A conserved differentiation programme facilitates inhibitory neuron production in the developing mouse and human cerebellum

Development. 2025 Dec 15;152(24):dev204811. doi: 10.1242/dev.204811. Epub 2025 Dec 19.

Abstract

Understanding the molecular mechanisms driving lineage decisions and differentiation during development is challenging in complex systems with a diverse progenitor pool, such as the mammalian cerebellum. Importantly, how different transcription factors cooperate to generate neural diversity and the gene regulatory mechanisms that drive neuron production, especially during the late stages of cerebellum development, are poorly understood. We used single cell RNA-sequencing (scRNA-seq) to investigate the developmental trajectories of nestin-expressing progenitors (NEPs) in the neonatal mouse cerebellum. We identified FOXO1 as a key regulator of NEP-to-inhibitory neuron differentiation, acting directly downstream of ASCL1. Genome occupancy and functional experiments using primary NEP cultures showed that both ASCL1 and FOXO1 regulate neurogenesis genes during differentiation while independently regulating proliferation and survival, respectively. Furthermore, we demonstrated that WNT signalling promotes the transition from an ASCL1+ to a FOXO1+ cellular state. Finally, the role of WNT signalling in promoting neuron production via FOXO1 is conserved in primary human NEP cultures. By resolving how cerebellar inhibitory neurons differentiate, our findings could have implications for cerebellar disorders such as spinocerebellar ataxia, where these cells are overproduced.

Keywords: Cerebellum; Differentiation; Forkhead box O1; Molecular layer interneurons; Neural development; Neurospheres.

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Proteins / genetics
  • Basic Helix-Loop-Helix Proteins / metabolism
  • Cell Differentiation* / genetics
  • Cell Proliferation
  • Cells, Cultured
  • Cerebellum* / cytology
  • Cerebellum* / embryology
  • Cerebellum* / growth & development
  • Cerebellum* / metabolism
  • Forkhead Box Protein O1 / genetics
  • Forkhead Box Protein O1 / metabolism
  • Gene Expression Regulation, Developmental
  • Humans
  • Mice
  • Nestin / genetics
  • Nestin / metabolism
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism
  • Neurogenesis* / genetics
  • Neurons* / cytology
  • Neurons* / metabolism
  • Wnt Signaling Pathway / genetics

Substances

  • Basic Helix-Loop-Helix Proteins
  • Forkhead Box Protein O1
  • Nestin
  • Ascl1 protein, mouse
  • Foxo1 protein, mouse
  • ASCL1 protein, human