The coordinated p53 and estrogen receptor cis-regulation at an FLT1 promoter SNP is specific to genotoxic stress and estrogenic compound

PLoS One. 2010 Apr 21;5(4):e10236. doi: 10.1371/journal.pone.0010236.

Abstract

Background: Recently, we established that a C>T single nucleotide polymorphism (SNP) in the promoter of the VEGF receptor FLT1 gene generates a (1/2) site p53 response element (RE-T) that results in p53 responsiveness of the promoter. The transcriptional control required an estrogen receptor (ER) (1/2) site response element (ERE1) 225 nt upstream to the RE-T.

Methodology/principal findings: Here we report the identification of a second ER (1/2) site (ERE2) located 145 bp downstream of the RE-T and establish that both EREs can impact p53-mediated transactivation of FLT1-T in a manner that is cell type and ER level dependent. Gene reporter assays and ChIP experiments conducted in the breast cancer-derived MCF7 cells revealed that the ERE2 site was sufficient for p53-mediated ERalpha recruitment and transactivation of the FLT1-T promoter/reporter construct. Surprisingly, unlike the case for other p53 target promoters, p53-mediated transactivation of FLT1-T constructs or expression of the endogenous FLT1 gene, as well as binding of p53 and ER at the promoter constructs, was inducible by doxorubicin but not by 5-fluorouracil. Furthermore, ER activity at FLT1-T was differentially affected by ER ligands, compared to a control TFF1/pS2 ER target promoter. The p53-related transcription factors (TFs) p73 and p63 had no effect on FLT1 transactivation.

Conclusions/significance: We establish a new dimension to the p53 master regulatory network where p53-mediated transcription from a (1/2) site RE can be determined by ER binding at one or more cis-acting EREs in manner that is dependent on level of ER protein, the type of ER ligand and the specific p53-inducing agent.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • DNA Damage / genetics
  • Doxorubicin / pharmacology
  • Enhancer Elements, Genetic
  • Estrogens / pharmacology
  • Fluorouracil / pharmacology
  • Gene Expression Regulation / drug effects
  • Gene Regulatory Networks
  • Humans
  • Polymorphism, Single Nucleotide*
  • Promoter Regions, Genetic / genetics*
  • Receptors, Estrogen / genetics*
  • Response Elements / genetics
  • Transcriptional Activation
  • Tumor Suppressor Protein p53 / genetics*
  • Vascular Endothelial Growth Factor Receptor-1 / genetics*

Substances

  • Estrogens
  • Receptors, Estrogen
  • Tumor Suppressor Protein p53
  • Doxorubicin
  • FLT1 protein, human
  • Vascular Endothelial Growth Factor Receptor-1
  • Fluorouracil