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The Journal of Neuroscience, May 15, 2000, 20(10):3915-3925

Do Glia Have Heart? Expression and Functional Role for Ether-A-Go-Go Currents in Hippocampal Astrocytes

Adriana Emmi¹, H. Jurgen Wenzel¹, Philip A. Schwartzkroin¹, Maurizio Taglialatela², Pasqualina Castaldo², Laura Bianchi³, Jeanne Nerbonne⁴, Gail A. Robertson⁵, and Damir Janigro⁶

¹ Department of Neurological Surgery, University of Washington, Seattle, Washington 98104, ² Section of Pharmacology, Department Neuroscience, University of Naples Federico II, Napoli, Italy, ³ Department of Pharmacology, Vanderbilt University, Nashville, Tennessee 37232, ⁴ Department of Molecular Biology and Pharmacology, Washington University, Saint Louis, Missouri 63110, ⁵ Department of Physiology, University of Wisconsin Medical School, Madison, Wisconsin 53706, and ⁶ Department of Neurological Surgery, Division of Cerebrovascular Research, Cleveland Clinic, Cleveland, Ohio 44195

Potassium homeostasis plays an important role in the control of neuronal excitability, and diminished buffering of extracellular K results in neuronal Hyperexcitability and abnormal synchronization. Astrocytes are the cellular elements primarily involved in this process. Potassium uptake into astrocytes occurs, at least in part, through voltage-dependent channels, but the exact mechanisms involved are not fully understood. Although most glial recordings reveal expression of inward rectifier currents (K_IR), it is not clear how spatial buffering consisting of accumulation and release of potassium may be mediated by exclusively inward potassium fluxes. We hypothesized that a combination of inward and outward rectifiers cooperate in the process of spatial buffering. Given the pharmacological properties of potassium homeostasis (sensitivity to Cs⁺), members of the ether-a-go-go (ERG) channel family widely expressed in the nervous system could underlie part of the process. We used electrophysiological recordings and pharmacological manipulations to demonstrate the expression of ERG-type currents in cultured and in situ hippocampal astrocytes. Specific ERG blockers (dofetilide and E 4031) inhibited hyperpolarization- and depolarization-activated glial currents, and ERG blockade impaired clearance of extracellular potassium with little direct effect on hippocampal neuron excitability. Immunocytochemical analysis revealed ERG protein mostly confined to astrocytes; ERG immunoreactivity was absent in presynaptic and postsynaptic elements, but pronounced in glia surrounding the synaptic cleft. Oligodendroglia did not reveal ERG immunoreactivity. Intense immunoreactivity was also found in perivascular astrocytic end feet at the blood-brain barrier. cDNA amplification showed that cortical astrocytes selectively express HERG1, but not HERG2-3 genes. This study provides insight into a possible physiological role of hippocampal ERG channels and links activation of ERG to control of potassium homeostasis.

Key words: spatial buffering; glia-neuronal interactions; epileptogenesis; long QT; synchronization; homeostasis; inherited epilepsy

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Copyright © 2000 Society for Neuroscience  0270-6474/00/20103915-11$05.00/0

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