Coupling of Slack and NaV1.6 sensitizes Slack to quinidine blockade and guides anti-seizure strategy development

Elife. 2024 Jan 30:12:RP87559. doi: 10.7554/eLife.87559.

Abstract

Quinidine has been used as an anticonvulsant to treat patients with KCNT1-related epilepsy by targeting gain-of-function KCNT1 pathogenic mutant variants. However, the detailed mechanism underlying quinidine's blockade against KCNT1 (Slack) remains elusive. Here, we report a functional and physical coupling of the voltage-gated sodium channel NaV1.6 and Slack. NaV1.6 binds to and highly sensitizes Slack to quinidine blockade. Homozygous knockout of NaV1.6 reduces the sensitivity of native sodium-activated potassium currents to quinidine blockade. NaV1.6-mediated sensitization requires the involvement of NaV1.6's N- and C-termini binding to Slack's C-terminus and is enhanced by transient sodium influx through NaV1.6. Moreover, disrupting the Slack-NaV1.6 interaction by viral expression of Slack's C-terminus can protect against SlackG269S-induced seizures in mice. These insights about a Slack-NaV1.6 complex challenge the traditional view of 'Slack as an isolated target' for anti-epileptic drug discovery efforts and can guide the development of innovative therapeutic strategies for KCNT1-related epilepsy.

Keywords: KCNT1-related epilepsy; NaV1.6; Slack; mouse; neuroscience; quinidine.

MeSH terms

  • Animals
  • Anticonvulsants / pharmacology
  • Anticonvulsants / therapeutic use
  • Epilepsy*
  • Homozygote
  • Humans
  • Mice
  • NAV1.6 Voltage-Gated Sodium Channel* / genetics
  • Nerve Tissue Proteins / genetics
  • Quinidine* / pharmacology
  • Sodium

Substances

  • Anticonvulsants
  • KCNT1 protein, human
  • NAV1.6 Voltage-Gated Sodium Channel
  • Nerve Tissue Proteins
  • Quinidine
  • Sodium
  • SCN8A protein, human