A Cyclometalated Ruthenium(II) Complex Induces Oncosis for Synergistic Activation of Innate and Adaptive Immunity

Angew Chem Int Ed Engl. 2024 Jul 29;63(31):e202405679. doi: 10.1002/anie.202405679. Epub 2024 Jun 30.

Abstract

An optimal cancer chemotherapy regimen should effectively address the drug resistance of tumors while eliciting antitumor-immune responses. Research has shown that non-apoptotic cell death, such as pyroptosis and ferroptosis, can enhance the immune response. Despite this, there has been limited investigation and reporting on the mechanisms of oncosis and its correlation with immune response. Herein, we designed and synthesized a Ru(II) complex that targeted the nucleus and mitochondria to induce cell oncosis. Briefly, the Ru(II) complex disrupts the nucleus and mitochondria DNA, which active polyADP-ribose polymerase 1, accompanied by ATP consumption and porimin activation. Concurrently, mitochondrial damage and endoplasmic reticulum stress result in the release of Ca2+ ions and increased expression of Calpain 1. Subsequently, specific pore proteins porimin and Calpain 1 promote cristae destruction or vacuolation, ultimately leading to cell membrane rupture. The analysis of RNA sequencing demonstrates that the Ru(II) complex can initiate the oncosis-associated pathway and activate both innate and adaptive immunity. In vivo experiments have confirmed that oncosis promotes dendritic cell maturation and awakens adaptive cytotoxic T lymphocytes but also activates the innate immune by inducing the polarization of macrophages towards an M1 phenotype.

Keywords: DNA Damage; Innate and Adaptive Immunity; Medicinal Inorganic Chemistry; Oncosis; Ruthenium.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptive Immunity* / drug effects
  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Cell Line, Tumor
  • Coordination Complexes* / chemistry
  • Coordination Complexes* / pharmacology
  • Humans
  • Immunity, Innate* / drug effects
  • Mice
  • Ruthenium* / chemistry
  • Ruthenium* / pharmacology

Substances

  • Ruthenium
  • Coordination Complexes
  • Antineoplastic Agents