Biophysical and computational studies of membrane penetration by the GRP1 pleckstrin homology domain

Structure. 2011 Sep 7;19(9):1338-46. doi: 10.1016/j.str.2011.04.010.

Abstract

The pleckstrin homology (PH) domain of the general receptor for phosphoinositides 1 (GRP1) exhibits specific, high-affinity, reversible binding to phosphatidylinositol (3,4,5)-trisphosphate (PI(3,4,5)P(3)) at the plasma membrane, but the nature and extent of the interaction between this bound complex and the surrounding membrane environment remains unclear. Combining equilibrium and nonequilibrium molecular dynamics (MD) simulations, NMR spectroscopy, and monolayer penetration experiments, we characterize the membrane-associated state of GRP1-PH. MD simulations show loops flanking the binding site supplement the interaction with PI(3,4,5)P(3) through multiple contacts with the lipid bilayer. NMR data show large perturbations in chemical shift for these loop regions on binding to PI(3,4,5)P(3)-containing DPC micelles. Monolayer penetration experiments and further MD simulations demonstrate that mutating hydrophobic residues to polar residues in the flanking loops reduces membrane penetration. This supports a "dual-recognition" model of binding, with specific GRP1-PH-PI(3,4,5)P(3) interactions supplemented by interactions of loop regions with the lipid bilayer.

Publication types

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

MeSH terms

  • Humans
  • Hydrogen Bonding
  • Hydrophobic and Hydrophilic Interactions
  • Membrane Proteins / chemistry*
  • Membranes, Artificial
  • Molecular Dynamics Simulation*
  • Mutagenesis, Site-Directed
  • Mutation, Missense
  • Phosphatidylinositol Phosphates / chemistry
  • Phospholipids / chemistry*
  • Protein Binding
  • Protein Structure, Tertiary
  • Receptors, Cytoplasmic and Nuclear / chemistry*
  • Receptors, Cytoplasmic and Nuclear / genetics
  • Structural Homology, Protein

Substances

  • Membrane Proteins
  • Membranes, Artificial
  • Phosphatidylinositol Phosphates
  • Phospholipids
  • Receptors, Cytoplasmic and Nuclear
  • phosphatidylinositol 3,4,5-triphosphate
  • phosphatidylinositol receptors