Manipulating Wnt signaling at different subcellular levels affects the fate of neonatal neural stem/progenitor cells

Brain Res. 2016 Nov 15:1651:73-87. doi: 10.1016/j.brainres.2016.09.026. Epub 2016 Sep 19.

Abstract

The canonical Wnt signaling pathway plays an important role in embryogenesis, and the establishment of neurogenic niches. It is involved in proliferation and differentiation of neural progenitors, since elevated Wnt/β-catenin signaling promotes differentiation of neural stem/progenitor cells (NS/PCs1) towards neuroblasts. Nevertheless, it remains elusive how the differentiation program of neural progenitors is influenced by the Wnt signaling output. Using transgenic mouse models, we found that in vitro activation of Wnt signaling resulted in higher expression of β-catenin protein and Wnt/β-catenin target genes, while Wnt signaling inhibition resulted in the reverse effect. Within differentiated cells, we identified three electrophysiologically and immunocytochemically distinct cell types, whose incidence was markedly affected by the Wnt signaling output. Activation of the pathway suppressed gliogenesis, and promoted differentiation of NS/PCs towards a neuronal phenotype, while its inhibition led to suppressed neurogenesis and increased counts of cells of glial phenotype. Moreover, Wnt signaling hyperactivation resulted in an increased incidence of cells expressing outwardly rectifying K+ currents, together with inwardly rectifying Na+ currents, a typical current pattern of immature neurons, while blocking the pathway led to the opposite effect. Taken together, our data indicate that the Wnt signaling pathway orchestrates neonatal NS/PCs differentiation towards cells with neuronal characteristics, which might be important for nervous tissue regeneration during central nervous system disorders. Furthermore, the transgenic mouse strains used in this study may serve as a convenient tool to manipulate β-catenin-dependent signaling in neural progenitors in the neonatal brain.

Keywords: Gliogenesis; Ion channel; Neonatal mouse; Neurogenesis; Patch-clamp technique; β-catenin signaling.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / metabolism
  • Brain / cytology
  • Brain / metabolism
  • Cells, Cultured
  • Immunohistochemistry
  • Intercellular Signaling Peptides and Proteins / genetics
  • Intercellular Signaling Peptides and Proteins / metabolism
  • Membrane Potentials / physiology
  • Mice, Transgenic
  • Neural Stem Cells / cytology
  • Neural Stem Cells / metabolism*
  • Neurogenesis / physiology*
  • Neuroglia / cytology
  • Neuroglia / metabolism*
  • Neurons / cytology
  • Neurons / metabolism*
  • Patch-Clamp Techniques
  • Transcription Factor 4
  • Wnt Signaling Pathway / physiology*
  • beta Catenin / genetics
  • beta Catenin / metabolism

Substances

  • Basic Helix-Loop-Helix Leucine Zipper Transcription Factors
  • CTNNB1 protein, mouse
  • Dkk1 protein, mouse
  • Intercellular Signaling Peptides and Proteins
  • Tcf4 protein, mouse
  • Transcription Factor 4
  • beta Catenin