Disease-causing Slack potassium channel mutations produce opposite effects on excitability of excitatory and inhibitory neurons

Cell Rep. 2024 Mar 26;43(3):113904. doi: 10.1016/j.celrep.2024.113904. Epub 2024 Mar 7.

Abstract

The KCNT1 gene encodes the sodium-activated potassium channel Slack (KCNT1, KNa1.1), a regulator of neuronal excitability. Gain-of-function mutations in humans cause cortical network hyperexcitability, seizures, and severe intellectual disability. Using a mouse model expressing the Slack-R455H mutation, we find that Na+-dependent K+ (KNa) and voltage-dependent sodium (NaV) currents are increased in both excitatory and inhibitory cortical neurons. These increased currents, however, enhance the firing of excitability neurons but suppress that of inhibitory neurons. We further show that the expression of NaV channel subunits, particularly that of NaV1.6, is upregulated and that the length of the axon initial segment and of axonal NaV immunostaining is increased in both neuron types. Our study on the coordinate regulation of KNa currents and the expression of NaV channels may provide an avenue for understanding and treating epilepsies and other neurological disorders.

Keywords: ADNFLE; CP: Neuroscience; EIMFS; KCNT1; Na(V)1.6; Slack channel; epilepsy; gain of function; neuronal excitability; voltage-gated sodium (Na(V)) channel.

MeSH terms

  • Animals
  • Axons / metabolism
  • Epilepsy* / genetics
  • Humans
  • Mice
  • Mutation / genetics
  • Nerve Tissue Proteins / metabolism
  • Neurons / metabolism
  • Potassium Channels* / metabolism
  • Potassium Channels, Sodium-Activated

Substances

  • KCNT1 protein, human
  • Nerve Tissue Proteins
  • Potassium Channels
  • Potassium Channels, Sodium-Activated
  • Slo2 protein, mouse