HIF1 activity in granulosa cells is required for FSH-regulated Vegfa expression and follicle survival in mice

Biol Reprod. 2014 Jun;90(6):135. doi: 10.1095/biolreprod.113.115634. Epub 2014 May 22.

Abstract

Recent evidence has suggested that vascular endothelial growth factor A (VEGFA) is an important regulator of ovarian follicle development and survival. Both LH and FSH regulate Vegfa expression in granulosa cells and signal via the transcription factor hypoxia inducible factor 1 (HIF1). To further study the mechanism of action of HIF1 in the regulation of Vegfa, we studied Vegfa(delta/delta) mice, which lack a hypoxia response element in the Vegfa promoter. Granulosa cells from Vegfa(delta/delta) mice failed to respond to FSH or LH with an increase in Vegfa mRNA expression in vitro, and granulosa cells isolated from eCG-treated immature Vegfa(delta/delta) mice had significantly lower Vegfa mRNA levels compared to controls. However, normal Vegfa mRNA levels were detected in the granulosa cells from immature Vegfa(delta/delta) mice following hCG treatment. Vegfa(delta/delta) females produced infrequent litters, and their pups died shortly after birth. Ovaries from Vegfa(delta/delta) mice were much smaller than controls and contained few antral follicles and corpora lutea. Antral follicles numbers were decreased by nearly 50% in ovaries from Vegfa(delta/delta) mice relative to controls, and 74% of antral follicles in Vegfa(delta/delta) ovaries were atretic. Serum progesterone levels in adult Vegfa(delta/delta) females were significantly lower, apparently reflecting reduced numbers of corpora lutea. This study demonstrates for the first time the requirement of HIF1 for FSH-regulated Vegfa expression in vivo and that HIF1 acts via a single hypoxia response element in the Vegfa promoter to exert its regulatory functions. Our findings also further define the physiological role of VEGFA in follicle development.

Keywords: HIF1; VEGFA; follicular development; granulosa cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aryl Hydrocarbon Receptor Nuclear Translocator / genetics
  • Aryl Hydrocarbon Receptor Nuclear Translocator / metabolism*
  • Cell Survival / physiology
  • Cells, Cultured
  • Corpus Luteum / physiology
  • Female
  • Follicle Stimulating Hormone / metabolism*
  • Gonadotropins / metabolism
  • Granulosa Cells / cytology
  • Granulosa Cells / physiology*
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Organ Size / physiology
  • Ovarian Follicle / cytology
  • Ovarian Follicle / physiology*
  • Pregnancy
  • Promoter Regions, Genetic / physiology
  • RNA, Messenger / metabolism
  • Reproduction / physiology
  • Vascular Endothelial Growth Factor A / genetics
  • Vascular Endothelial Growth Factor A / metabolism*

Substances

  • Arnt protein, mouse
  • Gonadotropins
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • RNA, Messenger
  • Vascular Endothelial Growth Factor A
  • vascular endothelial growth factor A, mouse
  • Aryl Hydrocarbon Receptor Nuclear Translocator
  • Follicle Stimulating Hormone