Drosophila Sirt2/mammalian SIRT3 deacetylates ATP synthase β and regulates complex V activity

J Cell Biol. 2014 Jul 21;206(2):289-305. doi: 10.1083/jcb.201404118. Epub 2014 Jul 14.

Abstract

Adenosine triphosphate (ATP) synthase β, the catalytic subunit of mitochondrial complex V, synthesizes ATP. We show that ATP synthase β is deacetylated by a human nicotinamide adenine dinucleotide (NAD(+))-dependent protein deacetylase, sirtuin 3, and its Drosophila melanogaster homologue, dSirt2. dsirt2 mutant flies displayed increased acetylation of specific Lys residues in ATP synthase β and decreased complex V activity. Overexpression of dSirt2 increased complex V activity. Substitution of Lys 259 and Lys 480 with Arg in human ATP synthase β, mimicking deacetylation, increased complex V activity, whereas substitution with Gln, mimicking acetylation, decreased activity. Mass spectrometry and proteomic experiments from wild-type and dsirt2 mitochondria identified the Drosophila mitochondrial acetylome and revealed dSirt2 as an important regulator of mitochondrial energy metabolism. Additionally, we unravel a ceramide-NAD(+)-sirtuin axis wherein increased ceramide, a sphingolipid known to induce stress responses, resulted in depletion of NAD(+) and consequent decrease in sirtuin activity. These results provide insight into sirtuin-mediated regulation of complex V and reveal a novel link between ceramide and Drosophila acetylome.

Publication types

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

MeSH terms

  • Acetylation
  • Animals
  • Ceramides / metabolism
  • Ceramides / physiology
  • Drosophila Proteins / genetics
  • Drosophila Proteins / metabolism*
  • Drosophila Proteins / physiology
  • Drosophila melanogaster / genetics
  • Drosophila melanogaster / metabolism*
  • Metabolic Networks and Pathways
  • Mitochondrial Proton-Translocating ATPases / metabolism*
  • Models, Molecular
  • Sirtuin 3
  • Stress, Physiological

Substances

  • Ceramides
  • Drosophila Proteins
  • complex V (mitochondrial oxidative phosphorylation system)
  • Sirtuin 3
  • Mitochondrial Proton-Translocating ATPases