Oxidative phosphorylation activation is an important characteristic of DOX resistance in hepatocellular carcinoma cells

Cell Commun Signal. 2018 Feb 5;16(1):6. doi: 10.1186/s12964-018-0217-2.

Abstract

Background: Despite the implications for tumor growth and cancer drug resistance, the mechanisms underlying differences in energy metabolism among cells remain unclear.

Methods: To analyze differences between cell types, cell viability, ATP and α-ketoglutaric acid levels, the oxygen consumption rate and extracellular acidification rate, and the expression of key enzymes involved in α-KG metabolism and transfer were examined. Additionally, UPLC-MS/MS was used to determine the doxorubicin (DOX) content in SMMC-7721 and SMMC-7721/DOX cells.

Results: We found that energy metabolism in SMMC-7721 cells is mainly dependent on the glycolysis pathway, whereas SMMC-7721/DOX cells depend more heavily on the oxidative phosphorylation pathway. Cell viability and intracellular ATP levels in SMMC-7721/DOX cells were significantly reduced by rotenone and oligomycin, inhibitors of oxidative phosphorylation. However, SMMC-7721 cell properties were more strongly influenced by an inhibitor of glycolysis, 2-deoxy-D-glucose. Furthermore, the suppressive effect of α-KG on ATP synthase plays an important role in the low levels of oxidative phosphorylation in SMMC-7721 cells; this effect could be strengthened by the metabolic poison methotrexate and reversed by L-(-)-malic acid, an accelerator of the malate-aspartate cycle.

Conclusions: The inhibitory effect of α-KG on ATP synthase was uncoupled with the tricarboxylic acid cycle and oxidative phosphorylation in SMMC-7721 cells; accordingly, energy metabolism was mainly determined by glycolysis. In drug-resistant cells, a remarkable reduction in the inhibitory effects of α-KG on ATP synthase resulted in better coordination among the TCA cycle, oxidative phosphorylation, and glycolysis, providing novel potential strategies for clinical treatment of liver cancer resistance.

Keywords: Drug resistance; Energy metabolism; Hepatocellular carcinoma; Mechanism; α-ketoglutaric acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • ATP Synthetase Complexes / antagonists & inhibitors
  • ATP Synthetase Complexes / metabolism
  • Adenosine Triphosphate / metabolism
  • Carcinoma, Hepatocellular / metabolism
  • Carcinoma, Hepatocellular / pathology
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Deoxyglucose / pharmacology
  • Doxorubicin / pharmacology*
  • Drug Resistance, Neoplasm*
  • Energy Metabolism / drug effects
  • Glycolysis / drug effects
  • Humans
  • Ketone Oxidoreductases / antagonists & inhibitors
  • Ketone Oxidoreductases / metabolism
  • Liver Neoplasms / metabolism
  • Liver Neoplasms / pathology
  • Malates / pharmacology
  • Methotrexate / pharmacology
  • Oxidative Phosphorylation / drug effects*

Substances

  • Malates
  • Doxorubicin
  • malic acid
  • Adenosine Triphosphate
  • Deoxyglucose
  • Ketone Oxidoreductases
  • 2-oxoglutarate synthase
  • ATP Synthetase Complexes
  • Methotrexate