Self-assembly of a ruthenium-based cGAS-STING photoactivator for carrier-free cancer immunotherapy

Eur J Med Chem. 2024 Sep 5:275:116638. doi: 10.1016/j.ejmech.2024.116638. Epub 2024 Jun 28.

Abstract

The cGAS (cyclic GMP-AMP synthase)-STING (stimulator of interferon genes) pathway promotes antitumor immune responses by sensing cytosolic DNA fragments leaked from nucleus and mitochondria. Herein, we designed a highly charged ruthenium photosensitizer (Ru1) with a β-carboline alkaloid derivative as the ligand for photo-activating of the cGAS-STING pathway. Due to the formation of multiple non-covalent intermolecular interactions, Ru1 can self-assemble into carrier-free nanoparticles (NPs). By incorporating the triphenylphosphine substituents, Ru1 can target and photo-damage mitochondrial DNA (mtDNA) to cause the cytoplasmic DNA leakage to activate the cGAS-STING pathway. Finally, Ru1 NPs show potent antitumor effects and elicit intense immune responses in vivo. In conclusion, we report the first self-assembling mtDNA-targeted photosensitizer, which can effectively activate the cGAS-STING pathway, thus providing innovations for the design of new photo-immunotherapeutic agents.

Keywords: DNA binding; Photoimmunotherapy; Ru(II) complexes; Self-assembly; cGAS-STING.

MeSH terms

  • Animals
  • Antineoplastic Agents* / chemical synthesis
  • Antineoplastic Agents* / chemistry
  • Antineoplastic Agents* / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • DNA, Mitochondrial / metabolism
  • Dose-Response Relationship, Drug
  • Drug Screening Assays, Antitumor
  • Humans
  • Immunotherapy*
  • Membrane Proteins* / metabolism
  • Mice
  • Molecular Structure
  • Nanoparticles / chemistry
  • Neoplasms / drug therapy
  • Neoplasms / pathology
  • Nucleotidyltransferases* / metabolism
  • Photosensitizing Agents* / chemical synthesis
  • Photosensitizing Agents* / chemistry
  • Photosensitizing Agents* / pharmacology
  • Ruthenium* / chemistry
  • Ruthenium* / pharmacology
  • Structure-Activity Relationship

Substances

  • Photosensitizing Agents
  • Nucleotidyltransferases
  • Membrane Proteins
  • Ruthenium
  • cGAS protein, human
  • Antineoplastic Agents
  • STING1 protein, human
  • DNA, Mitochondrial