Cystamine and Disulfiram Inhibit Human Transglutaminase 2 via an Oxidative Mechanism

Biochemistry. 2018 Jun 19;57(24):3359-3363. doi: 10.1021/acs.biochem.8b00204. Epub 2018 Mar 28.

Abstract

The catalytic activity of transglutaminase 2 (TG2), a ubiquitously expressed mammalian enzyme, is regulated by multiple post-translational mechanisms. Because elevated activity of TG2 in the extracellular matrix is associated with organ-specific diseases such as celiac disease and renal fibrosis, there is growing therapeutic interest in inhibitors of this enzyme. Cystamine, a symmetric disulfide compound, is one of the earliest reported TG2 inhibitors. Despite its widespread use as a tool compound to block TG2 activity in vitro and in vivo, its mechanism of action has remained unclear. Here, we demonstrate that cystamine irreversibly inhibits human TG2 ( kinh/ Ki = 1.2 mM-1 min-1) via a mechanism fundamentally distinct from those proposed previously. Through mass spectrometric disulfide mapping and site-directed mutagenesis, we show that cystamine promotes the formation of a physiologically relevant disulfide bond between Cys370 and Cys371 that allosterically abrogates the catalytic activity of human TG2. This discovery led us to evaluate clinically useful thiol → disulfide oxidants for TG2 inhibitory activity. It is demonstrated that disulfiram, a relatively safe oral thiuram disulfide, is a fairly potent TG2 inhibitor ( kinh/ Ki = 8.3 mM-1 min-1) and may therefore provide a practical tool for clinically validating this emerging therapeutic target in intestinal disorders such as celiac disease.

Publication types

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

MeSH terms

  • Biocatalysis
  • Cystamine / chemistry
  • Cystamine / pharmacology*
  • Disulfiram / chemistry
  • Disulfiram / pharmacology*
  • Dose-Response Relationship, Drug
  • GTP-Binding Proteins / antagonists & inhibitors*
  • GTP-Binding Proteins / metabolism
  • Humans
  • Kinetics
  • Molecular Structure
  • Oxidation-Reduction
  • Protein Glutamine gamma Glutamyltransferase 2
  • Structure-Activity Relationship
  • Transglutaminases / antagonists & inhibitors*
  • Transglutaminases / metabolism

Substances

  • Protein Glutamine gamma Glutamyltransferase 2
  • Transglutaminases
  • GTP-Binding Proteins
  • Cystamine
  • Disulfiram