Cited by 66Neuroscience and Neuropharmacology ResearchAmino Acid Enzymes and MetabolismReceptor Mechanisms and Signaling

AMPA receptor trafficking and LTP: Carboxy-termini, amino-termini and TARPs

Open access
Díaz-Alonso, Javier, Nicoll, Roger A.·2021·Neuropharmacology

Abstract

AMPA receptors (AMPARs) are fundamental elements in excitatory synaptic transmission and synaptic plasticity in the CNS. Long term potentiation (LTP), a form of synaptic plasticity which contributes to learning and memory formation, relies on the accumulation of AMPARs at the postsynapse. This phenomenon requires the coordinated recruitment of different elements in the AMPAR complex. Based on recent research reviewed herein, we propose an updated AMPAR trafficking and LTP model which incorporates both extracellular as well as intracellular mechanisms. This article is part of the special Issue on 'Glutamate Receptors - AMPA receptors'.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.neuropharm.2021.108710

Cites

27 of 27 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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?

  • Synaptic capture of AMPARs requires the PDZ domain interaction between TARPs and PSD-95.

    “It is also agreed that the synaptic capture of AMPARs requires the PDZ domain interaction between TARPs and PSD-95 (275, 279, 294, 440).”

    From Synaptic memory and CaMKII (2023) · cites this paper as [440]

    The section on TARP/MAGUK interactions says TARP–PSD-95 interactions stabilize AMPARs at the postsynaptic density and involve PSD-95 PDZ domains. It calls these interactions the most plausible AMPAR capture sites, but does not establish that this specific interaction is universally required; the reported requirement for the TARP binding motif comes from particular experimental conditions. (LLM, conf=0.84)

    Experimental — accuracy not yet measured
  • SAP97 acts as an adaptor between GluA1 and Myosin V and is essential for intracellular trafficking and targeting of AMPARs during LTP.

    “Synapse-associated protein 97 (SAP97), another MAGUK family protein, acts as an adaptor between GluA1 and Myosin V, being essential for intracellular trafficking and targeting of AMPARs during LTP [47].”

    From Molecular Physiology of the Neuronal Synapse (2026) · cites this paper as [47]

    The Introduction section on the GluA1 C-terminal domain (page unavailable) says that GluA1 binds the MAGUK SAP97, supporting their association. It does not describe SAP97 as an adaptor to Myosin V or establish that SAP97 is essential for AMPAR trafficking and targeting during LTP. Instead, it reports normal LTP when the GluA1 SAP97-binding motif is absent and says the motif’s role remains unclear. (LLM, conf=0.87)

    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

Flagged first, then by citations

Research works printed but not linked: 106

  1. Adesnik H, Nicoll RA, 2007. Conservation of glutamate receptor 2-containing AMPA receptors during long-term potentiation. J. Neurosci.: the official journal of the Society for Neuroscience 27, 4598– 4602. PMC6672988 17460072
  2. Andrasfalvy BK, Magee JC, 2004. Changes in AMPA receptor currents following LTP induction on rat CA1 pyramidal neurones. J. Physiol 559, 543– 554. 15235093 PMC1665120
  3. Angulo MC, Lambolez B, Audinat E, Hestrin S, Rossier J, 1997. Subunit composition, kinetic, and permeation properties of AMPA receptors in single neocortical nonpyramidal cells. J. Neurosci.: the official journal of the Society for Neuroscience 17, 6685– 6696. PMC6573153 9254681
  4. Ayalon G, Stern-Bach Y, 2001. Functional assembly of AMPA and kainate receptors is mediated by several discrete protein-protein interactions. Neuron 31, 103– 113. 11498054
  5. Barria A, Derkach V, Soderling T, 1997a. Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor. J. Biol. Chem 272, 32727– 32730. 9407043
  6. Barria A, Muller D, Derkach V, Griffith LC, Soderling TR, 1997b. Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation. Science 276, 2042– 2045. 9197267
  7. Bats C, Groc L, Choquet D, 2007. The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53, 719– 734. 17329211
  8. Beique JC, Lin DT, Kang MG, Aizawa H, Takamiya K, Huganir RL, 2006. Synapse-specific regulation of AMPA receptor function by PSD-95. Proc. Natl. Acad. Sci. U. S. A 103, 19535– 19540. 17148601 PMC1748260
  9. Biederer T, Kaeser PS, Blanpied TA, 2017. Transcellular nanoalignment of synaptic function. Neuron 96, 680– 696. 29096080 PMC5777221
  10. Bjartmar L, Huberman AD, Ullian EM, Renteria RC, Liu X, Xu W, Prezioso J, Susman MW, Stellwagen D, Stokes CC,, 2006. Neuronal pentraxins mediate synaptic refinement in the developing visual system. J. Neurosci.: the official journal of the Society for Neuroscience 26, 6269– 6281. PMC2579897 16763034
  11. Bliss TV, Lomo T, 1973. Long-lasting potentiation of synaptic transmission in the dentate area of the anaesthetized rabbit following stimulation of the perforant path. J. Physiol 232, 331– 356. 4727084 PMC1350458
  12. Bowie D, 2012. Redefining the classification of AMPA-selective ionotropic glutamate receptors. J. Physiol 590, 49– 61. 22106175 PMC3300045
  13. Cais O, Herguedas B, Krol K, Cull-Candy SG, Farrant M, Greger IH, 2014. Mapping the interaction sites between AMPA receptors and TARPs reveals a role for the receptor N-terminal domain in channel gating. Cell Rep. 9, 728– 740. 25373908 PMC4405707
  14. Chen H, Tang AH, Blanpied TA, 2018. Subsynaptic spatial organization as a regulator of synaptic strength and plasticity. Curr. Opin. Neurobiol 51, 147– 153. 29902592 PMC6295321
  15. Chen S, Gouaux E, 2019. Structure and mechanism of AMPA receptor - auxiliary protein complexes. Curr. Opin. Struct. Biol 54, 104– 111. 30825796 PMC6592759
  16. Chen X, Levy JM, Hou A, Winters C, Azzam R, Sousa AA, Leapman RD, Nicoll RA, Reese TS, 2015. PSD-95 family MAGUKs are essential for anchoring AMPA and NMDA receptor complexes at the postsynaptic density. Proc. Natl. Acad. Sci. U. S. A 112, E6983– E6992. 26604311 PMC4687590
  17. Choquet D, 2018. Linking nanoscale dynamics of AMPA receptor organization to plasticity of excitatory synapses and learning. J. Neurosci.: the official journal of the Society for Neuroscience 38, 9318– 9329. PMC6705996 30381423
  18. Clayton A, Siebold C, Gilbert RJ, Sutton GC, Harlos K, McIlhinney RA, Jones EY, Aricescu AR, 2009. Crystal structure of the GluR2 amino-terminal domain provides insights into the architecture and assembly of ionotropic glutamate receptors. J. Mol. Biol 392, 1125– 1132. 19651138
  19. de Wit J, Sylwestrak E, O’Sullivan ML, Otto S, Tiglio K, Savas JN, Yates JR 3rd, Comoletti D, Taylor P, Ghosh A, 2009. LRRTM2 interacts with Neurexin1 and regulates excitatory synapse formation. Neuron 64, 799– 806. 20064388 PMC2829666
  20. Devinsky O, Cross JH, Laux L, Marsh E, Miller I, Nabbout R, Scheffer IE, Thiele EA, Wright S, Cannabidiol in Dravet Syndrome Study, G., 2017. Trial of cannabidiol for drug-resistant seizures in the Dravet syndrome. N. Engl. J. Med 376, 2011– 2020. 28538134
  21. Devinsky O, Patel AD, Cross JH, Villanueva V, Wirrell EC, Privitera M, Greenwood SM, Roberts C, Checketts D, VanLandingham KE,, 2018. Effect of cannabidiol on drop seizures in the lennox-gastaut syndrome. N. Engl. J. Med 378, 1888– 1897. 29768152
  22. Diaz-Alonso J, Morishita W, Incontro S, Simms J, Holtzman J, Gill M, Mucke L, Malenka RC, Nicoll RA, 2020. Long-term potentiation is independent of the C-tail of the GluA1 AMPA receptor subunit. eLife 9. PMC7500950 32831170
  23. Diering GH, Heo S, Hussain NK, Liu B, Huganir RL, 2016. Extensive phosphorylation of AMPA receptors in neurons. Proc. Natl. Acad. Sci. U. S. A 113, E4920– E4927. 27482106 PMC4995952
  24. Dityatev A, Schachner M, Sonderegger P, 2010. The dual role of the extracellular matrix in synaptic plasticity and homeostasis. Nat. Rev. Neurosci 11, 735– 746. 20944663
  25. Ehrlich I, Malinow R, 2004. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci.: the official journal of the Society for Neuroscience 24, 916– 927. PMC6729816 14749436
  26. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA, 2006. Synapse-specific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52, 307– 320. 17046693
  27. Farhy-Tselnicker I, van Casteren ACM, Lee A, Chang VT, Aricescu AR, Allen NJ, 2017. Astrocyte-secreted glypican 4 regulates release of neuronal pentraxin 1 from axons to induce functional synapse formation. Neuron 96, 428– 445 e413. 29024665 PMC5663462
  28. Favuzzi E, Marques-Smith A, Deogracias R, Winterflood CM, Sanchez-Aguilera A, Mantoan L, Maeso P, Fernandes C, Ewers H, Rico B, 2017. Activity-dependent gating of parvalbumin interneuron function by the peri neuronal net protein brevican. Neuron 95, 639– 655 e610. 28712654
  29. Frischknecht R, Heine M, Perrais D, Seidenbecher CI, Choquet D, Gundelfinger ED, 2009. Brain extracellular matrix affects AMPA receptor lateral mobility and short-term synaptic plasticity. Nat. Neurosci 12, 897– 904. 19483686
  30. Fukaya M, Yamazaki M, Sakimura K, Watanabe M, 2005. Spatial diversity in gene expression for VDCCgamma subunit family in developing and adult mouse brains. Neurosci. Res 53, 376– 383. 16171881
  31. Garcia-Nafria J, Herguedas B, Watson JF, Greger IH, 2016. The dynamic AMPA receptor extracellular region: a platform for synaptic protein interactions. J. Physiol 594, 5449– 5458. 26891027 PMC5043031
  32. Geiger JR, Melcher T, Koh DS, Sakmann B, Seeburg PH, Jonas P, Monyer H, 1995. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193– 204. 7619522
  33. Granger AJ, Shi Y, Lu W, Cerpas M, Nicoll RA, 2013. LTP requires a reserve pool of glutamate receptors independent of subunit type. Nature 493, 495– 500. 23235828 PMC3998843
  34. Greger IH, Watson JF, Cull-Candy SG, 2017. Structural and functional architecture of AMPA-type glutamate receptors and their auxiliary proteins. Neuron 94, 713– 730. 28521126
  35. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R, 2000. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287, 2262– 2267. 10731148
  36. Henley JM, Wilkinson KA, 2016. Synaptic AMPA receptor composition in development, plasticity and disease. Nat. Rev. Neurosci 17, 337– 350. 27080385
  37. Herguedas B, Watson JF, Ho H, Cais O, Garcia-Nafria J, Greger IH, 2019. Architecture of the heteromeric GluA1/2 AMPA receptor in complex with the auxiliary subunit TARP garnma8. Science 364. PMC6513756 30872532
  38. Herring BE, Nicoll RA, 2016. Long-term potentiation: from CaMKII to AMPA receptor trafficking. Annu. Rev. Physiol 78, 351– 365. 26863325
  39. Hosokawa T, Mitsushima D, Kaneko R, Hayashi Y, 2015. Stoichiometry and phosphoisotypes of hippocampal AMPA-type glutamate receptor phosphorylation. Neuron 85, 60– 67. 25533481 PMC4289098
  40. Hruska M, Henderson N, Le Marchand SJ, Jafri H, Dalva MB, 2018. Synaptic nanomodules underlie the organization and plasticity of spine synapses. Nat. Neurosci 21, 671– 682. 29686261 PMC5920789
  41. Huganir RL, Nicoll RA, 2013. AMPARs and synaptic plasticity: the last 25 years. Neuron 80, 704– 717. 24183021 PMC4195488
  42. Incontro S, Diaz-Alonso J, Iafrati J, Vieira M, Asensio CS, Sohal VS, Roche KW, Bender KJ, Nicoll RA, 2018. The CaMKII/NMDA receptor complex controls hippocampal synaptic transmission by kinase-dependent and independent mechanisms. Nat. Commun 9, 2069. 29802289 PMC5970233
  43. Jackson AC, Nicoll RA, 2011. The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits. Neuron 70, 178– 199. 21521608 PMC3119519
  44. Jacobi E, von Engelhardt J, 2021. Modulation of information processing by AMPA receptor auxiliary subunits. J. Physiol 599, 471– 483. 32628275
  45. Jia Z, Agopyan N, Miu P, Xiong Z, Henderson J, Gerlai R, Taverna FA, Velumian A, MacDonald J, Carlen P,, 1996. Enhanced LTP in mice deficient in the AMPA receptor GluR2. Neuron 17, 945– 956. 8938126
  46. Jiang CH, Wei M, Zhang C, Shi YS, 2021. The amino-terminal domain of GluA1 mediates LTP maintenance via interaction with neuroplastin-65. Proc. Natl. Acad. Sci. U. S. A 118. PMC7936340 33627404
  47. Jin R, Clark S, Weeks AM, Dudman JT, Gouaux E, Partin KM, 2005. Mechanism of positive allosteric modulators acting on AMPA receptors. J. Neurosci.: the official journal of the Society for Neuroscience 25, 9027– 9036. PMC6725607 16192394
  48. Jin R, Singh SK, Gu S, Furukawa H, Sobolevsky AI, Zhou J, Jin Y, Gouaux E, 2009. Crystal structure and association behaviour of the GluR2 ami no-terminal domain. EMBO J. 28, 1812– 1823. 19461580 PMC2699365
  49. Kamalova A, Nakagawa T, 2021. AMPA receptor structure and auxiliary subunits. J. Physiol 599, 453– 469. 32004381 PMC7392800
  50. Kato AS, Burris KD, Gardinier KM, Gernert DL, Porter WJ, Reel J, Ding C, Tu Y, Schober DA, Lee MR,, 2016. Forebrain-selective AMPA-receptor antagonism guided by TARP gamma-8 as an antiepileptic mechanism. Nat. Med 22, 1496– 1501. 27820603
  51. Kauer JA, Malenka RC, Nicoll RA, 1988. A persistent postsynaptic modification mediates long-term potentiation in the hippocampus. Neuron 1, 911– 917. 2908443
  52. Kerr JM, Blanpied TA, 2012. Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density. J. Neurosci.: the official journal of the Society for Neuroscience 32, 658– 673. PMC3596168 22238102
  53. Kim CH, Takamiya K, Petralia RS, Sattler R, Yu S, Zhou W, Kalb R, Wenthold R, Huganir R, 2005. Persistent hippocampal CA1 LTP in mice lacking the C-terminal PDZ ligand of GluR1. Nat. Neurosci 8, 985– 987. 16007085
  54. Lee HK, Takamiya K, Han JS, Man H, Kim CH, Rumbaugh G, Yu S, Ding L, He C, Petralia RS,, 2003. Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory. Cell 112, 631– 643. 12628184
  55. Lee JY, Krieger J, Herguedas B, Garcia-Nafria J, Dutta A, Shaikh SA, Greger IH, Bahar I, 2019. Druggability simulations and X-ray crystallography reveal a ligand-binding site in the GluA3 AMPA receptor N-terminal domain. Structure 27, 241– 252 e243. 30528594 PMC6365164
  56. Leonard AS, Davare MA, Horne MC, Garner CC, Hell JW, 1998. SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem 273, 19518– 19524. 9677374
  57. Levy JM, Chen X, Reese TS, Nicoll RA, 2015. Synaptic consolidation normalizes AMPAR quantal size following MAGUK loss. Neuron 87, 534– 548. 26247861 PMC4596923
  58. Lisman J, Raghavachari S, 2006. A unified model of the presynaptic and postsynaptic changes during LTP at CA1 synapses. Sci. STKE, 2006, re11. 17033044
  59. Liu A, Ji H, Ren Q, Meng Y, Zhang H, Collingride G, Xie W, Jia Z, 2020. The requirement of the C-terminal domain of GluA1 in different forms of long-term potentiation in the Hippocampus is age-dependent. Front. Synaptic Neurosci 12, 588785. 33192442 PMC7661473
  60. Lledo PM, Hjelmstad GO, Mukherji S, Soderling TR, Malenka RC, Nicoll RA, 1995. Calcium/calmodulin-dependent kinase II and long-term potentiation enhance synaptic transmission by the same mechanism. Proc. Natl. Acad. Sci. U. S. A 92, 11175– 11179. 7479960 PMC40594
  61. Lledo PM, Zhang X, Sudhof TC, Malenka RC, Nicoll RA, 1998. Postsynaptic membrane fusion and long-term potentiation. Science 279, 399– 403. 9430593
  62. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA, 2009. Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62, 254– 268. 19409270 PMC3632349
  63. MacGillavry HD, Song Y, Raghavachari S, Blanpied TA, 2013. Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 78, 615– 622. 23719161 PMC3668352
  64. Maher MP, Wu N, Ravula S, Ameriks MK, Savall BM, Liu C, Lord B, Wyatt RM, Matta JA, Dugovic C,, 2016. Discovery and characterization of AMPA receptor modulators selective for TARP-gamma8. J. Pharmacol. Exp. Therapeut 357, 394– 414. 26989142
  65. Mammen AL, Kameyama K, Roche KW, Huganir RL, 1997. Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. J. Biol. Chem 272, 32528– 32533. 9405465
  66. Martin SJ, Grimwood PD, Morris RG, 2000. Synaptic plasticity and memory: an evaluation of the hypothesis. Annu. Rev. Neurosci 23, 649– 711. 10845078
  67. Menuz K, O’Brien JL, Karmizadegan S, Bredt DS, Nicoll RA, 2008. TARP redundancy is critical for maintaining AMPA receptor function. J. Neurosci.: the official journal of the Society for Neuroscience 28, 8740– 8746. PMC3159041 18753375
  68. Meyer D, Bonhoeffer T, Scheuss V, 2014. Balance and stability of synaptic structures during synaptic plasticity. Neuron 82, 430– 443. 24742464
  69. Muller D, Joly M, Lynch G, 1988. Contributions of quisqualate and NMDA receptors to the induction and expression of LTP. Science 242, 1694– 1697. 2904701
  70. Nabavi S, Fox R, Alfonso S, Aow J, Malinow R, 2014. GluA1 trafficking and metabotropic NMDA: addressing results from other laboratories inconsistent with ours. Phil. Trans. Roy. Soc. Lond. B Biol. Sci 369, 20130145. 24298147 PMC3843877
  71. Nair D, Hosy E, Petersen JD, Constals A, Giannone G, Choquet D, Sibarita JB, 2013. Super-resolution imaging reveals that AMPA receptors inside synapses are dynamically organized in nanodomains regulated by PSD95. J. Neurosci.: the official journal of the Society for Neuroscience 33, 13204– 13224. PMC6619720 23926273
  72. Nicoll RA, 2017. A brief history of long-term potentiation. Neuron 93, 281– 290. 28103477
  73. Nicoll RA, Malenka RC, 1995. Contrasting properties of two forms of long-term potentiation in the hippocampus. Nature 377, 115– 118. 7675078
  74. Nicoll RA, Schmitz D, 2005. Synaptic plasticity at hippocampal mossy fibre synapses. Nat. Rev. Neurosci 6, 863– 876. 16261180
  75. O’Brien RJ, Xu D, Petralia RS, Steward O, Huganir RL, Worley P, 1999. Synaptic clustering of AMPA receptors by the extracellular immediate-early gene product Narp. Neuron 23, 309– 323. 10399937
  76. Penn AC, Zhang CL, Georges F, Royer L, Breillat C, Hosy E, Petersen JD, Humeau Y, Choquet D, 2017. Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors. Nature 549, 384– 388. 28902836 PMC5683353
  77. Roche KW, O’Brien RJ, Mammen AL, Bernhardt J, Huganir RL, 1996. Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit. Neuron 16, 1179– 1188. 8663994
  78. Rossmann M, Sukumaran M, Penn AC, Veprintsev DB, Babu MM, Greger IH, 2011. Subunit-selective N-terminal domain associations organize the formation of AMPA receptor heteromers. EMBO J. 30, 959– 971. 21317873 PMC3049212
  79. Saglietti L, Dequidt C, Kamieniarz K, Rousset MC, Valnegri P, Thoumine O, Beretta F, Fagni L, Choquet D, Sala C,, 2007. Extracellular interactions between GluR2 and N-cadherin in spine regulation. Neuron 54, 461– 477. 17481398
  80. Sanes JR, Lichtman JW, 1999. Can molecules explain long-term potentiation? Nat. Neurosci 2, 597– 604. 10404178
  81. Schnell E, Sizemore M, Karimzadegan S, Chen L, Bredt DS, Nicoll RA, 2002. Direct interactions between PSD-95 and stargazin control synaptic AMPA receptor number. Proc. Natl. Acad. Sci. U. S. A 99, 13902– 13907. 12359873 PMC129795
  82. Schwenk J, Baehrens D, Haupt A, Bildl W, Boudkkazi S, Roeper J, Fakler B, Schulte U, 2014. Regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain. Neuron 84, 41– 54. 25242221
  83. Schwenk J, Fakler B, 2020. Building of AMPA-type glutamate receptors in the endoplasmic reticulum and its implication for excitatory neurotransmission. J. Physiol 32749711
  84. Schwenk J, Harmel N, Brechet A, Zolles G, Berkefeld H, Muller CS, Bildl W, Baehrens D, Huber B, Kulik A,, 2012. High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 74, 621– 633. 22632720
  85. Shepherd JD, Huganir RL, 2007. The cell biology of synaptic plasticity: AMPA receptor trafficking. Annu. Rev. Cell Dev. Biol 23, 613– 643. 17506699
  86. Shi S, Hayashi Y, Esteban JA, Malinow R, 2001. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105, 331– 343. 11348590
  87. Shi SH, Hayashi Y, Petralia RS, Zaman SH, Wenthold RJ, Svoboda K, Malinow R, 1999. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science 284, 1811– 1816. 10364548
  88. Shi Y, Lu W, Milstein AD, Nicoll RA, 2009. The stoichiometry of AMPA receptors and TARPs varies by neuronal cell type. Neuron 62, 633– 640. 19524523 PMC3119531
  89. Shibata ACE, Ueda HH, Eto K, Onda M, Sato A, Ohba T, Nabekura J, Murakoshi H, 2021. Photoactivatable CaMKII induces synaptic plasticity in single synapses. Nat. Commun 12, 751. 33531495 PMC7854602
  90. Silva AJ, Stevens CF, Tonegawa S, Wang Y, 1992. Deficient hippocampal long-term potentiation in alpha-calcium-calmodulin kinase II mutant mice. Science 257, 201– 206. 1378648
  91. Straub C, Tomita S, 2012. The regulation of glutamate receptor trafficking and function by TARPs and other transmembrane auxiliary subunits. Curr. Opin. Neurobiol 22, 488– 495. 21993243 PMC3265624
  92. Sumioka A, Brown TE, Kato AS, Bredt DS, Kauer JA, Tomita S, 2011. PDZ binding of TARPgamma-8 controls synaptic transmission but not synaptic plasticity. Nat. Neurosci 14, 1410– 1412. 22002768 PMC3206644
  93. Suzuki K, Elegheert J, Song I, Sasakura H, Senkov O, Matsuda K, Kakegawa W, Clayton AJ, Chang VT, Ferrer-Ferrer M,, 2020. A synthetic synaptic organizer protein restores glutamatergic neuronal circuits. Science 369. PMC7116145 32855309
  94. Takumi Y, Ramirez-Leon V, Laake P, Rinvik E, Ottersen OP, 1999. Different modes of expression of AMPA and NMDA receptors in hippocampal synapses. Nat. Neurosci 2, 618– 624. 10409387
  95. Tomita S, Chen L, Kawasaki Y, Petralia RS, Wenthold RJ, Nicoll RA, Bredt DS, 2003. Functional studies and distribution define a family of transmembrane AMPA receptor regulatory proteins. J. Cell Biol 161, 805– 816. 12771129 PMC2199354
  96. Tomita S, Shenoy A, Fukata Y, Nicoll RA, Bredt DS, 2007. Stargazin interacts functionally with the AMPA receptor glutamate-binding module. Neuropharmacology 52, 87– 91. 16919685
  97. Twomey EC, Yelshanskaya MV, Grassucci RA, Frank J, Sobolevsky AI, 2016. Elucidation of AMPA receptor-stargazin complexes by cryo-electron microscopy. Science 353, 83– 86. 27365450 PMC5125255
  98. Wang Q, Chiu SL, Koropouli E, Hong I, Mitchell S, Easwaran TP, Hamilton NR, Gustina AS, Zhu Q, Ginty DD,, 2017. Neuropilin-2/PlexinA3 receptors associate with GluA1 and mediate Sema3F-dependent homeostatic scaling in cortical neurons. Neuron 96, 1084– 1098 e1087. 29154130 PMC5726806
  99. Watkins JC, Evans RH, 1981. Excitatory amino acid transmitters. Annu. Rev. Pharmacol. Toxicol 21, 165– 204. 6112965
  100. Watson JF, Pinggera A, Ho H, Greger IH, 2020. AMPA receptor anchoring at CA1 synapses is determined by an interplay of N- terminal domain and TARP γ8 interactions. bioRxiv preprint, 10.1101/2020.07.09.196154. PMC8382838 34426577 · DOI
  101. Yu Y, Yang Z, Jin B, Qin X, Zhu X, Sun J, Huo L, Wang R, Shi Y, Jia Z,, 2020. Cannabidiol inhibits febrile seizure by modulating AMPA receptor kinetics through its interaction with the N-terminal domain of GluA1/GluA2. Pharmacol. Res 161, 105128. 32805354
  102. Zamanillo D, Sprengel R, Hvalby O, Jensen V, Burnashev N, Rozov A, Kaiser KM, Koster HJ, Borchardt T, Worley P,, 1999. Importance of AMPA receptors for hippocampal synaptic plasticity but not for spatial learning. Science 284, 1805– 1811. 10364547
  103. Zeng M, Diaz-Alonso J, Ye F, Chen X, Xu J, Ji Z, Nicoll RA, Zhang M, 2019. Phase separation-mediated TARP/MAGUK complex condensation and AMPA receptor synaptic transmission. Neuron 104, 529– 543 e526. 31492534 PMC6842113
  104. Zhao Y, Chen S, Swensen AC, Qian WJ, Gouaux E, 2019. Architecture and subunit arrangement of native AMPA receptors elucidated by cryo-EM. Science 364, 355– 362. 30975770 PMC6701862
  105. Zhou Z, Liu A, Xia S, Leung C, Qi J, Meng Y, Xie W, Park P, Collingridge GL, Jia Z, 2018. The C-terminal tails of endogenous GluA1 and GluA2 differentially contribute to hippocampal synaptic plasticity and learning. Nat. Neurosci 21, 50– 62. 29230056
  106. Zwart R, Sher E, Ping X, Jin X, Sims JR Jr, Chappell AS, Gleason SD, Hahn PJ, Gardinier K, Gernert DL,, 2014. Perampanel, an antagonist of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptors, for the treatment of epilepsy: studies in human epileptic brain and nonepileptic brain and in rodent models. J. Pharmacol. Exp. Therapeut 351, 124– 133. 25027316

Cited by

Sorted by citations

Authors
Díaz-Alonso, J., & Nicoll, R. A.
Affiliations
  • University of California, Irvine (US)
  • University of California, San Francisco (US)
Corresponding author
  • Díaz-Alonso, Javier
  • Nicoll, Roger A.
Venue
Neuropharmacology
Publisher
Elsevier BV
Published
2021-10
Volume
197
Pages
108710
ISSN
0028-3908 (ISSN-L)
OpenAlex
W3179784151
Cited by
66
References
27
Citations by year
2026: 9 · 2025: 8 · 2024: 13 · 2023: 19 · 2022: 14 · 2021: 3
FWCI
1.85
Type
journal article
Language
en
Open access
Locations
  • Neuropharmacology (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion, cc-by-nc-nd)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
Funders
  • National Institute of Mental Health (R01MH070957, R01MH117139)
  • University of California, Irvine
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, receptor trafficking, long-term potentiation, synaptic plasticity, synaptic transmission, C-terminal domain, N-terminal domain, TARP, learning and memory
MeSH terms
Animals, Humans, Long-Term Potentiation, Receptors, AMPA

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