LTP requires postsynaptic PDZ-domain interactions with glutamate receptor/auxiliary protein complexes
Open accessAbstract
Long-term potentiation (LTP) is a persistent strengthening of synaptic transmission in the brain and is arguably the most compelling cellular and molecular model for learning and memory. Previous work found that both AMPA receptors and exogenously expressed kainate receptors are equally capable of expressing LTP, despite their limited homology and their association with distinct auxiliary subunits, indicating that LTP is far more promiscuous than previously thought. What might these two subtypes of glutamate receptor have in common? Using a single-cell molecular replacement strategy, we demonstrate that the AMPA receptor auxiliary subunit TARP γ-8, via its PDZ-binding motif, is indispensable for both basal synaptic transmission and LTP. Remarkably, kainate receptors and their auxiliary subunits Neto proteins share the same requirement of PDZ-binding domains for synaptic trafficking and LTP. Together, these results suggest that a minimal postsynaptic requirement for LTP is the PDZ binding of glutamate receptors/auxiliary subunits to PSD scaffolding proteins.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Phosphomimic mutations of TARP serines greatly diminish both binding of the TARP CTD to PSD-95 and rescue of AMPAR transmission in AMPAR-deleted cells.
“Phosphomimic mutations greatly diminished both the binding of the TARP CTD to PSD-95 and the rescue of AMPAR transmission in AMPAR-deleted cells.”
From Synaptic memory and CaMKII (2023) · cites this paper as [288]
The Results and Significance passages report that deleting TARP γ-8’s PDZ-binding motif prevented rescue of synaptic currents in AMPAR-deleted cells; a separate passage says phosphor-null mutations did not fully rescue basal transmission. Neither passage reports the claimed effect of phosphomimic serine mutations, and the PSD-95 binding experiment described in our copy concerns GluK1/Neto1 rather than the TARP CTD. No page numbers are provided in our copy. (LLM, conf=0.82)
Experimental — accuracy not yet measuredAlanine substitutions of critical serines in the TARP CTD reduce AMPAR EPSCs but do not affect the magnitude of LTP.
“Furthermore, alanine substitutions of the critical serines in the TARP CTD, although reducing AMPAR EPSCs, do not affect the magnitude of LTP (288).”
From Synaptic memory and CaMKII (2023) · cites this paper as [288]
The passage supplied under Significance (page not given) reports that phosphor-null mutations in tethered TARP γ-8 did not fully rescue basal synaptic transmission, while LTP was normal. This supports the direction of both effects, but the paper's finding is limited to tethered γ-8 with homomeric GluA1 receptors; the passage does not identify the substitutions as alanine, and it cautions that phosphorylation might matter for heteromeric AMPARs. (LLM, conf=0.82)
Experimental — accuracy not yet measuredTARPs stabilize AMPARs both on the cell surface and at synapses, and loss of TARPs results in decreased AMPAR expression, suggesting TARPless AMPARs become unstable.
“TARPs have been shown to stabilize AMPARs both on the cell surface and at synapses (Bats et al., 2007, Sheng et al., 2018), and loss of TARPs results in decreased AMPAR expression, suggesting that “TARPless” AMPARs become unstable (Fukaya et al., 2006, Chen et al., 2000).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Sheng et al., 2018
The Discussion reports that the PDZ ligand of TARP γ-8 is essential for moving surface AMPARs to synapses, supporting the synaptic part of the claim. The Results report equal surface AMPAR currents with intact γ-8 and a PDZ-motif-deficient mutant; the paper does not establish that TARPs stabilize AMPARs on the cell surface. The decreased-expression and instability clause is attributed to other citations, not Sheng et al. (LLM, conf=0.86)
Experimental — accuracy not yet measuredPhosphorylation of the TARP C-terminus reduces interaction with membrane lipids and facilitates interaction with PSD95, serving to trap the TARP/AMPAR complex with the PSD.
“Phosphorylation reduces the interaction with membrane lipids and facilitates interaction with PSD95, serving to trap the TARP/AMPAR complex with the PSD (Opazo et al., 2012, Bats et al., 2007, Sheng et al., 2018).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Sheng et al., 2018
The Discussion (page not available) proposes that PSD-95 can capture AMPAR/TARP complexes through their PDZ ligands, supporting the trapping portion of the claim. It does not say that phosphorylation of the TARP C-terminus reduces membrane-lipid binding or facilitates PSD-95 binding; the phosphorylation described in that model is of synGAP. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
AMPA receptor trafficking at excitatory synapses
Bredt, D. S., & Nicoll, R. A. (2003) · Neuron · doi:10.1016/s0896-6273(03)00640-8 · Cited by 1,150 · see citing works
Self-citationStargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms
Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000) · Nature · doi:10.1038/35050030 · Cited by 1,111 · see citing works
Self-citationReceptor trafficking and synaptic plasticity
Collingridge, G. L., Isaac, J. T. R., & Wang, Y. T. (2004) · Nature Reviews Neuroscience · doi:10.1038/nrn1556 · Cited by 1,046 · see citing works
AMPARs and Synaptic Plasticity: The Last 25 Years
Huganir, R. L., & Nicoll, R. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.10.025 · Cited by 968 · see citing works
Self-citationA Brief History of Long-Term Potentiation
Nicoll, R. A. (2017) · Neuron · doi:10.1016/j.neuron.2016.12.015 · Cited by 841 · see citing works
Self-citationDirect interactions between PSD-95 and stargazin control synaptic AMPA receptor number
Schnell, E., Sizemore, M., Karimzadegan, S., Chen, L., Bredt, D. S., & Nicoll, R. A. (2002) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.172511199 · Cited by 691 · see citing works
Self-citationSubunit Composition of Synaptic AMPA Receptors Revealed by a Single-Cell Genetic Approach
Lu, W., Shi, Y., Jackson, A. C., Bjorgan, K., During, M. J., Sprengel, R., Seeburg, P. H., & Nicoll, R. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.02.027 · Cited by 660 · see citing works
Self-citationTomita, S., Chen, L., Kawasaki, Y., Petralia, R. S., Wenthold, R. J., Nicoll, R. A., & Bredt, D. S. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200212116 · Cited by 535 · see citing works
Self-citationAMPA Receptor Incorporation into Synapses during LTP: The Role of Lateral Movement and Exocytosis
Makino, H., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.08.035 · Cited by 501 · see citing works
Stargazin modulates AMPA receptor gating and trafficking by distinct domains
Tomita, S., Adesnik, H., Sekiguchi, M., Zhang, W., Wada, K., Howe, J. R., Nicoll, R. A., & Bredt, D. S. (2005) · Nature · doi:10.1038/nature03624 · Cited by 486 · see citing works
Self-citationLong-Term Potentiation: From CaMKII to AMPA Receptor Trafficking
Herring, B. E., & Nicoll, R. A. (2016) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021014-071753 · Cited by 425 · see citing works
Self-citationJackson, A. C., & Nicoll, R. A. (2011) · Neuron · doi:10.1016/j.neuron.2011.04.007 · Cited by 410 · see citing works
Self-citationStructural and Functional Architecture of AMPA-Type Glutamate Receptors and Their Auxiliary Proteins
Greger, I. H., Watson, J. F., & Cull-Candy, S. G. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.009 · Cited by 392 · see citing works
Bidirectional Synaptic Plasticity Regulated by Phosphorylation of Stargazin-like TARPs
Tomita, S., Stein, V., Stocker, T. J., Nicoll, R. A., & Bredt, D. S. (2005) · Neuron · doi:10.1016/j.neuron.2005.01.009 · Cited by 343 · see citing works
Self-citationHippocampal LTP and contextual learning require surface diffusion of AMPA receptors
Penn, A. C., Zhang, C. L., Georges, F., Royer, L., Breillat, C., Hosy, E., Petersen, J. D., Humeau, Y., & Choquet, D. (2017) · Nature · doi:10.1038/nature23658 · Cited by 324 · see citing works
LTP requires a reserve pool of glutamate receptors independent of subunit type
Granger, A. J., Shi, Y., Lu, W., Cerpas, M., & Nicoll, R. A. (2013) · Nature · doi:10.1038/nature11775 · Cited by 313 · see citing works
Self-citationTARP γ-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity
Rouach, N., Byrd, K., Petralia, R. S., Elias, G. M., Adesnik, H., Tomita, S., Karimzadegan, S., Kealey, C. P., Bredt, D. S., & Nicoll, R. A. (2005) · Nature Neuroscience · doi:10.1038/nn1551 · Cited by 280 · see citing works
Self-citationAraki, Y., Zeng, M., Zhang, M., & Huganir, R. L. (2015) · Neuron · doi:10.1016/j.neuron.2014.12.023 · Cited by 271 · see citing works
Patterson, M. A., Szatmari, E. M., & Yasuda, R. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0913875107 · Cited by 259 · see citing works
SAP90 Binds and Clusters Kainate Receptors Causing Incomplete Desensitization
Garcia, E. P., Mehta, S., Blair, L. A. C., Wells, D. G., Shang, J., Fukushima, T., Fallon, J. R., Garner, C. C., & Marshall, J. J. (1998) · Neuron · doi:10.1016/s0896-6273(00)80590-5 · Cited by 254 · see citing works
Regulation of AMPA receptor surface diffusion by PSD-95 slots
Opazo, P., Sainlos, M., & Choquet, D. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.10.010 · Cited by 234 · see citing works
Elias, G. M., Elias, L. A. B., Apostolides, P. F., Kriegstein, A. R., & Nicoll, R. A. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811025106 · Cited by 223 · see citing works
Self-citationPostsynaptic signaling during plasticity of dendritic spines
Murakoshi, H., & Yasuda, R. (2012) · Trends in Neurosciences · doi:10.1016/j.tins.2011.12.002 · Cited by 158 · see citing works
The Postsynaptic Density: There Is More than Meets the Eye
Dosemeci, A., Weinberg, R. J., Reese, T. S., & Tao-Cheng, J.-H. (2016) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2016.00023 · Cited by 138 · see citing works
The Stoichiometry of AMPA Receptors and TARPs Varies by Neuronal Cell Type
Shi, Y. S., Lü, W., Milstein, A. D., & Nicoll, R. A. (2009) · Neuron · doi:10.1016/j.neuron.2009.05.016 · Cited by 123 · see citing works
Self-citationCaMKII Phosphorylation of TARPγ-8 Is a Mediator of LTP and Learning and Memory
Park, J., Chávez, A. E., Mineur, Y. S., Morimoto-Tomita, M., Lutzu, S., Kim, K. S., Picciotto, M. R., Castillo, P. E., & Tomita, S. (2016) · Neuron · doi:10.1016/j.neuron.2016.09.002 · Cited by 121 · see citing works
Straub, C., & Tomita, S. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.09.005 · Cited by 119 · see citing works
Spatial diversity in gene expression for VDCCγ subunit family in developing and adult mouse brains
Fukaya, M., Yamazaki, M., Sakimura, K., & Watanabe, M. (2005) · Neuroscience Research · doi:10.1016/j.neures.2005.08.009 · Cited by 110 · see citing works
Dancing partners at the synapse: auxiliary subunits that shape kainate receptor function
Copits, B. A., & Swanson, G. T. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3335 · Cited by 97 · see citing works
CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses
Bemben, M. A., Shipman, S. L., Hirai, T., Herring, B. E., Li, Y., Badger, J. D., Nicoll, R. A., Diamond, J. S., & Roche, K. W. (2013) · Nature Neuroscience · doi:10.1038/nn.3601 · Cited by 95 · see citing works
Self-citationSubunit-specific role for the amino-terminal domain of AMPA receptors in synaptic targeting
Díaz-Alonso, J., Sun, Y. J., Granger, A. J., Levy, J. M., Blankenship, S. M., & Nicoll, R. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707472114 · Cited by 89 · see citing works
Self-citationWalkup, W. G., Mastro, T. L., Schenker, L. T., Vielmetter, J., Hu, R., Iancu, A., Reghunathan, M., Bannon, B. D., & Kennedy, M. B. (2016) · eLife · doi:10.7554/elife.16813 · Cited by 76 · see citing works
TARP Redundancy Is Critical for Maintaining AMPA Receptor Function
Menuz, K., O'Brien, J. L., Karmizadegan, S., Bredt, D. S., & Nicoll, R. A. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.1319-08.2008 · Cited by 71 · see citing works
Self-citationPDZ binding of TARPγ-8 controls synaptic transmission but not synaptic plasticity
Sumioka, A., Brown, T. E., Kato, A. S., Bredt, D. S., Kauer, J. A., & Tomita, S. (2011) · Nature Neuroscience · doi:10.1038/nn.2952 · Cited by 68 · see citing works
SynGAP moves out of the core of the postsynaptic density upon depolarization
Yang, Y., Tao-Cheng, J.-H., Reese, T. S., & Döṣemeci, A. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.06.061 · Cited by 57 · see citing works
Milstein, A. D., & Nicoll, R. A. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0905570106 · Cited by 51 · see citing works
Self-citationSheng, N., Shi, Y. S., Lomash, R. M., Roche, K. W., & Nicoll, R. A. (2015) · eLife · doi:10.7554/elife.11682 · Cited by 41 · see citing works
Self-citationCritical role for TARPs in early development despite broad functional redundancy
Menuz, K., Kerchner, G. A., O'Brien, J. L., & Nicoll, R. A. (2008) · Neuropharmacology · doi:10.1016/j.neuropharm.2008.06.037 · Cited by 32 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
The AMPA Receptor Code of Synaptic Plasticity
Diering, G. H., & Huganir, R. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.018 · Cited by 844 · see citing works
Structure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
CaMKII: a central molecular organizer of synaptic plasticity, learning and memory
Yasuda, R., Hayashi, Y., & Hell, J. W. (2022) · Nature Reviews Neuroscience · doi:10.1038/s41583-022-00624-2 · Cited by 431 · see citing works
Yang, S., & Chang, M. C. (2019) · International Journal of Molecular Sciences · doi:10.3390/ijms20133130 · Cited by 410 · see citing works
Substance P and pain chronicity
Zieglgänsberger, W. (2018) · Cell and Tissue Research · doi:10.1007/s00441-018-2922-y · Cited by 283 · see citing works
Phase Separation-Mediated TARP/MAGUK Complex Condensation and AMPA Receptor Synaptic Transmission
Zeng, M., Díaz-Alonso, J., Ye, F., Chen, X., Xu, J., Ji, Z., Nicoll, R. A., & Zhang, M. (2019) · Neuron · doi:10.1016/j.neuron.2019.08.001 · Cited by 171 · see citing works
Self-citationMolecular Mechanisms of Early and Late LTP
Baltaci, S. B., Mogulkoc, R., & Baltaci, A. K. (2019) · Neurochemical Research · doi:10.1007/s11064-018-2695-4 · Cited by 152 · see citing works
Choquet, D. (2018) · The Journal of Neuroscience · doi:10.1523/jneurosci.2119-18.2018 · Cited by 141 · see citing works
AMPA receptor structure and auxiliary subunits
Kamalova, A., & Nakagawa, T. (2020) · The Journal of Physiology · doi:10.1113/jp278701 · Cited by 139 · see citing works
Nicoll, R. A., & Schulman, H. (2023) · Physiological Reviews · doi:10.1152/physrev.00034.2022 · Cited by 126 · see citing works
“Furthermore, alanine substitutions of the critical serines in the TARP CTD, although reducing AMPAR EPSCs, do not affect the magnitude of LTP (288).”
BackgroundSelf-citationAMPA receptors and their minions: auxiliary proteins in AMPA receptor trafficking
Bissen, D., Foss, F., & Acker-Palmer, A. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03068-7 · Cited by 92 · see citing works
LTP induction by structural rather than enzymatic functions of CaMKII
Tullis, J. E., Larsen, M. E., Rumian, N. L., Freund, R. K., Boxer, E. E., Brown, C. N., Coultrap, S. J., Schulman, H., Aoto, J., Dell’Acqua, M. L., et al. (2023) · Nature · doi:10.1038/s41586-023-06465-y · Cited by 112 · see citing works
Ca 2+ ‐permeable AMPA receptors and their auxiliary subunits in synaptic plasticity and disease
Cull-Candy, S. G., & Farrant, M. (2021) · The Journal of Physiology · doi:10.1113/jp279029 · Cited by 99 · see citing works
Visualizing synaptic plasticity in vivo by large-scale imaging of endogenous AMPA receptors
Graves, A. R., Roth, R. H., Tan, H. L., Zhu, Q., Bygrave, A. M., Lopez-Ortega, E., Hong, I., Spiegel, A. C., Johnson, R. C., Vogelstein, J. T., et al. (2021) · eLife · doi:10.7554/elife.66809 · Cited by 84 · see citing works
PSD-95: An Effective Target for Stroke Therapy Using Neuroprotective Peptides
Ugalde‐Triviño, L., & Díaz‐Guerra, M. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222212585 · Cited by 83 · see citing works
Buonarati, O. R., Hammes, E. A., Watson, J. F., Greger, I. H., & Hell, J. W. (2019) · Science Signaling · doi:10.1126/scisignal.aar6889 · Cited by 81 · see citing works
Patriarchi, T., Buonarati, O. R., & Hell, J. W. (2018) · The EMBO Journal · doi:10.15252/embj.201899771 · Cited by 65 · see citing works
Qu, W., Yuan, B., Li, R., Liu, Q., Zhang, X., Cui, R., Yang, W., & Li, B. (2020) · Cell Proliferation · doi:10.1111/cpr.12959 · Cited by 64 · see citing works
AMPA receptor trafficking and LTP: Carboxy-termini, amino-termini and TARPs
Díaz-Alonso, J., & Nicoll, R. A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108710 · Cited by 66 · see citing works
Self-citationLetellier, M., Szíber, Z., Chamma, I., Saphy, C., Papasideri, I., Tessier, B., Sainlos, M., Czöndör, K., & Thoumine, O. R. (2018) · Nature Communications · doi:10.1038/s41467-018-06220-2 · Cited by 58 · see citing works
A revised view of the role of CaMKII in learning and memory
Bayer, K. U., & Giese, K.-P. (2024) · Nature Neuroscience · doi:10.1038/s41593-024-01809-x · Cited by 50 · see citing works
AMPA receptor anchoring at CA1 synapses is determined by N-terminal domain and TARP γ8 interactions
Watson, J. F., Pinggera, A., Ho, H., & Greger, I. H. (2021) · Nature Communications · doi:10.1038/s41467-021-25281-4 · Cited by 38 · see citing works
Jacobi, E., & von Engelhardt, J. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.008 · Cited by 37 · see citing works
Long-term potentiation is independent of the C-tail of the GluA1 AMPA receptor subunit
Díaz-Alonso, J., Morishita, W., Incontro, S., Simms, J., Holtzman, J., Gill, M., Mucke, L., Malenka, R. C., & Nicoll, R. A. (2020) · eLife · doi:10.7554/elife.58042 · Cited by 37 · see citing works
Self-citationIntramolecular domain dynamics regulate synaptic MAGUK protein interactions
Rademacher, N., Kuropka, B., Kunde, S., Wahl, M. C., Freund, C., & Shoichet, S. A. (2019) · eLife · doi:10.7554/elife.41299 · Cited by 34 · see citing works
RNF220 is an E3 ubiquitin ligase for AMPA receptors to regulate synaptic transmission
Ma, P., Wan, L. P., Li, Y., He, C.-H., Song, N., Zhao, S., Wang, H., Ding, Y., Mao, B., & Sheng, N. (2022) · Science Advances · doi:10.1126/sciadv.abq4736 · Cited by 31 · see citing works
Self-citationMahaman, Y. A. R., Huang, F., Salissou, M. T. M., Yacouba, M. B. M., Wang, J., Liu, R., Zhang, B., Li, H., Zhu, F., & Wang, X. (2023) · Neurotherapeutics · doi:10.1007/s13311-023-01356-6 · Cited by 33 · see citing works
The role of AMPAR lateral diffusion in memory
Choquet, D., & Opazo, P. (2022) · Seminars in Cell & Developmental Biology · doi:10.1016/j.semcdb.2022.01.009 · Cited by 31 · see citing works
Mahaman, Y. A. R., Feng, J., Huang, F., Salissou, M. T. M., Wang, J., Liu, R., Zhang, B., Li, H., Zhu, F., & Wang, X. (2022) · Nutrients · doi:10.3390/nu14204284 · Cited by 31 · see citing works
Tuning synaptic strength by regulation of AMPA glutamate receptor localization
Stockwell, I., Watson, J. F., & Greger, I. H. (2024) · BioEssays · doi:10.1002/bies.202400006 · Cited by 25 · see citing works
Biology of AMPA receptor interacting proteins - From biogenesis to synaptic plasticity
Matthews, P. M., Pinggera, A., Kampjut, D., & Greger, I. H. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108709 · Cited by 25 · see citing works
Long-term potentiation reconstituted with an artificial TARP/PSD-95 complex
Ravi, A. S., Zeng, M., Chen, X., Sandoval, G., Diaz-Alonso, J., Zhang, M., & Nicoll, R. A. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111483 · Cited by 25 · see citing works
Self-citationNitric oxide signaling in ctenophores
Moroz, L. L., Mukherjee, K., & Romanova, D. Y. (2023) · Frontiers in Neuroscience · doi:10.3389/fnins.2023.1125433 · Cited by 25 · see citing works
LTP expression mediated by autonomous activity of GluN2B-bound CaMKII
Rumian, N. L., Barker, C. M., Larsen, M. E., Tullis, J. E., Freund, R. K., Taslimi, A., Coultrap, S. J., Tucker, C. L., Dell’Acqua, M. L., & Bayer, K. U. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114866 · Cited by 20 · see citing works
Amer, A., & Martin, J. H. (2022) · Brain stimulation · doi:10.1016/j.brs.2022.07.005 · Cited by 20 · see citing works
The schizophrenia-associated missense variant rs13107325 regulates dendritic spine density
Li, S., Ma, C., Li, Y., Chen, R., Liu, Y., Wan, L. P., Xiong, Q., Wang, C., Huo, Y., Dang, X., et al. (2022) · Translational Psychiatry · doi:10.1038/s41398-022-02137-z · Cited by 20 · see citing works
Self-citationPeng, S.-X., Wang, Y., Zhang, M., Zang, Y., Wu, D., Pei, J., Li, Y., Dai, J., Guo, X., Luο, X., et al. (2021) · Scientific Reports · doi:10.1038/s41598-021-91415-9 · Cited by 18 · see citing works
Self-citationActivity-dependent diffusion trapping of AMPA receptors as a key step for expression of early LTP
Nowacka, A., Getz, A. M., Bessa‐Neto, D., & Choquet, D. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0220 · Cited by 19 · see citing works
Neto-α Controls Synapse Organization and Homeostasis at the Drosophila Neuromuscular Junction
Han, T. H., Vicidomini, R., Ramos, C. I., Wang, Q., Nguyen, P., Jarník, M., Lee, C., Stawarski, M., Hernandez, R. X., Macleod, G. T., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107866 · Cited by 17 · see citing works
Belfiore, M., Cariati, I., Matteucci, A., Gaddini, L., Macchia, G., Fioravanti, R., Frank, C., Tancredi, V., D’Arcangelo, G., & Diociaiuti, M. (2019) · Scientific Reports · doi:10.1038/s41598-019-41462-0 · Cited by 17 · see citing works
Mechanisms underlying the synaptic trafficking of the glutamate delta receptor GluD1
Tao, W., Ma, C., Bemben, M. A., Li, K. H., Burlingame, A. L., Zhang, M., & Nicoll, R. A. (2019) · Molecular Psychiatry · doi:10.1038/s41380-019-0378-4 · Cited by 16 · see citing works
Self-citationMolecular mechanisms of AMPAR reversible stabilization at synapses
Bessa‐Neto, D., & Choquet, D. (2023) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2023.103856 · Cited by 12 · see citing works
Choquet, D., Opazo, P., & Zhang, H. (2025) · Translational Neurodegeneration · doi:10.1186/s40035-025-00470-z · Cited by 11 · see citing works
Jiang, L., Zhang, H., He, Y., Liu, H., Li, S., Chen, R., Han, S., Zhou, Y., Zhang, J., Wan, X., et al. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.109076 · Cited by 11 · see citing works
Endocytosis of AMPA receptors: Role in neurological conditions
Bencsik, N., Morales, C. O. O., Haußer, A., & Schlett, K. (2022) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2022.09.007 · Cited by 9 · see citing works
The emerging role of kainate receptor functional dysregulation in pain
Li, H., Li, J., Guan, Y., & Wang, Y. (2021) · Molecular Pain · doi:10.1177/1744806921990944 · Cited by 8 · see citing works
The Effects of P75NTR on Learning Memory Mediated by Hippocampal Apoptosis and Synaptic Plasticity
Tang, J., Feng, S., Chen, X., Huang, H., Mao, M., Wang, H., Li, S., Lu, X., & Wang, Y. (2020) · Current Pharmaceutical Design · doi:10.2174/1381612826666200916145142 · Cited by 8 · see citing works
Wei, M., Wang, M., Wang, J., Su, F., Wang, Y., Sun, M., Wang, S., Liu, M., Wang, H., Lu, M., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00829 · Cited by 7 · see citing works
The many faces of the AMPA-type ionotropic glutamate receptor
Bowie, D. (2022) · Neuropharmacology · doi:10.1016/j.neuropharm.2022.108975 · Cited by 7 · see citing works
Chemogenetic regulation of the TARP-lipid interaction mimics LTP and reversibly modifies behavior
Park, J., Berthoux, C., Hoyos, E., Shan, L., Morimoto‐Tomita, M., Wang, Y., Castillo, P. E., & Tomita, S. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112826 · Cited by 4 · see citing works
Hippocampal place code plasticity in CA1 requires postsynaptic membrane fusion
Plitt, M. H., Kaganovsky, K., Say, E., Sosa, M., Südhof, T. C., & Giocomo, L. M. (2026) · Neuron · doi:10.1016/j.neuron.2026.03.006 · Cited by 4 · see citing works
Pinggera, A., Watson, J. F., & Greger, I. H. (2020) · Encyclopedia of Life Sciences · doi:10.1002/9780470015902.a0029223 · Cited by 4 · see citing works
A High-content Assay for Monitoring AMPA Receptor Trafficking
Ghane, M. A., Yakout, D. W., & Mabb, A. M. (2019) · Journal of Visualized Experiments · doi:10.3791/59048 · Cited by 3 · see citing works
Gaia, F. F. P., Dal-Pizzol, H. R., Malafaia, O., Roesler, R., & Isolan, G. R. (2026) · Cancers · doi:10.3390/cancers18101646 · Cited by 3 · see citing works
Kunde, S., Schmerl, B., von Sivers, J., Ahmadyar, E., Gupta, T., Rademacher, N., Zieger, H. L., & Shoichet, S. A. (2024) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2024.107263 · Cited by 2 · see citing works
Leana-Sandoval, G., Kolli, A. V., Sandoval, M. A., Saavedra, E., Li, K. H., Chen, L. Y., Burlingame, A. L., Ramírez‐Franco, J., & Díaz-Alonso, J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.12.02.626379 · Cited by 2 · see citing works
Self-citationGuo, R., Xue, J., Shao, P., Cai, C., & Wang, Y. (2023) · Neuroscience Letters · doi:10.1016/j.neulet.2023.137430 · Cited by 1 · see citing works
Synaptic Plasticity Linked to Ionotropic Glutamate Receptors After Nicotine Exposure
Kazmi, A., & Choe, E. S. (2025) · Current Neuropharmacology · doi:10.2174/011570159x365159250311142852 · Cited by 1 · see citing works
From Synapses to Circuits, the Role of KIBRA and the WWC Family in Adaptive Brain Function
Volk, L. J. (2026) · Journal of Neurochemistry · doi:10.1111/jnc.70514 · Cited by 1 · see citing works
A High-content Assay for Monitoring AMPA Receptor Trafficking
Ghane, M. A., Yakout, D. W., & Mabb, A. M. (2019) · Journal of Visualized Experiments · doi:10.3791/59048-v · Cited by 1 · see citing works
CaMKII mechanisms in plasticity, learning and memory: Approaches and concepts
Bayer, K. U., Brown, C. N., & Giese, K.-P. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00057-2
Transport intracellulaire des récepteurs AMPA et régulation par leurs protéines associées
Bonnet, C. (2021) · theses.fr (ABES) · doi:10.70675/a51a45f6zee8cz4c6az85a5z8b01dfd87159
From biogenesis to synaptic organization : developing tools to study AMPAR-associated proteins
Bessa‐Neto, D. (2021) · theses.fr (ABES) · doi:10.70675/a68a26edzb1c6z414ez927czebc71c64fb29
Leana-Sandoval, G., Sandoval, M. A., Kolli, A. V., Saavedra, E., Li, K. H., Burlingame, A. L., Ramírez‐Franco, J., & Díaz-Alonso, J. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107553
Self-citationQianqiong, Q., Feng, B., 任南新, Jiyao, Q., Tian, J., Changtong, M., Guoan, S., Zucai, X., Changyin, Y., & Zhang, H. (2026) · Neurobiology of Disease · doi:10.1016/j.nbd.2026.107646
- Authors
- Sheng, N., Bemben, M. A., Díaz-Alonso, J., Tao, W., Shi, Y. S., & Nicoll, R. A.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2018-03-26
- Volume
- 115
- Issue
- 15
- Pages
- 3948-3953
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5899490
- OpenAlex
- W2843061105
- Cited by
- 65
- References
- 39
- Citations by year
- 2026: 5 · 2025: 2 · 2024: 7 · 2023: 7 · 2022: 10 · 2021: 11 · 2020: 7 · 2019: 9 · 2018: 7
- FWCI
- 3.87
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- the Strategy Priority Research Program of the Chinese Academy of Sciences (XDB13000000)
- National Natural Science Foundation of China (31741055, 31371061, 31571060)
- the Chinese Academy of Sciences Pioneer Hundred Talents Program (N/A)
- Ministry of Science and Technology of the People's Republic of China (2014CB942804, 2015BAI08B02)
- Natural Science Foundation of Jiangsu Province Grant (BK20140018)
- HHS | NIH | National Institute of Mental Health (R01MH080379, R01MH070957, R56MH070957)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- long-term potentiation, PDZ domain, AMPA receptors, kainate receptors, postsynaptic scaffolding proteins, synaptic transmission, learning and memory
- MeSH terms
- Animals, Humans, Protein Binding, Synapses, Calcium Channels, Long-Term Potentiation, Receptors, AMPA, Kainic Acid Receptors, Receptors, Kainic Acid, PDZ Domains
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
