Heterarchy of transcription factors driving basal and luminal cell phenotypes in human urothelium

Cell Death Differ. 2017 May;24(5):809-818. doi: 10.1038/cdd.2017.10. Epub 2017 Mar 10.

Abstract

Cell differentiation is affected by complex networks of transcription factors that co-ordinate re-organisation of the chromatin landscape. The hierarchies of these relationships can be difficult to dissect. During in vitro differentiation of normal human uro-epithelial cells, formaldehyde-assisted isolation of regulatory elements (FAIRE-seq) and RNA-seq was used to identify alterations in chromatin accessibility and gene expression changes following activation of the nuclear receptor peroxisome proliferator-activated receptor gamma (PPARγ) as a differentiation-initiating event. Regions of chromatin identified by FAIRE-seq, as having altered accessibility during differentiation, were found to be enriched with sequence-specific binding motifs for transcription factors predicted to be involved in driving basal and differentiated urothelial cell phenotypes, including forkhead box A1 (FOXA1), P63, GRHL2, CTCF and GATA-binding protein 3 (GATA3). In addition, co-occurrence of GATA3 motifs was observed within subsets of differentiation-specific peaks containing P63 or FOXA1. Changes in abundance of GRHL2, GATA3 and P63 were observed in immunoblots of chromatin-enriched extracts. Transient siRNA knockdown of P63 revealed that P63 favoured a basal-like phenotype by inhibiting differentiation and promoting expression of basal marker genes. GATA3 siRNA prevented differentiation-associated downregulation of P63 protein and transcript, and demonstrated positive feedback of GATA3 on PPARG transcript, but showed no effect on FOXA1 transcript or protein expression. This approach indicates that as a transcriptionally regulated programme, urothelial differentiation operates as a heterarchy, wherein GATA3 is able to co-operate with FOXA1 to drive expression of luminal marker genes, but that P63 has potential to transrepress expression of the same genes.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • CCCTC-Binding Factor / genetics
  • CCCTC-Binding Factor / metabolism
  • Cell Differentiation / genetics*
  • Cell Line
  • Chromatin / chemistry
  • Chromatin / metabolism
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Epithelial Cells / cytology*
  • Epithelial Cells / metabolism*
  • Formaldehyde / chemistry
  • GATA3 Transcription Factor / antagonists & inhibitors
  • GATA3 Transcription Factor / genetics*
  • GATA3 Transcription Factor / metabolism
  • Gene Expression Regulation
  • Hepatocyte Nuclear Factor 3-alpha / antagonists & inhibitors
  • Hepatocyte Nuclear Factor 3-alpha / genetics*
  • Hepatocyte Nuclear Factor 3-alpha / metabolism
  • Humans
  • PPAR gamma / genetics
  • PPAR gamma / metabolism
  • Phenotype
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • RNA, Small Interfering / genetics
  • RNA, Small Interfering / metabolism
  • Regulatory Elements, Transcriptional
  • Sequence Analysis, RNA
  • Signal Transduction
  • Transcription Factors / antagonists & inhibitors
  • Transcription Factors / genetics*
  • Transcription Factors / metabolism
  • Tumor Suppressor Proteins / antagonists & inhibitors
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism
  • Urothelium / cytology
  • Urothelium / metabolism

Substances

  • CCCTC-Binding Factor
  • CTCF protein, human
  • Chromatin
  • DNA-Binding Proteins
  • FOXA1 protein, human
  • GATA3 Transcription Factor
  • GATA3 protein, human
  • GRHL2 protein, human
  • Hepatocyte Nuclear Factor 3-alpha
  • PPAR gamma
  • RNA, Messenger
  • RNA, Small Interfering
  • TP63 protein, human
  • Transcription Factors
  • Tumor Suppressor Proteins
  • Formaldehyde