Dioxin-Induced PAI-1 Expression: A Novel Pathway to Pancreatic β-Cell Failure in Type 2 Diabetes

Int J Mol Sci. 2024 Nov 7;25(22):11974. doi: 10.3390/ijms252211974.

Abstract

Exposure to environment-polluting chemicals (EPCs), which are ligands of the aryl hydrocarbon receptor (AhR), is associated with the development of type 2 diabetes (T2D). This study explores the mechanisms by which AhR ligands contribute to β-cell failure in T2D. Incubation of RINm5F rat pancreatic β-cells with low-dose 2,3,7,8-tetrachlorodibenzodioxin (TCDD), the most potent AhR ligand, inhibited glucose-stimulated insulin secretion (GSIS). A single injection of TCDD in wild type mice reduced the size of Langerhans islets, but not in AhR liver knock-out mice (AhR-LKO). RNA-seq database analysis identified Serpine1, encoding for plasminogen activator inhibitor type-1 (PAI-1) as a TCDD-mediated secretory protein that is synthesized in an AhR-dependent manner in the liver. Elevated PAI-1 levels were shown to induce Caspase-3/7-dependent apoptosis in RINm5F cells, suggesting a novel pathway through which EPCs exacerbate T2D. These findings support the hypothesis that chronic exposure to AhR ligands may directly inhibit GSIS in pancreatic β-cells and indirectly induce β-cell apoptosis through increased PAI-1. This study provides new insights into the EPC-PAI-1 axis as a missing link between pancreatic β-cell failure and the progression of T2D and offers a potential target for therapeutic intervention.

Keywords: AhR; PAI-1; TCDD; diabetes; β-cell failure.

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Caspase 3 / metabolism
  • Cell Line
  • Diabetes Mellitus, Type 2* / genetics
  • Diabetes Mellitus, Type 2* / metabolism
  • Diabetes Mellitus, Type 2* / pathology
  • Glucose / metabolism
  • Insulin / metabolism
  • Insulin Secretion / drug effects
  • Insulin-Secreting Cells* / drug effects
  • Insulin-Secreting Cells* / metabolism
  • Insulin-Secreting Cells* / pathology
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Plasminogen Activator Inhibitor 1* / genetics
  • Plasminogen Activator Inhibitor 1* / metabolism
  • Polychlorinated Dibenzodioxins / toxicity
  • Rats
  • Receptors, Aryl Hydrocarbon* / genetics
  • Receptors, Aryl Hydrocarbon* / metabolism

Substances

  • Plasminogen Activator Inhibitor 1
  • Receptors, Aryl Hydrocarbon
  • Polychlorinated Dibenzodioxins
  • Insulin
  • Serpine1 protein, rat
  • Glucose
  • Caspase 3