Human herpesvirus 8-encoded chemokine vCCL2/vMIP-II is an agonist of the atypical chemokine receptor ACKR3/CXCR7

Biochem Pharmacol. 2016 Aug 15:114:14-21. doi: 10.1016/j.bcp.2016.05.012. Epub 2016 May 27.

Abstract

The atypical chemokine receptor CXCR7/ACKR3 binds two endogenous chemokines, CXCL12 and CXCL11, and is upregulated in many cancers or following infection by several cancer-inducing viruses, including HHV-8. ACKR3 is a ligand-scavenging receptor and does not activate the canonical G protein pathways but was proposed to trigger β-arrestin-dependent signaling. Here, we identified the human herpesvirus 8-encoded CC chemokine vCCL2/vMIP-II as a third high-affinity ligand for ACKR3. vCCL2 acted as partial ACKR3 agonist, inducing β-arrestin recruitment to the receptor, subsequent reduction of its surface levels and its delivery to endosomes. In addition, ACKR3 reduced vCCL2-triggered MAP kinase and PI3K/Akt signaling through other chemokine receptors. Our data suggest that ACKR3 acts as a scavenger receptor for vCCL2, regulating its availability and activity toward human receptors, thereby likely controlling its function in HHV-8 infection. Our study provides new insights into the complex crosstalk between viral chemokines and host receptors as well as into the biology of ACKR3, this atypical and still enigmatic receptor.

Keywords: ACKR3; CXCR7; HHV-8; Kaposi’s sarcoma; vCCL2; vMIP-II.

MeSH terms

  • Animals
  • Binding, Competitive
  • CHO Cells
  • Cell Line, Tumor
  • Chemokine CCL2 / genetics
  • Chemokine CCL2 / metabolism*
  • Chemokine CXCL12 / metabolism
  • Chemokines / genetics
  • Chemokines / metabolism*
  • Cricetulus
  • Endosomes / metabolism
  • Flow Cytometry
  • Herpesvirus 8, Human / genetics
  • Herpesvirus 8, Human / immunology
  • Herpesvirus 8, Human / metabolism*
  • Humans
  • Ligands
  • Receptor Cross-Talk
  • Receptors, CXCR / agonists*
  • Receptors, CXCR / genetics
  • Transfection
  • beta-Arrestin 2 / metabolism

Substances

  • ACKR3 protein, human
  • CXCL12 protein, human
  • Chemokine CCL2
  • Chemokine CXCL12
  • Chemokines
  • Ligands
  • Receptors, CXCR
  • beta-Arrestin 2
  • vMIP-II