Potassium channel dysfunction in human neuronal models of Angelman syndrome

Science. 2019 Dec 20;366(6472):1486-1492. doi: 10.1126/science.aav5386.

Abstract

Disruptions in the ubiquitin protein ligase E3A (UBE3A) gene cause Angelman syndrome (AS). Whereas AS model mice have associated synaptic dysfunction and altered plasticity with abnormal behavior, whether similar or other mechanisms contribute to network hyperactivity and epilepsy susceptibility in AS patients remains unclear. Using human neurons and brain organoids, we demonstrate that UBE3A suppresses neuronal hyperexcitability via ubiquitin-mediated degradation of calcium- and voltage-dependent big potassium (BK) channels. We provide evidence that augmented BK channel activity manifests as increased intrinsic excitability in individual neurons and subsequent network synchronization. BK antagonists normalized neuronal excitability in both human and mouse neurons and ameliorated seizure susceptibility in an AS mouse model. Our findings suggest that BK channelopathy underlies epilepsy in AS and support the use of human cells to model human developmental diseases.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angelman Syndrome / metabolism*
  • Angelman Syndrome / physiopathology
  • Animals
  • Calcium Channels, N-Type / metabolism*
  • Epilepsy / metabolism
  • Humans
  • Mice
  • Models, Neurological
  • Neurons / drug effects
  • Neurons / metabolism
  • Organoids
  • Potassium Channel Blockers / pharmacology
  • Potassium Channel Blockers / therapeutic use
  • Seizures / metabolism
  • Ubiquitin-Protein Ligases / genetics
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitination

Substances

  • Calcium Channels, N-Type
  • Potassium Channel Blockers
  • voltage-dependent calcium channel (P-Q type)
  • UBE3A protein, human
  • Ubiquitin-Protein Ligases