Endothelin-1 induces endoplasmic reticulum stress by activating the PLC-IP(3) pathway: implications for placental pathophysiology in preeclampsia

Am J Pathol. 2012 Jun;180(6):2309-20. doi: 10.1016/j.ajpath.2012.03.005. Epub 2012 Apr 12.

Abstract

Recent evidence implicates placental endoplasmic reticulum (ER) stress in the pathophysiological characteristics of preeclampsia. Herein, we investigate whether endothelin (ET)-1, which induces Ca(2+) release from the ER, can induce placental ER stress. Loss of ER Ca(2+) homeostasis impairs post-translational modification of proteins, triggering ER stress-response pathways. IHC confirmed the presence of both ET-1 and its receptors in the syncytiotrophoblast. Protein levels and immunoreactivity of ET-1 and the endothelin B receptor (ETBR) were increased in preeclamptic samples compared with normotensive controls. JEG-3 and BeWo choriocarcinoma cells treated with ET-1 displayed an increase in ER stress markers. ET-1 induced phospho-activation of the ETBR. Treating cells with BQ788, an ETBR antagonist, or small-interfering RNA knockdown of the receptor inhibited induction of ER stress. ET-1 also stimulated p-phospholipase C (PLC)γ1 levels. By using inhibitors of PLC activation, U73122, and the inositol 1,4,5-triphosphate (IP(3)) receptor, xestospongin-C, we demonstrated that ET-1 induces ER stress via the PLC-IP(3) pathway. Furthermore, ET-1 levels increased in the syncytiotrophoblast of explants from normal placentas after hypoxia-reoxygenation in vitro. Conditioned medium from hypoxia-reoxygenation explants also contained higher ET-1 levels, which induced ER stress in JEG-3 cells that was abolished by an ET-1-neutralizing antibody. Collectively, the data show that ET-1 induced ER stress in trophoblasts via the ETBR and initiation of signaling through the PLC-IP(3) pathway, with the potential for autocrine stimulation.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Dose-Response Relationship, Drug
  • Endoplasmic Reticulum Stress / drug effects
  • Endoplasmic Reticulum Stress / physiology*
  • Endothelin-1 / metabolism
  • Endothelin-1 / pharmacology
  • Endothelin-1 / physiology*
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Inositol 1,4,5-Trisphosphate Receptors / physiology
  • Phosphorylation / drug effects
  • Placenta / metabolism
  • Placenta / physiopathology*
  • Pre-Eclampsia / metabolism
  • Pre-Eclampsia / physiopathology*
  • Pregnancy
  • RNA, Small Interfering / genetics
  • Receptor, Endothelin A / metabolism
  • Receptor, Endothelin B / metabolism
  • Signal Transduction / physiology
  • Tissue Culture Techniques
  • Trophoblasts / drug effects
  • Trophoblasts / metabolism
  • Tumor Cells, Cultured
  • Type C Phospholipases / physiology

Substances

  • Endothelin-1
  • Inositol 1,4,5-Trisphosphate Receptors
  • RNA, Small Interfering
  • Receptor, Endothelin A
  • Receptor, Endothelin B
  • Type C Phospholipases