CCAAT/enhancer-binding protein α is epigenetically silenced by histone deacetylation in endometriosis and promotes the pathogenesis of endometriosis

J Clin Endocrinol Metab. 2013 Sep;98(9):E1474-82. doi: 10.1210/jc.2013-1608. Epub 2013 Jul 5.

Abstract

Context: Accumulating evidence suggests that various epigenetic aberrations play definite roles in the pathogenesis of endometriosis.

Objective: The objective of the study was to determine the epigenetically silenced genes by histone deacetylation in endometriosis.

Design: Histone deacetylase-1 target mRNAs that were up-regulated by valproic acid (VPA) treatment in endometriotic cyst stromal cells (ECSCs) were identified by a global mRNA microarray technique.

Results: We identified 5 candidate genes and chose CCAAT/enhancer-binding protein α (C/EBPα) for further functional experiments. C/EBPα mRNA and protein expression is attenuated in ECSCs, and the expression was up-regulated by VPA stimulation. Immunohistochemical stainings also confirmed the decreased staining for C/EBPα protein in endometriotic tissues. VPA treatment resulted in an accumulation of acetylated histones H3 and H4 in the promoter region of the C/EBPα gene in ECSCs. The compulsory expression of C/EBPα in ECSCs directed the inhibition of cell proliferation and the induction of apoptosis. C/EBPα knockdown by small interfering RNA directed the stimulation of cell proliferation and the resistance to apoptosis in normal eutopic endometrial stromal cells. The expressions of peroxisome proliferator-activated receptor-γ (PPARγ), period homolog 2 (PER2), p53, apoptosis-inducing factor, mitochondrion-associated 1 (AIFM1), Bax, caspase-8, caspase-10, p16(INK4a), p21(Waf1/Cip1), cyclin-dependent kinase (cdk) 2, and cdk4 were down-regulated by C/EBPα knockdown.

Conclusions: Our findings suggest that an epigenetically suppressed tumor suppressor gene is involved in the pathogenesis of endometriosis by creating the proliferative, antiapoptotic, and other disease-specific characteristics of endometriosis. The results also suggest that histone deacetylase inhibitors are promising agents for the treatment of endometriosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Adult
  • Apoptosis / drug effects
  • Apoptosis / physiology
  • Apoptosis Inducing Factor / genetics
  • Apoptosis Inducing Factor / metabolism
  • CCAAT-Enhancer-Binding Protein-alpha / genetics*
  • CCAAT-Enhancer-Binding Protein-alpha / metabolism
  • Caspases / genetics
  • Caspases / metabolism
  • Endometriosis / genetics*
  • Endometriosis / metabolism
  • Epigenesis, Genetic
  • Female
  • Gene Silencing
  • Histones / genetics*
  • Histones / metabolism
  • Humans
  • Ovarian Diseases / genetics*
  • Ovarian Diseases / metabolism
  • PPAR gamma / genetics
  • PPAR gamma / metabolism
  • Period Circadian Proteins / genetics
  • Period Circadian Proteins / metabolism
  • Stromal Cells / drug effects
  • Stromal Cells / metabolism*
  • Valproic Acid / pharmacology
  • bcl-2-Associated X Protein / genetics
  • bcl-2-Associated X Protein / metabolism

Substances

  • AIFM1 protein, human
  • Apoptosis Inducing Factor
  • CCAAT-Enhancer-Binding Protein-alpha
  • Histones
  • PER2 protein, human
  • PPAR gamma
  • Period Circadian Proteins
  • bcl-2-Associated X Protein
  • Valproic Acid
  • Caspases