O-GlcNAcylation Mediates Glucose-Induced Alterations in Endothelial Cell Phenotype in Human Diabetes Mellitus

J Am Heart Assoc. 2020 Jun 16;9(12):e014046. doi: 10.1161/JAHA.119.014046. Epub 2020 Jun 6.

Abstract

Background Posttranslational protein modification with O-linked N-acetylglucosamine (O-GlcNAc) is linked to high glucose levels in type 2 diabetes mellitus (T2DM) and may alter cellular function. We sought to elucidate the involvement of O-GlcNAc modification in endothelial dysfunction in patients with T2DM. Methods and Results Freshly isolated endothelial cells obtained by J-wire biopsy from a forearm vein of patients with T2DM (n=18) was compared with controls (n=10). Endothelial O-GlcNAc levels were 1.8-ford higher in T2DM patients than in nondiabetic controls (P=0.003). Higher endothelial O-GlcNAc levels correlated with serum fasting blood glucose level (r=0.433, P=0.024) and hemoglobin A1c (r=0.418, P=0.042). In endothelial cells from patients with T2DM, normal glucose conditions (24 hours at 5 mmol/L) lowered O-GlcNAc levels and restored insulin-mediated activation of endothelial nitric oxide synthase, whereas high glucose conditions (30 mmol/L) maintained both O-GlcNAc levels and impaired insulin action. Treatment of endothelial cells with Thiamet G, an O-GlcNAcase inhibitor, increased O-GlcNAc levels and blunted the improvement of insulin-mediated endothelial nitric oxide synthase phosphorylation by glucose normalization. Conclusions Taken together, our findings indicate a role for O-GlcNAc modification in the dynamic, glucose-induced impairment of endothelial nitric oxide synthase activation in endothelial cells from patients with T2DM. O-GlcNAc protein modification may be a treatment target for vascular dysfunction in T2DM.

Keywords: O‐GlcNAc; diabetes mellitus; endothelial nitric oxide synthase; insulin resistance.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Case-Control Studies
  • Cells, Cultured
  • Diabetes Mellitus, Type 2 / diagnosis
  • Diabetes Mellitus, Type 2 / metabolism*
  • Endothelial Cells / drug effects*
  • Endothelial Cells / metabolism
  • Female
  • Forearm / blood supply*
  • Glucose / pharmacology*
  • Glucose / toxicity*
  • Glycosylation
  • Humans
  • Insulin / pharmacology
  • Male
  • Middle Aged
  • Nitric Oxide Synthase Type III / metabolism
  • Phenotype
  • Phosphorylation
  • Protein Processing, Post-Translational / drug effects*
  • beta-N-Acetylhexosaminidases / metabolism

Substances

  • Insulin
  • NOS3 protein, human
  • Nitric Oxide Synthase Type III
  • hexosaminidase C
  • beta-N-Acetylhexosaminidases
  • Glucose