Involvement of NDPK-B in Glucose Metabolism-Mediated Endothelial Damage via Activation of the Hexosamine Biosynthesis Pathway and Suppression of O-GlcNAcase Activity

Cells. 2020 Oct 19;9(10):2324. doi: 10.3390/cells9102324.

Abstract

Our previous studies identified that retinal endothelial damage caused by hyperglycemia or nucleoside diphosphate kinase-B (NDPK-B) deficiency is linked to elevation of angiopoietin-2 (Ang-2) and the activation of the hexosamine biosynthesis pathway (HBP). Herein, we investigated how NDPK-B is involved in the HBP in endothelial cells (ECs). The activities of NDPK-B and O-GlcNAcase (OGA) were measured by in vitro assays. Nucleotide metabolism and O-GlcNAcylated proteins were assessed by UPLC-PDA (Ultra-performance liquid chromatography with Photodiode array detection) and immunoblot, respectively. Re-expression of NDPK-B was achieved with recombinant adenoviruses. Our results show that NDPK-B depletion in ECs elevated UDP-GlcNAc levels and reduced NDPK activity, similar to high glucose (HG) treatment. Moreover, the expression and phosphorylation of glutamine:fructose-6-phosphate amidotransferase (GFAT) were induced, whereas OGA activity was suppressed. Furthermore, overall protein O-GlcNAcylation, along with O-GlcNAcylated Ang-2, was increased in NDPK-B depleted ECs. Pharmacological elevation of protein O-GlcNAcylation using Thiamet G (TMG) or OGA siRNA increased Ang-2 levels. However, the nucleoside triphosphate to diphosphate (NTP/NDP) transphosphorylase and histidine kinase activity of NDPK-B were dispensable for protein O-GlcNAcylation. NDPK-B deficiency hence results in the activation of HBP and the suppression of OGA activity, leading to increased protein O-GlcNAcylation and further upregulation of Ang-2. The data indicate a critical role of NDPK-B in endothelial damage via the modulation of the HBP.

Keywords: Ang-2; O-GlcNAcylation; OGA; UDP-GlcNAc; nucleoside diphosphate kinase B.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Angiopoietin-2 / metabolism
  • Animals
  • Biosynthetic Pathways*
  • Endothelial Cells / metabolism*
  • Endothelial Cells / pathology*
  • Glucose / metabolism*
  • Glycosylation
  • HEK293 Cells
  • Hexosamines / biosynthesis*
  • Histidine / metabolism
  • Human Umbilical Vein Endothelial Cells / metabolism
  • Human Umbilical Vein Endothelial Cells / pathology
  • Humans
  • Infant, Newborn
  • Mice
  • Models, Biological
  • NM23 Nucleoside Diphosphate Kinases / metabolism*
  • Nucleotides / metabolism
  • beta-N-Acetylhexosaminidases / metabolism*

Substances

  • Angiopoietin-2
  • Hexosamines
  • NM23 Nucleoside Diphosphate Kinases
  • Nucleotides
  • Histidine
  • hexosaminidase C
  • beta-N-Acetylhexosaminidases
  • Glucose