Follicle stimulating hormone controls granulosa cell glutamine synthesis to regulate ovulation

Protein Cell. 2024 Jul 1;15(7):512-529. doi: 10.1093/procel/pwad065.

Abstract

Polycystic ovary syndrome (PCOS) is the leading cause of anovulatory infertility. Inadequate understanding of the ovulation drivers hinders PCOS intervention. Herein, we report that follicle stimulating hormone (FSH) controls follicular fluid (FF) glutamine levels to determine ovulation. Murine ovulation starts from FF-exposing granulosa cell (GC) apoptosis. FF glutamine, which decreases in pre-ovulation porcine FF, elevates in PCOS patients FF. High-glutamine chow to elevate FF glutamine inhibits mouse GC apoptosis and induces hormonal, metabolic, and morphologic PCOS traits. Mechanistically, follicle-development-driving FSH promotes GC glutamine synthesis to elevate FF glutamine, which maintain follicle wall integrity by inhibiting GC apoptosis through inactivating ASK1-JNK apoptotic pathway. FSH and glutamine inhibit the rapture of cultured murine follicles. Glutamine removal or ASK1-JNK pathway activation with metformin or AT-101 reversed PCOS traits in PCOS models that are induced with either glutamine or EsR1-KO. These suggest that glutamine, FSH, and ASK1-JNK pathway are targetable to alleviate PCOS.

Keywords: FSH; PCOS; glutamine; granulosa cells; ovulation.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Female
  • Follicle Stimulating Hormone* / metabolism
  • Glutamine* / metabolism
  • Granulosa Cells* / drug effects
  • Granulosa Cells* / metabolism
  • Humans
  • MAP Kinase Kinase Kinase 5 / genetics
  • MAP Kinase Kinase Kinase 5 / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Ovulation*
  • Polycystic Ovary Syndrome* / metabolism
  • Polycystic Ovary Syndrome* / pathology
  • Swine

Substances

  • Glutamine
  • Follicle Stimulating Hormone
  • MAP Kinase Kinase Kinase 5
  • Map3k5 protein, mouse