Tail engagement of arrestin at the glucagon receptor.


Journal

Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462

Informations de publication

Date de publication:
Aug 2023
Historique:
received: 03 04 2023
accepted: 11 07 2023
medline: 25 8 2023
pubmed: 10 8 2023
entrez: 9 8 2023
Statut: ppublish

Résumé

Arrestins have pivotal roles in regulating G protein-coupled receptor (GPCR) signalling by desensitizing G protein activation and mediating receptor internalization

Identifiants

pubmed: 37558880
doi: 10.1038/s41586-023-06420-x
pii: 10.1038/s41586-023-06420-x
pmc: PMC10447241
doi:

Substances chimiques

beta-Arrestin 1 0
Glucagon 9007-92-5
Heterotrimeric GTP-Binding Proteins EC 3.6.5.1
Ligands 0
Phosphatidylinositols 0
Receptors, Glucagon 0

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

904-910

Informations de copyright

© 2023. The Author(s).

Références

Fredriksson, R., Lagerstrom, M. C., Lundin, L. G. & Schioth, H. B. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol. Pharmacol. 63, 1256–1272 (2003).
pubmed: 12761335 doi: 10.1124/mol.63.6.1256
Rajagopal, S. & Shenoy, S. K. GPCR desensitization: acute and prolonged phases. Cell Signal. 41, 9–16 (2018).
pubmed: 28137506 doi: 10.1016/j.cellsig.2017.01.024
Shukla, A. K. et al. Visualization of arrestin recruitment by a G-protein-coupled receptor. Nature 512, 218–222 (2014).
pubmed: 25043026 pmcid: 4134437 doi: 10.1038/nature13430
Cahill, T. J. III et al. Distinct conformations of GPCR–β-arrestin complexes mediate desensitization, signaling, and endocytosis. Proc. Natl. Acad. Sci. USA 114, 2562–2567 (2017).
Gilman, A. G. G proteins: transducers of receptor-generated signals. Annu. Rev. Biochem. 56, 615–649 (1987).
pubmed: 3113327 doi: 10.1146/annurev.bi.56.070187.003151
Moore, C. A., Milano, S. K. & Benovic, J. L. Regulation of receptor trafficking by GRKs and arrestins. Annu. Rev. Physiol. 69, 451–482 (2007).
pubmed: 17037978 doi: 10.1146/annurev.physiol.69.022405.154712
Kang, Y. et al. Crystal structure of rhodopsin bound to arrestin by femtosecond X-ray laser. Nature 523, 561–567 (2015).
pubmed: 26200343 pmcid: 4521999 doi: 10.1038/nature14656
Reiter, E., Ahn, S., Shukla, A. K. & Lefkowitz, R. J. Molecular mechanism of β-arrestin-biased agonism at seven-transmembrane receptors. Annu. Rev. Pharmacol. Toxicol. 52, 179–197 (2012).
pubmed: 21942629 doi: 10.1146/annurev.pharmtox.010909.105800
Oakley, R. H., Laporte, S. A., Holt, J. A., Barak, L. S. & Caron, M. G. Association of β-arrestin with G protein-coupled receptors during clathrin-mediated endocytosis dictates the profile of receptor resensitization. J. Biol. Chem. 274, 32248–32257 (1999).
pubmed: 10542263 doi: 10.1074/jbc.274.45.32248
Oakley, R. H., Laporte, S. A., Holt, J. A., Caron, M. G. & Barak, L. S. Differential affinities of visual arrestin, β arrestin1, and β arrestin2 for G protein-coupled receptors delineate two major classes of receptors. J. Biol. Chem. 275, 17201–17210 (2000).
pubmed: 10748214 doi: 10.1074/jbc.M910348199
Lee, M. H. et al. The conformational signature of β-arrestin2 predicts its trafficking and signalling functions. Nature 531, 665–668 (2016).
pubmed: 27007854 pmcid: 4973468 doi: 10.1038/nature17154
Latorraca, N. R. et al. Molecular mechanism of GPCR-mediated arrestin activation. Nature 557, 452–456 (2018).
pubmed: 29720655 pmcid: 6294333 doi: 10.1038/s41586-018-0077-3
Yin, W. et al. A complex structure of arrestin-2 bound to a G protein-coupled receptor. Cell Res. 29, 971–983 (2019).
pubmed: 31776446 pmcid: 6951264 doi: 10.1038/s41422-019-0256-2
Staus, D. P. et al. Structure of the M2 muscarinic receptor–β-arrestin complex in a lipid nanodisc. Nature 579, 297–302 (2020).
pubmed: 31945772 pmcid: 7367492 doi: 10.1038/s41586-020-1954-0
Huang, W. et al. Structure of the neurotensin receptor 1 in complex with β-arrestin 1. Nature 579, 303–308 (2020).
pubmed: 31945771 pmcid: 7100716 doi: 10.1038/s41586-020-1953-1
Lee, Y. et al. Molecular basis of β-arrestin coupling to formoterol-bound β
pubmed: 32555462 pmcid: 7115876 doi: 10.1038/s41586-020-2419-1
Bous, J. et al. Structure of the vasopressin hormone-V2 receptor–β-arrestin1 ternary complex. Sci. Adv. 8, eabo7761 (2022).
pubmed: 36054364 doi: 10.1126/sciadv.abo7761
Cao, C. et al. Signaling snapshots of a serotonin receptor activated by the prototypical psychedelic LSD. Neuron 110, 3154–3167 (2022).
pubmed: 36087581 doi: 10.1016/j.neuron.2022.08.006
Zhang, Y. et al. Cryo-EM structure of the activated GLP-1 receptor in complex with a G protein. Nature 546, 248–253 (2017).
pubmed: 28538729 pmcid: 5587415 doi: 10.1038/nature22394
Qiao, A. et al. Structural basis of G
pubmed: 32193322 doi: 10.1126/science.aaz5346
Wootten, D., Miller, L. J., Koole, C., Christopoulos, A. & Sexton, P. M. Allostery and biased agonism at class B G protein-coupled receptors. Chem. Rev. 117, 111–138 (2017).
pubmed: 27040440 doi: 10.1021/acs.chemrev.6b00049
Gesty-Palmer, D. et al. A β-arrestin-biased agonist of the parathyroid hormone receptor (PTH1R) promotes bone formation independent of G protein activation. Sci. Transl. Med. 1, 1ra1 (2009).
pubmed: 20368153 pmcid: 2852200 doi: 10.1126/scitranslmed.3000071
Zhang, H. et al. Autocrine selection of a GLP-1R G-protein biased agonist with potent antidiabetic effects. Nat. Commun. 6, 8918 (2015).
pubmed: 26621478 doi: 10.1038/ncomms9918
Hager, M. V., Johnson, L. M., Wootten, D., Sexton, P. M. & Gellman, S. H. β-Arrestin-biased agonists of the GLP-1 receptor from β-amino acid residue incorporation into GLP-1 analogues. J. Am. Chem. Soc. 138, 14970–14979 (2016).
pubmed: 27813409 pmcid: 5207657 doi: 10.1021/jacs.6b08323
Hager, M. V., Clydesdale, L., Gellman, S. H., Sexton, P. M. & Wootten, D. Characterization of signal bias at the GLP-1 receptor induced by backbone modification of GLP-1. Biochem. Pharmacol. 136, 99–108 (2017).
pubmed: 28363772 pmcid: 5794489 doi: 10.1016/j.bcp.2017.03.018
Darbalaei, S. et al. Evaluation of biased agonism mediated by dual agonists of the GLP-1 and glucagon receptors. Biochem. Pharmacol. 180, 114150 (2020).
pubmed: 32682761 doi: 10.1016/j.bcp.2020.114150
Ferrandon, S. et al. Sustained cyclic AMP production by parathyroid hormone receptor endocytosis. Nat. Chem. Biol. 5, 734–742 (2009).
pubmed: 19701185 pmcid: 3032084 doi: 10.1038/nchembio.206
Wehbi, V. L. et al. Noncanonical GPCR signaling arising from a PTH receptor–arrestin–Gβγ complex. Proc. Natl. Acad. Sci. USA 110, 1530–1535 (2013).
Kuna, R. S. et al. Glucagon-like peptide-1 receptor-mediated endosomal cAMP generation promotes glucose-stimulated insulin secretion in pancreatic β-cells. Am. J. Physiol. Endocrinol. Metab. 305, E161–E170 (2013).
pubmed: 23592482 doi: 10.1152/ajpendo.00551.2012
Vilardaga, J. P., Jean-Alphonse, F. G. & Gardella, T. J. Endosomal generation of cAMP in GPCR signaling. Nat. Chem. Biol. 10, 700–706 (2014).
pubmed: 25271346 pmcid: 4417940 doi: 10.1038/nchembio.1611
Yarwood, R. E. et al. Endosomal signaling of the receptor for calcitonin gene-related peptide mediates pain transmission. Proc. Natl. Acad. Sci. USA 114, 12309–12314 (2017).
Krilov, L., Nguyen, A., Miyazaki, T., Unson, C. G. & Bouscarel, B. Glucagon receptor recycling: role of carboxyl terminus, β-arrestins, and cytoskeleton. Am. J. Physiol. Cell Physiol. 295, C1230–C1237 (2008).
pubmed: 18787074 pmcid: 2584980 doi: 10.1152/ajpcell.00240.2008
Aydin, Y. et al. Structural details of a class B GPCR–arrestin complex revealed by genetically encoded crosslinkers in living cells. Nat. Commun. 14, 1151 (2023).
pubmed: 36859440 pmcid: 9977954 doi: 10.1038/s41467-023-36797-2
Janetzko, J. et al. Membrane phosphoinositides regulate GPCR–β-arrestin complex assembly and dynamics. Cell 185, 4560–4573 (2022).
pubmed: 36368322 pmcid: 10030194 doi: 10.1016/j.cell.2022.10.018
Gaidarov, I., Krupnick, J. G., Falck, J. R., Benovic, J. L. & Keen, J. H. Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18, 871–881 (1999).
pubmed: 10022830 pmcid: 1171180 doi: 10.1093/emboj/18.4.871
Milano, S. K., Kim, Y. M., Stefano, F. P., Benovic, J. L. & Brenner, C. Nonvisual arrestin oligomerization and cellular localization are regulated by inositol hexakisphosphate binding. J. Biol. Chem. 281, 9812–9823 (2006).
pubmed: 16439357 doi: 10.1074/jbc.M512703200
Zhang, H. et al. Structure of the full-length glucagon class B G-protein-coupled receptor. Nature 546, 259–264 (2017).
pubmed: 28514451 pmcid: 5492955 doi: 10.1038/nature22363
Wootten, D., Simms, J., Miller, L. J., Christopoulos, A. & Sexton, P. M. Polar transmembrane interactions drive formation of ligand-specific and signal pathway-biased family B G protein-coupled receptor conformations. Proc. Natl. Acad. Sci. USA 110, 5211–5216 (2013).
DeVree, B. T. et al. Allosteric coupling from G protein to the agonist-binding pocket in GPCRs. Nature 535, 182–186 (2016).
pubmed: 27362234 pmcid: 5702553 doi: 10.1038/nature18324
Namkung, Y. et al. Monitoring G protein-coupled receptor and β-arrestin trafficking in live cells using enhanced bystander BRET. Nat. Commun. 7, 12178 (2016).
pubmed: 27397672 pmcid: 4942582 doi: 10.1038/ncomms12178
Zhang, J. et al. Cellular trafficking of G protein-coupled receptor/β-arrestin endocytic complexes. J. Biol. Chem. 274, 10999–11006 (1999).
pubmed: 10196181 doi: 10.1074/jbc.274.16.10999
Gurevich, V. V. & Gurevich, E. V. The structural basis of arrestin-mediated regulation of G-protein-coupled receptors. Pharmacol. Ther. 110, 465–502 (2006).
pubmed: 16460808 pmcid: 2562282 doi: 10.1016/j.pharmthera.2005.09.008
Walker, J. K., Premont, R. T., Barak, L. S., Caron, M. G. & Shetzline, M. A. Properties of secretin receptor internalization differ from those of the β
pubmed: 10531354 doi: 10.1074/jbc.274.44.31515
Shetzline, M. A., Walker, J. K., Valenzano, K. J. & Premont, R. T. Vasoactive intestinal polypeptide type-1 receptor regulation. Desensitization, phosphorylation, and sequestration. J. Biol. Chem. 277, 25519–25526 (2002).
pubmed: 11978791 doi: 10.1074/jbc.M201815200
Kumari, P. et al. Core engagement with β-arrestin is dispensable for agonist-induced vasopressin receptor endocytosis and ERK activation. Mol. Biol. Cell 28, 1003–1010 (2017).
pubmed: 28228552 pmcid: 5391177 doi: 10.1091/mbc.e16-12-0818
Feinstein, T. N. et al. Noncanonical control of vasopressin receptor type 2 signaling by retromer and arrestin. J. Biol. Chem. 288, 27849–27860 (2013).
pubmed: 23935101 pmcid: 3784700 doi: 10.1074/jbc.M112.445098
Irannejad, R. et al. Conformational biosensors reveal GPCR signalling from endosomes. Nature 495, 534–538 (2013).
pubmed: 23515162 doi: 10.1038/nature12000
Calebiro, D. et al. Persistent cAMP-signals triggered by internalized G-protein-coupled receptors. PLoS Biol. 7, e1000172 (2009).
pubmed: 19688034 pmcid: 2718703 doi: 10.1371/journal.pbio.1000172
Thomsen, A. R. B. et al. GPCR–G protein–β-arrestin super-complex mediates sustained G protein signaling. Cell 166, 907–919 (2016).
pubmed: 27499021 pmcid: 5418658 doi: 10.1016/j.cell.2016.07.004
Nguyen, A. H. & Lefkowitz, R. J. Signaling at the endosome: cryo-EM structure of a GPCR–G protein–β-arrestin megacomplex. FEBS J. 288, 2562–2569 (2021).
pubmed: 33605032 pmcid: 8252779 doi: 10.1111/febs.15773
Kovoor, A., Celver, J., Abdryashitov, R. I., Chavkin, C. & Gurevich, V. V. Targeted construction of phosphorylation-independent β-arrestin mutants with constitutive activity in cells. J. Biol. Chem. 274, 6831–6834 (1999).
pubmed: 10066734 doi: 10.1074/jbc.274.11.6831
Nguyen, A. H. et al. Structure of an endosomal signaling GPCR–G protein–β-arrestin megacomplex. Nat. Struct. Mol. Biol. 26, 1123–1131 (2019).
pubmed: 31740855 pmcid: 7108872 doi: 10.1038/s41594-019-0330-y
Mastronarde, D. N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 152, 36–51 (2005).
pubmed: 16182563 doi: 10.1016/j.jsb.2005.07.007
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466 pmcid: 5494038 doi: 10.1038/nmeth.4193
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473 doi: 10.1038/nmeth.4169
Goddard, T. D. et al. UCSF ChimeraX: meeting modern challenges in visualization and analysis. Protein Sci. 27, 14–25 (2018).
pubmed: 28710774 doi: 10.1002/pro.3235
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
pubmed: 15572765 doi: 10.1107/S0907444904019158
Adams, P. D. et al. The Phenix software for automated determination of macromolecular structures. Methods 55, 94–106 (2011).
pubmed: 21821126 pmcid: 3193589 doi: 10.1016/j.ymeth.2011.07.005
Williams, C. J. et al. MolProbity: more and better reference data for improved all-atom structure validation. Protein Sci. 27, 293–315 (2018).
pubmed: 29067766 doi: 10.1002/pro.3330
Olsen, R. H. J. et al. TRUPATH, an open-source biosensor platform for interrogating the GPCR transducerome. Nat. Chem. Biol. 16, 841–849 (2020).
pubmed: 32367019 pmcid: 7648517 doi: 10.1038/s41589-020-0535-8
Jumper, J. et al. Highly accurate protein structure prediction with AlphaFold. Nature 596, 583–589 (2021).
pubmed: 34265844 pmcid: 8371605 doi: 10.1038/s41586-021-03819-2

Auteurs

Kun Chen (K)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.
University of Chinese Academy of Sciences, Beijing, China.

Chenhui Zhang (C)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.
University of Chinese Academy of Sciences, Beijing, China.

Shuling Lin (S)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.

Xinyu Yan (X)

School of Chinese Materia Medica, Nanjing University of Chinese Medicine, Nanjing, China.

Heng Cai (H)

School of Pharmaceutical Science and Technology, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, China.

Cuiying Yi (C)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.

Limin Ma (L)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.

Xiaojing Chu (X)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.

Yuchen Liu (Y)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.
University of Chinese Academy of Sciences, Beijing, China.

Ya Zhu (Y)

Lingang Laboratory, Shanghai, China.

Shuo Han (S)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China.
University of Chinese Academy of Sciences, Beijing, China.
School of Pharmaceutical Science and Technology, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, China.

Qiang Zhao (Q)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China. zhaoq@simm.ac.cn.
University of Chinese Academy of Sciences, Beijing, China. zhaoq@simm.ac.cn.
School of Chinese Materia Medica, Nanjing University of Chinese Medicine, Nanjing, China. zhaoq@simm.ac.cn.
Zhongshan Institute for Drug Discovery, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Zhongshan, China. zhaoq@simm.ac.cn.

Beili Wu (B)

State Key Laboratory of Drug Research, State Key Laboratory of Chemical Biology, Shanghai Institute of Materia Medica, Chinese Academy of Sciences, Shanghai, China. beiliwu@simm.ac.cn.
University of Chinese Academy of Sciences, Beijing, China. beiliwu@simm.ac.cn.
School of Pharmaceutical Science and Technology, Hangzhou Institute for Advanced Study, University of Chinese Academy of Sciences, Hangzhou, China. beiliwu@simm.ac.cn.
School of Life Science and Technology, ShanghaiTech University, Shanghai, China. beiliwu@simm.ac.cn.

Articles similaires

Conservation of the cooling agent binding pocket within the TRPM subfamily.

Kate Huffer, Matthew C S Denley, Elisabeth V Oskoui et al.
1.00
TRPM Cation Channels Animals Binding Sites Mice Pyrimidinones
Fucosyltransferases Drug Repositioning Molecular Docking Simulation Molecular Dynamics Simulation Humans
Receptor, Cannabinoid, CB1 Ligands Molecular Dynamics Simulation Protein Binding Thermodynamics
Humans Animals Adherens Junctions Intercellular Junctions Tight Junctions

Classifications MeSH