Fibrogenic actions of acetaldehyde are β-catenin dependent but Wingless independent: a critical role of nucleoredoxin and reactive oxygen species in human hepatic stellate cells

Free Radic Biol Med. 2013 Dec:65:1487-1496. doi: 10.1016/j.freeradbiomed.2013.07.017. Epub 2013 Jul 20.

Abstract

We investigated whether the fibrogenic actions of acetaldehyde, the immediate oxidation product of ethanol, are mediated via Wingless (WNT) and/or β-catenin pathways in human hepatic stellate cells (HSC). First, we show that both β-catenin small inhibitory RNA and a dominant negative-MYC expression vector markedly down-regulated the expressions of fibrogenic genes in freshly isolated HSC. We further show that acetaldehyde up-regulated platelet-derived growth factor receptor beta mRNA and protein expressions ranging from 4.0- to 7.2-fold (P<0.001). Acetaldehyde induced MYC and collagen type-1 alpha-2 mRNA and protein expressions were WNT independent because DKK1, an antagonist of the canonical WNT/β-catenin pathway, completely failed to block these inductions. Acetaldehyde increased phospho-glycogen synthase kinase-3 beta (GSK3B) protein by 31% (P<0.01), whereas phospho-β-catenin protein decreased by 50% (P ≤ 0.01). Significantly, in contrast to 43% (P<0.01) inhibition of β-catenin nuclear translocation in nucleoredoxin (NXN)-overexpressed HSC, acetaldehyde profoundly stimulated β-catenin nuclear translocation by 51%, (P<0.01). Acetaldehyde also increased the cellular reactive oxygen species level 2-fold (P<0.001) with a concomitant 2-fold (P<0.001) increase in 4-hydroxynonenal adducts. Conversely, there was a 44% decrease (P<0.001) in glutathione levels with a concomitant 76% (P<0.001) decrease in the level of NXN/ disheveled (DVL) complex. Based on these findings, we conclude that actions of acetaldehyde are mediated by a mechanism that inactivates NXN by releasing DVL, leading to the inactivation of GSK3B, and thereby blocks β-catenin phosphorylation and degradation. Thus, the stabilized β-catenin translocates to the nucleus where it up-regulates the fibrogenic pathway genes. This novel mechanism of action of acetaldehyde has the potential for therapeutic interventions in liver fibrosis induced by alcohol.

Keywords: 2′,7′- dichorofluorescein diacetate; 4-HNE; 4-hydroxynonenal; 5,5′-dithiobis(2-nitrobenzoic acid); ACH; ACTA1; Acetaldehyde; COL1A2; DCFDA; DMEM; DTNB; DVL; Dulbecco's modified Eagle's medium; FBS; GAPDH; GSH; GSK3B; HSC; Hepatic stellate cells; NXN; Nucleoredoxin; Oxidative stress; PDGFRB; PVDF; ROS; SDS-PAGE; TCF/LEFT; WNT; Wingless; acetaldehyde; alpha-smooth muscle actin; cell factor/lymphocyte enhancer factor; collagen type-1 alpha-2; disheveled; fetal bovine serum; glutathione; glyceraldehyde-3-phosphate dehydrogenase; glycogen synthase kinase-3 beta; hepatic stellate cells; nucleoredoxin; platelet-derived growth factor receptor beta; polyvinylidene difluoride; reactive oxygen species; sodium dodecyl sulfate polyacrylamide gel electrophoresis; β-Catenin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetaldehyde / pharmacology*
  • Active Transport, Cell Nucleus / drug effects
  • Adaptor Proteins, Signal Transducing / biosynthesis
  • Aldehydes / metabolism
  • Cells, Cultured
  • Collagen Type I / genetics
  • Dishevelled Proteins
  • Ethanol / chemistry
  • Ethanol / metabolism
  • Genes, myc / genetics
  • Glutathione / biosynthesis
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / biosynthesis
  • Glycogen Synthase Kinase 3 beta
  • Hepatic Stellate Cells / drug effects
  • Hepatic Stellate Cells / metabolism*
  • Humans
  • Intercellular Signaling Peptides and Proteins
  • Liver Cirrhosis, Alcoholic / pathology*
  • Nuclear Proteins / antagonists & inhibitors*
  • Nuclear Proteins / biosynthesis
  • Oxidative Stress / drug effects
  • Oxidoreductases / antagonists & inhibitors*
  • Oxidoreductases / biosynthesis
  • Phosphoproteins / biosynthesis
  • RNA Interference
  • RNA, Messenger / biosynthesis
  • RNA, Small Interfering
  • Reactive Oxygen Species / metabolism
  • Receptor, Platelet-Derived Growth Factor beta / biosynthesis
  • Receptor, Platelet-Derived Growth Factor beta / genetics
  • Wnt Proteins / metabolism
  • beta Catenin / antagonists & inhibitors
  • beta Catenin / genetics
  • beta Catenin / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • Aldehydes
  • Collagen Type I
  • DKK1 protein, human
  • Dishevelled Proteins
  • Intercellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Phosphoproteins
  • RNA, Messenger
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • Wnt Proteins
  • beta Catenin
  • Ethanol
  • Oxidoreductases
  • nucleoredoxin
  • Receptor, Platelet-Derived Growth Factor beta
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Glycogen Synthase Kinase 3
  • Glutathione
  • Acetaldehyde
  • 4-hydroxy-2-nonenal