Characterization of potent and selective iodonium-class inhibitors of NADPH oxidases

Biochem Pharmacol. 2017 Nov 1:143:25-38. doi: 10.1016/j.bcp.2017.07.007. Epub 2017 Jul 11.

Abstract

The NADPH oxidases (NOXs) play a recognized role in the development and progression of inflammation-associated disorders, as well as cancer. To date, several NOX inhibitors have been developed, through either high throughput screening or targeted disruption of NOX interaction partners, although only a few have reached clinical trials. To improve the efficacy and bioavailability of the iodonium class NOX inhibitor diphenylene iodonium (DPI), we synthesized 36 analogs of DPI, focusing on improved solubility and functionalization. The inhibitory activity of the analogs was interrogated through cell viability and clonogenic studies with a colon cancer cell line (HT-29) that depends on NOX for its proliferative potential. Lack of altered cellular respiration at relevant iodonium analog concentrations was also demonstrated. Additionally, inhibition of ROS generation was evaluated with a luminescence assay for superoxide, or by Amplex Red® assay for H2O2 production, in cell models expressing specific NOX isoforms. DPI and four analogs (NSCs 740104, 751140, 734428, 737392) strongly inhibited HT-29 cell growth and ROS production with nanomolar potency in a concentration-dependent manner. NSC 737392 and 734428, which both feature nitro functional groups at the meta position, had >10-fold higher activity against ROS production by cells that overexpress dual oxidase 2 (DUOX2) than the other compounds examined (IC50≈200-400nM). Based on these results, we synthesized and tested NSC 780521 with optimized potency against DUOX2. Iodonium analogs with anticancer activity, including the first generation of targeted agents with improved specificity against DUOX2, may provide a novel therapeutic approach to NOX-driven tumors.

Keywords: Colon cancer; Diphenylene iodonium; Dual oxidase; FAD (PubChem CID: 643975); NADPH oxidase; Reactive oxygen; di-2-thienyliodonium chloride, DTI (PubChem CID: 162551); diphenylene iodonium, DPI (PubChem CID:3101); diphenyliodonium, IDP (PubChem CID: 12877).

Publication types

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

MeSH terms

  • Cell Proliferation / drug effects*
  • Cell Survival / drug effects
  • Dose-Response Relationship, Drug
  • Dual Oxidases
  • Enzyme Inhibitors / chemical synthesis
  • Enzyme Inhibitors / chemistry
  • Enzyme Inhibitors / pharmacology*
  • HT29 Cells
  • Humans
  • Molecular Structure
  • NADH, NADPH Oxidoreductases / antagonists & inhibitors*
  • NADH, NADPH Oxidoreductases / genetics
  • NADPH Oxidases / antagonists & inhibitors
  • NADPH Oxidases / genetics
  • Onium Compounds / chemical synthesis
  • Onium Compounds / chemistry
  • Onium Compounds / pharmacology*
  • Oxygen Consumption / drug effects
  • Reactive Oxygen Species / antagonists & inhibitors
  • Thiophenes / chemical synthesis
  • Thiophenes / chemistry
  • Thiophenes / pharmacology*

Substances

  • Enzyme Inhibitors
  • Onium Compounds
  • Reactive Oxygen Species
  • Thiophenes
  • iodonium thiophene
  • diphenyleneiodonium
  • Dual Oxidases
  • NADH, NADPH Oxidoreductases
  • NADPH Oxidases
  • DUOX2 protein, human