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The Journal of Neuroscience, January 1, 2000, 20(1):89-102
Control of GluR1 AMPA Receptor Function by cAMP-Dependent Protein
Kinase
T. G.
Banke1, 2,
D.
Bowie1,
H.-K.
Lee3,
R. L.
Huganir3,
A.
Schousboe2, and
S. F.
Traynelis1
1 Department of Pharmacology, Emory University School
of Medicine, Atlanta, Georgia 30322, 2 Department of
Pharmacology, Royal Danish School of Pharmacy, Copenhagen, Denmark
DK-2100, and 3 Howard Hughes Medical Institute,
Johns Hopkins University School of Medicine, Baltimore, Maryland
21205
Modulation of postsynaptic AMPA receptors in the brain by
phosphorylation may play a role in the expression of synaptic
plasticity at central excitatory synapses. It is known from biochemical
studies that GluR1 AMPA receptor subunits can be phosphorylated within their C terminal by cAMP-dependent protein kinase A (PKA), which is
colocalized with the phosphatase calcineurin (i.e., phosphatase 2B). We
have examined the effect of PKA and calcineurin on the time
course, peak open probability
(PO,PEAK), and single-channel properties of glutamateevoked responses for neuronal AMPA receptors and homomeric GluR1(flip) receptors recorded in outside-out patches. Inclusion of purified catalytic subunit C -PKA in the pipette solution increased neuronal AMPA receptor
PO,PEAK (0.92) compared with recordings made
with calcineurin included in the pipette (PO,PEAK 0.39). Similarly, C-PKA
increased PO,PEAK for recombinant GluR1
receptors (0.78) compared with patches excised from cells cotransfected
with a cDNA encoding the PKA peptide inhibitor PKI (PO,PEAK 0.50) or patches with calcineurin
included in the pipette (PO,PEAK 0.42).
Neither PKA nor calcineurin altered the amplitude of single-channel
subconductance levels, weighted mean unitary current, mean channel open
period, burst length, or macroscopic response waveform for recombinant
GluR1 receptors. Substitution of an amino acid at the PKA
phosphorylation site (S845A) on GluR1 eliminated the PKA-induced
increase in PO,PEAK, whereas the
mutation of a Ca2+,calmodulin-dependent kinase II
and PKC phosphorylation site (S831A) was without effect. These results
suggest that AMPA receptor peak response open probability can be
increased by PKA through phosphorylation of GluR1 Ser845.
Key words:
AMPA receptors; glutamate; LTD; PKA; calcineurin; open
probability; GluR1
Copyright © 2000 Society for Neuroscience 0270-6474/0/20189-14$05.00/0
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A. M. Vanhoose and D. G. Winder
NMDA and {beta}1-Adrenergic Receptors Differentially Signal Phosphorylation of Glutamate Receptor Type 1 in Area CA1 of Hippocampus
J. Neurosci.,
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G. Rumbaugh, G.-M. Sia, C. C. Garner, and R. L. Huganir
Synapse-Associated Protein-97 Isoform-Specific Regulation of Surface AMPA Receptors and Synaptic Function in Cultured Neurons
J. Neurosci.,
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A. Momiyama, R A. Silver, M. Hausser, T. Notomi, Y. Wu, R. Shigemoto, and S. G Cull-Candy
The density of AMPA receptors activated by a transmitter quantum at the climbing fibre-Purkinje cell synapse in immature rats
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H.-X. Chen and S. N. Roper
PKA and PKC Enhance Excitatory Synaptic Transmission in Human Dentate Gyrus
J Neurophysiol,
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C.-H. Lin, S.-H. Yeh, T.-H. Leu, W.-C. Chang, S.-T. Wang, and P.-W. Gean
Identification of Calcineurin as a Key Signal in the Extinction of Fear Memory
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X. M Shao, Q. Ge, and J. L Feldman
Modulation of AMPA receptors by cAMP-dependent protein kinase in PreBotzinger complex inspiratory neurons regulates respiratory rhythm in the rat
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March 1, 2003;
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S. N. Duffy and P. V. Nguyen
Postsynaptic Application of a Peptide Inhibitor of cAMP-Dependent Protein Kinase Blocks Expression of Long-Lasting Synaptic Potentiation in Hippocampal Neurons
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February 15, 2003;
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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
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A. Robert and J. R. Howe
How AMPA Receptor Desensitization Depends on Receptor Occupancy
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S. F. Oliveria, L. L. Gomez, and M. L. Dell'Acqua
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C.-H. Lin, C.-C. Lee, and P.-W. Gean
Involvement of a Calcineurin Cascade in Amygdala Depotentiation and Quenching of Fear Memory
Mol. Pharmacol.,
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B. Lin, F. A. Brucher, L. L. Colgin, and G. Lynch
Long-Term Potentiation Alters the Modulator Pharmacology of AMPA-Type Glutamate Receptors
J Neurophysiol,
June 1, 2002;
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N. Otmakhov and J. E. Lisman
Postsynaptic Application of a cAMP Analogue Reverses Long-Term Potentiation in Hippocampal CA1 Pyramidal Neurons
J Neurophysiol,
June 1, 2002;
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S. J. Tavalin, M. Colledge, J. W. Hell, L. K. Langeberg, R. L. Huganir, and J. D. Scott
Regulation of GluR1 by the A-Kinase Anchoring Protein 79 (AKAP79) Signaling Complex Shares Properties with Long-Term Depression
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J. Choi, J. Ko, E. Park, J.-R. Lee, J. Yoon, S. Lim, and E. Kim
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U. Shalev, J. W. Grimm, and Y. Shaham
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F. Miskevich, W. Lu, S.-Y. Lin, and M. Constantine-Paton
Interaction between Metabotropic and NMDA Subtypes of Glutamate Receptors in Sprout Suppression at Young Synapses
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B. K. Andrasfalvy and J. C. Magee
Distance-Dependent Increase in AMPA Receptor Number in the Dendrites of Adult Hippocampal CA1 Pyramidal Neurons
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G. C. Castellani, E. M. Quinlan, L. N Cooper, and H. Z. Shouval
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D. D Mott, K. Erreger, T. G Banke, and S. F Traynelis
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D. Liao, R. H. Scannevin, and R. Huganir
Activation of Silent Synapses by Rapid Activity-Dependent Synaptic Recruitment of AMPA Receptors
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A. Robert, S. N. Irizarry, T. E. Hughes, and J. R. Howe
Subunit Interactions and AMPA Receptor Desensitization
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T. C. Foster, K. M. Sharrow, J. R. Masse, C. M. Norris, and A. Kumar
Calcineurin Links Ca2+ Dysregulation with Brain Aging
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P. V. Nguyen, S. N. Duffy, and J. Z. Young
Differential Maintenance and Frequency-Dependent Tuning of LTP at Hippocampal Synapses of Specific Strains of Inbred Mice
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W. Vandenberghe, E. C. Ihle, D. K. Patneau, W. Robberecht, and J. R. Brorson
AMPA Receptor Current Density, Not Desensitization, Predicts Selective Motoneuron Vulnerability
J. Neurosci.,
October 1, 2000;
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G. F. Reis, M. B. Lee, A. S. Huang, and K. D. Parfitt
Adenylate Cyclase-Mediated Forms of Neuronal Plasticity in Hippocampal Area CA1 Are Reduced With Aging
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J. L. Cornish and P. W. Kalivas
Glutamate Transmission in the Nucleus Accumbens Mediates Relapse in Cocaine Addiction
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