The importance of synapsin I and II for neurotransmitter levels and vesicular storage in cholinergic, glutamatergic and GABAergic nerve terminals

Albillos, 1997, The exocytotic event in chromaffin cells revealed by patch amperometry, Nature, 389, 509, 10.1038/39081 Alvarez de Toledo, 1993, Release of secretory products during transient vesicle fusion, Nature, 363, 554, 10.1038/363554a0 Atwood, 2002, Diversification of synaptic strength: presynaptic elements, Nat. Rev. Neurosci., 3, 497, 10.1038/nrn876 Awizio, 2007, Influence of synapsin I on synaptic vesicles: an analysis by force–volume mode of the atomic force microscope and dynamic light scattering, Biophys. J., 93, 1051, 10.1529/biophysj.107.104406 Bak, 2006, The glutamate/GABA-glutamine cycle: aspects of transport, neurotransmitter homeostasis and ammonia transfer, J. Neurochem., 98, 641, 10.1111/j.1471-4159.2006.03913.x Baldelli, 2007, Lack of synapsin I reduces the readily releasable pool of synaptic vesicles at central inhibitory synapses, J. Neurosci., 27, 13520, 10.1523/JNEUROSCI.3151-07.2007 Benfenati, 1993, Interactions of synapsin I with phospholipids: possible role in synaptic vesicle clustering and in the maintenance of bilayer structures, J. Cell Biol., 123, 1845, 10.1083/jcb.123.6.1845 Bloom, 2003, Colocalization of synapsin and actin during synaptic vesicle recycling, J. Cell Biol., 161, 737, 10.1083/jcb.200212140 Bogen, 2006, Absence of synapsin I and II is accompanied by decreases in vesicular transport of specific neurotransmitters, J. Neurochem., 96, 1458, 10.1111/j.1471-4159.2005.03636.x Bogen, 2008, Distinct changes in neuronal and astrocytic amino acid neurotransmitter metabolism in mice with reduced numbers of synaptic vesicles, J. Neurochem., 105, 2524, 10.1111/j.1471-4159.2008.05344.x Bogen, 2009, Synapsin-dependent development of glutamatergic synaptic vesicles and presynaptic plasticity in postnatal mouse brain, Neuroscience, 158, 231, 10.1016/j.neuroscience.2008.05.055 Bragina, 2007, Heterogeneity of glutamatergic and GABAergic release machinery in cerebral cortex, Neuroscience, 146, 1829, 10.1016/j.neuroscience.2007.02.060 Browning, 1993, Significant reductions in synapsin but not synaptophysin specific activity in the brains of some schizophrenics, Biol. Psychiatry, 34, 529, 10.1016/0006-3223(93)90195-J Bu, 1992, Two human glutamate decarboxylases, 65-kDa GAD and 67-kDa GAD, are each encoded by a single gene, Proc. Natl. Acad. Sci. U.S.A., 89, 2115, 10.1073/pnas.89.6.2115 Burger, 1991, GABA and glycine in synaptic vesicles: storage and transport characteristics, Neuron, 7, 287, 10.1016/0896-6273(91)90267-4 Burger, 1989, Synaptic vesicles immunoisolated from rat cerebral cortex contain high levels of glutamate, Neuron, 3, 715, 10.1016/0896-6273(89)90240-7 Cavalleri, 2007, Multicentre search for genetic susceptibility loci in sporadic epilepsy syndrome and seizure types: a case–control study, Lancet Neurol., 6, 970, 10.1016/S1474-4422(07)70247-8 Chen, 2003, Distinctive interactions in the holoenzyme formation for two isoforms of glutamate decarboxylase, Biochim. Biophys. Acta, 1645, 63, 10.1016/S1570-9639(02)00522-8 Chiappalone, M., Casagrande, S., Tedesco, M., Valtorta, F., Baldelli, P., Martinoia, S., Benfenati, F., in press. Opposite changes in glutamatergic and GABAergic transmission underlie the diffuse hyperexcitability of synapsin I-deficient cortical networks. Cerebral Cortex. doi:10.1093/cercor/bhn182. Chin, 1995, Impairment of axonal development and of synaptogenesis in hippocampal neurons of synapsin I-deficient mice, Proc. Natl. Acad. Sci. U.S.A., 92, 9230, 10.1073/pnas.92.20.9230 Coleman, 2008, Synapsin II and calcium regulate vesicle docking and the cross-talk between vesicle pools at the mouse motor terminals, J. Physiol., 586, 4649, 10.1113/jphysiol.2008.154666 Corradi, 2008, Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment, J. Cell Sci., 15, 3042, 10.1242/jcs.035063 Croft, 2005, Normal biogenesis and cycling of empty synaptic vesicles in dopamine neurons of vesicular monoamine transporter 2 knockout mice, Mol. Biol. Cell, 16, 306, 10.1091/mbc.e04-07-0559 Curthoys, 1973, Glutamate and glutamine distribution in the rat nephron in acidosis and alkalosis, Am. J. Physiol., 224, 884, 10.1152/ajplegacy.1973.224.4.884 De Camilli, 1983, Synapsin I (protein I), a nerve terminal-specific phosphoprotein. I. Its general distribution in synapses of the central and peripheral nervous system demonstrated by immunofluorescence in frozen and plastic sections, J. Cell Biol., 96, 1337, 10.1083/jcb.96.5.1337 De Camilli, 1983, Synapsin I (protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes, J. Cell Biol., 96, 1355, 10.1083/jcb.96.5.1355 Eid, 2007, Increased expression of phosphate-activated glutaminase in hippocampal neurons in human mesial temporal lobe epilepsy, Acta Neuropathol., 113, 137, 10.1007/s00401-006-0158-5 Erickson, 1990, Chloride ion increases [3H]dopamine accumulation by synaptic vesicles purified from rat striatum: inhibition by thiocyanate ion, Brain Res., 516, 155, 10.1016/0006-8993(90)90912-U Erlander, 1991, Two genes encode distinct glutamate decarboxylases, Neuron, 7, 91, 10.1016/0896-6273(91)90077-D Evergren, 2007, Intersectin is a negative regulator of dynamin recruitment to the synaptic endocytic zone in the central synapse, J. Neurosci., 27, 379, 10.1523/JNEUROSCI.4683-06.2007 Fdez, 2006, Vesicle pools and synapsins: new insights into old enigmas, Brain Cell Biol., 35, 107, 10.1007/s11068-007-9013-4 Ferreira, 1998, Distinct roles of synapsin I and synapsin II during neuronal development, Mol. Med., 4, 22, 10.1007/BF03401726 Ferreira, 1995, Suppression of synapsin II inhibits the formation and maintenance of synapses in hippocampal culture, Proc. Natl. Acad. Sci. U.S.A., 92, 9225, 10.1073/pnas.92.20.9225 Ferreira, 2000, Synapsin III: developmental expression, subcellular localization, and role in axon formation, J. Neurosci., 20, 3736, 10.1523/JNEUROSCI.20-10-03736.2000 Ferreira, 2002, The synapsins: beyond the regulation of neurotransmitter release, Cell. Mol. Life Sci., 59, 589, 10.1007/s00018-002-8451-5 Fon, 1997, Vesicular transport regulates monoamine storage and release but is not essential for amphetamine action, Neuron, 19, 1271, 10.1016/S0896-6273(00)80418-3 Fonnum, 1968, The distribution of glutamate decarboxylase and aspartate transaminase in subcellular fractions of rat and guinea-pig brain, Biochem. J., 106, 401, 10.1042/bj1060401 Fonnum, 1975, A rapid radiochemical method for the determination of choline acetyltransferase, J. Neurochem., 24, 407, 10.1111/j.1471-4159.1975.tb11895.x Fonnum, 1984, Glutamate: a neurotransmitter in mammalian brain, J. Neurochem., 42, 1, 10.1111/j.1471-4159.1984.tb09689.x Fremeau, 2004, Vesicular glutamate transporters 1 and 2 target to functionally distinct synaptic release sites, Science, 304, 1815, 10.1126/science.1097468 Gaffield, 2007, Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin, J. Neurosci., 27, 13691, 10.1523/JNEUROSCI.3910-07.2007 Garcia, 2004, Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy, J. Med. Genet., 41, 183, 10.1136/jmg.2003.013680 Giovedì, 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, 10.1074/jbc.M404168200 Gitler, 2004, Different presynaptic roles of synapsins at excitatory and inhibitory synapses, J. Neurosci., 24, 11368, 10.1523/JNEUROSCI.3795-04.2004 Gitler, 2008, Synapsin IIa controls the reserve pool of glutamatergic synaptic vesicles, J. Neurosci., 28, 10835, 10.1523/JNEUROSCI.0924-08.2008 Han, 1991, Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb, Nature, 349, 697, 10.1038/349697a0 Helle, 1975, The adrenal medulla: a model for studies of hormonal and neuronal storage and release mechanisms, Mol. Cell. Biochem., 6, 127, 10.1007/BF01732006 Hilfiker, 1998, Two sites of action for synapsin domain E in regulating neurotransmitter release, Nat. Neurosci., 1, 29, 10.1038/229 Hilfiker, 1999, Synapsins as regulators of neurotransmitter release, Philos. Trans. R. Soc. Lond. Series B, Biol. Sci., 354, 269, 10.1098/rstb.1999.0378 Ho, 1991, Synapsin I is a highly surface-active molecule, J. Biol. Chem., 266, 5600, 10.1016/S0021-9258(19)67637-4 Huttner, 1983, Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation, J. Cell Biol., 96, 1374, 10.1083/jcb.96.5.1374 Hvalby, 2006, Synapsin-regulated synaptic transmission from readily releasable synaptic vesicles in excitatory hippocampal synapses in mice, J. Physiol., 571, 75, 10.1113/jphysiol.2005.100685 Jensen, 2007, A delayed response enhancement during hippocampal presynaptic plasticity in mice, J. Physiol., 583, 129, 10.1113/jphysiol.2007.131300 Jin, 2003, Demonstration of functional coupling between gamma -aminobutyric acid (GABA) synthesis and vesicular GABA transport into synaptic vesicles, Proc. Natl. Acad. Sci. U.S.A., 100, 4293, 10.1073/pnas.0730698100 John, J.P., Sunyer, B., Höger, H., Pollak, A., Lubec, G., in press. Hippocampal synapsin isoform levels are linked to spatial memory enhancement by SGS742. Hippocampus. doi:10.1002/hipo.20553. Kao, 1998, A third member of the synapsin gene family, Proc. Natl. Acad. Sci. U.S.A., 95, 4667, 10.1073/pnas.95.8.4667 Kielland, 2006, Synapsin utilization differs among functional classes of synapses on thalamocortical cells, J. Neurosci., 26, 5786, 10.1523/JNEUROSCI.4631-05.2006 Kuriyama, 1968, Association of the gamma-aminobutyric acid system with a synaptic vesicle fraction from mouse brain, Brain Res., 8, 132, 10.1016/0006-8993(68)90176-5 Kushner, 2005, Modulation of presynaptic plasticity and learning by the H-ras/extracellular signal-regulated kinase/synapsin I signaling pathway, J. Neurosci., 25, 9721, 10.1523/JNEUROSCI.2836-05.2005 Lehmann, 1980, The nucleus basalis magnocellularis: the origin of a cholinergic projection to the neocortex of the rat, Neuroscience, 5, 1161, 10.1016/0306-4522(80)90195-5 Li, 1995, Impairment of synaptic vesicle clustering and of synaptic transmission, and increased seizure propensity, in synapsin I-deficient mice, Proc. Natl. Acad. Sci. U.S.A., 92, 9235, 10.1073/pnas.92.20.9235 Mandell, 1990, Synapsins in the vertebrate retina: absence from ribbon synapses and heterogeneous distribution among conventional synapses, Neuron, 5, 19, 10.1016/0896-6273(90)90030-J Mariussen, 2001, The effect of polychlorinated biphenyls on the high affinity uptake of the neurotransmitters, dopamine, serotonin, glutamate and GABA, into rat brain synaptosomes, Toxicology, 159, 11, 10.1016/S0300-483X(00)00374-7 Martin, 1993, Regulation of gamma-aminobutyric acid synthesis in the brain, J. Neurochem., 60, 395, 10.1111/j.1471-4159.1993.tb03165.x McGeer, 1988, Central cholinergic pathways: the histochemical evidence, 86, 615 Mesulam, 1988, Acetylcholinesterase-rich pyramidal neurons in the human neocortex and hippocampus: absence at birth, development during the life span, and dissolution in Alzheimer's disease, Ann. Neurol., 24, 765, 10.1002/ana.410240611 Mesulam, 1983, Central cholinergic pathways in the rat: an overview based on an alternative nomenclature (Ch1–Ch6), Neuroscience, 10, 1185, 10.1016/0306-4522(83)90108-2 Mirnics, 2000, Molecular characterization of schizophrenia viewed by microarray analysis of gene expression in prefrontal cortex, Neuron, 28, 53, 10.1016/S0896-6273(00)00085-4 Molinoff, 1968, The metabolism of gamma-aminobutyric acid (GABA) in the lobster nervous system—glutamic decarboxylase, J. Neurochem., 15, 391, 10.1111/j.1471-4159.1968.tb11626.x Mozhayeva, 2002, Development of vesicle pools during maturation of hippocampal synapses, J. Neurosci., 22, 654, 10.1523/JNEUROSCI.22-03-00654.2002 Ni, 1994, Cloning and expression of a cDNA encoding a brain-specific Na(+)-dependent inorganic phosphate cotransporter, Proc. Natl. Acad. Sci. U.S.A., 91, 5607, 10.1073/pnas.91.12.5607 Ottersen, 1984, Glutamate- and GABA-containing neurons in the mouse and rat brain, as demonstrated with a new immunocytochemical technique, J. Comp. Neurol., 229, 374, 10.1002/cne.902290308 Parks, 1991, Reduced in vitro phosphorylation of synapsin I (site 1) in Alzheimer's disease postmortem tissues, Brain Res. Mol. Brain Res., 9, 125, 10.1016/0169-328X(91)90137-M Pera, 2004, Using the atomic force microscope to study the interaction between two solid supported lipid bilayers and the influence of synapsin I, Biophys. J., 87, 2446, 10.1529/biophysj.104.044214 Perdahl, 1984, Synapsin I (protein I) in different brain regions in senile dementia of Alzheimer type and in multi-infarct dementia, J. Neural Transm., 60, 133, 10.1007/BF01245030 Pieribone, 1995, Distinct pools of synaptic vesicles in neurotransmitter release, Nature, 375, 493, 10.1038/375493a0 Pieribone, 2002, Expression of synapsin III in nerve terminals and neurogenic regions of the adult brain, J. Comp. Neurol., 454, 105, 10.1002/cne.10417 Porter, 1985, Transaminations catalysed by brain glutamate decarboxylase, Biochem. J., 231, 705, 10.1042/bj2310705 Porton, 1999, Characterization of transcripts from the synapsin III gene locus, J. Neurochem., 73, 2266, 10.1046/j.1471-4159.1999.0732266.x Prado, 2006, Mice deficient for the vesicular acetylcholine transporter are myasthenic and have deficits in object and social recognition, Neuron, 51, 601, 10.1016/j.neuron.2006.08.005 Qin, 2004, Regional alteration of synapsin I in the hippocampal formation of Alzheimer's disease patients, Acta Neuropathol., 107, 209, 10.1007/s00401-003-0800-4 Reigada, 2003, Control of neurotransmitter release by an internal gel matrix in synaptic vesicles, Proc. Natl. Acad. Sci. U.S.A., 100, 3485, 10.1073/pnas.0336914100 Roberg, 2000, Properties and submitochondrial localization of pig and rat renal phosphate-activated glutaminase, Am. J. Physiol. Cell Physiol., 279, C648, 10.1152/ajpcell.2000.279.3.C648 Rosahl, 1995, Essential functions of synapsins I and II in synaptic vesicle regulation, Nature, 375, 488, 10.1038/375488a0 Salganicoff, 1965, Subcellular distribution of the enzymes glutamic acid, glutamine and gamma-aminobutyric acid cycles in rat brain, J. Neurochem., 12, 287, 10.1111/j.1471-4159.1965.tb06766.x Samigullin, 2004, Regulation of transmitter release by synapsin II in mouse motor terminals, J. Physiol., 561, 149, 10.1113/jphysiol.2004.073494 Silva, 1996, Impaired learning in mice with abnormal short-lived plasticity, Curr. Biol., 6, 1509, 10.1016/S0960-9822(96)00756-7 Smith, 1985, Measurement of protein using bicinchoninic acid, Anal. Biochem., 150, 76, 10.1016/0003-2697(85)90442-7 Stadler, 1986, Simple and rapid measurement of acetylcholine and choline by HPLC and enzymatic–electrochemical detection, Neurochem. Int., 9, 127, 10.1016/0197-0186(86)90041-0 Südhof, 2004, The synaptic vesicle cycle, Annu. Rev. Neurosci., 27, 509, 10.1146/annurev.neuro.26.041002.131412 Südhof, 1989, Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins, Science, 245, 1474, 10.1126/science.2506642 Sugiyama, 2000, A novel function of synapsin II in neurotransmitter release, Brain Res. Mol. Brain Res., 85, 133, 10.1016/S0169-328X(00)00231-X Takei, 1995, Synapsin I deficiency results in the structural change in the presynaptic terminals in the murine nervous system, J. Cell Biol., 131, 1789, 10.1083/jcb.131.6.1789 Tan, 1998, A leucine-based motif mediates the endocytosis of vesicular monoamine and acetylcholine transporters, J. Biol. Chem., 273, 17351, 10.1074/jbc.273.28.17351 Tao-Cheng, 2006, Activity-related redistribution of presynaptic proteins at the active zone, Neuroscience, 141, 1217, 10.1016/j.neuroscience.2006.04.061 Terada, 1999, Impairment of inhibitory synaptic transmission in mice lacking synapsin I, J. Cell Biol., 145, 1039, 10.1083/jcb.145.5.1039 Usdin, 1995, Molecular biology of the vesicular ACh transporter, Trends Neurosci., 18, 218, 10.1016/0166-2236(95)93906-E Valtorta, 1995, Accelerated structural maturation induced by synapsin I at developing neuromuscular synapses of Xenopus laevis, Eur. J. Neurosci., 7, 261, 10.1111/j.1460-9568.1995.tb01062.x VanderHorst, 2006, The organization of the brain stem and spinal cord of the mouse: relationship between monoaminergic, cholinergic, and spinal projection systems, J. Chem. Neuroanat., 31, 2, 10.1016/j.jchemneu.2005.08.003 Vawter, 2002, Reduction of synapsin in the hippocampus of patients with bipolar disorder and schizophrenia, Mol. Psychiatry, 7, 571, 10.1038/sj.mp.4001158 Walaas, 1988, Synapsin Ia, synapsin Ib, protein IIIa, and protein IIIb, four related synaptic vesicle-associated phosphoproteins, share regional and cellular localization in rat brain, J. Neurochem., 51, 1214, 10.1111/j.1471-4159.1988.tb03089.x Wojcik, 2004, An essential role for vesicular glutamate transporter 1 (VGLUT1) in postnatal development and control of quantal size, Proc. Natl. Acad. Sci. U.S.A., 101, 7158, 10.1073/pnas.0401764101