Metabolic regulation of transcription through compartmentalized NAD+ biosynthesis

Science. 2018 May 11;360(6389):eaan5780. doi: 10.1126/science.aan5780.

Abstract

NAD+ (nicotinamide adenine dinucleotide in its oxidized state) is an essential molecule for a variety of physiological processes. It is synthesized in distinct subcellular compartments by three different synthases (NMNAT-1, -2, and -3). We found that compartmentalized NAD+ synthesis by NMNATs integrates glucose metabolism and adipogenic transcription during adipocyte differentiation. Adipogenic signaling rapidly induces cytoplasmic NMNAT-2, which competes with nuclear NMNAT-1 for the common substrate, nicotinamide mononucleotide, leading to a precipitous reduction in nuclear NAD+ levels. This inhibits the catalytic activity of poly[adenosine diphosphate (ADP)-ribose] polymerase-1 (PARP-1), a NAD+-dependent enzyme that represses adipogenic transcription by ADP-ribosylating the adipogenic transcription factor C/EBPβ. Reversal of PARP-1-mediated repression by NMNAT-2-mediated nuclear NAD+ depletion in response to adipogenic signals drives adipogenesis. Thus, compartmentalized NAD+ synthesis functions as an integrator of cellular metabolism and signal-dependent transcriptional programs.

Publication types

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

MeSH terms

  • Adipocytes / cytology*
  • Adipocytes / metabolism
  • Adipogenesis / genetics*
  • Animals
  • CCAAT-Enhancer-Binding Protein-beta
  • Cell Line, Tumor
  • Cell Nucleus / metabolism
  • Cytoplasm / metabolism
  • Glucose / metabolism
  • Humans
  • Mice
  • NAD / biosynthesis*
  • NAD / genetics
  • NIH 3T3 Cells
  • Nicotinamide-Nucleotide Adenylyltransferase / metabolism*
  • Poly (ADP-Ribose) Polymerase-1 / metabolism
  • Substrate Specificity
  • Transcription, Genetic*

Substances

  • CCAAT-Enhancer-Binding Protein-beta
  • NAD
  • PARP1 protein, human
  • Poly (ADP-Ribose) Polymerase-1
  • NMNAT1 protein, human
  • NMNAT2 protein, human
  • NMNAT3 protein, human
  • Nicotinamide-Nucleotide Adenylyltransferase
  • Glucose