A β-catenin-driven switch in TCF/LEF transcription factor binding to DNA target sites promotes commitment of mammalian nephron progenitor cells

Elife. 2021 Feb 15:10:e64444. doi: 10.7554/eLife.64444.

Abstract

The canonical Wnt pathway transcriptional co-activator β-catenin regulates self-renewal and differentiation of mammalian nephron progenitor cells (NPCs). We modulated β-catenin levels in NPC cultures using the GSK3 inhibitor CHIR99021 (CHIR) to examine opposing developmental actions of β-catenin. Low CHIR-mediated maintenance and expansion of NPCs are independent of direct engagement of TCF/LEF/β-catenin transcriptional complexes at low CHIR-dependent cell-cycle targets. In contrast, in high CHIR, TCF7/LEF1/β-catenin complexes replaced TCF7L1/TCF7L2 binding on enhancers of differentiation-promoting target genes. Chromosome confirmation studies showed pre-established promoter-enhancer connections to these target genes in NPCs. High CHIR-associated de novo looping was observed in positive transcriptional feedback regulation to the canonical Wnt pathway. Thus, β-catenin's direct transcriptional role is restricted to the induction of NPCs, where rising β-catenin levels switch inhibitory TCF7L1/TCF7L2 complexes to activating LEF1/TCF7 complexes at primed gene targets poised for rapid initiation of a nephrogenic program.

Keywords: TCF/LEF factors; Wnt signaling; developmental biology; kidney development; mouse; stem cells; transcriptional regulation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Differentiation
  • Cells, Cultured
  • Gene Expression Regulation
  • Lymphoid Enhancer-Binding Factor 1 / genetics
  • Lymphoid Enhancer-Binding Factor 1 / metabolism*
  • Mice
  • Nephrons / cytology
  • Nephrons / embryology
  • Nephrons / metabolism*
  • Promoter Regions, Genetic
  • Protein Binding
  • Stem Cells / cytology
  • Stem Cells / metabolism*
  • Transcription Factor 7-Like 1 Protein / genetics
  • Transcription Factor 7-Like 1 Protein / metabolism*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • beta Catenin / metabolism*

Substances

  • LZTR1 protein, mouse
  • Lymphoid Enhancer-Binding Factor 1
  • Tcf7l1 protein, mouse
  • Transcription Factor 7-Like 1 Protein
  • Transcription Factors
  • beta Catenin

Associated data

  • GEO/GSE131119