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Article
Atypical signaling and functional desensitization response of MAS receptor to peptide ligands
PLoS One
  • Kalyan C Tirupula, Cleveland Clinic
  • Russell Desnoyer, Cleveland Clinic
  • Robert C Speth, Nova Southeastern University
  • Sadashiva S Karnik, Cleveland Clinic
Document Type
Article
Publication Date
1-1-2014
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.

Creative Commons License
Creative Commons Attribution 4.0 International
ORCID ID

0000-0002-6434-2157

DOI
10.1371/journal.pone.0103520
Citation Information
Kalyan C Tirupula, Russell Desnoyer, Robert C Speth and Sadashiva S Karnik. "Atypical signaling and functional desensitization response of MAS receptor to peptide ligands" PLoS One Vol. 9 Iss. 7 (2014) p. e103520 ISSN: 1932-6203
Available at: http://works.bepress.com/robert-speth/81/