Cyclosporin A disrupts bradykinin signaling through superoxide

Hypertension. 2003 May;41(5):1136-42. doi: 10.1161/01.HYP.0000068201.48340.3B. Epub 2003 Apr 14.

Abstract

Cyclosporin A (CsA) is used to reduce transplant rejection rates. Chronic use, however, has a destructive toxic effect on the kidney, resulting in hypertension. In this study, we investigated the effects of CsA treatment on the bradykinin/soluble guanylate cyclase signaling cascade and the involvement of superoxide in LLC-PK1 porcine kidney proximal tubule cells. Treatment with 1 micromol/L CsA for 24 hours increased basal cGMP levels by 41%, whereas CsA inhibited bradykinin-stimulated cGMP production by 26%. Western blotting showed increased expression of eNOS, but no other protein in the bradykinin/soluble guanylate cyclase (sGC) pathway was affected. Using lucigenin-dependent chemiluminescence, we found that CsA treatment significantly increased superoxide production. Production of O2- was not significantly reduced by 10 micromol/L oxypurinol or 30 micromol/L ketoconazole. However, it was inhibited by the NADPH oxidase inhibitor diphenyleneiodonium chloride (10 micromol/L) as well as the O2- scavenger superoxide dismutase (SOD) (100 U). On treatment with 50 micromol/L quercetin, 10 mmol/L N-acetyl-cysteine, both antioxidants, as well as the O2- scavenger Tiron (10 mmol/L), concomitant with 1 micromol/L CsA for 24 hours the activation of cGMP production, was restored in combination with a reduction in O2-. Incubation with 100 micromol/L menadione, a reactive oxygen generator, and 10 nmol/L bradykinin showed similar effects on the level of cGMP as with CsA. CsA treatment was found to increase nitrotyrosine levels. These findings suggest that CsA activates a NADPH oxidase that releases O2- and disrupts the bradykinin/soluble guanylate cyclase pathway, probably by binding with NO to form peroxynitrite (ONOO-).

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 1,2-Dihydroxybenzene-3,5-Disulfonic Acid Disodium Salt / pharmacology
  • Acetylcysteine / pharmacology
  • Animals
  • Antioxidants / pharmacology
  • Blotting, Western
  • Bradykinin / pharmacology*
  • Cyclic GMP / metabolism
  • Cyclosporine / pharmacology*
  • Enzyme Activation / drug effects
  • Free Radical Scavengers / pharmacology
  • GTP-Binding Proteins / metabolism
  • Guanylate Cyclase / metabolism
  • LLC-PK1 Cells / drug effects
  • LLC-PK1 Cells / metabolism
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / metabolism
  • Nitric Oxide Synthase / metabolism
  • Nitric Oxide Synthase Type III
  • Onium Compounds / pharmacology
  • Phospholipases / metabolism
  • Quercetin / pharmacology
  • Receptor, Bradykinin B2
  • Receptors, Bradykinin / metabolism
  • Signal Transduction
  • Solubility
  • Superoxides / antagonists & inhibitors
  • Superoxides / metabolism*
  • Swine
  • Tyrosine / analogs & derivatives*
  • Tyrosine / metabolism
  • Vitamin K 3 / pharmacology

Substances

  • Antioxidants
  • Free Radical Scavengers
  • Onium Compounds
  • Receptor, Bradykinin B2
  • Receptors, Bradykinin
  • Superoxides
  • 3-nitrotyrosine
  • Tyrosine
  • 1,2-Dihydroxybenzene-3,5-Disulfonic Acid Disodium Salt
  • diphenyleneiodonium
  • Vitamin K 3
  • Cyclosporine
  • Quercetin
  • Nitric Oxide Synthase
  • Nitric Oxide Synthase Type III
  • NADPH Oxidases
  • Phospholipases
  • GTP-Binding Proteins
  • Guanylate Cyclase
  • Cyclic GMP
  • Bradykinin
  • Acetylcysteine