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The Journal of Neuroscience, August 12, 2009, 29(32):9977-9986; doi:10.1523/JNEUROSCI.3893-08.2009

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Neurobiology of Disease
BC1 Regulation of Metabotropic Glutamate Receptor-Mediated Neuronal Excitability

Jun Zhong,^1 * Shih-Chieh Chuang,^1,2 * Riccardo Bianchi,^1,2 Wangfa Zhao,^1,2 Heekyung Lee,^1,2 André A. Fenton,^1,2 Robert K. S. Wong,^1,2,3 and Henri Tiedge^1,2,3

¹The Robert F. Furchgott Center for Neural and Behavioral Science, Department of Physiology and Pharmacology, ²Program in Neural and Behavioral Science, and ³Department of Neurology, State University of New York, Health Science Center at Brooklyn, Brooklyn, New York 11203

Correspondence should be addressed to either Henri Tiedge or Jun Zhong, The Robert F. Furchgott Center for Neural and Behavioral Science, Department of Physiology and Pharmacology, State University of New York, Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, NY 11203, Email: htiedge{at}downstate.edu or Email: jzhong{at}downstate.edu

Regulatory RNAs have been suggested to contribute to the control of gene expression in eukaryotes. Brain cytoplasmic (BC) RNAs are regulatory RNAs that control translation initiation. We now report that neuronal BC1 RNA plays an instrumental role in the protein-synthesis-dependent implementation of neuronal excitation–repression equilibria. BC1 repression counter-regulates translational stimulation resulting from synaptic activation of group I metabotropic glutamate receptors (mGluRs). Absence of BC1 RNA precipitates plasticity dysregulation in the form of neuronal hyperexcitability, elicited by group I mGluR-stimulated translation and signaled through the mitogen-activated protein kinase kinase/extracellular signal-regulated kinase pathway. Dysregulation of group I mGluR function in the absence of BC1 RNA gives rise to abnormal brain function. Cortical EEG recordings from freely moving BC1^–/– animals show that group I mGluR-mediated oscillations in the gamma frequency range are significantly elevated. When subjected to sensory stimulation, these animals display an acute group I mGluR-dependent propensity for convulsive seizures. Inadequate RNA control in neurons is thus causally linked to heightened group I mGluR-stimulated translation, neuronal hyperexcitability, heightened gamma band oscillations, and epileptogenesis. These data highlight the significance of small RNA control in neuronal plasticity.

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Received Aug. 14, 2008; revised April 8, 2009; accepted July 1, 2009.

Correspondence should be addressed to either Henri Tiedge or Jun Zhong, The Robert F. Furchgott Center for Neural and Behavioral Science, Department of Physiology and Pharmacology, State University of New York, Health Science Center at Brooklyn, 450 Clarkson Avenue, Brooklyn, NY 11203, Email: htiedge{at}downstate.edu or Email: jzhong{at}downstate.edu

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