Synaptic vesicle phosphoproteins and regulation of synaptic function.

Complex brain functions, such as learning and memory, are believed to involve changes in the efficiency of communication between nerve cells. Therefore, the elucidation of the molecular mechanisms that regulate synaptic transmission, the process of intercellular communication, is an essential step toward understanding nervous system function. Several proteins associated with synaptic vesicles, the organelles that store neurotransmitters, are targets for protein phosphorylation and dephosphorylation. One of these phosphoproteins, synapsin I, by means of changes in its state of phosphorylation, appears to control the fraction of synaptic vesicles available for release and thereby to regulate the efficiency of neurotransmitter release. This article describes current understanding of the mechanism by which synapsin I modulates communication between nerve cells and reviews the properties and putative functions of other phosphoproteins associated with synaptic vesicles.

[1]  K. Hagino-Yamagishi,et al.  [Oncogene]. , 2019, Gan to kagaku ryoho. Cancer & chemotherapy.

[2]  P. Greengard,et al.  Calcium‐dependent serine phosphorylation of synaptophysin , 1993, Synapse.

[3]  P. Greengard,et al.  Synapsin I partially dissociates from synaptic vesicles during exocytosis induced by electrical stimulation , 1992, Neuron.

[4]  Fabio Benfenati,et al.  Synaptic vesicle-associated Ca2+/calmodulin-dependent protein kinase II is a binding protein for synapsin I , 1992, Nature.

[5]  P. Greengard,et al.  Antibodies to synaptophysin interfere with transmitter secretion at neuromuscular synapses , 1992, Neuron.

[6]  P. Greengard,et al.  Calcium-dependent transmitter secretion reconstituted in Xenopus oocytes: requirement for synaptophysin. , 1992, Science.

[7]  R. Scheller,et al.  Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones. , 1992, Science.

[8]  Alcino J. Silva,et al.  Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. , 1992, Science.

[9]  A. Ogura,et al.  Neurotransmitter Release from Synaptotagmin-Deficient Clonal Variants of PC 12 Cells , 1992, Science.

[10]  P. Greengard,et al.  Effects of the neuronal phosphoprotein synapsin I on actin polymerization. I. Evidence for a phosphorylation-dependent nucleating effect. , 1992, The Journal of biological chemistry.

[11]  P. Greengard,et al.  Effects of the neuronal phosphoprotein synapsin I on actin polymerization. II. Analytical interpretation of kinetic curves. , 1992, The Journal of biological chemistry.

[12]  R. Kelly,et al.  Specific association of the proto-oncogene product pp60c-src with an intracellular organelle, the PC12 synaptic vesicle , 1992, The Journal of cell biology.

[13]  T. Südhof,et al.  Synaptotagmin: a calcium sensor on the synaptic vesicle surface. , 1992, Science.

[14]  P. Greengard,et al.  Differential expression of synapsins I and II among rat retinal synapses , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[15]  R. Burgoyne,et al.  Neuroimaging Clinics of North America , 1992, Neurology.

[16]  P. Greengard,et al.  Structure and function of the synapsins. , 1992, The Journal of biological chemistry.

[17]  P. Greengard,et al.  Exogenous synapsin I promotes functional maturation of developing neuromuscular synapses , 1992, Neuron.

[18]  P. Greengard,et al.  Synapsin I Regulates Glutamate Release from Rat Brain Synaptosomes , 1992, Journal of neurochemistry.

[19]  P. Greengard,et al.  Interaction of free and synaptic vesicle-bound synapsin I with F-actin , 1992, Neuron.

[20]  T. Gotow,et al.  Cytoplasmic architecture of the axon terminal: Filamentous strands specifically associated with synaptic vesicles , 1991, Neuroscience.

[21]  Thomas C. Südhof,et al.  Binding of synaptotagmin to the α-latrotoxin receptor implicates both in synaptic vesicle exocytosis , 1991, Nature.

[22]  P. Greengard,et al.  A Novel Synaptic Vesicle‐Associated Phosphoprotein: SVAPP‐120 , 1991, Journal of neurochemistry.

[23]  M. Passafaro,et al.  Presynaptic localization of ω-conotoxin-sensitive calcium channels at the frog neuromuscular junction , 1991, Brain Research.

[24]  P. Greengard,et al.  Characterization of tissue-specific transcription by the human synapsin I gene promoter. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[25]  Allan Bradley,et al.  Targeted disruption of the c-src proto-oncogene leads to osteopetrosis in mice , 1991, Cell.

[26]  Paul Greengard,et al.  Induction of formation of presynaptic terminals in neuroblastoma cells by synapsin IIb , 1991, Nature.

[27]  F Benfenati,et al.  Computer modeling of synapsin I binding to synaptic vesicles and F-actin: implications for regulation of neurotransmitter release. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[28]  F. Valtorta,et al.  Neurotransmitter release and synaptic vesicle recycling , 1990, Neuroscience.

[29]  E. M. Adler,et al.  Strategic location of calcium channels at transmitter release sites of frog neuromuscular synapses , 1990, Neuron.

[30]  L Thomas,et al.  Synaptophysin binds to physophilin, a putative synaptic plasma membrane protein , 1990, The Journal of cell biology.

[31]  P. Greengard,et al.  Effects of synapsin I and calcium/calmodulin-dependent protein kinase II on spontaneous neurotransmitter release in the squid giant synapse. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[32]  B. Marquèze-Pouey,et al.  Synaptoporin, a novel putative channel protein of synaptic vesicles , 1990, Neuron.

[33]  P. Greengard,et al.  Time-resolved fluorescence study of the neuron-specific phosphoprotein synapsin I. Evidence for phosphorylation-dependent conformational changes. , 1990, The Journal of biological chemistry.

[34]  P. Greengard,et al.  Synapsins in the vertebrate retina: Absence from ribbon synapses and heterogeneous distribution among conventional synapses , 1990, Neuron.

[35]  J. Ferrell,et al.  Intracellular localization of pp60c-src in human platelets. , 1990, Oncogene.

[36]  P. Greengard,et al.  The synapsins and the regulation of synaptic function , 1990, BioEssays : news and reviews in molecular, cellular and developmental biology.

[37]  T. Südhof,et al.  Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C , 1990, Nature.

[38]  F. Hall,et al.  Phosphorylation of synapsin I at a novel site by proline-directed protein kinase. , 1990, The Journal of biological chemistry.

[39]  J. T. Hackett,et al.  Synapsin I injected presynaptically into goldfish mauthner axons reduces quantal synaptic transmission. , 1990, Journal of neurophysiology.

[40]  P. De Camilli,et al.  P29: a novel tyrosine-phosphorylated membrane protein present in small clear vesicles of neurons and endocrine cells , 1990, The Journal of cell biology.

[41]  P. Greengard,et al.  Calcium/calmodulin-dependent protein kinase II increases glutamate and noradrenaline release from synaptosomes , 1990, Nature.

[42]  P. Greengard,et al.  Redistribution of synaptophysin and synapsin I during alpha-latrotoxin- induced release of neurotransmitter at the neuromuscular junction , 1990, The Journal of cell biology.

[43]  M. L. Novas,et al.  The p65 protein is a calmodulin-binding protein present in several types of secretory vesicles , 1989, Neuroscience.

[44]  E. V. Bykova,et al.  Synapsin I from human brain , 1989, FEBS letters.

[45]  P. Greengard,et al.  Translocation of synapsin I in response to depolarization of isolated nerve terminals. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[46]  P. De Camilli,et al.  Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins. , 1989, Science.

[47]  M. Resh Specific and saturable binding of pp60v-src to plasma membranes: Evidence for a myristyl-src receptor , 1989, Cell.

[48]  P. Greengard,et al.  Characterization of synapsin I fragments produced by cysteine-specific cleavage: a study of their interactions with F-actin , 1989, The Journal of cell biology.

[49]  P. Greengard,et al.  Electrostatic and hydrophobic interactions of synapsin I and synapsin I fragments with phospholipid bilayers , 1989, The Journal of cell biology.

[50]  P. Greengard,et al.  Interactions of synapsin I with small synaptic vesicles: distinct sites in synapsin I bind to vesicle phospholipids and vesicle proteins , 1989, The Journal of cell biology.

[51]  K. Jensen,et al.  Ca2+/calmodulin-dependent protein kinase enriched in cerebellar granule cells. Identification of a novel neuronal calmodulin-dependent protein kinase. , 1989, The Journal of biological chemistry.

[52]  N. Hirokawa,et al.  The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1 , 1989, The Journal of cell biology.

[53]  H. Hanafusa,et al.  p60c-src is complexed with a cellular protein in subcellular compartments involved in exocytosis , 1988, The Journal of cell biology.

[54]  E. Bamberg,et al.  Identification of synaptophysin as a hexameric channel protein of the synaptic vesicle membrane. , 1988, Science.

[55]  R. Kelly The cell biology of the nerve terminal , 1988, Neuron.

[56]  P. Greengard,et al.  Widespread distribution of the c-src gene product in nerve cells and axon terminals in the adult rat brain. , 1988, Brain research.

[57]  T. Reese,et al.  The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse , 1988, Neuron.

[58]  P. Greengard,et al.  Protein Tyrosine Kinase Activity and Its Endogenous Substrates in Rat Brain: A Subcellular and Regional Survey , 1988, Journal of neurochemistry.

[59]  P. Greengard,et al.  Localization of synapsin I at the frog neuromuscular junction , 1988, Neuroscience.

[60]  P. Greengard,et al.  Protein tyrosine phosphorylation in synaptic vesicles. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[61]  P. Greengard,et al.  A synaptic vesicle protein with a novel cytoplasmic domain and four transmembrane regions. , 1987, Science.

[62]  P. Greengard,et al.  Amino acid sequences surrounding the cAMP-dependent and calcium/calmodulin-dependent phosphorylation sites in rat and bovine synapsin I. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[63]  T. Petrucci,et al.  Synapsin I: an actin-bundling protein under phosphorylation control , 1987, The Journal of cell biology.

[64]  P. Greengard,et al.  Purification and characterization of Ca2+/calmodulin-dependent protein kinase I from bovine brain. , 1987, The Journal of biological chemistry.

[65]  P. Greengard,et al.  Synapsin I bundles F-actin in a phosphorylation-dependent manner , 1987, Nature.

[66]  P. Greengard,et al.  Characterization of synapsin I binding to small synaptic vesicles. , 1986, The Journal of biological chemistry.

[67]  L. Sternberger,et al.  Association of synapsin I with neuronal cytoskeleton. Identification in cytoskeletal preparations in vitro and immunocytochemical localization in brain of synapsin I. , 1986, The Journal of biological chemistry.

[68]  P. Greengard,et al.  cAMP increases junctional conductance and stimulates phosphorylation of the 27-kDa principal gap junction polypeptide. , 1986, Proceedings of the National Academy of Sciences of the United States of America.

[69]  S. Parsons,et al.  p60c-src activity detected in the chromaffin granule membrane. , 1986, Biochemical and biophysical research communications.

[70]  A. Baines,et al.  Synapsin I is a microtubule-bundling protein , 1986, Nature.

[71]  J. Brugge,et al.  Neurones express high levels of a structurally modified, activated form of pp60c-src , 1985, Nature.

[72]  Bertram Wiedenmann,et al.  Identification and localization of synaptophysin, an integral membrane glycoprotein of Mr 38,000 characteristic of presynaptic vesicles , 1985, Cell.

[73]  P. Greengard,et al.  A 38,000-dalton membrane protein (p38) present in synaptic vesicles. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[74]  R Llinás,et al.  Intraterminal injection of synapsin I or calcium/calmodulin-dependent protein kinase II alters neurotransmitter release at the squid giant synapse. , 1985, Proceedings of the National Academy of Sciences of the United States of America.

[75]  J. Meldolesi,et al.  Specific localization of the alpha-latrotoxin receptor in the nerve terminal plasma membrane , 1984, The Journal of cell biology.

[76]  P. Greengard,et al.  Synapsin I (protein I), a nerve terminal-specific phosphoprotein. III. Its association with synaptic vesicles studied in a highly purified synaptic vesicle preparation , 1983, The Journal of cell biology.

[77]  P. Greengard,et al.  Synapsin I (Protein I), a nerve terminal-specific phosphoprotein. II. Its specific association with synaptic vesicles demonstrated by immunocytochemistry in agarose-embedded synaptosomes , 1983, The Journal of cell biology.

[78]  P. Greengard,et al.  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 , 1983, The Journal of cell biology.

[79]  L. Reichardt,et al.  Identification of a synaptic vesicle-specific membrane protein with a wide distribution in neuronal and neurosecretory tissue , 1981, The Journal of cell biology.

[80]  P. Greengard,et al.  Differential phosphorylation of multiple sites in purified protein I by cyclic AMP-dependent and calcium-dependent protein kinases. , 1981, The Journal of biological chemistry.

[81]  W. P. Hurlbut,et al.  Vesicle hypothesis of the release of quanta of acetylcholine. , 1980, Physiological reviews.

[82]  P. Greengard,et al.  Multiple phosphorylation sites in protein I and their differential regulation by cyclic AMP and calcium. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[83]  H. Schulman,et al.  Neuronal Ca2+/calmodulin-dependent protein kinases. , 1992, Annual review of biochemistry.

[84]  M. Kilimann Protein Phosphorylation in the Nervous System , 1991 .

[85]  P. De Camilli,et al.  Pathways to regulated exocytosis in neurons. , 1990, Annual review of physiology.

[86]  A. Baines,et al.  Synapsin I is a spectrin-binding protein immunologically related to erythrocyte protein 4.1 , 1985, Nature.

[87]  P. Greengard,et al.  Protein phosphorylation in the nervous system , 1984 .