TY - JOUR
T1 - Biased agonists of the chemokine receptor CXCR3 differentially signal through Gαi:β-arrestin complexes
AU - Zheng, Kevin
AU - Smith, Jeffrey S.
AU - Eiger, Dylan S.
AU - Warman, Anmol
AU - Choi, Issac
AU - Honeycutt, Christopher C.
AU - Boldizsar, Noelia
AU - Gundry, Jaimee N.
AU - Pack, Thomas F.
AU - Inoue, Asuka
AU - Caron, Marc G.
AU - Rajagopal, Sudarshan
N1 - Funding Information:
This work was supported by T32GM7171 (to J.S.S.); the Duke Medical Scientist Training Program (to J.S.S. and D.S.E.); F31DA041160 (to T.F.P.); the Japan Agency for Medical Research and Development 19gm5910013 (to A.I.), JP19gm0010004 (to A.I.), and JP20am0101095 (to A.I.); the Japan Society for the Promotion of Science 21H04791 (to A.I.); Japan Science and Technology Agency JPMJMS2023 (to A.I.); The Uehara Memorial Foundation (to A.I.), 17K08264R37MH073853 (to M.G.C.), 1R01GM122798-01A1 (to S.R.), K08HL114643-01A1 (to S.R.); and the Burroughs Wellcome Career Award for Medical Scientists (to S.R.).
Publisher Copyright:
© 2022 The Authors, some rights reserved.
PY - 2022/3/22
Y1 - 2022/3/22
N2 - G protein-coupled receptors (GPCRs) are the largest family of cell surface receptors and signal through the proximal effectors, G proteins and β-arrestins, to influence nearly every biological process. The G protein and β-arrestin signaling pathways have largely been considered separable; however, direct interactions between Gα proteins and β-arrestins have been described that appear to be part of a distinct GPCR signaling pathway. Within these complexes, Gαi/o, but not other Gα protein subtypes, directly interacts with β-arrestin, regardless of the canonical Gα protein that is coupled to the GPCR. Here, we report that the endogenous biased chemokine agonists of CXCR3 (CXCL9, CXCL10, and CXCL11), together with two small-molecule biased agonists, differentially formed Gαi:β-arrestin complexes. Formation of the Gαi:β-arrestin complexes did not correlate well with either G protein activation or β-arrestin recruitment. β-arrestin biosensors demonstrated that ligands that promoted Gαi:β-arrestin complex formation generated similar β-arrestin conformations. We also found that Gαi:β-arrestin complexes did not couple to the mitogen-activated protein kinase ERK, as is observed with other receptors such as the V2 vasopressin receptor, but did couple with the clathrin adaptor protein AP-2, which suggests context-dependent signaling by these complexes. These findings reinforce the notion that Gαi:β-arrestin complex formation is a distinct GPCR signaling pathway and enhance our understanding of the spectrum of biased agonism.
AB - G protein-coupled receptors (GPCRs) are the largest family of cell surface receptors and signal through the proximal effectors, G proteins and β-arrestins, to influence nearly every biological process. The G protein and β-arrestin signaling pathways have largely been considered separable; however, direct interactions between Gα proteins and β-arrestins have been described that appear to be part of a distinct GPCR signaling pathway. Within these complexes, Gαi/o, but not other Gα protein subtypes, directly interacts with β-arrestin, regardless of the canonical Gα protein that is coupled to the GPCR. Here, we report that the endogenous biased chemokine agonists of CXCR3 (CXCL9, CXCL10, and CXCL11), together with two small-molecule biased agonists, differentially formed Gαi:β-arrestin complexes. Formation of the Gαi:β-arrestin complexes did not correlate well with either G protein activation or β-arrestin recruitment. β-arrestin biosensors demonstrated that ligands that promoted Gαi:β-arrestin complex formation generated similar β-arrestin conformations. We also found that Gαi:β-arrestin complexes did not couple to the mitogen-activated protein kinase ERK, as is observed with other receptors such as the V2 vasopressin receptor, but did couple with the clathrin adaptor protein AP-2, which suggests context-dependent signaling by these complexes. These findings reinforce the notion that Gαi:β-arrestin complex formation is a distinct GPCR signaling pathway and enhance our understanding of the spectrum of biased agonism.
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U2 - 10.1126/scisignal.abg5203
DO - 10.1126/scisignal.abg5203
M3 - Article
C2 - 35316095
AN - SCOPUS:85126907541
SN - 1937-9145
VL - 15
JO - Science's STKE : signal transduction knowledge environment
JF - Science's STKE : signal transduction knowledge environment
IS - 726
M1 - eabg5203
ER -