Mitigation of carbon tetrachloride-induced hepatic injury by methylene blue, a repurposed drug, is mediated by dual inhibition of GSK3β downstream of PKA

Br J Pharmacol. 2014 Jun;171(11):2790-802. doi: 10.1111/bph.12637.

Abstract

Background and purpose: Methylene blue (MB) has recently been considered for new therapeutic applications. In this study, we investigated whether MB has antioxidant and mitochondria-protecting effects and can prevent the development of toxicant-induced hepatitis. In addition, we explored the underlying basis of its effects.

Experimental approach: Blood biochemistry and histopathology were assessed in mice injected with CCl4 (0.5 mL·kg(-1)) following MB administration (3 mg·kg(-1) ·day(-1), 3 days). Immunoblottings were performed to measure protein levels. Cell survival, H2 O2 , and mitochondrial superoxide and membrane permeability transition were determined in HepG2 cells.

Key results: MB protected cells from oxidative stress induced by arachidonic acid plus iron; it restored GSH content and decreased the production of H2 O2 . It consistently attenuated mitochondria dysfunction, as indicated by inhibition of superoxide production and mitochondrial permeability transition. MB inhibited glycogen synthase kinase-3β (GSK3β) and protected the liver against CCl4. Using siRNA, the inhibition of GSK3β was shown to depend on AMPK. MB increased the activation of AMPK in vitro (3-24 h) and in vivo. MB also increased the phosphorylation of liver kinase B1 (LKB1) via cAMP-dependent PKA. SiRNA knockdown of LKB1 eliminated phosphorylation of AMPK and inhibited MB activation of AMPK. In addition, MB treatment (≤1 h) facilitated PKA-mediated GSK3β serine phosphorylation independently of AMPK.

Conclusions and implications: MB has antioxidant and mitochondria-protecting effects and protects the liver from toxicants, which results from the dual inhibition of GSK3β by AMPK downstream of PKA-activated LKB1, and PKA itself. Our findings reveal a novel pharmacological effect of MB and its molecular basis.

Keywords: AMPK; GSK3β; LKB1; PKA; methylene blue.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinase Kinases
  • AMP-Activated Protein Kinases / metabolism
  • Animals
  • Carbon Tetrachloride
  • Cell Survival / drug effects
  • Chemical and Drug Induced Liver Injury / drug therapy
  • Chemical and Drug Induced Liver Injury / etiology
  • Chemical and Drug Induced Liver Injury / metabolism*
  • Chemical and Drug Induced Liver Injury / pathology
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • Drug Repositioning
  • Glutathione / metabolism
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors*
  • Glycogen Synthase Kinase 3 / metabolism
  • Glycogen Synthase Kinase 3 beta
  • HeLa Cells
  • Hep G2 Cells
  • Humans
  • Hydrogen Peroxide / metabolism
  • Liver / drug effects
  • Liver / metabolism
  • Liver / pathology
  • Male
  • Methylene Blue / pharmacology*
  • Methylene Blue / therapeutic use
  • Mice, Inbred C57BL
  • Mitochondria / drug effects
  • Mitochondria / metabolism
  • Phosphorylation / drug effects
  • Protective Agents / pharmacology*
  • Protective Agents / therapeutic use
  • Protein Serine-Threonine Kinases / metabolism
  • Reactive Oxygen Species / metabolism

Substances

  • Protective Agents
  • Reactive Oxygen Species
  • Hydrogen Peroxide
  • Carbon Tetrachloride
  • GSK3B protein, human
  • Glycogen Synthase Kinase 3 beta
  • Gsk3b protein, mouse
  • Protein Serine-Threonine Kinases
  • STK11 protein, human
  • Cyclic AMP-Dependent Protein Kinases
  • Glycogen Synthase Kinase 3
  • AMP-Activated Protein Kinase Kinases
  • AMP-Activated Protein Kinases
  • Glutathione
  • Methylene Blue