Lipids modulate the dynamics of GPCR:β-arrestin interaction

Abstract β-arrestins are key molecular partners of G Protein-Coupled Receptors (GPCRs), triggering not only their desensitization but also intracellular signaling. Existing structural data point to high conformational plasticity of GPCR:β-arrestin interaction, with two completely different orientati...

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Main Authors: Antoniel A. S. Gomes, Michela Di Michele, Rita Ann Roessner, Marjorie Damian, Paulo M. Bisch, Nathalie Sibille, Maxime Louet, Jean-Louis Banères, Nicolas Floquet
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59842-8
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author Antoniel A. S. Gomes
Michela Di Michele
Rita Ann Roessner
Marjorie Damian
Paulo M. Bisch
Nathalie Sibille
Maxime Louet
Jean-Louis Banères
Nicolas Floquet
author_facet Antoniel A. S. Gomes
Michela Di Michele
Rita Ann Roessner
Marjorie Damian
Paulo M. Bisch
Nathalie Sibille
Maxime Louet
Jean-Louis Banères
Nicolas Floquet
author_sort Antoniel A. S. Gomes
collection DOAJ
description Abstract β-arrestins are key molecular partners of G Protein-Coupled Receptors (GPCRs), triggering not only their desensitization but also intracellular signaling. Existing structural data point to high conformational plasticity of GPCR:β-arrestin interaction, with two completely different orientations between receptor and β-arrestin. Combining molecular dynamics simulations and fluorescence spectroscopy, we show that β-arrestin 1 interacts with membranes even in the absence of a receptor, an interaction that is enhanced by PI(4,5)P2, presumably holding the β-arrestin 1 C-edge loop into the lipid bilayer. This key interaction helps β-arrestin 1 to adopt a “receptor-ready” orientation and consequently favors its coupling to the ghrelin receptor (GHSR). In addition, we show that the GHSR:β-arrestin 1 assembly is a dynamic complex where β-arrestin can adopt several orientations. PI(4,5)P2 decreases the dynamics of the complex and shifts the equilibrium between the different arrangements, favoring one of them. Taken together, our results highlight how PI(4,5)P2 plays a true third-player role in the GPCR:β-arrestin interaction, not only by preparing β-arrestin for its further interaction with receptors but also by modulating its orientation once the protein:protein complex is formed.
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spelling doaj-art-682e45578c524f4c8c041ce63b528fb32025-08-20T02:03:31ZengNature PortfolioNature Communications2041-17232025-05-0116111610.1038/s41467-025-59842-8Lipids modulate the dynamics of GPCR:β-arrestin interactionAntoniel A. S. Gomes0Michela Di Michele1Rita Ann Roessner2Marjorie Damian3Paulo M. Bisch4Nathalie Sibille5Maxime Louet6Jean-Louis Banères7Nicolas Floquet8Institut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMLaboratório de Física Biológica, Instituto de Biofísica Carlos Chagas Filho, Universidade Federal doCentre de Biologie Structurale (CBS), CNRS, Université de Montpellier, InsermInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMInstitut des Biomolécules Max Mousseron (IBMM), UMR 5247 CNRS, Université de Montpellier, ENSCMAbstract β-arrestins are key molecular partners of G Protein-Coupled Receptors (GPCRs), triggering not only their desensitization but also intracellular signaling. Existing structural data point to high conformational plasticity of GPCR:β-arrestin interaction, with two completely different orientations between receptor and β-arrestin. Combining molecular dynamics simulations and fluorescence spectroscopy, we show that β-arrestin 1 interacts with membranes even in the absence of a receptor, an interaction that is enhanced by PI(4,5)P2, presumably holding the β-arrestin 1 C-edge loop into the lipid bilayer. This key interaction helps β-arrestin 1 to adopt a “receptor-ready” orientation and consequently favors its coupling to the ghrelin receptor (GHSR). In addition, we show that the GHSR:β-arrestin 1 assembly is a dynamic complex where β-arrestin can adopt several orientations. PI(4,5)P2 decreases the dynamics of the complex and shifts the equilibrium between the different arrangements, favoring one of them. Taken together, our results highlight how PI(4,5)P2 plays a true third-player role in the GPCR:β-arrestin interaction, not only by preparing β-arrestin for its further interaction with receptors but also by modulating its orientation once the protein:protein complex is formed.https://doi.org/10.1038/s41467-025-59842-8
spellingShingle Antoniel A. S. Gomes
Michela Di Michele
Rita Ann Roessner
Marjorie Damian
Paulo M. Bisch
Nathalie Sibille
Maxime Louet
Jean-Louis Banères
Nicolas Floquet
Lipids modulate the dynamics of GPCR:β-arrestin interaction
Nature Communications
title Lipids modulate the dynamics of GPCR:β-arrestin interaction
title_full Lipids modulate the dynamics of GPCR:β-arrestin interaction
title_fullStr Lipids modulate the dynamics of GPCR:β-arrestin interaction
title_full_unstemmed Lipids modulate the dynamics of GPCR:β-arrestin interaction
title_short Lipids modulate the dynamics of GPCR:β-arrestin interaction
title_sort lipids modulate the dynamics of gpcr β arrestin interaction
url https://doi.org/10.1038/s41467-025-59842-8
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