Cholinergic drugs ameliorate endothelial dysfunction by decreasing O-GlcNAcylation via M3 AChR-AMPK-ER stress signaling

Life Sci. 2019 Apr 1:222:1-12. doi: 10.1016/j.lfs.2019.02.036. Epub 2019 Feb 17.

Abstract

Aims: Obesity is associated with increased cardiovascular morbidity and mortality. It is accompanied by augmented O-linked β-N-acetylglucosamine (O-GlcNAc) modification of proteins via increasing hexosamine biosynthetic pathway (HBP) flux. However, the changes and regulation of the O-GlcNAc levels induced by obesity are unclear.

Main methods: High fat diet (HFD) model was induced obesity in mice with or without the cholinergic drug pyridostigmine (PYR, 3 mg/kg/d) for 22 weeks and in vitro human umbilical vein endothelial cells (HUVECs) was treated with high glucose (HG, 30 mM) with or without acetylcholine (ACh).

Key findings: PYR significantly reduced body weight, blood glucose, and O-GlcNAcylation levels and attenuated vascular endothelial cells detachment in HFD-fed mice. HG addition induced endoplasmic reticulum (ER) stress and increased O-GlcNAcylation levels and apoptosis in HUVECs in a time-dependent manner. Additionally, HG decreased levels of phosphorylated AMP-activated protein kinase (AMPK). Interestingly, ACh significantly blocked damage to HUVECs induced by HG. Furthermore, the effects of ACh on HG-induced ER stress, O-GlcNAcylation, and apoptosis were prevented by treating HUVECs with 4-diphenylacetoxy-N-methylpiperidine methiodide (4-DAMP, a selective M3 AChR antagonist) or compound C (Comp C, an AMPK inhibitor). Treatment with 5-aminoimidazole-4-carboxamide ribose (AICAR, an AMPK activator), 4-phenyl butyric acid (4-PBA, an ER stress inhibitor), and 6-diazo-5-oxonorleucine (DON, a GFAT antagonist) reproduced a similar effect with ACh.

Significance: Activation of cholinergic signaling ameliorated endothelium damage, reduced levels of ER stress, O-GlcNAcylation, and apoptosis in mice and HUVECs under obese conditions, which may function through M3 AChR-AMPK signaling.

Keywords: Cholinergic drugs; ER stress; Endothelial cell apoptosis; M3 AChR-AMPK; O-GlcNAc; Obesity.

MeSH terms

  • AMP-Activated Protein Kinase Kinases
  • Acetylcholine / pharmacology
  • Acetylglucosamine / antagonists & inhibitors
  • Acetylglucosamine / metabolism*
  • Animals
  • Cholinergic Agents / pharmacology*
  • Cholinesterase Inhibitors / pharmacology
  • Diet, High-Fat / adverse effects
  • Dose-Response Relationship, Drug
  • Endoplasmic Reticulum Stress / drug effects
  • Endoplasmic Reticulum Stress / physiology*
  • Endothelium, Vascular / drug effects
  • Endothelium, Vascular / metabolism*
  • Human Umbilical Vein Endothelial Cells / drug effects
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Humans
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Protein Kinases / metabolism*
  • Pyridostigmine Bromide / pharmacology
  • Receptor, Muscarinic M3 / antagonists & inhibitors
  • Receptor, Muscarinic M3 / metabolism*

Substances

  • Cholinergic Agents
  • Cholinesterase Inhibitors
  • Receptor, Muscarinic M3
  • Protein Kinases
  • AMP-Activated Protein Kinase Kinases
  • Pyridostigmine Bromide
  • Acetylcholine
  • Acetylglucosamine