Subunit-specific role for the amino-terminal domain of AMPA receptors in synaptic targeting
Open accessAbstract
The amino-terminal domain (ATD) of AMPA receptors (AMPARs) accounts for approximately 50% of the protein, yet its functional role, if any, remains a mystery. We have discovered that the translocation of surface GluA1, but not GluA2, AMPAR subunits to the synapse requires the ATD. GluA1A2 heteromers in which the ATD of GluA1 is absent fail to translocate, establishing a critical role of the ATD of GluA1. Inserting GFP into the ATD interferes with the constitutive synaptic trafficking of GluA1, but not GluA2, mimicking the deletion of the ATD. Remarkably, long-term potentiation (LTP) can override the masking effect of the GFP tag. GluA1, but not GluA2, lacking the ATD fails to show LTP. These findings uncover a role for the ATD in subunit-specific synaptic trafficking of AMPARs, both constitutively and during plasticity. How LTP, induced postsynaptically, engages these extracellular trafficking motifs and what specific cleft proteins participate in the process remain to be elucidated.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
Tagging GluA1 on the NH2 terminus severely impacts the trafficking of the GluA1-containing receptor.
“Third, most of these studies have tagged GluA1 on the NH2 terminus. This tagging severely impacts the trafficking of the GluA1-containing receptor (343, 344).”
From Synaptic memory and CaMKII (2023) · cites this paper as [344]
The amino terminal domain is not necessary for formation of functional ion channels, or delivery onto the cell surface, but is required for targeting and retention of GluA1 at synapses during LTP.
“Data show that the amino terminal domain is not necessary for the formation of functional ion channels, or delivery onto the cell surface, but is required for targeting and retention of GluA1 at synapses during LTP (Watson et al., 2017, Diaz-Alonso et al., 2017).”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Diaz-Alonso et al., 2017
Cites
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
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
Hayashi, Y., Shi, S.-H., Esteban, J. A., Piccini, A., Poncer, J.-C., & Malinow, R. (2000) · Science · doi:10.1126/science.287.5461.2262 · Cited by 1,524 · see citing works
Rapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276 · see citing works
Flip and Flop: A Cell-Specific Functional Switch in Glutamate-Operated Channels of the CNS
Sommer, B., KEINÄNEN, K. P., Verdoorn, T. A., Wisden, W., Burnashev, N., Herb, A., Köhler, M. G., Takagi, T., Sakmann, B. J., & Seeburg, P. H. (1990) · Science · doi:10.1126/science.1699275 · Cited by 1,259 · 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
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-citationLong-term depression in the CNS
Collingridge, G. L., Peineau, S., Howland, J. G., & Wang, Y. T. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2867 · Cited by 926 · 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
A 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-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-citationSubunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons
Passafaro, M., Piëch, V., & Sheng, M. (2001) · Nature Neuroscience · doi:10.1038/nn0901-917 · Cited by 655 · 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
Uemura, T., Lee, S.-J., Yasumura, M., Takeuchi, T., Yoshida, T., Ra, M., Taguchi, R., Sakimura, K., & Mishina, M. (2010) · Cell · doi:10.1016/j.cell.2010.04.035 · Cited by 496 · see citing works
Lledo, P. M., Hjelmstad, G. O., Mukherji, S., Soderling, T. R., Malenka, R. C., & Nicoll, R. A. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.24.11175 · Cited by 456 · see citing works
Self-citationPostnatal synaptic potentiation: delivery of GluR4-containing AMPA receptors by spontaneous activity
Zhu, J. J., Esteban, J. A., Hayashi, Y., & Malinow, R. (2000) · Nature Neuroscience · doi:10.1038/80614 · Cited by 437 · see citing works
Extracellular interactions between GluR2 and N-cadherin in spine regulation
Saglietti, L., Dequidt, C., Kamieniarz, K., Rousset, M.-C., Valnegri, P., Thoumine, O., Beretta, F., Fagni, L., Choquet, D., Sala, C., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.04.012 · Cited by 341 · see citing works
Cbln1 Is a Ligand for an Orphan Glutamate Receptor δ2, a Bidirectional Synapse Organizer
Matsuda, K., Miura, E., Miyazaki, T., Kakegawa, W., Emi, K., Narumi, S., Fukazawa, Y., Ito-Ishida, A., Kondo, T., Shigemoto, R., et al. (2010) · Science · doi:10.1126/science.1185152 · Cited by 332 · see citing works
Pettit, D. L., Perlman, S., & Malinow, R. (1994) · Science · doi:10.1126/science.7997883 · Cited by 329 · 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-citationAoto, J. N., Martinelli, D. C., Malenka, R. C., Tabuchi, K., & Südhof, T. C. (2013) · Cell · doi:10.1016/j.cell.2013.05.060 · Cited by 299 · see citing works
Pelkey, K. A., Barksdale, E., Craig, M. T., Yuan, X., Sukumaran, M., Vargish, G. A., Mitchell, R. M., Wyeth, M. S., Petralia, R. S., Chittajallu, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.020 · Cited by 245 · see citing works
Lissin, D., Carroll, R. C., Nicoll, R. A., Malenka, R. C., & von Zastrow, M. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-04-01263.1999 · Cited by 206 · see citing works
Self-citationTranssynaptic modulation of kainate receptor functions by C1q-like proteins
Matsuda, K., Budisantoso, T., Mitakidis, N., Sugaya, Y., Miura, E., Kakegawa, W., Yamasaki, M., Konno, K., Uchigashima, M., Abe, M., et al. (2016) · Neuron · doi:10.1016/j.neuron.2016.04.001 · Cited by 180 · see citing works
Presynaptic neuronal pentraxin receptor organizes excitatory and inhibitory synapses
Lee, S.-J., Wei, M., Zhang, C., Maxeiner, S., Pak, C., Calado Botelho, S., Trotter, J., Sterky, F. H., & Südhof, T. C. (2017) · The Journal of Neuroscience · doi:10.1523/jneurosci.2768-16.2016 · Cited by 146 · see citing works
Regulation of AMPA Receptor Gating by Ligand Binding Core Dimers
Horning, M. S., & Mayer, M. L. (2004) · Neuron · doi:10.1016/s0896-6273(04)00018-2 · Cited by 129 · see citing works
Pi, H. J., Otmakhov, N., Lemelin, D., De Koninck, P., & Lisman, J. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0133-10.2010 · Cited by 125 · 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
A Subtype-Specific Function for the Extracellular Domain of Neuroligin 1 in Hippocampal LTP
Shipman, S. L., & Nicoll, R. A. (2012) · Neuron · doi:10.1016/j.neuron.2012.07.024 · Cited by 101 · see citing works
Self-citationPasternack, A. H., Coleman, S. K., Jouppila, A., Mottershead, D. G., Lindfors, M., Pasternack, M., & KEINÄNEN, K. P. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m208349200 · Cited by 83 · see citing works
Leucine-Rich Repeat Transmembrane Proteins Are Essential for Maintenance of Long-Term Potentiation
Soler-Llavina, G. J., Arstikaitis, P., Morishita, W., Ahmad, M., Südhof, T. C., & Malenka, R. C. (2013) · Neuron · doi:10.1016/j.neuron.2013.06.007 · Cited by 77 · see citing works
Ayalon, G., Segev, E., Elgavish, S., & Stern-Bach, Y. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m408413200 · Cited by 69 · see citing works
Cais, O., Herguedas, B., Krol, K., Cull-Candy, S. G., Farrant, M., & Greger, I. H. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.09.029 · Cited by 67 · see citing works
Stargazin interacts functionally with the AMPA receptor glutamate-binding module
Tomita, S., Shenoy, A., Fukata, Y., Nicoll, R. A., & Bredt, D. S. (2006) · Neuropharmacology · doi:10.1016/j.neuropharm.2006.07.012 · Cited by 62 · see citing works
Self-citationKakegawa, W., Tsuzuki, K., Yoshida, Y., Kameyama, K., & Ozawa, S. (2004) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2004.03461.x · Cited by 54 · see citing works
Distinct Subunit Domains Govern Synaptic Stability and Specificity of the Kainate Receptor
Straub, C., Noam, Y., Nomura, T., Yamasaki, M., Yan, D., Fernandes, H. B., Zhang, P., Howe, J. R., Watanabe, M., Contractor, A., et al. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.05.093 · Cited by 41 · see citing works
Genetic analysis of neuronal ionotropic glutamate receptor subunits
Granger, A. J., Gray, J. A., Lü, W., & Nicoll, R. A. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2011.213033 · Cited by 35 · see citing works
Self-citationNabavi, S., Fox, R., Alfonso, S., Aow, J., & Malinow, R. (2013) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2013.0145 · Cited by 35 · see citing works
Möykkynen, T. P., Coleman, S. K., Semenov, A., & KEINÄNEN, K. P. (2014) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.526301 · Cited by 30 · see citing works
Sheng, N., Shi, Y. S., & Nicoll, R. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619253114 · Cited by 27 · 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
Transcellular Nanoalignment of Synaptic Function
Biederer, T., Kaeser, P. S., & Blanpied, T. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.006 · Cited by 352 · see citing works
Architecture and subunit arrangement of native AMPA receptors elucidated by cryo-EM
Zhao, Y., Chen, S., Swensen, A., Qian, W., & Gouaux, E. (2019) · Science · doi:10.1126/science.aaw8250 · Cited by 198 · 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-citationFunctional organization of postsynaptic glutamate receptors
Scheefhals, N., & MacGillavry, H. D. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.002 · Cited by 151 · 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
“This tagging severely impacts the traf fi cking of the GluA1-containing receptor (343, 344).”
BackgroundSelf-citationPurkey, A., & Dell’Acqua, M. L. (2020) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2020.00008 · Cited by 113 · see citing works
Architecture of the heteromeric GluA1/2 AMPA receptor in complex with the auxiliary subunit TARP γ8
Herguedas, B., Watson, J. F., Ho, H., Cais, O., García‐Nafría, J., & Greger, I. H. (2019) · Science · doi:10.1126/science.aav9011 · Cited by 105 · see citing works
AMPA Receptor Trafficking for Postsynaptic Potentiation
Park, M. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00361 · Cited by 102 · see citing works
Comparing plant and animal glutamate receptors: common traits but different fates?
Wudick, M. M., Michard, E., Nunes, C. O., & Feijó, J. A. (2018) · Journal of Experimental Botany · doi:10.1093/jxb/ery153 · 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
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
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-citationSheng, N., Bemben, M. A., Díaz-Alonso, J., Tao, W., Shi, Y. S., & Nicoll, R. A. (2018) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1800719115 · Cited by 65 · see citing works
Self-citationTrans-synaptic assemblies link synaptic vesicles and neuroreceptors
Martínez-Sánchez, A., Laugks, U., Kochovski, Z., Papantoniou, C., Zinzula, L., Baumeister, W. P., & Lučić, V. (2021) · Science Advances · doi:10.1126/sciadv.abe6204 · Cited by 62 · see citing works
The amino-terminal domain of GluA1 mediates LTP maintenance via interaction with neuroplastin-65
Jiang, C., Wei, M., Zhang, C., & Shi, Y. S. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2019194118 · Cited by 58 · see citing works
Hruska, M., Cain, R. E., & Dalva, M. B. (2022) · Nature Communications · doi:10.1038/s41467-022-28504-4 · Cited by 56 · see citing works
Getz, A. M., Ducros, M., Breillat, C., Lampin-Saint-Amaux, A., Daburon, S., François, U., Nowacka, A., Fernández-Monreal, M., Hosy, E., Lanore, F., et al. (2022) · Science Advances · doi:10.1126/sciadv.abm5298 · Cited by 55 · see citing works
Structural biology of glutamate receptor ion channels: towards an understanding of mechanism
Greger, I. H., & Mayer, M. L. (2019) · Current Opinion in Structural Biology · doi:10.1016/j.sbi.2019.05.004 · Cited by 54 · see citing works
Structural mobility tunes signalling of the GluA1 AMPA glutamate receptor
Zhang, D., Ivica, J., Krieger, J., Ho, H., Yamashita, K., Stockwell, I., Baradaran, R., Cais, O., & Greger, I. H. (2023) · Nature · doi:10.1038/s41586-023-06528-0 · Cited by 49 · see citing works
Noelin1 Affects Lateral Mobility of Synaptic AMPA Receptors
Pandya, N. J., Seeger, C., Babai, N. Z., Gonzalez‐Lozano, M. A., Mack, V., Lodder, J. C., Gouwenberg, Y., Mansvelder, H. D., Danielson, U. H., Li, K. W., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.06.102 · Cited by 48 · see citing works
mGluR5 is transiently confined in perisynaptic nanodomains to shape synaptic function
Scheefhals, N., Westra, M., & MacGillavry, H. D. (2023) · Nature Communications · doi:10.1038/s41467-022-35680-w · Cited by 43 · see citing works
Modulation of information processing by AMPA receptor auxiliary subunits
Jacobi, E., & von Engelhardt, J. (2020) · The Journal of Physiology · doi:10.1113/jp276698 · Cited by 38 · 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
Hiester, B. G., Bourke, A. M., Sinnen, B. L., Cook, S. G., Gibson, E. S., Smith, K. R., & Kennedy, M. J. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.10.105 · Cited by 37 · see citing works
Mechanisms and Role of Dendritic Membrane Trafficking for Long-Term Potentiation
Hiester, B. G., Becker, M. I., Bowen, A. B., Schwartz, S. L., & Kennedy, M. J. (2018) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2018.00391 · 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-citationDawe, G. B., Kadir, M. F., Venskutonytė, R., Perozzo, A. M., Yan, Y., Alexander, R. P. D., Navarrete, C., Santander, E. A., Arsenault, M., Fuentes, C., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.03.046 · Cited by 35 · see citing works
Sathler, M. F., Khatri, L., Roberts, J. P., Schmidt, I. G., Zaytseva, A., Kubrusly, R. C. C., Ziff, E. B., & Kim, S. (2021) · Journal of Cell Science · doi:10.1242/jcs.257972 · Cited by 35 · see citing works
Endophilin A1 Promotes Actin Polymerization in Dendritic Spines Required for Synaptic Potentiation
Yang, Y., Chen, J., Guo, Z., Deng, S., Du, X., Zhu, S., Ye, C., Shi, Y. S., & Liu, J. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00177 · Cited by 31 · see citing works
Plasticity of postsynaptic nanostructure
Droogers, W. J., & MacGillavry, H. D. (2023) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2023.103819 · Cited by 27 · see citing works
Neto proteins regulate gating of the kainate-type glutamate receptor GluK2 through two binding sites
Li, Y., Duan, G., Sun, J., Wu, D., Ye, C., Zang, Y., Chen, G., Shi, Y., Wang, J., Zhang, W., et al. (2019) · Journal of Biological Chemistry · doi:10.1074/jbc.ra119.008631 · Cited by 28 · 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
AMPA Receptors Exist in Tunable Mobile and Immobile Synaptic FractionsIn Vivo
Chen, H., Roth, R. H., Lopez-Ortega, E., Tan, H. L., & Huganir, R. L. (2021) · eNeuro · doi:10.1523/eneuro.0015-21.2021 · Cited by 26 · 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-citationEndophilin A1 drives acute structural plasticity of dendritic spines in response to Ca2+/calmodulin
Yang, Y., Jiang, C., Chen, X., Li, D., He, J., Wang, S., Zhao, S. S., Yang, X., Deng, S., Tong, C., et al. (2021) · The Journal of Cell Biology · doi:10.1083/jcb.202007172 · Cited by 22 · see citing works
Dynamics, nanoscale organization, and function of synaptic adhesion molecules
Chamma, I., & Thoumine, O. R. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.04.007 · Cited by 23 · see citing works
Ivica, J., Kejzar, N., Ho, H., Stockwell, I., Kuchtiak, V., Scrutton, A. M., Nakagawa, T., & Greger, I. H. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01369-5 · Cited by 19 · see citing works
Amyloid‐β oligomers suppress subunit‐specific glutamate receptor increase during LTP
Tanaka, H., Sakaguchi, D., & Hirano, T. (2019) · Alzheimer s & Dementia Translational Research & Clinical Interventions · doi:10.1016/j.trci.2019.10.003 · Cited by 19 · see citing works
Postnikova, T. Y., Amakhin, D. V., Trofimova, A. M., & Zaitsev, A. V. (2020) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2020.06.121 · Cited by 18 · see citing works
Allosteric competition and inhibition in AMPA receptors
Hale, W. D., Romero, A. M., Gonzalez, C. U., Jayaraman, V., Lau, A. Y., Huganir, R. L., & Twomey, E. C. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01328-0 · Cited by 18 · see citing works
Activity-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
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-citationAMPA 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
Sumino, A., Sumikama, T., Zhao, Y., Flechsig, H., Umeda, K., Kodera, N., Konno, H., Hattori, M., & Shibata, M. (2024) · ACS Nano · doi:10.1021/acsnano.4c06295 · Cited by 14 · see citing works
Trans-synaptic interactions of ionotropic glutamate receptors
Fossati, M., & Charrier, C. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.09.001 · Cited by 14 · see citing works
Molecular 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
Gating and noelin clustering of native Ca2+-permeable AMPA receptors
Fang, C., Spangler, C. J., Park, J., Sheldon, N., Trussell, L. O., & Gouaux, E. (2025) · Nature · doi:10.1038/s41586-025-09289-0 · Cited by 13 · 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
Regulation of AMPA receptor trafficking by secreted protein factors
Rennich, B. J., Luth, E. S., Moores, S., & Juo, P. (2023) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2023.1271169 · Cited by 10 · see citing works
Architecture, 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
Structure and organization of AMPA receptor-TARP complexes in the mammalian cerebellum
Scrutton, A. M., Sengupta, N., Ivica, J., Stockwell, I., Peak‐Chew, S., Singh, B., Suzuki, K., Chang, V. T.-C., McLaughlin, S. H., Krieger, J., et al. (2025) · Science · doi:10.1126/science.aeb3577 · Cited by 8 · see citing works
Dynamic extracellular interactions with AMPA receptors
Goldschmidt, H. L., Barber, C. N., Renuse, S., Cutler, J. A., Kreimer, S. D., Bygrave, A. M., Meyers, D. J., Hale, W. D., Pandey, A., & Huganir, R. L. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2517436122 · Cited by 7 · 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
Contrasting synaptic roles of MDGA1 and MDGA2Preprint
Bemben, M. A., Sandoval, M. A., Le, A. A., Won, S., Chau, V. N., Lauterborn, J. C., Incontro, S., Li, K. H., Burlingame, A. L., Roche, K. W., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.05.25.542333 · Cited by 7 · see citing works
Self-citationGenetically encoded intrabody probes for labeling and manipulating AMPA-type glutamate receptors
Kareemo, D. J., Winborn, C. S., Olah, S. S., Miller, C. N., Kim, J., Kadgien, C., Actor-Engel, H. S., Ramsay, H. J., Ramsey, A. M., Aoto, J. N., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54530-5 · Cited by 6 · see citing works
Kumaran, K. R., Wahab, H. A., & Hassan, Z. (2022) · Oriental Pharmacy and Experimental Medicine · doi:10.1007/s13596-022-00653-3 · Cited by 4 · see citing works
Using FASS-LTP in postmortem mice brain tissues to assess pathological synaptic function
Currie, J., Budhwani, S. M., Garza, K. H., Mallipudi, M., Natarajan, C., Sreenivasamurthy, S. G. S., & Krishnan, B. (2024) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2024.110219 · 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
Keifer, J. (2023) · Molecular Neurobiology · doi:10.1007/s12035-023-03528-z · 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-citationAMPA receptors in synaptic plasticity and learning and memory
Kim, K., & Park, M. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15754-7.00056-0 · Cited by 1 · 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
LARGE protein drives activity-induced homeostatic resetting
Seo, B. A., Kim, H.-B., Tuong, C. C., Kim, H. J., Dustov, F. A., Lee, S.-H., Choi, S., & Kang, M. (2025) · Science Advances · doi:10.1126/sciadv.adt0703 · Cited by 1 · see citing works
The AMPA receptor life cycle: assembly, regulation and synaptic diversity
Bowie, D., Wang, X.-T., Míguez‐Cabello, F., & Perozzo, A. M. (2026) · Nature reviews. Neuroscience · doi:10.1038/s41583-026-01055-z · Cited by 1 · see citing works
A reassessment of NMDA receptor-dependent presynaptic homeostatic plasticity
Chen, X., Dou, T., Zhang, J., Hong, Y., & Nicoll, R. A. (2026) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2617982123 · Cited by 2 · see citing works
Self-citationThe Endocannabinoid System and the Early Development of the Brain
Thapa, S., & Bukiya, A. N. (2025) · Springer eBooks · doi:10.1007/978-3-031-87990-6_4 · Cited by 1 · see citing works
Synaptic Organization of Surface AMPARs Changes by Brain Region and TauopathyPreprint
Vaidya, R. M., Zhang, J., Nall, D., Pendharkar, R., Lee, Y., Kim, E. C., Ma, D., Huang, F., Nonaka, H., Kiyonaka, S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.07.22.604547 · Cited by 1 · see citing works
NMDA receptor-dependent presynaptic homeostatic plasticity?Preprint
dou, T., Zhang, J., hong, Y., Chen, X., & Nicoll, R. A. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.02.28.708706 · Cited by 1 · see citing works
Self-citationRobust PHP in Adult Hippocampus: Essential Assay OptimizationsPreprint
Chipman, P. H., Fetter, R. D., Ragozzino, F. J., Lee, U., & Davis, G. W. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.03.12.711375 · Cited by 1 · see citing works
McKenzie, C. (2018) · Institute of Science and Technology Austria · doi:10.15479/at:ista:7132
AMPA receptor trafficking in the developing and mature glutamatergic synapse
Catsburg, L. A. E., & MacGillavry, H. D. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-823672-7.00023-5
Scheefhals, N. (2022) · doi:10.33540/1224
(2018) · Society for Neuroscience eBooks · doi:10.1523/hon.010011
Hassan, Z., Kumaran, K. R., Chear, N. J., Bakar, S. N. S., Retinasamy, T., Bhuvanendran, S., Majid, A. M. S. A., Shaikh, M. F., & Othman, I. (2023) · Neuroscience Research Notes · doi:10.31117/neuroscirn.v6i3.196
Curtis, A. J., Zhu, J., Studniarczyk, D., Church, T. W., Farrant, M., & Gold, M. G. (2025) · Journal of Neuroscience · doi:10.1523/jneurosci.0795-25.2025
Leana-Sandoval, G., Madrid, A., Kolli, A. V., Chinn, C. A., Sandoval, M. A., Lo, I., Vera, V. A., Simms, J. A., Wood, M. A., & Díaz-Alonso, J. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03328-y
Self-citationFrom biogenesis to synaptic organization : developing tools to study AMPAR-associated proteins
Bessa‐Neto, D. (2021) · theses.fr (ABES) · doi:10.70675/a68a26edzb1c6z414ez927czebc71c64fb29
Padmanabhan, N., Twilley, R. E., Oku, S., Rabbi, M. S., Skeens, A., Jones, G. C., Acharya, S., Basha, M. A., Rajapakse, D., Koltek, C., et al. (2026) · Neuron · doi:10.1016/j.neuron.2026.06.018
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-citationClustering and Interactions of Ionotropic Receptors – Processes, Mechanisms, Basis of Plasticity
Murzina, G. B. (2026) · Neuroscience and Behavioral Physiology · doi:10.1007/s11055-026-02048-2
Synaptic Organization of Surface AMPARs Changes by Brain Region and TauopathyPreprint
Vaidya, R. M., Zhang, J., Nall, D., Pendharkar, R., Lee, Y., Kim, E. C., Donghan, 马. M., Huang, F., Nonaka, H., Kiyonaka, S., et al. (2026) · eLife · doi:10.7554/elife.112632
Synaptic Organization of Surface AMPARs Changes by Brain Region and TauopathyPreprint
Vaidya, R. M., Zhang, J., Nall, D., Pendharkar, R., Lee, Y., Kim, E. C., Donghan, 马. M., Huang, F., Nonaka, H., Kiyonaka, S., et al. (2026) · eLife · doi:10.7554/elife.112632.1
- Authors
- Díaz-Alonso, J., Sun, Y. J., Granger, A. J., Levy, J. M., Blankenship, S. M., & Nicoll, R. A.
- Affiliations
- University of California, San Francisco (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2017-06-19
- Volume
- 114
- Issue
- 27
- Pages
- 7136-7141
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC5502653
- OpenAlex
- W2693601175
- Cited by
- 89
- References
- 40
- Citations by year
- 2026: 9 · 2025: 10 · 2024: 10 · 2023: 9 · 2022: 5 · 2021: 12 · 2020: 9 · 2019: 10 · 2018: 13 · 2017: 2
- FWCI
- 4.55
- 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)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- HHS | NIH | National Institute of Mental Health (R01MH080379, R01MH070957)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Amino Acid Enzymes and Metabolism
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Keywords
- AMPA receptors, N-terminal domain, GluR1, GluA2, synaptic targeting, receptor trafficking, long-term potentiation, synaptic plasticity, GFP tagging
- MeSH terms
- Protein Domains, Animals, Brain, Cytoplasm, Female, Hippocampus, Synaptic Transmission, Neurons, Synapses, Long-Term Potentiation, Receptors, AMPA, Electroporation, Excitatory Postsynaptic Potentials, Protein Isoforms, Amino Acid Motifs, Green Fluorescent Proteins, Mice, Rats, Protein Multimerization
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
