Context-Specific Effects of TGF-β/SMAD3 in Cancer Are Modulated by the Epigenome

Cell Rep. 2015 Dec 22;13(11):2480-2490. doi: 10.1016/j.celrep.2015.11.040. Epub 2015 Dec 10.

Abstract

The transforming growth factor beta (TGF-β) signaling pathway exerts opposing effects on cancer cells, acting as either a tumor promoter or a tumor suppressor. Here, we show that these opposing effects are a result of the synergy between SMAD3, a downstream effector of TGF-β signaling, and the distinct epigenomes of breast-tumor-initiating cells (BTICs). These effects of TGF-β are associated with distinct gene expression programs, but genomic SMAD3 binding patterns are highly similar in the BTIC-promoting and BTIC-suppressing contexts. Our data show cell-type-specific patterns of DNA and histone modifications provide a modulatory layer by determining accessibility of genes to regulation by TGF-β/SMAD3. LBH, one such context-specific target gene, is regulated according to its DNA methylation status and is crucial for TGF-β-dependent promotion of BTICs. Overall, these results reveal that the epigenome plays a central and previously overlooked role in shaping the context-specific effects of TGF-β in cancer.

MeSH terms

  • Binding Sites
  • Cell Line, Tumor
  • DNA / chemistry
  • DNA / metabolism
  • DNA Methylation
  • Epigenesis, Genetic
  • Histones / metabolism
  • Humans
  • Neoplastic Stem Cells / cytology
  • Neoplastic Stem Cells / metabolism
  • Promoter Regions, Genetic
  • Protein Binding
  • RNA Interference
  • RNA, Small Interfering / metabolism
  • Signal Transduction / drug effects*
  • Smad2 Protein / metabolism
  • Smad3 Protein / metabolism*
  • Trans-Activators / antagonists & inhibitors
  • Trans-Activators / genetics
  • Trans-Activators / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transforming Growth Factor beta / metabolism
  • Transforming Growth Factor beta / pharmacology*

Substances

  • Histones
  • LBH protein, human
  • RNA, Small Interfering
  • Smad2 Protein
  • Smad3 Protein
  • Trans-Activators
  • Transcription Factors
  • Transforming Growth Factor beta
  • VGLL3 protein, human
  • DNA