PLIN2 Functions As a Novel Link Between Progesterone Signaling and Metabolism in Uterine Leiomyoma Cells

J Clin Endocrinol Metab. 2019 Dec 1;104(12):6256-6264. doi: 10.1210/jc.2019-00762.

Abstract

Context: Uterine leiomyoma (fibroids) are the most common tumors in women. Recently, perilipin-2 (PLIN2) was identified as a critical target gene of the progesterone receptor; however, its function in the pathogenesis of fibroids is unknown.

Objective: To determine the function of PLIN2 in leiomyoma cells.

Design: Tissue and primary cells from leiomyoma and myometrium were analyzed. PLIN2 function in leiomyoma was assessed using small interfering RNA. RNA-sequencing was performed to identify genome-wide effects of PLIN2 depletion. Metabolic activity was measured using the Seahorse XF96 analyzer. Real-time quantitative PCR and immunoblotting were also performed.

Setting: Laboratory.

Patients or other participants: Forty-one premenopausal women undergoing surgery for fibroids.

Main outcome measures: Gene expression, oxygen consumption rate (OCR), extracellular acidification rate (ECAR), and cell proliferation.

Results: PLIN2 gene expression was 2.4-fold lower in leiomyoma compared with adjacent myometrium, suggesting a link between PLIN2 deficiency and fibroids. A total of 3877 genes were differentially expressed after PLIN2 knockdown. Gene ontology analysis identified metabolism as the second-highest biological process affected by PLIN2 depletion. OCR (mitochondrial respiration) and ECAR (glycolysis) were significantly upregulated after PLIN2 knockdown; PLIN2-depleted cells had a greater basal metabolic activity and higher metabolic stress response. Cell proliferation was also significantly increased after PLIN2 knockdown.

Conclusions: PLIN2 depletion increases mitochondrial respiration and glycolysis, suggesting that PLIN2 is a critical regulator of metabolic function in leiomyoma cells. PLIN2 deficiency also reprograms leiomyoma cells to a proproliferative phenotype. These findings introduce metabolomics as an area to explore to better understand leiomyoma tumorigenesis.

Publication types

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

MeSH terms

  • Adult
  • Biomarkers, Tumor / genetics
  • Biomarkers, Tumor / metabolism*
  • Case-Control Studies
  • Cell Proliferation
  • Female
  • Follow-Up Studies
  • Gene Expression Profiling
  • Gene Expression Regulation, Neoplastic
  • Glycolysis
  • Humans
  • Leiomyoma / genetics
  • Leiomyoma / metabolism
  • Leiomyoma / pathology*
  • Metabolome
  • Myometrium / metabolism
  • Myometrium / pathology*
  • Perilipin-2 / antagonists & inhibitors
  • Perilipin-2 / genetics
  • Perilipin-2 / metabolism*
  • Progesterone / metabolism*
  • Prognosis
  • RNA, Small Interfering
  • Receptors, Progesterone / genetics
  • Receptors, Progesterone / metabolism*
  • Signal Transduction
  • Uterine Neoplasms / genetics
  • Uterine Neoplasms / metabolism
  • Uterine Neoplasms / pathology*

Substances

  • Biomarkers, Tumor
  • PLIN2 protein, human
  • Perilipin-2
  • RNA, Small Interfering
  • Receptors, Progesterone
  • Progesterone