Synaptic plasticity through activation of GluA3-containing AMPA-receptors
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Excitatory synaptic transmission is mediated by AMPA-type glutamate receptors (AMPARs). In CA1 pyramidal neurons of the hippocampus two types of AMPARs predominate: those that contain subunits GluA1 and GluA2 (GluA1/2), and those that contain GluA2 and GluA3 (GluA2/3). Whereas subunits GluA1 and GluA2 have been extensively studied, the contribution of GluA3 to synapse physiology has remained unclear. Here we show in mice that GluA2/3s are in a low-conductance state under basal conditions, and although present at synapses they contribute little to synaptic currents. When intracellular cyclic AMP (cAMP) levels rise, GluA2/3 channels shift to a high-conductance state, leading to synaptic potentiation. This cAMP-driven synaptic potentiation requires the activation of both protein kinase A (PKA) and the GTPase Ras, and is induced upon the activation of β-adrenergic receptors. Together, these experiments reveal a novel type of plasticity at CA1 hippocampal synapses that is expressed by the activation of GluA3-containing AMPARs.
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GluA3-containing receptors are mostly inert under basal conditions due to a very low open probability, although they are robustly targeted to synapses.
“Here it was shown GluA3 containing receptors are mostly inert under basal conditions due to a very low-open probability, although these receptors are robustly targeted to synapses (Renner et al., 2017).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Renner et al., 2017
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A simple method for organotypic cultures of nervous tissue
Stoppini, L., Buchs, P., & Muller, D. (1991) · Journal of Neuroscience Methods · doi:10.1016/0165-0270(91)90128-m · Cited by 3,097 · see citing works
Shi, S.-H., Hayashi, Y., Esteban, J. A., & Malinow, R. (2001) · Cell · doi:10.1016/s0092-8674(01)00321-x · Cited by 1,094 · see citing works
Synaptic AMPA receptor plasticity and behavior
Kessels, H. W., & Malinow, R. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.015 · Cited by 993 · see citing works
Self-citationTuning arousal with optogenetic modulation of locus coeruleus neurons
Carter, M. E., Yizhar, O., Chikahisa, S., Nguyen, H., Adamantidis, A., Nishino, S., Deisseroth, K., & de Lecea, L. (2010) · Nature Neuroscience · doi:10.1038/nn.2682 · Cited by 993 · 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
PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity
Esteban, J. A., Shi, S.-H., Wilson, C., Nuriya, M., Huganir, R. L., & Malinow, R. (2003) · Nature Neuroscience · doi:10.1038/nn997 · Cited by 894 · see citing works
Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons
Wenthold, R., Petralia, R., Blahos J, II, & Niedzielski, A. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-06-01982.1996 · Cited by 850 · see citing works
The Tetrameric Structure of a Glutamate Receptor Channel
Rosenmund, C., Stern-Bach, Y., & Stevens, C. F. (1998) · Science · doi:10.1126/science.280.5369.1596 · Cited by 794 · see citing works
Importance of AMPA Receptors for Hippocampal Synaptic Plasticity But Not for Spatial Learning
Zamanillo, D., Sprengel, R., Hvalby, Ø., Jensen, V., Burnashev, N., Rozov, A., Kaiser, K. M. M., Köster, H. J., Borchardt, T., Worley, P., et al. (1999) · Science · doi:10.1126/science.284.5421.1805 · Cited by 791 · see citing works
Postsynaptic receptor trafficking underlying a form of associative learning
Rumpel, S., LeDoux, J., Zador, A., & Malinow, R. (2005) · Science · doi:10.1126/science.1103944 · Cited by 775 · see citing works
Ras and Rap control AMPA receptor trafficking during synaptic plasticity
Zhu, J. J., Qin, Y., Zhao, M., Van Aelst, L., & Malinow, R. (2002) · Cell · doi:10.1016/s0092-8674(02)00897-8 · Cited by 769 · see citing works
A novel Epac-specific cAMP analogue demonstrates independent regulation of Rap1 and ERK
Enserink, J. M., Christensen, A. E., de Rooij, J., van Triest, M. H., Schwede, F., Genieser, H., Døskeland, S. O., Blank, J. L., & Bos, J. L. (2002) · Nature Cell Biology · doi:10.1038/ncb874 · Cited by 704 · see citing works
Subunit 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
Silent synapses and the emergence of a postsynaptic mechanism for LTP
Kerchner, G. A., & Nicoll, R. A. (2008) · Nature reviews. Neuroscience · doi:10.1038/nrn2501 · Cited by 602 · see citing works
Regulation of AMPA receptor trafficking and synaptic plasticity
Anggono, V., & Huganir, R. L. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.006 · Cited by 588 · see citing works
AMPA 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
Emotion Enhances Learning via Norepinephrine Regulation of AMPA-Receptor Trafficking
Hu, H., Real, E., Takamiya, K., Kang, M.-G., Ledoux, J., Huganir, R. L., & Malinow, R. (2007) · Cell · doi:10.1016/j.cell.2007.09.017 · Cited by 496 · see citing works
Epac: Defining a New Mechanism for cAMP Action
Gloerich, M., & Bos, J. L. (2010) · The Annual Review of Pharmacology and Toxicology · doi:10.1146/annurev.pharmtox.010909.105714 · Cited by 476 · see citing works
Nanoscale Scaffolding Domains within the Postsynaptic Density Concentrate Synaptic AMPA Receptors
MacGillavry, H. D., Song, Y., Raghavachari, S., & Blanpied, T. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.03.009 · Cited by 442 · see citing works
Liang, K., Juler, R. G., & McGaugh, J. L. (1986) · Brain Research · doi:10.1016/0006-8993(86)91049-8 · Cited by 392 · 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
Man, H.-Y., Sekine-Aizawa, Y., & Huganir, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611698104 · Cited by 311 · see citing works
Regional Diversity and Developmental Dynamics of the AMPA-Receptor Proteome in the Mammalian Brain
Schwenk, J., Baehrens, D., Haupt, A., Bildl, W., Boudkkazi, S., Roeper, J., Fakler, B., & Schulte, U. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.044 · Cited by 270 · see citing works
SynGAP regulates synaptic strength and mitogen-activated protein kinases in cultured neurons
Rumbaugh, G., Adams, J. P., Kim, J. H., & Huganir, R. L. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0600084103 · Cited by 260 · see citing works
Synaptic transmission and plasticity in the absence of AMPA glutamate receptor GluR2 and GluR3
Meng, Y., Zhang, Y., & Jia, Z. (2003) · Neuron · doi:10.1016/s0896-6273(03)00368-4 · Cited by 251 · see citing works
Compartmentalized versus Global Synaptic Plasticity on Dendrites Controlled by Experience
Makino, H., & Malinow, R. (2011) · Neuron · doi:10.1016/j.neuron.2011.09.036 · Cited by 219 · see citing works
Contextual learning requires synaptic AMPA receptor delivery in the hippocampus
Mitsushima, D., Ishihara, K., Sano, A., Kessels, H. W. H. G., & Takahashi, T. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1104558108 · Cited by 163 · see citing works
Self-citationMechanism and treatment for learning and memory deficits in mouse models of Noonan syndrome
Lee, Y., Ehninger, D., Zhou, M., Oh, J.-Y., Kang, M., Kwak, C., Ryu, H.-H., Butz, D. H., Araki, T., Cai, Y., et al. (2014) · Nature Neuroscience · doi:10.1038/nn.3863 · Cited by 150 · see citing works
COUNTING CHANNELS: A TUTORIAL GUIDE ON ION CHANNEL FLUCTUATION ANALYSIS
Alvarez, O. A., Gonzalez, C. L., & Latorre, R. (2002) · AJP Advances in Physiology Education · doi:10.1152/advan.00006.2002 · Cited by 149 · see citing works
Humeau, Y., Reisel, D., Johnson, A. W., Borchardt, T., Jensen, V., Gebhardt, C., Bosch, V., Gass, P., Bannerman, D. M., Good, M. A., et al. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.2603-07.2007 · Cited by 147 · see citing works
Involvement of the AMPA Receptor GluR-C Subunit in Alcohol-Seeking Behavior and Relapse
Sanchis‐Segura, C., Borchardt, T., Vengeliene, V., Zghoul, T., Bachteler, D., Gass, P., Sprengel, R., & Spanagel, R. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4237-05.2006 · Cited by 143 · see citing works
Amyloid-β effects on synapses and memory require AMPA receptor subunit GluA3
Reinders, N. R., Pao, Y., Renner, M., Matos, C. D. S., Lodder, T. R., Malinow, R., & Kessels, H. W. H. G. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1614249113 · Cited by 126 · see citing works
Self-citationAKAP-Lbc enhances cyclic AMP control of the ERK1/2 cascade
Smith, F. D., Langeberg, L. K., Cellurale, C., Pawson, T. J., Morrison, D. K., Davis, R. J., & Scott, J. D. (2010) · Nature Cell Biology · doi:10.1038/ncb2130 · Cited by 123 · see citing works
Structure and organization of heteromeric AMPA-type glutamate receptors
Herguedas, B., García‐Nafría, J., Cais, O., Fernández-Leiro, R., Krieger, J., Ho, H., & Greger, I. H. (2016) · Science · doi:10.1126/science.aad3873 · Cited by 121 · see citing works
Synaptic transmission and plasticity require AMPA receptor anchoring via its N-terminal domain
Watson, J. F., Ho, H., & Greger, I. H. (2017) · eLife · doi:10.7554/elife.23024 · Cited by 117 · see citing works
Impaired Regulation of Synaptic Strength in Hippocampal Neurons from GluR1‐Deficient Mice
Andrásfalvy, B. K., Smith, M. A., Borchardt, T., Sprengel, R., & Magee, J. C. (2003) · The Journal of Physiology · doi:10.1113/jphysiol.2003.045575 · Cited by 112 · see citing works
Gutierrez-Castellanos, N., Da Silva-Matos, C. M., Zhou, K., Canto, C. B., Renner, M. C., Koene, L. M. C., Ozyildirim, O., Sprengel, R., Kessels, H. W., & De Zeeuw, C. I. (2017) · Neuron · doi:10.1016/j.neuron.2016.11.046 · Cited by 111 · see citing works
Self-citationFasano, S., D'Antoni, A., Orban, P. C., Valjent, E., Putignano, E., Vara, H., Pizzorusso, T., Giustetto, M., Yoon, B.-J., Soloway, P. D., et al. (2009) · Biological Psychiatry · doi:10.1016/j.biopsych.2009.03.014 · Cited by 107 · see citing works
Tangential synaptic distribution of NMDA and AMPA receptors in rat neocortex
Kharazia, V. N., & Weinberg, R. J. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00846-x · Cited by 104 · see citing works
Modulation of synaptic efficacy in field CA1 of the rat hippocampus by forskolin
Chavez-Noriega, L. E., & Stevens, C. F. (1992) · Brain Research · doi:10.1016/0006-8993(92)90803-h · Cited by 103 · see citing works
Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1
Kim, C., Takamiya, K., Petralia, R. S., Sattler, R., Yu, S., Zhou, W., Kalb, R. G., Wenthold, R. J., & Huganir, R. L. (2005) · Nature Neuroscience · doi:10.1038/nn1432 · Cited by 103 · see citing works
Quantitative analysis of AMPA receptor subunit composition in addiction-related brain regions
Reimers, J. M., Milovanovic, M., & Wolf, M. E. (2010) · Brain Research · doi:10.1016/j.brainres.2010.10.016 · Cited by 101 · see citing works
Assembly of a β2‐adrenergic receptor—GluR1 signalling complex for localized cAMP signalling
Joiner, M.-L. A., Lisé, M.-F., Yuen, E. Y., Kam, A. Y. F., Zhang, M., Hall, D. D., Malik, Z. A., Qian, H., Chen, Y., Ulrich, J. D., et al. (2009) · The EMBO Journal · doi:10.1038/emboj.2009.344 · Cited by 101 · see citing works
Cell Type-specific Regulation of B-Raf Kinase by cAMP and 14-3-3 Proteins
Qiu, W., Zhuang, S., von Lintig, F. C., Boss, G. R., & Pilz, R. B. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m003327200 · Cited by 101 · see citing works
Gelinas, J. N., Banko, J. L., Peters, M. M., Klann, E., Weeber, E. J., & Nguyen, P. (2008) · Learning & Memory · doi:10.1101/lm.830008 · Cited by 100 · see citing works
Roles of stargazin and phosphorylation in the control of AMPA receptor subcellular distribution
Kessels, H. W. H. G., Kopec, C. D., Klein, M. E., & Malinow, R. (2009) · Nature Neuroscience · doi:10.1038/nn.2340 · Cited by 96 · see citing works
Self-citationSynaptic AMPA Receptor Exchange Maintains Bidirectional Plasticity
McCormack, S. G., Stornetta, R. L., & Zhu, J. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.027 · Cited by 92 · see citing works
Effects of PKA and PKC on Miniature Excitatory Postsynaptic Currents in CA1 Pyramidal Cells
Carroll, R. C., Nicoll, R. A., & Malenka, R. C. (1998) · Journal of Neurophysiology · doi:10.1152/jn.1998.80.5.2797 · Cited by 90 · see citing works
Epac mediates PACAP‐dependent long‐term depression in the hippocampus
Ster, J., de Bock, F., Bertaso, F., Abitbol, K., Daniel, H., Bockaert, J., & Fagni, L. (2008) · The Journal of Physiology · doi:10.1113/jphysiol.2008.157461 · Cited by 86 · see citing works
Adamczyk, A. L., Mejı́as, R., Takamiya, K., Yocum, J., Krasnova, I. N., Calderón, J. F., Cadet, J. L., Huganir, R. L., Pletnikov, M. V., & Wang, T. (2012) · Behavioural Brain Research · doi:10.1016/j.bbr.2012.01.007 · Cited by 85 · see citing works
β2-Adrenergic receptor supports prolonged theta tetanus-induced LTP
Qian, H., Matt, L., Zhang, M., Nguyen, M., Patriarchi, T., Koval, O. M., Anderson, M. E., He, K., Lee, H., & Hell, J. W. (2012) · Journal of Neurophysiology · doi:10.1152/jn.00374.2011 · Cited by 82 · see citing works
Absolute quantification of AMPA receptor subunit mRNAs in single hippocampal neurons
Tsuzuki, K., Lambolez, B., Rossier, J., & Ozawa, S. (2001) · Journal of Neurochemistry · doi:10.1046/j.1471-4159.2001.00388.x · Cited by 80 · see citing works
Hartveit, E., & Veruki, M. L. (2007) · Nature Protocols · doi:10.1038/nprot.2007.47 · Cited by 68 · see citing works
Norepinephrine Stimulated Increase of Cyclic AMP Levels in Developing Mouse Brain Cell Cultures
Seeds, N. W., & Gilman, A. G. (1971) · Science · doi:10.1126/science.174.4006.292 · Cited by 65 · see citing works
Dynamics and allosteric potential of the AMPA receptor N‐terminal domain
Sukumaran, M., Rossmann, M., Shrivastava, I. H., Dutta, A., Bahar, İ., & Greger, I. H. (2011) · The EMBO Journal · doi:10.1038/emboj.2011.17 · Cited by 56 · see citing works
cAMP cascade leads to Ras activation in cortical neurons
Ambrosini, A., Tininini, S., Barassi, A., Racagni, G., Sturani, E., & Zippel, R. (2000) · Molecular Brain Research · doi:10.1016/s0169-328x(99)00294-6 · Cited by 56 · see citing works
Shinohara, Y. (2009) · Frontiers in Neuroanatomy · doi:10.3389/neuro.05.010.2009 · Cited by 51 · see citing works
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Bruss, M. D., Richter, W., Horner, K., Jin, S.-L. C., & Conti, M. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m803306200 · Cited by 49 · see citing works
A necessary role for GluR1 serine 831 phosphorylation in appetitive incentive learning
Crombag, H. S., Sutton, J. M., Takamiya, K., Lee, H., Holland, P. C., Gallagher, M., & Huganir, R. L. (2008) · Behavioural Brain Research · doi:10.1016/j.bbr.2008.03.026 · Cited by 45 · see citing works
Frey, M. C., Sprengel, R., & Nevian, T. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5314-08.2009 · Cited by 42 · see citing works
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Jacob, A., & Weinberg, R. J. (2014) · Hippocampus · doi:10.1002/hipo.22404 · Cited by 40 · see citing works
Li, Y., Dillon, T. J., Takahashi, M., Earley, K. T., & Stork, P. A. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.730978 · Cited by 40 · see citing works
Baillie, G. S., & Houslay, M. D. (2005) · Biochemical Society Transactions · doi:10.1042/bst20051333 · Cited by 40 · see citing works
The mode of action of Y13‐259 scFv fragment intracellularly expressed in mammalian cells
Cardinale, A., Lener, M., Messina, S., Cattaneo, A., & Biocca, S. (1998) · FEBS Letters · doi:10.1016/s0014-5793(98)01369-6 · Cited by 40 · see citing works
A robust automated method to analyze rodent motion during fear conditioning
Kopec, C. D., Kessels, H. W. H. G., Bush, D. E. A., Cain, C. K., LeDoux, J. E., & Malinow, R. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.028 · Cited by 39 · see citing works
Self-citationGluR3 subunit regulates sleep, breathing and seizure generation
Steenland, H. W., Kim, S. S., & Zhuo, M. (2008) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2008.06078.x · Cited by 39 · see citing works
Gebhardt, C., & Cull-Candy, S. G. (2006) · The Journal of Physiology · doi:10.1113/jphysiol.2005.102723 · Cited by 35 · see citing works
Houslay, M. D., & Baillie, G. S. (2005) · Biochemical Society Transactions · doi:10.1042/bst0331333 · Cited by 31 · see citing works
Chay, A., Zamparo, I., Koschinski, A., Zaccolo, M., & Blackwell, K. T. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004735 · Cited by 28 · see citing works
Postsynaptic Mechanisms Are Essential for Forskolin-Induced Potentiation of Synaptic Transmission
Соколова, И. В., Lester, H. A., & Davidson, N. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00617.2005 · Cited by 26 · see citing works
Li, Y., Takahashi, M., & Stork, P. A. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.463067 · Cited by 26 · see citing works
García-Hernández, S., Abe, M., Sakimura, K., & Rubio, M. E. (2016) · Hearing Research · doi:10.1016/j.heares.2016.12.006 · Cited by 23 · see citing works
Aggregation Limits Surface Expression of Homomeric GluA3 Receptors
Coleman, S. K., Hou, Y., Willibald, M., Semenov, A., Möykkynen, T. P., & KEINÄNEN, K. P. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m115.689125 · Cited by 17 · see citing works
Breese, C. R., Logel, J., Adams, C. E., & Leonard, S. S. (1996) · Journal of Molecular Neuroscience · doi:10.1007/bf02737065 · Cited by 15 · see citing works
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Kita, K., Albergaria, C., Machado, A. S., Carey, M. R., Müller, M., & Delvendahl, I. (2021) · eLife · doi:10.7554/elife.65152 · Cited by 20 · see citing works
GluA3-containing AMPA receptors: From physiology to synaptic dysfunction in brain disorders
Italia, M., Ferrari, E. S., Luca, M. D., & Gardoni, F. (2021) · Neurobiology of Disease · doi:10.1016/j.nbd.2021.105539 · Cited by 33 · see citing works
The role of post-translational modifications in synaptic AMPA receptor activity
Corti, E., & Duarte, C. B. (2023) · Biochemical Society Transactions · doi:10.1042/bst20220827 · Cited by 23 · see citing works
Peter, S., Urbanus, B. H. A., Klaassen, R. V., Wu, B., Boele, H., Azizi, S., Slotman, J. A., Houtsmuller, A. B., Schonewille, M., Hoebeek, F. E., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.03.079 · Cited by 24 · see citing works
AMPA Receptors: A Key Piece in the Puzzle of Memory Retrieval
Pereyra, M., & Medina, J. H. (2021) · Frontiers in Human Neuroscience · doi:10.3389/fnhum.2021.729051 · Cited by 21 · see citing works
Lee, J. Y., Krieger, J., Herguedas, B., García‐Nafría, J., Dutta, A., Shaikh, S. A., Greger, I. H., & Bahar, İ. (2018) · Structure · doi:10.1016/j.str.2018.10.017 · Cited by 21 · see citing works
Argyrousi, E. K., Heckman, P. R. A., van Hagen, B. T. J., Muysers, H., van Goethem, N. P., & Prickaerts, J. (2019) · Journal of Psychopharmacology · doi:10.1177/0269881119885262 · Cited by 21 · see citing works
Wang, K., Xu, F., Campbell, S., Hart, K. D., Durham, T. A., Maylie, J., & Xu, J. (2019) · The FASEB Journal · doi:10.1096/fj.201902217r · Cited by 20 · see citing works
van der Spek, S. J. F., Pandya, N. J., Koopmans, F., Paliukhovich, I., van der Schors, R. C., Otten, M., Smit, A. B., & Li, K. W. (2022) · Cells · doi:10.3390/cells11223648 · Cited by 20 · see citing works
Blackwood, C. A., McCoy, M. T., Ladenheim, B., & Cadet, J. L. (2021) · Scientific Reports · doi:10.1038/s41598-021-82206-3 · Cited by 20 · see citing works
Experience Recruits MSK1 to Expand the Dynamic Range of Synapses and Enhance Cognition
Privitera, L., Morè, L., Cooper, D. D., Richardson, P., Tsogka, M., Hebenstreit, D., Arthur, J. S. C., & Frenguelli, B. G. (2020) · Journal of Neuroscience · doi:10.1523/jneurosci.2765-19.2020 · Cited by 19 · see citing works
Bardsley, E. N., Davis, H., Ajijola, O. A., Buckler, K. J., Ardell, J. L., Shivkumar, K., & Paterson, D. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-26651-7 · Cited by 17 · see citing works
Xi, S., Yue, G.-X., Liu, Y., Wang, Y., Qiu, Y., Li, Z., Ma, P., Liu, T., Jiang, Y.-M., Yuan, L., et al. (2020) · Aging · doi:10.18632/aging.103912 · Cited by 15 · see citing works
The Role of Ca2+ Permeable AMPA Receptors in Neurodegeneration, Neurotoxicity, and Neuroinflammation
Schröder, N., & da Silva, J. A. C. (2022) · CNS & Neurological Disorders - Drug Targets · doi:10.2174/1871527321666220510141735 · Cited by 16 · see citing works
Genetic manipulations of AMPA glutamate receptors in hippocampal synaptic plasticity
Gugustea, R., & Jia, Z. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108630 · Cited by 15 · see citing works
Deng, T., Li, J., Liu, J., Xu, F., Liu, X., Mi, J., Bergquist, J., Wang, H. H., Yang, C., Lu, L., et al. (2021) · Frontiers in Neuroscience · doi:10.3389/fnins.2021.745668 · Cited by 15 · see citing works
Targeting the dysfunction of glutamate receptors for the development of novel antidepressants
Xia, C., He, J., Du, L., Yan, Y., Lian, W., Xu, J., & Zhang, W. (2021) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2021.107875 · Cited by 14 · see citing works
AMPA receptors in the synapse: Very little space and even less time
Baranovic, J. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108711 · Cited by 14 · see citing works
Zhang, T., Dolga, A. M., Eisel, U. L. M., & Schmidt, M. (2023) · Neurobiology of Disease · doi:10.1016/j.nbd.2023.106389 · Cited by 14 · see citing works
Temporal dynamics of learning‐promoted synaptic diversity in CA1 pyramidal neurons
Sakimoto, Y., Kida, H., & Mitsushima, D. (2019) · The FASEB Journal · doi:10.1096/fj.201801893rrr · Cited by 13 · see citing works
GRIA3 p.Met661Thr variant in a female with developmental epileptic encephalopathy
Okano, S., Makita, Y., Miyamoto, A., Taketazu, G., Kimura, K., Fukuda, I., Tanaka, H., Yanagi, K., & Kaname, T. (2023) · Human Genome Variation · doi:10.1038/s41439-023-00232-1 · Cited by 11 · see citing works
Zhang, T., Musheshe, N., van der Veen, C. H. T. J., Kessels, H. W. H. G., Dolga, A. M., Deyn, P. P. D., Eisel, U. L. M., & Schmidt, M. (2023) · Biomedicines · doi:10.3390/biomedicines11082096 · Cited by 11 · see citing works
Self-citationAdvancements in the study of synaptic plasticity and mitochondrial autophagy relationship
Zhu, Y., Hui, Q., Zhang, Z., Fu, H., Qin, Y., Zhao, Q., Li, Q., Zhang, J., Guo, L., He, W., et al. (2024) · Journal of Neuroscience Research · doi:10.1002/jnr.25309 · Cited by 11 · see citing works
Rinaldi, B., Ge, Y.-H., Freri, E., Tucci, A., Granata, T., Estienne, M., Sun, J., Gérard, B., Bayat, A., Efthymiou, S., et al. (2021) · Neurogenetics · doi:10.1007/s10048-021-00666-1 · Cited by 10 · see citing works
Reinders, N. R., van der Spek, S. J. F., Klaassen, R. V., Koymans, K. J., MacGillavry, H. D., Smit, A. B., & Kessels, H. W. H. G. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0393-24.2024 · Cited by 9 · see citing works
Self-citationArchitecture, dynamics and biogenesis of GluA3 AMPA glutamate receptors
Pokharna, A., Stockwell, I., Ivica, J., Singh, B., Schwab, J., Vega-Gutiérrez, C., Herguedas, B., Cais, O., Krieger, J., & Greger, I. H. (2025) · Nature · doi:10.1038/s41586-025-09325-z · Cited by 9 · see citing works
Roles of AMPA receptors in social behaviors
Xu, Q. W., Larosa, A., & Wong, T. P. (2024) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2024.1405510 · Cited by 6 · see citing works
Fluorescence lifetime imaging of AMPA receptor endocytosis in living neurons: effects of Aβ and PP1
Prinkey, K., Thompson, E., Saikia, J. M., Cid, T., & Doré, K. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2024.1409401 · Cited by 8 · see citing works
McKarns, S. C. (2022) · Current Clinical Pharmacology · doi:10.2174/2772432817666220301104118 · Cited by 7 · see citing works
Characterization of Hippocampal Adult-borne Granule Cells in a Transient Cerebral Ischemia Model
Ceangă, M., Guenther, M., Ingrisch, I., & Kunze, A. (2021) · BIO-PROTOCOL · doi:10.21769/bioprotoc.3890 · Cited by 6 · see citing works
Distinct effects of AMPAR subunit depletion on spatial memory
Eltokhi, A., Bertocchi, I., Rozov, A. V., Jensen, V., Borchardt, T., Taylor, A. M., Proenca, C. C., Rawlins, J. N. P., Bannerman, D. M., & Sprengel, R. (2023) · iScience · doi:10.1016/j.isci.2023.108116 · Cited by 5 · see citing works
Brosens, N., Simon, C., Kessels, H. W. H. G., Lucassen, P. J., & Krugers, H. J. (2023) · Journal of Neuroendocrinology · doi:10.1111/jne.13346 · Cited by 5 · see citing works
Self-citationPawar, H. N., Balivada, S., & Kenney, M. (2018) · Neuroscience Letters · doi:10.1016/j.neulet.2018.09.062 · Cited by 5 · see citing works
Jami, S. A., Wilkinson, B., Guglietta, R., Hartel, N. G., Babiec, W. E., Graham, N. A., Coba, M. P., & O’Dell, T. J. (2023) · Scientific Reports · doi:10.1038/s41598-023-34401-7 · Cited by 4 · see citing works
Milham, L. T., Morris, G. P., Konen, L. M., Rentsch, P., Avgan, N., & Vissel, B. (2024) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2023.1338065 · Cited by 4 · see citing works
Anti-AMPA Receptor Autoantibodies Reduce Excitatory Currents in Rat Hippocampal Neurons
Day, C., Silva, J., Munro, R., BAKER, T. S., Wolff, C., Bithell, A., & Stephens, G. J. (2023) · Pharmaceuticals · doi:10.3390/ph16010077 · Cited by 4 · see citing works
Cofilin overactivation improves hippocampus-dependent short-term memory
Raven, F., Riemersma, I. W., Olthuis, M. F., Rybakovaite, I., Meijer, E. L., Meerlo, P., van der Zee, E. A., & Havekes, R. (2023) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2023.1243524 · Cited by 4 · see citing works
Wang, S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.17632/hybhjg885b.1 · 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
Clarin, J. D., Bouras, N. N., & Gao, W. (2024) · Genes · doi:10.3390/genes15091214 · Cited by 4 · see citing works
Targeting Epac2 and GluA3-containing AMPARs: a novel therapeutic strategy for Alzheimer’s disease
Zhang, T., & Schmidt, M. (2024) · Neural Regeneration Research · doi:10.4103/nrr.nrr-d-24-00751 · Cited by 3 · see citing works
Paradoxical Expression of Ionotropic Glutamate Receptors in Leucocytes
Clanchy, F. I. L., Williams, R. O., & Stone, T. W. (2026) · Clinical Reviews in Allergy & Immunology · doi:10.1007/s12016-025-09126-2 · Cited by 2 · see citing works
Glutamatergic Neurotransmission in the Hippocampus
Tóth, K. (2018) · Springer series in computational neuroscience · doi:10.1007/978-3-319-99103-0_4 · Cited by 2 · see citing works
Lumeij, L. B., van Huijstee, A. N., Cappaert, N. L. M., & Kessels, H. W. H. G. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1232541 · Cited by 2 · see citing works
Self-citationItalia, M., Spinola, A., Borroni, B., Luca, M. D., & Gardoni, F. (2025) · Neurobiology of Disease · doi:10.1016/j.nbd.2025.106843 · Cited by 2 · see citing works
Wang, S., van Rhijn, J.-R., Akkouh, I. A., Kogo, N., Maas, N., Bleeck, A., Ortiz, I. S., Lewerissa, E., Wu, K. M., Schoenmaker, C., et al. (2021) · SSRN Electronic Journal · doi:10.2139/ssrn.3956652 · Cited by 2 · see citing works
GluA1-containing AMPA receptors are necessary for sparse memory engram formation
Willems, T. S., Xiong, H., Kessels, H. W. H. G., & Lesuis, S. L. (2025) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2025.108031 · Cited by 1 · see citing works
Self-citationOliver, & Robert, J. (2017) · UNM’s Digital Repository (University of New Mexico)
S.21.03 Amyloid-beta effects on synapses and memory require AMPA-receptor subunit GluA3
Kessels, H. W. H. G. (2019) · European Neuropsychopharmacology · doi:10.1016/j.euroneuro.2018.11.960
Self-citationTranscriptomic and epigenetic changes after the phenotypic rescue of a Rett Syndrome mouse model
Vargas-Landín, D. B. (2021) · UWA Profiles and Research Repository (UWA) · doi:10.26182/9kh2-8h70
β-amyloid−driven synaptic depression requires PDZ protein interaction at AMPA-receptor subunit GluA3Preprint
Reinders, N. R., van der Spek, S. J. F., Klaassen, R. V., Koymans, K. J., Li, K. W., Smit, A. B., & Kessels, H. W. H. G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.10.03.462970
Self-citationScheefhals, N. (2022) · doi:10.33540/1224
Woodruff, S., Hibicke, M., & Nichols, C. D. (2025) · Psychedelic Medicine · doi:10.1177/28314425251393186
Pathophysiological consequences of a Fragile X missense mutation
Garcia, M. P. (2020) · theses.fr (ABES) · doi:10.70675/b8e86263z5926z4a83zbaf6z0f61bf2d15f9
Anchored kinase and phosphatase signaling networks in amyloid β-induced synaptic dysfunction
Koek, L. A., Jo, H.-N., Kennedy, M. J., & Dell’Acqua, M. L. (2026) · Molecular Pharmacology · doi:10.1016/j.molpha.2026.100141
Distinct roles of AMPA receptor subunits as potential therapeutic targets in Alzheimer’s disease
Seo, J., Kim, K., & Park, M. (2026) · Pharmacological Research · doi:10.1016/j.phrs.2026.108394
- Authors
- Renner, M. C., Albers, E. H., Gutierrez-Castellanos, N., Reinders, N. R., van Huijstee, A. N., Xiong, H., Lodder, T. R., & Kessels, H. W.
- Affiliations
- Northwestern University (US)
- Synaptic Plasticity and Behavior Group, The Netherlands Institute for Neuroscience, Royal Netherlands Academy of Arts and Sciences, Amsterdam, The Netherlands
- Corresponding author
- Kessels, Helmut W
- Venue
- eLife
- Publisher
- eLife Sciences Publications, Ltd
- Published
- 2017-08-01
- Volume
- 6
- ISSN
- 2050-084X (ISSN-L)
- PMC
- PMC5578739
- OpenAlex
- W2740449411
- Cited by
- 75
- References
- 74
- Citations by year
- 2026: 3 · 2025: 6 · 2024: 8 · 2023: 11 · 2022: 6 · 2021: 16 · 2020: 9 · 2019: 6 · 2018: 9 · 2017: 1
- FWCI
- 3.35
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- eLife (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
- KNAW Research Portal (The Royal Netherlands Academy of Arts and Sciences) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (821.02.016, 864.11.014)
- 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
- GluA3, AMPA receptors, synaptic plasticity, synaptic potentiation, cyclic AMP, protein kinase A, Ras GTPase, beta-adrenergic receptors, CA1 pyramidal neurons, hippocampus, excitatory synaptic transmission
- MeSH terms
- Cyclic AMP, Animals, Female, Gene Expression Regulation, Male, Synaptic Transmission, Neuronal Plasticity, Receptors, Adrenergic, beta, Synapses, Signal Transduction, Cyclic AMP-Dependent Protein Kinases, Pyramidal Cells, Receptors, AMPA, Mice, Knockout, Patch-Clamp Techniques, ras Proteins, Excitatory Postsynaptic Potentials, Mice, CA1 Region, Hippocampal
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