The regulation of vascular endothelial growth factor by hypoxia and prostaglandin F₂α during human endometrial repair

J Clin Endocrinol Metab. 2011 Aug;96(8):2475-83. doi: 10.1210/jc.2010-2971. Epub 2011 Jun 15.

Abstract

Context: The human endometrium has an exceptional capacity for repeated repair after menses, but its regulation remains undefined. Premenstrually, progesterone levels fall and prostaglandin (PG) F₂α synthesis increases, causing spiral arteriole constriction. We hypothesized that progesterone withdrawal, PGF₂α, and hypoxia increase vascular endothelial growth factor (VEGF), an endometrial repair factor.

Design and results: Endometrial biopsies were collected (n = 47) with ethical approval and consent. VEGF mRNA, quantified by quantitative RT-PCR, was increased during menstruation (P < 0.01).VEGF protein was maximally secreted from proliferative endometrial explants. Treatment of an endometrial epithelial cell line and primary human endometrial stromal cells with 100 nm PGF₂α or hypoxia (0.5% O₂) resulted in significant increases in VEGF mRNA and protein. VEGF was maximal when cells were cotreated with PGF(2α) and hypoxia simultaneously (P < 0.05-0.001). Secretory-phase endometrial explants also showed an increase in VEGF with cotreatment (P < 0.05). However, proliferative-phase explants showed no increase in VEGF on treatment with PGF₂α and/or hypoxia. Proliferative tissue was induced to increase VEGF mRNA expression when exposed to progesterone and its withdrawal in vitro but only in the presence of hypoxia and PG. Hypoxia-inducible factor-1α (HIF-1α) silencing with RNA interference suppressed hypoxia-induced VEGF expression in endometrial cells but did not alter PGF₂α-induced VEGF expression.

Conclusions: Endometrial VEGF is increased at the time of endometrial repair. Progesterone withdrawal, PGF₂α, and hypoxia are necessary for this perimenstrual VEGF expression. Hypoxia acts via HIF-1α to increase VEGF, whereas PGF₂α acts in a HIF-1α-independent manner. Hence, two pathways regulate the expression of VEGF during endometrial repair.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Biopsy
  • Cells, Cultured
  • Cyclooxygenase Inhibitors / pharmacology
  • Dinoprost / metabolism*
  • Endometrium / cytology
  • Endometrium / drug effects
  • Endometrium / physiology*
  • Estradiol / blood
  • Female
  • Hormone Antagonists / pharmacology
  • Humans
  • Hypoxia / metabolism*
  • Hypoxia / physiopathology*
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Indomethacin / pharmacology
  • Menstrual Cycle / physiology*
  • Middle Aged
  • Mifepristone / pharmacology
  • Progesterone / antagonists & inhibitors
  • Progesterone / blood
  • RNA, Messenger / metabolism
  • Regeneration / physiology
  • Vascular Endothelial Growth Factor A / genetics*
  • Young Adult

Substances

  • Cyclooxygenase Inhibitors
  • HIF1A protein, human
  • Hormone Antagonists
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • RNA, Messenger
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Mifepristone
  • Progesterone
  • Estradiol
  • Dinoprost
  • Indomethacin