Oxygen Tension and the VHL-Hif1α Pathway Determine Onset of Neuronal Polarization and Cerebellar Germinal Zone Exit

Neuron. 2020 May 20;106(4):607-623.e5. doi: 10.1016/j.neuron.2020.02.025. Epub 2020 Mar 16.

Abstract

Postnatal brain circuit assembly is driven by temporally regulated intrinsic and cell-extrinsic cues that organize neurogenesis, migration, and axo-dendritic specification in post-mitotic neurons. While cell polarity is an intrinsic organizer of morphogenic events, environmental cues in the germinal zone (GZ) instructing neuron polarization and their coupling during postnatal development are unclear. We report that oxygen tension, which rises at birth, and the von Hippel-Lindau (VHL)-hypoxia-inducible factor 1α (Hif1α) pathway regulate polarization and maturation of post-mitotic cerebellar granule neurons (CGNs). At early postnatal stages with low GZ vascularization, Hif1α restrains CGN-progenitor cell-cycle exit. Unexpectedly, cell-intrinsic VHL-Hif1α pathway activation also delays the timing of CGN differentiation, germinal zone exit, and migration initiation through transcriptional repression of the partitioning-defective (Pard) complex. As vascularization proceeds, these inhibitory mechanisms are downregulated, implicating increasing oxygen tension as a critical switch for neuronal polarization and cerebellar GZ exit.

Keywords: Hif1 Pathway; Integrin; Pard Complex; Zeb1; cell polarity; neuronal differentiation; vascularization.

Publication types

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

MeSH terms

  • Animals
  • Cell Differentiation / physiology
  • Cell Polarity / physiology*
  • Cerebellum / growth & development*
  • Cerebellum / physiology*
  • Female
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Male
  • Mice
  • Neurogenesis / physiology*
  • Neurons / cytology*
  • Neurons / metabolism
  • Oxygen
  • Signal Transduction / physiology
  • Von Hippel-Lindau Tumor Suppressor Protein / metabolism

Substances

  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Von Hippel-Lindau Tumor Suppressor Protein
  • Oxygen