PEG-GO@XN nanocomposite suppresses breast cancer metastasis via inhibition of mitochondrial oxidative phosphorylation and blockade of epithelial-to-mesenchymal transition

Eur J Pharmacol. 2021 Mar 15:895:173866. doi: 10.1016/j.ejphar.2021.173866. Epub 2021 Jan 14.

Abstract

Metastatic breast cancer is a significant contributor to mortality among women, but its complex regulation represents a barrier to precision targeting. In the present study, a graphene-based nanocomposite which probes and selectively inhibits cancer cell motility is described. By controllable coupling of prenylated chalcone xanthohumol, an efficient inhibitor of mitochondrial electron transport chain complex I, with PEGylated graphene oxide nanosheet, a PEG-GO@XN nanocomposite with good stability and biocompatibility is synthesized. PEG-GO@XN is capable of inhibiting mitochondrial oxidative phosphorylation selectively in MDA-MB-231 and MDA-MB-436 metastatic breast cancer cells. PEG-GO@XN reduces the production of ATP, impairs the formation of F-actin cytoskeleton in the lamellipodia, and blocks the migration and invasion of breast cancer cells in vitro, without interfering the proliferation and metabolism of non-cancerous cells. More importantly, PEG-GO@XN suppresses the metastasis of MDA-MB-231 cells to lung in nude mice. PEG-GO@XN abolishes the TGF-β1-induced down-regulation of E-cadherin and up-regulation of N-cadherin, vimentin, Snail and Twist, thus causes the maintenance of "epithelial-like" rather than the "mesenchymal-like" features, and decreases the motility potential of breast cancer cells. Taken together, this research unveils the enormous potential of PEG-GO@XN to suppress metastatic breast cancer by selective targeting oxidative phosphorylation and epithelial-mesenchymal transition of cancer cells and thereby providing insights on metastatic cancer treatment.

Keywords: Breast cancer metastasis; Energy metabolism; Epithelial-mesenchymal transition; Graphene oxide; Mitochondria; Xanthohumol.

MeSH terms

  • Actin Cytoskeleton / drug effects
  • Actin Cytoskeleton / metabolism
  • Actin Cytoskeleton / pathology
  • Adenosine Triphosphate / metabolism
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Breast Neoplasms / drug therapy*
  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Drug Compounding
  • Epithelial-Mesenchymal Transition / drug effects*
  • Female
  • Humans
  • Lung Neoplasms / metabolism
  • Lung Neoplasms / prevention & control*
  • Lung Neoplasms / secondary
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • Nanocomposites*
  • Neoplasm Invasiveness
  • Oxidative Phosphorylation / drug effects*
  • Polyethylene Glycols / pharmacology*
  • Pseudopodia / drug effects
  • Pseudopodia / metabolism
  • Pseudopodia / pathology
  • Signal Transduction
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Polyethylene Glycols
  • Adenosine Triphosphate