Cation-π interactions as lipid-specific anchors for phosphatidylinositol-specific phospholipase C

J Am Chem Soc. 2013 Apr 17;135(15):5740-50. doi: 10.1021/ja312656v. Epub 2013 Apr 8.

Abstract

Amphitropic proteins, such as the virulence factor phosphatidylinositol-specific phospholipase C (PI-PLC) from Bacillus thuringiensis , often depend on lipid-specific recognition of target membranes. However, the recognition mechanisms for zwitterionic lipids, such as phosphatidylcholine, which is enriched in the outer leaflet of eukaryotic cells, are not well understood. A 500 ns long molecular dynamics simulation of PI-PLC at the surface of a lipid bilayer revealed a strikingly high number of interactions between tyrosines at the interfacial binding site and lipid choline groups with structures characteristic of cation-π interactions. Membrane affinities of PI-PLC tyrosine variants mostly tracked the simulation results, falling into two classes: (i) those with minor losses in affinity, Kd(mutant)/Kd(wild-type) ≤ 5 and (ii) those where the apparent Kd was 50-200 times higher than wild-type. Estimating ΔΔG for these Tyr/PC interactions from the apparent Kd values reveals that the free energy associated with class I is ~1 kcal/mol, comparable to the value predicted by the Wimley-White hydrophobicity scale. In contrast, removal of class II tyrosines has a higher energy cost: ~2.5 kcal/mol toward pure PC vesicles. These higher energies correlate well with the occupancy of the cation-π adducts throughout the MD simulation. Together, these results strongly indicate that PI-PLC interacts with PC headgroups via cation-π interactions with tyrosine residues and suggest that cation-π interactions at the interface may be a mechanism for specific lipid recognition by amphitropic and membrane proteins.

Publication types

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

MeSH terms

  • Bacillus thuringiensis / enzymology
  • Dimyristoylphosphatidylcholine / metabolism
  • Lipid Bilayers / metabolism
  • Molecular Docking Simulation
  • Molecular Dynamics Simulation
  • Mutation
  • Phosphatidylinositols / metabolism*
  • Protein Conformation
  • Substrate Specificity
  • Type C Phospholipases / chemistry
  • Type C Phospholipases / genetics
  • Type C Phospholipases / metabolism*
  • Unilamellar Liposomes / metabolism

Substances

  • Lipid Bilayers
  • Phosphatidylinositols
  • Unilamellar Liposomes
  • Type C Phospholipases
  • Dimyristoylphosphatidylcholine