Interleukin-1β inhibits insulin signaling and prevents insulin-stimulated system A amino acid transport in primary human trophoblasts

Mol Cell Endocrinol. 2013 Dec 5;381(1-2):46-55. doi: 10.1016/j.mce.2013.07.013. Epub 2013 Jul 25.

Abstract

Interleukin-1β (IL-1β) promotes insulin resistance in tissues such as liver and skeletal muscle; however the influence of IL-1β on placental insulin signaling is unknown. We recently reported increased IL-1β protein expression in placentas of obese mothers, which could contribute to insulin resistance. In this study, we tested the hypothesis that IL-1β inhibits insulin signaling and prevents insulin-stimulated amino acid transport in cultured primary human trophoblast (PHT) cells. Cultured trophoblasts isolated from term placentas were treated with physiological concentrations of IL-1β (10pg/ml) for 24h. IL-1β increased the phosphorylation of insulin receptor substrate-1 (IRS-1) at Ser307 (inhibitory) and decreased total IRS-1 protein abundance but did not affect insulin receptor β expression. Furthermore, IL-1β inhibited insulin-stimulated phosphorylation of IRS-1 (Tyr612, activation site) and Akt (Thr308) and prevented insulin-stimulated increase in PI3K/p85 and Grb2 protein expression. IL-1β alone stimulated cRaf (Ser338), MEK (Ser221) and Erk1/2 (Thr202/Tyr204) phosphorylation. The inflammatory pathways nuclear factor kappa B and c-Jun N-terminal kinase, which are involved in insulin resistance, were also activated by IL-1β treatment. Moreover, IL-1β inhibited insulin-stimulated System A, but not System L amino acid uptake, indicating functional impairment of insulin signaling. In conclusion, IL-1β inhibited the insulin signaling pathway by inhibiting IRS-1 signaling and prevented insulin-stimulated System A transport, thereby promoting insulin resistance in cultured PHT cells. These findings indicate that conditions which lead to increased systemic maternal or placental IL-1β levels may attenuate the effects of maternal insulin on placental function and consequently fetal growth.

Keywords: Inflammation; Insulin-resistance; Maternal–fetal exchange; Placenta.

Publication types

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

MeSH terms

  • Amino Acid Transport System A / metabolism*
  • Amino Acid Transport System L / metabolism
  • Amino Acids / metabolism
  • Biological Transport
  • Cells, Cultured
  • Enzyme Activation
  • Female
  • GRB2 Adaptor Protein / metabolism
  • Humans
  • Insulin / physiology*
  • Insulin Receptor Substrate Proteins / metabolism
  • Interleukin-1beta / physiology*
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • MAP Kinase Signaling System
  • Metabolic Networks and Pathways
  • NF-kappa B / metabolism
  • Phosphorylation
  • Primary Cell Culture
  • Protein Processing, Post-Translational
  • Trophoblasts / metabolism*

Substances

  • Amino Acid Transport System A
  • Amino Acid Transport System L
  • Amino Acids
  • GRB2 Adaptor Protein
  • GRB2 protein, human
  • IRS1 protein, human
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Interleukin-1beta
  • NF-kappa B
  • JNK Mitogen-Activated Protein Kinases