Sulfasalazine induces haem oxygenase-1 via ROS-dependent Nrf2 signalling, leading to control of neointimal hyperplasia

Cardiovasc Res. 2009 Jun 1;82(3):550-60. doi: 10.1093/cvr/cvp072. Epub 2009 Feb 21.

Abstract

Aims: Inflammation, and the subsequent proliferative activity of vascular smooth muscle cells (VSMCs), is one of the major pathophysiological mechanisms associated with neointimal hyperplasia following vascular injury. Although sulfasalazine (SSZ) has been used as an anti-inflammatory and immune-modulatory agent in various inflammatory diseases, its primary targets and therapeutic effects on vascular disease have not yet been determined. We investigated whether SSZ could suppress VSMC growth and prevent neointimal hyperplasia.

Methods and results: SSZ was found to have pro-apoptotic and anti-proliferative activity in cultured VSMCs. Unexpectedly, these effects were not mediated by nuclear factor kappa B (NF-kappaB) inhibition, which has been suggested to be the anti-inflammatory mechanism associated with the effects of SSZ. Instead, cell-cycle arrest of the VSMCs was observed, which was mediated by induction of haem oxygenase-1 (HO-1) followed by an increased expression of p21(waf1/Cip1). The underlying mechanism for SSZ-induced HO-1 expression was by reactive oxygen species (ROS)-dependent nuclear translocation and activation of nuclear factor erythroid-2-related factor 2 (Nrf2). In a rat carotid artery balloon injury model, administration of SSZ significantly suppressed neointimal growth. In a series of reverse experiments, inhibition of HO-1 by shRNA, ROS by N-acetylcysteine (NAC) or Nrf2 by dominant-negative Nrf2 abrogated the beneficial effects of SSZ.

Conclusion: Our data demonstrate that SSZ inhibits VSMC proliferation in vitro and in vivo through a novel signalling pathway and may be a promising therapeutic option for the treatment of proliferative vascular disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Anti-Inflammatory Agents, Non-Steroidal / pharmacology
  • Anti-Inflammatory Agents, Non-Steroidal / therapeutic use*
  • Antioxidants / metabolism
  • Apoptosis / drug effects
  • Carotid Artery Diseases / prevention & control
  • Carotid Artery, Common / pathology
  • Cell Proliferation / drug effects
  • Cells, Cultured
  • Cyclin-Dependent Kinase Inhibitor p21 / metabolism
  • Gene Expression Regulation
  • Graft Occlusion, Vascular / prevention & control*
  • Heme Oxygenase-1 / metabolism*
  • Hyperplasia / prevention & control
  • Muscle, Smooth, Vascular / drug effects
  • Myocytes, Smooth Muscle / drug effects
  • NF-E2-Related Factor 2 / metabolism*
  • NF-kappa B / metabolism
  • Oxidative Stress / drug effects
  • Rats
  • Rats, Sprague-Dawley
  • Reactive Oxygen Species / metabolism
  • Sulfasalazine / pharmacology
  • Sulfasalazine / therapeutic use*
  • Tumor Necrosis Factor-alpha / metabolism

Substances

  • Anti-Inflammatory Agents, Non-Steroidal
  • Antioxidants
  • Cyclin-Dependent Kinase Inhibitor p21
  • NF-E2-Related Factor 2
  • NF-kappa B
  • Nfe2l2 protein, rat
  • Reactive Oxygen Species
  • Tumor Necrosis Factor-alpha
  • Sulfasalazine
  • Heme Oxygenase-1