Human sirtuins are differentially sensitive to inhibition by nitrosating agents and other cysteine oxidants

J Biol Chem. 2020 Jun 19;295(25):8524-8536. doi: 10.1074/jbc.RA119.011988. Epub 2020 May 5.

Abstract

Sirtuins (e.g. human Sirt1-7) catalyze the removal of acyl groups from lysine residues in proteins in an NAD+-dependent manner, and loss of sirtuin deacylase activity correlates with the development of aging-related diseases. Although multiple reports suggest that sirtuin activity is regulated by oxidative post-translational modifications of cysteines during inflammation and aging, no systematic comparative study of potential direct sirtuin cysteine oxidative modifications has been performed. Here, using IC50 and kinact/KI analyses, we quantified the ability of nitrosothiols (S-nitrosoglutathione and S-nitroso-N-acetyl-d,l-penicillamine), nitric oxide, oxidized GSH, and hydrogen peroxide to post-translationally modify and inhibit the deacylase activity of Sirt1, Sirt2, Sirt3, Sirt5, and Sirt6. The inhibition was correlated with cysteine modification and assessed with chemical-probe and blot-based assays for cysteine S-nitrosation, sulfenylation, and glutathionylation. We show that the primarily nuclear sirtuins Sirt1 and Sirt6, as well as the primarily cytosolic sirtuin Sirt2, are modified and inhibited by cysteine S-nitrosation in response to exposure to both free nitric oxide and nitrosothiols (kinact/KI ≥ 5 m-1 s-1), which is the first report of Sirt2 and Sirt6 inhibition by S-nitrosation. Surprisingly, the mitochondrial sirtuins Sirt3 and Sirt5 were resistant to inhibition by cysteine oxidants. Collectively, these results suggest that nitric oxide-derived oxidants may causatively link nuclear and cytosolic sirtuin inhibition to aging-related inflammatory disease development.

Keywords: S-nitrosylation; enzyme inactivation; glutathionylation; hydrogen peroxide; nicotinamide adenine dinucleotide (NAD); nitric oxide; protein acylation; reactive nitrogen species (RNS); redox signaling; sirtuin.

Publication types

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

MeSH terms

  • Cysteine / chemistry
  • Cysteine / metabolism*
  • Glutathione / chemistry
  • Glutathione / metabolism
  • Humans
  • Kinetics
  • Mitochondria / metabolism
  • Nitric Oxide / chemistry
  • Nitric Oxide / metabolism
  • Oxidants / chemistry
  • Oxidants / metabolism*
  • Protein Processing, Post-Translational
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / isolation & purification
  • S-Nitrosoglutathione / chemistry
  • S-Nitrosoglutathione / metabolism
  • Sirtuin 1 / antagonists & inhibitors
  • Sirtuin 1 / genetics
  • Sirtuin 1 / metabolism
  • Sirtuin 2 / antagonists & inhibitors
  • Sirtuin 2 / genetics
  • Sirtuin 2 / metabolism
  • Sirtuins / antagonists & inhibitors
  • Sirtuins / genetics
  • Sirtuins / metabolism*

Substances

  • Oxidants
  • Recombinant Proteins
  • Nitric Oxide
  • S-Nitrosoglutathione
  • SIRT6 protein, human
  • Sirtuin 1
  • Sirtuin 2
  • Sirtuins
  • Glutathione
  • Cysteine