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Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation

The glucagon-like peptide-1 receptor (GLP-1R) has broad physiological roles and is a validated target for treatment of metabolic disorders. Despite recent advances in GLP-1R structure elucidation, detailed mechanistic understanding of how different peptides generate profound differences in G protein...

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Autores principales: Deganutti, Giuseppe, Liang, Yi-Lynn, Zhang, Xin, Khoshouei, Maryam, Clydesdale, Lachlan, Belousoff, Matthew J., Venugopal, Hari, Truong, Tin T., Glukhova, Alisa, Keller, Andrew N., Gregory, Karen J., Leach, Katie, Christopoulos, Arthur, Danev, Radostin, Reynolds, Christopher A., Zhao, Peishen, Sexton, Patrick M., Wootten, Denise
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8748714/
https://www.ncbi.nlm.nih.gov/pubmed/35013280
http://dx.doi.org/10.1038/s41467-021-27760-0
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author Deganutti, Giuseppe
Liang, Yi-Lynn
Zhang, Xin
Khoshouei, Maryam
Clydesdale, Lachlan
Belousoff, Matthew J.
Venugopal, Hari
Truong, Tin T.
Glukhova, Alisa
Keller, Andrew N.
Gregory, Karen J.
Leach, Katie
Christopoulos, Arthur
Danev, Radostin
Reynolds, Christopher A.
Zhao, Peishen
Sexton, Patrick M.
Wootten, Denise
author_facet Deganutti, Giuseppe
Liang, Yi-Lynn
Zhang, Xin
Khoshouei, Maryam
Clydesdale, Lachlan
Belousoff, Matthew J.
Venugopal, Hari
Truong, Tin T.
Glukhova, Alisa
Keller, Andrew N.
Gregory, Karen J.
Leach, Katie
Christopoulos, Arthur
Danev, Radostin
Reynolds, Christopher A.
Zhao, Peishen
Sexton, Patrick M.
Wootten, Denise
author_sort Deganutti, Giuseppe
collection PubMed
description The glucagon-like peptide-1 receptor (GLP-1R) has broad physiological roles and is a validated target for treatment of metabolic disorders. Despite recent advances in GLP-1R structure elucidation, detailed mechanistic understanding of how different peptides generate profound differences in G protein-mediated signalling is still lacking. Here we combine cryo-electron microscopy, molecular dynamics simulations, receptor mutagenesis and pharmacological assays, to interrogate the mechanism and consequences of GLP-1R binding to four peptide agonists; glucagon-like peptide-1, oxyntomodulin, exendin-4 and exendin-P5. These data reveal that distinctions in peptide N-terminal interactions and dynamics with the GLP-1R transmembrane domain are reciprocally associated with differences in the allosteric coupling to G proteins. In particular, transient interactions with residues at the base of the binding cavity correlate with enhanced kinetics for G protein activation, providing a rationale for differences in G protein-mediated signalling efficacy from distinct agonists.
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spelling pubmed-87487142022-01-20 Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation Deganutti, Giuseppe Liang, Yi-Lynn Zhang, Xin Khoshouei, Maryam Clydesdale, Lachlan Belousoff, Matthew J. Venugopal, Hari Truong, Tin T. Glukhova, Alisa Keller, Andrew N. Gregory, Karen J. Leach, Katie Christopoulos, Arthur Danev, Radostin Reynolds, Christopher A. Zhao, Peishen Sexton, Patrick M. Wootten, Denise Nat Commun Article The glucagon-like peptide-1 receptor (GLP-1R) has broad physiological roles and is a validated target for treatment of metabolic disorders. Despite recent advances in GLP-1R structure elucidation, detailed mechanistic understanding of how different peptides generate profound differences in G protein-mediated signalling is still lacking. Here we combine cryo-electron microscopy, molecular dynamics simulations, receptor mutagenesis and pharmacological assays, to interrogate the mechanism and consequences of GLP-1R binding to four peptide agonists; glucagon-like peptide-1, oxyntomodulin, exendin-4 and exendin-P5. These data reveal that distinctions in peptide N-terminal interactions and dynamics with the GLP-1R transmembrane domain are reciprocally associated with differences in the allosteric coupling to G proteins. In particular, transient interactions with residues at the base of the binding cavity correlate with enhanced kinetics for G protein activation, providing a rationale for differences in G protein-mediated signalling efficacy from distinct agonists. Nature Publishing Group UK 2022-01-10 /pmc/articles/PMC8748714/ /pubmed/35013280 http://dx.doi.org/10.1038/s41467-021-27760-0 Text en © The Author(s) 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Deganutti, Giuseppe
Liang, Yi-Lynn
Zhang, Xin
Khoshouei, Maryam
Clydesdale, Lachlan
Belousoff, Matthew J.
Venugopal, Hari
Truong, Tin T.
Glukhova, Alisa
Keller, Andrew N.
Gregory, Karen J.
Leach, Katie
Christopoulos, Arthur
Danev, Radostin
Reynolds, Christopher A.
Zhao, Peishen
Sexton, Patrick M.
Wootten, Denise
Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title_full Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title_fullStr Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title_full_unstemmed Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title_short Dynamics of GLP-1R peptide agonist engagement are correlated with kinetics of G protein activation
title_sort dynamics of glp-1r peptide agonist engagement are correlated with kinetics of g protein activation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8748714/
https://www.ncbi.nlm.nih.gov/pubmed/35013280
http://dx.doi.org/10.1038/s41467-021-27760-0
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