A SMAD1/5-YAP signalling module drives radial glia self-amplification and growth of the developing cerebral cortex

Development. 2020 Jul 13;147(13):dev187005. doi: 10.1242/dev.187005.

Abstract

The growth and evolutionary expansion of the cerebral cortex are defined by the spatial-temporal production of neurons, which itself depends on the decision of radial glial cells (RGCs) to self-amplify or to switch to neurogenic divisions. The mechanisms regulating these RGC fate decisions are still incompletely understood. Here, we describe a novel and evolutionarily conserved role of the canonical BMP transcription factors SMAD1/5 in controlling neurogenesis and growth during corticogenesis. Reducing the expression of both SMAD1 and SMAD5 in neural progenitors at early mouse cortical development caused microcephaly and an increased production of early-born cortical neurons at the expense of late-born ones, which correlated with the premature differentiation and depletion of the pool of cortical progenitors. Gain- and loss-of-function experiments performed during early cortical neurogenesis in the chick revealed that SMAD1/5 activity supports self-amplifying RGC divisions and restrains the neurogenic ones. Furthermore, we demonstrate that SMAD1/5 stimulate RGC self-amplification through the positive post-transcriptional regulation of the Hippo signalling effector YAP. We anticipate this SMAD1/5-YAP signalling module to be fundamental in controlling growth and evolution of the amniote cerebral cortex.

Keywords: Bone morphogenetic proteins (BMPs); Cerebral cortex; Mouse; Neurogenesis; Radial glial cells; SMAD transcription factors; YAP.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Bone Morphogenetic Proteins / genetics
  • Bone Morphogenetic Proteins / metabolism
  • Cell Cycle Proteins / genetics
  • Cell Cycle Proteins / metabolism
  • Cerebral Cortex / embryology
  • Cerebral Cortex / metabolism*
  • Ependymoglial Cells / cytology
  • Ependymoglial Cells / metabolism
  • Female
  • Mice
  • Neural Stem Cells / metabolism*
  • Neurogenesis / genetics
  • Neurogenesis / physiology
  • Signal Transduction / physiology
  • Smad1 Protein / genetics
  • Smad1 Protein / metabolism*
  • Smad5 Protein / genetics
  • Smad5 Protein / metabolism*
  • YAP-Signaling Proteins

Substances

  • Adaptor Proteins, Signal Transducing
  • Bone Morphogenetic Proteins
  • Cell Cycle Proteins
  • Smad1 Protein
  • Smad5 Protein
  • YAP-Signaling Proteins
  • Yap1 protein, mouse