Dose-dependent responses to canonical Wnt transcriptional complexes in the regulation of mammalian nephron progenitors

Development. 2024 Sep 15;151(18):dev202279. doi: 10.1242/dev.202279. Epub 2024 Sep 30.

Abstract

In vivo and in vitro studies argue that concentration-dependent Wnt signaling regulates mammalian nephron progenitor cell (NPC) programs. Canonical Wnt signaling is regulated through the stabilization of β-catenin, a transcriptional co-activator when complexed with Lef/Tcf DNA-binding partners. Using the GSK3β inhibitor CHIR99021 (CHIR) to block GSK3β-dependent destruction of β-catenin, we examined dose-dependent responses to β-catenin in mouse NPCs, using mRNA transduction to modify gene expression. Low CHIR-dependent proliferation of NPCs was blocked on β-catenin removal, with evidence of NPCs arresting at the G2-M transition. While NPC identity was maintained following β-catenin removal, mRNA-seq identified low CHIR and β-catenin dependent genes. High CHIR activated nephrogenesis. Nephrogenic programming was dependent on Lef/Tcf factors and β-catenin transcriptional activity. Molecular and cellular features of early nephrogenesis were driven in the absence of CHIR by a mutated stabilized form of β-catenin. Chromatin association studies indicate low and high CHIR response genes are likely direct targets of canonical Wnt transcriptional complexes. Together, these studies provide evidence for concentration-dependent Wnt signaling in the regulation of NPCs and provide new insight into Wnt targets initiating mammalian nephrogenesis.

Keywords: Differentiation; Induction; Nephron progenitor cells; Proliferation; Wnt/β-catenin signaling.

MeSH terms

  • Animals
  • Cell Proliferation
  • Gene Expression Regulation, Developmental
  • Glycogen Synthase Kinase 3 beta / genetics
  • Glycogen Synthase Kinase 3 beta / metabolism
  • Mice
  • Nephrons* / cytology
  • Nephrons* / metabolism
  • Organogenesis / genetics
  • Pyridines / pharmacology
  • Pyrimidines / pharmacology
  • Stem Cells* / cytology
  • Stem Cells* / metabolism
  • Transcription, Genetic
  • Wnt Signaling Pathway*
  • beta Catenin* / metabolism

Substances

  • beta Catenin
  • Chir 99021
  • Pyrimidines
  • Pyridines
  • Glycogen Synthase Kinase 3 beta