Citron binds to PSD-95 at glutamatergic synapses on inhibitory neurons in the hippocampus
Open accessAbstract
Synaptic NMDA-type glutamate receptors are anchored to the second of three PDZ (PSD-95/Discs large/ZO-1) domains in the postsynaptic density (PSD) protein PSD-95. Here, we report that citron, a protein target for the activated form of the small GTP-binding protein Rho, preferentially binds the third PDZ domain of PSD-95. In GABAergic neurons from the hippocampus, citron forms a complex with PSD-95 and is concentrated at the postsynaptic side of glutamatergic synapses. Citron is expressed only at low levels in glutamatergic neurons in the hippocampus and is not detectable at synapses onto these neurons. In contrast to citron, p135 SynGAP, an abundant synaptic Ras GTPase-activating protein that can bind to all three PDZ domains of PSD-95, and Ca 2+/calmodulin-dependent protein kinase II (CaM kinase II) are concentrated postsynaptically at glutamatergic synapses on glutamatergic neurons. CaM kinase II is not expressed and p135 SynGAP is expressed in less than half of hippocampal GABAergic neurons. Segregation of citron into inhibitory neurons does not occur in other brain regions. For example, citron is expressed at high levels in most thalamic neurons, which are primarily glutamatergic and contain CaM kinase II. In several other brain regions, citron is present in a subset of neurons that can be either GABAergic or glutamatergic and can sometimes express CaM kinase II. Thus, in the hippocampus, signal transduction complexes associated with postsynaptic NMDA receptors are different in glutamatergic and GABAergic neurons and are specialized in a way that is specific to the hippocampus.
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SYNGAP1 encodes a synaptic RasGAP (SynGAP) largely localized to dendritic spines in neocortical pyramidal neurons, where it suppresses signaling linked to NMDAR-mediated plasticity and AMPAR membrane insertion.
“SYNGAP1 encodes a synaptic RasGAP (SynGAP) that is largely localized to dendritic spines in neocortical pyramidal neurons (Chen et al., 1998; Kim et al., 1998; Zhang et al., 1999), where it suppresses signaling pathways linked to NMDA receptor (NMDAR) mediated synaptic plasticity and AMPA receptor (AMPAR) membrane insertion”
From Pathogenic SYNGAP1 Mutations Impair Cognitive Development by Disrupting Maturation of Dendritic Spine Synapses (2012) · cites this paper as Zhang et al., 1999
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The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585 · see citing works
A synaptic model of memory: long-term potentiation in the hippocampus
Bliss, T. V. P., & Collingridge, G. L. (1993) · Nature · doi:10.1038/361031a0 · Cited by 11,566 · see citing works
Rho GTPases and the Actin Cytoskeleton
Hall, A. (1998) · Science · doi:10.1126/science.279.5350.509 · Cited by 6,138 · see citing works
AChE-stained horizontal sections of the rat brain in stereotaxic coordinates
Paxinos, G., WATSON, C. R. R., & Emson, P. C. (1980) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(80)90021-7 · Cited by 4,497 · see citing works
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,423 · see citing works
Brewer, G. J., Torricelli, J. R., Evege, E. K., & Price, P. J. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490350513 · Cited by 2,094 · see citing works
Domain Interaction Between NMDA Receptor Subunits and the Postsynaptic Density Protein PSD-95
Kornau, H., Schenker, L. T., Kennedy, M. B., & Seeburg, P. H. (1995) · Science · doi:10.1126/science.7569905 · Cited by 1,882 · see citing works
Self-citation[12] Determination of total protein
Peterson, G. L. (1983) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(83)91014-5 · Cited by 1,281 · see citing works
Cho, K.-O., Hunt, C. A., & Kennedy, M. B. (1992) · Neuron · doi:10.1016/0896-6273(92)90245-9 · Cited by 1,193 · see citing works
Self-citationMatsui, T., Amano, M., Yamamoto, T., Chihara, K., Nakafuku, M., Ito, M., Nakano, T., Okawa, K., Iwamatsu, A., & Kaibuchi, K. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00574.x · Cited by 1,062 · see citing works
Kim, E., Niethammer, M., Rothschild, A., Jan, Y. N., & Sheng, M. (1995) · Nature · doi:10.1038/378085a0 · Cited by 999 · see citing works
Woods, D. F., & Bryant, P. J. (1991) · Cell · doi:10.1016/0092-8674(81)90009-x · Cited by 898 · see citing works
Ishizaki, T., Maekawa, M., Fujisawa, K., Okawa, K., Iwamatsu, A., Fujita, A., Watanabe, N., Saito, Y., Kakizuka, A., Morii, N., et al. (1996) · The EMBO Journal · doi:10.1002/j.1460-2075.1996.tb00539.x · Cited by 882 · see citing works
Niethammer, M., Kim, E., & Sheng, M. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-07-02157.1996 · Cited by 750 · see citing works
Binding of Neuroligins to PSD-95
Irie, M., Hata, Y., Takeuchi, M., Ichtchenko, K., Toyoda, A., Hirao, K., Takai, Y., Rosahl, T. W., & Südhof, T. C. (1997) · Science · doi:10.1126/science.277.5331.1511 · Cited by 749 · see citing works
LEUNG, T. K. C., Manser, E. J., Tan, L. H.-P., & Lim, L. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.49.29051 · Cited by 720 · see citing works
SynGAP: a Synaptic RasGAP that Associates with the PSD-95/SAP90 Protein Family
Kim, J. H., Liao, D., Lau, L.-F., & Huganir, R. L. (1998) · Neuron · doi:10.1016/s0896-6273(00)81008-9 · Cited by 634 · see citing works
Regional distribution of type II Ca2+/calmodulin-dependent protein kinase in rat brain
Erondu, N., & Kennedy, M. (1985) · The Journal of Neuroscience · doi:10.1523/jneurosci.05-12-03270.1985 · Cited by 630 · see citing works
Self-citationA multivalent PDZ-domain protein assembles signalling complexes in a G-protein-coupled cascade
Tsunoda, S., Sierralta, J. A., Sun, Y., Bodner, R. A., Suzuki, E., Becker, A., Socolich, M., & Zuker, C. S. (1997) · Nature · doi:10.1038/40805 · Cited by 614 · see citing works
Competitive binding of α-actinin and calmodulin to the NMDA receptor
Wyszynski, M., Lin, J., Rao, A., Nigh, E., Beggs, A. H., Craig, A. M., & Sheng, M. (1997) · Nature · doi:10.1038/385439a0 · Cited by 596 · see citing works
A Synaptic Ras-GTPase Activating Protein (p135 SynGAP) Inhibited by CaM Kinase II
Chen, H.-J., Rojas-Soto, M., Oguni, A., & Kennedy, M. B. (1998) · Neuron · doi:10.1016/s0896-6273(00)80471-7 · Cited by 590 · see citing works
Self-citationCamilli, 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
Kim, E., Naisbitt, S., Hsueh, Y.-P., Rao, A., Rothschild, A., Craig, A. M., & Sheng, M. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.3.669 · Cited by 516 · see citing works
The postsynaptic density at glutamatergic synapses
Kennedy, M. B. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01033-8 · Cited by 475 · see citing works
Self-citationWillott, E., Balda, M. S., Fanning, A. S., Jameson, B., Itallie, C. M. V., & Anderson, J. M. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.16.7834 · Cited by 469 · see citing works
Differential effects of the Rac GTPase on Purkinje cell axons and dendritic trunks and spines
Luo, L., Hensch, T. K., Ackerman, L. D., Barbel, S., Jan, L. Y., & Jan, Y. N. (1996) · Nature · doi:10.1038/379837a0 · Cited by 453 · see citing works
McGlade-McCulloh, E., Yamamoto, H., Tan, S.-E., Brickey, D. A., & Soderling, T. (1993) · Nature · doi:10.1038/362640a0 · Cited by 441 · see citing works
SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo.
Müller, B., Kistner, U., Kindler, S., Chung, W. J., Kuhlendahl, S., Fenster, S. D., Lau, L.-F., Veh, R., Huganir, R., Gundelfinger, E., et al. (1996) · Neuron · doi:10.1016/s0896-6273(00)80157-9 · Cited by 435 · see citing works
Kistner, U., Wenzel, B., Veh, R. W., Cases-Langhoff, C., Garner, A. M., APPELTAUER, U., Voss, B., Gundelfinger, E. D., & Garner, C. C. (1993) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)53433-5 · Cited by 414 · see citing works
Role of citron kinase as a target of the small GTPase Rho in cytokinesis
Madaule, P., Eda, M., Watanabe, N., Fujisawa, K., Matsuoka, T., Bito, H., Ishizaki, T., & Narumiya, S. (1998) · Nature · doi:10.1038/28873 · Cited by 402 · see citing works
High actin concentrations in brain dendritic spines and postsynaptic densities.
Matus, A., Ackermann, M., Pehling, G., Byers, H. R., & Fujiwara, K. (1982) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.79.23.7590 · Cited by 401 · see citing works
Rao, A., Kim, E., Sheng, M., & Craig, A. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01217.1998 · Cited by 392 · see citing works
Muller, B., Kistner, U., Veh, R. W., Cases-Langhoff, C., Becker, B., Gundelfinger, E., & Garner, C. C. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-03-02354.1995 · Cited by 381 · see citing works
Interaction of ion channels and receptors with PDZ domain proteins
Kornau, H., Seeburg, P. H., & Kennedy, M. B. (1997) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(97)80064-5 · Cited by 360 · see citing works
Self-citationCloning and Characterization of Postsynaptic Density 93, a Nitric Oxide Synthase Interacting Protein
Brenman, J. E., Christopherson, K. S., Craven, S. E., McGee, A. W., & Bredt, D. S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-23-07407.1996 · Cited by 333 · see citing works
Hunt, C., Schenker, L. J., & Kennedy, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-04-01380.1996 · Cited by 313 · see citing works
Self-citationMoon, I. S., Apperson, M., & Kennedy, M. B. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.9.3954 · Cited by 309 · see citing works
Self-citationOmkumar, R. V., Kiely, M. J., Rosenstein, A. J., Min, K.-T., & Kennedy, M. B. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.49.31670 · Cited by 304 · see citing works
Self-citationCRIPT, a Novel Postsynaptic Protein that Binds to the Third PDZ Domain of PSD-95/SAP90
Niethammer, M., Valtschanoff, J. G., Kapoor, T. M., Allison, D. W., Weinberg, R. J., Craig, A. M., & Sheng, M. (1998) · Neuron · doi:10.1016/s0896-6273(00)81009-0 · Cited by 303 · see citing works
Chevesich, J., Kreuz, A. J., & Montell, C. (1997) · Neuron · doi:10.1016/s0896-6273(01)80049-0 · Cited by 290 · see citing works
Leung, T., Chen, X., Tan, I., Manser, E. J., & Lim, L. (1998) · Molecular and Cellular Biology · doi:10.1128/mcb.18.1.130 · Cited by 272 · see citing works
Essential Role fordlgin Synaptic Clustering of Shaker K+ChannelsIn Vivo
Tejedor, F. J., Bokhari, A., Rogero, O., Gorczyca, M. G., Zhang, J., Kim, E., Sheng, M., & Budnik, V. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00152.1997 · Cited by 264 · see citing works
Craig, A. M., Blackstone, C. D., Huganir, R. L., & Banker, G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.26.12373 · Cited by 237 · see citing works
Target-Specific Expression of Presynaptic Mossy Fiber Plasticity
Maccaferri, G., Tóth, K., & McBain, C. J. (1998) · Science · doi:10.1126/science.279.5355.1368 · Cited by 225 · 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
The absence of a major Ca <sup>2+</sup> signaling pathway in GABAergic neurons of the hippocampus
Sík, A., Hájos, N., Gulácsi, A., Mody, I., & Freund, T. F. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3245 · Cited by 186 · see citing works
Hippocampal Interneurons Express a Novel Form of Synaptic Plasticity
McMahon, L. L., & Kauer, J. A. (1997) · Neuron · doi:10.1016/s0896-6273(00)80269-x · Cited by 182 · see citing works
Lau, L., Mammen, A. L., Ehlers, M., Kindler, S., Chung, W. J., Garner, C. C., & Huganir, R. L. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.35.21622 · Cited by 177 · see citing works
A novel partner for the GTP‐bound forms of rho and rac
Madaule, P., Furuyashiki, T., Reid, T., Ishizaki, T., Watanabe, G., Morii, N., & Narumiya, S. (1995) · FEBS Letters · doi:10.1016/0014-5793(95)01351-2 · Cited by 168 · see citing works
Benson, D. L., Isackson, P. J., Hendry, S., & Jones, E. G. (1991) · Journal of Neuroscience · doi:10.1523/jneurosci.11-06-01540.1991 · Cited by 163 · see citing works
Apperson, M., Moon, I. S., & Kennedy, M. B. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-21-06839.1996 · Cited by 163 · see citing works
Self-citationIsoform Specificity in the Relationship of Actin to Dendritic Spines
Kaech, S., Fischer, M., Doll, T., & Matus, A. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-24-09565.1997 · Cited by 155 · see citing works
Jones, E. G., Huntley, G. W., & Benson, D. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00611.1994 · Cited by 141 · see citing works
Laube, G., Röper, J., Pitt, J. C., Sewing, S., Kistner, U., Garner, C. C., Pongs, O., & Veh, R. W. (1996) · Molecular Brain Research · doi:10.1016/s0169-328x(96)00120-9 · Cited by 139 · see citing works
Kennedy, M. B. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90145-o · Cited by 136 · see citing works
Self-citationLong-Term Potentiation in Distinct Subtypes of Hippocampal Nonpyramidal Neurons
Maccaferri, G., & McBain, C. J. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-17-05334.1996 · Cited by 133 · see citing works
Molloy, S. S., & Kennedy, M. B. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.11.4756 · Cited by 132 · see citing works
Self-citationGenghis Khan (Gek) as a putative effector for Drosophila Cdc42 and regulator of actin polymerization
Luo, L., Lee, T., Tsai, L. T.-Y., Tang, G. L., Jan, L. Y., & Jan, Y. N. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.24.12963 · Cited by 68 · see citing works
Patton, B. L., Molloy, S. S., & Kennedy, M. B. (1993) · Molecular Biology of the Cell · doi:10.1091/mbc.4.2.159 · Cited by 37 · see citing works
Self-citationA modified method for obtaining large amounts of high titer polyclonal ascites fluid
Ou, S. K.-H., Hwang, J. M.-C., & Patterson, P. H. (1993) · Journal of Immunological Methods · doi:10.1016/0022-1759(93)90108-j · Cited by 37 · see citing works
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Millar, J. K. (2000) · Human Molecular Genetics · doi:10.1093/hmg/9.9.1415 · Cited by 1,254 · see citing works
PDZ Domains and the Organization of Supramolecular Complexes
Sheng, M., & Sala, C. (2001) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.24.1.1 · Cited by 1,191 · see citing works
The Postsynaptic Architecture of Excitatory Synapses: A More Quantitative View
Sheng, M., & Hoogenraad, C. C. (2007) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.76.060805.160029 · Cited by 1,003 · see citing works
Signal-Processing Machines at the Postsynaptic Density
Kennedy, M. B. (2000) · Science · doi:10.1126/science.290.5492.750 · Cited by 788 · see citing works
Self-citationThe Postsynaptic Organization of Synapses
Sheng, M., & Kim, E. (2011) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a005678 · Cited by 603 · see citing works
Molecular Mechanisms of Glutamate Receptor-Mediated Excitotoxic Neuronal Cell Death
Sattler, R., & Tymianski, M. (2001) · Molecular Neurobiology · doi:10.1385/mn:24:1-3:107 · Cited by 537 · see citing works
PDZ domains in synapse assembly and signalling
Garner, C. C., Nash, J. E., & Huganir, R. L. (2000) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01783-9 · Cited by 520 · see citing works
Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product narp.
O’Brien, R. J., Xu, D., Petralia, R. S., Steward, O., Huganir, R. L., & Worley, P. (1999) · Neuron · doi:10.1016/s0896-6273(00)80782-5 · Cited by 471 · see citing works
Postsynaptic organisation and regulation of excitatory synapses
Scannevin, R. H., & Huganir, R. L. (2000) · Nature reviews. Neuroscience · doi:10.1038/35039075 · Cited by 460 · see citing works
Dendrite growth increased by visual activity requires NMDA receptor and Rho GTPases
Sin, W. C., Haas, K. Z., Ruthazer, E. S., & Cline, H. T. (2002) · Nature · doi:10.1038/nature00987 · Cited by 433 · 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
Identification of Proteins in the Postsynaptic Density Fraction by Mass Spectrometry
Walikonis, R. S., Jensen, O. N., Mann, M., Provance, D. W., Mercer, J. A., & Kennedy, M. B. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04069.2000 · Cited by 395 · see citing works
Self-citationOzeki, Y., Tomoda, T., Kleiderlein, J. J., Kamiya, A., Bord, L., Fujii, K., Okawa, M., Yamada, N., Hatten, M. E., Snyder, S. H., et al. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0136913100 · Cited by 388 · see citing works
Clement, J. P., Aceti, M., Creson, T. K., Ozkan, E. D., Shi, Y., Reish, N. J., Almonte, A. G., Miller, B. H., Wiltgen, B. J., Miller, C. A., et al. (2012) · Cell · doi:10.1016/j.cell.2012.08.045 · Cited by 385 · see citing works
Morris, J. A. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg162 · Cited by 376 · see citing works
Wenthold, R. J., Prybylowski, K., Standley, S., Sans, N., & Petralia, R. S. (2003) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.43.100901.135803 · Cited by 363 · see citing works
Ligand-Gated Ion Channel Interactions with Cytoskeletal and Signaling Proteins
Sheng, M., & Pak, D. T. S. (2000) · Annual Review of Physiology · doi:10.1146/annurev.physiol.62.1.755 · Cited by 348 · see citing works
Kinney, J. W., Davis, C. N., Tabarean, I., Conti, B., Bartfai, T., & Behrens, M. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4722-05.2006 · Cited by 329 · see citing works
Protein modules as organizers of membrane structure
Fanning, A. S., & Anderson, J. M. (1999) · Current Opinion in Cell Biology · doi:10.1016/s0955-0674(99)80062-3 · Cited by 309 · see citing works
Laminar Organization of the NMDA Receptor Complex within the Postsynaptic Density
Valtschanoff, J. G., & Weinberg, R. J. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-04-01211.2001 · Cited by 301 · see citing works
PAK and other Rho-associated kinases – effectors with surprisingly diverse mechanisms of regulation
Zhao, Z.-S., & Manser, E. (2005) · Biochemical Journal · doi:10.1042/bj20041638 · Cited by 292 · see citing works
Parnas, D., Haghighi, A. P., Fetter, R. D., Kim, S. W., & Goodman, C. S. (2001) · Neuron · doi:10.1016/s0896-6273(01)00485-8 · Cited by 291 · see citing works
Ouyang, Y., Rosenstein, A. J., Kreiman, G., Schuman, E., & Kennedy, M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-18-07823.1999 · Cited by 310 · see citing works
Self-citationTranscriptional signatures in Huntington's disease
Cha, J.-H. J. (2007) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2007.03.004 · Cited by 267 · see citing works
Defective Neurogenesis in Citron Kinase Knockout Mice by Altered Cytokinesis and Massive Apoptosis
Cunto, F. D., Imarisio, S., Hirsch, E., Broccoli, V., Bulfone, A., Migheli, A., Atzori, C., Turco, E., Triolo, R., Dotto, G. P., et al. (2000) · Neuron · doi:10.1016/s0896-6273(00)00090-8 · Cited by 252 · see citing works
Proteomics Analysis of Rat Brain Postsynaptic Density
Li, K. W., Hornshaw, M. P., van der Schors, R. C., Watson, R. B., Tate, S. A., Casetta, B., Jiménez, C. R., Gouwenberg, Y., Gundelfinger, E. D., Smalla, K., et al. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m303116200 · Cited by 246 · see citing works
Neuropathological studies of synaptic connectivity in the hippocampal formation in schizophrenia
Harrison, P. J., & Eastwood, S. L. (2001) · Hippocampus · doi:10.1002/hipo.1067 · Cited by 221 · see citing works
Physiological roles of Rho and Rho effectors in mammals
Thumkeo, D., Watanabe, S., & Narumiya, S. (2013) · European Journal of Cell Biology · doi:10.1016/j.ejcb.2013.09.002 · Cited by 215 · see citing works
SynGAP regulates spine formation
Vazquez, L. E., Chen, H.-J., Sokolova, I., Knuesel, I., & Kennedy, M. B. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.3213-04.2004 · Cited by 203 · see citing works
Self-citationYamashiro, S., Totsukawa, G., Yamakita, Y., Sasaki, Y., Madaule, P., Ishizaki, T., Narumiya, S., & Matsumura, F. (2003) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-07-0427 · Cited by 202 · see citing works
Meyer, G. R. Y. D., Varoqueaux, F., Neeb, A., Oschlies, M., & Brose, N. (2004) · Neuropharmacology · doi:10.1016/j.neuropharm.2004.06.023 · Cited by 199 · see citing works
Akama, K. T., & McEwen, B. S. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-06-02333.2003 · Cited by 197 · see citing works
Memory-specific temporal profiles of gene expression in the hippocampus
Cavallaro, S., D’Agata, V., Manickam, P., Dufour, F., & Alkon, D. L. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.242597199 · Cited by 191 · see citing works
DISC1-binding proteins in neural development, signalling and schizophrenia
Bradshaw, N. J., & Porteous, D. J. (2011) · Neuropharmacology · doi:10.1016/j.neuropharm.2010.12.027 · Cited by 188 · see citing works
Nithianantharajah, J., Barkus, C., Murphy, M., & Hannan, A. J. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.11.006 · Cited by 187 · see citing works
Xia, Z., Gray, J. A., Compton-Toth, B. A., & Roth, B. L. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301905200 · Cited by 178 · see citing works
Leonoudakis, D., Conti, L. R., Radeke, C. M., McGuire, L. M. M., & Vandenberg, C. A. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m400284200 · Cited by 177 · see citing works
Kitano, J., Kimura, K., Yamazaki, Y., Soda, T., Shigemoto, R., Nakajima, Y., & Nakanishi, S. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-04-01280.2002 · Cited by 177 · see citing works
Loi, P. K., & Tublitz, N. J. (2000) · The Journal of Comparative Neurology · doi:10.1002/(sici)1096-9861(20000515)420:4 · Cited by 38 · see citing works
β1-Adrenergic Receptor Association with PSD-95
Hu, L. A., Tang, Y., Miller, W. E., Cong, M., Lau, A. G., Lefkowitz, R. J., & Hall, R. A. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m005938200 · Cited by 166 · see citing works
Lim, I. A., Hall, D. D., & Hell, J. W. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m112339200 · Cited by 140 · see citing works
Molecular heterogeneity of central synapses: afferent and target regulation
Craig, A. M., & Boudin, H. (2001) · Nature Neuroscience · doi:10.1038/88388 · Cited by 140 · see citing works
Rao, V. L. R., Dhodda, V. K., Song, G., Bowen, K. K., & Dempsey, R. J. (2002) · Journal of Neuroscience Research · doi:10.1002/jnr.10486 · Cited by 139 · see citing works
Son, H., Yu, I. T., Hwang, S., Kim, J. S., Lee, S., Lee, Y., & Kaang, B. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.01725.x · Cited by 138 · see citing works
Ozkan, E. D., Creson, T. K., Kramár, E. A., Rojas, C., Seese, R. R., Babyan, A. H., Shi, Y., Lucero, R., Xu, X., Noebels, J. L., et al. (2014) · Neuron · doi:10.1016/j.neuron.2014.05.015 · Cited by 137 · see citing works
Xu, J., Paquet, M., Lau, A. G., Wood, J., Ross, C. A., & Hall, R. A. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m107480200 · Cited by 132 · see citing works
Linkage of schizophrenia with chromosome 1q loci in Taiwanese families
Hwu, H., Liu, C.-M., Fann, C. S. J., Ouyang, W. ‐., & Lee, S. F. ‐. (2003) · Molecular Psychiatry · doi:10.1038/sj.mp.4001235 · Cited by 129 · see citing works
PSD93 Regulates Synaptic Stability at Neuronal Cholinergic Synapses
Parker, M. J., Zhao, S., Bredt, D. S., Sanes, J. R., & Feng, G. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.3865-03.2004 · Cited by 118 · see citing works
Oh, J. S., Manzerra, P., & Kennedy, M. B. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m314109200 · Cited by 118 · see citing works
Self-citationMapping Synapses by Conjugate Light-Electron Array Tomography
Collman, F., Buchanan, J., Phend, K. D., Micheva, K. D., Weinberg, R. J., & Smith, S. J. (2015) · Journal of Neuroscience · doi:10.1523/jneurosci.4274-14.2015 · Cited by 116 · see citing works
Comabella, M., Craig, D. W., Morcillo-Suárez, C., Río, J., Navarro, A., Fernández, M., Martinꝉ, R., & Montalbán, X. (2009) · Archives of Neurology · doi:10.1001/archneurol.2009.150 · Cited by 114 · see citing works
Microtubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95
Passafaro, M., Sala, C., Niethammer, M., & Sheng, M. (1999) · Nature Neuroscience · doi:10.1038/15990 · Cited by 110 · see citing works
Koh, Y., Gramates, L., & Budnik, V. (2000) · Microscopy research and technique (Print) · doi:10.1002/(sici)1097-0029(20000401)49:1 · Cited by 120 · see citing works
Activity-Dependent Movements of Postsynaptic Scaffolds at Inhibitory Synapses
Hanus, C., Ehrensperger, M.-V., & Triller, A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.5123-05.2006 · Cited by 98 · see citing works
Kanhema, T., Dagestad, G., Panja, D., Tiron, A., Messaoudi, E., Håvik, B., Ying, S., Nairn, A. C., Sonenberg, N., & Bramham, C. R. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04158.x · Cited by 98 · see citing works
Firestein, B. L., Brenman, J. E., Aoki, C. J., Sánchez‐Pérez, A. M., El-Husseini, A., & Bredt, D. S. (1999) · Neuron · doi:10.1016/s0896-6273(00)81120-4 · Cited by 98 · see citing works
Citron, a Rho-Target, Interacts with PSD-95/SAP-90 at Glutamatergic Synapses in the Thalamus
Furuyashiki, T., Fujisawa, K., Fujita, A., Madaule, P., Uchino, S., Mishina, M., Bito, H., & Narumiya, S. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-01-00109.1999 · Cited by 98 · see citing works
Ma, X., Wang, Y., Ferraro, F., Mains, R. E., & Eipper, B. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.5283-07.2008 · Cited by 97 · see citing works
Thomas, U., Ebitsch, S., Gorczyca, M. G., Koh, Y. H., Hough, C. D., Woods, D., Gundelfinger, E. D., & Budnik, V. (2000) · Current Biology · doi:10.1016/s0960-9822(00)00696-5 · Cited by 97 · see citing works
Berryer, M. H., Chattopadhyaya, B., Xing, P., Riebe, I., Bosoi, C., Sanon, N., Antoine-Bertrand, J., Lévesque, M., Avoli, M., Hamdan, F. F., et al. (2016) · Nature Communications · doi:10.1038/ncomms13340 · Cited by 93 · see citing works
Nithianantharajah, J., & Hannan, A. J. (2012) · Neuroscience · doi:10.1016/j.neuroscience.2012.05.043 · Cited by 91 · see citing works
Aarts, M. M., & Tymianski, M. (2003) · Biochemical Pharmacology · doi:10.1016/s0006-2952(03)00297-1 · Cited by 86 · see citing works
Håvik, B., Røkke, H., Bårdsen, K., Davanger, S., & Bramham, C. R. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02712.x · Cited by 84 · see citing works
Profilin, a multi‐modal regulator of neuronal plasticity
Birbach, A. (2008) · BioEssays · doi:10.1002/bies.20822 · Cited by 84 · see citing works
DrosophilaCitron Kinase Is Required for the Final Steps of Cytokinesis
Naim, V., Imarisio, S., Cunto, F. D., Gatti, M., & Bonaccorsi, S. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-06-0536 · Cited by 83 · see citing works
A cross-species proteomic map reveals neoteny of human synapse development
Wang, L., Pang, K., Zhou, L., Cebrián-Silla, A., González-Granero, S., Wang, S., Bi, Q., White, M. L., Ho, B., Li, J., et al. (2023) · Nature · doi:10.1038/s41586-023-06542-2 · Cited by 82 · see citing works
A cross-species proteomic map reveals neoteny of human synapse development
Wang, L., Pang, K., Zhou, L., Cebrián-Silla, A., González-Granero, S., Wang, S., Bi, Q., White, M. L., Ho, B., Li, J., et al. (2022) · doi:10.1101/2022.10.24.513541 · Cited by 82 · see citing works
Regulation of proteins affecting NMDA receptor-induced excitotoxicity in a Huntington's mouse model
Jarabek, B. R. (2003) · Brain · doi:10.1093/brain/awh058 · Cited by 82 · see citing works
Farr, C. D., Gafken, P. R., Norbeck, A. D., Doneanu, C. E., Stapels, M. D., Barofsky, D. F., Minami, M., & Saugstad, J. A. (2004) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2004.02735.x · Cited by 82 · see citing works
Species-conserved SYNGAP1 phenotypes associated with neurodevelopmental disorders
Kılınç, M., Creson, T. K., Rojas, C., Aceti, M., Ellegood, J., Vaissière, T., Lerch, J. P., & Rumbaugh, G. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.03.008 · Cited by 81 · see citing works
Saro, D., Li, T., Rupasinghe, C. N., Paredes, A., Caspers, N. L., & Spaller, M. R. (2007) · Biochemistry · doi:10.1021/bi062088k · Cited by 77 · see citing works
Camera, P., Da Silva, J. S., Griffiths, G., Giuffrida, M. G., Ferrara, L., Schubert, V., Imarisio, S., Silengo, L., Dotti, C. G., & Di Cunto, F. (2003) · Nature Cell Biology · doi:10.1038/ncb1064 · Cited by 78 · see citing works
Reynaud, C., Fabre, S., & Jalinot, P. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m000465200 · Cited by 72 · see citing works
Lim, I. A., Merrill, M. A., Chen, Y., & Hell, J. W. (2003) · Neuropharmacology · doi:10.1016/s0028-3908(03)00276-4 · Cited by 72 · see citing works
Laube, G., Seidenbecher, C. I., Richter, K., Dieterich, D. C., Hoffmann, B., Landwehr, M., Smalla, K., Winter, C., Böckers, T. M., Wolf, G. L., et al. (2002) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2001.1078 · Cited by 72 · see citing works
Muhia, M., Yee, B. K., Feldon, J., Markopoulos, F., & Knuesel, I. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07079.x · Cited by 71 · see citing works
SYNGAP1 mutations: Clinical, genetic, and pathophysiological features
Agarwal, M., Johnston, M. V., & Stafstrom, C. E. (2019) · International Journal of Developmental Neuroscience · doi:10.1016/j.ijdevneu.2019.08.003 · Cited by 72 · see citing works
Ying, Z., Bingaman, W. E., & Najm, I. (2004) · Epilepsia · doi:10.1111/j.0013-9580.2004.37703.x · Cited by 70 · see citing works
Regulation of dendritic spine stability
Smart, F. M., & Halpain, S. (2000) · Hippocampus · doi:10.1002/1098-1063(2000)10:5 · Cited by 93 · see citing works
Sarkisian, M. R., Li, W., Cunto, F. D., D’Mello, S. R., & LoTurco, J. J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-08-j0001.2002 · Cited by 68 · see citing works
Tight Junctions and the Intestinal Barrier
Ma, T. Y., Anderson, J. M., & Turner, J. R. (2012) · Elsevier eBooks · doi:10.1016/b978-0-12-382026-6.00038-5 · Cited by 67 · see citing works
Sema4C, a Transmembrane Semaphorin, Interacts with a Post-synaptic Density Protein, PSD-95
Inagaki, S., Ohoka, Y., Sugimoto, H., Fujioka, S., Amazaki, M., Kurinami, H., Miyazaki, N., Tohyama, M., & Furuyama, T. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m009051200 · Cited by 63 · see citing works
Molecular constituents and phosphorylation‐dependent regulation of the post‐synaptic density
Yamauchi, T. (2002) · Mass Spectrometry Reviews · doi:10.1002/mas.10033 · Cited by 63 · see citing works
Cytoskeletal Links of Neuronal Acetylcholine Receptors Containing α7 Subunits
Shoop, R. D., Yamada, N., & Berg, D. K. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-11-04021.2000 · Cited by 62 · see citing works
Furusawa, T., Ikawa, S., Yanai, N., & Obinata, M. (2000) · Biochemical and Biophysical Research Communications · doi:10.1006/bbrc.2000.2377 · Cited by 62 · see citing works
Berto, G. E., Camera, P., Fusco, C., Imarisio, S., Ambrogio, C., Chiarle, R., Silengo, L., & Cunto, F. D. (2007) · Journal of Cell Science · doi:10.1242/jcs.000703 · Cited by 60 · see citing works
Structure and molecular organization of dendritic spines.
Tashiro, A., & Yuste, R. (2003) · PubMed · doi:10.14670/hh-18.617 · Cited by 60 · see citing works
Mao, W., Watanabe, T., Cho, S., Frost, J. L., Truong, T., Zhao, X., & Futai, K. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.12877 · Cited by 59 · see citing works
Insights into the regulation of 5-HT2A serotonin receptors by scaffolding proteins and kinases
Allen, J., Yadav, P. N., & Roth, B. L. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.048 · Cited by 59 · see citing works
Jeon, S., Kim, S., Park, J., Suh, P., Kim, Y. S., Bae, C., & Park, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m110380200 · Cited by 55 · see citing works
Citron Kinase, a RhoA Effector, Enhances HIV‐1 Virion Production by Modulating Exocytosis
Loomis, R. J., Holmes, D. A., Elms, A. R., Solski, P. A., Der, C. J., & Su, L. (2006) · Traffic · doi:10.1111/j.1600-0854.2006.00503.x · Cited by 55 · see citing works
Citron, a Rho target that affects contractility during cytokinesis
Madaule, P., Furuyashiki, T., Eda, M., Bito, H., Ishizaki, T., & Narumiya, S. (2000) · Microscopy Research and Technique · doi:10.1002/(sici)1097-0029(20000415)49:2 · Cited by 55 · see citing works
Mi, R., Tang, X., Sutter, R., Xu, D., Worley, P. F., & O’Brien, R. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-17-07606.2002 · Cited by 55 · see citing works
Citron Kinase Is a Cell Cycle-dependent, Nuclear Protein Required for G2/M Transition of Hepatocytes
Liu, H., Cunto, F. D., Imarisio, S., & Reid, L. M. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m210391200 · Cited by 54 · see citing works
Two Conserved Residues Govern the Salt and pH Dependencies of the Binding Reaction of a PDZ Domain
Celestine, N., Engström, Å., Gianni, S., Larsson, M., & Jemth, P. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m607883200 · Cited by 54 · see citing works
A role for synGAP in regulating neuronal apoptosis
Knuesel, I., Elliott, A., Chen, H., Mansuy, I. M., & Kennedy, M. B. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03908.x · Cited by 54 · see citing works
Self-citationActivation of Rho GTPases by synaptic transmission in the hippocampus
O'Kane, E. M., Stone, T. W., & MORRIS, B. J. (2003) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2003.02102.x · Cited by 50 · see citing works
Building and remodeling synapses
Benson, D. L., & Huntley, G. W. (2010) · Hippocampus · doi:10.1002/hipo.20872 · Cited by 48 · see citing works
Milner, T. A., Shah, P., & Pierce, J. P. (2000) · Synapse · doi:10.1002/(sici)1098-2396(20000601)36:3 · Cited by 60 · see citing works
Analyses of the spatiotemporal expression and subcellular localization of liprin‐α proteins
Zürner, M., Mittelstaedt, T., Dieck, S. T., Becker, A. J., & Schoch, S. (2011) · The Journal of Comparative Neurology · doi:10.1002/cne.22664 · Cited by 47 · see citing works
- Authors
- Zhang, W., Vazquez, L., Apperson, M., & Kennedy, M. B.
- Affiliations
- California Institute of Technology (US)
- ORCID
- Kennedy, Mary B.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 1999-01-01
- Volume
- 19
- Issue
- 1
- Pages
- 96-108
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6782379
- OpenAlex
- W2111810014
- Cited by
- 190
- References
- 60
- Citations by year
- 2026: 1 · 2025: 5 · 2024: 5 · 2023: 2 · 2022: 2 · 2021: 2 · 2020: 3 · 2019: 5 · 2018: 4 · 2017: 3 · 2016: 4 · 2015: 4 · 2014: 3 · 2013: 2 · 2012: 3
- FWCI
- 7.36
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- CaltechAUTHORS (California Institute of Technology) (submittedVersion, cc-by-nc-sa)
- Funders
- National Science Foundation (9023446)
- U.S. Public Health Service
- National Institute of Neurological Disorders and Stroke (R01NS028710, NS28710)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Kinase Regulation and GTPase Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- citron, PSD-95, PDZ domain, glutamatergic synapses, GABAergic neurons, hippocampus, Rho GTPases, SynGAP, CaM kinase II, thalamic neurons, synaptic protein localization
- MeSH terms
- Amino Acid Sequence, Brain Chemistry, Cells, Cultured, gamma-Aminobutyric Acid, Hippocampus, Molecular Sequence Data, Nerve Tissue Proteins, Neural Inhibition, Neurons, Protein Binding, Proteins, Synapses, Signal Transduction, Sequence Homology, Amino Acid, Glutamic Acid
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