Cu(II) complex that synergistically potentiates cytotoxicity and an antitumor immune response by targeting cellular redox homeostasis

Proc Natl Acad Sci U S A. 2024 Jun 11;121(24):e2404668121. doi: 10.1073/pnas.2404668121. Epub 2024 Jun 4.

Abstract

Developing anticancer drugs with low side effects is an ongoing challenge. Immunogenic cell death (ICD) has received extensive attention as a potential synergistic modality for cancer immunotherapy. However, only a limited set of drugs or treatment modalities can trigger an ICD response and none of them have cytotoxic selectivity. This provides an incentive to explore strategies that might provide more effective ICD inducers free of adverse side effects. Here, we report a metal-based complex (Cu-1) that disrupts cellular redox homeostasis and effectively stimulates an antitumor immune response with high cytotoxic specificity. Upon entering tumor cells, this Cu(II) complex enhances the production of intracellular radical oxidative species while concurrently depleting glutathione (GSH). As the result of heightening cellular oxidative stress, Cu-1 gives rise to a relatively high cytotoxicity to cancer cells, whereas normal cells with low levels of GSH are relatively unaffected. The present Cu(II) complex initiates a potent ferroptosis-dependent ICD response and effectively inhibits in vivo tumor growth in an animal model (c57BL/6 mice challenged with colorectal cancer). This study presents a strategy to develop metal-based drugs that could synergistically potentiate cytotoxic selectivity and promote apoptosis-independent ICD responses through perturbations in redox homeostasis.

Keywords: disrupting redox homeostasis; ferroptosis; immunogenic cell death; metal complex.

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / immunology
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology
  • Coordination Complexes / chemistry
  • Coordination Complexes / pharmacology
  • Copper*
  • Drug Synergism
  • Ferroptosis / drug effects
  • Glutathione* / metabolism
  • Homeostasis*
  • Humans
  • Immunogenic Cell Death / drug effects
  • Mice
  • Mice, Inbred C57BL
  • Oxidation-Reduction*
  • Oxidative Stress / drug effects
  • Reactive Oxygen Species / metabolism

Substances

  • Copper
  • Glutathione
  • Antineoplastic Agents
  • Coordination Complexes
  • Reactive Oxygen Species