SIRT3 aggravates metformin-induced energy stress and apoptosis in ovarian cancer cells

Exp Cell Res. 2018 Jun 15;367(2):137-149. doi: 10.1016/j.yexcr.2018.03.030. Epub 2018 Mar 23.

Abstract

Increasing evidence suggests that mitochondrial respiratory chain complex I participates in carcinogenesis and cancer progression by providing energy and maintaining mitochondrial function. However, the role of complex I in ovarian cancer is largely unknown. In this study we showed that metformin, considered to be an inhibitor of complex I, simultaneously inhibited cell growth and induced mitochondrial-related apoptosis in human ovarian cancer cells. Metformin interrupted cellular energy metabolism mainly by causing damage to complex I that impacted mitochondrial function. Additionally, treatment with metformin increased the activation of sirtuin 3 (SIRT3), a mitochondrial deacetylase. We demonstrated that SIRT3 overexpression aggravated metformin-induced apoptosis, energy stress and mitochondrial dysfunction. Moreover, treatment with metformin or SIRT3 overexpression increased activation of AMP-activated protein kinase (AMPK), a major sensor of cellular energy status. AMPK compensated for energy loss by increasing glycolysis. The impact of this was assessed by reducing glucose levels in the media or by using inhibitors (2-deoxyglucose, Compound C) of glycolysis and AMPK. The combination of these factors with metformin intensified cytotoxicity through further downregulation of ATP. Our study outlines an important role for SIRT3 in the antitumor effect of mitochondrial complex I inhibitors in human ovarian cancer cells. This effect appears to be mediated by induction of energy stress and apoptosis. Strategies that target the mitochondria could be enhanced by modulating glycolysis to further aggravate energy stress that may increase the antitumor effect.

Keywords: Apoptosis; Energy stress; Metformin; Mitochondrial dysfunction; Ovarian cancer; Sirtuin-3.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • Antineoplastic Agents / pharmacology*
  • Apoptosis*
  • Cell Line, Tumor
  • Electron Transport Complex I / metabolism
  • Female
  • Glucose / metabolism
  • Humans
  • Metformin / pharmacology*
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Ovarian Neoplasms / metabolism*
  • Ovarian Neoplasms / pathology
  • Sirtuin 3 / biosynthesis
  • Sirtuin 3 / metabolism*
  • Stress, Physiological

Substances

  • Antineoplastic Agents
  • Metformin
  • AMP-Activated Protein Kinases
  • SIRT3 protein, human
  • Sirtuin 3
  • Electron Transport Complex I
  • Glucose