Glutamate is the major excitatory neurotransmitter in the mammalian central nervous system. There are three distinct subtypes of ionotropic glutamate receptors (GluRs) that have been identified including 2-amino-3-(5-methyl-3-oxo-1,2-oxazol-4-yl)propanoic acid receptors (AMPARs), N-methyl-D-aspartate receptors (NMDARs) and kainate receptors. The most common GluRs in mature synapses are AMPARs that mediate the fast excitatory neurotransmission and NMDARs that mediate the slow excitatory neurotransmission. There have been large numbers of recent reports studying how a single neuron regulates synaptic numbers and types of AMPARs and NMDARs. Our current research is centered primarily on NMDARs and, therefore, we will focus in this review on recent knowledge of molecular mechanisms occurring (1) early in the biosynthetic pathway of NMDARs, (2) in the transport of NMDARs after their release from the endoplasmic reticulum (ER); and (3) at the plasma membrane including excitatory synapses. Because a growing body of evidence also indicates that abnormalities in NMDAR functioning are associated with a number of human psychiatric and neurological diseases, this review together with other chapters in this issue may help to enhance research and to gain further knowledge of normal synaptic physiology as well as of the etiology of many human brain diseases.

Advanced Imaging Core National Institute on Deafness and Other Communication Disorders National Institutes of Health Bethesda MD USA

Institute of Physiology Academy of Sciences of the Czech Republic v v i Prague Czech Republic

Neurocentre Magendie Institut National de la Santé et de la Recherche Médicale U862 Bordeaux France ; Neurocentre Magendie University of Bordeaux U862 Bordeaux France

Zobrazit více v PubMed

Al-Hallaq R. A., Conrads T. P., Veenstra T. D., Wenthold R. J. (2007). NMDA di-heteromeric receptor populations and associated proteins in rat hippocampus. J. Neurosci. 27, 8334–8343. 10.1523/jneurosci.2155-07.2007 PubMed DOI PMC

Amparan D., Avram D., Thomas C. G., Lindahl M. G., Yang J., Bajaj G., et al. . (2005). Direct interaction of myosin regulatory light chain with the NMDA receptor. J. Neurochem. 92, 349–361. 10.1111/j.1471-4159.2004.02869.x PubMed DOI

Atlason P. T., Garside M. L., Meddows E., Whiting P., Mcilhinney R. A. (2007). N-Methyl-D-aspartate (NMDA) receptor subunit NR1 forms the substrate for oligomeric assembly of the NMDA receptor. J. Biol. Chem. 282, 25299–25307. 10.1074/jbc.m702778200 PubMed DOI

Balasuriya D., Goetze T. A., Barrera N. P., Stewart A. P., Suzuki Y., Edwardson J. M. (2013). α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) and N-methyl-D-aspartate (NMDA) receptors adopt different subunit arrangements. J. Biol. Chem. 288, 21987–21998. 10.1074/jbc.M113.469205 PubMed DOI PMC

Bard L., Sainlos M., Bouchet D., Cousins S., Mikasova L., Breillat C., et al. . (2010). Dynamic and specific interaction between synaptic NR2-NMDA receptor and PDZ proteins. Proc. Natl. Acad. Sci. U S A 107, 19561–19566. 10.1073/pnas.1002690107 PubMed DOI PMC

Bartlett T. E., Wang Y. T. (2013). The intersections of NMDAR-dependent synaptic plasticity and cell survival. Neuropharmacology 74, 59–68. 10.1016/j.neuropharm.2013.01.012 PubMed DOI

Bassand P., Bernard A., Rafiki A., Gayet D., Khrestchatisky M. (1999). Differential interaction of the tSXV motifs of the NR1 and NR2A NMDA receptor subunits with PSD-95 and SAP97. Eur. J. Neurosci. 11, 2031–2043. 10.1046/j.1460-9568.1999.00611.x PubMed DOI

Bellone C., Nicoll R. A. (2007). Rapid bidirectional switching of synaptic NMDA receptors. Neuron 55, 779–785. 10.1016/j.neuron.2007.07.035 PubMed DOI

Berger S. J., Carter J. C., Lowry O. H. (1977). The distribution of glycine, GABA, glutamate and aspartate in rabbit spinal cord, cerebellum and hippocampus. J. Neurochem. 28, 149–158. 10.1111/j.1471-4159.1977.tb07720.x PubMed DOI

Blanpied T. A., Kerr J. M., Ehlers M. D. (2008). Structural plasticity with preserved topology in the postsynaptic protein network. Proc. Natl. Acad. Sci. U S A 105, 12587–12592. 10.1073/pnas.0711669105 PubMed DOI PMC

Blanpied T. A., Scott D. B., Ehlers M. D. (2002). Dynamics and regulation of clathrin coats at specialized endocytic zones of dendrites and spines. Neuron 36, 435–449. 10.1016/s0896-6273(02)00979-0 PubMed DOI

Borgland S. L., Taha S. A., Sarti F., Fields H. L., Bonci A. (2006). Orexin A in the VTA is critical for the induction of synaptic plasticity and behavioral sensitization to cocaine. Neuron 49, 589–601. 10.1016/j.neuron.2006.01.016 PubMed DOI

Brenman J. E., Chao D. S., Gee S. H., McGee A. W., Craven S. E., Santillano D. R., et al. . (1996). Interaction of nitric oxide synthase with the postsynaptic density protein PSD-95 and alpha1-syntrophin mediated by PDZ domains. Cell 84, 757–767. 10.1016/s0092-8674(00)81053-3 PubMed DOI

Brickley S. G., Misra C., Mok M. H., Mishina M., Cull-Candy S. G. (2003). NR2B and NR2D subunits coassemble in cerebellar Golgi cells to form a distinct NMDA receptor subtype restricted to extrasynaptic sites. J. Neurosci. 23, 4958–4966. PubMed PMC

Chazot P. L., Stephenson F. A. (1997). Biochemical evidence for the existence of a pool of unassembled C2 exon-containing NR1 subunits of the mammalian forebrain NMDA receptor. J. Neurochem. 68, 507–516. 10.1046/j.1471-4159.1997.68020507.x PubMed DOI

Chen B. S., Roche K. W. (2009). Growth factor-dependent trafficking of cerebellar NMDA receptors via protein kinase B/Akt phosphorylation of NR2C. Neuron 62, 471–478. 10.1016/j.neuron.2009.04.015 PubMed DOI PMC

Chen B. S., Thomas E. V., Sanz-Clemente A., Roche K. W. (2011). NMDA receptor-dependent regulation of dendritic spine morphology by SAP102 splice variants. J. Neurosci. 31, 89–96. 10.1523/JNEUROSCI.1034-10.2011 PubMed DOI PMC

Choquet D., Triller A. (2013). The dynamic synapse. Neuron 80, 691–703. 10.1016/j.neuron.2013.10.013 PubMed DOI

Chowdhury D., Marco S., Brooks I. M., Zandueta A., Rao Y., Haucke V., et al. . (2013). Tyrosine phosphorylation regulates the endocytosis and surface expression of GluN3A-containing NMDA receptors. J. Neurosci. 33, 4151–4164. 10.1523/JNEUROSCI.2721-12.2013 PubMed DOI PMC

Choy R. W., Park M., Temkin P., Herring B. E., Marley A., Nicoll R. A., et al. . (2014). Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82, 55–62. 10.1016/j.neuron.2014.02.018 PubMed DOI PMC

Chung H. J., Huang Y. H., Lau L. F., Huganir R. L. (2004). Regulation of the NMDA receptor complex and trafficking by activity-dependent phosphorylation of the NR2B subunit PDZ ligand. J. Neurosci. 24, 10248–10259. 10.1523/jneurosci.0546-04.2004 PubMed DOI PMC

Collins B. M. (2008). The structure and function of the retromer protein complex. Traffic 9, 1811–1822. 10.1111/j.1600-0854.2008.00777.x PubMed DOI

Correia S. S., Bassani S., Brown T. C., Lisé M. F., Backos D. S., El-Husseini A., et al. . (2008). Motor protein-dependent transport of AMPA receptors into spines during long-term potentiation. Nat. Neurosci. 11, 457–466. 10.1038/nn2063 PubMed DOI

Cousins S. L., Innocent N., Stephenson F. A. (2013). Neto1 associates with the NMDA receptor/amyloid precursor protein complex. J. Neurochem. 126, 554–564. 10.1111/jnc.12280 PubMed DOI

Cousins S. L., Kenny A. V., Stephenson F. A. (2009). Delineation of additional PSD-95 binding domains within NMDA receptor NR2 subunits reveals differences between NR2A/PSD-95 and NR2B/PSD-95 association. Neuroscience 158, 89–95. 10.1016/j.neuroscience.2007.12.051 PubMed DOI

Dalva M. B., Takasu M. A., Lin M. Z., Shamah S. M., Hu L., Gale N. W., et al. . (2000). EphB receptors interact with NMDA receptors and regulate excitatory synapse formation. Cell 103, 945–956. 10.1016/s0092-8674(00)00197-5 PubMed DOI

de Vreede G., Schoenfeld J. D., Windler S. L., Morrison H., Lu H., Bilder D. (2014). The scribble module regulates retromer-dependent endocytic trafficking during epithelial polarization. Development 141, 2796–2802. 10.1242/dev.105403 PubMed DOI PMC

Duguid I. C. (2013). Presynaptic NMDA receptors: are they dendritic receptors in disguise? Brain Res. Bull. 93, 4–9. 10.1016/j.brainresbull.2012.12.004 PubMed DOI

El-Husseini A. E., Craven S. E., Chetkovich D. M., Firestein B. L., Schnell E., Aoki C., et al. . (2000). Dual palmitoylation of PSD-95 mediates its vesiculotubular sorting, postsynaptic targeting and ion channel clustering. J. Cell Biol. 148, 159–172. 10.1083/jcb.148.1.159 PubMed DOI PMC

Elias G. M., Elias L. A., Apostolides P. F., Kriegstein A. R., Nicoll R. A. (2008). Differential trafficking of AMPA and NMDA receptors by SAP102 and PSD-95 underlies synapse development. Proc. Natl. Acad. Sci. U S A 105, 20953–20958. 10.1073/pnas.0811025106 PubMed DOI PMC

Elias G. M., Nicoll R. A. (2007). Synaptic trafficking of glutamate receptors by MAGUK scaffolding proteins. Trends Cell Biol. 17, 343–352. 10.1016/j.tcb.2007.07.005 PubMed DOI

Eriksson M., Nilsson A., Samuelsson H., Samuelsson E.-B., Mo L., Åkesson E., et al. . (2007). On the role of NR3A in human NMDA receptors. Physiol. Behav. 92, 54–59. 10.1016/j.physbeh.2007.05.026 PubMed DOI

Farina A. N., Blain K. Y., Maruo T., Kwiatkowski W., Choe S., Nakagawa T. (2011). Separation of domain contacts is required for heterotetrameric assembly of functional NMDA receptors. J. Neurosci. 31, 3565–3579. 10.1523/JNEUROSCI.6041-10.2011 PubMed DOI PMC

Fukaya M., Fukushima D., Hara Y., Sakagami H. (2014). EFA6A, a guanine nucleotide exchange factor for Arf6, interacts with sorting nexin-1 and regulates neurite outgrowth. J. Neurochem. 129, 21–36. 10.1111/jnc.12524 PubMed DOI

Fukaya M., Kato A., Lovett C., Tonegawa S., Watanabe M. (2003). Retention of NMDA receptor NR2 subunits in the lumen of endoplasmic reticulum in targeted NR1 knockout mice. Proc. Natl. Acad. Sci. U S A 100, 4855–4860. 10.1073/pnas.0830996100 PubMed DOI PMC

Gallon M., Clairfeuille T., Steinberg F., Mas C., Ghai R., Sessions R. B., et al. . (2014). A unique PDZ domain and arrestin-like fold interaction reveals mechanistic details of endocytic recycling by SNX27-retromer. Proc. Natl. Acad. Sci. U S A 111, E3604–E3613. 10.1073/pnas.1410552111 PubMed DOI PMC

Garcia R. A., Vasudevan K., Buonanno A. (2000). The neuregulin receptor ErbB-4 interacts with PDZ-containing proteins at neuronal synapses. Proc. Natl. Acad. Sci. U S A 97, 3596–3601. 10.1073/pnas.97.7.3596 PubMed DOI PMC

Gardoni F., Mauceri D., Fiorentini C., Bellone C., Missale C., Cattabeni F., et al. . (2003). CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J. Biol. Chem. 278, 44745–44752. 10.1074/jbc.m303576200 PubMed DOI

Gerges N. Z., Backos D. S., Rupasinghe C. N., Spaller M. R., Esteban J. A. (2006). Dual role of the exocyst in AMPA receptor targeting and insertion into the postsynaptic membrane. EMBO J. 25, 1623–1634. 10.1038/sj.emboj.7601065 PubMed DOI PMC

Gladding C. M., Raymond L. A. (2011). Mechanisms underlying NMDA receptor synaptic/extrasynaptic distribution and function. Mol. Cell. Neurosci. 48, 308–320. 10.1016/j.mcn.2011.05.001 PubMed DOI

Groc L., Choquet D., Stephenson F. A., Verrier D., Manzoni O. J., Chavis P. (2007). NMDA receptor surface trafficking and synaptic subunit composition are developmentally regulated by the extracellular matrix protein Reelin. J. Neurosci. 27, 10165–10175. 10.1523/jneurosci.1772-07.2007 PubMed DOI PMC

Groc L., Heine M., Cognet L., Brickley K., Stephenson F. A., Lounis B., et al. . (2004). Differential activity-dependent regulation of the lateral mobilities of AMPA and NMDA receptors. Nat. Neurosci. 7, 695–696. 10.1038/nn1270 PubMed DOI

Groc L., Heine M., Cousins S. L., Stephenson F. A., Lounis B., Cognet L., et al. . (2006). NMDA receptor surface mobility depends on NR2A-2B subunits. Proc. Natl. Acad. Sci. U S A 103, 18769–18774. 10.1073/pnas.0605238103 PubMed DOI PMC

Grosshans D. R., Clayton D. A., Coultrap S. J., Browning M. D. (2002). LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1. Nat. Neurosci. 5, 27–33. 10.1038/nn779 PubMed DOI

Guillaud L., Setou M., Hirokawa N. (2003). KIF17 dynamics and regulation of NR2B trafficking in hippocampal neurons. J. Neurosci. 23, 131–140. PubMed PMC

Guillaud L., Wong R., Hirokawa N. (2008). Disruption of KIF17-Mint1 interaction by CaMKII-dependent phosphorylation: a molecular model of kinesin-cargo release. Nat. Cell Biol. 10, 19–29. 10.1038/ncb1665 PubMed DOI

Hahn C. G., Wang H. Y., Cho D. S., Talbot K., Gur R. E., Berrettini W. H., et al. . (2006). Altered neuregulin 1-erbB4 signaling contributes to NMDA receptor hypofunction in schizophrenia. Nat. Med. 12, 824–828. 10.1038/nm1418 PubMed DOI

Hansen K. B., Furukawa H., Traynelis S. F. (2010). Control of assembly and function of glutamate receptors by the amino-terminal domain. Mol. Pharmacol. 78, 535–549. 10.1124/mol.110.067157 PubMed DOI PMC

Hanus C., Kochen L., Tom Dieck S., Racine V., Sibarita J. B., Schuman E. M., et al. . (2014). Synaptic control of secretory trafficking in dendrites. Cell Rep. 7, 1771–1778. 10.1016/j.celrep.2014.05.028 PubMed DOI PMC

Hardingham G. E., Bading H. (2010). Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat. Rev. Neurosci. 11, 682–696. 10.1038/nrn2911 PubMed DOI PMC

Harney S. C., Jane D. E., Anwyl R. (2008). Extrasynaptic NR2D-containing NMDARs are recruited to the synapse during LTP of NMDAR-EPSCs. J. Neurosci. 28, 11685–11694. 10.1523/JNEUROSCI.3035-08.2008 PubMed DOI PMC

Harris A. Z., Pettit D. L. (2007). Extrasynaptic and synaptic NMDA receptors form stable and uniform pools in rat hippocampal slices. J. Physiol. 584, 509–519. 10.1113/jphysiol.2007.137679 PubMed DOI PMC

Hatton C. J., Paoletti P. (2005). Modulation of triheteromeric NMDA receptors by N-terminal domain ligands. Neuron 46, 261–274. 10.1016/j.neuron.2005.03.005 PubMed DOI

Hawkins L. M., Prybylowski K., Chang K., Moussan C., Stephenson F. A., Wenthold R. J. (2004). Export from the endoplasmic reticulum of assembled N-methyl-d-aspartic acid receptors is controlled by a motif in the c terminus of the NR2 subunit. J. Biol. Chem. 279, 28903–28910. 10.1074/jbc.m402599200 PubMed DOI

Hedegaard M., Hansen K. B., Andersen K. T., Bräuner-Osborne H., Traynelis S. F. (2012). Molecular pharmacology of human NMDA receptors. Neurochem. Int. 61, 601–609. 10.1016/j.neuint.2011.11.016 PubMed DOI PMC

Horak M., Al-Hallaq R. A., Chang K., Wenthold R. J. (2008a). Role of the fourth membrane domain of the NR2B subunit in the assembly of the NMDA receptor. Channels (Austin) 2, 159–160. 10.4161/chan.2.3.6188 PubMed DOI PMC

Horak M., Chang K., Wenthold R. J. (2008b). Masking of the endoplasmic reticulum retention signals during assembly of the NMDA receptor. J. Neurosci. 28, 3500–3509. 10.1523/JNEUROSCI.5239-07.2008 PubMed DOI PMC

Horak M., Seabold G. K., Petralia R. S. (2014). “Trafficking of glutamate receptors and associated proteins in synaptic plasticity,” in The Synapse: Structure and Function, eds Pickel V., Segal M. (New York: Elsevier; ), 221–279.

Horak M., Wenthold R. J. (2009). Different roles of C-terminal cassettes in the trafficking of full-length NR1 subunits to the cell surface. J. Biol. Chem. 284, 9683–9691. 10.1074/jbc.M807050200 PubMed DOI PMC

Howard M. A., Elias G. M., Elias L. A., Swat W., Nicoll R. A. (2010). The role of SAP97 in synaptic glutamate receptor dynamics. Proc. Natl. Acad. Sci. U S A 107, 3805–3810. 10.1073/pnas.0914422107 PubMed DOI PMC

Hsu S. C., Hazuka C. D., Foletti D. L., Scheller R. H. (1999). Targeting vesicles to specific sites on the plasma membrane: the role of the sec6/8 complex. Trends Cell Biol. 9, 150–153. 10.1016/s0962-8924(99)01516-0 PubMed DOI

Hsu S. C., Ting A. E., Hazuka C. D., Davanger S., Kenny J. W., Kee Y., et al. . (1996). The mammalian brain rsec6/8 complex. Neuron 17, 1209–1219. 10.1016/s0896-6273(00)80251-2 PubMed DOI

Huh K. H., Wenthold R. J. (1999). Turnover analysis of glutamate receptors identifies a rapidly degraded pool of the N-methyl-D-aspartate receptor subunit, NR1, in cultured cerebellar granule cells. J. Biol. Chem. 274, 151–157. 10.1074/jbc.274.1.151 PubMed DOI

Jantzie L. L., Talos D. M., Jackson M. C., Park H.-K., Graham D. A., Lechpammer M., et al. . (2013). Developmental expression of N-methyl-D-aspartate (NMDA) receptor subunits in human white and gray matter: potential mechanism of increased vulnerability in the immature brain. Cereb. Cortex [Epub ahead of print]. 10.1093/cercor/bht246 PubMed DOI PMC

Jeyifous O., Waites C. L., Specht C. G., Fujisawa S., Schubert M., Lin E. I., et al. . (2009). SAP97 and CASK mediate sorting of NMDA receptors through a previously unknown secretory pathway. Nat. Neurosci. 12, 1011–1019. 10.1038/nn.2362 PubMed DOI PMC

Jourdain P., Bergersen L. H., Bhaukaurally K., Bezzi P., Santello M., Domercq M., et al. . (2007). Glutamate exocytosis from astrocytes controls synaptic strength. Nat. Neurosci. 10, 331–339. 10.1038/nn1849 PubMed DOI

Kaniakova M., Krausova B., Vyklicky V., Korinek M., Lichnerova K., Vyklicky L., et al. . (2012a). Key amino acid residues within the third membrane domains of NR1 and NR2 subunits contribute to the regulation of the surface delivery of N-methyl-D-aspartate receptors. J. Biol. Chem. 287, 26423–26434. 10.1074/jbc.M112.339085 PubMed DOI PMC

Kaniakova M., Lichnerova K., Vyklicky L., Horak M. (2012b). Single amino acid residue in the M4 domain of GluN1 subunit regulates the surface delivery of NMDA receptors. J. Neurochem. 123, 385–395. 10.1111/jnc.12002 PubMed DOI

Kapitein L. C., Hoogenraad C. C. (2011). Which way to go? Cytoskeletal organization and polarized transport in neurons. Mol. Cell. Neurosci. 46, 9–20. 10.1016/j.mcn.2010.08.015 PubMed DOI

Karakas E., Furukawa H. (2014). Crystal structure of a heterotetrameric NMDA receptor ion channel. Science 344, 992–997. 10.1126/science.1251915 PubMed DOI PMC

Karpova A., Mikhaylova M., Bera S., Bär J., Reddy P. P., Behnisch T., et al. . (2013). Encoding and transducing the synaptic or extrasynaptic origin of NMDA receptor signals to the nucleus. Cell 152, 1119–1133. 10.1016/j.cell.2013.02.002 PubMed DOI

Kenny A. V., Cousins S. L., Pinho L., Stephenson F. A. (2009). The integrity of the glycine co-agonist binding site of N-methyl-D-aspartate receptors is a functional quality control checkpoint for cell surface delivery. J. Biol. Chem. 284, 324–333. 10.1074/jbc.M804023200 PubMed DOI

Kim E., Cho K. O., Rothschild A., Sheng M. (1996). Heteromultimerization and NMDA receptor-clustering activity of Chapsyn-110, a member of the PSD-95 family of proteins. Neuron 17, 103–113. 10.1016/s0896-6273(00)80284-6 PubMed DOI

Kirson E. D., Schirra C., Konnerth A., Yaari Y. (1999). Early postnatal switch in magnesium sensitivity of NMDA receptors in rat CA1 pyramidal cells. J. Physiol. 521(Pt. 1), 99–111. 10.1111/j.1469-7793.1999.00099.x PubMed DOI PMC

Kornau H. C., Schenker L. T., Kennedy M. B., Seeburg P. H. (1995). Domain interaction between NMDA receptor subunits and the postsynaptic density protein PSD-95. Science 269, 1737–1740. 10.1126/science.7569905 PubMed DOI

Kornau H. C., Seeburg P. H., Kennedy M. B. (1997). Interaction of ion channels and receptors with PDZ domain proteins. Curr. Opin. Neurobiol. 7, 368–373. 10.1016/s0959-4388(97)80064-5 PubMed DOI

Kwon H. B., Castillo P. E. (2008). Long-term potentiation selectively expressed by NMDA receptors at hippocampal mossy fiber synapses. Neuron 57, 108–120. 10.1016/j.neuron.2007.11.024 PubMed DOI PMC

Larsen R. S., Corlew R. J., Henson M. A., Roberts A. C., Mishina M., Watanabe M., et al. . (2011). NR3A-containing NMDARs promote neurotransmitter release and spike timing-dependent plasticity. Nat. Neurosci. 14, 338–344. 10.1038/nn.2750 PubMed DOI PMC

Lau L. F., Mammen A., Ehlers M. D., Kindler S., Chung W. J., Garner C. C., et al. . (1996). Interaction of the N-methyl-D-aspartate receptor complex with a novel synapse-associated protein, SAP102. J. Biol. Chem. 271, 21622–21628. 10.1074/jbc.271.35.21622 PubMed DOI

Lau C. G., Takayasu Y., Rodenas-Ruano A., Paternain A. V., Lerma J., Bennett M. V., et al. . (2010). SNAP-25 is a target of protein kinase C phosphorylation critical to NMDA receptor trafficking. J. Neurosci. 30, 242–254. 10.1523/JNEUROSCI.4933-08.2010 PubMed DOI PMC

Lavezzari G., McCallum J., Dewey C. M., Roche K. W. (2004). Subunit-specific regulation of NMDA receptor endocytosis. J. Neurosci. 24, 6383–6391. 10.1523/jneurosci.1890-04.2004 PubMed DOI PMC

Lee C. H., Lü W., Michel J. C., Goehring A., Du J., Song X., et al. . (2014). NMDA receptor structures reveal subunit arrangement and pore architecture. Nature 511, 191–197. 10.1038/nature13548 PubMed DOI PMC

Lee M. C., Yasuda R., Ehlers M. D. (2010). Metaplasticity at single glutamatergic synapses. Neuron 66, 859–870. 10.1016/j.neuron.2010.05.015 PubMed DOI PMC

Lei S., Czerwinska E., Czerwinski W., Walsh M. P., MacDonald J. F. (2001). Regulation of NMDA receptor activity by F-actin and mysoin light chain kinase. J. Neurosci. 21, 8464–8472. PubMed PMC

Leonard A. S., Davare M. A., Horne M. C., Garner C. C., Hell J. W. (1998). SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J. Biol. Chem. 273, 19518–19524. 10.1074/jbc.273.31.19518 PubMed DOI

Leonoudakis D., Conti L. R., Radeke C. M., McGuire L. M., Vandenberg C. A. (2004). A multiprotein trafficking complex composed of SAP97, CASK, Veli and Mint1 is associated with inward rectifier Kir2 potassium channels. J. Biol. Chem. 279, 19051–19063. 10.1074/jbc.m400284200 PubMed DOI

Li D., Specht C. G., Waites C. L., Butler-Munro C., Leal-Ortiz S., Foote J. W., et al. . (2011). SAP97 directs NMDA receptor spine targeting and synaptic plasticity. J. Physiol. 589, 4491–4510. 10.1113/jphysiol.2011.215566 PubMed DOI PMC

Lin E. I., Jeyifous O., Green W. N. (2013). CASK regulates SAP97 conformation and its interactions with AMPA and NMDA receptors. J. Neurosci. 33, 12067–12076. 10.1523/JNEUROSCI.0816-13.2013 PubMed DOI PMC

Lisé M. F., Wong T. P., Trinh A., Hines R. M., Liu L., Kang R., et al. . (2006). Involvement of myosin Vb in glutamate receptor trafficking. J. Biol. Chem. 281, 3669–3678. 10.1074/jbc.m511725200 PubMed DOI

Liu Y., Wong T. P., Aarts M., Rooyakkers A., Liu L., Lai T. W., et al. . (2007). NMDA receptor subunits have differential roles in mediating excitotoxic neuronal death both in vitro and in vivo. J. Neurosci. 27, 2846–2857. 10.1523/jneurosci.0116-07.2007 PubMed DOI PMC

Losi G., Prybylowski K., Fu Z., Luo J., Wenthold R. J., Vicini S. (2003). PSD-95 regulates NMDA receptors in developing cerebellar granule neurons of the rat. J. Physiol. 548, 21–29. 10.1113/jphysiol.2002.034918 PubMed DOI PMC

Lue R. A., Marfatia S. M., Branton D., Chishti A. H. (1994). Cloning and characterization of hdlg: the human homologue of the Drosophila discs large tumor suppressor binds to protein 4.1. Proc. Natl. Acad. Sci. U S A 91, 9818–9822. 10.1073/pnas.91.21.9818 PubMed DOI PMC

Mao L., Takamiya K., Thomas G., Lin D. T., Huganir R. L. (2010). GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions. Proc. Natl. Acad. Sci. U S A 107, 19038–19043. 10.1073/pnas.1013494107 PubMed DOI PMC

Matsuda K., Fletcher M., Kamiya Y., Yuzaki M. (2003). Specific assembly with the NMDA receptor 3B subunit controls surface expression and calcium permeability of NMDA receptors. J. Neurosci. 23, 10064–10073. PubMed PMC

Matta J. A., Ashby M. C., Sanz-Clemente A., Roche K. W., Isaac J. T. (2011). mGluR5 and NMDA receptors drive the experience- and activity-dependent NMDA receptor NR2B to NR2A subunit switch. Neuron 70, 339–351. 10.1016/j.neuron.2011.02.045 PubMed DOI PMC

Mauceri D., Cattabeni F., Di Luca M., Gardoni F. (2004). Calcium/calmodulin-dependent protein kinase II phosphorylation drives synapse-associated protein 97 into spines. J. Biol. Chem. 279, 23813–23821. 10.1074/jbc.m402796200 PubMed DOI

Mauceri D., Gardoni F., Marcello E., Di Luca M. (2007). Dual role of CaMKII-dependent SAP97 phosphorylation in mediating trafficking and insertion of NMDA receptor subunit NR2A. J. Neurochem. 100, 1032–1046. 10.1111/j.1471-4159.2006.04267.x PubMed DOI

McIlhinney R. A., Le Bourdellès B., Molnár E., Tricaud N., Streit P., Whiting P. J. (1998). Assembly intracellular targeting and cell surface expression of the human N-methyl-D-aspartate receptor subunits NR1a and NR2A in transfected cells. Neuropharmacology 37, 1355–1367. 10.1016/s0028-3908(98)00121-x PubMed DOI

Meddows E., Le Bourdelles B., Grimwood S., Wafford K., Sandhu S., Whiting P., et al. . (2001). Identification of molecular determinants that are important in the assembly of N-methyl-D-aspartate receptors. J. Biol. Chem. 276, 18795–18803. 10.1074/jbc.m101382200 PubMed DOI

Meeker R. B., Swanson D. J., Hayward J. N. (1989). Light and electron microscopic localization of glutamate immunoreactivity in the supraoptic nucleus of the rat hypothalamus. Neuroscience 33, 157–167. 10.1016/0306-4522(89)90318-7 PubMed DOI

Minatohara K., Ichikawa S. H., Seki T., Fujiyoshi Y., Doi T. (2013). Ligand binding of PDZ domains has various roles in the synaptic clustering of SAP102 and PSD-95. Neurosci. Lett. 533, 44–49. 10.1016/j.neulet.2012.11.019 PubMed DOI

Mok H., Shin H., Kim S., Lee J. R., Yoon J., Kim E. (2002). Association of the kinesin superfamily motor protein KIF1Balpha with postsynaptic density-95 (PSD-95), synapse-associated protein-97 and synaptic scaffolding molecule PSD-95/discs large/zona occludens-1 proteins. J. Neurosci. 22, 5253–5258. PubMed PMC

Mu Y., Otsuka T., Horton A. C., Scott D. B., Ehlers M. D. (2003). Activity-dependent mRNA splicing controls ER export and synaptic delivery of NMDA receptors. Neuron 40, 581–594. 10.1016/s0896-6273(03)00676-7 PubMed DOI

Müller B. M., Kistner U., Kindler S., Chung W. J., Kuhlendahl S., Fenster S. D., et al. . (1996). SAP102, a novel postsynaptic protein that interacts with NMDA receptor complexes in vivo. Neuron 17, 255–265. 10.1016/s0896-6273(00)80157-9 PubMed DOI

Müller B. M., Kistner U., Veh R. W., Cases-Langhoff C., Becker B., Gundelfinger E. D., et al. . (1995). Molecular characterization and spatial distribution of SAP97, a novel presynaptic protein homologous to SAP90 and the Drosophila discs-large tumor suppressor protein. J. Neurosci. 15, 2354–2366. PubMed PMC

Nakagawa T., Futai K., Lashuel H. A., Lo I., Okamoto K., Walz T., et al. . (2004). Quaternary structure, protein dynamics and synaptic function of SAP97 controlled by L27 domain interactions. Neuron 44, 453–467. 10.1016/j.neuron.2004.10.012 PubMed DOI

Ng D., Pitcher G. M., Szilard R. K., Sertié A., Kanisek M., Clapcote S. J., et al. . (2009). Neto1 is a novel CUB-domain NMDA receptor-interacting protein required for synaptic plasticity and learning. PLoS Biol. 7:e41. 10.1371/journal.pbio.1000041 PubMed DOI PMC

Niethammer M., Kim E., Sheng M. (1996). Interaction between the C terminus of NMDA receptor subunits and multiple members of the PSD-95 family of membrane-associated guanylate kinases. J. Neurosci. 16, 2157–2163. PubMed PMC

Nilsson A., Eriksson M., Muly E. C., Åkesson E., Samuelsson E.-B., Bogdanovic N., et al. . (2007). Analysis of NR3A receptor subunits in human native NMDA receptors. Brain Res. 1186, 102–112. 10.1016/j.brainres.2007.09.008 PubMed DOI

Okabe S., Miwa A., Okado H. (1999). Alternative splicing of the C-terminal domain regulates cell surface expression of the NMDA receptor NR1 subunit. J. Neurosci. 19, 7781–7792. PubMed PMC

Oshima S., Fukaya M., Masabumi N., Shirakawa T., Oguchi H., Watanabe M. (2002). Early onset of NMDA receptor GluRε1 (NR2A) expression and its abundant postsynaptic localization in developing motoneurons of the mouse hypoglossal nucleus. Neurosci. Res. 43, 239–250. 10.1016/s0168-0102(02)00035-4 PubMed DOI

Osterweil E., Wells D. G., Mooseker M. S. (2005). A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J. Cell Biol. 168, 329–338. 10.1083/jcb.200410091 PubMed DOI PMC

Ozaki M., Sasner M., Yano R., Lu H. S., Buonanno A. (1997). Neuregulin-beta induces expression of an NMDA-receptor subunit. Nature 390, 691–694. PubMed

Pabba M., Wong A. Y., Ahlskog N., Hristova E., Biscaro D., Nassrallah W., et al. . (2014). NMDA receptors are upregulated and trafficked to the plasma membrane after Sigma-1 receptor activation in the rat hippocampus. J. Neurosci. 34, 11325–11338. 10.1523/JNEUROSCI.0458-14.2014 PubMed DOI PMC

Paoletti P. (2011). Molecular basis of NMDA receptor functional diversity. Eur. J. Neurosci. 33, 1351–1365. 10.1111/j.1460-9568.2011.07628.x PubMed DOI

Paoletti P., Bellone C., Zhou Q. (2013). NMDA receptor subunit diversity: impact on receptor properties, synaptic plasticity and disease. Nat. Rev. Neurosci. 14, 383–400. 10.1038/nrn3504 PubMed DOI

Papadakis M., Hawkins L. M., Stephenson F. A. (2004). Appropriate NR1-NR1 disulfide-linked homodimer formation is requisite for efficient expression of functional, cell surface N-methyl-D-aspartate NR1/NR2 receptors. J. Biol. Chem. 279, 14703–14712. 10.1074/jbc.m313446200 PubMed DOI

Papouin T., Ladépêche L., Ruel J., Sacchi S., Labasque M., Hanini M., et al. . (2012). Synaptic and extrasynaptic NMDA receptors are gated by different endogenous coagonists. Cell 150, 633–646. 10.1016/j.cell.2012.06.029 PubMed DOI

Parsons M. P., Raymond L. A. (2014). Extrasynaptic NMDA receptor involvement in central nervous system disorders. Neuron 82, 279–293. 10.1016/j.neuron.2014.03.030 PubMed DOI

Peng Y., Zhao J., Gu Q. H., Chen R. Q., Xu Z., Yan J. Z., et al. . (2010). Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses. Hippocampus 20, 646–658. 10.1002/hipo.20654 PubMed DOI

Penn A. C., Williams S. R., Greger I. H. (2008). Gating motions underlie AMPA receptor secretion from the endoplasmic reticulum. EMBO J. 27, 3056–3068. 10.1038/emboj.2008.222 PubMed DOI PMC

Pérez-Otaño I., Luján R., Tavalin S. J., Plomann M., Modregger J., Liu X. B., et al. . (2006). Endocytosis and synaptic removal of NR3A-containing NMDA receptors by PACSIN1/syndapin1. Nat. Neurosci. 9, 611–621. 10.1038/nn1680 PubMed DOI PMC

Perez-Otano I., Schulteis C. T., Contractor A., Lipton S. A., Trimmer J. S., Sucher N. J., et al. . (2001). Assembly with the NR1 subunit is required for surface expression of NR3A-containing NMDA receptors. J. Neurosci. 21, 1228–1237. PubMed PMC

Petralia R. S. (2012). Distribution of extrasynaptic NMDA receptors on neurons. ScientificWorldJournal 2012:267120. 10.1100/2012/267120 PubMed DOI PMC

Petralia R. S., Al-Hallaq R. A., Wenthold R. J. (2009). “Trafficking and targeting of NMDA receptors,” in Biology of the NMDA Receptor, ed Van Dongen A. M. (Boca Raton, FL: Taylor and Francis Group; ), 149–200. PubMed

Petralia R. S., Sans N., Wang Y. X., Wenthold R. J. (2005). Ontogeny of postsynaptic density proteins at glutamatergic synapses. Mol. Cell. Neurosci. 29, 436–452. 10.1016/j.mcn.2005.03.013 PubMed DOI PMC

Petralia R. S., Wang Y. X., Hua F., Yi Z., Zhou A., Ge L., et al. . (2010). Organization of NMDA receptors at extrasynaptic locations. Neuroscience 167, 68–87. 10.1016/j.neuroscience.2010.01.022 PubMed DOI PMC

Petralia R. S., Wang Y. X., Wenthold R. J. (2002). NMDA receptors and PSD-95 are found in attachment plaques in cerebellar granular layer glomeruli. Eur. J. Neurosci. 15, 583–587. 10.1046/j.1460-9568.2002.01896.x PubMed DOI

Petralia R. S., Wang Y. X., Wenthold R. J. (2003). Internalization at glutamatergic synapses during development. Eur. J. Neurosci. 18, 3207–3217. 10.1111/j.1460-9568.2003.03074.x PubMed DOI

Petralia R. S., Wenthold R. J. (2008). “NMDA receptors,” in The Glutamate Receptors, eds Gereau R. W., Swanson G. T. (Totowa, NJ: Humana Press; ), 45–98.

Piguel N. H., Fievre S., Blanc J.-M., Carta M., Moreau M. M., Moutin E., et al. . (2014). Scribble1/AP2 complex coordinates NMDA receptor endocytic recycling. Cell Rep. [Epub ahead of print]. S2211-1247(14)00785-2. 10.1016/j.celrep.2014.09.017 PubMed DOI

Priel A., Selak S., Lerma J., Stern-Bach Y. (2006). Block of kainate receptor desensitization uncovers a key trafficking checkpoint. Neuron 52, 1037–1046. 10.1016/j.neuron.2006.12.006 PubMed DOI

Prybylowski K., Chang K., Sans N., Kan L., Vicini S., Wenthold R. J. (2005). The synaptic localization of NR2B-containing NMDA receptors is controlled by interactions with PDZ proteins and AP-2. Neuron 47, 845–857. 10.1016/j.neuron.2005.08.016 PubMed DOI PMC

Qiu S., Hua Y. L., Yang F., Chen Y. Z., Luo J. H. (2005). Subunit assembly of N-methyl-d-aspartate receptors analyzed by fluorescence resonance energy transfer. J. Biol. Chem. 280, 24923–24930. 10.1074/jbc.m413915200 PubMed DOI

Qiu S., Zhang X. M., Cao J. Y., Yang W., Yan Y. G., Shan L., et al. . (2009). An endoplasmic reticulum retention signal located in the extracellular amino-terminal domain of the NR2A subunit of N-Methyl-D-aspartate receptors. J. Biol. Chem. 284, 20285–20298. 10.1074/jbc.M109.004960 PubMed DOI PMC

Quinlan E. M., Olstein D. H., Bear M. F. (1999a). Bidirectional, experience-dependent regulation of N-methyl-D-aspartate receptor subunit composition in the rat visual cortex during postnatal development. Proc. Natl. Acad. Sci. U S A 96, 12876–12880. 10.1073/pnas.96.22.12876 PubMed DOI PMC

Quinlan E. M., Philpot B. D., Huganir R. L., Bear M. F. (1999b). Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 2, 352–357. 10.1038/7263 PubMed DOI

Rácz B., Blanpied T. A., Ehlers M. D., Weinberg R. J. (2004). Lateral organization of endocytic machinery in dendritic spines. Nat. Neurosci. 7, 917–918. 10.1038/nn1303 PubMed DOI

Rebola N., Srikumar B. N., Mulle C. (2010). Activity-dependent synaptic plasticity of NMDA receptors. J. Physiol. 588, 93–99. 10.1113/jphysiol.2009.179382 PubMed DOI PMC

Riefler G. M., Balasingam G., Lucas K. G., Wang S., Hsu S. C., Firestein B. L. (2003). Exocyst complex subunit sec8 binds to postsynaptic density protein-95 (PSD-95): a novel interaction regulated by cypin (cytosolic PSD-95 interactor). Biochem. J. 373, 49–55. 10.1042/bj20021838 PubMed DOI PMC

Roberts A. C., Díez-Garcia J., Rodriguiz R. M., López I. P., Luján R., Martínez-Turrillas R., et al. . (2009). Downregulation of NR3A-containing NMDARs is required for synapse maturation and memory consolidation. Neuron 63, 342–356. 10.1016/j.neuron.2009.06.016 PubMed DOI PMC

Roche K. W., Standley S., McCallum J., Dune Ly C., Ehlers M. D., Wenthold R. J. (2001). Molecular determinants of NMDA receptor internalization. Nat. Neurosci. 4, 794–802. 10.1038/90498 PubMed DOI

Rodenas-Ruano A., Chávez A. E., Cossio M. J., Castillo P. E., Zukin R. S. (2012). REST-dependent epigenetic remodeling promotes the developmental switch in synaptic NMDA receptors. Nat. Neurosci. 15, 1382–1390. 10.1038/nn.3214 PubMed DOI PMC

Salussolia C. L., Corrales A., Talukder I., Kazi R., Akgul G., Bowen M., et al. . (2011). Interaction of the M4 segment with other transmembrane segments is required for surface expression of mammalian AMPA receptors. J. Biol. Chem. 286, 40205–40218. 10.1074/jbc.m111.268839 PubMed DOI PMC

Salussolia C. L., Gan Q., Kazi R., Singh P., Allopenna J., Furukawa H., et al. . (2013). A eukaryotic specific transmembrane segment is required for tetramerization in AMPA receptors. J. Neurosci. 33, 9840–9845. 10.1523/JNEUROSCI.2626-12.2013 PubMed DOI PMC

Sans N., Petralia R. S., Wang Y. X., Blahos J., 2nd, Hell J. W., Wenthold R. J. (2000). A developmental change in NMDA receptor-associated proteins at hippocampal synapses. J. Neurosci. 20, 1260–1271. PubMed PMC

Sans N., Prybylowski K., Petralia R. S., Chang K., Wang Y. X., Racca C., et al. . (2003). NMDA receptor trafficking through an interaction between PDZ proteins and the exocyst complex. Nat. Cell Biol. 5, 520–530. 10.1038/ncb990 PubMed DOI

Sans N., Racca C., Petralia R. S., Wang Y. X., McCallum J., Wenthold R. J. (2001). Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J. Neurosci. 21, 7506–7516. PubMed PMC

Sans N., Wang P. Y., Du Q., Petralia R. S., Wang Y. X., Nakka S., et al. . (2005). mPins modulates PSD-95 and SAP102 trafficking and influences NMDA receptor surface expression. Nat. Cell Biol. 7, 1179–1190. 10.1038/ncb1325 PubMed DOI

Sanz-Clemente A., Gray J. A., Ogilvie K. A., Nicoll R. A., Roche K. W. (2013a). Activated CaMKII couples GluN2B and casein kinase 2 to control synaptic NMDA receptors. Cell Rep. 3, 607–614. 10.1016/j.celrep.2013.02.011 PubMed DOI PMC

Sanz-Clemente A., Matta J. A., Isaac J. T., Roche K. W. (2010). Casein kinase 2 regulates the NR2 subunit composition of synaptic NMDA receptors. Neuron 67, 984–996. 10.1016/j.neuron.2010.08.011 PubMed DOI PMC

Sanz-Clemente A., Nicoll R. A., Roche K. W. (2013b). Diversity in NMDA receptor composition: many regulators, many consequences. Neuroscientist 19, 62–75. 10.1177/1073858411435129 PubMed DOI PMC

Schlüter O. M., Xu W., Malenka R. C. (2006). Alternative N-terminal domains of PSD-95 and SAP97 govern activity-dependent regulation of synaptic AMPA receptor function. Neuron 51, 99–111. 10.1016/j.neuron.2006.05.016 PubMed DOI

Schorge S., Colquhoun D. (2003). Studies of NMDA receptor function and stoichiometry with truncated and tandem subunits. J. Neurosci. 23, 1151–1158. PubMed PMC

Schüler T., Mesic I., Madry C., Bartholomäus I., Laube B. (2008). Formation of NR1/NR2 and NR1/NR3 heterodimers constitutes the initial step in N-methyl-D-aspartate receptor assembly. J. Biol. Chem. 283, 37–46. 10.1074/jbc.m703539200 PubMed DOI

Scott D. B., Blanpied T. A., Swanson G. T., Zhang C., Ehlers M. D. (2001). An NMDA receptor ER retention signal regulated by phosphorylation and alternative splicing. J. Neurosci. 21, 3063–3072. PubMed PMC

Seaman M. N., Gautreau A., Billadeau D. D. (2013). Retromer-mediated endosomal protein sorting: all WASHed up! Trends Cell Biol. 23, 522–528. 10.1016/j.tcb.2013.04.010 PubMed DOI PMC

Setou M., Nakagawa T., Seog D. H., Hirokawa N. (2000). Kinesin superfamily motor protein KIF17 and mLin-10 in NMDA receptor-containing vesicle transport. Science 288, 1796–1802. 10.1126/science.288.5472.1796 PubMed DOI

She K., Ferreira J. S., Carvalho A. L., Craig A. M. (2012). Glutamate binding to the GluN2B subunit controls surface trafficking of N-methyl-D-aspartate (NMDA) receptors. J. Biol. Chem. 287, 27432–27445. 10.1074/jbc.M112.345108 PubMed DOI PMC

Sheng M. (1996). PDZs and receptor/channel clustering: rounding up the latest suspects. Neuron 17, 575–578. 10.1016/s0896-6273(00)80190-7 PubMed DOI

Sheng M., Cummings J., Roldan L. A., Jan Y. N., Jan L. Y. (1994). Changing subunit composition of heteromeric NMDA receptors during development of rat cortex. Nature 368, 144–147. 10.1038/368144a0 PubMed DOI

Sheng M., Kim E. (1996). Ion channel associated proteins. Curr. Opin. Neurobiol. 6, 602–608. 10.1016/s0959-4388(96)80091-2 PubMed DOI

Shinohara Y., Hirase H., Watanabe M., Itakura M., Takahashi M., Shigemoto R. (2008). Left-right asymmetry of the hippocampal synapses with differential subunit allocation of glutamate receptors. Proc. Natl. Acad. Sci. U S A 105, 19498–19503. 10.1073/pnas.0807461105 PubMed DOI PMC

Siegler Retchless B., Gao W., Johnson J. W. (2012). A single GluN2 subunit residue controls NMDA receptor channel properties via intersubunit interaction. Nat. Neurosci. 15, 406–413. 10.1038/nn.3025 PubMed DOI PMC

Songyang Z., Fanning A. S., Fu C., Xu J., Marfatia S. M., Chishti A. H., et al. . (1997). Recognition of unique carboxyl-terminal motifs by distinct PDZ domains. Science 275, 73–77. 10.1126/science.275.5296.73 PubMed DOI

Standley S., Petralia R. S., Gravell M., Hamilton R., Wang Y. X., Schubert M., et al. . (2012). Trafficking of the NMDAR2B receptor subunit distal cytoplasmic tail from endoplasmic reticulum to the synapse. PLoS One 7:e39585. 10.1371/journal.pone.0039585 PubMed DOI PMC

Standley S., Roche K. W., McCallum J., Sans N., Wenthold R. J. (2000). PDZ domain suppression of an ER retention signal in NMDA receptor NR1 splice variants. Neuron 28, 887–898. 10.1016/s0896-6273(00)00161-6 PubMed DOI

Suh Y. H., Terashima A., Petralia R. S., Wenthold R. J., Isaac J. T., Roche K. W., et al. . (2010). A neuronal role for SNAP-23 in postsynaptic glutamate receptor trafficking. Nat. Neurosci. 13, 338–343. 10.1038/nn.2488 PubMed DOI PMC

Swanwick C. C., Shapiro M. E., Yi Z., Chang K., Wenthold R. J. (2009). NMDA receptors interact with flotillin-1 and -2, lipid raft-associated proteins. FEBS Lett. 583, 1226–1230. 10.1016/j.febslet.2009.03.017 PubMed DOI

Tall G. G., Gilman A. G. (2005). Resistance to inhibitors of cholinesterase 8A catalyzes release of Galphai-GTP and nuclear mitotic apparatus protein (NuMA) from NuMA/LGN/Galphai-GDP complexes. Proc. Natl. Acad. Sci. U S A 102, 16584–16589. 10.1073/pnas.0508306102 PubMed DOI PMC

Thomas C. G., Miller A. J., Westbrook G. L. (2006). Synaptic and extrasynaptic NMDA receptor NR2 subunits in cultured hippocampal neurons. J. Neurophysiol. 95, 1727–1734. 10.1152/jn.00771.2005 PubMed DOI

Tovar K. R., McGinley M. J., Westbrook G. L. (2013). Triheteromeric NMDA receptors at hippocampal synapses. J. Neurosci. 33, 9150–9160. 10.1523/JNEUROSCI.0829-13.2013 PubMed DOI PMC

Tovar K. R., Westbrook G. L. (1999). The incorporation of NMDA receptors with a distinct subunit composition at nascent hippocampal synapses in vitro. J. Neurosci. 19, 4180–4188. PubMed PMC

Tovar K. R., Westbrook G. L. (2002). Mobile NMDA receptors at hippocampal synapses. Neuron 34, 255–264. 10.1016/s0896-6273(02)00658-x PubMed DOI

Traynelis S. F., Wollmuth L. P., McBain C. J., Menniti F. S., Vance K. M., Ogden K. K., et al. . (2010). Glutamate receptor ion channels: structure, regulation and function. Pharmacol. Rev. 62, 405–496. 10.1124/pr.109.002451 PubMed DOI PMC

Vissel B., Krupp J. J., Heinemann S. F., Westbrook G. L. (2001). A use-dependent tyrosine dephosphorylation of NMDA receptors is independent of ion flux. Nat. Neurosci. 4, 587–596. 10.1038/88404 PubMed DOI

Wang P. Y., Petralia R. S., Wang Y. X., Wenthold R. J., Brenowitz S. D. (2011). Functional NMDA receptors at axonal growth cones of young hippocampal neurons. J. Neurosci. 31, 9289–9297. 10.1523/JNEUROSCI.5639-10.2011 PubMed DOI PMC

Wang X., Zhao Y., Zhang X., Badie H., Zhou Y., Mu Y., et al. . (2013). Loss of sorting nexin 27 contributes to excitatory synaptic dysfunction by modulating glutamate receptor recycling in down’s syndrome. Nat. Med. 19, 473–480. 10.1038/nm.3117 PubMed DOI PMC

Washbourne P., Bennett J. E., McAllister A. K. (2002). Rapid recruitment of NMDA receptor transport packets to nascent synapses. Nat. Neurosci. 5, 751–759. 10.1038/nn883 PubMed DOI

Washbourne P., Liu X. B., Jones E. G., McAllister A. K. (2004). Cycling of NMDA receptors during trafficking in neurons before synapse formation. J. Neurosci. 24, 8253–8264. 10.1523/jneurosci.2555-04.2004 PubMed DOI PMC

Wenthold R. J., Prybylowski K., Standley S., Sans N., Petralia R. S. (2003). Trafficking of NMDA receptors. Annu. Rev. Pharmacol. Toxicol. 43, 335–358. 10.1146/annurev.pharmtox.43.100901.135803 PubMed DOI

Wong H. K., Liu X. B., Matos M. F., Chan S. F., Pérez-Otaño I., Boysen M., et al. . (2002). Temporal and regional expression of NMDA receptor subunit NR3A in the mammalian brain. J. Comp. Neurol. 450, 303–317. 10.1002/cne.10314 PubMed DOI

Wu H., Nash J. E., Zamorano P., Garner C. C. (2002). Interaction of SAP97 with minus-end-directed actin motor myosin VI. Implications for AMPA receptor trafficking. J. Biol. Chem. 277, 30928–30934. 10.1074/jbc.m203735200 PubMed DOI

Wyeth M. S., Pelkey K. A., Petralia R. S., Salter M. W., McInnes R. R., McBain C. J. (2014). Neto auxiliary protein interactions regulate kainate and NMDA receptor subunit localization at mossy fiber-CA3 pyramidal cell synapses. J. Neurosci. 34, 622–628. 10.1523/JNEUROSCI.3098-13.2014 PubMed DOI PMC

Xu Z., Chen R. Q., Gu Q. H., Yan J. Z., Wang S. H., Liu S. Y., et al. . (2009). Metaplastic regulation of long-term potentiation/long-term depression threshold by activity-dependent changes of NR2A/NR2B ratio. J. Neurosci. 29, 8764–8773. 10.1523/JNEUROSCI.1014-09.2009 PubMed DOI PMC

Yang W., Zheng C., Song Q., Yang X., Qiu S., Liu C., et al. . (2007). A three amino acid tail following the TM4 region of the N-methyl-D-aspartate receptor (NR) 2 subunits is sufficient to overcome endoplasmic reticulum retention of NR1–1a subunit. J. Biol. Chem. 282, 9269–9278. 10.1074/jbc.m700050200 PubMed DOI

Yashiro K., Corlew R., Philpot B. D. (2005). Visual deprivation modifies both presynaptic glutamate release and the composition of perisynaptic/extrasynaptic NMDA receptors in adult visual cortex. J. Neurosci. 25, 11684–11692. 10.1523/jneurosci.4362-05.2005 PubMed DOI PMC

Yi Z., Petralia R. S., Fu Z., Swanwick C. C., Wang Y. X., Prybylowski K., et al. . (2007). The role of the PDZ protein GIPC in regulating NMDA receptor trafficking. J. Neurosci. 27, 11663–11675. 10.1523/jneurosci.3252-07.2007 PubMed DOI PMC

Yin X., Takei Y., Kido M. A., Hirokawa N. (2011). Molecular motor KIF17 is fundamental for memory and learning via differential support of synaptic NR2A/2B levels. Neuron 70, 310–325. 10.1016/j.neuron.2011.02.049 PubMed DOI

Yoshii A., Sheng M. H., Constantine-Paton M. (2003). Eye opening induces a rapid dendritic localization of PSD-95 in central visual neurons. Proc. Natl. Acad. Sci. U S A 100, 1334–1339. 10.1073/pnas.0335785100 PubMed DOI PMC

Yuan T., Mameli M., O’Connor E. C., Dey P. N., Verpelli C., Sala C., et al. . (2013). Expression of cocaine-evoked synaptic plasticity by GluN3A-containing NMDA receptors. Neuron 80, 1025–1038. 10.1016/j.neuron.2013.07.050 PubMed DOI

Zhang J., Diamond J. S. (2009). Subunit- and pathway-specific localization of NMDA receptors and scaffolding proteins at ganglion cell synapses in rat retina. J. Neurosci. 29, 4274–4286. 10.1523/JNEUROSCI.5602-08.2009 PubMed DOI PMC

Zhao J., Peng Y., Xu Z., Chen R. Q., Gu Q. H., Chen Z., et al. . (2008). Synaptic metaplasticity through NMDA receptor lateral diffusion. J. Neurosci. 28, 3060–3070. 10.1523/JNEUROSCI.5450-07.2008 PubMed DOI PMC

Zheng C. Y., Petralia R. S., Wang Y. X., Kachar B., Wenthold R. J. (2010). SAP102 is a highly mobile MAGUK in spines. J. Neurosci. 30, 4757–4766. 10.1523/JNEUROSCI.6108-09.2010 PubMed DOI PMC

Zheng C. Y., Seabold G. K., Horak M., Petralia R. S. (2011). MAGUKs, synaptic development and synaptic plasticity. Neuroscientist 17, 493–512. 10.1177/1073858410386384 PubMed DOI PMC

Characterization of Mice Carrying a Neurodevelopmental Disease-Associated GluN2B(L825V) Variant

Subunit-Dependent Surface Mobility and Localization of NMDA Receptors in Hippocampal Neurons Measured Using Nanobody Probes

The Extracellular Domains of GluN Subunits Play an Essential Role in Processing NMDA Receptors in the ER

The pathogenic S688Y mutation in the ligand-binding domain of the GluN1 subunit regulates the properties of NMDA receptors

Structural features in the glycine-binding sites of the GluN1 and GluN3A subunits regulate the surface delivery of NMDA receptors

N-Glycosylation Regulates the Trafficking and Surface Mobility of GluN3A-Containing NMDA Receptors