Human iPSC-Derived Cerebral Organoids Model Cellular Features of Lissencephaly and Reveal Prolonged Mitosis of Outer Radial Glia

Cell Stem Cell. 2017 Apr 6;20(4):435-449.e4. doi: 10.1016/j.stem.2016.12.007. Epub 2017 Jan 19.

Abstract

Classical lissencephaly is a genetic neurological disorder associated with mental retardation and intractable epilepsy, and Miller-Dieker syndrome (MDS) is the most severe form of the disease. In this study, to investigate the effects of MDS on human progenitor subtypes that control neuronal output and influence brain topology, we analyzed cerebral organoids derived from control and MDS-induced pluripotent stem cells (iPSCs) using time-lapse imaging, immunostaining, and single-cell RNA sequencing. We saw a cell migration defect that was rescued when we corrected the MDS causative chromosomal deletion and severe apoptosis of the founder neuroepithelial stem cells, accompanied by increased horizontal cell divisions. We also identified a mitotic defect in outer radial glia, a progenitor subtype that is largely absent from lissencephalic rodents but critical for human neocortical expansion. Our study, therefore, deepens our understanding of MDS cellular pathogenesis and highlights the broad utility of cerebral organoids for modeling human neurodevelopmental disorders.

Keywords: cerebral organoids; human lissencephaly; migration; outer radial glia; spindle orientation.

Publication types

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

MeSH terms

  • Adult
  • Apoptosis
  • Cell Movement
  • Cerebrum / pathology*
  • Chromosome Duplication
  • Classical Lissencephalies and Subcortical Band Heterotopias / pathology
  • Cytokinesis
  • Epithelium / pathology
  • Female
  • Humans
  • Induced Pluripotent Stem Cells / pathology*
  • Infant
  • Infant, Newborn
  • Lissencephaly / pathology*
  • Male
  • Middle Aged
  • Mitosis*
  • Neuroglia / pathology*
  • Neurons / pathology
  • Organoids / pathology*