A fragment integrational approach to GPCR inhibition: Identification of a high affinity small molecule CXCR4 antagonist

Eur J Med Chem. 2022 Mar 5:231:114150. doi: 10.1016/j.ejmech.2022.114150. Epub 2022 Jan 28.

Abstract

Targeting the protein-protein interactions involving CXCR4, a member of chemokine receptor family and G-protein-coupled receptor superfamily, has become an attractive therapeutic strategy for HIV-1 infection, hematopoietic stem cell mobilization, and cancer metastasis. As such, new small molecule CXCR4 antagonists are needed to offer therapeutic alternatives with enhanced clinical outcomes. Here, employing a fragment integrational approach we designed and synthesized a new and potent small molecule CXCR4 antagonist (named as HF51116), as well as a fluorescent (FITC)-labeled HF51116 (FITC-HF51116). HF51116 exhibited very high CXCR4 binding affinity with IC50 of 12 nM in competitive binding with a CXCR4 specific antibody 12G5, which is comparable to the wild type chemokines or synthetic peptides of much larger molecular sizes. Direct binding measurement using FITC-HF51116 further revealed the compound's high CXCR4 affinity. HF51116 strongly antagonized SDF-1α-induced cell migration, calcium mobilization, and CXCR4 internalization. Furthermore, HF51116 inhibited HIV-1 infection via CXCR4, demonstrating its antiviral therapeutic potential. The mechanism of HF51116-CXCR4 interaction was analyzed by site-directed mutagenesis and molecular modeling which suggested that the compound recognizes the minor and major subpockets of CXCR4. Its binding to CXCR4 was found to block G protein-dependent downstream signal pathways as detected by luciferase reporter assays. With its potent bioactivities and asymmetric structure amenable to chemical diversification, HF51116 may serve as a prototype for developing a new class of CXCR4-targeted therapeutics and proof of the concept of similar strategies for studying other GPCRs.

Keywords: Chemokine receptor CXCR4; Drug design; G protein coupled receptor; HIV infection; Protein-protein interaction; Small molecule antagonist.

MeSH terms

  • Binding, Competitive
  • Chemokine CXCL12
  • HIV Infections*
  • Humans
  • Models, Molecular
  • Receptors, CXCR4*
  • Signal Transduction

Substances

  • CXCR4 protein, human
  • Chemokine CXCL12
  • Receptors, CXCR4