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Glutamate-induced transient modification of the postsynaptic density
Open accessAbstract
Depolarization of rat hippocampal neurons with a high concentration of external potassium induces a thickening of postsynaptic densities (PSDs) within 1.5-3 min. After high-potassium treatment, PSDs thicken 2.1-fold in cultured neurons and 1.4-fold in hippocampal slices compared with their respective controls. Thin-section immunoelectron microscopy of hippocampal cultures indicates that at least part of the observed thickening of PSDs can be accounted for by an accumulation of Ca(2+)/calmodulin-dependent protein kinase II (CaMKII) on their cytoplasmic faces. Indeed, PSD-associated gold label for CaMKII increases 5-fold after depolarization with potassium. The effects of high-potassium treatment on the composition and structure of the PSDs are mimicked by direct application of glutamate. In cultures, glutamate-induced thickening of PSDs and the accumulation of CaMKII on PSDs are reversed within 5 min of removal of glutamate and Ca(2+) from the extracellular medium. These results suggest that PSDs are dynamic structures whose thickness and composition are subject to rapid and transient changes during synaptic activity.
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“activation of CaMKII results in the rapid translocation of CaMKII to the PSD (137, 140, 169, 216–220).”
From Synaptic memory and CaMKII (2023) · cites this paper as [137]
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“Glutamate treatment of neuronal cultures causes CaMKII clustering at excitatory synapses (136–140).”
From Synaptic memory and CaMKII (2023) · cites this paper as [137]
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Heavy chain of cytoplasmic dynein is a major component of the postsynaptic density fraction
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MethodTao-Cheng, J.-H., Azzam, R. N., Crocker, V. T., Winters, C. A., & Reese, T. S. (2015) · eNeuro · doi:10.1523/eneuro.0066-15.2015 · Cited by 18
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“…electron microscopy to study the effect of tPA on the postsynaptic density (PSD), an electron-dense structure attached to the post-synaptic terminal that undergoes rapid changes in molecular composition, structure, and function in response to variations in synaptic activity (Dosemeci et al., 2001).”
Cold‐induced exodus of postsynaptic proteins from dendritic spines
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“…(Carlin et al., 1982), between the PSD samples isolated from brain tissues with and without being subjected to electrical or chemical stimulation (Dosemeci et al., 2001; Ehlers, 2003; Shulman, 2004) and between the PSD samples isolated from the brains of control rats and those isolated from the…”
BackgroundHsieh, M.-Y., Tuan, L., Chang, H., Wang, Y., Chen, C., Shy, H.-T., Lee, L., & Gau, S. S. (2022) · Cerebral Cortex · doi:10.1093/cercor/bhac379 · Cited by 15
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Farley, M. M., Swulius, M. T., & Waxham, M. N. (2015) · Neuroscience · doi:10.1016/j.neuroscience.2015.07.062 · Cited by 14
“In support of this concept, the composition and structure of the PSD change in an activity-dependent manner (Dosemeci et al., 2001, Ehlers, 2003, Tao-Cheng et al., 2010, Yang et al., 2011) and through development (Harris et al., 1992, Petralia et al., 2005, Swulius et al., 2010, Swulius et al.,…”
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“After neuronal depolarization a thicker layer of CaMKII, which includes clusters, accumulates on the cytoplasmic surfaces of PSDs (Dosemeci et al., 2001).”
BackgroundInfluentialSelf-citationKnockdown of CLC-3 in the hippocampal CA1 impairs contextual fear memory
Chen, Y.-F., Chen, Z.-X., Wang, R., Shi, Y., Li, X., Wang, X., & Zhao, H. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2018.07.004 · Cited by 12
Ca MKII ‐mediated displacement of AIDA ‐1 out of the postsynaptic density core
Döṣemeci, A., Toy, D., Burch, A. M., Bayer, K. U., & Tao-Cheng, J.-H. (2016) · FEBS Letters · doi:10.1002/1873-3468.12334 · Cited by 11
Self-citationActivation of NMDA receptors thickens the postsynaptic density via proteolysis
Fukunaga, Y., Nakajima, E., Hatano, E., Itoh, S., Kashino, Y., & Miyazawa, A. (2015) · Neuroscience Research · doi:10.1016/j.neures.2015.07.003 · Cited by 10
“…known about the intracellular mechanisms underlying the ultrastructural changes in the PSD. Activation of glutamate receptors evoked by application of glutamate or NMDA in vitro mimics PSD thickening in ischemic neurons in vivo and in in vitro models of brain ischemia (Dosemeci et al., 2001, 2002).”
BackgroundAnalysis of organelles within the nervous system: impact on brain and organelle functions
Tribl, F., Meyer, H. E., & Marcus, K. (2008) · Expert Review of Proteomics · doi:10.1586/14789450.5.2.333 · Cited by 11
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“CaMKII, a Ca2+-regulated protein kinase, is a major component of the PSD and accumulates at the PSD under excitatory conditions [8].”
Self-citationPósfai, B., Cserép, C., Hegedüs, P., Szabadits, E., Otte, D. M., Zimmer, A., Watanabe, M., Freund, T. F., & Nyíri, G. (2016) · Translational Psychiatry · doi:10.1038/tp.2016.74 · Cited by 9
Direct investigation of charge transfer in neurons by electrostatic force microscopy
Zhao, W., Cui, W., Xu, S., Wang, Y. Y., Zhang, K., Wang, D., Cheong, L., Besenbacher, F., & Shen, C. (2018) · Ultramicroscopy · doi:10.1016/j.ultramic.2018.09.015 · Cited by 8
NCK1 Modulates Neuronal Actin Dynamics and Promotes Dendritic Spine, Synapse, and Memory Formation
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“This characteristic is of particular importance given that changes in the size and composition of the PSD are associated with stable changes in synaptic strength [22,23].”
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Tao-Cheng, J.-H. (2014) · Elsevier eBooks · doi:10.1016/b978-0-12-418675-0.00011-0 · Cited by 8
Self-citationModification of the synaptic cleft under excitatory conditions
Tao-Cheng, J.-H., Moreira, S. L., Winters, C. A., Reese, T. S., & Döṣemeci, A. (2023) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2023.1239098 · Cited by 7
“Most images (including depolarization with high K+, NMDA, and EGTA experiments) were from previously published reports (Dosemeci et al., 2001; Tao-Cheng, 2006, 2020; Tao-Cheng et al., 2006, 2016) and reexamined here for structural changes of the synaptic cleft.”
Self-citationAIDA-1 Moves out of the Postsynaptic Density Core under Excitatory Conditions
Döṣemeci, A., Toy, D., Reese, T. S., & Tao-Cheng, J.-H. (2015) · PLoS ONE · doi:10.1371/journal.pone.0137216 · Cited by 7
“Under excitatory conditions, more CaMKII, Shank and CYLD accumulate within the deeper zone of the PSD, contiguous to the electron dense core [10], [11], [12], while another abundant PSD protein, SynGAP, moves out of the PSD core [13].”
BackgroundSelf-citationRubio, F. J., Olivares, D. E., Dunn, C., Zhang, S., Hilaire, E., Henry, A., Mejías-Aponte, C. A., Nogueras‐Ortiz, C. J., Selvam, P. V., Cruz, F. C., et al. (2023) · Journal of Neuroscience · doi:10.1523/jneurosci.0927-22.2023 · Cited by 7
Long-Term Memory, Neurogenesis, and Signal Novelty
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“PSD is composed of various cells and components, and its composition and thickness can be dynamically modified.(40) The PSD thickness is closely relevant to synaptic transmission and plasticity, which, therefore, is an important indicator of its function in learning and memory.”
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“We reported the phenomenon of PSD thickening, which was caused by translocation of CaMKII into PSDs. 18 It was later shown that PSD thickening occurs not only under pathological conditions such as ischemia, as we suggested initially, but also occurs under near physiological conditions upon synaptic activation or poten…”
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Altered parabrachial nucleus nociceptive processing may underlie central pain in Parkinson’s disease
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Molecular Properties and Cell Biology of the NMDA Receptor
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“Studies using transfection of wild type and mutant NMDAR subunits Activity-dependent calcium influx induces autophosphorylation of Ca/ calmodulin-dependent protein kinase II (CaMKII), leading to its increased localization at the postsynaptic density (67, 299).”
Miranda-Riestra, A., Cercós, M. G., Trueta, C., Oikawa‐Sala, J., Argueta, J., Constantino-Jonapa, L. A., Cruz‐Garduño, R., Benítez‐King, G., & Estrada‐Reyes, R. (2024) · Molecular Pharmacology · doi:10.1124/molpharm.124.000890 · Cited by 4
Visualizing the Ultrastructures and Dynamics of Synapses by Single-Molecule Nanoscopy
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Assembling microtubules disintegrate the postsynaptic density in vitro
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Postsynaptic Targeting of Protein Kinases and Phosphatases
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CaMKII: Mechanisms of a Prototypical Memory Model
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The Role of the Postsynaptic Density and the Spine Cytoskeleton in Synaptic Plasticity
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Dendritic spine neck plasticity controls synaptic expression of long-term potentiationPreprint
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“Here, 540 kPSDB Phos is always greater than kspine Phos , as CaMKII preferentially binds PSD95 [85,86] and are frequently 541”
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CaMKII: A Master Functional and Structural Molecule in Synaptic Plasticity and Memory
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Proteomic Analysis of the Postsynaptic Density
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“Following recovery, excitatory conditions can, once again, elicit thickening of the PSD ( Dosemeci et al., 2001 ).”
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CaMKIIα holoenzymes self-organize into chain-like mesoscale clusters
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“It is plausible that the chain-like or “grape-like” clusters identified here serve as the initial nuclei that subsequently fuse and propagate into the macroscopic organizations reported in earlier protein studies ( 35 , 36 ) and isolated PSDs ( 62 , 63 ).”
Thomas, C. I., Anderson, J. R., Alexis, A., Guerrero‐Given, D., Chavez, A., McNabb, M. C., Ünal, B., Ehlers, M., Bolton, M. M., & Kamasawa, N. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.11.07.566075 · Cited by 1
Optical analysis of synaptic plasticity in rat hippocampus
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“Soon after, using immunogold labeling with antibody against CaMKII, Reese and his colleagues showed that exposure of cultured hippocampal neurons to high K+ resulted in 5-fold increase of PSD-associated CaMKII and 1.7-fold increase after glutamate/glycine treatment (Dosemeci et al., 2001).”
MethodInfluentialDevelopmental Changes in the Structure and Composition of the Postsynaptic Density
Swulius, M. T. (2010) · Digital Commons-TMC (Texas Medical Center)
Synapse Loss, Synaptic Plasticity and the Postsynaptic Density
Sheng, M. (2008) · Springer eBooks · doi:10.1007/978-3-540-76330-7_4
“many hours, particularly by protein degradation via the ubiquitin-proteasome system (UPS; Ehlers 2003; Pak and Sheng 2003) and translocation of specific proteins (e.g., CaMKIIα and AMPARs) to and away from the PSD ( Dosemeci et al. 2001; Hu et al, 1998; Inoue and Okabe 2003; Malinow and Malenka 2002).”
BackgroundRoles of CaMKII in Learning and Memory ☆
Stephenson, J. R., & Colbran, R. J. (2017) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.21106-1
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Podor, B. (2017) · DalSpace (Dalhousie University)
Heuser, J. E. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.04.22.489201
Concerted remodelling of the postsynaptic spine and RNA granule by cLTPPreprint
Mendoza, M. B., Yahya, G., Alomoto, K., Soria-Villalba, A., Aldea, M., & Gallego, C. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.07.16.665171
“In cultured hippocampal neurons, the postsynaptic pallium becomes more electron-dense after depolarisation with KCl or treatment with glutamate, likely due to the accumulation and redistribution of postsynaptic proteins 12 .”
Tao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062118
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062133
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062124
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062109
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062142
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062094
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062100
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062160
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062115
Self-citationTao-Cheng, J.-H. (2020) · Figshare · doi:10.6084/m9.figshare.12062148
Self-citationThe Scrib1 Interactome and its relevance for synaptic plasticity & neurodevelopmental disorders
Pinheiro, V. L. M. (2014) · theses.fr (ABES) · doi:10.70675/b1c2e418zac9cz44c5zb050z72f9b6a47586
Pathophysiological consequences of a Fragile X missense mutation
Garcia, M. P. (2020) · theses.fr (ABES) · doi:10.70675/b8e86263z5926z4a83zbaf6z0f61bf2d15f9
Triggering hippocampal LTP and learning by dopamine : a teaching signal
Sayegh, F. J. P. (2022) · theses.fr (ABES) · doi:10.70675/70062eccz03ecz44b6z8916zb715dcb4edff
Metadata
- Authors
- Dosemeci, A., Tao-Cheng, J.-H., Vinade, L., Winters, C. A., Pozzo-Miller, L., & Reese, T. S.
- Affiliations
- Marine Biological Laboratories, Woods Hole, MA 02543; Laboratory of Neurobiology, Electron Microscopy Facility, National Institute of Neurological Disorders and Stroke, National Institutes of Health, Bethesda, MD 20892; and Department of Neurobiology, University of Alabama, Birmingham, AL 35294
- National Institutes of Health (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-08-21
- Volume
- 98
- Issue
- 18
- Pages
- 10428-10432
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC56977
- OpenAlex
- W2131475149
- Cited by
- 184
- References
- 24
- Citations by year
- 2026: 2 · 2025: 4 · 2024: 4 · 2023: 7 · 2022: 6 · 2021: 3 · 2020: 18 · 2019: 4 · 2018: 8 · 2017: 6 · 2016: 13 · 2015: 7 · 2014: 6 · 2013: 5 · 2012: 5
- FWCI
- 3.33
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (9817317)
- National Institutes of Health
- 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 › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Keywords
- postsynaptic density, glutamate, CaMKII, hippocampal neurons, depolarization, high potassium, synaptic plasticity, calcium/calmodulin-dependent protein kinase, calcium signaling
- MeSH terms
- Animals, Cells, Cultured, Hippocampus, Nerve Tissue Proteins, Neurons, Potassium, Microscopy, Immunoelectron, Calcium-Calmodulin-Dependent Protein Kinases, Glutamic Acid, Rats, Calcium-Calmodulin-Dependent Protein Kinase Type 2
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