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The Journal of Neuroscience, October 1, 2000, 20(19):7258-7267

Phosphorylation of the AMPA Receptor Subunit GluR2 Differentially Regulates Its Interaction with PDZ Domain-Containing Proteins

Hee Jung Chung, Jun Xia, Robert H. Scannevin, Xiaoqun Zhang, and Richard L. Huganir

Department of Neuroscience, Howard Hughes Medical Institute, Johns Hopkins University School of Medicine, Baltimore, Maryland 21205

PSD-95, DLG, ZO-1 (PDZ) domain-mediated protein interactions have been shown to play important roles in the regulation of glutamate receptor function at excitatory synapses. Recent studies demonstrating the rapid regulation of AMPA receptor function during synaptic plasticity have suggested that AMPA receptor interaction with PDZ domain-containing proteins may be dynamically modulated. Here we show that PKC phosphorylation of the AMPA receptor GluR2 subunit differentially modulates its interaction with the PDZ domain-containing proteins GRIP1 and PICK1. The serine residue [serine-880 (Ser880)] in the GluR2 C-terminal sequence (IESVKI) critical for PDZ domain binding is a substrate of PKC and is phosphorylated in vivo. In vitro binding and coimmunoprecipitation studies show that phosphorylation of serine-880 within the GluR2 PDZ ligand significantly decreases GluR2 binding to GRIP1 but not to PICK1. Immunostaining of cultured hippocampal neurons demonstrates that the Ser880-phosphorylated GluR2 subunits are enriched and colocalized with PICK1 in the dendrites, with very little staining observed at excitatory synapses. Interestingly, PKC activation in neurons increases the Ser880 phosphorylation of GluR2 subunits and recruits PICK1 to excitatory synapses. Moreover, PKC stimulation in neurons results in rapid internalization of surface GluR2 subunits. These results suggest that GluR2 phosphorylation of serine-880 may be important in the regulation of the AMPA receptor internalization during synaptic plasticity.

Key words: GRIP1; PICK1; AMPA receptor; phosphorylation; PKC; PDZ domain


Copyright © 2000 Society for Neuroscience  0270-6474/00/20197258-10$05.00/0


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J. Fu, S. deSouza, and E. B. Ziff
Intracellular Membrane Targeting and Suppression of Ser880 Phosphorylation of Glutamate Receptor 2 by the Linker I-Set II Domain of AMPA Receptor-Binding Protein
J. Neurosci., August 20, 2003; 23(20): 7592 - 7601.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
V. Raghuram, H. Hormuth, and J. K. Foskett
A kinase-regulated mechanism controls CFTR channel gating by disrupting bivalent PDZ domain interactions
PNAS, August 5, 2003; 100(16): 9620 - 9625.
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J. Biol. Chem.Home page
A. Perron, Z.-g. Chen, D. Gingras, D. J. Dupre, J. Stankova, and M. Rola-Pleszczynski
Agonist-independent Desensitization and Internalization of the Human Platelet-activating Factor Receptor by Coumermycin-Gyrase B-induced Dimerization
J. Biol. Chem., July 18, 2003; 278(30): 27956 - 27965.
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ScienceHome page
H. J. Chung, J. P. Steinberg, R. L. Huganir, and D. J. Linden
Requirement of AMPA Receptor GluR2 Phosphorylation for Cerebellar Long-Term Depression
Science, June 13, 2003; 300(5626): 1751 - 1755.
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J. Biol. Chem.Home page
L. L. Parker, J. R. Backstrom, E. Sanders-Bush, and B.-H. Shieh
Agonist-induced Phosphorylation of the Serotonin 5-HT2C Receptor Regulates Its Interaction with Multiple PDZ Protein 1
J. Biol. Chem., June 6, 2003; 278(24): 21576 - 21583.
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Proc. Natl. Acad. Sci. USAHome page
W. Deng, P. A. Rosenberg, J. J. Volpe, and F. E. Jensen
Calcium-permeable AMPA/kainate receptors mediate toxicity and preconditioning by oxygen-glucose deprivation in oligodendrocyte precursors
PNAS, May 27, 2003; 100(11): 6801 - 6806.
[Abstract] [Full Text] [PDF]


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DevelopmentHome page
K. Beumer, H. J. G. Matthies, A. Bradshaw, and K. Broadie
Integrins regulate DLG/FAS2 via a CaM kinase II-dependent pathway to mediate synapse elaboration and stabilization during postembryonic development
Development, March 9, 2003; 129(14): 3381 - 3391.
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J. Biol. Chem.Home page
S. S. Correia, C. B. Duarte, C. J. Faro, E. V. Pires, and A. L. Carvalho
Protein Kinase Cgamma Associates Directly with the GluR4 alpha -Amino-3-hydroxy-5-methyl-4-isoxazole Propionate Receptor Subunit. EFFECT ON RECEPTOR PHOSPHORYLATION
J. Biol. Chem., February 14, 2003; 278(8): 6307 - 6313.
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J. Neurosci.Home page
W.-M. Zho, J.-L. You, C.-C. Huang, and K.-S. Hsu
The Group I Metabotropic Glutamate Receptor Agonist (S)-3,5-Dihydroxyphenylglycine Induces a Novel Form of Depotentiation in the CA1 Region of the Hippocampus
J. Neurosci., October 15, 2002; 22(20): 8838 - 8849.
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Mol. Pharmacol.Home page
M. I. Gonzalez, M. G. Kazanietz, and M. B. Robinson
Regulation of the Neuronal Glutamate Transporter Excitatory Amino Acid Carrier-1 (EAAC1) by Different Protein Kinase C Subtypes
Mol. Pharmacol., October 1, 2002; 62(4): 901 - 910.
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Circ. Res.Home page
J. Zhou, H.-G. Shin, J. Yi, W. Shen, C. P. Williams, and K. T. Murray
Phosphorylation and Putative ER Retention Signals Are Required for Protein Kinase A-Mediated Potentiation of Cardiac Sodium Current
Circ. Res., September 20, 2002; 91(6): 540 - 546.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
Lisa. L. Gomez, S. Alam, K. E. Smith, E. Horne, and M. L. Dell'Acqua
Regulation of A-Kinase Anchoring Protein 79/150-cAMP-Dependent Protein Kinase Postsynaptic Targeting by NMDA Receptor Activation of Calcineurin and Remodeling of Dendritic Actin
J. Neurosci., August 15, 2002; 22(16): 7027 - 7044.
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J. Neurosci.Home page
D. M. Chetkovich, L. Chen, T. J. Stocker, R. A. Nicoll, and D. S. Bredt
Phosphorylation of the Postsynaptic Density-95 (PSD-95)/Discs Large/Zona Occludens-1 Binding Site of Stargazin Regulates Binding to PSD-95 and Synaptic Targeting of AMPA Receptors
J. Neurosci., July 15, 2002; 22(14): 5791 - 5796.
[Abstract] [Full Text] [PDF]


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ScienceHome page
A. Contractor, C. Rogers, C. Maron, M. Henkemeyer, G. T. Swanson, and S. F. Heinemann
Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP
Science, June 7, 2002; 296(5574): 1864 - 1869.
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Proc. Natl. Acad. Sci. USAHome page
S. P. Braithwaite, H. Xia, and R. C. Malenka
Differential roles for NSF and GRIP/ABP in AMPA receptor cycling
PNAS, May 14, 2002; 99(10): 7096 - 7101.
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J. Biol. Chem.Home page
H. Hirbec, O. Perestenko, A. Nishimune, G. Meyer, S. Nakanishi, J. M. Henley, and K. K. Dev
The PDZ Proteins PICK1, GRIP, and Syntenin Bind Multiple Glutamate Receptor Subtypes. ANALYSIS OF PDZ BINDING MOTIFS
J. Biol. Chem., May 3, 2002; 277(18): 15221 - 15224.
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J. Neurosci.Home page
S. DeSouza, J. Fu, B. A. States, and E. B. Ziff
Differential Palmitoylation Directs the AMPA Receptor-Binding Protein ABP to Spines or to Intracellular Clusters
J. Neurosci., May 1, 2002; 22(9): 3493 - 3503.
[Abstract] [Full Text] [PDF]


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NeuroscientistHome page
E. Molnar, L. Pickard, and J. K. Duckworth
Book Review: Developmental Changes in Ionotropic Glutamate Receptors: Lessons from Hippocampal Synapses
Neuroscientist, April 1, 2002; 8(2): 143 - 153.
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J. Neurosci.Home page
D. K. Fong, A. Rao, F. T. Crump, and A. M. Craig
Rapid Synaptic Remodeling by Protein Kinase C: Reciprocal Translocation of NMDA Receptors and Calcium/Calmodulin-Dependent Kinase II
J. Neurosci., March 15, 2002; 22(6): 2153 - 2164.
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J. Biol. Chem.Home page
A. Y. Hung and M. Sheng
PDZ Domains: Structural Modules for Protein Complex Assembly
J. Biol. Chem., February 15, 2002; 277(8): 5699 - 5702.
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J. Biol. Chem.Home page
J. Cheng, B. D. Moyer, M. Milewski, J. Loffing, M. Ikeda, J. E. Mickle, G. R. Cutting, M. Li, B. A. Stanton, and W. B. Guggino
A Golgi-associated PDZ Domain Protein Modulates Cystic Fibrosis Transmembrane Regulator Plasma Membrane Expression
J. Biol. Chem., January 25, 2002; 277(5): 3520 - 3529.
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J. Biol. Chem.Home page
Q. Zhang, J.-S. Fan, and M. Zhang
Interdomain Chaperoning between PSD-95, Dlg, and Zo-1 (PDZ) Domains of Glutamate Receptor-interacting Proteins
J. Biol. Chem., November 9, 2001; 276(46): 43216 - 43220.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
D. J. Linden
The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance
PNAS, November 9, 2001; (2001) 241384598.
[Abstract] [Full Text] [PDF]


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Mol. Pharmacol.Home page
S. H. S. Lin, A. C. Arai, Z. Wang, H.-P. Nothacker, and O. Civelli
The Carboxyl Terminus of the Prolactin-Releasing Peptide Receptor Interacts with PDZ Domain Proteins Involved in alpha -Amino-3-hydroxy-5-methylisoxazole-4-propionic Acid Receptor Clustering
Mol. Pharmacol., November 1, 2001; 60(5): 916 - 923.
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J. Biol. Chem.Home page
Y. Iwakura, T. Nagano, M. Kawamura, H. Horikawa, K. Ibaraki, N. Takei, and H. Nawa
N-Methyl-D-aspartate-induced alpha -Amino-3-hydroxy-5-methyl-4-isoxazoleproprionic Acid (AMPA) Receptor Down-regulation Involves Interaction of the Carboxyl Terminus of GluR2/3 with Pick1. LIGAND-BINDING STUDIES USING Sindbis VECTORS CARRYING AMPA RECEPTOR DECOYS
J. Biol. Chem., October 19, 2001; 276(43): 40025 - 40032.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
C.-H. Kim, H. J. Chung, H.-K. Lee, and R. L. Huganir
Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression
PNAS, September 25, 2001; 98(20): 11725 - 11730.
[Abstract] [Full Text] [PDF]


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J. Neurosci.Home page
J. L. Perez, L. Khatri, C. Chang, S. Srivastava, P. Osten, and E. B. Ziff
PICK1 Targets Activated Protein Kinase C{alpha} to AMPA Receptor Clusters in Spines of Hippocampal Neurons and Reduces Surface Levels of the AMPA-Type Glutamate Receptor Subunit 2
J. Neurosci., August 1, 2001; 21(15): 5417 - 5428.
[Abstract] [Full Text] [PDF]


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Physiol. Rev.Home page
M. Ito
Cerebellar Long-Term Depression: Characterization, Signal Transduction, and Functional Roles
Physiol Rev, July 1, 2001; 81(3): 1143 - 1195.
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Proc. Natl. Acad. Sci. USAHome page
M. Sheng
Molecular organization of the postsynaptic specialization
PNAS, June 19, 2001; 98(13): 7058 - 7061.
[Abstract] [Full Text] [PDF]


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JCBHome page
S. Tomita, R. A. Nicoll, and D. S. Bredt
PDZ Protein Interactions Regulating Glutamate Receptor Function and Plasticity
J. Cell Biol., May 28, 2001; 153(5): 19 - 24.
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J. Biol. Chem.Home page
F. Jaulin-Bastard, H. Saito, A. Le Bivic, V. Ollendorff, S. Marchetto, D. Birnbaum, and J.-P. Borg
The ERBB2/HER2 Receptor Differentially Interacts with ERBIN and PICK1 PSD-95/DLG/ZO-1 Domain Proteins
J. Biol. Chem., April 27, 2001; 276(18): 15256 - 15263.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
H. Boudin and A. M. Craig
Molecular Determinants for PICK1 Synaptic Aggregation and mGluR7a Receptor Coclustering. ROLE OF THE PDZ, COILED-COIL, AND ACIDIC DOMAINS
J. Biol. Chem., August 3, 2001; 276(32): 30270 - 30276.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
L. A. Hu, W. Chen, R. T. Premont, M. Cong, and R. J. Lefkowitz
G Protein-coupled Receptor Kinase 5 Regulates beta 1-Adrenergic Receptor Association with PSD-95
J. Biol. Chem., January 4, 2002; 277(2): 1607 - 1613.
[Abstract] [Full Text] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
D. J. Linden
The expression of cerebellar LTD in culture is not associated with changes in AMPA-receptor kinetics, agonist affinity, or unitary conductance
PNAS, November 20, 2001; 98(24): 14066 - 14071.
[Abstract] [Full Text] [PDF]



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