Chemoproteomic Profiling Reveals Ethacrynic Acid Targets Adenine Nucleotide Translocases to Impair Mitochondrial Function

Mol Pharm. 2018 Jun 4;15(6):2413-2422. doi: 10.1021/acs.molpharmaceut.8b00250. Epub 2018 May 15.

Abstract

Ethacrynic acid (EA) is a diuretic drug that is widely used to treat high-blood pressure and swelling caused by congestive heart failure or kidney failure. It acts through noncovalent inhibition of the Na+-K+-2Cl- cotransporter in the thick ascending limb of Henle's loop. Chemically, EA contains a Michael acceptor group that can react covalently with nucleophilic residues in proteins; however, the proteome reactivity of EA remains unexplored. Herein, we took a quantitative chemoproteomic approach to globally profile EA's targets in cancer cells. We discovered that EA induces impaired mitochondrial function accompanied by increased ROS production. Our profiling revealed that EA targets functional proteins on mitochondrial membranes, including adenine nucleotide translocases (ANTs). Site-specific mapping identified that EA covalently modifies a functional cysteine in ANTs, a mutation of which resulted in the rescuing effect on EA-induced mitochondrial dysfunction. The newly discovered modes of action offer valuable information to repurpose EA for cancer treatment.

Keywords: Michael acceptor; adenine nucleotide translocases; chemical proteomics; cysteine; ethacrynic acid.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Line, Tumor
  • Cysteine / chemistry
  • Drug Repositioning*
  • Drug Screening Assays, Antitumor
  • Ethacrynic Acid / pharmacology*
  • Humans
  • Mitochondria / drug effects*
  • Mitochondria / metabolism
  • Mitochondrial ADP, ATP Translocases / antagonists & inhibitors*
  • Mitochondrial ADP, ATP Translocases / chemistry
  • Mitochondrial ADP, ATP Translocases / metabolism
  • Neoplasms / drug therapy*
  • Neoplasms / pathology
  • Proteome / chemistry
  • Proteome / drug effects
  • Proteomics
  • Reactive Oxygen Species / metabolism

Substances

  • Proteome
  • Reactive Oxygen Species
  • Mitochondrial ADP, ATP Translocases
  • Cysteine
  • Ethacrynic Acid