Nitric oxide inhibits neointimal hyperplasia following vascular injury via differential, cell-specific modulation of SOD-1 in the arterial wall

Nitric Oxide. 2015 Jan 30:44:8-17. doi: 10.1016/j.niox.2014.10.009. Epub 2014 Nov 7.

Abstract

Superoxide (O2(•-)) promotes neointimal hyperplasia following arterial injury. Conversely, nitric oxide ((•)NO) inhibits neointimal hyperplasia through various cell-specific mechanisms, including redox regulation. What remains unclear is whether (•)NO exerts cell-specific regulation of the vascular redox environment following arterial injury to inhibit neointimal hyperplasia. Therefore, the aim of the present study was to assess whether (•)NO exerts cell-specific, differential modulation of O2(•-) levels throughout the arterial wall, establish the mechanism of such modulation, and determine if it regulates (•)NO-dependent inhibition of neointimal hyperplasia. In vivo, (•)NO increased superoxide dismutase-1 (SOD-1) levels following carotid artery balloon injury in a rat model. In vitro, (•)NO increased SOD-1 levels in vascular smooth muscle cells (VSMC), but had no effect on SOD-1 in endothelial cells or adventitial fibroblasts. This SOD-1 increase was associated with an increase in sod1 gene expression, increase in SOD-1 activity, and decrease in O2(•-) levels. Lastly, to determine the role of SOD-1 in (•)NO-mediated inhibition of neointimal hyperplasia, we performed the femoral artery wire injury model in wild type and SOD-1 knockout (KO) mice, with and without (•)NO. Interestingly, (•)NO inhibited neointimal hyperplasia only in wild type mice, with no effect in SOD-1 KO mice. In conclusion, these data show the cell-specific modulation of O2(•-) by (•)NO through regulation of SOD-1 in the vasculature, highlighting its importance on the inhibition of neointimal hyperplasia. These results also shed light into the mechanism of (•)NO-dependent redox balance, and suggest a novel VSMC redox target to prevent neointimal hyperplasia.

Keywords: Neointimal hyperplasia; Nitric oxide; SOD1; Superoxide; Vascular.

MeSH terms

  • Animals
  • Carotid Artery Injuries / metabolism*
  • Cell Proliferation
  • Cells, Cultured
  • Femoral Artery / injuries
  • Femoral Artery / metabolism
  • Femoral Artery / pathology
  • Hyperplasia / metabolism*
  • Hyperplasia / pathology
  • Male
  • Mice
  • Mice, Knockout
  • Muscle, Smooth, Vascular / cytology
  • Neointima / metabolism*
  • Neointima / pathology
  • Nitric Oxide / pharmacology*
  • Oxidative Stress / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Superoxide Dismutase / analysis
  • Superoxide Dismutase / genetics*
  • Superoxide Dismutase / metabolism
  • Superoxide Dismutase-1

Substances

  • Nitric Oxide
  • Sod1 protein, mouse
  • Sod1 protein, rat
  • Superoxide Dismutase
  • Superoxide Dismutase-1