Peroxisome Proliferator-activated Receptor-γ Activation Augments the β-Cell Unfolded Protein Response and Rescues Early Glycemic Deterioration and β Cell Death in Non-obese Diabetic Mice

J Biol Chem. 2016 Oct 21;291(43):22524-22533. doi: 10.1074/jbc.M116.741694. Epub 2016 Sep 9.

Abstract

Type 1 diabetes is an autoimmune disorder that is characterized by a failure of the unfolded protein response in islet β cells with subsequent endoplasmic reticulum stress and cellular death. Thiazolidinediones are insulin sensitizers that activate the nuclear receptor PPAR-γ and have been shown to partially ameliorate autoimmune type 1 diabetes in humans and non-obese diabetic (NOD) mice. We hypothesized that thiazolidinediones reduce β cell stress and death independently of insulin sensitivity. To test this hypothesis, female NOD mice were administered pioglitazone during the pre-diabetic phase and assessed for insulin sensitivity and β cell function relative to controls. Pioglitazone-treated mice showed identical weight gain, body fat distribution, and insulin sensitivity compared with controls. However, treated mice showed significantly improved glucose tolerance with enhanced serum insulin levels, reduced β cell death, and increased β cell mass. The effect of pioglitazone was independent of actions on T cells, as pancreatic lymph node T cell populations were unaltered and T cell proliferation was unaffected by pioglitazone. Isolated islets of treated mice showed a more robust unfolded protein response, with increases in Bip and ATF4 and reductions in spliced Xbp1 mRNA. The effect of pioglitazone appears to be a direct action on β cells, as islets from mice treated with pioglitazone showed reductions in PPAR-γ (Ser-273) phosphorylation. Our results demonstrate that PPAR-γ activation directly improves β cell function and survival in NOD mice by enhancing the unfolded protein response and suggest that blockade of PPAR-γ (Ser-273) phosphorylation may prevent type 1 diabetes.

Keywords: autoimmunity; beta cell (B-cell); diabetes; endoplasmic reticulum stress (ER stress); insulin; peroxisome proliferator-activated receptor (PPAR); unfolded protein response (UPR).

MeSH terms

  • Activating Transcription Factor 4 / genetics
  • Activating Transcription Factor 4 / metabolism
  • Animals
  • Cell Line
  • Endoplasmic Reticulum Chaperone BiP
  • Female
  • Heat-Shock Proteins / genetics
  • Heat-Shock Proteins / metabolism
  • Insulin / genetics
  • Insulin / metabolism
  • Insulin-Secreting Cells / metabolism*
  • Mice
  • Mice, Inbred NOD
  • PPAR gamma / genetics
  • PPAR gamma / metabolism*
  • Pioglitazone
  • Thiazolidinediones / pharmacology*
  • Unfolded Protein Response / drug effects*
  • X-Box Binding Protein 1 / genetics
  • X-Box Binding Protein 1 / metabolism

Substances

  • Atf4 protein, mouse
  • Endoplasmic Reticulum Chaperone BiP
  • Heat-Shock Proteins
  • Insulin
  • PPAR gamma
  • Thiazolidinediones
  • X-Box Binding Protein 1
  • Xbp1 protein, mouse
  • Activating Transcription Factor 4
  • Pioglitazone