A small molecule activator of Nav 1.1 channels increases fast-spiking interneuron excitability and GABAergic transmission in vitro and has anti-convulsive effects in vivo

Eur J Neurosci. 2017 Aug;46(3):1887-1896. doi: 10.1111/ejn.13626. Epub 2017 Jul 20.

Abstract

Nav 1.1 (SCN1A) channels primarily located in gamma-aminobutyric acid (GABA)ergic fast-spiking interneurons are pivotal for action potential generation and propagation in these neurons. Inappropriate function of fast-spiking interneurons, leading to disinhibition of pyramidal cells and network desynchronization, correlates with decreased cognitive capability. Further, reduced functionality of Nav 1.1 channels is linked to various diseases in the central nervous system. There is, at present, however no subtype selective pharmacological activators of Nav 1.1 channels available for studying pharmacological modulation of interneuron function. In the current study, we identified a small molecule Nav 1.1 activator, 3-amino-5-(4-methoxyphenyl)thiophene-2-carboxamide, named AA43279, and provided an in vitro to in vivo characterization of the compound. In HEK-293 cells expressing human Nav 1.1 channels, AA43279 increased the Nav 1.1-mediated current in a concentration-dependent manner mainly by impairing the fast inactivation kinetics of the channels. In rat hippocampal brain slices, AA43279 increased the firing activity of parvalbumin-expressing, fast-spiking GABAergic interneurons and increased the spontaneous inhibitory post-synaptic currents (sIPSCs) recorded from pyramidal neurons. When tested in vivo, AA43279 had anti-convulsive properties in the maximal electroshock seizure threshold test. AA43279 was tested for off-target effects on 72 different proteins, including Nav 1.2, Nav 1.4, Nav 1.5, Nav 1.6 and Nav 1.7 and exhibited reasonable selectivity. Taken together, AA43279 might constitute a valuable tool compound for revealing biological functions of Nav 1.1 channels.

Keywords: SCNA1; activators; interneurons; maximal electroshock seizures threshold; slice electrophysiology.

MeSH terms

  • Action Potentials
  • Animals
  • Anticonvulsants / chemical synthesis
  • Anticonvulsants / pharmacology*
  • Anticonvulsants / therapeutic use
  • CA1 Region, Hippocampal / cytology
  • CA1 Region, Hippocampal / metabolism
  • CA1 Region, Hippocampal / physiology
  • Excitatory Postsynaptic Potentials
  • GABAergic Neurons / drug effects*
  • GABAergic Neurons / metabolism
  • GABAergic Neurons / physiology
  • HEK293 Cells
  • Humans
  • Interneurons / drug effects*
  • Interneurons / metabolism
  • Interneurons / physiology
  • Male
  • Mice
  • NAV1.1 Voltage-Gated Sodium Channel / metabolism*
  • Rats
  • Rats, Sprague-Dawley
  • Seizures / drug therapy*
  • Sodium Channel Blockers / chemical synthesis
  • Sodium Channel Blockers / pharmacology*
  • Sodium Channel Blockers / therapeutic use
  • Thiophenes / pharmacology*

Substances

  • AA43279
  • Anticonvulsants
  • NAV1.1 Voltage-Gated Sodium Channel
  • Sodium Channel Blockers
  • Thiophenes