ROS-Responsive and Self-Catalytic Nanocarriers for a Combination of Chemotherapy and Reinforced Ferroptosis against Breast Cancer

ACS Biomater Sci Eng. 2024 Oct 14;10(10):6352-6362. doi: 10.1021/acsbiomaterials.4c01233. Epub 2024 Sep 12.

Abstract

Ferroptosis is an appealing cancer therapy strategy based on the H2O2-involved Fenton reaction to produce toxic OH for lipid peroxidation. However, intracellular H2O2 is easily consumed and results in a deficient Fenton reaction. This obstacle can be overcome by traditional chemotherapeutic drugs for H2O2 supplements. Moreover, a recent work illustrated that dihydroartemisinin (DHA) could promote ferroptosis against tumoral cells, particularly in the presence of ferrous compounds. To achieve combined chemotherapy and ferroptosis, a nanocarrier (TKNPDHA-Fc) was constructed by using thioketal (TK)-bridged paclitaxel prodrug (PEG-TK-PTX) and ferrocene (Fc)-conjugated PEG-Fc, where DHA was encapsulated by a hydrophobic-hydrophobic interaction. Upon cellular uptake, TKNPDHA-Fc could facilitate PTX release through TK breakage under an excess H2O2 microenvironment. Owing to the loss of the hydrophobic PTX component, TKNPDHA-Fc underwent a rapid dissociation for improving DHA to act as a ferroptotic inducer along with Fe supplied from Fc. Moreover, both the chemotherapy-induced reactive oxygen species and the OH produced from reinforced ferroptosis further stimulated the TK cleavage. The "self-catalytic" loop of TKNPDHA-Fc remarkably improved the antitumor performance in vivo via combined mechanisms, and its tumor inhibition rate reached 78.3%. This work highlights the contribution of ROS-responsive and self-catalytic nanoplatforms for enhancing the potential of combined chemotherapy and ferroptosis for cancer therapy in the future.

Keywords: Fenton reaction; ROS-responsive; cancer therapy; ferroptosis; nanoparticle; self-catalytic.

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Antineoplastic Agents / therapeutic use
  • Artemisinins / chemistry
  • Artemisinins / pharmacology
  • Artemisinins / therapeutic use
  • Breast Neoplasms* / drug therapy
  • Breast Neoplasms* / pathology
  • Catalysis
  • Cell Line, Tumor
  • Drug Carriers* / chemistry
  • Female
  • Ferroptosis* / drug effects
  • Ferrous Compounds* / chemistry
  • Ferrous Compounds* / pharmacology
  • Humans
  • Hydrogen Peroxide / chemistry
  • Hydrogen Peroxide / pharmacology
  • Metallocenes / chemistry
  • Mice
  • Mice, Inbred BALB C
  • Mice, Nude
  • Nanoparticles / chemistry
  • Nanoparticles / therapeutic use
  • Paclitaxel* / chemistry
  • Paclitaxel* / pharmacology
  • Paclitaxel* / therapeutic use
  • Polyethylene Glycols / chemistry
  • Polyethylene Glycols / pharmacology
  • Prodrugs / chemistry
  • Prodrugs / pharmacology
  • Prodrugs / therapeutic use
  • Reactive Oxygen Species* / metabolism

Substances

  • Reactive Oxygen Species
  • Paclitaxel
  • Drug Carriers
  • Ferrous Compounds
  • Metallocenes
  • ferrocene
  • artenimol
  • Artemisinins
  • Antineoplastic Agents
  • Prodrugs
  • Hydrogen Peroxide
  • Polyethylene Glycols