Pre-pregnancy maternal obesity associates with endoplasmic reticulum stress in human umbilical vein endothelium

Biochim Biophys Acta Mol Basis Dis. 2018 Oct;1864(10):3195-3210. doi: 10.1016/j.bbadis.2018.07.007. Epub 2018 Jul 11.

Abstract

Obesity associates with the endoplasmic reticulum (ER) stress-induced endothelial dysfunction. Pregnant women with pre-pregnancy maternal obesity (PGMO) may transfer this potential risk to their offspring; however, whether ER stress occurs and associates with foetoplacental endothelial dysfunction in PGMO is unknown. We studied the l-arginine transport and nitric oxide (NO) synthesis in human umbilical vein endothelial cells (HUVECs) from women with PGMO or with a normal pre-pregnancy weight. We analysed the expression and activation of the ER stress sensors protein kinase RNA-like endoplasmic reticulum kinase (PERK), inositol-requiring enzyme 1α (IRE1α), and activating transcription factor 6 (ATF6). PGMO associated with lower endothelial NO synthase activity due to increased Thr495-inhibitor and decreased Ser1177-stimulator phosphorylation. However, higher expression and activity of the human cationic amino acid transporter 1 was found. PGMO caused activation of PERK and its downstream targets eukaryotic initiation factor 2 (eIF2α), C/EBP homologous protein 10 (CHOP), and tribbles-like protein 3 (TRB3). Increased IRE1α protein abundance (but not its phosphorylation or X-box binding protein 1-mRNA splicing) and increased c-Jun N-terminal kinase 1 phosphorylation was seen in PGMO. A preferential nuclear location of the activating transcription factor 6 (ATF6) was found in HUVECs from PGMO. All the changes seen in PGMO were blocked by TUDCA but unaltered by tunicamycin. Thus, PGMO may determine a state of ER stress via upregulation of the PERK-eIF2α-CHOP-TRB3 axis signalling in HUVECs. This phenomenon results in foetoplacental vascular endothelial dysfunction at birth.

Keywords: Arginine; Endoplasmic reticulum stress; Endothelium; Nitric oxide; Obesity; Pre-pregnancy.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Activating Transcription Factor 6 / metabolism
  • Adult
  • Arginine / metabolism
  • Cell Cycle Proteins / metabolism
  • Endoplasmic Reticulum / metabolism*
  • Endoplasmic Reticulum Stress*
  • Endoribonucleases / metabolism
  • Female
  • Human Umbilical Vein Endothelial Cells / metabolism*
  • Humans
  • Nitric Oxide / metabolism
  • Obesity / metabolism*
  • Pregnancy
  • Protein Serine-Threonine Kinases / antagonists & inhibitors
  • Protein Serine-Threonine Kinases / metabolism
  • Repressor Proteins / metabolism
  • Signal Transduction*
  • Transcription Factor CHOP / metabolism
  • Young Adult
  • eIF-2 Kinase / metabolism

Substances

  • ATF6 protein, human
  • Activating Transcription Factor 6
  • Cell Cycle Proteins
  • DDIT3 protein, human
  • Repressor Proteins
  • TRIB3 protein, human
  • Transcription Factor CHOP
  • Nitric Oxide
  • Arginine
  • EIF2AK3 protein, human
  • ERN1 protein, human
  • Protein Serine-Threonine Kinases
  • eIF-2 Kinase
  • Endoribonucleases