Nano-targeted induction of dual ferroptotic mechanisms eradicates high-risk neuroblastoma

J Clin Invest. 2018 Aug 1;128(8):3341-3355. doi: 10.1172/JCI99032. Epub 2018 Jun 25.

Abstract

High-risk neuroblastoma is a devastating malignancy with very limited therapeutic options. Here, we identify withaferin A (WA) as a natural ferroptosis-inducing agent in neuroblastoma, which acts through a novel double-edged mechanism. WA dose-dependently either activates the nuclear factor-like 2 pathway through targeting of Kelch-like ECH-associated protein 1 (noncanonical ferroptosis induction) or inactivates glutathione peroxidase 4 (canonical ferroptosis induction). Noncanonical ferroptosis induction is characterized by an increase in intracellular labile Fe(II) upon excessive activation of heme oxygenase-1, which is sufficient to induce ferroptosis. This double-edged mechanism might explain the superior efficacy of WA as compared with etoposide or cisplatin in killing a heterogeneous panel of high-risk neuroblastoma cells, and in suppressing the growth and relapse rate of neuroblastoma xenografts. Nano-targeting of WA allows systemic application and suppressed tumor growth due to an enhanced accumulation at the tumor site. Collectively, our data propose a novel therapeutic strategy to efficiently kill cancer cells by ferroptosis.

Keywords: Drug therapy; Nanotechnology; Neurological disorders; Neuroscience; Oncology.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Apoptosis / drug effects*
  • Cell Line, Tumor
  • Chick Embryo
  • Heme Oxygenase-1 / metabolism
  • Humans
  • Kelch-Like ECH-Associated Protein 1 / metabolism
  • Mice
  • Neoplasm Proteins / metabolism
  • Neuroblastoma / drug therapy*
  • Neuroblastoma / metabolism
  • Neuroblastoma / pathology
  • Withanolides / pharmacology*
  • Xenograft Model Antitumor Assays

Substances

  • Kelch-Like ECH-Associated Protein 1
  • Neoplasm Proteins
  • Withanolides
  • HMOX1 protein, human
  • Heme Oxygenase-1
  • withaferin A