Heme-dependent Metabolite Switching Regulates H2S Synthesis in Response to Endoplasmic Reticulum (ER) Stress

J Biol Chem. 2016 Aug 5;291(32):16418-16423. doi: 10.1074/jbc.C116.742213. Epub 2016 Jun 30.

Abstract

Substrate ambiguity and relaxed reaction specificity underlie the diversity of reactions catalyzed by the transsulfuration pathway enzymes, cystathionine β-synthase (CBS) and γ-cystathionase (CSE). These enzymes either commit sulfur metabolism to cysteine synthesis from homocysteine or utilize cysteine and/or homocysteine for synthesis of H2S, a signaling molecule. We demonstrate that a kinetically controlled heme-dependent metabolite switch in CBS regulates these competing reactions where by cystathionine, the product of CBS, inhibits H2S synthesis by the second enzyme, CSE. Under endoplasmic reticulum stress conditions, induction of CSE and up-regulation of the CBS inhibitor, CO, a product of heme oxygenase-1, flip the operating preference of CSE from cystathionine to cysteine, transiently stimulating H2S production. In contrast, genetic deficiency of CBS leads to chronic stimulation of H2S production. This metabolite switch from cystathionine to cysteine and/or homocysteine renders H2S synthesis by CSE responsive to the known modulators of CBS: S-adenosylmethionine, NO, and CO. Used acutely, it regulates H2S synthesis; used chronically, it might contribute to disease pathology.

Keywords: endoplasmic reticulum stress (ER stress); enzyme kinetics; homocysteine; hydrogen sulfide; metabolic regulation.

Publication types

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

MeSH terms

  • Animals
  • Cystathionine beta-Synthase / biosynthesis
  • Cystathionine beta-Synthase / genetics
  • Cystathionine gamma-Lyase / biosynthesis
  • Cystathionine gamma-Lyase / genetics
  • Endoplasmic Reticulum Stress / physiology*
  • Gene Expression Regulation, Enzymologic / physiology
  • HEK293 Cells
  • Heme / genetics
  • Heme / metabolism*
  • Heme Oxygenase-1 / genetics
  • Heme Oxygenase-1 / metabolism
  • Homocysteine / genetics
  • Homocysteine / metabolism
  • Humans
  • Hydrogen Sulfide / metabolism*
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism
  • Mice
  • Mice, Knockout
  • Signal Transduction / physiology
  • Up-Regulation / physiology

Substances

  • Membrane Proteins
  • Homocysteine
  • Heme
  • Heme Oxygenase-1
  • Hmox1 protein, mouse
  • Cystathionine beta-Synthase
  • Cystathionine gamma-Lyase
  • Hydrogen Sulfide