Blocking HIF signaling via novel inhibitors of CA9 and APE1/Ref-1 dramatically affects pancreatic cancer cell survival

Sci Rep. 2018 Sep 13;8(1):13759. doi: 10.1038/s41598-018-32034-9.

Abstract

Pancreatic ductal adenocarcinoma (PDAC) has reactive stroma that promotes tumor signaling, fibrosis, inflammation, and hypoxia, which activates HIF-1α to increase tumor cell metastasis and therapeutic resistance. Carbonic anhydrase IX (CA9) stabilizes intracellular pH following induction by HIF-1α. Redox effector factor-1 (APE1/Ref-1) is a multifunctional protein with redox signaling activity that converts certain oxidized transcription factors to a reduced state, enabling them to upregulate tumor-promoting genes. Our studies evaluate PDAC hypoxia responses and APE1/Ref-1 redox signaling contributions to HIF-1α-mediated CA9 transcription. Our previous studies implicated this pathway in PDAC cell survival under hypoxia. We expand those studies, comparing drug responses using patient-derived PDAC cells displaying differential hypoxic responses in 3D spheroid tumor-stroma models to characterize second generation APE1/Ref-1 redox signaling and CA9 inhibitors. Our data demonstrates that HIF-1α-mediated CA9 induction differs between patient-derived PDAC cells and that APE1/Ref-1 redox inhibition attenuates this induction by decreasing hypoxia-induced HIF-1 DNA binding. Dual-targeting of APE1/Ref-1 and CA9 in 3D spheroids demonstrated that this combination effectively kills PDAC tumor cells displaying drastically different levels of CA9. New APE1/Ref-1 and CA9 inhibitors were significantly more potent alone and in combination, highlighting the potential of combination therapy targeting the APE1-Ref-1 signaling axis with significant clinical potential.

Publication types

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

MeSH terms

  • Antigens, Neoplasm / genetics*
  • Carbonic Anhydrase IX / antagonists & inhibitors
  • Carbonic Anhydrase IX / genetics*
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival
  • DNA-(Apurinic or Apyrimidinic Site) Lyase / antagonists & inhibitors
  • DNA-(Apurinic or Apyrimidinic Site) Lyase / genetics*
  • Gene Expression Regulation, Neoplastic / genetics
  • Humans
  • Hypoxia-Inducible Factor 1, alpha Subunit / genetics*
  • Pancreatic Neoplasms / drug therapy*
  • Pancreatic Neoplasms / genetics
  • Signal Transduction / drug effects
  • Small Molecule Libraries / pharmacology
  • Transcription, Genetic / drug effects

Substances

  • Antigens, Neoplasm
  • HIF1A protein, human
  • Hypoxia-Inducible Factor 1, alpha Subunit
  • Small Molecule Libraries
  • CA9 protein, human
  • Carbonic Anhydrase IX
  • APEX1 protein, human
  • DNA-(Apurinic or Apyrimidinic Site) Lyase