Chemokine receptor CXCR4 oligomerization is disrupted selectively by the antagonist ligand IT1t

J Biol Chem. 2021 Jan-Jun:296:100139. doi: 10.1074/jbc.RA120.016612. Epub 2020 Dec 6.

Abstract

CXCR4, a member of the family of chemokine-activated G protein-coupled receptors, is widely expressed in immune response cells. It is involved in both cancer development and progression as well as viral infection, notably by HIV-1. A variety of methods, including structural information, have suggested that the receptor may exist as a dimer or an oligomer. However, the mechanistic details surrounding receptor oligomerization and its potential dynamic regulation remain unclear. Using both biochemical and biophysical means, we confirm that CXCR4 can exist as a mixture of monomers, dimers, and higher-order oligomers in cell membranes and show that oligomeric structure becomes more complex as receptor expression levels increase. Mutations of CXCR4 residues located at a putative dimerization interface result in monomerization of the receptor. Additionally, binding of the CXCR4 antagonist IT1t-a small drug-like isothiourea derivative-rapidly destabilizes the oligomeric structure, whereas AMD3100, another well-characterized CXCR4 antagonist, does not. Although a mutation that regulates constitutive activity of CXCR4 also results in monomerization of the receptor, binding of IT1t to this variant promotes receptor dimerization. These results provide novel insights into the basal organization of CXCR4 and how antagonist ligands of different chemotypes differentially regulate its oligomerization state.

Keywords: G protein–coupled receptor (GPCR); chemokine; confocal microscopy; dimerization; microscopic imaging; oligomerization; tertiary structure.

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

  • Anti-HIV Agents / pharmacology
  • Benzylamines / pharmacology*
  • Cells, Cultured
  • Cyclams / pharmacology*
  • Green Fluorescent Proteins / metabolism
  • Heterocyclic Compounds / chemistry
  • Heterocyclic Compounds / pharmacology
  • Humans
  • Ligands
  • Protein Binding
  • Protein Conformation / drug effects
  • Protein Multimerization / drug effects
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / chemistry
  • Receptors, CXCR4 / metabolism*
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / isolation & purification
  • Recombinant Fusion Proteins / metabolism
  • Signal Transduction
  • Small Molecule Libraries / pharmacology*
  • Thiourea / pharmacology*

Substances

  • Anti-HIV Agents
  • Benzylamines
  • CXCR4 protein, human
  • Cyclams
  • Heterocyclic Compounds
  • Ligands
  • Receptors, CXCR4
  • Recombinant Fusion Proteins
  • Small Molecule Libraries
  • Green Fluorescent Proteins
  • Thiourea
  • plerixafor