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Science 27 June 1997:
Vol. 276. no. 5321, pp. 2042 - 2045
DOI: 10.1126/science.276.5321.2042
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Reports

Regulatory Phosphorylation of AMPA-Type Glutamate Receptors by CaM-KII During Long-Term Potentiation

Andres Barria, Dominique Muller, Victor Derkach, Leslie C. Griffith, Thomas R. Soderling *

Long-term potentiation (LTP), a cellular model of learning and memory, requires calcium-dependent protein kinases. Induction of LTP increased the phosphorus-32 labeling of alpha -amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA)-type glutamate receptors (AMPA-Rs), which mediate rapid excitatory synaptic transmission. This AMPA-R phosphorylation appeared to be catalyzed by Ca2+- and calmodulin-dependent protein kinase II (CaM-KII): (i) it correlated with the activation and autophosphorylation of CaM-KII, (ii) it was blocked by the CaM-KII inhibitor KN-62, and (iii) its phosphorus-32 peptide map was the same as that of GluR1 coexpressed with activated CaM-KII in HEK-293 cells. This covalent modulation of AMPA-Rs in LTP provides a postsynaptic molecular mechanism for synaptic plasticity.

A. Barria, V. Derkach, T. R. Soderling, Vollum Institute, Oregon Health Sciences University, Portland, OR 97201, USA.
D. Muller, Department of Neuropharmacology, Centre Medical Universitaire, 1211 Geneva 4, Switzerland.
L. C. Griffith, Department of Biology, Brandeis University, Waltham, MA 02254, USA.
*   To whom correspondence should be addressed.

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Calcium/Calmodulin-Dependent Protein Kinase II Regulates Caenorhabditis elegans Locomotion in Concert With a Go/Gq Signaling Network.
M. Robatzek and J. H. Thomas (2000)
Genetics 156, 1069-1082
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Activity-Dependent Maintenance of Long-Term Potentiation at Visual Cortical Inhibitory Synapses.
Y. Komatsu and Y. Yoshimura (2000)
J. Neurosci. 20, 7539-7546
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Protein Phosphatase-Mediated Regulation of Protein Kinase C during Long-Term Depression in the Adult Hippocampus In Vivo.
E. Thiels, B. I. Kanterewicz, L. T. Knapp, G. Barrionuevo, and E. Klann (2000)
J. Neurosci. 20, 7199-7207
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Involvement of neurogranin in the modulation of calcium/calmodulin-dependent protein kinase II, synaptic plasticity, and spatial learning: A study with knockout mice.
J. H. Pak, F. L. Huang, J. Li, D. Balschun, K. G. Reymann, C. Chiang, H. Westphal, and K.-P. Huang (2000)
PNAS
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Synaptic Plasticity in Hippocampal CA1 Neurons of Mice Lacking Type 1 Inositol-1,4,5-Trisphosphate Receptors.
S. Fujii, M. Matsumoto, K. Igarashi, H. Kato, and K. Mikoshiba (2000)
Learn. Mem. 7, 312-320
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Impaired Synaptic Plasticity and cAMP Response Element-Binding Protein Activation in Ca2+/Calmodulin-Dependent Protein Kinase Type IV/Gr-Deficient Mice.
N. Ho, J. A. Liauw, F. Blaeser, F. Wei, S. Hanissian, L. M. Muglia, D. F. Wozniak, A. Nardi, K. L. Arvin, D. M. Holtzman, et al. (2000)
J. Neurosci. 20, 6459-6472
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Mice Deficient in the Polysialyltransferase ST8SiaIV/PST-1 Allow Discrimination of the Roles of Neural Cell Adhesion Molecule Protein and Polysialic Acid in Neural Development and Synaptic Plasticity.
M. Eckhardt, O. Bukalo, G. Chazal, L. Wang, C. Goridis, M. Schachner, R. Gerardy-Schahn, H. Cremer, and A. Dityatev (2000)
J. Neurosci. 20, 5234-5244
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Regulation of Phosphorylation of the GluR1 AMPA Receptor in the Neostriatum by Dopamine and Psychostimulants In Vivo.
G. L. Snyder, P. B. Allen, A. A. Fienberg, C. G. Valle, R. L. Huganir, A. C. Nairn, and P. Greengard (2000)
J. Neurosci. 20, 4480-4488
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Three-dimensional Reconstructions of Calcium/Calmodulin-dependent (CaM) Kinase IIalpha and Truncated CaM Kinase IIalpha Reveal a Unique Organization for Its Structural Core and Functional Domains.
S. J. Kolodziej, A. Hudmon, M. N. Waxham, and J. K. Stoops (2000)
J. Biol. Chem. 275, 14354-14359
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Brain-Derived Neurotrophic Factor Differentially Regulates Excitatory and Inhibitory Synaptic Transmission in Hippocampal Cultures.
M. M. Bolton, A. J. Pittman, and D. C. Lo (2000)
J. Neurosci. 20, 3221-3232
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Synaptic Control of Motoneuronal Excitability.
J. C. Rekling, G. D. Funk, D. A. Bayliss, X.-W. Dong, and J. L. Feldman (2000)
Physiol Rev 80, 767-852
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Driving AMPA Receptors into Synapses by LTP and CaMKII: Requirement for GluR1 and PDZ Domain Interaction.
Y. Hayashi, S. Shi, J. A. Esteban, A. Piccini, J. Poncer, and R. Malinow (2000)
Science 287, 2262-2267
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Brain-Derived Neurotrophic Factor Acutely Inhibits AMPA-Mediated Currents in Developing Sensory Relay Neurons.
A. Balkowiec, D. L. Kunze, and D. M. Katz (2000)
J. Neurosci. 20, 1904-1911
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Brain Actin-associated Protein Phosphatase 1 Holoenzymes Containing Spinophilin, Neurabin, and Selected Catalytic Subunit Isoforms.
L. B. MacMillan, M. A. Bass, N. Cheng, E. F. Howard, M. Tamura, S. Strack, B. E. Wadzinski, and R. J. Colbran (1999)
J. Biol. Chem. 274, 35845-35854
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