A repressive role of enhancer of zeste homolog 2 in 11β-hydroxysteroid dehydrogenase type 2 expression in the human placenta

J Biol Chem. 2017 May 5;292(18):7578-7587. doi: 10.1074/jbc.M116.765800. Epub 2017 Mar 16.

Abstract

The expression of 11β-hydroxysteroid dehydrogenase type 2 (11β-HSD2), which acts as a placental glucocorticoid barrier, is silenced in cytotrophoblasts but substantially up-regulated during syncytialization. However, the repressive mechanism of 11β-HSD2 expression before syncytialization and how this repression is lifted during syncytialization remain mostly unresolved. Here we found that enhancer of zeste homolog 2 (EZH2) accounts for the silence of 11β-HSD2 expression via trimethylation of histone H3 lysine 27 at the promoter of the 11β-HSD2 gene. Further studies revealed that, upon syncytialization, human chorionic gonadotropin reduced the phosphorylation of retinoblastoma protein (pRB) via activation of the cAMP/PKA pathway, which sequesters E2F transcription factor 1 (E2F1), the transcription factor for EZH2 expression. As a result of inactivation of the pRB-E2F1-EZH2 pathway, the repressive marker trimethylation of histone H3 lysine 27 at the 11β-HSD2 promoter is removed, which leads to the robust expression of 11β-HSD2 during syncytialization.

Keywords: 11β-hydroxysteroid dehydrogenase 2; E2F transcription factor; EZH2; fetal development; glucocorticoid; histone methylation; histone modification; placenta; trophoblast.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 11-beta-Hydroxysteroid Dehydrogenase Type 2 / biosynthesis*
  • 11-beta-Hydroxysteroid Dehydrogenase Type 2 / genetics
  • Adult
  • Cyclic AMP / genetics
  • Cyclic AMP / metabolism
  • E2F1 Transcription Factor / genetics
  • E2F1 Transcription Factor / metabolism
  • Enhancer of Zeste Homolog 2 Protein / genetics
  • Enhancer of Zeste Homolog 2 Protein / metabolism*
  • Female
  • Gene Expression Regulation, Enzymologic / physiology*
  • Histones / genetics
  • Histones / metabolism
  • Humans
  • Methylation
  • Placenta / enzymology*
  • Pregnancy
  • Pregnancy Proteins / genetics
  • Pregnancy Proteins / metabolism*
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism*
  • Retinoblastoma Protein / genetics
  • Retinoblastoma Protein / metabolism
  • Second Messenger Systems / physiology*

Substances

  • E2F1 Transcription Factor
  • E2F1 protein, human
  • Histones
  • Pregnancy Proteins
  • Repressor Proteins
  • Retinoblastoma Protein
  • Cyclic AMP
  • 11-beta-Hydroxysteroid Dehydrogenase Type 2
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein