High glucose levels induce inhibition of Na,K-ATPase via stimulation of aldose reductase, formation of microtubules and formation of an acetylated tubulin/Na,K-ATPase complex

Int J Biochem Cell Biol. 2012 Aug;44(8):1203-13. doi: 10.1016/j.biocel.2012.04.011. Epub 2012 Apr 27.

Abstract

Our previous studies demonstrated that acetylated tubulin forms a complex with Na(+),K(+)-ATPase and thereby inhibits its enzyme activity in cultured COS and CAD cells. The enzyme activity was restored by treatment of cells with l-glutamate, which caused dissociation of the acetylated tubulin/Na(+),K(+)-ATPase complex. Addition of glucose, but not elimination of glutamate, led to re-formation of the complex and inhibition of the Na(+),K(+)-ATPase activity. The purpose of the present study was to elucidate the mechanism underlying this effect of glucose. We found that exposure of cells to high glucose concentrations induced: (a) microtubule formation; (b) activation of aldose reductase by the microtubules; (c) association of tubulin with membrane; (d) formation of the acetylated tubulin/Na(+),K(+)-ATPase complex and consequent inhibition of enzyme activity. Exposure of cells to sorbitol caused similar effects. Studies on erythrocytes from diabetic patients and on tissues containing insulin-insensitive glucose transporters gave similar results. Na(+),K(+)-ATPase activity was >50% lower and membrane-associated tubulin content was >200% higher in erythrocyte membranes from diabetic patients as compared with normal subjects. Immunoprecipitation analysis showed that acetylated tubulin was a constituent of a complex with Na(+),K(+)-ATPase in erythrocyte membranes from diabetic patients. Based on these findings, we propose a mechanism whereby glucose triggers a synergistic effect of tubulin and sorbitol, leading to activation of aldose reductase, microtubule formation, and consequent Na(+),K(+)-ATPase inhibition.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetylation
  • Adult
  • Aldehyde Reductase / metabolism*
  • Animals
  • Brain / drug effects
  • Brain / enzymology
  • Brain / metabolism
  • COS Cells
  • Cell Line, Tumor
  • Chlorocebus aethiops
  • Diabetes Mellitus / enzymology
  • Diabetes Mellitus / metabolism
  • Dose-Response Relationship, Drug
  • Erythrocyte Membrane / drug effects
  • Erythrocyte Membrane / metabolism
  • Female
  • Glucose / pharmacology*
  • Humans
  • Immunoblotting
  • Male
  • Microscopy, Confocal
  • Microtubules / metabolism*
  • Middle Aged
  • Protein Binding / drug effects
  • Rats
  • Rats, Wistar
  • Sodium-Potassium-Exchanging ATPase / antagonists & inhibitors
  • Sodium-Potassium-Exchanging ATPase / metabolism*
  • Sorbitol / pharmacology
  • Tubulin / metabolism*
  • Tubulin / pharmacology

Substances

  • Tubulin
  • Sorbitol
  • Aldehyde Reductase
  • Sodium-Potassium-Exchanging ATPase
  • Glucose