Lipid-based DNA/siRNA transfection agents disrupt neuronal bioenergetics and mitophagy

Biochem J. 2017 Nov 10;474(23):3887-3902. doi: 10.1042/BCJ20170632.

Abstract

A multitude of natural and artificial compounds have been recognized to modulate autophagy, providing direct or, through associated pathways, indirect entry points to activation and inhibition. While these pharmacological tools are extremely useful in the study of autophagy, their abundance also suggests the potential presence of unidentified autophagic modulators that may interfere with experimental designs if applied unknowingly. Here, we report unanticipated effects on autophagy and bioenergetics in neuronal progenitor cells (NPCs) incubated with the widely used lipid-based transfection reagent lipofectamine (LF), which induced mitochondria depolarization followed by disruption of electron transport. When NPCs were exposed to LF for 5 h followed by 24, 48, and 72 h in LF-free media, an immediate increase in mitochondrial ROS production and nitrotyrosine formation was observed. These events were accompanied by disrupted mitophagy (accumulation of dysfunctional and damaged mitochondria, and of LC3II and p62), in an mTOR- and AMPK-independent manner, and despite the increased mitochondrial PINK1 (PTEN-inducible kinase 1) localization. Evidence supported a role for a p53-mediated abrogation of parkin translocation and/or abrogation of membrane fusion between autophagosome and lysosomes. While most of the outcomes were LF-specific, only two were shared by OptiMEM exposure (with no serum and reduced glucose levels) albeit at lower extents. Taken together, our findings show that the use of transfection reagents requires critical evaluation with respect to consequences for overall cellular health, particularly in experiments designed to address autophagy-inducing effects and/or energy stress.

Keywords: autophagy; mitophagy; oxidative stress; stress; transfection agent.

MeSH terms

  • AMP-Activated Protein Kinases / metabolism
  • DNA / chemistry*
  • Energy Metabolism*
  • HeLa Cells
  • Humans
  • Lipids / chemistry*
  • Mitochondria / metabolism
  • Mitophagy*
  • Neural Stem Cells / metabolism*
  • Protein Kinases / metabolism
  • RNA, Small Interfering / chemistry*
  • Reactive Oxygen Species / metabolism
  • TOR Serine-Threonine Kinases / metabolism
  • Transfection*
  • Tumor Suppressor Protein p53 / metabolism

Substances

  • Lipids
  • Lipofectamine
  • RNA, Small Interfering
  • Reactive Oxygen Species
  • TP53 protein, human
  • Tumor Suppressor Protein p53
  • DNA
  • Protein Kinases
  • MTOR protein, human
  • PTEN-induced putative kinase
  • TOR Serine-Threonine Kinases
  • AMP-Activated Protein Kinases