A bleomycin-mimicking manganese-porphyrin-conjugated mitochondria-targeting peptoid for cancer therapy

Bioorg Med Chem. 2025 Jan 1:117:118023. doi: 10.1016/j.bmc.2024.118023. Epub 2024 Nov 24.

Abstract

Bleomycin (BLM) is a natural product with established anticancer activity, attributed to its ability to cleave intracellular DNA. BLM complexes with iron (BLM-Fe3+) exhibit peroxidase-like activity, generate reactive oxygen species (ROS), and cause DNA cleavage. Inspired by the mechanism of BLM, we synthesized a novel conjugate of manganese tetraphenylporphyrin (MnTPP) with a biomimetic peptoid (i.e., oligo-N-substituted glycines); this conjugate harnesses the oxidative capabilities of manganese porphyrins combined with the cell-penetrating ability of a previously reported mitochondria-targeting peptoid (MTP). UV-vis spectroscopy showed the formation of Mn(V)-oxo porphyrin, a potent oxidative species, in the presence of hydrogen peroxide, simulating metallobleomycin reactivity. Biological assays demonstrated that MnTPP-MTP significantly boosted ROS production and induced cytotoxicity toward cancer cells, while sparing normal fibroblasts. Tetramethylrhodamine ethyl ester (TMRE) assay revealed reversible, dose-dependent impairment of the mitochondrial membrane potential by MnTPP-MTP treatment. DNA cleavage assays showed that MnTPP-MTP, specifically in the presence of hydrogen peroxide, could elicit substantial DNA damage, in a similar way to BLM. In vivo studies using liposome-encapsulated MnTPP-MTP (lipo-peptoid) indicated superior tumor suppression, without systemic toxicity, when administered locally. Immunofluorescence staining for Ki67 and TUNEL confirmed reduced cell proliferation and increased apoptosis, respectively, validating the anticancer efficacy of lipo-peptoid. These results suggest that MnTPP-MTP, particularly in a liposomal formulation, is a promising new chemotherapeutic agent with robust oxidative mechanisms, poised for further development and application against diverse cancers.

Keywords: Chemotherapy; Liposomes; Mitochondria; Peptoid; Porphyrin; Reactive oxygen species.

MeSH terms

  • Animals
  • Antineoplastic Agents / chemical synthesis
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects
  • Bleomycin* / chemistry
  • Bleomycin* / pharmacology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Dose-Response Relationship, Drug
  • Drug Screening Assays, Antitumor
  • Humans
  • Manganese* / chemistry
  • Manganese* / pharmacology
  • Membrane Potential, Mitochondrial / drug effects
  • Metalloporphyrins / chemical synthesis
  • Metalloporphyrins / chemistry
  • Metalloporphyrins / pharmacology
  • Mice
  • Mitochondria* / drug effects
  • Mitochondria* / metabolism
  • Molecular Structure
  • Peptoids / chemical synthesis
  • Peptoids / chemistry
  • Peptoids / pharmacology
  • Porphyrins / chemical synthesis
  • Porphyrins / chemistry
  • Porphyrins / pharmacology
  • Reactive Oxygen Species / metabolism

Substances

  • Bleomycin
  • Manganese
  • Peptoids
  • Reactive Oxygen Species
  • Antineoplastic Agents
  • Porphyrins
  • Metalloporphyrins