Phosphorylation by a G protein-coupled kinase inhibits signaling and promotes internalization of the monocyte chemoattractant protein-1 receptor. Critical role of carboxyl-tail serines/threonines in receptor function

J Immunol. 1996 Dec 15;157(12):5606-12.

Abstract

Monocyte chemoattractant protein-1 (MCP-1) is a member of the chemokine family of chemotactic cytokines and signals via activation of a G protein-coupled seven-transmembrane domain receptor to mediate chemotaxis. Monocyte activation is limited by desensitization and internalization of the MCP-1R, but these mechanisms are not well understood. In this study, we show that the type B MCP-1R (MCP-1RB/CCR2B) is rapidly phosphorylated and internalized in response to nanomolar concentrations of MCP-1. Co-expression of CCR2B in Xenopus oocytes with beta-adrenergic receptor kinase 2 (beta ark2), but not beta ark1 or rhodopsin kinase, specifically blocked receptor activation by MCP-1. Mutation of serine (Ser) and threonine (Thr) residues in the terminal carboxyl-tail of the receptor, which are potential targets of beta ark-mediated phosphorylation, prevented inhibition of receptor activation by beta ark2 in microinjected oocytes. Finally, a construct in which multiple Ser and Thr residues in the carboxyl-tail were changed to alanine significantly prolonged the agonist-dependent intracellular calcium flux and inhibited receptor internalization in transfected human embryonic kidney (HEK)-293 cells. These studies demonstrate that phosphorylation of Ser and Thr residues in the carboxyl-tail of CCR2B mediates receptor desensitization and internalization and may serve to limit the chemotactic response of leukocytes to MCP-1 and related chemokines.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • Amino Acid Sequence
  • Cyclic AMP-Dependent Protein Kinases / metabolism
  • GTP-Binding Proteins / physiology*
  • Humans
  • Molecular Sequence Data
  • Mutagenesis, Site-Directed
  • Phosphorylation
  • Receptors, CCR2
  • Receptors, Chemokine*
  • Receptors, Cytokine / chemistry
  • Receptors, Cytokine / physiology*
  • Recombinant Fusion Proteins
  • Serine / chemistry
  • Signal Transduction
  • Structure-Activity Relationship
  • Threonine / chemistry
  • Tumor Cells, Cultured
  • beta-Adrenergic Receptor Kinases

Substances

  • CCR2 protein, human
  • Receptors, CCR2
  • Receptors, Chemokine
  • Receptors, Cytokine
  • Recombinant Fusion Proteins
  • Threonine
  • Serine
  • Cyclic AMP-Dependent Protein Kinases
  • beta-Adrenergic Receptor Kinases
  • GTP-Binding Proteins