Sulforaphane attenuates hepatic fibrosis via NF-E2-related factor 2-mediated inhibition of transforming growth factor-β/Smad signaling

Free Radic Biol Med. 2012 Feb 1;52(3):671-682. doi: 10.1016/j.freeradbiomed.2011.11.012. Epub 2011 Dec 1.

Abstract

Sulforaphane (SFN) is a dietary isothiocyanate that exerts chemopreventive effects via NF-E2-related factor 2 (Nrf2)-mediated induction of antioxidant/phase II enzymes, such as heme oxygenase-1 (HO-1) and NAD(P)H quinone oxidoreductase 1 (NQO1). This work was undertaken to evaluate the effects of SFN on hepatic fibrosis and profibrotic transforming growth factor (TGF)-β/Smad signaling, which are closely associated with oxidative stress. SFN suppressed TGF-β-enhanced expression of α-smooth muscle actin (α-SMA), a marker of hepatic stellate cell (HSC) activation, and profibrogenic genes such as type I collagen, fibronectin, tissue inhibitor of matrix metalloproteinase (TIMP)-1, and plasminogen activator inhibitor (PAI)-1 in hTERT, an immortalized human HSC line. SFN inhibited TGF-β-stimulated activity of a PAI-1 promoter construct and (CAGA)(9) MLP-Luc, an artificial Smad3/4-specific reporter, in addition to reducing phosphorylation and nuclear translocation of Smad3. Nrf2 overexpression was sufficient to inhibit the TGF-β/Smad signaling and PAI-1 expression. Conversely, knockdown of Nrf2, but not inhibition of HO-1 or NQO1 activity, significantly abolished the inhibitory effect of SFN on (CAGA)(9) MLP-Luc activity. However, inhibition of NQO1 activity reversed repression of TGF-β-stimulated expression of type I collagen by SFN, suggesting the involvement of antioxidant activity of SFN in the suppression of Smad-independent fibrogenic gene expression. Finally, SFN treatment attenuated the development and progression of early stage hepatic fibrosis induced by bile duct ligation in mice, accompanied by reduced expression of type I collagen and α-SMA. Collectively, these results show that SFN elicits an antifibrotic effect on hepatic fibrosis through Nrf2-mediated inhibition of the TGF-β/Smad signaling and subsequent suppression of HSC activation and fibrogenic gene expression.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Active Transport, Cell Nucleus
  • Animals
  • Cell Line
  • Enzyme Induction / drug effects
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism
  • Fibrosis
  • Gene Expression / drug effects
  • Genes, Reporter
  • Humans
  • Isothiocyanates
  • Liver Diseases / pathology
  • Liver Diseases / prevention & control*
  • Luciferases / biosynthesis
  • Luciferases / genetics
  • Male
  • Mice
  • Mice, Inbred C57BL
  • NF-E2-Related Factor 2 / metabolism*
  • Phosphorylation
  • Promoter Regions, Genetic
  • Protein Binding
  • Serpin E2 / genetics
  • Serpin E2 / metabolism
  • Signal Transduction
  • Smad Proteins / antagonists & inhibitors
  • Smad Proteins / metabolism*
  • Sulfoxides
  • Thiocyanates / pharmacology*
  • Thiocyanates / therapeutic use
  • Transforming Growth Factor beta / antagonists & inhibitors
  • Transforming Growth Factor beta / metabolism*

Substances

  • Extracellular Matrix Proteins
  • Isothiocyanates
  • NF-E2-Related Factor 2
  • Serpin E2
  • Serpine2 protein, mouse
  • Smad Proteins
  • Sulfoxides
  • Thiocyanates
  • Transforming Growth Factor beta
  • Luciferases
  • sulforaphane