Sodium Channel SCN3A (NaV1.3) Regulation of Human Cerebral Cortical Folding and Oral Motor Development

Neuron. 2018 Sep 5;99(5):905-913.e7. doi: 10.1016/j.neuron.2018.07.052. Epub 2018 Aug 23.

Abstract

Channelopathies are disorders caused by abnormal ion channel function in differentiated excitable tissues. We discovered a unique neurodevelopmental channelopathy resulting from pathogenic variants in SCN3A, a gene encoding the voltage-gated sodium channel NaV1.3. Pathogenic NaV1.3 channels showed altered biophysical properties including increased persistent current. Remarkably, affected individuals showed disrupted folding (polymicrogyria) of the perisylvian cortex of the brain but did not typically exhibit epilepsy; they presented with prominent speech and oral motor dysfunction, implicating SCN3A in prenatal development of human cortical language areas. The development of this disorder parallels SCN3A expression, which we observed to be highest early in fetal cortical development in progenitor cells of the outer subventricular zone and cortical plate neurons and decreased postnatally, when SCN1A (NaV1.1) expression increased. Disrupted cerebral cortical folding and neuronal migration were recapitulated in ferrets expressing the mutant channel, underscoring the unexpected role of SCN3A in progenitor cells and migrating neurons.

Keywords: Cortical Development; Na(V)1.1; Na(V)1.3; Oromotor; Outer Radial Glia; Polymicrogyria; SCN1A; SCN3A; Speech; Voltage-Gated Sodium Channel (VGSC).

Publication types

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

MeSH terms

  • Adolescent
  • Adult
  • Animals
  • Cell Movement / physiology
  • Cells, Cultured
  • Cerebral Cortex / diagnostic imaging*
  • Cerebral Cortex / growth & development*
  • Cerebral Cortex / pathology
  • Child
  • Child, Preschool
  • Female
  • Ferrets
  • HEK293 Cells
  • Humans
  • Infant
  • Language Development*
  • Male
  • Megalencephaly / diagnostic imaging
  • Megalencephaly / genetics
  • Megalencephaly / pathology
  • Middle Aged
  • NAV1.3 Voltage-Gated Sodium Channel / genetics*
  • Pedigree
  • Polymicrogyria / diagnostic imaging
  • Polymicrogyria / genetics
  • Polymicrogyria / pathology
  • Sodium Channels / genetics*

Substances

  • NAV1.3 Voltage-Gated Sodium Channel
  • SCN3A protein, human
  • Sodium Channels