Ischemic preconditioning attenuates ischemia/reperfusion injury in rat steatotic liver: role of heme oxygenase-1-mediated autophagy

Oncotarget. 2016 Nov 29;7(48):78372-78386. doi: 10.18632/oncotarget.13281.

Abstract

Steatotic livers are more susceptible to ischemia/reperfusion (I/R) injury, which is ameliorated by ischemic preconditioning (IPC). Autophagy possesses protective action on liver I/R injury and declines in steatotic livers. The aim of this study was to test the hypothesis that the increased susceptibility of steatotic livers to I/R injury was associated with defective hepatic autophagy, which could be restored by IPC via heme oxygenase-1 (HO-1) signaling. Obesity and hepatic steatosis was induced using a high fat diet. Obesity impaired hepatic autophagy activity and decreased hepatic HO-1 expression. Induction of HO-1 restored autophagy activity and inhibited calpain 2 activity. Additionally, suppression of calpain 2 activity also restored autophagy activity. Mitochondrial dysfunction and hepatocellular injury were significantly increased in steatotic livers compared to lean livers in response to I/R injury. This increase in sensitivity to I/R injury was associated with defective hepatic autophagy activity in steatotic livers. IPC increased autophagy and reduced mitochondrial dysfunction and hepatocellular damage in steatotic livers following I/R injury. Furthermore, IPC increased HO-1 expression. Inhibition of HO-1 decreased the IPC-induced autophagy, increased calpain 2 activity and diminished the protective effect of IPC against I/R injury. Inhibition of calpain 2 restored autophagic defect and attenuated mitochondrial dysfunction in steatotic livers after I/R. Collectively, IPC might ameliorate steatotic liver damage and restore mitochondrial function via HO-1-mediated autophagy.

Keywords: autophagy; heme oxygenase-1, Pathology Section; ischemic preconditioning; liver ischemia/reperfusion injury; steatosis.

MeSH terms

  • Animals
  • Autophagy*
  • Autophagy-Related Protein 7 / genetics
  • Autophagy-Related Protein 7 / metabolism
  • Calpain / metabolism
  • Cells, Cultured
  • Diet, High-Fat
  • Disease Models, Animal
  • Fatty Liver / enzymology
  • Fatty Liver / genetics
  • Fatty Liver / pathology
  • Fatty Liver / therapy*
  • Heme Oxygenase (Decyclizing) / genetics
  • Heme Oxygenase (Decyclizing) / metabolism*
  • Hepatocytes / enzymology*
  • Hepatocytes / pathology
  • Ischemic Preconditioning / methods*
  • Liver / enzymology*
  • Liver / pathology
  • Male
  • Mitochondria, Liver / enzymology
  • Mitochondria, Liver / pathology
  • RNA Interference
  • Rats, Sprague-Dawley
  • Reperfusion Injury / enzymology
  • Reperfusion Injury / genetics
  • Reperfusion Injury / pathology
  • Reperfusion Injury / prevention & control*
  • Signal Transduction
  • Time Factors
  • Transfection

Substances

  • Atg7 protein, rat
  • Heme Oxygenase (Decyclizing)
  • Hmox1 protein, rat
  • Calpain
  • Capn2 protein, rat
  • Autophagy-Related Protein 7