Atypical signaling and functional desensitization response of MAS receptor to peptide ligands

PLoS One. 2014 Jul 28;9(7):e103520. doi: 10.1371/journal.pone.0103520. eCollection 2014.

Abstract

MAS is a G protein-coupled receptor (GPCR) implicated in multiple physiological processes. Several physiological peptide ligands such as angiotensin-(1-7), angiotensin fragments and neuropeptide FF (NPFF) are reported to act on MAS. Studies of conventional G protein signaling and receptor desensitization upon stimulation of MAS with the peptide ligands are limited so far. Therefore, we systematically analyzed G protein signals activated by the peptide ligands. MAS-selective non-peptide ligands that were previously shown to activate G proteins were used as controls for comparison on a common cell based assay platform. Activation of MAS by the non-peptide agonist (1) increased intracellular calcium and D-myo-inositol-1-phosphate (IP1) levels which are indicative of the activation of classical Gαq-phospholipase C signaling pathways, (2) decreased Gαi mediated cAMP levels and (3) stimulated Gα12-dependent expression of luciferase reporter. In all these assays, MAS exhibited strong constitutive activity that was inhibited by the non-peptide inverse agonist. Further, in the calcium response assay, MAS was resistant to stimulation by a second dose of the non-peptide agonist after the first activation has waned suggesting functional desensitization. In contrast, activation of MAS by the peptide ligand NPFF initiated a rapid rise in intracellular calcium with very weak IP1 accumulation which is unlike classical Gαq-phospholipase C signaling pathway. NPFF only weakly stimulated MAS-mediated activation of Gα12 and Gαi signaling pathways. Furthermore, unlike non-peptide agonist-activated MAS, NPFF-activated MAS could be readily re-stimulated the second time by the agonists. Functional assays with key ligand binding MAS mutants suggest that NPFF and non-peptide ligands bind to overlapping regions. Angiotensin-(1-7) and other angiotensin fragments weakly potentiated an NPFF-like calcium response at non-physiological concentrations (≥100 µM). Overall, our data suggest that peptide ligands induce atypical signaling and functional desensitization of MAS.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Angiotensin I / metabolism
  • Angiotensin I / pharmacology
  • Binding Sites / genetics
  • Calcium / metabolism
  • HEK293 Cells
  • Humans
  • Inositol Phosphates / metabolism
  • Intracellular Space / drug effects
  • Intracellular Space / metabolism
  • Ligands
  • Microscopy, Confocal
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Neuropeptides / metabolism
  • Neuropeptides / pharmacology
  • Oligopeptides / metabolism
  • Oligopeptides / pharmacology
  • Peptide Fragments / metabolism
  • Peptide Fragments / pharmacology
  • Peptides / metabolism*
  • Peptides / pharmacology
  • Protein Binding / drug effects
  • Protein Structure, Secondary
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins / chemistry
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / metabolism*
  • Receptors, G-Protein-Coupled / chemistry
  • Receptors, G-Protein-Coupled / genetics
  • Receptors, G-Protein-Coupled / metabolism*
  • Signal Transduction*

Substances

  • Inositol Phosphates
  • Ligands
  • Neuropeptides
  • Oligopeptides
  • Peptide Fragments
  • Peptides
  • Proto-Oncogene Mas
  • Proto-Oncogene Proteins
  • Receptors, G-Protein-Coupled
  • Angiotensin I
  • phenylalanyl-leucyl-phenylalanyl-glutaminyl-prolyl-glutaminyl-arginyl-phenylalaninamide
  • angiotensin I (1-7)
  • Calcium