Role of O-linked N-acetylglucosamine modification in diabetic nephropathy

Am J Physiol Renal Physiol. 2016 Dec 1;311(6):F1172-F1181. doi: 10.1152/ajprenal.00545.2015. Epub 2016 Mar 30.

Abstract

Increased O-linked β-N-acetylglucosamine glycosylation (O-GlcNAcylation) is a known contributor to diabetes; however, its relevance in diabetic nephropathy (DN) is poorly elucidated. Here, we studied the process and enzymes of O-GlcNAcylation with a special emphasis on Akt-endothelial nitric oxide synthase (eNOS) and heat shock protein (HSP)72 signaling. Since tubular injury is the prominent site of DN, the effect of hyperglycemia was first measured in proximal tubular (HK2) cells cultured in high glucose. In vivo O-GlcNAcylation and protein levels of O-GlcNAc transferase (OGT), O-GlcNAcase (OGA), phosphorylated (p)Akt/Akt, peNOS/eNOS, and HSP72 were assessed in the kidney cortex of streptozotocin-induced diabetic rats. The effects of various renin-angiotensin-aldosterone system (RAAS) inhibitors were also evaluated. In proximal tubular cells, hyperglycemia-induced OGT expression led to increased O-GlcNAcylation, which was followed by a compensatory increase of OGA. In parallel, peNOS and pAkt levels decreased, whereas HSP72 increased. In diabetic rats, elevated O-GlcNAcylation was accompanied by decreased OGT and OGA. RAAS inhibitors ameliorated diabetes-induced kidney damage and prevented the elevation of O-GlcNAcylation and the decrement of pAkt, peNOS, and HSP72. In conclusion, hyperglycemia-induced elevation of O-GlcNAcylation contributes to the progression of DN via inhibition of Akt/eNOS phosphorylation and HSP72 induction. RAAS blockers successfully inhibit this process, suggesting a novel pathomechanism of their renoprotective action in the treatment of DN.

Keywords: O-linked β-N-acetylglucosamine glycosylation; diabetic nephropathy; endothelial nitric oxide synthase; heat shock protein 72; renin-angiotensin-aldosterone system.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylglucosamine / metabolism*
  • Angiotensin II Type 1 Receptor Blockers / pharmacology
  • Angiotensin-Converting Enzyme Inhibitors / pharmacology
  • Animals
  • Blood Pressure / drug effects
  • Blood Pressure / physiology
  • Cell Line
  • Cell Survival / drug effects
  • Diabetes Mellitus, Experimental / metabolism*
  • Diabetic Nephropathies / metabolism*
  • Enalapril / pharmacology
  • Glycosylation
  • HSP72 Heat-Shock Proteins / metabolism
  • Humans
  • Kidney / drug effects
  • Kidney / metabolism*
  • Kidney Tubules, Proximal / cytology
  • Kidney Tubules, Proximal / drug effects
  • Kidney Tubules, Proximal / metabolism
  • Losartan / pharmacology
  • Male
  • Nitric Oxide Synthase Type III / metabolism
  • Phosphorylation / drug effects
  • Protein Processing, Post-Translational / drug effects
  • Protein Processing, Post-Translational / physiology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Rats
  • Rats, Wistar
  • Renin-Angiotensin System / drug effects
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*

Substances

  • Angiotensin II Type 1 Receptor Blockers
  • Angiotensin-Converting Enzyme Inhibitors
  • HSP72 Heat-Shock Proteins
  • Enalapril
  • Nitric Oxide Synthase Type III
  • Proto-Oncogene Proteins c-akt
  • Losartan
  • Acetylglucosamine