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Previous Article | Next Article
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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Trans-Synaptic Eph Receptor-Ephrin Signaling in Hippocampal Mossy Fiber LTP
Science, June 7, 2002; 296(5574): 1864 - 1869.
[Abstract] [Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
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]
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.
[Abstract] [PDF]
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.
[Abstract] [Full Text] [PDF]
A. Y. Hung and M. Sheng
PDZ Domains: Structural Modules for Protein Complex Assembly
J. Biol. Chem., February 15, 2002; 277(8): 5699 - 5702.
[Full Text] [PDF]
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.
[Abstract] [Full Text] [PDF]
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]
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]
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.
[Abstract] [Full Text] [PDF]
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]
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]
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]
M. Ito
Cerebellar Long-Term Depression: Characterization, Signal Transduction, and Functional Roles
Physiol Rev, July 1, 2001; 81(3): 1143 - 1195.
[Abstract] [Full Text] [PDF]
M. Sheng
Molecular organization of the postsynaptic specialization
PNAS, June 19, 2001; 98(13): 7058 - 7061.
[Abstract] [Full Text] [PDF]
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.
[Full Text] [PDF]
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]
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]
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]
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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