Mitochondrial ND5 mutation mediated elevated ROS regulates apoptotic pathway epigenetically in a P53 dependent manner for generating pro-cancerous phenotypes

Mitochondrion. 2017 Jul:35:35-43. doi: 10.1016/j.mito.2017.05.001. Epub 2017 May 11.

Abstract

We have previously observed concomitant events of mutations in mitochondrial and nuclear genes, along with elevated reactive oxygen species (ROS) and differential methylation within the promoters of nuclear genes in tumors and in vitro experiments of tumorigenesis. These observations have made it pertinent to replicate and understand the role of acquired mitochondrial condition in tuning a cell to accomplish a pro-cancerous state. Using a codon optimized vector system for exogenous over-expression and mitochondrial localization; we have characterized here the role of over-expressed wild type mtND5 and one of its non-synonymous somatic mutation, ND5:P265H. The ectopically over-expressed ND5:P265H in mitochondria resulted in a reduced Complex I activity, generation of higher ADP/ATP ratio, reactive oxygen species (ROS) and carbonylation of proteins as compared to mock-transfected cells. Cells over-expressing mtND5 variant produced both peroxide as well as super-oxide ROS; the generation of which was dependent on the functional status of P53; modulating epigenetically the expression of key apoptosis pathway genes. The pro-cancerous phenotypes, of anchorage dependent and independent growth; increased glucose uptake and lactate production, were selectively observed only in P53 non-functional cells over-expressing mutant ND5:P265H. We propose that somatic mutation in mtND5 resulting in down-regulated complex I enzyme activity, elevated ROS and up-regulation of a set of nuclear anti-apoptotic genes epigenetically in the P53 dysfunctional cellular background, has provided a unique understanding of the molecular mechanism of mitochondrial mutation; and the concomitant existence of somatically acquired mitochondrial and nuclear p53 mutations, in cancer progression and promotion.

Keywords: Apoptotic pathway; Differential methylation; Mitochondrial DNA mutation; Reactive oxygen species; mtND5.

MeSH terms

  • Adenosine Diphosphate / metabolism
  • Adenosine Triphosphate / metabolism
  • Apoptosis
  • Cell Line
  • Electron Transport Complex I / genetics*
  • Electron Transport Complex I / metabolism*
  • Epigenesis, Genetic*
  • Humans
  • Mitochondrial Proteins / genetics*
  • Mitochondrial Proteins / metabolism*
  • Mutation, Missense*
  • Phenotype
  • Precancerous Conditions*
  • Reactive Oxygen Species / metabolism*
  • Tumor Suppressor Protein p53 / metabolism*

Substances

  • Mitochondrial Proteins
  • Reactive Oxygen Species
  • Tumor Suppressor Protein p53
  • Adenosine Diphosphate
  • Adenosine Triphosphate
  • MT-ND5 protein, human
  • Electron Transport Complex I