Bio-molecular Fe(III) and Zn(II) complexes stimulate the interplay between PI3K/AKT1/EGFR inhibition and induce autophagy and apoptosis in epidermal skin cell cancer

J Inorg Biochem. 2025 Jan:262:112720. doi: 10.1016/j.jinorgbio.2024.112720. Epub 2024 Sep 4.

Abstract

This study investigated the effectiveness and safety of a hybrid thiosemicarbazone ligand (HL) and its metal complexes (MnII-L, FeIII-L, NiII-HL, and ZnII-HL) against epidermoid carcinoma (A-431). The results indicated that FeIII-L is the most effective, with a high selectivity index of 8.01 and an IC50 of 17.49 ± 2.12 μM for FeIII-L. The study also revealed that the synthesized complexes effectively inhibited gene expression of the Phosphoinositide 3-kinases (PI3K), alpha serine/threonine-protein kinase (AKT1), epidermal growth factor receptor (EGFR2) axis mechanism (P < 0.0001). Additionally, these complexes trigger a chain of events that include the inhibition of proliferating cell nuclear antigen (PCNA), transforming growth factor β1 (TGF β1), and topoisomerase II, and leading to a decrease in epidermoid cell proliferation. Furthermore, the inhibitory activity also resulted in the upregulation of caspases 3 and 9, indicating the acceleration of apoptotic markers, and the down regulation of miRNA221, suggesting a decrease in epidermoid proliferation. Molecular modeling of FeIII-L revealed that it had the best binding energy -8.02 kcal/mol and interacted with five hydrophobic π-interactions with Val270, Gln79, Leu210, and Trp80 against AKT1. Furthermore, the binding orientation of FeIII-L with Topoisomerase II was found to be the most stable, with a binding energy -8.25 kcal/mol. This stability was attributed to the presence of five hydrophobic π-interactions with His759, Guanin13, Cytosin8, and Ala465, and numerous ionic interactions, which were more favorable than those of doxorubicin and etoposide for new regimens of chemotherapeutic activities against skin cancer.

Keywords: Apoptosis; Autophagy; Epidermoid cell; Phosphoinositide 3-kinases (PI3K); Thiosemicarbazone complexes; Topoisomerase II.

MeSH terms

  • Antineoplastic Agents / chemical synthesis
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology
  • Apoptosis* / drug effects
  • Autophagy* / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Coordination Complexes / chemical synthesis
  • Coordination Complexes / chemistry
  • Coordination Complexes / pharmacology
  • ErbB Receptors* / antagonists & inhibitors
  • ErbB Receptors* / metabolism
  • Ferric Compounds / chemistry
  • Ferric Compounds / pharmacology
  • Humans
  • Iron / chemistry
  • Iron / metabolism
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proto-Oncogene Proteins c-akt* / metabolism
  • Skin Neoplasms / drug therapy
  • Skin Neoplasms / metabolism
  • Skin Neoplasms / pathology
  • Zinc* / chemistry
  • Zinc* / pharmacology

Substances

  • Proto-Oncogene Proteins c-akt
  • ErbB Receptors
  • Zinc
  • EGFR protein, human
  • Coordination Complexes
  • Phosphatidylinositol 3-Kinases
  • AKT1 protein, human
  • Antineoplastic Agents
  • Ferric Compounds
  • Iron