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Originally published In Press as doi:10.1074/jbc.M203752200 on July 30, 2002

J. Biol. Chem., Vol. 277, Issue 39, 36553-36562, September 27, 2002
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Serotonin 5-HT1A Receptors Regulate AMPA Receptor Channels through Inhibiting Ca2+/Calmodulin-dependent Kinase II in Prefrontal Cortical Pyramidal Neurons*

Xiang Cai, Zhenglin Gu, Ping Zhong, Yong Ren, and Zhen YanDagger

From the Department of Physiology and Biophysics, School of Medicine and Biomedical Sciences, State University of New York, Buffalo, New York 14214

We have studied the regulation of AMPA (alpha -amino-3-hydroxy-5-methylisoxazole-4-propionic acid) receptor channels by serotonin signaling in pyramidal neurons of prefrontal cortex (PFC). Application of serotonin reduced the amplitude of AMPA-evoked currents, an effect mimicked by 5-HT1A receptor agonists and blocked by 5-HT1A antagonists, indicating the mediation by 5-HT1A receptors. The serotonergic modulation of AMPA receptor currents was blocked by protein kinase A (PKA) activators and occluded by PKA inhibitors. Inhibiting the catalytic activity of protein phosphatase 1 (PP1) also eliminated the effect of serotonin on AMPA currents. Furthermore, the serotonergic modulation of AMPA currents was occluded by application of the Ca2+/calmodulin-dependent kinase II (CaMKII) inhibitors and blocked by intracellular injection of calmodulin or recombinant CaMKII. Application of serotonin or 5-HT1A agonists to PFC slices reduced CaMKII activity and the phosphorylation of AMPA receptor subunit GluR1 at the CaMKII site in a PP1-dependent manner. We concluded that serotonin, by activating 5-HT1A receptors, suppress glutamatergic signaling through the inhibition of CaMKII, which is achieved by the inhibition of PKA and ensuing activation of PP1. This modulation demonstrates the critical role of CaMKII in serotonergic regulation of PFC neuronal activity, which may explain the neuropsychiatric behavioral phenotypes seen in CaMKII knockout mice.

* This work was supported by National Institutes of Health Grant MH63128 (to Z. Y.), National Science Foundation Grant IBN-0117026 (to Z. Y.), and Howard Hughes Medical Institute Biomedical Research Support Program grant 53000261 (State University of New York at Buffalo).The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Dagger To whom correspondence should be addressed: Dept. of Physiology and Biophysics, State University of New York, 124 Sherman Hall, Buffalo, NY 14214. Tel.: 716-829-3058; Fax: 716-829-2699; E-mail: zhenyan@buffalo.edu.

Copyright © 2002 by The American Society for Biochemistry and Molecular Biology, Inc.
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