Tumor necrosis factor-alpha induces endothelial dysfunction in the prediabetic metabolic syndrome

Circ Res. 2006 Jul 7;99(1):69-77. doi: 10.1161/01.RES.0000229685.37402.80. Epub 2006 Jun 1.

Abstract

Inflammation is a condition that underscores many cardiovascular pathologies including endothelial dysfunction, but no link is yet established between the vascular pathology of the metabolic syndrome with a particular inflammatory cytokine. We hypothesized that impairments in coronary endothelial function in the obese condition the prediabetic metabolic syndrome is caused by TNF-alpha overexpression. To test this, we measured endothelium-dependent (acetylcholine) and -independent vasodilation (sodium nitroprusside) of isolated, pressurized coronary small arteries from lean control and Zucker obese fatty (ZOF, a model of prediabetic metabolic syndrome) rats. In ZOF rats, dilation to ACh was blunted compared with lean rats, but sodium nitroprusside-induced dilation was comparable. Superoxide (O2*-) generation was elevated in vessels from ZOF rats compared with lean rats, and administration of the O2*- scavenger TEMPOL, NAD(P)H oxidase inhibitor (apocynin), or anti-TNF-alpha restored endothelium-dependent dilation in the ZOF rats. Real-time PCR and Western blotting revealed that mRNA and protein of TNF-alpha were higher in ZOF rats than that in lean rats, whereas eNOS protein levels were reduced in the ZOF versus lean rats. Immunostaining showed that TNF-alpha in ZOF rat heart is localized in endothelial cells and vascular smooth muscle cells. Expression of NAD(P)H subunits p22 and p40-phox were elevated in ZOF compared with lean animals. Administration of TNF-alpha more than 3 days also induced expression of these NAD(P)H subunits and abrogated endothelium-dependent dilation. In conclusion, the results demonstrate the endothelial dysfunction occurring in the metabolic syndrome is the result of effects of the inflammatory cytokine TNF-alpha and subsequent production of O2*-.

Publication types

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

MeSH terms

  • Acetylcholine / pharmacology
  • Animals
  • Coronary Vessels / drug effects
  • Coronary Vessels / metabolism
  • Coronary Vessels / physiopathology*
  • Endothelial Cells / metabolism
  • Endothelium, Vascular / physiopathology*
  • In Vitro Techniques
  • Male
  • Metabolic Syndrome / blood
  • Metabolic Syndrome / physiopathology*
  • Muscle, Smooth, Vascular / metabolism
  • Myocytes, Cardiac / metabolism
  • Myocytes, Smooth Muscle / metabolism
  • NADPH Oxidases / metabolism
  • Nitric Oxide / metabolism
  • Nitric Oxide Synthase Type III / metabolism
  • Obesity / blood
  • Obesity / physiopathology
  • Osmolar Concentration
  • Prediabetic State / blood
  • Prediabetic State / physiopathology*
  • RNA, Messenger / blood
  • Rats
  • Rats, Zucker
  • Superoxides / metabolism
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / metabolism*
  • Vasodilation
  • Vasodilator Agents / pharmacology

Substances

  • RNA, Messenger
  • Tumor Necrosis Factor-alpha
  • Vasodilator Agents
  • Superoxides
  • Nitric Oxide
  • Nitric Oxide Synthase Type III
  • NADPH Oxidases
  • Acetylcholine