A non-canonical mechanism of GPCR activation

Abstract The goal of designing safer, more effective drugs has led to tremendous interest in molecular mechanisms through which ligands can precisely manipulate the signaling of G-protein-coupled receptors (GPCRs), the largest class of drug targets. Decades of research have led to the widely accepte...

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Main Authors: Alexander S. Powers, Aasma Khan, Joseph M. Paggi, Naomi R. Latorraca, Sarah Souza, Jerry Di Salvo, Jun Lu, Stephen M. Soisson, Jennifer M. Johnston, Adam B. Weinglass, Ron O. Dror
Format: Article
Language:English
Published: Nature Portfolio 2024-11-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54103-6
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author Alexander S. Powers
Aasma Khan
Joseph M. Paggi
Naomi R. Latorraca
Sarah Souza
Jerry Di Salvo
Jun Lu
Stephen M. Soisson
Jennifer M. Johnston
Adam B. Weinglass
Ron O. Dror
author_facet Alexander S. Powers
Aasma Khan
Joseph M. Paggi
Naomi R. Latorraca
Sarah Souza
Jerry Di Salvo
Jun Lu
Stephen M. Soisson
Jennifer M. Johnston
Adam B. Weinglass
Ron O. Dror
author_sort Alexander S. Powers
collection DOAJ
description Abstract The goal of designing safer, more effective drugs has led to tremendous interest in molecular mechanisms through which ligands can precisely manipulate the signaling of G-protein-coupled receptors (GPCRs), the largest class of drug targets. Decades of research have led to the widely accepted view that all agonists—ligands that trigger GPCR activation—function by causing rearrangement of the GPCR’s transmembrane helices, opening an intracellular pocket for binding of transducer proteins. Here we demonstrate that certain agonists instead trigger activation of free fatty acid receptor 1 by directly rearranging an intracellular loop that interacts with transducers. We validate the predictions of our atomic-level simulations by targeted mutagenesis; specific mutations that disrupt interactions with the intracellular loop convert these agonists into inverse agonists. Further analysis suggests that allosteric ligands could regulate the signaling of many other GPCRs via a similar mechanism, offering rich possibilities for precise control of pharmaceutically important targets.
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publishDate 2024-11-01
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spelling doaj-art-4b97ff53806049ee92388f4ef8a727d42024-11-17T12:36:27ZengNature PortfolioNature Communications2041-17232024-11-0115111210.1038/s41467-024-54103-6A non-canonical mechanism of GPCR activationAlexander S. Powers0Aasma Khan1Joseph M. Paggi2Naomi R. Latorraca3Sarah Souza4Jerry Di Salvo5Jun Lu6Stephen M. Soisson7Jennifer M. Johnston8Adam B. Weinglass9Ron O. Dror10Department of Chemistry, Stanford UniversityDepartment of Quantitative Biosciences, Merck & Co., Inc.Department of Computer Science, Stanford UniversityDepartment of Computer Science, Stanford UniversityDepartment of Quantitative Biosciences, Merck & Co., Inc.EvotecDepartment of Structural Chemistry, Merck & Co., Inc.Department of Structural Chemistry, Merck & Co., Inc.Department of Modeling and Informatics, Merck & Co., Inc.Department of Quantitative Biosciences, Merck & Co., Inc.Department of Computer Science, Stanford UniversityAbstract The goal of designing safer, more effective drugs has led to tremendous interest in molecular mechanisms through which ligands can precisely manipulate the signaling of G-protein-coupled receptors (GPCRs), the largest class of drug targets. Decades of research have led to the widely accepted view that all agonists—ligands that trigger GPCR activation—function by causing rearrangement of the GPCR’s transmembrane helices, opening an intracellular pocket for binding of transducer proteins. Here we demonstrate that certain agonists instead trigger activation of free fatty acid receptor 1 by directly rearranging an intracellular loop that interacts with transducers. We validate the predictions of our atomic-level simulations by targeted mutagenesis; specific mutations that disrupt interactions with the intracellular loop convert these agonists into inverse agonists. Further analysis suggests that allosteric ligands could regulate the signaling of many other GPCRs via a similar mechanism, offering rich possibilities for precise control of pharmaceutically important targets.https://doi.org/10.1038/s41467-024-54103-6
spellingShingle Alexander S. Powers
Aasma Khan
Joseph M. Paggi
Naomi R. Latorraca
Sarah Souza
Jerry Di Salvo
Jun Lu
Stephen M. Soisson
Jennifer M. Johnston
Adam B. Weinglass
Ron O. Dror
A non-canonical mechanism of GPCR activation
Nature Communications
title A non-canonical mechanism of GPCR activation
title_full A non-canonical mechanism of GPCR activation
title_fullStr A non-canonical mechanism of GPCR activation
title_full_unstemmed A non-canonical mechanism of GPCR activation
title_short A non-canonical mechanism of GPCR activation
title_sort non canonical mechanism of gpcr activation
url https://doi.org/10.1038/s41467-024-54103-6
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