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The Journal of Neuroscience, September 10, 2008, 28(37):9133-9144; doi:10.1523/JNEUROSCI.1820-08.2008

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Neurobiology of Disease
Status Epilepticus Induces a Particular Microglial Activation State Characterized by Enhanced Purinergic Signaling

Elena Avignone,^1,2 Lauriane Ulmann,^3,4 Françoise Levavasseur,^1,2 François Rassendren,^3,4 and Etienne Audinat^1,2

¹Inserm U603, and ²Université Paris Descartes, Unité Mixte de Recherche (UMR)-S603, Centre National de la Recherche Scientifique (CNRS) UMR 8154, 75006 Paris, France, ³CNRS UMR 5203, Institut de Génomique fonctionnelle, Universités Montpellier 1 et 2, UMR-S661, and ⁴Inserm U661, 34094 Montpellier, France

Correspondence should be addressed to Etienne Audinat, Laboratoire de Neurophysiologie et Nouvelles Microscopies, Inserm U603, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8154, Université Paris Descartes, 45 rue des Saints-Pères, 75006 Paris, France. Email: etienne.audinat{at}univ-paris5.fr

Microglia cells are the resident macrophages of the CNS, and their activation plays a critical role in inflammatory reactions associated with many brain disorders, including ischemia, Alzheimer's and Parkinson's diseases, and epilepsy. However, the changes of microglia functional properties in epilepsy have rarely been studied. Here, we used a model of status epilepticus (SE) induced by intraperitoneal kainate injections to characterize the properties of microglial cells in hippocampal slices from CX3CR1^eGFP/+ mice. SE induced within 3 h an increased expression of inflammatory mediators in the hippocampus, followed by a modification of microglia morphology, a microglia proliferation, and a significant neurodegeneration in CA1. Changes in electrophysiological intrinsic membrane properties of hippocampal microglia were detected at 24–48 h after SE with, in particular, the appearance of new voltage-activated potassium currents. Consistent with the observation of an upregulation of purinergic receptor mRNAs in the hippocampus, we also provide pharmacological evidence that microglia membrane currents mediated by the activation of P2 receptors, including P2X₇, P2Y₆, and P2Y₁₂, were increased 48 h after SE. As a functional consequence of this modification of purinergic signaling, motility of microglia processes toward a source of P2Y₁₂ receptor agonist was twice as fast in the epileptic hippocampus. This study is the first functional description of microglia activation in an in vivo model of inflammation and provides evidence for the existence of a particular microglial activation state after a status epilepticus.

Key words: glial cells; ATP; inflammation; epilepsy; cytokines; hippocampus

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Received April 25, 2008; revised July 10, 2008; accepted Aug. 6, 2008.

Correspondence should be addressed to Etienne Audinat, Laboratoire de Neurophysiologie et Nouvelles Microscopies, Inserm U603, Centre National de la Recherche Scientifique Unité Mixte de Recherche 8154, Université Paris Descartes, 45 rue des Saints-Pères, 75006 Paris, France. Email: etienne.audinat{at}univ-paris5.fr

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