A novel ruthenium complex with xanthoxylin induces S-phase arrest and causes ERK1/2-mediated apoptosis in HepG2 cells through a p53-independent pathway

Cell Death Dis. 2018 Jan 23;9(2):79. doi: 10.1038/s41419-017-0104-6.

Abstract

Ruthenium-based compounds have gained great interest due to their potent cytotoxicity in cancer cells; however, much of their potential applications remain unexplored. In this paper, we report the synthesis of a novel ruthenium complex with xanthoxylin (RCX) and the investigation of its cellular and molecular action in human hepatocellular carcinoma HepG2 cells. We found that RCX exhibited a potent cytotoxic effect in a panel of cancer cell lines in monolayer cultures and in a 3D model of multicellular cancer spheroids formed from HepG2 cells. This compound is detected at a high concentration in the cell nuclei, induces DNA intercalation and inhibits DNA synthesis, arresting the cell cycle in the S-phase, which is followed by the activation of the caspase-mediated apoptosis pathway in HepG2 cells. Gene expression analysis revealed changes in the expression of genes related to cell cycle control, apoptosis and the MAPK pathway. In addition, RCX induced the phosphorylation of ERK1/2, and pretreatment with U-0126, an MEK inhibitor known to inhibit the activation of ERK1/2, prevented RCX-induced apoptosis. In contrast, pretreatment with a p53 inhibitor (cyclic pifithrin-α) did not prevent RCX-induced apoptosis, indicating the activation of a p53-independent apoptosis pathway. RCX also presented a potent in vivo antitumor effect in C.B-17 SCID mice engrafted with HepG2 cells. Altogether, these results indicate that RCX is a novel anticancer drug candidate.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acetophenones / chemical synthesis
  • Acetophenones / chemistry
  • Acetophenones / pharmacology*
  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Caspase Inhibitors / pharmacology
  • Caspases / metabolism
  • Cell Cycle Checkpoints / drug effects*
  • DNA / biosynthesis
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • Hep G2 Cells
  • Humans
  • Intercalating Agents / pharmacology
  • MAP Kinase Signaling System / drug effects*
  • Membrane Potential, Mitochondrial / drug effects
  • Mice, SCID
  • Models, Biological
  • Protein Kinase Inhibitors / pharmacology
  • Proton Magnetic Resonance Spectroscopy
  • Ruthenium / pharmacology*
  • S Phase / drug effects*
  • Spheroids, Cellular / drug effects
  • Spheroids, Cellular / metabolism
  • Spheroids, Cellular / pathology
  • Tumor Suppressor Protein p53 / metabolism*
  • Xenograft Model Antitumor Assays

Substances

  • Acetophenones
  • Antineoplastic Agents
  • Caspase Inhibitors
  • Intercalating Agents
  • Protein Kinase Inhibitors
  • Tumor Suppressor Protein p53
  • Ruthenium
  • DNA
  • Caspases
  • xanthoxyline