Single-Cell Sequencing of iPSC-Dopamine Neurons Reconstructs Disease Progression and Identifies HDAC4 as a Regulator of Parkinson Cell Phenotypes

Cell Stem Cell. 2019 Jan 3;24(1):93-106.e6. doi: 10.1016/j.stem.2018.10.023. Epub 2018 Nov 29.

Abstract

Induced pluripotent stem cell (iPSC)-derived dopamine neurons provide an opportunity to model Parkinson's disease (PD), but neuronal cultures are confounded by asynchronous and heterogeneous appearance of disease phenotypes in vitro. Using high-resolution, single-cell transcriptomic analyses of iPSC-derived dopamine neurons carrying the GBA-N370S PD risk variant, we identified a progressive axis of gene expression variation leading to endoplasmic reticulum stress. Pseudotime analysis of genes differentially expressed (DE) along this axis identified the transcriptional repressor histone deacetylase 4 (HDAC4) as an upstream regulator of disease progression. HDAC4 was mislocalized to the nucleus in PD iPSC-derived dopamine neurons and repressed genes early in the disease axis, leading to late deficits in protein homeostasis. Treatment of iPSC-derived dopamine neurons with HDAC4-modulating compounds upregulated genes early in the DE axis and corrected PD-related cellular phenotypes. Our study demonstrates how single-cell transcriptomics can exploit cellular heterogeneity to reveal disease mechanisms and identify therapeutic targets.

Keywords: Parkinson’s disease; histone deacetylase 4; induced pluripotent stem cells; single-cell RNA sequencing.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Disease Progression
  • Dopamine / metabolism
  • Dopaminergic Neurons / metabolism
  • Dopaminergic Neurons / pathology*
  • Endoplasmic Reticulum Stress
  • Gene Expression Profiling
  • Gene Expression Regulation*
  • Glucosylceramidase / genetics
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism*
  • Humans
  • Induced Pluripotent Stem Cells / metabolism
  • Induced Pluripotent Stem Cells / pathology*
  • Mutation
  • Parkinson Disease / genetics
  • Parkinson Disease / metabolism
  • Parkinson Disease / pathology*
  • Phenotype
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Single-Cell Analysis / methods*
  • Transcriptome

Substances

  • Repressor Proteins
  • GBA protein, human
  • Glucosylceramidase
  • HDAC4 protein, human
  • Histone Deacetylases
  • Dopamine