Chromatin immunoprecipitation on microarray analysis of Smad2/3 binding sites reveals roles of ETS1 and TFAP2A in transforming growth factor beta signaling

Mol Cell Biol. 2009 Jan;29(1):172-86. doi: 10.1128/MCB.01038-08. Epub 2008 Oct 27.

Abstract

The Smad2 and Smad3 (Smad2/3) proteins are principally involved in the transmission of transforming growth factor beta (TGF-beta) signaling from the plasma membrane to the nucleus. Many transcription factors have been shown to cooperate with the Smad2/3 proteins in regulating the transcription of target genes, enabling appropriate gene expression by cells. Here we identified 1,787 Smad2/3 binding sites in the promoter regions of over 25,500 genes by chromatin immunoprecipitation on microarray in HaCaT keratinocytes. Binding elements for the v-ets erythroblastosis virus E26 oncogene homolog (ETS) and transcription factor AP-2 (TFAP2) were significantly enriched in Smad2/3 binding sites, and knockdown of either ETS1 or TFAP2A resulted in overall alteration of TGF-beta-induced transcription, suggesting general roles for ETS1 and TFAP2A in the transcription induced by TGF-beta-Smad pathways. We identified novel Smad binding sites in the CDKN1A gene where Smad2/3 binding was regulated by ETS1 and TFAP2A. Moreover, we showed that small interfering RNAs for ETS1 and TFAP2A affected TGF-beta-induced cytostasis. We also analyzed Smad2- or Smad3-specific target genes regulated by TGF-beta and found that their specificity did not appear to be solely determined by the amounts of the Smad2/3 proteins bound to the promoters. These findings reveal novel regulatory mechanisms of Smad2/3-induced transcription and provide an essential resource for understanding their roles.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Binding Sites
  • Cell Death / drug effects
  • Cell Line
  • Chromatin Immunoprecipitation*
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism
  • Gene Expression Profiling
  • Gene Knockdown Techniques
  • Humans
  • Introns / genetics
  • Microarray Analysis*
  • Promoter Regions, Genetic
  • Proto-Oncogene Protein c-ets-1 / metabolism*
  • Proto-Oncogene Proteins c-jun / metabolism
  • Signal Transduction / drug effects
  • Smad2 Protein / metabolism*
  • Smad3 Protein / metabolism*
  • Transcription Factor AP-1 / metabolism
  • Transcription Factor AP-2 / metabolism*
  • Transcription Initiation Site
  • Transcription, Genetic / drug effects
  • Transforming Growth Factor beta / metabolism*
  • Transforming Growth Factor beta / pharmacology
  • Up-Regulation / drug effects

Substances

  • CDKN1A protein, human
  • Cyclin-Dependent Kinase Inhibitor p21
  • ETS1 protein, human
  • Proto-Oncogene Protein c-ets-1
  • Proto-Oncogene Proteins c-jun
  • SMAD2 protein, human
  • SMAD3 protein, human
  • Smad2 Protein
  • Smad3 Protein
  • TFAP2A protein, human
  • Transcription Factor AP-1
  • Transcription Factor AP-2
  • Transforming Growth Factor beta