Suppression of the inducible form of nitric oxide synthase prior to traumatic brain injury improves cytochrome c oxidase activity and normalizes cellular energy levels

Neuroscience. 2008 Jan 2;151(1):148-54. doi: 10.1016/j.neuroscience.2007.09.029. Epub 2007 Sep 20.

Abstract

We have previously shown that the observed immediate increase in nitric oxide (NO) plays a significant role in the control of the cerebral microcirculation following traumatic brain injury (TBI). However, a second consequence of increased NO production after TBI may be impaired mitochondrial function, due to the fact that NO is a well-known inhibitor of cytochrome c oxidase (CcO). CcO is a key enzyme of the mitochondrial oxidative phosphorylation (OxPhos) machinery, which creates cellular energy in the form of ATP. NO competes with oxygen at the heme a(3)-Cu(B) reaction center of CcO. We thus hypothesized that TBI triggers inhibition of CcO, which would in turn lead to a decreased energy production by OxPhos at a time of an elevated energy demand for tissue remodeling. Here we show that TBI as induced by an acceleration weight drop model of diffuse brain injury in rats leads to CcO inhibition and dramatically decreased ATP levels in brain cortex. CcO inhibition can be partially restored by application of iNOS antisense oligonucleotides prior to TBI, which leads to a normalization of ATP levels similar to the controls. We propose that a lack of energy after TBI caused by inhibition of CcO is an important aspect of trauma pathology.

Publication types

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

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Animals
  • Blotting, Western
  • Brain / pathology
  • Brain Injuries / enzymology
  • Brain Injuries / metabolism*
  • Brain Injuries / pathology
  • Electron Transport Complex IV / metabolism*
  • Energy Metabolism / physiology*
  • Enzyme Inhibitors / pharmacology*
  • In Situ Hybridization
  • Male
  • Mitochondria / drug effects
  • Mitochondria / enzymology
  • Nitric Oxide / biosynthesis
  • Nitric Oxide Synthase Type II / antagonists & inhibitors
  • Nitric Oxide Synthase Type II / biosynthesis*
  • Nitric Oxide Synthase Type II / physiology
  • Oligoribonucleotides, Antisense / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Up-Regulation / drug effects

Substances

  • Enzyme Inhibitors
  • Oligoribonucleotides, Antisense
  • Nitric Oxide
  • Adenosine Triphosphate
  • Nitric Oxide Synthase Type II
  • Electron Transport Complex IV