The epigenetic state of EED-Gli3-Gli1 regulatory axis controls embryonic cortical neurogenesis

Stem Cell Reports. 2022 Sep 13;17(9):2064-2080. doi: 10.1016/j.stemcr.2022.07.004. Epub 2022 Aug 4.

Abstract

Mutations in the embryonic ectoderm development (EED) cause Weaver syndrome, but whether and how EED affects embryonic brain development remains elusive. Here, we generated a mouse model in which Eed was deleted in the forebrain to investigate the role of EED. We found that deletion of Eed decreased the number of upper-layer neurons but not deeper-layer neurons starting at E16.5. Transcriptomic and genomic occupancy analyses revealed that the epigenetic states of a group of cortical neurogenesis-related genes were altered in Eed knockout forebrains, followed by a decrease of H3K27me3 and an increase of H3K27ac marks within the promoter regions. The switching of H3K27me3 to H3K27ac modification promoted the recruitment of RNA-Pol2, thereby enhancing its expression level. The small molecule activator SAG or Ptch1 knockout for activating Hedgehog signaling can partially rescue aberrant cortical neurogenesis. Taken together, we proposed a novel EED-Gli3-Gli1 regulatory axis that is critical for embryonic brain development.

Keywords: EED; EED-Gli3-Gli1 regulatory axis; PRC2; cortical development; hedgehog signaling; neurogenesis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain* / growth & development
  • Epigenesis, Genetic
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism
  • Histones / metabolism
  • Mice
  • Nerve Tissue Proteins / metabolism
  • Neurogenesis* / genetics
  • Polycomb Repressive Complex 2* / genetics
  • Polycomb Repressive Complex 2* / metabolism
  • Zinc Finger Protein GLI1* / genetics
  • Zinc Finger Protein GLI1* / metabolism
  • Zinc Finger Protein Gli3* / genetics
  • Zinc Finger Protein Gli3* / metabolism

Substances

  • Eed protein, mouse
  • Gli1 protein, mouse
  • Gli3 protein, mouse
  • Hedgehog Proteins
  • Histones
  • Nerve Tissue Proteins
  • Zinc Finger Protein GLI1
  • Zinc Finger Protein Gli3
  • Polycomb Repressive Complex 2