Partial ligand-receptor engagement yields functional bias at the human complement receptor, C5aR1

J Biol Chem. 2019 Jun 14;294(24):9416-9429. doi: 10.1074/jbc.RA119.007485. Epub 2019 Apr 29.

Abstract

The human complement component, C5a, binds two different seven-transmembrane receptors termed C5aR1 and C5aR2. C5aR1 is a prototypical G-protein-coupled receptor that couples to the Gαi subfamily of heterotrimeric G-proteins and β-arrestins (βarrs) following C5a stimulation. Peptide fragments derived from the C terminus of C5a can still interact with the receptor, albeit with lower affinity, and can act as agonists or antagonists. However, whether such fragments might display ligand bias at C5aR1 remains unexplored. Here, we compare C5a and a modified C-terminal fragment of C5a, C5apep, in terms of G-protein coupling, βarr recruitment, endocytosis, and extracellular signal-regulated kinase 1/2 mitogen-activated protein kinase activation at the human C5aR1. We discover that C5apep acts as a full agonist for Gαi coupling as measured by cAMP response and extracellular signal-regulated kinase 1/2 phosphorylation, but it displays partial agonism for βarr recruitment and receptor endocytosis. Interestingly, C5apep exhibits full-agonist efficacy with respect to inhibiting lipopolysaccharide-induced interleukin-6 secretion in human macrophages, but its ability to induce human neutrophil migration is substantially lower compared with C5a, although both these responses are sensitive to pertussis toxin treatment. Taken together, our data reveal that compared with C5a, C5apep exerts partial efficacy for βarr recruitment, receptor trafficking, and neutrophil migration. Our findings therefore uncover functional bias at C5aR1 and also provide a framework that can potentially be extended to chemokine receptors, which also typically interact with chemokines through a biphasic mechanism.

Keywords: G-protein–coupled receptor (GPCR); arrestin; cell signaling; complement; signal transduction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Cell Movement
  • Complement C5a / genetics
  • Complement C5a / metabolism*
  • Endocytosis*
  • HEK293 Cells
  • Humans
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Macrophages / cytology
  • Macrophages / metabolism
  • Mitogen-Activated Protein Kinase 1 / genetics
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3 / genetics
  • Mitogen-Activated Protein Kinase 3 / metabolism
  • Neutrophils / metabolism
  • Phosphorylation
  • Protein Binding
  • Receptor, Anaphylatoxin C5a / genetics
  • Receptor, Anaphylatoxin C5a / metabolism*
  • Sequence Homology
  • Signal Transduction
  • beta-Arrestins / genetics
  • beta-Arrestins / metabolism*

Substances

  • C5AR1 protein, human
  • Interleukin-6
  • Receptor, Anaphylatoxin C5a
  • beta-Arrestins
  • Complement C5a
  • MAPK1 protein, human
  • MAPK3 protein, human
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3