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Volume 17, Number 19, Issue of October 1, 1997 pp. 7330-7338
Copyright ©1997 Society for Neuroscience

Dopaminergic Modulation of Sodium Current in Hippocampal Neurons via cAMP-Dependent Phosphorylation of Specific Sites in the Sodium Channel  Subunit

Received June 26, 1997; accepted July 23, 1997.

Angela R. Cantrell¹, Raymond D. Smith², Alan L. Goldin², Todd Scheuer¹, and William A. Catterall¹

¹ Department of Pharmacology, University of Washington, Seattle, Washington 98195-7280, and ² Department of Microbiology and Molecular Genetics, University of California, Irvine, California 92697

Phosphorylation of brain Na⁺ channel  subunits by cAMP-dependent protein kinase (PKA) decreases peak Na⁺ current in cultured brain neurons and in mammalian cells and Xenopus oocytes expressing cloned brain Na⁺ channels. We have studied PKA regulation of Na⁺ channel function by activation of D1-like dopamine receptors in acutely isolated hippocampal neurons using whole-cell voltage-clamp recording techniques. The D1 agonist SKF 81297 reversibly reduced peak Na⁺ current in a concentration-dependent manner. No changes in the voltage dependence or kinetics of activation or inactivation were observed. This effect was mediated by PKA, as it was mimicked by application of the PKA activator Sp-5,6-dichloro-1--D-ribofuranosylbenzimidazole-3,5-monophosphorothioate(cBIMPS) and was inhibited by the specific PKA inhibitor peptide PKAI_5-24. cBIMPS had similar effects on type IIA brain Na⁺ channel  subunits expressed in tsA-201 cells, but no effect was observed on a mutant Na⁺ channel  subunit in which serine residues in five PKA phosphorylation sites in the intracellular loop connecting domains I and II (L_I-II) had been replaced by alanine. A single mutation, S573A, similarly eliminated cBIMPS modulation. Thus, activation of D1-like dopamine receptors results in PKA-dependent phosphorylation of specific sites in L_I-II of the Na⁺ channel  subunit, causing a reduction in Na⁺ current. Such modulation is expected to exert a profound influence on overall neuronal excitability. Dopaminergic input to the hippocampus from the mesocorticolimbic system may exert this influence in vivo.

Key words: Na⁺ current; neuromodulation; cAMP-dependent protein kinase; hippocampus; dopamine receptors; phosphorylation

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