PICK1 Interacts with ABP/GRIP to Regulate AMPA Receptor Trafficking

PICK1 and ABP/GRIP bind to the AMPA receptor (AMPAR) GluR2 subunit C terminus. Transfer of the receptor from ABP/GRIP to PICK1, facilitated by GluR2 S880 phosphorylation, may initiate receptor trafficking. Here we report protein interactions that regulate these steps. The PICK1 BAR domain interacts intermolecularly with the ABP/GRIP linker II region and intramolecularly with the PICK1 PDZ domain. Binding of PKCalpha or GluR2 to the PICK1 PDZ domain disrupts the intramolecular interaction and facilitates the PICK1 BAR domain association with ABP/GRIP. Interference with the PICK1-ABP/GRIP interaction impairs S880 phosphorylation of GluR2 by PKC and decreases the constitutive surface expression of GluR2, the NMDA-induced endocytosis of GluR2, and recycling of internalized GluR2. We suggest that the PICK1 interaction with ABP/GRIP is a critical step in controlling GluR2 trafficking.

[1]  Akira Terashima,et al.  Regulation of Synaptic Strength and AMPA Receptor Subunit Composition by PICK1 , 2004, The Journal of Neuroscience.

[2]  R. Huganir,et al.  Interaction of the AMPA receptor subunit GluR2/3 with PDZ domains regulates hippocampal long-term depression , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[3]  Dane M. Chetkovich,et al.  Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms , 2000, Nature.

[4]  S. Nakanishi,et al.  PICK1 Interacts with and Regulates PKC Phosphorylation of mGLUR7 , 2000, The Journal of Neuroscience.

[5]  G. Collingridge,et al.  PDZ Proteins Interacting with C-Terminal GluR2/3 Are Involved in a PKC-Dependent Regulation of AMPA Receptors at Hippocampal Synapses , 2000, Neuron.

[6]  M. Ehlers,et al.  Reinsertion or Degradation of AMPA Receptors Determined by Activity-Dependent Endocytic Sorting , 2000, Neuron.

[7]  D. Linden,et al.  Expression of Cerebellar Long-Term Depression Requires Postsynaptic Clathrin-Mediated Endocytosis , 2000, Neuron.

[8]  R. Weinberg,et al.  Interaction between GRIP and liprin-alpha/SYD2 is required for AMPA receptor targeting. , 2002, Neuron.

[9]  P. Osten,et al.  Mutagenesis Reveals a Role for ABP/GRIP Binding to GluR2 in Synaptic Surface Accumulation of the AMPA Receptor , 2000, Neuron.

[10]  R. Weinberg,et al.  Association of AMPA Receptors with a Subset of Glutamate Receptor-Interacting Protein In Vivo , 1999, The Journal of Neuroscience.

[11]  S. Nakanishi,et al.  The protein kinase Cα binding protein PICK1 interacts with short but not long form alternative splice variants of AMPA receptor subunits , 1999, Neuropharmacology.

[12]  R. Huganir,et al.  Requirement of AMPA Receptor GluR2 Phosphorylation for Cerebellar Long-Term Depression , 2003, Science.

[13]  G. Collingridge,et al.  Surface Expression of AMPA Receptors in Hippocampal Neurons Is Regulated by an NSF-Dependent Mechanism , 1999, Neuron.

[14]  E. Ziff,et al.  Receptor trafficking and the plasticity of excitatory synapses , 2002, Current Opinion in Neurobiology.

[15]  R. Malenka,et al.  AMPA receptor trafficking and synaptic plasticity. , 2002, Annual review of neuroscience.

[16]  S Matsuda,et al.  Phosphorylation of Serine‐880 in GluR2 by Protein Kinase C Prevents Its C Terminus from Binding with Glutamate Receptor‐Interacting Protein , 1999, Journal of neurochemistry.

[17]  R. Abagyan,et al.  Novel Anchorage of GluR2/3 to the Postsynaptic Density by the AMPA Receptor–Binding Protein ABP , 1998, Neuron.

[18]  Andreas Lüthi,et al.  Hippocampal LTD Expression Involves a Pool of AMPARs Regulated by the NSF–GluR2 Interaction , 1999, Neuron.

[19]  R. Huganir,et al.  Calcium-Permeable AMPA Receptor Plasticity Is Mediated by Subunit-Specific Interactions with PICK1 and NSF , 2005, Neuron.

[20]  P. Hanson,et al.  NSF ATPase and α-/β-SNAPs Disassemble the AMPA Receptor-PICK1 Complex , 2002, Neuron.

[21]  S. Mikawa,et al.  Disruption of AMPA receptor GluR2 clusters following long‐term depression induction in cerebellar Purkinje neurons , 2000, The EMBO journal.

[22]  S. Heinemann,et al.  Cloned glutamate receptors. , 1994, Annual review of neuroscience.

[23]  P. Hanson,et al.  NSF ATPase and alpha-/beta-SNAPs disassemble the AMPA receptor-PICK1 complex. , 2002, Neuron.

[24]  Sebastian Pascarelle,et al.  Unusual spectral energy distribution of a galaxy previously reported to be at redshift 6.68 , 2000, Nature.

[25]  R. Huganir,et al.  Cerebellar Long-Term Depression Requires PKC-Regulated Interactions between GluR2/3 and PDZ Domain–Containing Proteins , 2000, Neuron.

[26]  Pavel Osten,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 , 2001, The Journal of Neuroscience.

[27]  Mikyoung Park,et al.  Recycling Endosomes Supply AMPA Receptors for LTP , 2004, Science.

[28]  R. Malenka,et al.  Differential roles for NSF and GRIP/ABP in AMPA receptor cycling , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[29]  R. Wenthold,et al.  Evidence for multiple AMPA receptor complexes in hippocampal CA1/CA2 neurons , 1996, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[30]  Richard L. Huganir,et al.  GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors , 1997, Nature.

[31]  山崎 真弥.  Differential palmitoylation of two mouse glutamate receptor interacting protein 1 forms with different N-terminal sequences , 2004 .

[32]  Roberto Malinow,et al.  Subunit-Specific Rules Governing AMPA Receptor Trafficking to Synapses in Hippocampal Pyramidal Neurons , 2001, Cell.

[33]  Jie Fu,et al.  Intracellular Membrane Targeting and Suppression of Ser880 Phosphorylation of Glutamate Receptor 2 by the Linker I-Set II Domain of AMPA Receptor-Binding Protein , 2003, The Journal of Neuroscience.

[34]  G. Collingridge,et al.  Rapid and Differential Regulation of AMPA and Kainate Receptors at Hippocampal Mossy Fibre Synapses by PICK1 and GRIP , 2003, Neuron.

[35]  Mark F Bear,et al.  NMDA Induces Long-Term Synaptic Depression and Dephosphorylation of the GluR1 Subunit of AMPA Receptors in Hippocampus , 1998, Neuron.

[36]  R. Huganir,et al.  PDZ Proteins Bind, Cluster, and Synaptically Colocalize with Eph Receptors and Their Ephrin Ligands , 1998, Neuron.

[37]  R. Nicoll,et al.  Dynamin-dependent endocytosis of ionotropic glutamate receptors. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[38]  Yu Tian Wang,et al.  Regulation of AMPA Receptor–Mediated Synaptic Transmission by Clathrin-Dependent Receptor Internalization , 2000, Neuron.

[39]  R. Nicoll,et al.  AMPA Receptor Trafficking at Excitatory Synapses , 2003, Neuron.

[40]  R. Huganir,et al.  Clustering of AMPA Receptors by the Synaptic PDZ Domain–Containing Protein PICK1 , 1999, Neuron.

[41]  E. Olson,et al.  Specific Interaction of the PDZ Domain Protein PICK1 with the COOH Terminus of Protein Kinase C-α* , 1997, The Journal of Biological Chemistry.

[42]  S. Cull-Candy,et al.  Subunit interaction with PICK and GRIP controls Ca2+ permeability of AMPARs at cerebellar synapses , 2005, Nature Neuroscience.

[43]  V. Piëch,et al.  Subunit-specific temporal and spatial patterns of AMPA receptor exocytosis in hippocampal neurons , 2001, Nature Neuroscience.

[44]  N. Hirokawa,et al.  Glutamate-receptor-interacting protein GRIP1 directly steers kinesin to dendrites , 2002, Nature.

[45]  R. Weinberg,et al.  Interaction between GRIP and Liprin-α/SYD2 Is Required for AMPA Receptor Targeting , 2002, Neuron.

[46]  Jie Fu,et al.  Differential Palmitoylation Directs the AMPA Receptor-Binding Protein ABP to Spines or to Intracellular Clusters , 2002, The Journal of Neuroscience.

[47]  R. Huganir,et al.  Glutamate Receptor Subunit 2 Serine 880 Phosphorylation Modulates Synaptic Transmission and Mediates Plasticity in CA1 Pyramidal Cells , 2003, The Journal of Neuroscience.

[48]  M. Sheng,et al.  Subunit Rules Governing the Sorting of Internalized AMPA Receptors in Hippocampal Neurons , 2004, Neuron.

[49]  I. Greger,et al.  RNA Editing at Arg607 Controls AMPA Receptor Exit from the Endoplasmic Reticulum , 2002, Neuron.

[50]  S. Nakanishi,et al.  The PDZ Proteins PICK1, GRIP, and Syntenin Bind Multiple Glutamate Receptor Subtypes , 2002, The Journal of Biological Chemistry.

[51]  B. Peter,et al.  BAR Domains as Sensors of Membrane Curvature: The Amphiphysin BAR Structure , 2004, Science.

[52]  R. Huganir,et al.  Phosphorylation of the AMPA Receptor Subunit GluR2 Differentially Regulates Its Interaction with PDZ Domain-Containing Proteins , 2000, The Journal of Neuroscience.