The potassium channel KCa3.1 constitutes a pharmacological target for neuroinflammation associated with ischemia/reperfusion stroke

J Cereb Blood Flow Metab. 2016 Dec;36(12):2146-2161. doi: 10.1177/0271678X15611434. Epub 2015 Nov 2.

Abstract

Activated microglia/macrophages significantly contribute to the secondary inflammatory damage in ischemic stroke. Cultured neonatal microglia express the K+ channels Kv1.3 and KCa3.1, both of which have been reported to be involved in microglia-mediated neuronal killing, oxidative burst and cytokine production. However, it is questionable whether neonatal cultures accurately reflect the K+ channel expression of activated microglia in the adult brain. We here subjected mice to middle cerebral artery occlusion with eight days of reperfusion and patch-clamped acutely isolated microglia/macrophages. Microglia from the infarcted area exhibited higher densities of K+ currents with the biophysical and pharmacological properties of Kv1.3, KCa3.1 and Kir2.1 than microglia from non-infarcted control brains. Similarly, immunohistochemistry on human infarcts showed strong Kv1.3 and KCa3.1 immunoreactivity on activated microglia/macrophages. We next investigated the effect of genetic deletion and pharmacological blockade of KCa3.1 in reversible middle cerebral artery occlusion. KCa3.1-/- mice and wild-type mice treated with the KCa3.1 blocker TRAM-34 exhibited significantly smaller infarct areas on day-8 after middle cerebral artery occlusion and improved neurological deficit. Both manipulations reduced microglia/macrophage activation and brain cytokine levels. Our findings suggest KCa3.1 as a pharmacological target for ischemic stroke. Of potential, clinical relevance is that KCa3.1 blockade is still effective when initiated 12 h after the insult.

Keywords: KCa3.1; TRAM-34; microglia activation; middle cerebral artery occlusion; potassium channel.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Brain / metabolism
  • Brain Ischemia / pathology
  • Cells, Cultured
  • Disease Models, Animal
  • Humans
  • Infarction, Middle Cerebral Artery
  • Intermediate-Conductance Calcium-Activated Potassium Channels / antagonists & inhibitors*
  • Macrophage Activation
  • Mice
  • Molecular Targeted Therapy
  • Neurogenic Inflammation / drug therapy*
  • Pyrazoles / pharmacology
  • Pyrazoles / therapeutic use
  • Stroke / pathology*

Substances

  • Intermediate-Conductance Calcium-Activated Potassium Channels
  • Kcnn4 protein, mouse
  • Pyrazoles
  • TRAM 34