Receptor trafficking and synaptic plasticity (original) (raw)
Bliss, T. V. & Collingridge, G. L. A synaptic model of memory: long-term potentiation in the hippocampus. Nature361, 31–39 (1993). ArticleCASPubMed Google Scholar
Benke, T. A., Luthi, A., Isaac, J. T. & Collingridge, G. L. Modulation of AMPA receptor unitary conductance by synaptic activity. Nature393, 793–797 (1998). ArticleCASPubMed Google Scholar
Liu, S. Q. & Cull-Candy, S. G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature405, 454–458 (2000). This was the first research to show that synaptic activity can rapidly regulate the subunit composition of AMPARs at synapses. ArticleCASPubMed Google Scholar
Palmer, M. J., Isaac, J. T. & Collingridge, G. L. Multiple, developmentally regulated expression mechanisms of long-term potentiation at CA1 synapses. J. Neurosci.24, 4903–4911 (2004). ArticleCASPubMedPubMed Central Google Scholar
Malinow, R. & Malenka, R. C. AMPA receptor trafficking and synaptic plasticity. Annu. Rev. Neurosci.25, 103–126 (2002). ArticleCASPubMed Google Scholar
Luthi, A. et al. Hippocampal LTD expression involves a pool of AMPARs regulated by the NSF-GluR2 interaction. Neuron24, 389–399 (1999). The first evidence that LTD involves receptor internalization, and that this uses a mechanism involving the NSF-sensitive pool of AMPARs. ArticleCASPubMed Google Scholar
Richmond, S. A. et al. Localization of the glutamate receptor subunit GluR1 on the surface of living and within cultured hippocampal neurons. Neuroscience75, 69–82 (1996). This work introduced the use of antibodies for live cell imaging of glutamate receptors and showed marked differences in the surface and intracellular distributions of AMPARs at synapses. ArticleCASPubMed Google Scholar
Bredt, D. S. & Nicoll, R. A. AMPA receptor trafficking at excitatory synapses. Neuron40, 361–379 (2003). ArticleCASPubMed Google Scholar
Shi, S. H. et al. Rapid spine delivery and redistribution of AMPA receptors after synaptic NMDA receptor activation. Science284, 1811–1816 (1999). ArticleCASPubMed Google Scholar
Hayashi, Y. et al. Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science287, 2262–2267 (2000). The first direct electrophysiological evidence that AMPARs are incorporated into synapses during LTP. ArticleCASPubMed Google Scholar
Ashby, M. C. et al. Removal of AMPA receptors (AMPARs) from synapses is preceded by transient endocytosis of extrasynaptic AMPARs. J. Neurosci.24, 5172–5176 (2004). ArticleCASPubMedPubMed Central Google Scholar
Beattie, E. C. et al. Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD. Nature Neurosci.3, 1291–1300 (2000). This paper reports that NMDA stimulation of cultured hippocampal neurons results in a rapid dynamin-dependent endocytosis of AMPARs and depression of miniature excitatory postsynaptic currents (mEPSCs) using mechanisms similar to LTD in the CA1 region of hippocampal slices. ArticleCASPubMed Google Scholar
Carroll, R. C., Beattie, E. C., von Zastrow, M. & Malenka, R. C. Role of AMPA receptor endocytosis in synaptic plasticity. Nature Rev. Neurosci.2, 315–324 (2001). ArticleCAS Google Scholar
Lu, W. et al. Activation of synaptic NMDA receptors induces membrane insertion of new AMPA receptors and LTP in cultured hippocampal neurons. Neuron29, 243–254 (2001). ArticleCASPubMed Google Scholar
Pickard, L. et al. Transient synaptic activation of NMDA receptors leads to the insertion of native AMPA receptors at hippocampal neuronal plasma membranes. Neuropharmacology41, 700–713 (2001). References 14 & 15 were the first papers to show that native AMPARs can be inserted into synapses during LTP. ArticleCASPubMed Google Scholar
Snyder, E. M. et al. Internalization of ionotropic glutamate receptors in response to mGluR activation. Nature Neurosci.4, 1079–1085 (2001). ArticleCASPubMed Google Scholar
Xiao, M. Y., Zhou, Q. & Nicoll, R. A. Metabotropic glutamate receptor activation causes a rapid redistribution of AMPA receptors. Neuropharmacology41, 664–671 (2001). ArticleCASPubMed Google Scholar
Borgdorff, A. J. & Choquet, D. Regulation of AMPA receptor lateral movements. Nature417, 649–653 (2002). The first direct evidence that lateral diffusion of AMPARs in the plasma membrane might be an important aspect of synaptic plasticity. ArticleCASPubMed Google Scholar
Tardin, C., Cognet, L., Bats, C., Lounis, B. & Choquet, D. Direct imaging of lateral movements of AMPA receptors inside synapses. EMBO J.22, 4656–4665 (2003). ArticleCASPubMedPubMed Central Google Scholar
Passafaro, M., Piech, V. & Sheng, M. Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons. Nature Neurosci.4, 917–926 (2001). ArticleCASPubMed Google Scholar
Blanpied, T. A., Scott, D. B. & Ehlers, M. D. Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron36, 435–449 (2002). ArticleCASPubMed Google Scholar
Esteban, J. A. et al. PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity. Nature Neurosci.6, 136–143 (2003). ArticleCASPubMed Google Scholar
Man, H. Y. et al. Activation of PI3-kinase is required for AMPA receptor insertion during LTP of mEPSCs in cultured hippocampal neurons. Neuron38, 611–624 (2003). ArticleCASPubMed Google Scholar
Nishimune, A. et al. NSF binding to GluR2 regulates synaptic transmission. Neuron21, 87–97 (1998). The first evidence that there is a rapidly recycling pool of AMPARs at synapses and that this is regulated by the direct interaction between NSF and the GluR2 subunit. ArticleCASPubMed Google Scholar
Osten, P. et al. The AMPA receptor GluR2 C terminus can mediate a reversible, ATP-dependent interaction with NSF and α- and β-SNAPs. Neuron21, 99–110 (1998). ArticleCASPubMed Google Scholar
Lledo, P. M., Zhang, X., Sudhof, T. C., Malenka, R. C. & Nicoll, R. A. Postsynaptic membrane fusion and long-term potentiation. Science279, 399–403 (1998). ArticleCASPubMed Google Scholar
Noel, J. et al. Surface expression of AMPA receptors in hippocampal neurons is regulated by an NSF-dependent mechanism. Neuron23, 365–376 (1999). ArticleCASPubMed Google Scholar
Luscher, C. et al. Role of AMPA receptor cycling in synaptic transmission and plasticity. Neuron24, 649–658 (1999). This paper provides evidence for a crucial role of dynamin-dependent endocytosis of postsynaptic AMPARs in the expression of LTD in hippocampal CA1. ArticleCASPubMed Google Scholar
Kim, C. H. & Lisman, J. E. A labile component of AMPA receptor-mediated synaptic transmission is dependent on microtubule motors, actin, and _N_-ethylmaleimide-sensitive factor. J. Neurosci.21, 4188–4194 (2001). ArticleCASPubMedPubMed Central Google Scholar
Zhou, Q., Xiao, M. & Nicoll, R. A. Contribution of cytoskeleton to the internalization of AMPA receptors. Proc. Natl Acad. Sci. USA98, 1261–1266 (2001). ArticleCASPubMedPubMed Central Google Scholar
Shen, L., Liang, F., Walensky, L. D. & Huganir, R. L. Regulation of AMPA receptor GluR1 subunit surface expression by a 4.1N-linked actin cytoskeletal association. J. Neurosci.20, 7932–7940 (2000). ArticleCASPubMedPubMed Central Google Scholar
Man, H. Y. et al. Regulation of AMPA receptor-mediated synaptic transmission by clathrin-dependent receptor internalization. Neuron25, 649–662 (2000). Direct evidence that clathrin-dependent internalization of AMPARs is involved in LTD at hippocampal CA1 synapses. ArticleCASPubMed Google Scholar
Lee, S. H., Liu, L., Wang, Y. T. & Sheng, M. Clathrin adaptor AP2 and NSF interact with overlapping sites of GluR2 and play distinct roles in AMPA receptor trafficking and hippocampal LTD. Neuron36, 661–674 (2002). Research showing that NSF and AP2 bind on overlapping regions of GluR2 and that the GluR2–NSF and GluR2–AP2 interactions are involved in maintaining basal synaptic transmission and regulated internalization, respectively. ArticleCASPubMed Google Scholar
Wang, Y. T. & Linden, D. J. Expression of cerebellar long-term depression requires postsynaptic clathrin-mediated endocytosis. Neuron25, 635–647 (2000). ArticleCASPubMed Google Scholar
Lee, S. H., Simonetta, A. & Sheng, M. Subunit rules governing the sorting of internalized AMPA receptors in hippocampal neurons. Neuron43, 221–236 (2004). ArticleCASPubMed Google Scholar
Dong, H. et al. GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors. Nature386, 279–284 (1997). ArticleCASPubMed Google Scholar
Osten, P. et al. Mutagenesis reveals a role for ABP/GRIP binding to GluR2 in synaptic surface accumulation of the AMPA receptor. Neuron27, 313–325 (2000). ArticleCASPubMed Google Scholar
Daw, M. I. et al. PDZ proteins interacting with C-terminal GluR2/3 are involved in a PKC-dependent regulation of AMPA receptors at hippocampal synapses. Neuron28, 873–886 (2000). The first electrophysiological evidence that PICK1 and GRIP/ABP interactions with synaptic AMPARs are involved in acute regulation of hippocampal synaptic function and LTD. ArticleCASPubMed Google Scholar
DeSouza, S., Fu, J., States, B. A. & Ziff, E. B. Differential palmitoylation directs the AMPA receptor-binding protein ABP to spines or to intracellular clusters. J. Neurosci.22, 3493–3503 (2002). ArticleCASPubMedPubMed Central Google Scholar
Setou, M. et al. Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites. Nature417, 83–87 (2002). ArticleCASPubMed Google Scholar
Wyszynski, M. et al. Interaction between GRIP and liprin-α/SYD2 is required for AMPA receptor targeting. Neuron34, 39–52 (2002). ArticleCASPubMed Google Scholar
Ye, B. et al. GRASP-1: a neuronal RasGEF associated with the AMPA receptor/GRIP complex. Neuron26, 603–617 (2000). ArticleCASPubMed Google Scholar
Zhu, J. J., Qin, Y., Zhao, M., Van Aelst, L. & Malinow, R. Ras and Rap control AMPA receptor trafficking during synaptic plasticity. Cell110, 443–455 (2002). ArticleCASPubMed Google Scholar
Chung, H. J., Xia, J., Scannevin, R. H., Zhang, X. & Huganir, R. L. Phosphorylation of the AMPA receptor subunit GluR2 differentially regulates its interaction with PDZ domain-containing proteins. J. Neurosci.20, 7258–7267 (2000). ArticleCASPubMedPubMed Central Google Scholar
Perez, J. L. et al. PICK1 targets activated protein kinase Cα to AMPA receptor clusters in spines of hippocampal neurons and reduces surface levels of the AMPA-type glutamate receptor subunit 2. J. Neurosci.21, 5417–5428 (2001). ArticleCASPubMedPubMed Central Google Scholar
Hanley, J. G., Khatri, L., Hanson, P. I. & Ziff, E. B. NSF ATPase and α-/β-SNAPs disassemble the AMPA receptor–PICK1 complex. Neuron34, 53–67 (2002). ArticleCASPubMed Google Scholar
Kim, C. H., Chung, H. J., Lee, H. K. & Huganir, R. L. Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression. Proc. Natl Acad. Sci. USA98, 11725–11730 (2001). ArticleCASPubMedPubMed Central Google Scholar
Matsuda, S., Mikawa, S. & Hirai, H. Phosphorylation of serine-880 in GluR2 by protein kinase C prevents its C terminus from binding with glutamate receptor-interacting protein. J. Neurochem.73, 1765–1768 (1999). ArticleCASPubMed Google Scholar
Xia, J., Chung, H. J., Wihler, C., Huganir, R. L. & Linden, D. J. Cerebellar long-term depression requires PKC-regulated interactions between GluR2/3 and PDZ domain-containing proteins. Neuron28, 499–510 (2000). The first evidence for the molecular mechanism of LTD involving PKC, and the interaction between PICK1 and GluR2/3 AMPAR subunits. ArticleCASPubMed Google Scholar
Terashima, A. et al. Regulation of synaptic strength and AMPA receptor subunit composition by PICK1. J. Neurosci.24, 5381–5390 (2004). ArticleCASPubMedPubMed Central Google Scholar
Ahmadian, G. et al. Tyrosine phosphorylation of GluR2 is required for insulin-stimulated AMPA receptor endocytosis and LTD. EMBO J.23, 1040–1050 (2004). ArticleCASPubMedPubMed Central Google Scholar
Hayashi, T. & Huganir, R. L. Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases. J. Neurosci.24, 6152–6160 (2004). ArticleCASPubMedPubMed Central Google Scholar
Shi, S., Hayashi, Y., Esteban, J. A. & Malinow, R. Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell105, 331–343 (2001). ArticleCASPubMed Google Scholar
Mauceri, D., Cattabeni, F., Di Luca, M. & Gardoni, F. Calcium/calmodulin-dependent protein kinase II phosphorylation drives synapse-associated protein 97 into spines. J. Biol. Chem.279, 23813–23821 (2004). ArticleCASPubMed Google Scholar
Wu, H., Nash, J. E., Zamorano, P. & Garner, C. C. Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking. J. Biol. Chem.277, 30928–30934 (2002). ArticleCASPubMed Google Scholar
Chen, L. et al. Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature408, 936–943 (2000). The first description of the function of stargazin, a protein that was genetically identified as important for motor coordination, showing that stargazin interacts with PSD-95 and is required for the surface expression of AMPARs. ArticleCASPubMed Google Scholar
Stein, V., House, D. R., Bredt, D. S. & Nicoll, R. A. Postsynaptic density-95 mimics and occludes hippocampal long-term potentiation and enhances long-term depression. J. Neurosci.23, 5503–5506 (2003). ArticleCASPubMedPubMed Central Google Scholar
Ehrlich, I. & Malinow, R. Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J. Neurosci.24, 916–927 (2004). ArticleCASPubMedPubMed Central Google Scholar
El-Husseini Ael, D. et al. Synaptic strength regulated by palmitate cycling on PSD-95. Cell108, 849–863 (2002). Article Google Scholar
Tomita, S., Fukata, M., Nicoll, R. A. & Bredt, D. S. Dynamic interaction of stargazin-like TARPs with cycling AMPA receptors at synapses. Science303, 1508–1511 (2004). ArticleCASPubMed Google Scholar
Benke, T. A., Jones, O. T., Collingridge, G. L. & Angelides, K. J. _N_-Methyl-D-aspartate receptors are clustered and immobilized on dendrites of living cortical neurons. Proc. Natl Acad. Sci. USA90, 7819–7823 (1993). ArticleCASPubMedPubMed Central Google Scholar
Groc, L. et al. Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nature Neurosci.7, 695–696 (2004). ArticleCASPubMed Google Scholar
Tovar, K. R. & Westbrook, G. L. Mobile NMDA receptors at hippocampal synapses. Neuron34, 255–264 (2002). ArticleCASPubMed Google Scholar
Guillaud, L., Setou, M. & Hirokawa, N. KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J. Neurosci.23, 131–140 (2003). ArticleCASPubMedPubMed Central Google Scholar
Washbourne, P., Bennett, J. E. & McAllister, A. K. Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nature Neurosci.5, 751–759 (2002). ArticleCASPubMed Google Scholar
Lei, S., Czerwinska, E., Czerwinski, W., Walsh, M. P. & MacDonald, J. F. Regulation of NMDA receptor activity by F-actin and myosin light chain kinase. J. Neurosci.21, 8464–8472 (2001). ArticleCASPubMedPubMed Central Google Scholar
Standley, S., Roche, K. W., McCallum, J., Sans, N. & Wenthold, R. J. PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron28, 887–898 (2000). ArticleCASPubMed Google Scholar
Roche, K. W. et al. Molecular determinants of NMDA receptor internalization. Nature Neurosci.4, 794–802 (2001). ArticleCASPubMed Google Scholar
Li, B., Otsu, Y., Murphy, T. H. & Raymond, L. A. Developmental decrease in NMDA receptor desensitization associated with shift to synapse and interaction with postsynaptic density-95. J. Neurosci.23, 11244–11254 (2003). ArticleCASPubMedPubMed Central Google Scholar
Nong, Y. et al. Glycine binding primes NMDA receptor internalization. Nature422, 302–307 (2003). ArticleCASPubMed Google Scholar
Barria, A. & Malinow, R. Subunit-specific NMDA receptor trafficking to synapses. Neuron35, 345–353 (2002). ArticleCASPubMed Google Scholar
Vissel, B., Krupp, J. J., Heinemann, S. F. & Westbrook, G. L. A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nature Neurosci.4, 587–596 (2001). ArticleCASPubMed Google Scholar
Li, B. et al. Differential regulation of synaptic and extra-synaptic NMDA receptors. Nature Neurosci.5, 833–834 (2002). ArticleCASPubMed Google Scholar
Skeberdis, V. A., Lan, J., Zheng, X., Zukin, R. S. & Bennett, M. V. Insulin promotes rapid delivery of _N_-methyl-D-aspartate receptors to the cell surface by exocytosis. Proc. Natl Acad. Sci. USA98, 3561–3566 (2001). ArticleCASPubMedPubMed Central Google Scholar
Lan, J. Y. et al. Protein kinase C modulates NMDA receptor trafficking and gating. Nature Neurosci.4, 382–390 (2001). ArticleCASPubMed Google Scholar
Lan, J. Y. et al. Activation of metabotropic glutamate receptor 1 accelerates NMDA receptor trafficking. J. Neurosci.21, 6058–6068 (2001). ArticleCASPubMedPubMed Central Google Scholar
Grosshans, D. R., Clayton, D. A., Coultrap, S. J. & Browning, M. D. LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nature Neurosci.5, 27–33 (2002). ArticleCASPubMed Google Scholar
Lerma, J. Roles and rules of kainate receptors in synaptic transmission. Nature Rev. Neurosci.4, 481–495 (2003). ArticleCAS Google Scholar
Bortolotto, Z. A. et al. Kainate receptors are involved in synaptic plasticity. Nature402, 297–301 (1999). ArticleCASPubMed Google Scholar
Kidd, F. L. & Isaac, J. T. Developmental and activity-dependent regulation of kainate receptors at thalamocortical synapses. Nature400, 569–573 (1999). ArticleCASPubMed Google Scholar
Garcia, E. P. et al. SAP90 binds and clusters kainate receptors causing incomplete desensitization. Neuron21, 727–739 (1998). ArticleCASPubMed Google Scholar
Ren, Z. et al. Cell surface expression of GluR5 kainate receptors is regulated by an endoplasmic reticulum retention signal. J. Biol. Chem.278, 52700–52709 (2003). ArticleCASPubMed Google Scholar
Jaskolski, F. et al. Subunit composition and alternative splicing regulate membrane delivery of kainate receptors. J. Neurosci.24, 2506–2515 (2004). ArticleCASPubMedPubMed Central Google Scholar
Gallyas, F., Jr, Ball, S. M. & Molnar, E. Assembly and cell surface expression of KA-2 subunit-containing kainate receptors. J. Neurochem.86, 1414–1427 (2003). ArticleCASPubMed Google Scholar
Hirbec, H. et al. Rapid and differential regulation of AMPA and kainate receptors at hippocampal mossy fibre synapses by PICK1 and GRIP. Neuron37, 625–638 (2003). ArticleCASPubMedPubMed Central Google Scholar
Anwyl, R. Metabotropic glutamate receptors: electrophysiological properties and role in plasticity. Brain Res. Brain Res. Rev.29, 83–120 (1999). ArticleCASPubMed Google Scholar
Bortolotto, Z. A., Bashir, Z. I., Davies, C. H. & Collingridge, G. L. A molecular switch activated by metabotropic glutamate receptors regulates induction of long-term potentiation. Nature368, 740–743 (1994). ArticleCASPubMed Google Scholar
Bolshakov, V. Y. & Siegelbaum, S. A. Postsynaptic induction and presynaptic expression of hippocampal long-term depression. Science264, 1148–1152 (1994). ArticleCASPubMed Google Scholar
Fagni, L., Ango, F., Perroy, J. & Bockaert, J. Identification and functional roles of metabotropic glutamate receptor-interacting proteins. Semin. Cell Dev. Biol.15, 289–298 (2004). ArticleCASPubMed Google Scholar
Ango, F. et al. Dendritic and axonal targeting of type 5 metabotropic glutamate receptor is regulated by homer1 proteins and neuronal excitation. J. Neurosci.20, 8710–8716 (2000). ArticleCASPubMedPubMed Central Google Scholar
Roche, K. W. et al. Homer 1b regulates the trafficking of group I metabotropic glutamate receptors. J. Biol. Chem.274, 25953–25957 (1999). ArticleCASPubMed Google Scholar
Doherty, A. J., Coutinho, V., Collingridge, G. L. & Henley, J. M. Rapid internalization and surface expression of a functional, fluorescently tagged G-protein-coupled glutamate receptor. Biochem. J.341, 415–422 (1999). ArticleCASPubMedPubMed Central Google Scholar
Mundell, S. J., Matharu, A. L., Pula, G., Roberts, P. J. & Kelly, E. Agonist-induced internalization of the metabotropic glutamate receptor 1a is arrestin- and dynamin-dependent. J. Neurochem.78, 546–551 (2001). ArticleCASPubMed Google Scholar
Serge, A., Fourgeaud, L., Hemar, A. & Choquet, D. Receptor activation and homer differentially control the lateral mobility of metabotropic glutamate receptor 5 in the neuronal membrane. J. Neurosci.22, 3910–3920 (2002). ArticleCASPubMedPubMed Central Google Scholar
Gaiarsa, J. L., Caillard, O. & Ben-Ari, Y. Long-term plasticity at GABAergic and glycinergic synapses: mechanisms and functional significance. Trends Neurosci.25, 564–570 (2002). ArticleCASPubMed Google Scholar
Nusser, Z., Hajos, N., Somogyi, P. & Mody, I. Increased number of synaptic GABAA receptors underlies potentiation at hippocampal inhibitory synapses. Nature395, 172–177 (1998). ArticleCASPubMed Google Scholar
Kittler, J. T. & Moss, S. J. Modulation of GABAA receptor activity by phosphorylation and receptor trafficking: implications for the efficacy of synaptic inhibition. Curr. Opin. Neurobiol.13, 341–347 (2003). ArticleCASPubMed Google Scholar
Wan, Q. et al. Recruitment of functional GABAA receptors to postsynaptic domains by insulin. Nature388, 686–690 (1997). The first evidence that the number of postsynaptic GABAARs can be rapidly increased by translocation from an intracellular compartment to postsynaptic membranes, and that this is a powerful means of strengthening synaptic efficacy. ArticleCASPubMed Google Scholar
Wang, Q. et al. Control of synaptic strength, a novel function of Akt. Neuron38, 915–928 (2003). ArticleCASPubMed Google Scholar
Jovanovic, J. N., Thomas, P., Kittler, J. T., Smart, T. G. & Moss, S. J. Brain-derived neurotrophic factor modulates fast synaptic inhibition by regulating GABAA receptor phosphorylation, activity, and cell-surface stability. J. Neurosci.24, 522–530 (2004). ArticleCASPubMedPubMed Central Google Scholar
Kittler, J. T. et al. Constitutive endocytosis of GABAA receptors by an association with the adaptin AP2 complex modulates inhibitory synaptic currents in hippocampal neurons. J. Neurosci.20, 7972–7977 (2000). Identification of a direct interaction between AP2 and GABAARs and results showing that constitutive clathrin-dependent GABAAR endocytosis regulates synaptic transmission in cultured hippocampal neurons. ArticleCASPubMedPubMed Central Google Scholar
Velazquez, J. L., Thompson, C. L., Barnes, E. M., Jr & Angelides, K. J. Distribution and lateral mobility of GABA/benzodiazepine receptors on nerve cells. J. Neurosci.9, 2163–2169 (1989). ArticleCASPubMedPubMed Central Google Scholar
Peran, M., Hooper, H., Rayner, S. L., Stephenson, F. A. & Salas, R. GABAA receptor α1 and α6 subunits mediate cell surface anchoring in cultured cells. Neurosci. Lett.364, 67–70 (2004). ArticleCASPubMed Google Scholar
Beck, M. et al. Identification, molecular cloning, and characterization of a novel GABAA receptor-associated protein, GRIF-1. J. Biol. Chem.277, 30079–30090 (2002). ArticleCASPubMed Google Scholar
Wang, H., Bedford, F. K., Brandon, N. J., Moss, S. J. & Olsen, R. W. GABAA-receptor-associated protein links GABAA receptors and the cytoskeleton. Nature397, 69–72 (1999). ArticleCASPubMed Google Scholar
Bedford, F. K. et al. GABAA receptor cell surface number and subunit stability are regulated by the ubiquitin-like protein Plic-1. Nature Neurosci.4, 908–916 (2001). ArticleCASPubMed Google Scholar
Essrich, C., Lorez, M., Benson, J. A., Fritschy, J. M. & Luscher, B. Postsynaptic clustering of major GABAA receptor subtypes requires the γ2 subunit and gephyrin. Nature Neurosci.1, 563–571 (1998). ArticleCASPubMed Google Scholar
Kneussel, M. et al. Gephyrin-independent clustering of postsynaptic GABAA receptor subtypes. Mol. Cell. Neurosci.17, 973–982 (2001). ArticleCASPubMed Google Scholar
Davies, C. H., Starkey, S. J., Pozza, M. F. & Collingridge, G. L. GABA autoreceptors regulate the induction of LTP. Nature349, 609–611 (1991). ArticleCASPubMed Google Scholar
Vernon, E. et al. GABAB receptors couple directly to the transcription factor ATF4. Mol. Cell. Neurosci.17, 637–645 (2001). ArticleCASPubMed Google Scholar
Nehring, R. B. et al. The metabotropic GABAB receptor directly interacts with the activating transcription factor 4. J. Biol. Chem.275, 35185–35191 (2000). ArticleCASPubMed Google Scholar
White, J. H. et al. The GABAB receptor interacts directly with the related transcription factors CREB2 and ATFx. Proc. Natl Acad. Sci. USA97, 13967–13972 (2000). ArticleCASPubMedPubMed Central Google Scholar
Couve, A. et al. Marlin-1, a novel RNA-binding protein associates with GABAB receptors. J. Biol. Chem.279, 3934–3943 (2004). ArticleCAS Google Scholar
Couve, A. et al. Cyclic AMP-dependent protein kinase phosphorylation facilitates GABAB receptor-effector coupling. Nature Neurosci.5, 415–424 (2002). ArticleCASPubMed Google Scholar
Lisman, J. A mechanism for the Hebb and the anti-Hebb processes underlying learning and memory. Proc. Natl Acad. Sci. USA86, 9574–9578 (1989). ArticleCASPubMedPubMed Central Google Scholar
Sakimura, K. et al. Reduced hippocampal LTP and spatial learning in mice lacking NMDA receptor ε1 subunit. Nature373, 151–155 (1995). ArticleCASPubMed Google Scholar
Hrabetova, S. & Sacktor, T. C. Long-term potentiation and long-term depression are induced through pharmacologically distinct NMDA receptors. Neurosci. Lett.226, 107–110 (1997). ArticleCASPubMed Google Scholar
Hrabetova, S. et al. Distinct NMDA receptor subpopulations contribute to long-term potentiation and long-term depression induction. J. Neurosci.20, RC81 (2000).
Sjostrom, P. J., Turrigiano, G. G. & Nelson, S. B. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron39, 641–654 (2003). ArticlePubMed Google Scholar
Hendricson, A. W., Miao, C. L., Lippmann, M. J. & Morrisett, R. A. Ifenprodil and ethanol enhance NMDA receptor-dependent long-term depression. J. Pharmacol. Exp. Ther.301, 938–944 (2002). ArticleCASPubMed Google Scholar
Yoshimura, Y., Ohmura, T. & Komatsu, Y. Two forms of synaptic plasticity with distinct dependence on age, experience, and NMDA receptor subtype in rat visual cortex. J. Neurosci.23, 6557–6566 (2003). ArticleCASPubMedPubMed Central Google Scholar
Kutsuwada, T. et al. Impairment of suckling response, trigeminal neuronal pattern formation, and hippocampal LTD in NMDA receptor ε2 subunit mutant mice. Neuron16, 333–344 (1996). ArticleCASPubMed Google Scholar
Tang, Y. P. et al. Genetic enhancement of learning and memory in mice. Nature401, 63–69 (1999). ArticleCASPubMed Google Scholar
Clayton, D. A., Mesches, M. H., Alvarez, E., Bickford, P. C. & Browning, M. D. A hippocampal NR2B deficit can mimic age-related changes in long-term potentiation and spatial learning in the Fischer 344 rat. J. Neurosci.22, 3628–3637 (2002). ArticleCASPubMedPubMed Central Google Scholar
Sprengel, R. et al. Importance of the intracellular domain of NR2 subunits for NMDA receptor function in vivo. Cell92, 279–289 (1998). ArticleCASPubMed Google Scholar
Liu, L. et al. Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity. Science304, 1021–1024 (2004). This study showed that activation of NR2A- and NR2B-containing NMDAR subpopulations is required for hippocampal homosynaptic LTP and LTD, respectively. Therefore, this paper provides strong evidence that NR2 subunit composition might be a crucial molecular determinant that dictates the polarity of synaptic plasticity. ArticleCASPubMed Google Scholar
Massey, P. V. et al. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci.24, 7821–7828 (2004). This paper shows that activation of extrasynaptic NR2B-containing NMDARs is both necessary and sufficient for LTD, and that activation of synaptic NR2A-containing NMDARs is required for LTP and its reversal, depotentiation at cortical synapses. This was the first evidence for a crucial role of NMDAR localization in synaptic plasticity and also indicates that distinct mechanisms might underlie depotentiation andde novoLTD. ArticleCASPubMedPubMed Central Google Scholar
Stocca, G. & Vicini, S. Increased contribution of NR2A subunit to synaptic NMDA receptors in developing rat cortical neurons. J. Physiol.507, 13–24 (1998). ArticleCASPubMedPubMed Central Google Scholar
Scimemi, A., Fine, A., Kullmann, D. M. & Rusakov, D. A. NR2B-containing receptors mediate cross talk among hippocampal synapses. J. Neurosci.24, 4767–4777 (2004). ArticleCASPubMedPubMed Central Google Scholar