Shh signaling protects Atoh1 from degradation mediated by the E3 ubiquitin ligase Huwe1 in neural precursors

Dev Cell. 2014 Jun 23;29(6):649-61. doi: 10.1016/j.devcel.2014.05.014.

Abstract

Signaling networks controlled by Sonic hedgehog (SHH) and the transcription factor Atoh1 regulate the proliferation and differentiation of cerebellar granule neuron progenitors (GNPs). Deregulations in those developmental processes lead to medulloblastoma formation, the most common malignant brain tumor in childhood. Although the protein Atoh1 is a key factor during both cerebellar development and medulloblastoma formation, up-to-date detailed mechanisms underlying its function and regulation have remained poorly understood. Here, we report that SHH regulates Atoh1 stability by preventing its phosphodependent degradation by the E3 ubiquitin ligase Huwe1. Our results reveal that SHH and Atoh1 contribute to a positive autoregulatory loop promoting neuronal precursor expansion. Consequently, Huwe1 loss in mouse SHH medulloblastoma illustrates the disruption of this developmental mechanism in cancer. Hence, the crosstalk between SHH signaling and Atoh1 during cerebellar development highlights a collaborative network that could be further targeted in medulloblastoma.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / physiology*
  • Cell Differentiation
  • Cells, Cultured
  • Cerebellar Neoplasms / genetics
  • Cerebellar Neoplasms / metabolism
  • Cerebellar Neoplasms / mortality
  • Chromatography, Affinity
  • Female
  • Hedgehog Proteins / genetics
  • Hedgehog Proteins / metabolism*
  • Humans
  • Male
  • Medulloblastoma / genetics
  • Medulloblastoma / metabolism
  • Medulloblastoma / mortality
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neurons / cytology
  • Neurons / metabolism*
  • Patched Receptors
  • Phosphorylation
  • Proteolysis
  • Receptors, Cell Surface / physiology*
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Stem Cells / cytology
  • Stem Cells / metabolism*
  • Survival Rate
  • Tumor Suppressor Proteins
  • Ubiquitin-Protein Ligases / metabolism*
  • Ubiquitin-Protein Ligases / physiology*

Substances

  • Atoh1 protein, mouse
  • Basic Helix-Loop-Helix Transcription Factors
  • Hedgehog Proteins
  • Patched Receptors
  • Receptors, Cell Surface
  • Shh protein, mouse
  • Tumor Suppressor Proteins
  • HUWE1 protein, human
  • Huwe1 protein, mouse
  • Ubiquitin-Protein Ligases