Effects of Ferroportin-Mediated Iron Depletion in Cells Representative of Different Histological Subtypes of Prostate Cancer

Antioxid Redox Signal. 2019 Mar 10;30(8):1043-1061. doi: 10.1089/ars.2017.7023. Epub 2017 Dec 11.

Abstract

Aims: Ferroportin (FPN) is an iron exporter that plays an important role in cellular and systemic iron metabolism. Our previous work has demonstrated that FPN is decreased in prostate tumors. We sought to identify the molecular pathways regulated by FPN in prostate cancer cells.

Results: We show that overexpression of FPN induces profound effects in cells representative of multiple histological subtypes of prostate cancer by activating different but converging pathways. Induction of FPN induces autophagy and activates the transcription factors tumor protein 53 (p53) and Kruppel-like factor 6 (KLF6) and their common downstream target, cyclin-dependent kinase inhibitor 1A (p21). FPN also induces cell cycle arrest and stress-induced DNA-damage genes. Effects of FPN are attributable to its effects on intracellular iron and can be reproduced with iron chelators. Importantly, expression of FPN not only inhibits proliferation of all prostate cancer cells studied but also reduces growth of tumors derived from castrate-resistant adenocarcinoma C4-2 cells in vivo.

Innovation: We use a novel model of FPN expression to interrogate molecular pathways triggered by iron depletion in prostate cancer cells. Since prostate cancer encompasses different subtypes with a highly variable clinical course, we further explore how histopathological subtype influences the response to iron depletion. We demonstrate that prostate cancer cells that derive from different histopathological subtypes activate converging pathways in response to FPN-mediated iron depletion. Activation of these pathways is sufficient to significantly reduce the growth of treatment-refractory C4-2 prostate tumors in vivo.

Conclusions: Our results may explain why FPN is dramatically suppressed in cancer cells, and they suggest that FPN agonists may be beneficial in the treatment of prostate cancer.

Keywords: autophagy; cell cycle; chelator; ferroportin; iron; prostate cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Autophagy
  • Cation Transport Proteins / genetics*
  • Cation Transport Proteins / metabolism
  • Cell Cycle Checkpoints
  • Cell Line, Tumor
  • Cell Proliferation
  • Gene Expression Regulation, Neoplastic
  • Genetic Vectors / administration & dosage*
  • Humans
  • Iron / metabolism
  • Iron Deficiencies*
  • Lentivirus / genetics
  • Male
  • Mice
  • PC-3 Cells
  • Prostatic Neoplasms / genetics
  • Prostatic Neoplasms / metabolism
  • Prostatic Neoplasms / pathology*
  • Signal Transduction
  • Up-Regulation*
  • Xenograft Model Antitumor Assays

Substances

  • Cation Transport Proteins
  • metal transporting protein 1
  • Iron