Insulin Reduces Reaction of Follicular Granulosa Cells to FSH Stimulation in Women With Obesity-Related Infertility During IVF

J Clin Endocrinol Metab. 2019 Jul 1;104(7):2547-2560. doi: 10.1210/jc.2018-00686.

Abstract

Context: Women with obesity usually need larger doses of FSH for ovarian stimulation, resulting in poor outcomes; however, the mechanism is still unclear.

Objective: To investigate the molecular regulation of FSH receptor (FSHR) expression associated with obesity.

Design: Case-control study to improve in vitro fertilization (IVF) outcomes.

Patients: Women with obesity (82) and women who were overweight (457) undergoing IVF and 1790 age-matched controls with normal weight from our reproductive medicine center.

Main outcome measures: FSHR expression was decreased in parallel with body mass index (BMI), whereas the estradiol (E2) level on the human chorionic gonadotropin (hCG) trigger day was significantly lower.

Results: FSHR expression in human granulosa cells (hGCs), both mRNA (P = 0.02) and protein (P = 0.001) levels, was decreased in women who were overweight or obese. Both insulin (P < 0.001) and glucose (P = 0.0017) levels were positively correlated with BMI in fasting blood and follicle fluids (FFs) but not with FFs leptin level. We treated human granulosa-like tumor cells (KGN) cells with insulin; E2 production was compromised; the level of phosphorylated (p)-protein kinase B (p-Akt2) decreased, whereas p-glycogen synthase kinase 3 (GSK3) increased; and there were similar changes in hGCs from women with obesity. Stimulated hGCs from women with obesity with compound 21 (CP21), an inhibitor of GSK3β, resulted in upregulated β-catenin activation and increased FSHR expression. CP21 also increased the expression of insulin receptor substrate 1 and phosphatidylinositol 3-kinase (PI3K), as well as p-Akt2.

Conclusions: Women with obesity in IVF were associated with reduced FSHR expression and E2 production caused by a dysfunctional insulin pathway. Decreased FSHR expression in hGCs from women with obesity and insulin-treated KGN cells could be rescued by an inhibitor of GSK3β, which might be a potential target for the improvement of the impaired FSH-stimulation response in women with obesity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Case-Control Studies
  • Dose-Response Relationship, Drug
  • Estradiol / metabolism
  • Female
  • Fertilization in Vitro / methods
  • Follicle Stimulating Hormone / administration & dosage*
  • Follicular Fluid / metabolism
  • Glycogen Synthase Kinase 3 beta / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 beta / metabolism
  • Granulosa Cells / drug effects
  • Granulosa Cells / metabolism
  • Humans
  • Infertility, Female / blood
  • Infertility, Female / complications
  • Infertility, Female / therapy*
  • Insulin / analysis
  • Insulin / metabolism*
  • Leptin / analysis
  • Leptin / metabolism
  • Obesity / blood
  • Obesity / complications
  • Obesity / metabolism*
  • Ovulation Induction / methods
  • Receptors, FSH / metabolism*
  • Treatment Outcome

Substances

  • Insulin
  • Leptin
  • Receptors, FSH
  • Estradiol
  • Follicle Stimulating Hormone
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta