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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) 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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Cites
The Rat Brain in Stereotaxic Coordinates
Paxinos, G., & Watson, C. (1983) · Elsevier eBooks · doi:10.1016/c2009-0-63235-9 · Cited by 28,585
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
Rho GTPases and the Actin Cytoskeleton
Hall, A. (1998) · Science · doi:10.1126/science.279.5350.509 · Cited by 6,138
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 4,514
Interneurons of the hippocampus
Freund, T. F., & Buzsáki, G. (1998) · Hippocampus · doi:10.1002/(sici)1098-1063(1996)6:4 · Cited by 3,478
Brewer, G. J., Torricelli, J. R., Evege, E. K., & Price, P. J. (1993) · Journal of Neuroscience Research · doi:10.1002/jnr.490350513 · Cited by 2,325
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 1,916
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
Cho, K.-O., Hunt, C. A., & Kennedy, M. B. (1992) · Neuron · doi:10.1016/0896-6273(92)90245-9 · Cited by 1,188
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
Kim, E., Niethammer, M., Rothschild, A., Jan, Y. N., & Sheng, M. (1995) · Nature · doi:10.1038/378085a0 · Cited by 1,003
Woods, D. F., & Bryant, P. J. (1991) · Cell · doi:10.1016/0092-8674(81)90009-x · Cited by 898
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 887
Niethammer, M., Kim, E., & Sheng, M. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-07-02157.1996 · Cited by 750
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
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 722
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
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
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
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
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
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 554
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
The postsynaptic density at glutamatergic synapses
Kennedy, M. B. (1997) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)01033-8 · Cited by 475
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
McGlade‐McCulloh, E., Yamamoto, H., Tan, S.-E., Brickey, D. A., & Soderling, T. R. (1993) · Nature · doi:10.1038/362640a0 · Cited by 456
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
SAP102, a Novel Postsynaptic Protein That Interacts with NMDA Receptor Complexes In Vivo
Müller, B. M., Kistner, U., Kindler, S., Chung, W. J., Kuhlendahl, S., Fenster, S. D., Lau, L., Veh, R. W., Huganir, R. L., Gundelfinger, E. D., et al. (1996) · Neuron · doi:10.1016/s0896-6273(00)80157-9 · Cited by 424
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
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
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
Rao, A., Kim, E., Sheng, M., & Craig, A. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01217.1998 · Cited by 399
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
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 351
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
Hunt, C., Schenker, L. J., & Kennedy, M. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-04-01380.1996 · Cited by 313
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 312
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
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
Chevesich, J., Kreuz, A. J., & Montell, C. (1997) · Neuron · doi:10.1016/s0896-6273(01)80049-0 · Cited by 290
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
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
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
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
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
The absence of a major Ca 2+ 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
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
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 178
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
Apperson, M., Moon, I. S., & Kennedy, M. B. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-21-06839.1996 · Cited by 166
Self-citationBenson, 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
Isoform 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
Jones, E. G., Huntley, G. W., & Benson, D. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-02-00611.1994 · Cited by 145
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
Kennedy, M. B. (1993) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(93)90145-o · Cited by 136
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
Molloy, S. S., & Kennedy, M. B. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.11.4756 · Cited by 133
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
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
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
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Metadata
- 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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