Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 29 September 1989:
Vol. 245. no. 4925, pp. 1474 - 1480
DOI: 10.1126/science.2506642
Prev | Table of Contents | Next

Articles

Science, Vol 245, Issue 4925, 1474-1480
Copyright © 1989 by American Association for the Advancement of Science

articles

Synapsins: mosaics of shared and individual domains in a family of synaptic vesicle phosphoproteins

TC Sudhof, AJ Czernik, HT Kao, K Takei, PA Johnston, A Horiuchi, SD Kanazir, MA Wagner, MS Perin, P De Camilli, and al. et

Howard Hughes Medical Institute, Dallas, TX.

Synapsins are neuronal phosphoproteins that coat synaptic vesicles, bind to the cytoskeleton, and are believed to function in the regulation of neurotransmitter release. Molecular cloning reveals that the synapsins comprise a family of four homologous proteins whose messenger RNA's are generated by differential splicing of transcripts from two genes. Each synapsin is a mosaic composed of homologous amino-terminal domains common to all synapsins and different combinations of distinct carboxyl-terminal domains. Immunocytochemical studies demonstrate that all four synapsins are widely distributed in nerve terminals, but that their relative amounts vary among different kinds of synapses. The structural diversity and differential distribution of the four synapsins suggest common and different roles of each in the integration of distinct signal transduction pathways that modulate neurotransmitter release in various types of neurons.


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Opposite Changes in Glutamatergic and GABAergic Transmission Underlie the Diffuse Hyperexcitability of Synapsin I-Deficient Cortical Networks.
M. Chiappalone, S. Casagrande, M. Tedesco, F. Valtorta, P. Baldelli, S. Martinoia, and F. Benfenati (2009)
Cereb Cortex 19, 1422-1439
   Abstract »    Full Text »    PDF »
Synapsin IIa Controls the Reserve Pool of Glutamatergic Synaptic Vesicles.
D. Gitler, Q. Cheng, P. Greengard, and G. J. Augustine (2008)
J. Neurosci. 28, 10835-10843
   Abstract »    Full Text »    PDF »
Synapsin-I- and synapsin-II-null mice display an increased age-dependent cognitive impairment.
A. Corradi, A. Zanardi, C. Giacomini, F. Onofri, F. Valtorta, M. Zoli, and F. Benfenati (2008)
J. Cell Sci. 121, 3042-3051
   Abstract »    Full Text »    PDF »
5-HT4 receptor activation facilitates recovery from synaptic rundown and increases transmitter release from single varicosities of myenteric neurons.
J. Ren, X. Zhou, and J. J. Galligan (2008)
Am J Physiol Gastrointest Liver Physiol 294, G1376-G1383
   Abstract »    Full Text »    PDF »
Lack of Synapsin I Reduces the Readily Releasable Pool of Synaptic Vesicles at Central Inhibitory Synapses.
P. Baldelli, A. Fassio, F. Valtorta, and F. Benfenati (2007)
J. Neurosci. 27, 13520-13531
   Abstract »    Full Text »    PDF »
Expression of a synapsin IIb site 1 phosphorylation mutant in 3T3-L1 adipocytes inhibits basal intracellular retention of Glut4.
J. M. Muretta, I. Romenskaia, P. A. Cassiday, and C. C. Mastick (2007)
J. Cell Sci. 120, 1168-1177
   Abstract »    Full Text »    PDF »
Protein Kinase A-Mediated Synapsin I Phosphorylation Is a Central Modulator of Ca2+-Dependent Synaptic Activity..
A. Menegon, D. Bonanomi, C. Albertinazzi, F. Lotti, G. Ferrari, H.-T. Kao, F. Benfenati, P. Baldelli, and F. Valtorta (2006)
J. Neurosci. 26, 11670-11681
   Abstract »    Full Text »    PDF »
The synapsin domain E accelerates the exoendocytotic cycle of synaptic vesicles in cerebellar Purkinje cells.
A. Fassio, D. Merlo, J. Mapelli, A. Menegon, A. Corradi, M. Mete, S. Zappettini, G. Bonanno, F. Valtorta, E. D'Angelo, et al. (2006)
J. Cell Sci. 119, 4257-4268
   Abstract »    Full Text »    PDF »
Synapsin Utilization Differs among Functional Classes of Synapses on Thalamocortical Cells.
A. Kielland, A. Erisir, S. I. Walaas, and P. Heggelund (2006)
J. Neurosci. 26, 5786-5793
   Abstract »    Full Text »    PDF »
Synapsin I Is a Major Endogenous Substrate for Protein L-Isoaspartyl Methyltransferase in Mammalian Brain.
K. J. Reissner, M. V. Paranandi, T. M. Luc, H. A. Doyle, M. J. Mamula, J. D. Lowenson, and D. W. Aswad (2006)
J. Biol. Chem. 281, 8389-8398
   Abstract »    Full Text »    PDF »
Synapsins regulate use-dependent synaptic plasticity in the calyx of Held by a Ca2+/calmodulin-dependent pathway.
J. Sun, P. Bronk, X. Liu, W. Han, and T. C. Sudhof (2006)
PNAS 103, 2880-2885
   Abstract »    Full Text »    PDF »
Gonadotropin-Releasing Hormone-Expressing Neurons Immortalized Conditionally Are Activated by Insulin: Implication of the Mitogen-Activated Protein Kinase Pathway.
R. Salvi, E. Castillo, M.-J. Voirol, M. Glauser, J.-P. Rey, R. C. Gaillard, P. Vollenweider, and F. P. Pralong (2006)
Endocrinology 147, 816-826
   Abstract »    Full Text »    PDF »
A segment of the Mecp2 promoter is sufficient to drive expression in neurons.
M. Adachi, E. W. Keefer, and F. S. Jones (2005)
Hum. Mol. Genet. 14, 3709-3722
   Abstract »    Full Text »    PDF »
Distinct Roles of Calcineurin-Nuclear Factor of Activated T-Cells and Protein Kinase A-cAMP Response Element-Binding Protein Signaling in Presynaptic Differentiation.
T. Yoshida and M. Mishina (2005)
J. Neurosci. 25, 3067-3079
   Abstract »    Full Text »    PDF »
Structural Domains Involved in the Regulation of Transmitter Release by Synapsins.
S. Hilfiker, F. Benfenati, F. Doussau, A. C. Nairn, A. J. Czernik, G. J. Augustine, and P. Greengard (2005)
J. Neurosci. 25, 2658-2669
   Abstract »    Full Text »    PDF »
A Protein Phosphatase 2c{alpha}-Ca2+ Channel Complex for Dephosphorylation of Neuronal Ca2+ Channels Phosphorylated by Protein Kinase C.
D. Li, F. Wang, M. Lai, Y. Chen, and J.-f. Zhang (2005)
J. Neurosci. 25, 1914-1923
   Abstract »    Full Text »    PDF »
Different Presynaptic Roles of Synapsins at Excitatory and Inhibitory Synapses.
D. Gitler, Y. Takagishi, J. Feng, Y. Ren, R. M. Rodriguiz, W. C. Wetsel, P. Greengard, and G. J. Augustine (2004)
J. Neurosci. 24, 11368-11380
   Abstract »    Full Text »    PDF »
Mast cells: A unique source of renin.
R. B. Silver, A. C. Reid, C. J. Mackins, T. Askwith, U. Schaefer, D. Herzlinger, and R. Levi (2004)
PNAS 101, 13607-13612
   Abstract »    Full Text »    PDF »
Molecular Determinants of Synapsin Targeting to Presynaptic Terminals.
D. Gitler, Y. Xu, H.-T. Kao, D. Lin, S. Lim, J. Feng, P. Greengard, and G. J. Augustine (2004)
J. Neurosci. 24, 3711-3720
   Abstract »    Full Text »    PDF »
Tetramerization and ATP Binding by a Protein Comprising the A, B, and C Domains of Rat Synapsin I.
C. A. Brautigam, Y. Chelliah, and J. Deisenhofer (2004)
J. Biol. Chem. 279, 11948-11956
   Abstract »    Full Text »    PDF »
Identification of a mutation in synapsin I, a synaptic vesicle protein, in a family with epilepsy.
C C Garcia, H J Blair, M Seager, A Coulthard, S Tennant, M Buddles, A Curtis, and J A Goodship (2004)
J. Med. Genet. 41, 183-186
   Abstract »    Full Text »    PDF »
Phosphorylation-regulated Inhibition of the Gz GTPase-activating Protein Activity of RGS Proteins by Synapsin I.
Y. Tu, S. K. Nayak, J. Woodson, and E. M. Ross (2003)
J. Biol. Chem. 278, 52273-52281
   Abstract »    Full Text »    PDF »
Serotonin Stimulates Phosphorylation of Aplysia Synapsin and Alters Its Subcellular Distribution in Sensory Neurons.
A. Angers, D. Fioravante, J. Chin, L. J. Cleary, A. J. Bean, and J. H. Byrne (2002)
J. Neurosci. 22, 5412-5422
   Abstract »    Full Text »    PDF »
Regulation of Neurotransmitter Release by Synapsin III.
J. Feng, P. Chi, T. A. Blanpied, Y. Xu, A. M. Magarinos, A. Ferreira, R. H. Takahashi, H.-T. Kao, B. S. McEwen, T. A. Ryan, et al. (2002)
J. Neurosci. 22, 4372-4380
   Abstract »    Full Text »    PDF »
Synapsin I is expressed in epithelial cells: localization to a unique trans-Golgi compartment.
R. Bustos, E. R. Kolen, L. Braiterman, A. J. Baines, F. S. Gorelick, and A. L. Hubbard (2002)
J. Cell Sci. 114, 3695-3704
   Abstract »    Full Text »    PDF »
Agrin Differentially Regulates the Rates of Axonal and Dendritic Elongation in Cultured Hippocampal Neurons.
K. B. Mantych and A. Ferreira (2001)
J. Neurosci. 21, 6802-6809
   Abstract »    Full Text »    PDF »
Synapsin Controls Both Reserve and Releasable Synaptic Vesicle Pools during Neuronal Activity and Short-Term Plasticity in Aplysia.
Y. Humeau, F. Doussau, F. Vitiello, P. Greengard, F. Benfenati, and B. Poulain (2001)
J. Neurosci. 21, 4195-4206
   Abstract »    Full Text »    PDF »
Synapsin III: Developmental Expression, Subcellular Localization, and Role in Axon Formation.
A. Ferreira, H.-T. Kao, J. Feng, M. Rapoport, and P. Greengard (2000)
J. Neurosci. 20, 3736-3744
   Abstract »    Full Text »    PDF »
Presynaptic Heterogeneity: Vive la difference.
J. K. Staple, F. Morgenthaler, and S. Catsicas (2000)
Physiology 15, 45-49
   Abstract »    Full Text »    PDF »
All three PACSIN isoforms bind to endocytic proteins and inhibit endocytosis.
J Modregger, B Ritter, B Witter, M Paulsson, and M Plomann (2000)
J. Cell Sci. 113, 4511-4521
   Abstract »    PDF »
Use of phosphosynapsin I-specific antibodies for image analysis of signal transduction in single nerve terminals.
A Menegon, D. Dunlap, F Castano, F Benfenati, A. Czernik, P Greengard, and F Valtorta (2000)
J. Cell Sci. 113, 3573-3582
   Abstract »    PDF »
Proteins involved in synaptic vesicle trafficking.
G. J Augustine, M. E Burns, W. M DeBello, S. Hilfiker, J. R Morgan, F. E Schweizer, H. Tokumaru, and K. Umayahara (1999)
J. Physiol. 520, 33-41
   Abstract »    Full Text »    PDF »
Homo- and Heterodimerization of Synapsins.
M. Hosaka and T. C. Sudhof (1999)
J. Biol. Chem. 274, 16747-16753
   Abstract »    Full Text »    PDF »
Impairment of Inhibitory Synaptic Transmission in Mice Lacking Synapsin I.
S. Terada, T. Tsujimoto, Y. Takei, T. Takahashi, and N. Hirokawa (1999)
J. Cell Biol. 145, 1039-1048
   Abstract »    Full Text »    PDF »
Cloning from Insulinoma Cells of Synapsin I Associated with Insulin Secretory Granules.
K. Matsumoto, K. Ebihara, H. Yamamoto, H. Tabuchi, K. Fukunaga, M. Yasunami, H. Ohkubo, M. Shichiri, and E. Miyamoto (1999)
J. Biol. Chem. 274, 2053-2059
   Abstract »    Full Text »    PDF »
Myosin I heavy chain kinase: Cloning of the full-length gene and acidic lipid-dependent activation by Rac and Cdc42.
H. Brzeska, R. Young, U. Knaus, and E. D. Korn (1999)
PNAS 96, 394-399
   Abstract »    Full Text »    PDF »
Abnormal synapse formation in agrin-depleted hippocampal neurons.
A Ferreira (1999)
J. Cell Sci. 112, 4729-4738
   Abstract »    PDF »
Newly Synthesized Phosphatidylinositol Phosphates Are Required for Synaptic Norepinephrine but Not Glutamate or gamma -Aminobutyric Acid (GABA) Release.
M. Khvotchev and T. C. Sudhof (1998)
J. Biol. Chem. 273, 21451-21454
   Abstract »    Full Text »    PDF »
Synapsin III, a Novel Synapsin with an Unusual Regulation by Ca2+.
M. Hosaka and T. C. Sudhof (1998)
J. Biol. Chem. 273, 13371-13374
   Abstract »    Full Text »    PDF »
A third member of the synapsin gene family.
H.-T. Kao, B. Porton, A. J. Czernik, J. Feng, G. Yiu, M. Haring, F. Benfenati, and P. Greengard (1998)
PNAS 95, 4667-4672
   Abstract »    Full Text »    PDF »
Synapsins I and II Are ATP-binding Proteins with Differential Ca2+ Regulation.
M. Hosaka and T. C. Sudhof (1998)
J. Biol. Chem. 273, 1425-1429
   Abstract »    Full Text »    PDF »
Synapsin I interacts with c-Src and stimulates its tyrosine kinase activity.
F. Onofri, S. Giovedi, P. Vaccaro, A. J. Czernik, F. Valtorta, P. De Camilli, P. Greengard, and F. Benfenati (1997)
PNAS 94, 12168-12173
   Abstract »    Full Text »    PDF »
Molecular Characterization of GCP170, a 170-kDa Protein Associated with the Cytoplasmic Face of the Golgi Membrane.
Y. Misumi, M. Sohda, A. Yano, T. Fujiwara, and Y. Ikehara (1997)
J. Biol. Chem. 272, 23851-23858
   Abstract »    Full Text »    PDF »
Post-Transcriptional Regulation of Synaptic Vesicle Protein Expression and the Developmental Control of Synaptic Vesicle Formation.
C. Daly and E. B. Ziff (1997)
J. Neurosci. 17, 2365-2375
   Abstract »    Full Text »    PDF »
Similarities of Integumentary Mucin B.1 from Xenopus laevis and Prepro-von Willebrand Factor at Their Amino-terminal Regions.
W. Joba and W. Hoffmann (1997)
J. Biol. Chem. 272, 1805-1810
   Abstract »    Full Text »    PDF »
Site-specific Phosphorylation of Synapsin I by Mitogen-activated Protein Kinase and Cdk5 and Its Effects on Physiological Functions.
M. Matsubara, M. Kusubata, K. Ishiguro, T. Uchida, K. Titani, and H. Taniguchi (1996)
J. Biol. Chem. 271, 21108-21113
   Abstract »    Full Text »    PDF »
Invertebrate Synapsins: A Single Gene Codes for Several Isoforms in Drosophila.
B. R. E. Klagges, G. Heimbeck, T. A. Godenschwege, A. Hofbauer, G. O. Pflugfelder, R. Reifegerste, D. Reisch, M. Schaupp, S. Buchner, and E. Buchner (1996)
J. Neurosci. 16, 3154-3165
   Abstract »    Full Text »    PDF »
Neuron-specific Gene Expression of Synapsin I.
S. Schoch, G. Cibelli, and G. Thiel (1996)
J. Biol. Chem. 271, 3317-3323
   Abstract »    Full Text »    PDF »
The Human Synapsin II Gene Promoter.
D. Petersohn, S. Schoch, D. R. Brinkmann, and G. Thiel (1995)
J. Biol. Chem. 270, 24361-24369
   Abstract »    Full Text »    PDF »
A Systematic Approach to Studying Synaptic Function in Vertebrates.
R. Janz and T.C. Sudhof (1995)
Cold Spring Harb Symp Quant Biol 60, 309-314
   Abstract »    PDF »
Synaptic vesicle phosphoproteins and regulation of synaptic function.
P Greengard, F Valtorta, A. Czernik, and F Benfenati (1993)
Science 259, 780-785
   Abstract »    PDF »
Syntaxin: a synaptic protein implicated in docking of synaptic vesicles at presynaptic active zones.
M. Bennett, N Calakos, and R. Scheller (1992)
Science 257, 255-259
   Abstract »    PDF »
Neurexins: synaptic cell surface proteins related to the alpha-latrotoxin receptor and laminin.
Y. Ushkaryov, A. Petrenko, M Geppert, and T. Sudhof (1992)
Science 257, 50-56
   Abstract »    PDF »
Neurexins.
M. Geppert, Y.A. Ushkaryov, Y. Hata, B. Davletov, A.G. Petrenko, and T.C. Sudhof (1992)
Cold Spring Harb Symp Quant Biol 57, 483-490
   Abstract »    PDF »
An Analysis of Synapsin II, a Neuronal Phosphoprotein, in Postmortem Brain Tissue From Alcoholic and Neuropsychiatrically Ill Adults and Medically Ill Children and Young Adults.
J. A. Grebb and P. Greengard (1990)
Arch Gen Psychiatry 47, 1149-1156
   Abstract »    PDF »
Specificity of the Binding of Synapsin I to Src Homology 3 Domains.
F. Onofri, S. Giovedi, H.-T. Kao, F. Valtorta, L. B. Borbone, P. De Camilli, P. Greengard, and F. Benfenati (2000)
J. Biol. Chem. 275, 29857-29867
   Abstract »    Full Text »    PDF »
Cyclosporine A-induced hypertension involves synapsin in renal sensory nerve endings.
W. Zhang, J.-L. Li, M. Hosaka, R. Janz, J. M. Shelton, G. M. Albright, J. A. Richardson, T. C. Sudhof, and R. G. Victor (2000)
PNAS 97, 9765-9770
   Abstract »    Full Text »    PDF »
Neuronal nitric-oxide synthase localization mediated by a ternary complex with synapsin and CAPON.
S. R. Jaffrey, F. Benfenati, A. M. Snowman, A. J. Czernik, and S. H. Snyder (2002)
PNAS 99, 3199-3204
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)