Formononetin Defeats Multidrug-Resistant Cancers by Induction of Oxidative Stress and Suppression of P-Glycoprotein

Int J Mol Sci. 2024 Aug 2;25(15):8471. doi: 10.3390/ijms25158471.

Abstract

Multidrug resistance (MDR) remains the most difficult problem facing conventional chemotherapy for cancers. Astragalus membranaceus is a historically traditional Chinese medicine. One of its bioactive components, formononetin, exhibits antitumor effects on various cancers. However, the effects of formononetin on MDR cancers have not been evaluated. Therefore, we investigated the defense's effects of formononetin on MDR. We used rhodamine 123 and doxorubicin efflux assays to analyze the inhibition kinetics of P-glycoprotein (P-gp) mediated-efflux. Cell viability was detected by sulforhodamine B assay, and the synergistic effects of formononetin combined with chemotherapeutic agents were further calculated using CompuSyn software. Molecular docking was performed with iGEMDOCK. We discovered that formononetin considerably induced oxidative stress and the disruption of mitochondrial membrane potential in MDR cancer cells. Furthermore, formononetin inhibits the P-gp efflux function by ATPase stimulation and the uncompetitive inhibition of P-gp-mediated effluxes of rhodamine 123 and doxorubicin. The molecular docking model indicates that formononetin may bind to P-gp by strong hydrogen bonds at Arginine (Arg) 489 and Glutamine (Gln) 912. Formononetin exhibits significant synergistic effects with vincristine and doxorubicin toward MDR cancer cells, and it synergistically suppressed tumor growth in vivo with paclitaxel. These results suggest that formononetin should be seen as a potential candidate for the adjuvant therapy of MDR cancers.

Keywords: P-glycoprotein; formononetin; multidrug resistance cancer; oxidative stress.

MeSH terms

  • ATP Binding Cassette Transporter, Subfamily B, Member 1 / metabolism
  • Animals
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Doxorubicin* / pharmacology
  • Drug Resistance, Multiple* / drug effects
  • Drug Resistance, Neoplasm* / drug effects
  • Drug Synergism
  • Humans
  • Isoflavones* / chemistry
  • Isoflavones* / pharmacology
  • Membrane Potential, Mitochondrial / drug effects
  • Mice
  • Molecular Docking Simulation*
  • Neoplasms / drug therapy
  • Neoplasms / metabolism
  • Neoplasms / pathology
  • Oxidative Stress* / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • formononetin
  • Isoflavones
  • Doxorubicin
  • ATP Binding Cassette Transporter, Subfamily B, Member 1