Pathway analysis reveals common pro-survival mechanisms of metyrapone and carbenoxolone after traumatic brain injury

PLoS One. 2013;8(1):e53230. doi: 10.1371/journal.pone.0053230. Epub 2013 Jan 9.

Abstract

Developing new pharmacotherapies for traumatic brain injury (TBI) requires elucidation of the neuroprotective mechanisms of many structurally and functionally diverse compounds. To test our hypothesis that diverse neuroprotective drugs similarly affect common gene targets after TBI, we compared the effects of two drugs, metyrapone (MT) and carbenoxolone (CB), which, though used clinically for noncognitive conditions, improved learning and memory in rats and humans. Although structurally different, both MT and CB inhibit a common molecular target, 11β hydroxysteroid dehydrogenase type 1, which converts inactive cortisone to cortisol, thereby effectively reducing glucocorticoid levels. We examined injury-induced signaling pathways to determine how the effects of these two compounds correlate with pro-survival effects in surviving neurons of the injured rat hippocampus. We found that treatment of TBI rats with MT or CB acutely induced in hippocampal neurons transcriptional profiles that were remarkably similar (i.e., a coordinated attenuation of gene expression across multiple injury-induced cell signaling networks). We also found, to a lesser extent, a coordinated increase in cell survival signals. Analysis of injury-induced gene expression altered by MT and CB provided additional insight into the protective effects of each. Both drugs attenuated expression of genes in the apoptosis, death receptor and stress signaling pathways, as well as multiple genes in the oxidative phosphorylation pathway such as subunits of NADH dehydrogenase (Complex1), cytochrome c oxidase (Complex IV) and ATP synthase (Complex V). This suggests an overall inhibition of mitochondrial function. Complex 1 is the primary source of reactive oxygen species in the mitochondrial oxidative phosphorylation pathway, thus linking the protective effects of these drugs to a reduction in oxidative stress. The net effect of the drug-induced transcriptional changes observed here indicates that suppressing expression of potentially harmful genes, and also, surprisingly, reduced expression of pro-survival genes may be a hallmark of neuroprotective therapeutic effects.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Brain Injuries / complications
  • Brain Injuries / drug therapy*
  • Brain Injuries / genetics*
  • Brain Injuries / pathology
  • Carbenoxolone / pharmacology
  • Carbenoxolone / therapeutic use*
  • Cell Death / drug effects
  • Cell Death / genetics
  • Cell Survival / drug effects
  • Cell Survival / genetics
  • Gene Expression Regulation / drug effects
  • Hippocampus / drug effects
  • Hippocampus / pathology
  • Humans
  • Male
  • Metyrapone / pharmacology
  • Metyrapone / therapeutic use*
  • Nerve Degeneration / complications
  • Nerve Degeneration / drug therapy
  • Nerve Degeneration / pathology
  • Neuroprotective Agents / pharmacology
  • Neuroprotective Agents / therapeutic use
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Stress, Physiological / drug effects
  • Stress, Physiological / genetics

Substances

  • Neuroprotective Agents
  • Reactive Oxygen Species
  • Carbenoxolone
  • Metyrapone

Grants and funding

This study was supported by the Department of Anesthesiology, the Moody Foundation and the Moody Center for Traumatic Brain Injury and Spinal Cord Injury Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.