Prevention of brain damage after traumatic brain injury by pharmacological enhancement of KCNQ (Kv7, "M-type") K+ currents in neurons

J Cereb Blood Flow Metab. 2020 Jun;40(6):1256-1273. doi: 10.1177/0271678X19857818. Epub 2019 Jul 4.

Abstract

Nearly three million people in the USA suffer traumatic brain injury (TBI) yearly; however, there are no pre- or post-TBI treatment options available. KCNQ2-5 voltage-gated K+ channels underlie the neuronal "M current", which plays a dominant role in the regulation of neuronal excitability. Our strategy towards prevention of TBI-induced brain damage is predicated on the suggested hyper-excitability of neurons induced by TBIs, and the decrease in neuronal excitation upon pharmacological augmentation of M/KCNQ K+ currents. Seizures are very common after a TBI, making further seizures and development of epilepsy disease more likely. Our hypothesis is that TBI-induced hyperexcitability and ischemia/hypoxia lead to metabolic stress, cell death and a maladaptive inflammatory response that causes further downstream morbidity. Using the mouse controlled closed-cortical impact blunt TBI model, we found that systemic administration of the prototype M-channel "opener", retigabine (RTG), 30 min after TBI, reduces the post-TBI cascade of events, including spontaneous seizures, enhanced susceptibility to chemo-convulsants, metabolic stress, inflammatory responses, blood-brain barrier breakdown, and cell death. This work suggests that acutely reducing neuronal excitability and energy demand via M-current enhancement may be a novel model of therapeutic intervention against post-TBI brain damage and dysfunction.

Keywords: Cell death; K+ channels; KCNQ; seizures; traumatic brain injury.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Anticonvulsants / pharmacology*
  • Brain Injuries, Traumatic / metabolism*
  • Carbamates / pharmacology*
  • KCNQ Potassium Channels / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Neurons / drug effects*
  • Neurons / metabolism*
  • Phenylenediamines / pharmacology*

Substances

  • Anticonvulsants
  • Carbamates
  • KCNQ Potassium Channels
  • Phenylenediamines
  • ezogabine