Peroxisome proliferator-activated receptor gamma is a target of progesterone regulation in the preovulatory follicles and controls ovulation in mice

Mol Cell Biol. 2008 Mar;28(5):1770-82. doi: 10.1128/MCB.01556-07. Epub 2008 Jan 2.

Abstract

The progesterone receptor (PR) plays a critical role during ovulation. Mice lacking the PR gene are anovulatory due to a failure in the rupture of the preovulatory follicles. The pathways that operate downstream of PR to control ovulation are poorly understood. Using gene expression profiling, we identified peroxisome proliferator-activated receptor gamma (PPARgamma) as a target of regulation by PR in the granulosa cells of the preovulatory follicles during the ovulatory process. To investigate the function of PPARgamma during ovulation, we created a conditional knockout mouse in which this gene was deleted via Cre-Lox-mediated excision in granulosa cells. When these mutant mice were subjected to gonadotropin-induced superovulation, the preovulatory follicles failed to rupture and the number of eggs released from the mutant ovaries declined drastically. Gene expression analysis identified endothelin-2, interleukin-6, and cyclic GMP-dependent protein kinase II as novel targets of regulation by PPARgamma in the ovary. Our studies also suggested that cycloxygenase 2-derived metabolites of long-chain fatty acids function as endogenous activating ligands of PPARgamma in the preovulatory follicles. Collectively, these studies revealed that PPARgamma is a key mediator of the biological actions of PR in the granulosa cells and activation of its downstream pathways critically controls ovulation.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Anilides / pharmacology
  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Cells, Cultured
  • Colforsin / pharmacology
  • Culture Media, Serum-Free
  • Dose-Response Relationship, Drug
  • Female
  • Gene Deletion
  • Gene Expression Profiling
  • Gonadotropins / pharmacology
  • Granulosa Cells / metabolism
  • Hormone Antagonists / pharmacology
  • Immunohistochemistry
  • In Situ Hybridization
  • Indomethacin / pharmacology
  • Mice
  • Mice, Knockout
  • Mifepristone / pharmacology
  • Models, Genetic
  • Nitrobenzenes / pharmacology
  • Ovarian Follicle / metabolism*
  • Ovary / metabolism
  • Ovulation / drug effects
  • Ovulation / physiology*
  • PPAR gamma / genetics
  • PPAR gamma / metabolism*
  • Progesterone / physiology*
  • Receptors, Progesterone / genetics
  • Receptors, Progesterone / metabolism
  • Sulfonamides / pharmacology
  • Tetradecanoylphorbol Acetate / pharmacology
  • Time Factors

Substances

  • 2-chloro-5-nitrobenzanilide
  • Anilides
  • Anti-Inflammatory Agents, Non-Steroidal
  • Culture Media, Serum-Free
  • Gonadotropins
  • Hormone Antagonists
  • Nitrobenzenes
  • PPAR gamma
  • Receptors, Progesterone
  • Sulfonamides
  • N-(2-cyclohexyloxy-4-nitrophenyl)methanesulfonamide
  • Colforsin
  • Mifepristone
  • Progesterone
  • Tetradecanoylphorbol Acetate
  • Indomethacin