The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse
Abstract
The axoplasm at the presynaptic active zone of excitatory synapses between parallel fibers and Purkinje cell spines contains a meshwork of distinct filaments intermingled with synaptic vesicles, seen most clearly after the rapid freezing, freeze-etch technique of tissue preparation. One set of filaments extends radially from synaptic vesicles and intersects similar filaments associated with vesicles as well as larger filaments arising from the presynaptic membrane. The small, vesicle-associated filaments appear to link synaptic vesicles to one another and to enmesh them in the vicinity of the synaptic junction. The vesicle-associated filaments could be synapsin I because they have the same molecular dimensions and are distributed in the same pattern as synapsin I immunoreactivity.
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?
In cryo-EM studies of unfixed and unstained synapse preparations, no dense projections are detectable; the only structures visible are the plasma membrane, synaptic vesicles, and sparse filaments that connect vesicles to each other or tether vesicles to the presynaptic plasma membrane.
“In cryo-EM studies of unfixed and unstained synapse preparations, however, no dense projections are detectable. The only structures visible are the plasma membrane, synaptic vesicles, and sparse filaments that either connect vesicles to each others (“connectors,” average length ~10 nm) or tether vesicles to the presynaptic plasma membrane (“tethers”—5–20 nm; Landis et al., 1988; Fernández-Busnadie”
From The Presynaptic Active Zone (2012) · cites this paper as Landis et al., 1988
Cites
Heuser, J. E., & Reese, T. S. (1973) · The Journal of Cell Biology · doi:10.1083/jcb.57.2.315 · Cited by 2,147 · see citing works
Self-citationThe Fine Structure of the Nervous System.
Tennyson, V. M. (1970) · Archives of Neurology · doi:10.1001/archneur.1970.00480240094019 · Cited by 1,946 · see citing works
Heuser, J. E., Reese, T. S., Dennis, M. J., Jan, Y. N., Jan, L. Y., & Evans, L. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.81.2.275 · Cited by 1,415 · 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
Relationship between presynaptic calcium current and postsynaptic potential in squid giant synapse
Llinas, R. H., Steinberg, I. Z., & Walton, K. D. (1981) · Biophysical Journal · doi:10.1016/s0006-3495(81)84899-0 · Cited by 706 · see citing works
Aghajanian, G. K., & Bloom, F. E. (1967) · Brain Research · doi:10.1016/0006-8993(67)90128-x · Cited by 667 · 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
fine structure of the nervous system
Peters, A., Palay, S. L., & Webster, H. D. (1976) · Cited by 592 · see citing works
Three-dimensional visualization of coated vesicle formation in fibroblasts.
Heuser, J. E. (1980) · The Journal of Cell Biology · doi:10.1083/jcb.84.3.560 · Cited by 580 · 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
The molecular structure of human erythrocyte spectrin
Shotton, D. M., Burke, B. E., & Branton, D. (1979) · Journal of Molecular Biology · doi:10.1016/0022-2836(79)90078-0 · Cited by 544 · 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
Functional changes in frog neuromuscular junctions studied with freeze-fracture
Heuser, J. E., Reese, T. S., & Landis, D. M. D. (1974) · Journal of Neurocytology · doi:10.1007/bf01111936 · Cited by 515 · see citing works
Self-citationOrganization of mammalian neurofilament polypeptides within the neuronal cytoskeleton.
Hirokawa, N., Glicksman, M. A., & Willard, M. B. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.4.1523 · Cited by 496 · see citing works
Fodrin: axonally transported polypeptides associated with the internal periphery of many cells.
Levine, J., & Willard, M. B. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.90.3.631 · Cited by 476 · see citing works
Structural changes after transmitter release at the frog neuromuscular junction.
Heuser, J. E., & Reese, T. S. (1981) · The Journal of Cell Biology · doi:10.1083/jcb.88.3.564 · Cited by 469 · see citing works
Self-citationStructure and Function of Synapses.
(1972) · Archives of Neurology · doi:10.1001/archneur.1972.00490160092019 · Cited by 444 · see citing works
Rotary shadowing of extended molecules dried from glycerol
Tyler, J. M., & Branton, D. (1980) · Journal of Ultrastructure Research · doi:10.1016/s0022-5320(80)90098-2 · Cited by 420 · see citing works
A STUDY OF EXTRACELLULAR SPACE IN CENTRAL NERVOUS TISSUE BY FREEZE-SUBSTITUTION
Harreveld, A. V., Crowell, J., & Malhotra, S. K. (1965) · The Journal of Cell Biology · doi:10.1083/jcb.25.1.117 · Cited by 412 · 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
Electron microscopy after rapid freezing on a metal surface and substitution fixation
Harreveld, A. V., & Crowell, J. (1964) · The Anatomical Record · doi:10.1002/ar.1091490307 · Cited by 365 · see citing works
Are the presynaptic membrane particles the calcium channels?
Pumplin, D. W., Reese, T. S., & Llinas, R. H. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.11.7210 · Cited by 316 · 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
Kennedy, M. B., & Greengard, P. (1981) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.78.2.1293 · Cited by 298 · 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
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
Cytoplasmic structure in rapid-frozen axons.
Schnapp, B. J., & Reese, T. S. (1982) · The Journal of Cell Biology · doi:10.1083/jcb.94.3.667 · Cited by 230 · see citing works
Self-citationGlenney, J. R., Glenney, P., & Weber, K. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.13.4002 · Cited by 227 · see citing works
Cytoplasmic organization in cerebellar dendritic spines.
Landis, D. M. D., & Reese, T. S. (1983) · The Journal of Cell Biology · doi:10.1083/jcb.97.4.1169 · Cited by 220 · see citing works
Self-citationCytochemistry of Synapses: Selective Staining for Electron Microscopy
Bloom, F. E., & Aghajanian, G. K. (1966) · Science · doi:10.1126/science.154.3756.1575 · Cited by 215 · 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
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
Preservation of Synaptic Structure by Rapid FreezingPreprint
Heuser, J. E., Reese, T. S., & Landis, D. M. D. (1976) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1976.040.01.004 · Cited by 194 · see citing works
Self-citationSynapsin I: A synaptic vesicle-associated neuronal phosphoprotein
Camilli, P. V. D., & Greengard, O. (1986) · Biochemical Pharmacology · doi:10.1016/0006-2952(86)90747-1 · Cited by 168 · see citing works
Spectrin subtypes in mammalian brain: an immunoelectron microscopic study
Zagon, I., Higbee, R. G., Riederer, B. M., & Goodman, S. R. (1986) · Journal of Neuroscience · doi:10.1523/jneurosci.06-10-02977.1986 · Cited by 136 · see citing works
Structure of axon terminals and active zones at synapses on lizard twitch and tonic muscle fibers
Walrond, J., & Reese, T. S. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-05-01118.1985 · Cited by 131 · see citing works
Self-citationDeep-etch views of clathrin assemblies
Heuser, J., & Kirchhausen, T. L. (1985) · Journal of Ultrastructure Research · doi:10.1016/0889-1605(85)90123-5 · Cited by 129 · see citing works
Bridgman, P. C., & Reese, T. S. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.5.1655 · Cited by 124 · see citing works
Self-citationUse of Aldehyde Fixatives to Determine the Rate of Synaptic Transmitter Release
Smith, J. E., & Reese, T. S. (1980) · Journal of Experimental Biology · doi:10.1242/jeb.89.1.19 · Cited by 123 · see citing works
Self-citationHeuser, J. E., & Reese, T. S. (1977) · Comprehensive physiology · doi:10.1002/cphy.cp010108 · Cited by 92 · see citing works
Self-citationHigh-resolution metal replication of macromolecules
Slayter, H. S. (1976) · Ultramicroscopy · doi:10.1016/0304-3991(76)90050-4 · Cited by 69 · see citing works
Nestler, E. J., & Greengard, P. (1982) · Journal of Neuroscience · doi:10.1523/jneurosci.02-08-01011.1982 · Cited by 57 · see citing works
Nakajima, Y., & Reese, T. S. (1983) · The Journal of Comparative Neurology · doi:10.1002/cne.902130106 · Cited by 56 · see citing works
Self-citationMEMBRANE STRUCTURE IN ASTROCYTES
Landis, D. M. D. (1986) · Elsevier eBooks · doi:10.1016/b978-0-12-250453-2.50007-4 · Cited by 10 · see citing works
Self-citationvan der Want, J. J. L., Cardozo, J. J. N., & Vrensen, G. F. J. M. (1984) · Brain Research · doi:10.1016/0006-8993(84)90478-5 · Cited by 8 · see citing works
Flagged first, then by citations
1 of the 46 references couldn’t be matched to a known paper.
Cited by
Sorted by citations
SNAP receptors implicated in vesicle targeting and fusion
Söllner, T. H., Whiteheart, S. W., Brunner, M., Erdjument‐Bromage, H., Geromanos, S. J., Tempst, P., & Rothman, J. E. (1993) · Nature · doi:10.1038/362318a0 · Cited by 3,239 · see citing works
The synaptic vesicle cycle: a cascade of proteinprotein interactions
Südhof, T. (1995) · Nature · doi:10.1038/375645a0 · Cited by 2,002 · 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
Syntaxin: A Synaptic Protein Implicated in Docking of Synaptic Vesicles at Presynaptic Active Zones
Bennett, M. K., Calakos, N., & Scheller, R. H. (1992) · Science · doi:10.1126/science.1321498 · Cited by 1,263 · see citing works
Südhof, T. C. (2012) · Neuron · doi:10.1016/j.neuron.2012.06.012 · Cited by 1,062 · see citing works
Structural Changes Accompanying Memory Storage
Bailey, C. H., & Kandel, E. R. (1993) · Annual Review of Physiology · doi:10.1146/annurev.ph.55.030193.002145 · Cited by 856 · see citing works
Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy.
Cingolani, L. A., & Goda, Y. (2008) · Nature Reviews Neuroscience · doi:10.1038/nrn2373 · Cited by 831 · see citing works
Oyler, G. A., Higgins, G. A., Hart, R. A., Battenberg, E. L. F., Billingsley, M. L., Bloom, F. E., & Wilson, M. C. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.109.6.3039 · Cited by 809 · see citing works
Optical Analysis of Synaptic Vesicle Recycling at the Frog Neuromuscular Junction
Betz, W. J., & Bewick, G. S. (1992) · Science · doi:10.1126/science.1553547 · Cited by 763 · see citing works
Abnormal Spine Morphology and Enhanced LTP in LIMK-1 Knockout Mice
Meng, Y., Zhang, Y., Tregoubov, V., Janus, C., Cruz, L., Jackson, M., Lu, W.-Y., MacDonald, J. F., Wang, J. Y., Falls, D. L., et al. (2002) · Neuron · doi:10.1016/s0896-6273(02)00758-4 · Cited by 688 · see citing works
The synapsins: Key actors of synapse function and plasticity
Cesca, F., Baldelli, P., Valtorta, F., & Benfenati, F. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.006 · Cited by 654 · see citing works
Calcium ions, active zones and synaptic transmitter release
Smith, S. J., & Augustine, G. J. (1988) · Trends in Neurosciences · doi:10.1016/0166-2236(88)90199-3 · Cited by 604 · see citing works
Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminals
Betz, W. J., Mao, F., & Bewick, G. S. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-02-00363.1992 · Cited by 576 · see citing works
Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans
Hall, D. H., & Hedgecock, E. M. (1991) · Cell · doi:10.1016/0092-8674(91)90391-b · Cited by 564 · 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
Proteins of synaptic vesicles involved in exocytosis and membrane recycling
Südhof, T. C., & Jahn, R. (1991) · Neuron · doi:10.1016/0896-6273(91)90165-v · Cited by 522 · see citing works
Dieck, S., Sanmartí-Vila, L., Langnaese, K., Richter, K., Kindler, S., Soyke, A., Wex, H., Smalla, K.-H., Kämpf, U., Fränzer, J.-T., et al. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.2.499 · Cited by 482 · see citing works
The actin cytoskeleton: integrating form and function at the synapse
Dillon, C., & Goda, Y. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135757 · Cited by 447 · see citing works
Phillips, G. R., Huang, J. K., Wang, Y., Tanaka, H., Shapiro, L. S., Zhang, W., Shan, W., Arndt, K., Frank, M., Gordon, R. E., et al. (2001) · Neuron · doi:10.1016/s0896-6273(01)00450-0 · Cited by 438 · see citing works
Ultrastructure of Synapses in the Mammalian BrainPreprint
Harris, K. M., & Weinberg, R. J. (2012) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005587 · Cited by 423 · see citing works
Assembling the Presynaptic Active Zone
Zhai, R. G., Vardinon-Friedman, H., Cases-Langhoff, C., Becker, B., Gundelfinger, E. D., Ziv, N. E., & Garner, C. C. (2001) · Neuron · doi:10.1016/s0896-6273(01)00185-4 · Cited by 424 · see citing works
The septin CDCrel-1 binds syntaxin and inhibits exocytosis
Beites, C. L., Xie, H., Bowser, R. P., & Trimble, W. S. (1999) · Nature Neuroscience · doi:10.1038/8100 · Cited by 377 · see citing works
The liprin protein SYD-2 regulates the differentiation of presynaptic termini in C. elegans
Zhen, M., & Jin, Y. (1999) · Nature · doi:10.1038/43886 · Cited by 374 · see citing works
Molecular organization of the presynaptic active zone
Schoch, S., & Gundelfinger, E. D. (2006) · Cell and Tissue Research · doi:10.1007/s00441-006-0244-y · Cited by 334 · 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
C ELL B IOLOGY OF THE P RESYNAPTIC T ERMINAL
Murthy, V. N., & Camilli, P. V. D. (2003) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.26.041002.131445 · Cited by 330 · 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
A post-docking role for active zone protein Rim
Koushika, S. P., Richmond, J. E., Hadwiger, G., Weimer, R. M., Jørgensen, E. M., & Nonet, M. L. (2001) · Nature Neuroscience · doi:10.1038/nn732 · Cited by 320 · see citing works
Cellular and molecular mechanisms of presynaptic assembly
Ziv, N. E., & Garner, C. C. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1370 · Cited by 306 · see citing works
The Architecture of the Active Zone in the Presynaptic Nerve Terminal
Zhai, R. G., & Bellen, H. J. (2004) · Physiology · doi:10.1152/physiol.00014.2004 · Cited by 291 · see citing works
Ohtsuka, T., Takao‐Rikitsu, E., Inoue, E., Inoue, M., Takeuchi, M., Matsubara, K., Deguchi‐Tawarada, M., Satoh, K., Morimoto, K., Nakanishi, H., et al. (2002) · The Journal of Cell Biology · doi:10.1083/jcb.200202083 · Cited by 295 · see citing works
Piccolo, a presynaptic zinc finger protein structurally related to bassoon
Fenster, S. D., Chung, W. J., Zhai, R., Cases-Langhoff, C., Voss, B., Garner, A. M., Kaempf, U., Kindler, S., Gundelfinger, E. D., & Garner, C. C. (2000) · Neuron · doi:10.1016/s0896-6273(00)80883-1 · Cited by 295 · see citing works
Actin-Dependent Regulation of Neurotransmitter Release at Central Synapses
Morales, M., Colicos, M. A., & Goda, Y. (2000) · Neuron · doi:10.1016/s0896-6273(00)00064-7 · Cited by 300 · see citing works
Phase separation at the synapse
Chen, X., Wu, X., Wu, H., & Zhang, M. (2020) · Nature Neuroscience · doi:10.1038/s41593-019-0579-9 · Cited by 261 · see citing works
Quantitative analysis of the native presynaptic cytomatrix by cryoelectron tomography
Fernández-Busnadiego, R., Zuber, B., Maurer, U. E., Cyrklaff, M., Baumeister, W., & Lučić, V. (2010) · Journal of Cell Biology · doi:10.1083/jcb.200908082 · Cited by 267 · see citing works
Prekeris, R., & Terrian, D. M. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.7.1589 · Cited by 245 · see citing works
Synapsin I, Synapsin II, and Synaptophysin: Marker Proteins of Synaptic Vesicles
Thiel, G. (1993) · Brain Pathology · doi:10.1111/j.1750-3639.1993.tb00729.x · Cited by 237 · see citing works
Zhen, M., Huang, X., Bamber, B. A., & Jin, Y. (2000) · Neuron · doi:10.1016/s0896-6273(00)81167-8 · Cited by 233 · 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
The glutamatergic nerve terminal
Nicholls, D. G. (1993) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1993.tb17700.x · Cited by 222 · see citing works
Molecular determinants of presynaptic active zones
Garner, C. C., Kindler, S., & Gundelfinger, E. D. (2000) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(00)00093-3 · Cited by 221 · see citing works
Takao-Rikitsu, E., Mochida, S., Inoue, E., Deguchi-Tawarada, M., Inoue, M., Ohtsuka, T., & Takai, Y. (2004) · The Journal of Cell Biology · doi:10.1083/jcb.200307101 · Cited by 221 · see citing works
The C. elegans unc-104 4 gene encodes a putative kinesin heavy chain-like protein
Otsuka, A. J., Jeyaprakash, A., Garcı́a-Añoveros, J., Tang, L., Fisk, G. J., Hartshorne, T. A., Franco, R., & Bornt, T. (1991) · Neuron · doi:10.1016/0896-6273(91)90126-k · Cited by 217 · see citing works
The presynaptic cytomatrix of brain synapses
Dresbach, T., Qualmann, B., Kessels, M. M., Garner, C. C., & Gundelfinger, E. D. (2001) · Cellular and Molecular Life Sciences · doi:10.1007/pl00000781 · Cited by 216 · see citing works
Betz, W. J., & Bewick, G. S. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019472 · Cited by 214 · see citing works
Molecular mechanisms of CNS synaptogenesis
Garner, C. C., Zhai, R. G., Gundelfinger, E. D., & Ziv, N. E. (2002) · Trends in Neurosciences · doi:10.1016/s0166-2236(02)02152-5 · Cited by 206 · see citing works
Wang, X., Kibschull, M., Laue, M. M., Lichte, B., Petrasch-Parwez, E., & Kilimann, M. W. (1999) · The Journal of Cell Biology · doi:10.1083/jcb.147.1.151 · Cited by 194 · see citing works
Exocytosis from Neuronal Large Dense-Cored Vesicles
Thureson‐Klein, Å., & Klein, R. L. (1990) · International review of cytology · doi:10.1016/s0074-7696(08)60659-2 · Cited by 193 · 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
GENETICS OF SYNAPTIC VESICLE FUNCTION: Toward the Complete Functional Anatomy of an Organelle
Fernández‐Chacón, R., & Südhof, T. C. (1999) · Annual Review of Physiology · doi:10.1146/annurev.physiol.61.1.753 · Cited by 182 · see citing works
Nakata, T., Sobue, K., & Hirokawa, N. (1990) · The Journal of Cell Biology · doi:10.1083/jcb.110.1.13 · Cited by 183 · see citing works
Multiple roles for the actin cytoskeleton during regulated exocytosis
Porat-Shliom, N., Milberg, O., Masedunskas, A., & Weigert, R. (2013) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-012-1156-5 · Cited by 181 · see citing works
Estes, P. S., Roos, J., van der Bliek, A., Kelly, R. B., Krishnan, K. S., & Ramaswami, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05443.1996 · Cited by 177 · see citing works
A dynamic formin-dependent deep F-actin network in axons
Ganguly, A., Tang, Y., Wang, L., Ladt, K. C., Loi, J., Dargent, B., Leterrier, C., & Roy, S. (2015) · The Journal of Cell Biology · doi:10.1083/jcb.201506110 · Cited by 173 · see citing works
Synaptic 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
Horstmann, H., Körber, C., Sätzler, K., Aydin, D., & Kuner, T. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035172 · Cited by 157 · see citing works
Synaptic structure and function: Dynamic organization yields architectural precision
Burns, M. E., & Augustine, G. J. (1995) · Cell · doi:10.1016/0092-8674(95)90160-4 · Cited by 164 · 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
A common molecular basis for membrane docking and functional priming of synaptic vesicles
Siksou, L., Varoqueaux, F., Pascual, O., Triller, A., Brose, N., & Marty, S. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06811.x · Cited by 160 · see citing works
Perkins, G. A., Tjong, J., Brown, J. M., Poquiz, P., Scott, R. T., Kolson, D. R., Ellisman, M. H., & Spirou, G. A. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1517-09.2010 · Cited by 160 · see citing works
Cellular and Molecular Biology of the Presynaptic Nerve Terminal
Trimble, W. S., Michal Linial, B., & Scheller, R. H. (1991) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.14.030191.000521 · Cited by 158 · see citing works
Analysis of synaptic ultrastructure without fixative using high‐pressure freezing and tomography
Rostaing, P., Réal, É., Siksou, L., Lechaire, J. P., Boudier, T., Boeckers, T. M., Gertler, F. B., Gundelfinger, E. D., Triller, A., & Marty, S. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05234.x · Cited by 152 · see citing works
The actin cytoskeleton and neurotransmitter release: An overview
Doussau, F. (2000) · Biochimie · doi:10.1016/s0300-9084(00)00217-0 · Cited by 149 · see citing works
The synaptic vesicle: cycle of exocytosis and endocytosis
Schweizer, F. E., & Ryan, T. A. (2006) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2006.05.006 · Cited by 142 · see citing works
Brain spectrin: Of mice and men
Goodman, S. R., Zimmer, W. E., Clark, M. B., Zagon, I. S., Barker, J. E., & Bloom, M. L. (1995) · Brain Research Bulletin · doi:10.1016/0361-9230(94)00264-2 · Cited by 133 · 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
Pre- and Postfusion Regulation of Transmitter Release
Rahamimoff, R., & Fernández, J. M. (1997) · Neuron · doi:10.1016/s0896-6273(01)80043-x · Cited by 132 · see citing works
Cryo–electron tomography reveals a critical role of RIM1α in synaptic vesicle tethering
Fernández‐Busnadiego, R., Asano, S. M., Oprişoreanu, A., Sakata, E., Doengi, M., Kochovski, Z., Zürner, M., Stein, V., Schoch, S., Baumeister, W. P., et al. (2013) · The Journal of Cell Biology · doi:10.1083/jcb.201206063 · Cited by 128 · see citing works
Diversity of structure and function at mammalian central synapses
Walmsley, B. D., Álvarez, F. J., & Fyffe, R. E. W. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01170-3 · Cited by 124 · see citing works
The bioenergetics of neurotransmitter release
McMahon, H. T., & Nicholls, D. G. (1991) · Biochimica et Biophysica Acta (BBA) - Bioenergetics · doi:10.1016/s0005-2728(05)80210-5 · Cited by 120 · see citing works
Ruiz, R., Cano, R., Casañas, J. J., Gaffield, M. A., Betz, W. J., & Tabares, L. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4663-10.2011 · Cited by 121 · see citing works
Stigloher, C., Zhan, H., Zhen, M., Richmond, J. E., & Bessereau, J. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6164-10.2011 · Cited by 115 · see citing works
Inoue, E., Mochida, S., Takagi, H., Higa, S., Deguchi‐Tawarada, M., Takao‐Rikitsu, E., Inoue, M., Yao, I., Takeuchi, K., Kitajima, I., et al. (2006) · Neuron · doi:10.1016/j.neuron.2006.03.018 · Cited by 113 · see citing works
Okadaic acid disrupts clusters of synaptic vesicles in frog motor nerve terminals
Betz, W. J., & Henkel, A. W. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.124.5.843 · Cited by 114 · see citing works
Dresbach, T., Hempelmann, A., Spilker, C., Dieck, S. T., Altrock, W. D., Zuschratter, W., Garner, C. C., & Gundelfinger, E. D. (2003) · Molecular and Cellular Neuroscience · doi:10.1016/s1044-7431(03)00015-0 · Cited by 113 · see citing works
The structure of the human synapsin I gene and protein.
Südhof, T. C. (1990) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(19)39008-8 · Cited by 109 · see citing works
Nagwaney, S., Harlow, M. L., Jung, J. H., Szule, J. A., Ress, D. B., Xu, J., Marshall, R. M., & McMahan, U. J. (2009) · The Journal of Comparative Neurology · doi:10.1002/cne.21975 · Cited by 108 · see citing works
5 Intracellular membrane fusion
Rothman, J. E. (1994) · Advances in second messenger and phosphoprotein research · doi:10.1016/s1040-7952(06)80008-x · Cited by 108 · see citing works
Trimble, W. S. (1999) · The Journal of Membrane Biology · doi:10.1007/s002329900519 · Cited by 108 · see citing works
Kraszewski, K., DANIELL, L. W., Mundigl, O., & Camilli, P. V. D. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-05905.1996 · Cited by 106 · see citing works
Fenster, S. D., Kessels, M. M., Qualmann, B., Chung, W. J., Nash, J. E., Gundelfinger, E. D., & Garner, C. C. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210792200 · Cited by 103 · see citing works
How synapsin I may cluster synaptic vesicles
Shupliakov, O., Haucke, V., & Pechstein, A. (2011) · Seminars in Cell and Developmental Biology · doi:10.1016/j.semcdb.2011.07.006 · Cited by 102 · see citing works
Betz, W. J., & Angleson, J. K. (1998) · Annual Review of Physiology · doi:10.1146/annurev.physiol.60.1.347 · Cited by 102 · see citing works
Regulation of Spine Morphology and Synaptic Function by LIMK and the Actin Cytoskeleton
Meng, Y., Zhang, Y., Tregoubov, V., Falls, D. L., & Jia, Z. (2003) · Reviews in the Neurosciences · doi:10.1515/revneuro.2003.14.3.233 · Cited by 101 · see citing works
Henkel, A. W., Simpson, L. L., Ridge, R. M., & Betz, W. J. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-12-03960.1996 · Cited by 101 · see citing works
Ohara‐Imaizumi, M., Ohtsuka, T., Matsushima, S., Akimoto, Y., Nishiwaki, C., Nakamichi, Y., Kikuta, T., Nagai, S., Kawakami, H., Watanabe, T., et al. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-09-0816 · Cited by 99 · 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
Chen, J., Billings, S. E., & Nishimune, H. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.3771-10.2011 · Cited by 94 · see citing works
Castellino, F., Heuser, J., Marchetti, S., Bruno, B., & Luini, A. (1992) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.89.9.3775 · Cited by 95 · see citing works
Leube, R. E., Wiedenmann, B. J., & Franke, W. W. (1989) · Cell · doi:10.1016/0092-8674(89)90028-7 · Cited by 95 · see citing works
Limbach, C., Laue, M. M., Wang, X., Hu, B., Thiede, N., Hultqvist, G., & Kilimann, M. W. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1101707108 · Cited by 92 · see citing works
The mechanism and regulation of fast axonal transport
Sheetz, M. P., Steuer, E. R., & Schroer, T. A. (1989) · Trends in Neurosciences · doi:10.1016/0166-2236(89)90099-4 · Cited by 92 · see citing works
Gotow, T., Miyaguchi, K., & Hashimoto, P. H. (1991) · Neuroscience · doi:10.1016/0306-4522(91)90143-c · Cited by 91 · see citing works
Betz, W. J., Bewick, G. S., & Ridge, R. M. (1992) · Neuron · doi:10.1016/0896-6273(92)90235-6 · Cited by 91 · see citing works
The synapsin cycle: A view from the synaptic endocytic zone
Evergren, E., Benfenati, F., & Shupliakov, O. (2007) · Journal of Neuroscience Research · doi:10.1002/jnr.21176 · Cited by 91 · see citing works
The synapsins and the regulation of synaptic function
Bähler, M., Benfenati, F., Valtorta, F., & Greengard, P. (1990) · BioEssays · doi:10.1002/bies.950120603 · Cited by 91 · see citing works
Secretory Vesicle-Associated Proteins And Their Role In Exocytosis
Burgoyne, R. D. (1990) · Annual Review of Physiology · doi:10.1146/annurev.ph.52.030190.003243 · Cited by 91 · see citing works
Deguchi‐Tawarada, M., Inoue, E., Takao‐Rikitsu, E., Inoue, M., Ohtsuka, T., & Takai, Y. (2004) · Genes to Cells · doi:10.1111/j.1356-9597.2004.00697.x · 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
- Authors
- Landis, D. M. D., Hall, A. K., Weinstein, L. A., & Reese, T. S.
- Affiliations
- Case Western Reserve University (US)
- National Institutes of Health (US)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1988-05
- Volume
- 1
- Issue
- 3
- Pages
- 201-209
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2024032585
- Cited by
- 333
- References
- 46
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 4 · 2023: 6 · 2022: 4 · 2021: 6 · 2020: 3 · 2019: 8 · 2018: 10 · 2017: 9 · 2016: 4 · 2015: 7 · 2014: 12 · 2013: 10 · 2012: 12
- FWCI
- 5.23
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Neurological Disorders and Stroke (NS 23641)
- 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 › Molecular Biology › Extracellular vesicles in disease
- Keywords
- active zone, axoplasm, synaptic vesicles, parallel fibers, synapsin I, cytoskeletal filaments, synapses, excitatory synapses, central nervous system synapses
- MeSH terms
- Animals, Cerebellum, Cytoplasm, Mice, Inbred C57BL, Microscopy, Electron, Nerve Tissue Proteins, Synapses, Synapsins, Mice
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