Live-cell lipid biochemistry reveals a role of diacylglycerol side-chain composition for cellular lipid dynamics and protein affinities

Proc Natl Acad Sci U S A. 2020 Apr 7;117(14):7729-7738. doi: 10.1073/pnas.1912684117. Epub 2020 Mar 25.

Abstract

Every cell produces thousands of distinct lipid species, but insight into how lipid chemical diversity contributes to biological signaling is lacking, particularly because of a scarcity of methods for quantitatively studying lipid function in living cells. Using the example of diacylglycerols, prominent second messengers, we here investigate whether lipid chemical diversity can provide a basis for cellular signal specification. We generated photo-caged lipid probes, which allow acute manipulation of distinct diacylglycerol species in the plasma membrane. Combining uncaging experiments with mathematical modeling, we were able to determine binding constants for diacylglycerol-protein interactions, and kinetic parameters for diacylglycerol transbilayer movement and turnover in quantitative live-cell experiments. Strikingly, we find that affinities and kinetics vary by orders of magnitude due to diacylglycerol side-chain composition. These differences are sufficient to explain differential recruitment of diacylglycerol binding proteins and, thus, differing downstream phosphorylation patterns. Our approach represents a generally applicable method for elucidating the biological function of single lipid species on subcellular scales in quantitative live-cell experiments.

Keywords: caged lipid probes; diacylglycerol; mathematical modeling; protein kinase C; signaling lipids.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism
  • Biosensing Techniques
  • Cell Membrane / metabolism
  • Cell Membrane / radiation effects
  • Cell Survival
  • Diglycerides / chemistry*
  • Isoenzymes / metabolism
  • Kinetics
  • Light
  • Lipids / chemistry*
  • Models, Biological
  • Protein Kinase C / metabolism
  • Proteins / metabolism*
  • Signal Transduction

Substances

  • 1,2-diacylglycerol
  • Diglycerides
  • Isoenzymes
  • Lipids
  • Proteins
  • Adenosine Triphosphate
  • Protein Kinase C