in synapse function and plasticity.166”
From Epigenetic regulation in major depression and other stress-related disorders: molecular mechanisms, clinical relevance and therapeutic potential (2023) · cites this paper as [166]
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
Rab GTPases as coordinators of vesicle traffic
Stenmark, H. (2009) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm2728 · Cited by 3,413 · see citing works
Cahoy, J. D., Emery, B., Kaushal, A., Foo, L. C., Zamanian, J. L., Christopherson, K. S., Xing, Y., Lubischer, J. L., Krieg, P. A., Krupenko, S. A., et al. (2008) · The Journal of Neuroscience · doi:10.1523/jneurosci.4178-07.2008 · Cited by 3,129 · see citing works
Wilschut, J. (1990) · Cited by 2,407 · see citing works
Molecular anatomy of a trafficking organelle
Takamori, S., Holt, M., Stenius, K., Lemke, E. A., Grønborg, M., Riedel, D., Urlaub, H., Schenck, S., Brügger, B., Ringler, P., et al. (2006) · Cell · doi:10.1016/j.cell.2006.10.030 · Cited by 2,373 · see citing works
Astrocytes, from brain glue to communication elements: the revolution continues
Volterra, A., & Meldolesi, J. (2005) · Nature reviews. Neuroscience · doi:10.1038/nrn1722 · Cited by 1,763 · see citing works
Jahn, R., Lang, T., & Südhof, T. C. (2003) · Cell · doi:10.1016/s0092-8674(03)00112-0 · Cited by 1,331 · see citing works
Synaptic Vesicle Phosphoproteins and Regulation of Synaptic Function
Greengard, P., Valtorta, F., Czernik, A. J., & Benfenati, F. (1993) · Science · doi:10.1126/science.8430330 · Cited by 1,311 · see citing works
Self-citationHuttner, W. Β., SCHIEBLER, W., Greengard, P., & Camilli, P. V. D. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.96.5.1374 · Cited by 1,172 · see citing works
REST: A mammalian silencer protein that restricts sodium channel gene expression to neurons
Chong, J. A., Tapia-Ramı́rez, J., Kim, S. S. Y., Toledo‐Aral, J. J., Zheng, Y., Boutros, M., Altshuller, Y. M., Frohman, M. A., Kraner, S. D., & Mandel, G. (1995) · Cell · doi:10.1016/0092-8674(95)90298-8 · Cited by 1,089 · see citing works
Schoenherr, C. J., & Anderson, D. J. (1995) · Science · doi:10.1126/science.7871435 · Cited by 1,088 · 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
Moore, K. A., Kohno, T., Karchewski, L. A., Scholz, J., Baba, H., & Woolf, C. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-15-06724.2002 · Cited by 859 · see citing works
The Multifunctional Calcium/Calmodulin-Dependent Protein Kinase: From Form to Function
Braun, A. P., & Schulman, H. (1995) · Annual Review of Physiology · doi:10.1146/annurev.ph.57.030195.002221 · Cited by 820 · see citing works
Essential functions of synapsins I and II in synaptic vesicle regulation
Rosahl, T. W., Spillane, D., Missler, M., Herz, J., Selig, D. K., Wolff, J. R., Hammer, R. E., Malenka, R. C., & Südhof, T. C. (1995) · Nature · doi:10.1038/375488a0 · Cited by 719 · see citing works
Tyler, W. J., Alonso, M., Bramham, C. R., & Pozzo‐Miller, L. D. (2002) · Learning & Memory · doi:10.1101/lm.51202 · Cited by 679 · see citing works
Llinas, R. H., McGuinness, T. L., Leonard, C. S., Sugimori, M., & Greengard, P. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.9.3035 · Cited by 641 · see citing works
Potentiation of synaptic transmission in the hippocampus by phorbol esters
Malenka, R. C., Madison, D. V., & Nicoll, R. A. (1986) · Nature · doi:10.1038/321175a0 · Cited by 633 · see citing works
Assembly of presynaptic active zones from cytoplasmic transport packets
Ahmari, S. E., Buchanan, J., & Smith, S. J. (2000) · Nature Neuroscience · doi:10.1038/74814 · Cited by 596 · see citing works
A general amphipathic α-helical motif for sensing membrane curvature
Drin, G., Casella, J.-F., Gautier, R., Boehmer, T., Schwartz, T., & Antonny, B. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1194 · Cited by 572 · see citing works
Synapsins as mediators of BDNF-enhanced neurotransmitter release
Jovanovic, J. N., Czernik, A. J., Fienberg, A. A., Greengard, P., & Sihra, T. S. (2000) · Nature Neuroscience · doi:10.1038/73888 · Cited by 566 · see citing works
Camilli, P. V. D., Cameron, R. S., & Greengard, P. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.96.5.1337 · Cited by 562 · see citing works
Synapsins as Regulators of Neurotransmitter Release
Hilfiker, S., Pieribone, V. A., Czernik, A. J., Kao, H.-T., Augustine, G. J., & Greengard, P. (1999) · Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences · doi:10.1098/rstb.1999.0378 · Cited by 537 · see citing works
Synapsins: Mosaics of Shared and Individual Domains in a Family of Synaptic Vesicle Phosphoproteins
Südhof, T. C., Czernik, A. J., Kao, H., Takei, K., Johnston, P. A., Horiuchi, A., Kanazir, S., Wagner, M. A., Perin, M. S., Camilli, P. V. D., et al. (1989) · Science · doi:10.1126/science.2506642 · Cited by 533 · see citing works
Distinct pools of synaptic vesicles in neurotransmitter release
Pieribone, V. A., Shupliakov, O., Brodin, L., Hilfiker, S., Czernik, A. J., & Greengard, P. (1995) · Nature · doi:10.1038/375493a0 · Cited by 532 · see citing works
Camilli, P. V. D., Harris, S. M., Huttner, W. Β., & Greengard, P. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.96.5.1355 · Cited by 532 · see citing works
The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1.
Hirokawa, N., Sobue, K., Kanda, K., Harada, A., & Yorifuji, H. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.1.111 · Cited by 501 · see citing works
Vesicular Glutamate Transporters 1 and 2 Target to Functionally Distinct Synaptic Release Sites
Fremeau, R. T., Kam, K., Qureshi, T., Johnson, J., Copenhagen, D. R., Storm‐Mathisen, J., Chaudhry, F. A., Nicoll, R. A., & Edwards, R. H. (2004) · Science · doi:10.1126/science.1097468 · Cited by 500 · see citing works
Invertebrate Synapsins: A Single Gene Codes for Several Isoforms inDrosophila
Klagges, B. R. E., Heimbeck, G., Godenschwege, T. A., Hofbauer, A., Pflugfelder, G. O., Reifegerste, R., Reisch, D., Schaupp, M., Buchner, S., & Buchner, E. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-10-03154.1996 · Cited by 492 · see citing works
The role of Rab3A in neurotransmitter release
Geppert, M., Bolshakov, V., Siegelbaum, S., Takei, K., Camilli, P. D., Hammer, R., & Südhof, T. (1994) · Nature · doi:10.1038/369493a0 · Cited by 481 · see citing works
The distribution of synapsin I and synaptophysin in hippocampal neurons developing in culture
Fletcher, T., Cameron, P. L., Camilli, P. V. D., & Banker, G. A. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01617.1991 · Cited by 454 · see citing works
Scholz, J., Broom, D. C., Youn, D. H., Mills, C. D., Kohno, T., Suter, M. R., Moore, K. A., Décosterd, I., Coggeshall, R. E., & Woolf, C. J. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1526-05.2005 · Cited by 437 · see citing works
Wells, L., Vosseller, K., Cole, R. N., Cronshaw, J. M., Matunis, M. J., & Hart, G. W. (2002) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m200048-mcp200 · Cited by 421 · see citing works
Mori, N., Schoenherr, C. J., Vandenbergh, D. J., & Anderson, D. J. (1992) · Neuron · doi:10.1016/0896-6273(92)90219-4 · Cited by 420 · see citing works
Synapsin I bundles F-actin in a phosphorylation-dependent manner
Bähler, M., & Greengard, P. (1987) · Nature · doi:10.1038/326704a0 · Cited by 417 · see citing works
Ueda, T., & Greengard, P. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40170-0 · Cited by 407 · see citing works
Xu, B., Gottschalk, W., Chow, A., Wilson, R. I., Schnell, E., Zang, K., Wang, D., Nicoll, R. A., Lu, B., & Reichardt, L. F. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-18-06888.2000 · Cited by 401 · see citing works
Jovanovic, J. N., Benfenati, F., Siow, Y. L., Sihra, T. S., Sanghera, J. S., Pelech, S., Greengard, P., & Czernik, A. J. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3679 · Cited by 393 · see citing works
Self-citationRingstad, N., Nemoto, Y., & Camilli, P. V. D. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.16.8569 · Cited by 390 · see citing works
Krueger, B. K., FORN, J., & Greengard, P. (1977) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)40523-0 · Cited by 387 · see citing works
Reetz, A., Solimena, M., Matteoli, M., Folli, F. B., Takei, K., & Camilli, P. V. D. (1991) · The EMBO Journal · doi:10.1002/j.1460-2075.1991.tb08069.x · Cited by 384 · see citing works
Synapsin dispersion and reclustering during synaptic activity
Chi, P., Greengard, P., & Ryan, T. A. (2001) · Nature Neuroscience · doi:10.1038/nn756 · Cited by 362 · see citing works
Calmodulin mediates rapid recruitment of fast-releasing synaptic vesicles at a calyx-type synapse.
Sakaba, T., & Neher, E. (2001) · Neuron · doi:10.1016/s0896-6273(01)00543-8 · Cited by 355 · see citing works
Li, L., Chin, L., Shupliakov, O., Brodin, L., Sihra, T., Hvalby, O., Jensen, V., Zheng, D., McNamara, J. O., & Greengard, P. (1995) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.92.20.9235 · Cited by 351 · see citing works
Ueda, T., Maeno, H., & Greengard, P. (1973) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)43227-4 · Cited by 339 · see citing works
Different Presynaptic Roles of Synapsins at Excitatory and Inhibitory Synapses
Gitler, D., Takagishi, Y., Feng, J., Ren, Y., Rodriguiz, R. M., Wetsel, W. C., Greengard, P., & Augustine, G. J. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3795-04.2004 · Cited by 334 · see citing works
The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse
Landis, D. M. D., Hall, A. K., Weinstein, L. A., & Reese, T. S. (1988) · Neuron · doi:10.1016/0896-6273(88)90140-7 · Cited by 333 · see citing works
The dephosphins: dephosphorylation by calcineurin triggers synaptic vesicle endocytosis
Cousin, M. A., & Robinson, P. J. (2001) · Trends in Neurosciences · doi:10.1016/s0166-2236(00)01930-5 · Cited by 330 · see citing works
Chi, P., Greengard, P., & Ryan, T. A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00151-x · Cited by 329 · see citing works
Three-Dimensional Architecture of Presynaptic Terminal Cytomatrix
Siksou, L., Rostaing, P., Lechaire, J., Boudier, T., Ohtsuka, T., Fejtová, A., Kao, H., Greengard, P., Gundelfinger, E. D., Triller, A., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1773-07.2007 · Cited by 329 · see citing works
Short-term synaptic plasticity is altered in mice lacking synapsin I
Rosahl, T. (1993) · Cell · doi:10.1016/0092-8674(93)90487-b · Cited by 328 · see citing works
Actin has a molecular scaffolding, not propulsive, role in presynaptic function
Sankaranarayanan, S., Atluri, P. P., & Ryan, T. A. (2003) · Nature Neuroscience · doi:10.1038/nn1002 · Cited by 324 · see citing works
Llinas, R. H., Gruner, J. A., Sugimori, M., McGuinness, T. L., & Greengard, P. (1991) · The Journal of Physiology · doi:10.1113/jphysiol.1991.sp018549 · Cited by 317 · see citing works
Electroconvulsive Seizures Regulate Gene Expression of Distinct Neurotrophic Signaling Pathways
Altar, C. A., Laeng, P., Jurata, L. W., Brockman, J. A., Lemire, A. L., Bullard, J., Bukhman, Y. V., Young, T. A., Charles, V., & Palfreyman, M. G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5377-03.2004 · Cited by 317 · see citing works
Silencing the type II sodium channel gene: A model for neural-specific gene regulation
Kraner, S. D., Chong, J. A., Tsay, H.-J., & Mandel, G. (1992) · Neuron · doi:10.1016/0896-6273(92)90218-3 · Cited by 309 · see citing works
Benfenati, F., Valtorta, F., Rubenstein, J. L., Gorelick, F. S., Greengard, P., & Czernik, A. J. (1992) · Nature · doi:10.1038/359417a0 · Cited by 304 · see citing works
Self-citationCharacterization of synapsin I binding to small synaptic vesicles.
SCHIEBLER, W., Jahn, R., Doucet, J. P., Rothlein, J. E., & Greengard, P. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83924-8 · Cited by 302 · see citing works
Qualmann, B., Roos, J., DiGregorio, P. J., & Kelly, R. B. (1999) · Molecular Biology of the Cell · doi:10.1091/mbc.10.2.501 · Cited by 294 · see citing works
Kim, E., Lowenson, J. D., MacLaren, D. C., Clarke, S. G., & Young, S. G. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.12.6132 · Cited by 293 · see citing works
Nichols, R. A., Sihra, T. S., Czernik, A. J., Nairn, A. C., & Greengard, P. (1990) · Nature · doi:10.1038/343647a0 · Cited by 283 · see citing works
A phospho-switch controls the dynamic association of synapsins with synaptic vesicles.
Hosaka, M., Hammer, R., & Südhof, T. (1999) · Neuron · doi:10.1016/s0896-6273(00)80851-x · Cited by 283 · see citing works
Synaptic Innervation Density Is Regulated by Neuron-Derived BDNF
Causing, C. G., Gloster, A. T., Aloyz, R. S., Bamji, S. X., Chang, E., Fawcett, J., Kuchel, G. A., & Miller, F. D. (1997) · Neuron · doi:10.1016/s0896-6273(00)80266-4 · Cited by 283 · see citing works
A diverse superfamily of enzymes with ATP‐dependent carboxylate—amine/thiol ligase activity
Galperin, M. Y., & Koonin, E. V. (1997) · Protein Science · doi:10.1002/pro.5560061218 · Cited by 283 · see citing works
Huttner, W. Β., & Greengard, P. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.10.5402 · Cited by 282 · see citing works
RAB3 and synaptotagmin: the yin and yang of synaptic membrane fusion.
Geppert, M., & Südhof, T. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.75 · Cited by 278 · see citing works
Kennedy, M., McGuinness, T. L., & Greengard, P. (1983) · Journal of Neuroscience · doi:10.1523/jneurosci.03-04-00818.1983 · Cited by 262 · see citing works
Synaptophysin, a major synaptic vesicle protein, is not essential for neurotransmitter release
McMahon, H. T., Bolshakov, V. Y., Janz, R., Hammer, R. E., Siegelbaum, S. A., & Südhof, T. C. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.10.4760 · Cited by 262 · see citing works
Pulver, A. E., Lasseter, V. K., Kasch, L. M., Wolyniec, P. S., Nestadt, G., Blouin, J., Kimberland, M. L., Babb, R., Vourlis, S., Chen, H., et al. (1995) · American Journal of Medical Genetics · doi:10.1002/ajmg.1320600316 · Cited by 255 · see citing works
Neurotrophins promote maturation of developing neuromuscular synapses
Wang, T., Xie, K., & Lu, B. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-07-04796.1995 · Cited by 249 · see citing works
Cocaine Increases Dopamine Release by Mobilization of a Synapsin-Dependent Reserve Pool
Venton, B. J., Seipel, A. T., Phillips, P. E. M., Wetsel, W. C., Gitler, D., Greengard, P., Augustine, G. J., & Wightman, R. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4901-04.2006 · Cited by 246 · see citing works
Chin, L., Li, L., Ferreira, A., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9230 · Cited by 244 · see citing works
A third member of the synapsin gene family
Kao, H., Porton, B., Czernik, A. J., Feng, J., Yiu, G. C., Häring, M., Benfenati, F., & Greengard, P. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4667 · Cited by 244 · see citing works
Self-citationColocalization of synapsin and actin during synaptic vesicle recycling
Bloom, O., Evergren, E., Tomilin, N. V., Kjærulff, O., Löw, P., Brodin, L., Pieribone, V. A., Greengard, P., & Shupliakov, O. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212140 · Cited by 241 · see citing works
Matsubara, M., Kusubata, M., Ishiguro, K., Uchida, T., Titani, K., & Taniguchi, H. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.35.21108 · Cited by 241 · see citing works
Huttner, W. Β., DeGennaro, L. J., & Greengard, P. (1981) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)69988-6 · Cited by 232 · see citing works
Mandell, J. W., Townes‐Anderson, E., Czernik, A. J., Cameron, R. S., Greengard, P., & Camilli, P. V. D. (1990) · Neuron · doi:10.1016/0896-6273(90)90030-j · Cited by 230 · see citing works
Fukunaga, K., Muller, D., & Miyamoto, E. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.11.6119 · Cited by 226 · see citing works
Localization of estrogen receptor ?-immunoreactivity in astrocytes of the adult rat brain
Azcoitia, Í., Sierra, A., & García‐Segura, L. M. (1999) · Glia · doi:10.1002/(sici)1098-1136(199905)26:3 · Cited by 222 · see citing works
Development of Vesicle Pools during Maturation of Hippocampal Synapses
Mozhayeva, M. G., Sara, Y., Liu, X., & Kavalali, E. T. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-03-00654.2002 · Cited by 216 · see citing works
Localized Synaptic Potentiation by BDNF Requires Local Protein Synthesis in the Developing Axon
Zhang, X.-H., & Poo, M. (2002) · Neuron · doi:10.1016/s0896-6273(02)01023-1 · Cited by 209 · see citing works
Synapsin I in Nerve Terminals: Selective Association with Small Synaptic Vesicles
Navone, F., Greengard, P., & Camilli, P. V. D. (1984) · Science · doi:10.1126/science.6438799 · Cited by 208 · see citing works
Roos, J., & Kelly, R. B. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.30.19108 · Cited by 205 · see citing works
Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy
Garcia, C. C., Blair, H. J., Seager, M., Coulthard, A., Tennant, S., Buddles, M., Curtis, A., & Goodship, J. A. (2004) · Journal of Medical Genetics · doi:10.1136/jmg.2003.013680 · Cited by 205 · see citing works
Regulation of synapsin I gene expression by the zinc finger transcription factor zif268/egr-1.
Thiel, G., Schoch, S., & Petersohn, D. (1994) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36605-x · Cited by 204 · see citing works
Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4.1
Baines, A. J., & Bennett, V. (1985) · Nature · doi:10.1038/315410a0 · Cited by 203 · see citing works
Structure and function of the synapsins.
Valtorta, F., Benfenati, F., & Greengard, P. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)42501-x · Cited by 191 · see citing works
Self-citationReduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia
Vawter, M. P., Thatcher, L. N., Usen, N., Hyde, T. M., Kleinman, J. E., & Freed, W. J. (2002) · Molecular Psychiatry · doi:10.1038/sj.mp.4001158 · Cited by 188 · see citing works
Kushner, S. A., Elgersma, Y., Murphy, G. G., Jaarsma, D., van Woerden, G. M., Hojjati, M. R., Cui, Y., LeBoutillier, J. C., Marrone, D. F., Choi, E. S., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2836-05.2005 · Cited by 188 · see citing works
Cavalleri, G. L., Weale, M. E., Shianna, K. V., Singh, R., Lynch, J. M., Grinton, B. E., Szoeke, C. E. I., Murphy, K. C., Kinirons, P., O’Rourke, D., et al. (2007) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70247-8 · Cited by 188 · see citing works
Benfenati, F., Bähler, M., Jahn, R., et al. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.5.1863 · Cited by 184 · see citing works
Self-citationJovanovic, J. N., Sihra, T. S., Nairn, A. C., Hemmings, H. C., Greengard, P., & Czernik, A. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-20-07944.2001 · Cited by 183 · see citing works
Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb
Han, H.-Q., Nichols, R. A., Rubin, M. R., et al. (1991) · Nature · doi:10.1038/349697a0 · Cited by 181 · see citing works
Czernik, A. J., Pang, D. T., & Greengard, P. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.21.7518 · Cited by 180 · see citing works
FORN, J., & Greengard, P. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.10.5195 · Cited by 177 · see citing works
Johnson, E. M., Ueda, T., Maeno, H., et al. (1972) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(20)81153-3 · Cited by 176 · see citing works
Synapsin I: an actin-bundling protein under phosphorylation control.
Petrucci, T. C., & Morrow, J. S. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.3.1355 · Cited by 176 · see citing works
Baldelli, P., Fassio, A., Valtorta, F., & Benfenati, F. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3151-07.2007 · Cited by 173 · see citing works
Self-citationSynaptic vesicle recycling in synapsin I knock-out mice
Ryan, T. A., Li, L., Chin, L., Greengard, P., & Smith, S. J. (1996) · Journal of Cell Biology · doi:10.1083/jcb.134.5.1219 · Cited by 172 · see citing works
Impaired learning in mice with abnormal short-lived plasticity
Silva, A. J., Rosahl, T. W., Chapman, P. F., Marowitz, Z., Friedman, E. L., Frankland, P. W., Cestari, V., Cioffi, D., Südhof, T. C., & Bourtchuladze, R. (1996) · Current Biology · doi:10.1016/s0960-9822(96)00756-7 · Cited by 171 · see citing works
Interaction of free and synaptic vesicle-bound synapsin I with F-actin
Benfenati, F., Valtorta, F., Chieregatti, E., et al. (1992) · Neuron · doi:10.1016/0896-6273(92)90303-u · Cited by 168 · see citing works
Self-citationLi, L., Suzuki, T., Mori, N., & Greengard, P. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.4.1460 · Cited by 168 · see citing works
Takei, Y., Harada, A., Takeda, S., Kobayashi, K., Terada, S., Noda, T., Takahashi, T., & Hirokawa, N. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.6.1789 · Cited by 166 · see citing works
Camilli, P. D., Benfenati, F., Valtorta, F., & Greengard, P. (1990) · Annual Review of Cell Biology · doi:10.1146/annurev.cb.06.110190.002245 · Cited by 165 · see citing works
Self-citationTwo sites of action for synapsin domain E in regulating neurotransmitter release
Hilfiker, S., Schweizer, F. E., Kao, H., et al. (1998) · Nature Neuroscience · doi:10.1038/229 · Cited by 162 · see citing works
High Mobility of Vesicles Supports Continuous Exocytosis at a Ribbon Synapse
Holt, M. G., Cooke, A., Neef, A., & Lagnado, L. (2004) · Current Biology · doi:10.1016/j.cub.2003.12.053 · Cited by 161 · see citing works
Ceccaldi, P., Grohovaz, F., Benfenati, F., Chieregatti, E., Greengard, P., & Valtorta, F. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.128.5.905 · Cited by 161 · see citing works
Self-citationInteraction of Grb2 via its Src homology 3 domains with synaptic proteins including synapsin I.
McPherson, P. S., Czernik, A. J., Chilcote, T. J., Onofri, F., Benfenati, F., Greengard, P., Schlessinger, J., & Camilli, P. V. D. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.14.6486 · Cited by 160 · see citing works
Self-citationDeficiency in Protein l-Isoaspartyl Methyltransferase Results in a Fatal Progressive Epilepsy
Yamamoto, A., Takagi, H., Kitamura, D., Tatsuoka, H., Nakano, H., Kawano, H., Kuroyanagi, H., Yahagi, Y., Kobayashi, S., Koizumi, K.-I., et al. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02063.1998 · Cited by 154 · see citing works
Flies lacking all synapsins are unexpectedly healthy but are impaired in complex behaviour
Godenschwege, T. A., Reisch, D., Diegelmann, S., Eberle, K. K., Funk, N., Heisenberg, M., Hoppe, V., Hoppe, J., Klagges, B. R. E., Martin, J., et al. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03527.x · Cited by 154 · see citing works
Browning, M. D., Dudek, E. M., Rapier, J. L., Leonard, S. S., & Freedman, R. (1993) · Biological Psychiatry · doi:10.1016/0006-3223(93)90195-j · Cited by 153 · see citing works
Regulation of Neurotransmitter Release by Synapsin III
Feng, J., Chi, P., Blanpied, T. A., et al. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04372.2002 · Cited by 151 · see citing works
Brzustowicz, L. M., Simone, J., Mohseni, P., Hayter, J. E., Hodgkinson, K. A., Chow, E. W. C., & Bassett, A. S. (2004) · The American Journal of Human Genetics · doi:10.1086/420774 · Cited by 150 · see citing works
Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses
Lu, B., Greengard, P., & Poo, M.-M. (1992) · Neuron · doi:10.1016/0896-6273(92)90280-q · Cited by 147 · see citing works
Menegon, A., Bonanomi, D., Albertinazzi, C., Lotti, F., Ferrari, G., Kao, H., Benfenati, F., Baldelli, P., & Valtorta, F. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3321-06.2006 · Cited by 147 · see citing works
Self-citationNeuron-specific Gene Expression of Synapsin I
Schoch, S., Cibelli, G., & Thiel, G. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.6.3317 · Cited by 147 · see citing works
The Human Synapsin II Gene Promoter
Petersohn, D., Schoch, S., Brinkmann, D. R., & Thiel, G. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.41.24361 · Cited by 144 · see citing works
A protein kinase A–dependent molecular switch in synapsins regulates neurite outgrowth
Kao, H., Song, H.-J., Porton, B., et al. (2002) · Nature Neuroscience · doi:10.1038/nn840 · Cited by 143 · see citing works
Structures and chromosomal localizations of two human genes encoding synaptobrevins 1 and 2.
Archer, B. T., Özçelık, T., Jahn, R., Francke, U., & Südhof, T. C. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)44898-8 · Cited by 142 · see citing works
Structural Domains Involved in the Regulation of Transmitter Release by Synapsins
Hilfiker, S., Benfenati, F., Doussau, F., et al. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.4278-04.2005 · Cited by 142 · see citing works
Self-citationSynapsin I is a microtubule-bundling protein
Baines, A. J., & Bennett, V. (1986) · Nature · doi:10.1038/319145a0 · Cited by 142 · see citing works
The Evolutionary Pressure to Inactivate
von Poser, C., Ichtchenko, K., Shao, X., Rizo, J., & Südhof, T. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.22.14314 · Cited by 139 · see citing works
Visualizing Postendocytic Traffic of Synaptic Vesicles at Hippocampal Synapses
Li, Z., & Murthy, V. N. (2001) · Neuron · doi:10.1016/s0896-6273(01)00398-1 · Cited by 137 · see citing works
Bloom, F. E., Ueda, T., Battenberg, E. L. F., et al. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5982 · Cited by 135 · see citing works
Molecular Determinants of Synapsin Targeting to Presynaptic Terminals
Gitler, D., Xu, Y., Kao, H., et al. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.5225-03.2004 · Cited by 135 · see citing works
Humeau, Y., Doussau, F., Vitiello, F., Greengard, P., Benfenati, F., & Poulain, B. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-12-04195.2001 · Cited by 132 · see citing works
Self-citationDistinct Roles of Synapsin I and Synapsin II during Neuronal Development
Ferreira, A., Chin, L.-S., Li, L., Lanier, L. M., Kosik, K. S., & Greengard, P. (1998) · Molecular Medicine · doi:10.1007/bf03401726 · Cited by 131 · see citing works
Cytoplasmic ATM in Neurons Modulates Synaptic Function
Li, J., Han, Y. R., Plummer, M. R., & Herrup, K. (2009) · Current Biology · doi:10.1016/j.cub.2009.10.039 · Cited by 130 · see citing works
Benfenati, F., Greengard, P., Brunner, J., & Bähler, M. (1989) · Journal of Cell Biology · doi:10.1083/jcb.108.5.1851 · Cited by 130 · see citing works
Self-citationTallent, M. K., Varghis, N., Skorobogatko, Y. V., Hernandez‐Cuebas, L., Whelan, K. A., Vocadlo, D. J., & Vosseller, K. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m807431200 · Cited by 128 · see citing works
Sauerwald, A., Hoesche, C., Oschwald, R., et al. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)77206-2 · Cited by 127 · see citing works
Synapsin I is structurally similar to ATP‐utilizing enzymes
Esser, L., Wang, C.-R., Hosaka, M., Smagula, C. S., Südhof, T. C., & Deisenhofer, J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.4.977 · Cited by 126 · see citing works
Tarelli, F. T., Villa, A., Valtorta, F., Camilli, P. V. D., Greengard, P., & Ceccarelli, B. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.110.2.449 · Cited by 122 · see citing works
Self-citationWang, J. K., Walaas, S. I., & Greengard, P. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-01-00281.1988 · Cited by 121 · see citing works
Stanton, P. K., & Sarvey, J. M. (1987) · Brain Research Bulletin · doi:10.1016/0361-9230(87)90039-6 · Cited by 121 · see citing works
Two Lipid-Packing Sensor Motifs Contribute to the Sensitivity of ArfGAP1 to Membrane Curvature
Mesmin, B., Drin, G., Levi, S., Rawet, M., Cassel, D., Bigay, J., & Antonny, B. (2007) · Biochemistry · doi:10.1021/bi062288w · Cited by 119 · see citing works
Synapsin IIa Controls the Reserve Pool of Glutamatergic Synaptic Vesicles
Gitler, D., Cheng, Q., Greengard, P., & Augustine, G. J. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.0924-08.2008 · Cited by 119 · see citing works
Bähler, M., Benfenati, F., Valtorta, F., et al. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.5.1841 · Cited by 117 · see citing works
Self-citationNeuronal nitric-oxide synthase localization mediated by a ternary complex with synapsin and CAPON
Jaffrey, S. R., Benfenati, F., Snowman, A. M., Czernik, A. J., & Snyder, S. H. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.261705799 · Cited by 115 · see citing works
Self-citationChiappalone, M., Casagrande, S., Tedesco, M., Valtorta, F., Baldelli, P., Sergio Martinoia, A., & Benfenati, F. (2008) · Cerebral Cortex · doi:10.1093/cercor/bhn182 · Cited by 114 · see citing works
Self-citationSpatial learning induces neurotrophin receptor and synapsin I in the hippocampus
Gómez‐Pinilla, F., So, V., & Kesslak, J. P. (2001) · Brain Research · doi:10.1016/s0006-8993(01)02394-0 · Cited by 113 · see citing works
von Kriegstein, K., Schmitz, F., Link, E., & Südhof, T. C. (1999) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.1999.00542.x · Cited by 113 · see citing works
Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment
Corradi, A. M., Zanardi, A., Giacomini, C., Onofri, F., Valtorta, F., Zoli, M., & Benfenati, F. (2008) · Journal of Cell Science · doi:10.1242/jcs.035063 · Cited by 112 · see citing works
Self-citationOntogeny of synaptic phosphoproteins in brain.
Lohmann, S. M., Ueda, T., & Greengard, P. (1978) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.75.8.4037 · Cited by 112 · see citing works
Xu, B., Wratten, N. S., Charych, E. I., Buyske, S. G., Firestein, B. L., & Brzustowicz, L. M. (2005) · PLoS Medicine · doi:10.1371/journal.pmed.0020263 · Cited by 111 · see citing works
Synapsin III: Developmental Expression, Subcellular Localization, and Role in Axon Formation
Ferreira, A., Kao, H., Feng, J., Rapoport, M., & Greengard, P. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-10-03736.2000 · Cited by 109 · see citing works
Giachello, C. N., Fiumara, F., Giacomini, C., Corradi, A. M., Milanese, C., Ghirardi, M., Benfenati, F., & Montarolo, P. G. (2010) · Journal of Cell Science · doi:10.1242/jcs.056846 · Cited by 108 · see citing works
Self-citationWidespread distribution of protein I in the central and peripheral nervous systems.
Camilli, P. V. D., Ueda, T., Bloom, F. E., Battenberg, E. L. F., & Greengard, P. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.11.5977 · Cited by 108 · see citing works
Synaptophysin: a substrate for the protein tyrosine kinase pp60c-src in intact synaptic vesicles.
Barnekow, A., Jahn, R., & Schartl, M. (1990) · PubMed · Cited by 107 · see citing works
Valtorta, F., Greengard, P., Fesce, R., et al. (1992) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)49908-0 · Cited by 107 · see citing works
Self-citationDubin, M. W. (1988) · Birkhäuser Boston eBooks · doi:10.1007/978-1-4899-6647-6_26 · Cited by 105 · see citing works
Aberrant Neurites and Synaptic Vesicle Protein Deficiency in Synapsin II-Depleted Neurons
Ferreira, A., Kosik, K. S., Greengard, P., et al. (1994) · Science · doi:10.1126/science.8178158 · Cited by 104 · see citing works
Homo- and Heterodimerization of Synapsins
Hosaka, M., & Südhof, T. C. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.16747 · Cited by 103 · see citing works
Ho, L. (2001) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01753-5 · Cited by 103 · see citing works
Glycosylation Sites Flank Phosphorylation Sites on Synapsin I
Cole, R. N., & Hart, G. W. (1999) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.1999.0730418.x · Cited by 102 · see citing works
Goldenring, J., Lasher, R. S., Vallano, M. L., et al. (1986) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)83938-8 · Cited by 102 · see citing works
Synapsins I and II Are ATP-binding Proteins with Differential Ca2+ Regulation*
Hosaka, M., & Südhof, T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.3.1425 · Cited by 100 · see citing works
Murrey, H. E., Gama, C. I., Kalovidouris, S. A., et al. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503381102 · Cited by 99 · see citing works
Chin, J., Angers, A., Cleary, L. J., Eskin, A., & Byrne, J. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-j0004.2002 · Cited by 99 · see citing works
Pera, I., Stark, R., Kappl, M., Butt, H., & Benfenati, F. (2004) · Biophysical Journal · doi:10.1529/biophysj.104.044214 · Cited by 98 · see citing works
Self-citationEvergren, E., Gad, H., Walther, K., Sundborger, A., Tomilin, N., & Shupliakov, O. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4683-06.2007 · Cited by 97 · see citing works
Differential expression of synapsins I and II among rat retinal synapses
Mandell, J., Czernik, A. J., Camilli, P. V. D., Greengard, P., & Townes‐Anderson, E. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-05-01736.1992 · Cited by 96 · see citing works
Translocation of synapsin I in response to depolarization of isolated nerve terminals.
Sihra, T. S., Wang, J. K., Gorelick, F. S., & Greengard, P. (1989) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.86.20.8108 · Cited by 96 · see citing works
Characterization of tissue-specific transcription by the human synapsin I gene promoter.
Thiel, G., Greengard, P., & Südhof, T. C. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.8.3431 · Cited by 95 · see citing works
Ferreira, A., Han, H., Greengard, P., et al. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.20.9225 · Cited by 95 · see citing works
Synapsin III, a Novel Synapsin with an Unusual Regulation by Ca2+
Hosaka, M., & Südhof, T. C. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.22.13371 · Cited by 95 · see citing works
Src interacts with dynamin and synapsin in neuronal cells
Foster‐Barber, A., & Bishop, J. M. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.8.4673 · Cited by 94 · see citing works
Aswad, D. W., & Deight, E. A. (1983) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1983.tb08147.x · Cited by 94 · see citing works
Daly, C., & Ziff, E. B. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02365.1997 · Cited by 94 · see citing works
Tarelli, F. T., Bossi, M., Fesce, R., et al. (1992) · Neuron · doi:10.1016/0896-6273(92)90072-l · Cited by 92 · see citing works
Zhu, J. X., Doyle, H. A., Mamula, M. J., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m606958200 · Cited by 92 · see citing works
Thiel, G., Lietz, M., & Cramer, M. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.41.26891 · Cited by 90 · see citing works
Yang-Feng, T. L., DeGennaro, L. J., & Francke, U. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.22.8679 · Cited by 90 · see citing works
Axon development in mouse cerebellum: Embryonic axon forms and expression of synapsin I
Mason, C. A. (1986) · Neuroscience · doi:10.1016/0306-4522(86)90146-6 · Cited by 89 · see citing works
Synapsin I-mediated interaction of brain spectrin with synaptic vesicles.
Sikorski, A. F., Terlecki, G., Zagon, I. S., & Goodman, S. R. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.2.313 · Cited by 89 · see citing works
Angers, A., Fioravante, D., Chin, J., Cleary, L. J., Bean, A. J., & Byrne, J. H. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-13-05412.2002 · Cited by 89 · see citing works
Bonanomi, D., Menegon, A., Miccio, A., Ferrari, G., Corradi, A. M., Kao, H., Benfenati, F., & Valtorta, F. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1573-05.2005 · Cited by 88 · see citing works
Self-citationNayak, A., Moore, C., & Browning, M. (1996) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.93.26.15451 · Cited by 88 · see citing works
Evidence for targeted vesicular glutamate exocytosis in osteoblasts
Ps, B., Genever, P. G., Spencer, G. J., Grewal, T. S., & Skerry, T. M. (2001) · Bone · doi:10.1016/s8756-3282(01)00482-3 · Cited by 86 · see citing works
Cyclosporine A-induced hypertension involves synapsin in renal sensory nerve endings
Zhang, W., Li, J.-L., Hosaka, M., Janz, R., Shelton, J. M., Albright, G. M., Richardson, J. A., Südhof, T. C., & Victor, R. G. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.170160397 · Cited by 86 · see citing works
Camilli, P. V. D., Vitadello, M., Canevini, M. P., et al. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-05-01625.1988 · Cited by 86 · see citing works
Lowenson, J. D., Kim, E., Young, S. G., & Clarke, S. G. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m100987200 · Cited by 86 · see citing works
Synaptic Vesicle Mobility in Mouse Motor Nerve Terminals with and without Synapsin
Gaffield, M. A., & Betz, W. J. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3910-07.2007 · Cited by 84 · see citing works
Impairment of Inhibitory Synaptic Transmission in Mice Lacking Synapsin I
Terada, S., Tsujimoto, T., Takei, Y., et al. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.145.5.1039 · Cited by 83 · see citing works
Nestler, E. J., & Greengard, P. (1980) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.77.12.7479 · Cited by 83 · see citing works
Benfenati, F., Valtorta, F., Rossi, M. C., Onofri, F., Sihra, T. S., & Greengard, P. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.123.6.1845 · Cited by 83 · see citing works
Self-citationIncrease in synaptic vesicle proteins accompanies long-term potentiation in the dentate gyrus
Lynch, M. A., Voss, K. L., Rodrı́guez-Álvarez, J., et al. (1994) · Neuroscience · doi:10.1016/0306-4522(94)90197-x · Cited by 82 · see citing works
Synapsin I Regulates Glutamate Release from Rat Brain Synaptosomes
Nichols, R. A., Chilcote, T. J., Czernik, A. J., & Greengard, P. (1992) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.1992.tb09788.x · Cited by 82 · see citing works
Bogen, I. L., Boulland, J., Mariussen, E., Wright, M., Fonnum, F., Kao, H., & Walaas, S. I. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2005.03636.x · Cited by 80 · see citing works
Serotonin stimulates phosphorylation of Protein I in the facial motor nucleus of rat brain
DOLPHIN, A. C., & Greengard, P. (1981) · Nature · doi:10.1038/289076a0 · Cited by 80 · see citing works
Lee, J. S., Kim, M., Ho, W., & Lee, S. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.2165-08.2008 · Cited by 80 · see citing works
Sun, J., Bronk, P., Liu, X., Han, W., & Südhof, T. C. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0511300103 · Cited by 79 · see citing works
Liévens, J.-C. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2002.1152 · Cited by 78 · see citing works
Hackett, J. T., Cochran, S. L., Greenfield, L. J., Brosius, D. C., & Ueda, T. (1990) · Journal of Neurophysiology · doi:10.1152/jn.1990.63.4.701 · Cited by 78 · see citing works
Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex
Bragina, L., Candiracci, C., Barbaresi, P., Giovedı̀, S., Benfenati, F., & Conti, F. (2007) · Neuroscience · doi:10.1016/j.neuroscience.2007.02.060 · Cited by 77 · see citing works
Self-citationSynapsin Is a Novel Rab3 Effector Protein on Small Synaptic Vesicles
Giovedì, S., Vaccaro, P., Valtorta, F., Darchen, F., Greengard, P., Cesareni, G., & Benfenati, F. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m403293200 · Cited by 76 · see citing works
Self-citationValtorta, F., Lezzi, N., Benfenati, F., et al. (1995) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.1995.tb01062.x · Cited by 74 · see citing works
Self-citationA role for Synapsin in associative learning: The Drosophila larva as a study casePreprint
Michels, B., Diegelmann, S., Tanimoto, H., Schwenkert, I., Buchner, E., & Gerber, B. (2005) · Learning & Memory · doi:10.1101/lm.92805 · Cited by 74 · see citing works
Zheng, Y., Li, H., Qin, W. D., Chen, W., Duan, Y., Xiao, Y., Li, C., Zhang, J., Li, X., Feng, G., et al. (2005) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2005.01.037 · Cited by 71 · see citing works
Modregger, J., Schmidt, A., Ritter, B., Huttner, W. Β., & Plomann, M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m208568200 · Cited by 71 · see citing works
Phosphorylation-dependent inhibition by synapsin I of organelle movement in squid axoplasm
McGuinness, T. L., Brady, S., Gruner, J. A., et al. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-12-04138.1989 · Cited by 71 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
The Cell Biology of Synaptic Plasticity
Ho, V. M., Lee, J.-A., & Martin, K. C. (2011) · Science · doi:10.1126/science.1209236 · Cited by 573 · see citing works
Short-term forms of presynaptic plasticity
Fioravante, D., & Regehr, W. G. (2011) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.02.003 · Cited by 375 · see citing works
Synaptic vesicle recycling: steps and principles
Rizzoli, S. O. (2014) · The EMBO Journal · doi:10.1002/embj.201386357 · Cited by 317 · see citing works
Yuan, M., Yang, B., Rothschild, G., Mann, J. J., Sanford, L. D., Tang, X., Huang, C., Wang, C., & Zhang, W. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01519-z · Cited by 246 · see citing works
“166 Other forms of histone methylation include H3K9me2 and H3K27me3, are repressive in the gene promoter region in response to stress.”
BackgroundDevelopmental and epileptic encephalopathies: from genetic heterogeneity to phenotypic continuum
Guerrini, R., Conti, V., Mantegazza, M., Balestrini, S., Galanopoulou, A. S., & Benfenati, F. (2023) · Physiological Reviews · doi:10.1152/physrev.00063.2021 · Cited by 196 · see citing works
Self-citationTreccani, G., Musazzi, L., Perego, C., Milanese, M., Nava, N., Bonifacino, T., Lamanna, J., Malgaroli, A., Drago, F., Racagni, G., et al. (2014) · Molecular Psychiatry · doi:10.1038/mp.2014.5 · Cited by 133 · see citing works
Cruceanu, C., Alda, M., Nagy, C., Freemantle, E., Rouleau, G. A., & Turecki, G. (2013) · International Journal of Neuropsychopharmacology · doi:10.1017/s1461145712000363 · Cited by 93 · see citing works
Ionescu, I. A., Dine, J., Yen, Y.-C., Buell, D. R., Herrmann, L., Holsboer, F., Eder, M., Landgraf, R., & Schmidt, U. (2012) · Neuropsychopharmacology · doi:10.1038/npp.2011.317 · Cited by 87 · see citing works
Imaging Synaptic Density: The Next Holy Grail of Neuroscience?
Serrano, M. E., Kim, E., Petrinovic, M. M., Turkheimer, F., & Cash, D. (2022) · Frontiers in Neuroscience · doi:10.3389/fnins.2022.796129 · Cited by 67 · see citing works
Recent advances in gene therapy for neurodevelopmental disorders with epilepsy
Turner, T. J., Zourray, C., Schorge, S., & Lignani, G. (2021) · Journal of Neurochemistry · doi:10.1111/jnc.15168 · Cited by 71 · see citing works
Millard, S. J., Weston-Green, K., & Newell, K. A. (2020) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2020.109908 · Cited by 62 · see citing works
Selective lowering of synapsins induced by oligomeric α-synuclein exacerbates memory deficits
Larson, M. E., Greimel, S. J., Amar, F., LaCroix, M., Boyle, G., Sherman, M. A., Schley, H., Miel, C., Schneider, J. A., Kayed, R., et al. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1704698114 · Cited by 61 · see citing works
Self-citationCounotte, D. S., Li, K. W., Wortel, J., Gouwenberg, Y., Van Der Schors, R. C., Smit, A. B., & Spijker, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07404.x · Cited by 47 · see citing works
Ojelade, S. A., Lee, T. V., Giagtzoglou, N., Yu, L., Ugur, B., Li, Y., Duraine, L., Zuo, Z., Petyuk, V., De Jager, P. L., et al. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.07.041 · Cited by 42 · see citing works
Dagyte, G., Luiten, P. G., De Jager, T., Gabriel, C., Mocaër, E., Den Boer, J. A., & Van der Zee, E. A. (2011) · Journal of Neuroscience Research · doi:10.1002/jnr.22697 · Cited by 32 · see citing works
Perić, I., Costina, V., Gass, P., Findeisen, P., & Filipović, D. (2021) · Brain Research Bulletin · doi:10.1016/j.brainresbull.2020.11.013 · Cited by 18 · see citing works
Rosi, S. (2018) · Brain Circulation · doi:10.4103/bc.bc_24_18 · Cited by 18 · see citing works
Roth, J. R., Moraes, R. C. M. D., Xu, B. P., Crawley, S. R., Khan, M. A., & Melkani, G. C. (2023) · Frontiers in Aging Neuroscience · doi:10.3389/fnagi.2023.1223911 · Cited by 16 · see citing works
- Authors
- Cesca, F., Baldelli, P., Valtorta, F., & Benfenati, F.
- Affiliations
- Italian Institute of Technology (IT)
- Vita-Salute San Raffaele University (IT)
- Corresponding author
- Benfenati, F.
- Venue
- Progress in Neurobiology
- Publisher
- Elsevier BV
- Published
- 2010-08
- Volume
- 91
- Issue
- 4
- Pages
- 313-348
- ISSN
- 0301-0082 (ISSN-L)
- OpenAlex
- W2142790764
- Cited by
- 654
- References
- 375
- Citations by year
- 2026: 35 · 2025: 52 · 2024: 39 · 2023: 34 · 2022: 50 · 2021: 39 · 2020: 38 · 2019: 41 · 2018: 45 · 2017: 44 · 2016: 37 · 2015: 34 · 2014: 36 · 2013: 49 · 2012: 40
- FWCI
- 3.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Progress in Neurobiology (publishedVersion)
- PubMed (publishedVersion)
- ArTS Archivio della ricerca di Trieste (University of Trieste https://www.units.it/) (submittedVersion)
- CINECA IRIS Institutial Research Information System (University of Genoa) (submittedVersion)
- Archivio Istituzionale della Ricerca - Università Vita-Salute San Raffaele (submittedVersion)
- Padua Research Archive (University of Padova) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- synapsin, synaptic vesicle tethering, neurotransmitter release, synaptic vesicle recycling, actin cytoskeleton, kinase regulation, synaptic plasticity, epilepsy, schizophrenia, central nervous system disorders
- MeSH terms
- Animals, Models, Biological, Neuronal Plasticity, Neurons, Phosphorylation, Protein Binding, Synapses, Synapsins
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