Axonal Charcot-Marie-Tooth disease patient-derived motor neurons demonstrate disease-specific phenotypes including abnormal electrophysiological properties

Exp Neurol. 2015 Jan:263:190-9. doi: 10.1016/j.expneurol.2014.10.005. Epub 2014 Oct 30.

Abstract

Objective: Charcot-Marie-Tooth (CMT) disease is a group of inherited peripheral neuropathies associated with mutations or copy number variations in over 70 genes encoding proteins with fundamental roles in the development and function of Schwann cells and peripheral axons. Here, we used iPSC-derived cells to identify common pathophysiological mechanisms in axonal CMT.

Methods: iPSC lines from patients with two distinct forms of axonal CMT (CMT2A and CMT2E) were differentiated into spinal cord motor neurons and used to study axonal structure and function and electrophysiological properties in vitro.

Results: iPSC-derived motor neurons exhibited gene and protein expression, ultrastructural and electrophysiological features of mature primary spinal cord motor neurons. Cytoskeletal abnormalities were found in neurons from a CMT2E (NEFL) patient and corroborated by a mouse model of the same NEFL point mutation. Abnormalities in mitochondrial trafficking were found in neurons derived from this patient, but were only mildly present in neurons from a CMT2A (MFN2) patient. Novel electrophysiological abnormalities, including reduced action potential threshold and abnormal channel current properties were observed in motor neurons derived from both of these patients.

Interpretation: Human iPSC-derived motor neurons from axonal CMT patients replicated key pathophysiological features observed in other models of MFN2 and NEFL mutations, including abnormal cytoskeletal and mitochondrial dynamics. Electrophysiological abnormalities found in axonal CMT iPSC-derived human motor neurons suggest that these cells are hyperexcitable and have altered sodium and calcium channel kinetics. These findings may provide a new therapeutic target for this group of heterogeneous inherited neuropathies.

Keywords: Axonal Charcot–Marie–Tooth disease; Axonal transport; Electrophysiology; Induced pluripotent stem cells; Inherited Neuropathies; Motor neurons.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Cell Separation
  • Charcot-Marie-Tooth Disease / genetics*
  • Charcot-Marie-Tooth Disease / pathology
  • Charcot-Marie-Tooth Disease / physiopathology*
  • Child
  • Electrophysiological Phenomena
  • Female
  • GTP Phosphohydrolases / genetics
  • Gene Knock-In Techniques
  • Humans
  • Induced Pluripotent Stem Cells
  • Intermediate Filaments / pathology
  • Male
  • Mice
  • Mitochondria / pathology
  • Mitochondrial Proteins / genetics
  • Motor Neurons / pathology*
  • Neurofilament Proteins / genetics
  • Patch-Clamp Techniques
  • Phenotype
  • Point Mutation
  • Real-Time Polymerase Chain Reaction

Substances

  • Mitochondrial Proteins
  • Neurofilament Proteins
  • neurofilament protein L
  • GTP Phosphohydrolases
  • MFN2 protein, human