Suppression of COUP-TFII by proinflammatory cytokines contributes to the pathogenesis of endometriosis

J Clin Endocrinol Metab. 2014 Mar;99(3):E427-37. doi: 10.1210/jc.2013-3717. Epub 2014 Jan 1.

Abstract

Context: Endometriosis is one of the most common gynecological diseases in women with a prevalence rate of approximately 10%. Chronic pelvic inflammation has been observed in patients with endometriosis and is associated with disease severity. However, how pelvic inflammation promotes endometriosis progression remains unknown.

Objective: The objective of the study was to investigate the regulatory network of proinflammatory cytokines in endometriosis progression.

Design, settings, and patients: Immunostaining of human endometrial (n = 21) and endometriotic (n = 36) sections, quantitative RT-PCR, Western blotting, chromatin immunoprecipitation, and luciferase reporter assays in primary culture human endometrial stromal cells were performed. Autologous transplantation of uterine endometrium from control chicken ovalbumin upstream promoter-transcription factor II [(COUP-TFII) flox/flox] and uterus-specific COUP-TFII knockout mice was performed.

Results: Expression of COUP-TFII was significantly reduced in endometriotic stroma. Reduction of COUP-TFII in endometriotic stromal cells was mediated by proinflammatory cytokines including IL-1β, TNF-α, and TGF-β1 via a common effector, microRNA-302a. Treatment with these proinflammatory cytokines increased the expression of microRNA-302a, which targets the 3'untranslated region of COUP-TFII to cause its down-regulation. Intriguingly, down-regulation of COUP-TFII in endometrial stromal cells resulted in de-repression of cyclooxygenase-2 (COX-2). Further investigation demonstrated that COUP-TFII directly binds to COX-2 promoter to inhibit its transcription. Forced expression of COUP-TFII inhibited IL-1β-induced COX-2 up-regulation, whereas the knockdown of COUP-TFII augmented this effect.

Conclusion: Because overexpression of COX-2 has been demonstrated to be a master regulator in endometriosis progression, our data demonstrate the critical function of proinflammatory cytokines and the COUP-TFII regulatory gene network in the progression of endometriosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • COUP Transcription Factor II / genetics*
  • COUP Transcription Factor II / metabolism
  • Cells, Cultured
  • Cytokines / pharmacology
  • Cytokines / physiology*
  • Down-Regulation / drug effects
  • Down-Regulation / genetics
  • Endometriosis / genetics*
  • Endometriosis / metabolism
  • Endometrium / metabolism
  • Endometrium / pathology
  • Female
  • Gene Regulatory Networks / drug effects
  • Humans
  • Inflammation Mediators / pharmacology
  • Inflammation Mediators / physiology*
  • Mice
  • Mice, Knockout
  • Stromal Cells / metabolism
  • Stromal Cells / pathology
  • Uterine Diseases / genetics*
  • Uterine Diseases / metabolism

Substances

  • COUP Transcription Factor II
  • Cytokines
  • Inflammation Mediators
  • Nr2f2 protein, mouse