The Ligand Binding Landscape of Diacylglycerol Kinases

Cell Chem Biol. 2017 Jul 20;24(7):870-880.e5. doi: 10.1016/j.chembiol.2017.06.007. Epub 2017 Jul 14.

Abstract

Diacylglycerol kinases (DGKs) are integral components of signal transduction cascades that regulate cell biology through ATP-dependent phosphorylation of the lipid messenger diacylglycerol. Methods for direct evaluation of DGK activity in native biological systems are lacking and needed to study isoform-specific functions of these multidomain lipid kinases. Here, we utilize ATP acyl phosphate activity-based probes and quantitative mass spectrometry to define, for the first time, ATP and small-molecule binding motifs of representative members from all five DGK subtypes. We use chemical proteomics to discover an unusual binding mode for the DGKα inhibitor, ritanserin, including interactions at the atypical C1 domain distinct from the ATP binding region. Unexpectedly, deconstruction of ritanserin yielded a fragment compound that blocks DGKα activity through a conserved binding mode and enhanced selectivity against the kinome. Collectively, our studies illustrate the power of chemical proteomics to profile protein-small molecule interactions of lipid kinases for fragment-based lead discovery.

Keywords: activity-based protein profiling; cancer immunotherapy; chemical proteomics; diacylglycerol kinase; diacylglycerol signaling; fragment-based drug discovery; ligand deconstruction; lipid kinase inhibitors; lipid phosphorylation; phosphatidic acid signaling.

MeSH terms

  • Adenosine Triphosphate / chemistry
  • Adenosine Triphosphate / metabolism
  • Binding Sites
  • Chromatography, High Pressure Liquid
  • Diacylglycerol Kinase / chemistry
  • Diacylglycerol Kinase / genetics
  • Diacylglycerol Kinase / metabolism*
  • HEK293 Cells
  • Humans
  • Isotope Labeling
  • Ketanserin / chemistry
  • Ketanserin / metabolism
  • Ligands*
  • Peptides / analysis
  • Protein Binding
  • Protein Isoforms / chemistry
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Proteome / analysis
  • Recombinant Proteins / biosynthesis
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / isolation & purification
  • Ritanserin / chemistry
  • Ritanserin / metabolism
  • Tandem Mass Spectrometry

Substances

  • Ligands
  • Peptides
  • Protein Isoforms
  • Proteome
  • Recombinant Proteins
  • Ritanserin
  • Adenosine Triphosphate
  • Ketanserin
  • Diacylglycerol Kinase