Dyshomeostatic modulation of Ca2+-activated K+ channels in a human neuronal model of KCNQ2 encephalopathy

Elife. 2021 Feb 5:10:e64434. doi: 10.7554/eLife.64434.

Abstract

Mutations in KCNQ2, which encodes a pore-forming K+ channel subunit responsible for neuronal M-current, cause neonatal epileptic encephalopathy, a complex disorder presenting with severe early-onset seizures and impaired neurodevelopment. The condition is exceptionally difficult to treat, partially because the effects of KCNQ2 mutations on the development and function of human neurons are unknown. Here, we used induced pluripotent stem cells (iPSCs) and gene editing to establish a disease model and measured the functional properties of differentiated excitatory neurons. We find that patient iPSC-derived neurons exhibit faster action potential repolarization, larger post-burst afterhyperpolarization and a functional enhancement of Ca2+-activated K+ channels. These properties, which can be recapitulated by chronic inhibition of M-current in control neurons, facilitate a burst-suppression firing pattern that is reminiscent of the interictal electroencephalography pattern in patients. Our findings suggest that dyshomeostatic mechanisms compound KCNQ2 loss-of-function leading to alterations in the neurodevelopmental trajectory of patient iPSC-derived neurons.

Keywords: AHP; KCNQ2; M-current; burst-suppression; disease modeling; dyshomeostatic; epileptic encephalopathy; excitatory neurons; homeostatic plasticity; human; human iPSCs; neuroscience; potassium channel; regenerative medicine; stem cells.

Publication types

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

MeSH terms

  • Action Potentials / physiology
  • Brain Diseases / genetics*
  • Brain Diseases / physiopathology
  • Cell Line
  • Humans
  • KCNQ2 Potassium Channel / genetics*
  • KCNQ2 Potassium Channel / metabolism
  • Neurons / physiology*
  • Pluripotent Stem Cells

Substances

  • KCNQ2 Potassium Channel
  • KCNQ2 protein, human