Characterization, Dynamics, and Mechanism of CXCR4 Antagonists on a Constitutively Active Mutant

Cell Chem Biol. 2019 May 16;26(5):662-673.e7. doi: 10.1016/j.chembiol.2019.01.012. Epub 2019 Feb 28.

Abstract

The G protein-coupled receptor (GPCR) CXCR4 is a co-receptor for HIV and is involved in cancers and autoimmune diseases. We characterized five purine or quinazoline core polyamine pharmacophores used for targeting CXCR4 dysregulation in diseases. All were neutral antagonists for wild-type CXCR4 and two were biased antagonists with effects on β-arrestin-2 only at high concentrations. These compounds displayed various activities for a constitutively active mutant (CAM). We use the IT1t-CXCR4 crystal structure and molecular dynamics (MD) simulations to develop two hypotheses for the activation of the N1193.35A CAM. The N1193.35A mutation facilitates increased coupling of TM helices III and VI. IT1t deactivates the CAM by disrupting the coupling between TM helices III and VI, mediated primarily by residue F872.53. Mutants of F872.53 in N1193.35A CXCR4 precluded constitutive signaling and prevented inverse agonism. This work characterizes CXCR4 ligands and provides a mechanism for N1193.35A constitutive activation.

Keywords: CXCL12; CXCR4; G protein-coupled receptor (GPCR); constitutively active mutant (CAM); molecular dynamics (MD); small molecule ligands.

Publication types

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

MeSH terms

  • Benzylamines
  • Chemokine CXCL12 / pharmacology
  • Cyclams
  • HEK293 Cells
  • HIV Infections / metabolism
  • HIV Infections / pathology
  • HIV Infections / virology
  • HIV-1 / drug effects
  • Heterocyclic Compounds / pharmacology
  • Humans
  • Hydrophobic and Hydrophilic Interactions
  • Ligands
  • Molecular Dynamics Simulation*
  • Mutagenesis, Site-Directed
  • Protein Conformation, alpha-Helical
  • Protein Structure, Tertiary
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / genetics
  • Receptors, CXCR4 / metabolism
  • Signal Transduction / drug effects
  • Small Molecule Libraries / chemistry
  • Small Molecule Libraries / metabolism*
  • Small Molecule Libraries / pharmacology
  • beta-Arrestin 2 / metabolism

Substances

  • Benzylamines
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Cyclams
  • Heterocyclic Compounds
  • Ligands
  • Receptors, CXCR4
  • Small Molecule Libraries
  • beta-Arrestin 2
  • plerixafor