Progressive Motor Neuron Pathology and the Role of Astrocytes in a Human Stem Cell Model of VCP-Related ALS

Cell Rep. 2017 May 30;19(9):1739-1749. doi: 10.1016/j.celrep.2017.05.024.

Abstract

Motor neurons (MNs) and astrocytes (ACs) are implicated in the pathogenesis of amyotrophic lateral sclerosis (ALS), but their interaction and the sequence of molecular events leading to MN death remain unresolved. Here, we optimized directed differentiation of induced pluripotent stem cells (iPSCs) into highly enriched (> 85%) functional populations of spinal cord MNs and ACs. We identify significantly increased cytoplasmic TDP-43 and ER stress as primary pathogenic events in patient-specific valosin-containing protein (VCP)-mutant MNs, with secondary mitochondrial dysfunction and oxidative stress. Cumulatively, these cellular stresses result in synaptic pathology and cell death in VCP-mutant MNs. We additionally identify a cell-autonomous VCP-mutant AC survival phenotype, which is not attributable to the same molecular pathology occurring in VCP-mutant MNs. Finally, through iterative co-culture experiments, we uncover non-cell-autonomous effects of VCP-mutant ACs on both control and mutant MNs. This work elucidates molecular events and cellular interplay that could guide future therapeutic strategies in ALS.

Keywords: amyotrophic lateral sclerosis (ALS); astrocytes (ACs); disease modeling; induced pluripotent stem cells (iPSCs); motor neurons (MNs).

MeSH terms

  • Amyotrophic Lateral Sclerosis / metabolism*
  • Amyotrophic Lateral Sclerosis / pathology*
  • Astrocytes / pathology*
  • Cell Survival
  • DNA-Binding Proteins / metabolism
  • Endoplasmic Reticulum / metabolism
  • Endoplasmic Reticulum / ultrastructure
  • Endoplasmic Reticulum Stress
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Membrane Potential, Mitochondrial
  • Mitochondria / metabolism
  • Mitochondria / ultrastructure
  • Models, Biological*
  • Motor Neurons / pathology*
  • Mutation / genetics
  • Nerve Degeneration / pathology
  • Neurogenesis
  • Oxidative Stress
  • Phenotype
  • Synapses / pathology
  • Valosin Containing Protein / metabolism*

Substances

  • DNA-Binding Proteins
  • TARDBP protein, human
  • Valosin Containing Protein