Anthracyclines suppress pheochromocytoma cell characteristics, including metastasis, through inhibition of the hypoxia signaling pathway

Oncotarget. 2017 Apr 4;8(14):22313-22324. doi: 10.18632/oncotarget.16224.

Abstract

Pheochromocytomas (PHEOs) and paragangliomas (PGLs) are rare, neuroendocrine tumors derived from adrenal or extra-adrenal chromaffin cells, respectively. Metastases are discovered in 3-36% of patients at the time of diagnosis. Currently, only suboptimal treatment options exist. Therefore, new therapeutic compounds targeting metastatic PHEOs/PGLs are urgently needed. Here, we investigated if anthracyclines were able to suppress the progression of metastatic PHEO. We explored their effects on experimental mouse PHEO tumor cells using in vitro and in vivo models, and demonstrated that anthracyclines, particularly idarubicin (IDA), suppressed hypoxia signaling by preventing the binding of hypoxia-inducible factor 1 and 2 (HIF-1 and HIF-2) to the hypoxia response element (HRE) sites on DNA. This resulted in reduced transcriptional activation of HIF target genes, including erythropoietin (EPO), phosphoglycerate kinase 1 (PGK1), endothelin 1 (EDN1), glucose transporter 1 (GLUT1), lactate dehydrogenase A (LDHA), and vascular endothelial growth factor (VEGFA), which consequently inhibited the growth of metastatic PHEO. Additionally, IDA downregulated hypoxia signaling by interfering with the transcriptional activation of HIF1A and HIF2A. Furthermore, our animal model demonstrated the dose-dependent suppressive effect of IDA on metastatic PHEO growth in vivo. Our results indicate that anthracyclines are prospective candidates for inclusion in metastatic PHEO/PGL therapy, especially in patients with gene mutations involved in the hypoxia signaling pathway.

Keywords: anthracyclines; hypoxia-inducible factors; metastatic; paraganglioma; pheochromocytoma.

MeSH terms

  • Adrenal Gland Neoplasms / drug therapy*
  • Adrenal Gland Neoplasms / pathology
  • Animals
  • Antineoplastic Agents / therapeutic use*
  • Basic Helix-Loop-Helix Transcription Factors / metabolism
  • Cell Growth Processes / drug effects
  • Cell Line, Tumor
  • Endothelin-1 / genetics
  • Endothelin-1 / metabolism
  • Erythropoietin / genetics
  • Erythropoietin / metabolism
  • Humans
  • Hypoxia / drug therapy*
  • Hypoxia / pathology
  • Hypoxia-Inducible Factor 1, alpha Subunit / metabolism
  • Idarubicin / therapeutic use*
  • Mice
  • Mice, Nude
  • Neoplasm Metastasis
  • Pheochromocytoma / drug therapy*
  • Pheochromocytoma / pathology
  • Phosphoglycerate Kinase / genetics
  • Phosphoglycerate Kinase / metabolism
  • Protein Binding
  • Signal Transduction / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Basic Helix-Loop-Helix Transcription Factors
  • Endothelin-1
  • Hif1a protein, mouse
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Erythropoietin
  • endothelial PAS domain-containing protein 1
  • Pgk1 protein, mouse
  • Phosphoglycerate Kinase
  • Idarubicin