Metformin delays AKT/c-Met-driven hepatocarcinogenesis by regulating signaling pathways for de novo lipogenesis and ATP generation

Toxicol Appl Pharmacol. 2019 Feb 15:365:51-60. doi: 10.1016/j.taap.2019.01.004. Epub 2019 Jan 6.

Abstract

Hepatocellular carcinoma (HCC) is a lethal malignancy with few effective options for therapeutic treatment in its advanced stages. Metformin, a first-line oral agent used in the treatment of type 2 diabetes, exhibits efficacy in metabolic reprogramming fueling changes in cell growth and proliferation for multiple cancer types, including HCC. However, the molecular mechanism by which metformin delays hepatocarcinogenesis in individuals with hepatic steatosis remains rare. Here, we investigate the preventive efficacy of metformin in a rapid AKT/c-Met-triggered HCC mouse model featuring excessive levels of steatosis. Hematoxylin and eosin staining, Oil Red O staining and immunoblotting were applied for mechanistic investigations. Pharmacological and biochemical strategies were employed to illuminate molecular evidence for HCC cell lines. The results show that metformin obstructs the malignant transformation of hepatocytes in AKT/c-Met mice. Mechanistically, metformin reduces the expression of phospho-ERK (Thr202/Tyr204) and two forms of proto-oncogenes, Cyclin D1 and c-Myc, in AKT/c-Met mice. Moreover, metformin ameliorates FASN-mediated aberrant lipogenesis and HK2/PKM2-driven ATP generation in vivo. Furthermore, metformin represses the expression of FASN and HK-2 by targeting c-Myc in an AMPK-dependent manner in vitro. In addition, metformin is effective at inhibiting PKM2 expression in the presence of an AMPK inhibitor compound C, suggesting that its functioning in PKM2 is AMPK-independent. Our study experimentally validates a novel molecular mechanism by which metformin alleviates enhanced lipogenesis and high energy metabolism during hepatocarcinogenesis, indicating that metformin may serve as an agent for the prevention of HCC in patients with nonalcoholic fatty liver diseases.

Keywords: Fatty acid synthase; Hepatocarcinogenesis; Hexokinase 2; Metformin; Pyruvate kinase M2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Animals
  • Anticarcinogenic Agents / pharmacology*
  • Carcinoma, Hepatocellular / enzymology
  • Carcinoma, Hepatocellular / genetics
  • Carcinoma, Hepatocellular / pathology
  • Carcinoma, Hepatocellular / prevention & control*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Transformation, Neoplastic / drug effects*
  • Cell Transformation, Neoplastic / genetics
  • Cell Transformation, Neoplastic / metabolism
  • Cell Transformation, Neoplastic / pathology
  • Disease Models, Animal
  • Energy Metabolism / drug effects*
  • Fatty Acid Synthase, Type I / metabolism
  • Fatty Liver / drug therapy*
  • Fatty Liver / enzymology
  • Fatty Liver / genetics
  • Fatty Liver / pathology
  • Hexokinase / metabolism
  • Humans
  • Lipogenesis / drug effects*
  • Liver / drug effects*
  • Liver / enzymology
  • Liver / pathology
  • Liver Neoplasms / enzymology
  • Liver Neoplasms / genetics
  • Liver Neoplasms / pathology
  • Liver Neoplasms / prevention & control*
  • Metformin / pharmacology*
  • Mice
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism*
  • Proto-Oncogene Proteins c-met / genetics
  • Proto-Oncogene Proteins c-met / metabolism*
  • Pyruvate Kinase / metabolism
  • Signal Transduction / drug effects

Substances

  • Anticarcinogenic Agents
  • Adenosine Triphosphate
  • Metformin
  • Fatty Acid Synthase, Type I
  • Hexokinase
  • hexokinase 2, mouse
  • Pkm protein, mouse
  • Pyruvate Kinase
  • Proto-Oncogene Proteins c-met
  • Proto-Oncogene Proteins c-akt