Cardiac glycosides suppress the maintenance of stemness and malignancy via inhibiting HIF-1α in human glioma stem cells

Oncotarget. 2017 Jun 20;8(25):40233-40245. doi: 10.18632/oncotarget.16714.

Abstract

Tissue hypoxia contributes to solid tumor pathogenesis by activating a series of adaptive programs. We previously showed that hypoxia promotes the preferential expansion and maintenance of CD133 positive human glioma stem cells (GSC) in a hypoxia inducible factor 1 alpha (HIF-1α)-dependent mechanism. Here, we examined the activity of digitoxin (DT), a cardiac glycoside and a putative inhibitor of HIF-1α, on human GSC in vitro and in vivo. During hypoxic conditions (1% O2), we observed the effect of DT on the intracellular level of HIF-1α and the extracellular level of vascular endothelial growth factor (VEGF) in human GSC. We found that DT at clinically achievable concentrations, suppressed HIF-1α accumulation during hypoxic conditions in human GSC and established glioma cell lines. DT treatment also significantly attenuated hypoxia-induced expression of VEGF, a downstream target of HIF-1α. Exposure to DT also reduced hypoxia-induced activation of the extracellular signal-regulated kinase 1/2 (ERK1/2) signaling pathway. Furthermore, DT potently inhibited neurosphere formation, and decreased CD133 expression even at concentrations that were not overtly cytotoxic. Lastly, treatment with DT reduced GSC engraftment in an in vivo xenograft model of glioblastoma. Intraperitoneal injections of DT significantly inhibited the growth of established glioblastoma xenografts, and suppressed expression of HIF-1α and carbonic anhydrase (CA9), a surrogate marker of hypoxia. Taken together, these results suggest that DT at clinically achievable concentration functions as an inhibitor of HIF-1α, worthy of further investigations in the therapy of glioblastoma.

Keywords: HIF; cancer stem cell; cardiac glycoside; digitoxin; hypoxia.

MeSH terms

  • AC133 Antigen / metabolism
  • Animals
  • Carbonic Anhydrases / biosynthesis*
  • Digitoxin / pharmacology*
  • Enzyme Activation / drug effects
  • Extracellular Signal-Regulated MAP Kinases / genetics
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Glioblastoma / pathology*
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / antagonists & inhibitors*
  • Hypoxia-Inducible Factor 1, alpha Subunit / biosynthesis*
  • Mice
  • Mice, SCID
  • Neoplastic Stem Cells / pathology*
  • RNA Interference
  • RNA, Small Interfering / genetics
  • Spheroids, Cellular
  • Tumor Cells, Cultured
  • Tumor Hypoxia / physiology
  • Vascular Endothelial Growth Factor A / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • AC133 Antigen
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • PROM1 protein, human
  • RNA, Small Interfering
  • VEGFA protein, human
  • Vascular Endothelial Growth Factor A
  • Digitoxin
  • Extracellular Signal-Regulated MAP Kinases
  • Carbonic Anhydrases