A human forebrain organoid model of fragile X syndrome exhibits altered neurogenesis and highlights new treatment strategies

Nat Neurosci. 2021 Oct;24(10):1377-1391. doi: 10.1038/s41593-021-00913-6. Epub 2021 Aug 19.

Abstract

Fragile X syndrome (FXS) is caused by the loss of fragile X mental retardation protein (FMRP), an RNA-binding protein that can regulate the translation of specific mRNAs. In this study, we developed an FXS human forebrain organoid model and observed that the loss of FMRP led to dysregulated neurogenesis, neuronal maturation and neuronal excitability. Bulk and single-cell gene expression analyses of FXS forebrain organoids revealed that the loss of FMRP altered gene expression in a cell-type-specific manner. The developmental deficits in FXS forebrain organoids could be rescued by inhibiting the phosphoinositide 3-kinase pathway but not the metabotropic glutamate pathway disrupted in the FXS mouse model. We identified a large number of human-specific mRNAs bound by FMRP. One of these human-specific FMRP targets, CHD2, contributed to the altered gene expression in FXS organoids. Collectively, our study revealed molecular, cellular and electrophysiological abnormalities associated with the loss of FMRP during human brain development.

Publication types

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

MeSH terms

  • Adult
  • Brain / pathology
  • Cell Differentiation
  • DNA-Binding Proteins / genetics
  • Electrophysiological Phenomena
  • Fragile X Syndrome / drug therapy*
  • Fragile X Syndrome / pathology*
  • Humans
  • Male
  • Models, Neurological
  • Neurogenesis / drug effects
  • Neurogenesis / genetics*
  • Neurons / pathology
  • Phosphatidylinositol 3-Kinases / drug effects
  • Prosencephalon / pathology*
  • Protein Binding
  • Protein Kinase Inhibitors / therapeutic use
  • RNA, Messenger / genetics
  • Receptors, Metabotropic Glutamate / drug effects

Substances

  • CHD2 protein, human
  • DNA-Binding Proteins
  • Protein Kinase Inhibitors
  • RNA, Messenger
  • Receptors, Metabotropic Glutamate