Electrophysiological and pharmacological characterization of a novel and potent neuronal Kv7 channel opener SCR2682 for antiepilepsy

FASEB J. 2019 Aug;33(8):9154-9166. doi: 10.1096/fj.201802848RR. Epub 2019 May 7.

Abstract

Voltage-gated Kv7/KCNQ/M potassium channels play an essential role in the control of membrane potential and neuronal excitability. Activation of the neuronal Kv7/KCNQ/M-current represents an attractive therapeutic strategy for treatment of hyperexcitability-related neuropsychiatric disorders such as epilepsy, pain, and depression, which is an unmet medical need. In this study, we synthesized and characterized a novel compound, N-(4-(2-bromo-6,7-dihydrothieno[3,2-c]pyridin-5(4H)-yl)-2,6-dimethylphenyl)-3,3-dimethylbutanamide (SCR2682) 2,6-dimethyl-4-(piperidin-yl) phenyl)-amide derivative, that exhibits selective and potent activation of neuronal Kv7/KCNQ/M-channels. Whole-cell patch-clamp recordings of human embryonic kidney 293 cells expressing Kv7.2/Kv7.3 channels show that SCR2682 selectively activates the channel current in a dose-dependent manner with an EC50 of 9.8 ± 0.4 nM, which is ∼100-fold more potent than a U.S. Food and Drug Administration-approved antiepileptic drug (retigabine) for treatment of partial epilepsy. SCR2682 shifts voltage-dependent activation of the Kv7.2/7.3 current toward more negative membrane potential, to about -37 mV (V1/2). SCR2682 also activates the native M-current in rat hippocampal or cortical neurons, causing marked hyperpolarization and potent inhibition of neuronal firings. Mechanistically, mutating the tryptophan residue 236 located at the fifth transmembrane segment of Kv7.2 abolishes the chemical activation of the channel by SCR2682. Furthermore, intraperitoneal or intragastric administration of SCR2682 results in a dose-dependent inhibition of seizures by maximal electroshock. Taken together, our findings demonstrate that a novel small molecule, SCR2682, selectively and potently activates neuronal Kv7 channels and reverses epileptic seizures in rodents. Thus, SCR2682 may warrant further evaluation for clinical development of antiepileptic therapy.-Zhang, F., Liu, Y., Tang, F., Liang, B., Chen, H., Zhang, H., Wang, K. Electrophysiological and pharmacological characterization of a novel and potent neuronal Kv7 channel opener SCR2682 for antiepilepsy.

Keywords: Kv7/KCNQ/M-channel; neurons; seizures.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • Animals
  • Anticonvulsants / chemical synthesis
  • Anticonvulsants / chemistry
  • Anticonvulsants / pharmacology*
  • Cells, Cultured
  • ERG1 Potassium Channel / antagonists & inhibitors
  • Epilepsy / drug therapy
  • HEK293 Cells
  • Humans
  • KCNQ Potassium Channels / agonists
  • KCNQ2 Potassium Channel / agonists*
  • KCNQ2 Potassium Channel / genetics
  • KCNQ2 Potassium Channel / metabolism
  • KCNQ3 Potassium Channel / agonists*
  • Male
  • Membrane Potentials / drug effects
  • Membrane Transport Modulators / chemical synthesis
  • Membrane Transport Modulators / chemistry
  • Membrane Transport Modulators / pharmacology*
  • Mice
  • Mutagenesis, Site-Directed
  • Neurons / drug effects
  • Neurons / metabolism
  • Patch-Clamp Techniques
  • Pyridines / chemical synthesis
  • Pyridines / chemistry
  • Pyridines / pharmacology*
  • Rats
  • Seizures / drug therapy

Substances

  • Anticonvulsants
  • ERG1 Potassium Channel
  • KCNH2 protein, human
  • KCNQ Potassium Channels
  • KCNQ2 Potassium Channel
  • KCNQ3 Potassium Channel
  • KCNQ4 protein, human
  • KCNQ5 protein, human
  • Membrane Transport Modulators
  • Pyridines
  • SCR2682