Na+/H+-exchanger-1 inhibition counteracts diabetic cataract formation and retinal oxidative-nitrative stress and apoptosis

Int J Mol Med. 2012 Jun;29(6):989-98. doi: 10.3892/ijmm.2012.933. Epub 2012 Mar 7.

Abstract

The Na⁺-H⁺-exchanger-1 (NHE-1) controls intracellular pH and glycolytic enzyme activities, and its expression and activity are increased by diabetes and high glucose. NHE-1-dependent upregulation of the upper part of glycolysis, under conditions of inhibition (lens) or insufficient activation (retina) of glyceraldehyde 3-phosphate dehydrogenase, underlies diversion of the excessive glycolytic flux towards several pathways contributing to oxidative stress, a causative factor in diabetic cataractogenesis and retinopathy. This study evaluated the role for NHE-1 in diabetic cataract formation and retinal oxidative stress and apoptosis. Control and streptozotocin-diabetic rats were maintained with or without treatment with the NHE-1 inhibitor cariporide (Sanofi-Aventis, 10 mgkg-1d-1) for 3.5 months. In in vitro studies, bovine retinal pericytes and endothelial cells were cultured in 5 or 30 mM glucose, with or without 10 µM cariporide, for 7 days. A several-fold increase of the by-product of glycolysis, α-glycerophosphate, indicative of activation of the upper part of glycolysis, was present in both rat lens and retina at an early (1-month) stage of streptozotocin-diabetes. Cariporide did not affect diabetic hyperglycemia and counteracted lens oxidative-nitrative stress and p38 MAPK activation, without affecting glucose or sorbitol pathway intermediate accumulation. Cataract formation (indirect ophthalmoscopy and slit-lamp examination) was delayed, but not prevented. The number of TUNEL-positive cells per flat-mounted retina was increased 4.4-fold in diabetic rats (101 ± 17 vs. 23 ± 8 in controls , P<0.01), and this increase was attenuated by cariporide (45 ± 12, P<0.01). Nitrotyrosine and poly(ADP-ribose) fluorescence and percentage of TUNEL-positive cells were increased in pericytes and endothelial cells cultured in 30 mM glucose, and these changes were at least partially prevented by cariporide. In conclusion, NHE-1 contributes to diabetic cataract formation, and retinal oxidative-nitrative stress and apoptosis. The findings identify a new therapeutic target for diabetic ocular complications.

Publication types

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

MeSH terms

  • Aldehydes / metabolism
  • Animals
  • Apoptosis* / drug effects
  • Blood Glucose / metabolism
  • Blotting, Western
  • Cataract / blood
  • Cataract / drug therapy
  • Cataract / pathology*
  • Cattle
  • Diabetes Complications / blood
  • Diabetes Complications / drug therapy
  • Diabetes Complications / pathology*
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Fasting / blood
  • Guanidines / pharmacology
  • Guanidines / therapeutic use
  • In Situ Nick-End Labeling
  • Lens, Crystalline / drug effects
  • Lens, Crystalline / enzymology
  • Lens, Crystalline / pathology
  • Male
  • Nitrosation / drug effects
  • Oxidative Stress* / drug effects
  • Phosphorylation / drug effects
  • Poly(ADP-ribose) Polymerases / metabolism
  • Rats
  • Rats, Wistar
  • Retina / pathology*
  • Sodium-Hydrogen Exchangers / antagonists & inhibitors*
  • Sodium-Hydrogen Exchangers / metabolism
  • Sulfones / pharmacology
  • Sulfones / therapeutic use
  • Tyrosine / analogs & derivatives
  • Tyrosine / metabolism
  • p38 Mitogen-Activated Protein Kinases / metabolism

Substances

  • Aldehydes
  • Blood Glucose
  • Guanidines
  • Sodium-Hydrogen Exchangers
  • Sulfones
  • 3-nitrotyrosine
  • Tyrosine
  • cariporide
  • Poly(ADP-ribose) Polymerases
  • Extracellular Signal-Regulated MAP Kinases
  • p38 Mitogen-Activated Protein Kinases
  • 4-hydroxy-2-nonenal