Nuclear Thioredoxin-1 Overexpression Attenuates Alcohol-Mediated Nrf2 Signaling and Lung Fibrosis

Alcohol Clin Exp Res. 2016 Sep;40(9):1846-56. doi: 10.1111/acer.13148. Epub 2016 Jul 20.

Abstract

Background: Alcohol abuse, which impairs antioxidant defenses and promotes acute lung injury, increases Nrf2 nuclear translocation but nevertheless inhibits its activation of the antioxidant response element (ARE). Thioredoxin-1 (Trx1) is required for optimal Nrf2 binding and activation of the ARE, and we hypothesized that its inhibition contributes to impaired Nrf2-ARE signaling in the alcoholic lung.

Methods: Lung tissue and primary lung fibroblasts (PLFs) were isolated from C57/BL6 wild-type (WT) and transgenic mice overexpressing the human Trx1 gene with a nuclear localizing sequence (NLS-Tg); some mice consumed alcohol in water prior to lung tissue and PLF isolation; in some mice, acute lung injury was induced with intratracheal bleomycin. In other experiments, PLFs were isolated from WT and NLS-Tg mice and then exposed to alcohol. Finally, PLF isolated from WT mice were transfected with Trx1 expression vector containing either a cytosolic localized sequence (NES) or a nuclear localized sequence (NLS) prior to alcohol exposure.

Results: Alcohol treatment in vivo or in vitro decreased Trx1 expression, and bleomycin-treated alcohol-fed mice had fibrotic disrepair in their lungs. In parallel, whereas alcohol exposure in vitro increased TGFβ1 expression and decreased Nrf2-ARE activity in PLF from WT mice, these effects were not observed in PLF from NLS-Tg mice. Finally, selective overexpression of Trx1 in the nucleus but not in the cytosol preserved Nrf2-ARE activity during alcohol exposure.

Conclusions: Although alcohol-induced redox stress actually promotes Nrf2 nuclear translocation, the coincident suppression of Trx1 impairs Nrf2-ARE activity within the nuclear compartment. Nuclear overexpression of Trx1 restored Nrf2-ARE activity and attenuated alcohol-induced TGFβ1 expression and alcohol-induced exaggerate response to bleomycin-induced acute lung injury.

Keywords: Alcohol; Bleomycin; Lung Fibroblasts; TGFβ1; Thioredoxin-1.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Cell Nucleus / drug effects
  • Cell Nucleus / metabolism*
  • Cells, Cultured
  • Ethanol / administration & dosage*
  • Gene Expression
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • NF-E2-Related Factor 2 / antagonists & inhibitors
  • NF-E2-Related Factor 2 / metabolism*
  • Pulmonary Fibrosis / chemically induced
  • Pulmonary Fibrosis / metabolism*
  • Pulmonary Fibrosis / prevention & control
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Thioredoxins / biosynthesis*
  • Thioredoxins / genetics

Substances

  • NF-E2-Related Factor 2
  • Nfe2l2 protein, mouse
  • TXN protein, human
  • Ethanol
  • Thioredoxins