 |
|||||
|
|||||
|
|||||
|
|||||
|
|||||
The Journal of Neuroscience, June 9, 2004, 24(23):5381-5390; doi:10.1523/JNEUROSCI.4378-03.2004
Previous Article | Next Article
Cellular/Molecular
Regulation of Synaptic Strength and AMPA Receptor Subunit Composition by PICK1
Akira Terashima, * Lucy Cotton, * Kumlesh K. Dev, Guido Meyer, Shahid Zaman, Fabrice Duprat, Jeremy M. Henley, Graham L. Collingridge, andJohn T. R. Isaac Medical Research Council Centre for Synaptic Plasticity, Department of Anatomy, University of Bristol, Bristol BS8 1TD, United Kingdom
PICK1 (protein interacting with C kinase-1) regulates the surface expression of the AMPA receptor (AMPAR) GluR2 subunit, however, the functional consequences of this interaction are not well understood. Previous work has suggested that PICK1 promotes the internalization of AMPARs. However, we found that when PICK1 is virally expressed in the CA1 region of hippocampal slices, it causes an increase in AMPAR-mediated EPSC amplitude. This effect is associated with increased AMPAR rectification and sensitivity to polyamine toxin. These effects are blocked by PKC or calcium/calmodulin-dependent protein kinase II inhibitors, indicating that the virally expressed PICK1 signals through an endogenous kinase cascade. In contrast, blockade of interactions with GluR2 at the N-ethylmaleimide-sensitive factor site did not cause a change in subunit composition, suggesting that the effects of PICK1 are not simply a nonspecific consequence of removing AMPARs from the surface. Immunocytochemical and biochemical analyses in dissociated cultured hippocampal neurons show that PICK1 causes a decrease in endogenous GluR2 surface expression but no change in GluR1 surface levels. To address the physiological role of PICK1, we virally expressed C-terminal GluR2 peptides. Blockade of endogenous PICK1 PDZ (postsynaptic density-95/Discs large/zona occludens-1) domain interactions produced opposite effects on synaptic strength and AMPAR rectification to those observed with PICK1 expression. This demonstrates that AMPAR subunit composition is physiologically regulated through a mechanism involving PICK1 PDZ domain interactions. These findings suggest that PICK1 acts to downregulate the GluR2 content of AMPARs at hippocampal CA1 synapses, thereby increasing synaptic strength at resting membrane potentials.
Key words: glutamate; synaptic plasticity; hippocampus; interacting protein; AMPA receptor trafficking; protein interacting with C kinase
Received Sep 26, 2003; revised April 20, 2004; accepted April 21, 2004.
This article has been cited by other articles:
T. M. Ho, K. A. Pelkey, J. G. Pelletier, R. L. Huganir, J.-C. Lacaille, and C. J. McBain
Burst firing induces postsynaptic LTD at developing mossy fibre\#8211;CA3 pyramid synapses
J. Physiol., September 15, 2009; 587(18): 4441 - 4454.
[Abstract] [Full Text] [PDF]
R. M. Dixon, J. R. Mellor, and J. G. Hanley
PICK1-mediated Glutamate Receptor Subunit 2 (GluR2) Trafficking Contributes to Cell Death in Oxygen/Glucose-deprived Hippocampal Neurons
J. Biol. Chem., May 22, 2009; 284(21): 14230 - 14235.
[Abstract] [Full Text] [PDF]
K. R. Famous, V. Kumaresan, G. Sadri-Vakili, H. D. Schmidt, D. F. Mierke, J.-H. J. Cha, and R. C. Pierce
Phosphorylation-Dependent Trafficking of GluR2-Containing AMPA Receptors in the Nucleus Accumbens Plays a Critical Role in the Reinstatement of Cocaine Seeking
J. Neurosci., October 22, 2008; 28(43): 11061 - 11070.
[Abstract] [Full Text] [PDF]
D.-T. Lin and R. L. Huganir
PICK1 and Phosphorylation of the Glutamate Receptor 2 (GluR2) AMPA Receptor Subunit Regulates GluR2 Recycling after NMDA Receptor-Induced Internalization
J. Neurosci., December 12, 2007; 27(50): 13903 - 13908.
[Abstract] [Full Text] [PDF]
M. Cao, J. Xu, C. Shen, C. Kam, R. L. Huganir, and J. Xia
PICK1 ICA69 Heteromeric BAR Domain Complex Regulates Synaptic Targeting and Surface Expression of AMPA Receptors
J. Neurosci., November 21, 2007; 27(47): 12945 - 12956.
[Abstract] [Full Text] [PDF]
M. T.-W. Ho, K. A. Pelkey, L. Topolnik, R. S. Petralia, K. Takamiya, J. Xia, R. L. Huganir, J.-C. Lacaille, and C. J. McBain
Developmental Expression of Ca2+-Permeable AMPA Receptors Underlies Depolarization-Induced Long-Term Depression at Mossy Fiber CA3 Pyramid Synapses
J. Neurosci., October 24, 2007; 27(43): 11651 - 11662.
[Abstract] [Full Text] [PDF]
J. Shin, F. Shen, and J. Huguenard
PKC and polyamine modulation of GluR2-deficient AMPA receptors in immature neocortical pyramidal neurons of the rat
J. Physiol., June 1, 2007; 581(2): 679 - 691.
[Abstract] [Full Text] [PDF]
X.-d. Hu, Q. Huang, X. Yang, and H. Xia
Differential Regulation of AMPA Receptor Trafficking by Neurabin-Targeted Synaptic Protein Phosphatase-1 in Synaptic Transmission and Long-Term Depression in Hippocampus
J. Neurosci., April 25, 2007; 27(17): 4674 - 4686.
[Abstract] [Full Text] [PDF]
P. Arstikaitis and C. Gauthier-Campbell
BARS at the Synapse: PICK-1 Lipid Binding Domain Regulates Targeting, Trafficking, and Synaptic Plasticity
J. Neurosci., June 28, 2006; 26(26): 6909 - 6910.
[Full Text] [PDF]
C. Gebhardt and S. G. Cull-Candy
Influence of agonist concentration on AMPA and kainate channels in CA1 pyramidal cells in rat hippocampal slices
J. Physiol., June 1, 2006; 573(2): 371 - 394.
[Abstract] [Full Text] [PDF]
B. Liu, M. Liao, J. G. Mielke, K. Ning, Y. Chen, L. Li, Y. H. El-Hayek, E. Gomez, R. S. Zukin, M. G. Fehlings, et al.
Ischemic insults direct glutamate receptor subunit 2-lacking AMPA receptors to synaptic sites.
J. Neurosci., May 17, 2006; 26(20): 5309 - 5319.
[Abstract] [Full Text] [PDF]
A. W. Baxter and D. J. A. Wyllie
Phosphatidylinositol 3 kinase activation and AMPA receptor subunit trafficking underlie the potentiation of miniature EPSC amplitudes triggered by the activation of L-type calcium channels.
J. Neurosci., May 17, 2006; 26(20): 5456 - 5469.
[Abstract] [Full Text] [PDF]
W. Jin, W.-P. Ge, J. Xu, M. Cao, L. Peng, W. Yung, D. Liao, S. Duan, M. Zhang, and J. Xia
Lipid Binding Regulates Synaptic Targeting of PICK1, AMPA Receptor Trafficking, and Synaptic Plasticity
J. Neurosci., March 1, 2006; 26(9): 2380 - 2390.
[Abstract] [Full Text] [PDF]
C. Hansel
When the B-team runs plasticity: GluR2 receptor trafficking in cerebellar long-term potentiation
PNAS, December 20, 2005; 102(51): 18245 - 18246.
[Full Text] [PDF]
C. L. Palmer, L. Cotton, and J. M. Henley
The Molecular Pharmacology and Cell Biology of {alpha}-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid Receptors
Pharmacol. Rev., June 1, 2005; 57(2): 253 - 277.
[Abstract] [Full Text] [PDF]
T. Makinen, R. H. Adams, J. Bailey, Q. Lu, A. Ziemiecki, K. Alitalo, R. Klein, and G. A. Wilkinson
PDZ interaction site in ephrinB2 is required for the remodeling of lymphatic vasculature
Genes & Dev., February 1, 2005; 19(3): 397 - 410.
[Abstract] [Full Text] [PDF]
B. J. Maher, R. L. MacKinnon II, J. Bai, E. R. Chapman, and P. T. Kelly
Activation of Postsynaptic Ca2+ Stores Modulates Glutamate Receptor Cycling in Hippocampal Neurons
J Neurophysiol, January 1, 2005; 93(1): 178 - 188.
[Abstract] [Full Text] [PDF]
|
|
|
|
 |
|