Activity-dependent Regulation of Histone Lysine Demethylase KDM1A by a Putative Thiol/Disulfide Switch

J Biol Chem. 2016 Nov 18;291(47):24756-24767. doi: 10.1074/jbc.M116.734426. Epub 2016 Sep 15.

Abstract

Lysine demethylation of proteins such as histones is catalyzed by several classes of enzymes, including the FAD-dependent amine oxidases KDM1A/B. The KDM1 family is homologous to the mitochondrial monoamine oxidases MAO-A/B and produces hydrogen peroxide in the nucleus as a byproduct of demethylation. Here, we show KDM1A is highly thiol-reactive in vitro and in cellular models. Enzyme activity is potently and reversibly inhibited by the drug disulfiram and by hydrogen peroxide. Hydrogen peroxide produced by KDM1A catalysis reduces thiol labeling and inactivates demethylase activity over time. MALDI-TOF mass spectrometry indicates that hydrogen peroxide blocks labeling of cysteine 600, which we propose forms an intramolecular disulfide with cysteine 618 to negatively regulate the catalytic activity of KDM1A. This activity-dependent regulation is unique among histone-modifying enzymes but consistent with redox sensitivity of epigenetic regulators.

Keywords: chemical biology; disulfide; drug screening; enzyme inactivation; flavoprotein; histone demethylase; hydrogen peroxide; reactive oxygen species (ROS); redox regulation; thiol.

MeSH terms

  • Cysteine / chemistry
  • Cysteine / metabolism
  • Disulfides / chemistry
  • Disulfiram / chemistry
  • HeLa Cells
  • Histone Demethylases / chemistry*
  • Histone Demethylases / genetics
  • Histone Demethylases / metabolism
  • Humans
  • Hydrogen Peroxide / chemistry
  • Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization
  • Sulfhydryl Compounds / chemistry

Substances

  • Disulfides
  • Sulfhydryl Compounds
  • Hydrogen Peroxide
  • Histone Demethylases
  • KDM1A protein, human
  • Cysteine
  • Disulfiram

Associated data

  • PDB/2HKO
  • PDB/4GUU
  • PDB/2BXR
  • PDB/2XFU