Inhibition of Copper Transport Induces Apoptosis in Triple-Negative Breast Cancer Cells and Suppresses Tumor Angiogenesis

Mol Cancer Ther. 2019 May;18(5):873-885. doi: 10.1158/1535-7163.MCT-18-0667. Epub 2019 Mar 1.

Abstract

Treatment of advanced breast cancer remains challenging. Copper and some of the copper-dependent proteins are emerging therapeutic targets because they are essential for cell proliferation and survival, and have been shown to stimulate angiogenesis and metastasis. Here, we show that DCAC50, a recently developed small-molecule inhibitor of the intracellular copper chaperones, ATOX1 and CCS, reduces cell proliferation and elevates oxidative stress, triggering apoptosis in a panel of triple-negative breast cancer (TNBC) cells. Inhibition of ATOX1 activity with DCAC50 disrupts copper homeostasis, leading to increased copper levels, altered spatial copper redistribution, and accumulation of ATP7B to the cellular perinuclear region. The extent and impact of this disruption to copper homeostasis vary across cell lines and correlate with cellular baseline copper and glutathione levels. Ultimately, treatment with DCAC50 attenuates tumor growth and suppresses angiogenesis in a xenograft mouse model, and prevents endothelial cell network formation in vitro Co-treatment with paclitaxel and DCAC50 enhances cytotoxicity in TNBC and results in favorable dose reduction of both drugs. These data demonstrate that inhibition of intracellular copper transport targets tumor cells and the tumor microenvironment, and is a promising approach to treat breast cancer.

Publication types

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

MeSH terms

  • Animals
  • Apoptosis / drug effects
  • Benzothiazoles / pharmacology*
  • Benzothiazoles / therapeutic use
  • Bromobenzenes / pharmacology*
  • Bromobenzenes / therapeutic use
  • Cell Line, Tumor
  • Cell Movement / drug effects
  • Cell Proliferation / drug effects
  • Copper / metabolism
  • Copper Transport Proteins / genetics*
  • Copper-Transporting ATPases / genetics*
  • Female
  • Fluorobenzenes / pharmacology*
  • Fluorobenzenes / therapeutic use
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Mice
  • Molecular Chaperones / genetics*
  • Molybdenum / pharmacology*
  • Neovascularization, Pathologic / drug therapy*
  • Neovascularization, Pathologic / genetics
  • Neovascularization, Pathologic / pathology
  • Oxidative Stress / drug effects
  • Paclitaxel / pharmacology
  • Small Molecule Libraries / pharmacology
  • Triple Negative Breast Neoplasms / drug therapy*
  • Triple Negative Breast Neoplasms / genetics
  • Triple Negative Breast Neoplasms / pathology
  • Tumor Microenvironment / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • ATOX1 protein, human
  • Benzothiazoles
  • Bromobenzenes
  • CCS protein, human
  • Copper Transport Proteins
  • DCAC50
  • Fluorobenzenes
  • Molecular Chaperones
  • Small Molecule Libraries
  • Copper
  • Molybdenum
  • tetrathiomolybdate
  • Copper-Transporting ATPases
  • Paclitaxel