Vibrational spectroscopy analysis of ligand efficacy in human M
Journal
Communications biology
ISSN: 2399-3642
Titre abrégé: Commun Biol
Pays: England
ID NLM: 101719179
Informations de publication
Date de publication:
23 11 2021
23 11 2021
Historique:
received:
11
04
2021
accepted:
01
11
2021
entrez:
24
11
2021
pubmed:
25
11
2021
medline:
25
12
2021
Statut:
epublish
Résumé
The intrinsic efficacy of ligand binding to G protein-coupled receptors (GPCRs) reflects the ability of the ligand to differentially activate its receptor to cause a physiological effect. Here we use attenuated total reflection-Fourier transform infrared (ATR-FTIR) spectroscopy to examine the ligand-dependent conformational changes in the human M
Identifiants
pubmed: 34815515
doi: 10.1038/s42003-021-02836-1
pii: 10.1038/s42003-021-02836-1
pmc: PMC8635417
doi:
Substances chimiques
CHRM2 protein, human
0
Ligands
0
Receptor, Muscarinic M2
0
Banques de données
figshare
['10.6084/m9.figshare.16608511']
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1321Subventions
Organisme : MEXT | Japan Society for the Promotion of Science (JSPS)
ID : 18K14662
Organisme : MEXT | Japan Science and Technology Agency (JST)
ID : JPMJPR19G4
Informations de copyright
© 2021. The Author(s).
Références
Kenakin, T. Drug efficacy at G protein-coupled receptors. Annu. Rev. Pharmacol. Toxicol. 42, 349–379 (2002).
pubmed: 11807176
doi: 10.1146/annurev.pharmtox.42.091401.113012
Weis, W. I. & Kobilka, B. K. The molecular basis of G protein-coupled receptor activation. Annu. Rev. Biochem. 87, 897–919 (2018).
pubmed: 29925258
pmcid: 6535337
doi: 10.1146/annurev-biochem-060614-033910
Manglik, A. et al. Structural insights into the dynamics process of β
pubmed: 25981665
pmcid: 4441853
doi: 10.1016/j.cell.2015.04.043
Kobilka, B. K. & Deupi, X. Conformational complexity of G-protein-coupled receptors. Trends Pharmacol. Sci. 28, 397–406 (2007).
pubmed: 17629961
doi: 10.1016/j.tips.2007.06.003
Rosenbaum, D. M., Rasmussen, S. G. & Kobilka, B. K. The structure and function of G-protein-coupled receptors. Nature 459, 356–363 (2009).
pubmed: 19458711
pmcid: 3967846
doi: 10.1038/nature08144
Wacker, D., Stevens, R. C. & Roth, B. L. How ligands illuminate GPCR molecular pharmacology. Cell 170, 414–427 (2017).
pubmed: 28753422
pmcid: 5560499
doi: 10.1016/j.cell.2017.07.009
Kenakin, T. & Christopoulos, A. Analytical pharmacology: the impact of numbers on pharmacology. Trends Pharmacol. Sci. 32, 189–196 (2011).
pubmed: 21397341
doi: 10.1016/j.tips.2011.01.002
Kenakin, T. Efficacy at G-protein-coupled receptors. Nat. Rev. Drug. Discov. 1, 103–110 (2002).
pubmed: 12120091
doi: 10.1038/nrd722
Herenbrink, C. K. et al. The role of kinetic context in apparent biased agonism at GPCRs. Nat. Commun. 7, 10842–10856 (2016).
doi: 10.1038/ncomms10842
Katritch, V., Cherezov, V. & Stevens, R. C. Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci. 33, 17–27 (2012).
pubmed: 22032986
doi: 10.1016/j.tips.2011.09.003
Warne, T., Edwards, P. C., Doré, A. S., Leslie, A. G. W. & Tate, C. G. Moleular basis for high-affinity agonist binding in GPCRs. Science 364, 775–778 (2019).
pubmed: 31072904
pmcid: 6586556
doi: 10.1126/science.aau5595
Liu, X. et al. Structural insights into the process of GPCR-G protein complex formation. Cell 177, 1243–1251 (2019).
pubmed: 31080070
pmcid: 6991123
doi: 10.1016/j.cell.2019.04.021
García-Nafría, J. & Tate, C. G. Cryo-electron microscopy: moving beyond X-ray crystal structures for drug receptors and drug development. Annu. Rev. Pharmacol. Toxicol. 60, 51–71 (2020).
pubmed: 31348870
doi: 10.1146/annurev-pharmtox-010919-023545
Haga, K. et al. Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482, 547–551 (2012).
pubmed: 22278061
pmcid: 3345277
doi: 10.1038/nature10753
Suno, R. et al. Structural insights into the subtype-selective antagonist binding to the M
pubmed: 30420692
pmcid: 6462224
doi: 10.1038/s41589-018-0152-y
Kruse, A. C. et al. Activation and allosteric modulation of a muscarinic acetylcholine receptor. Nature 504, 101–106 (2013).
pubmed: 24256733
pmcid: 4020789
doi: 10.1038/nature12735
Maeda, S., Qu, Q., Robertson, M. J., Skiniotis, G. & Kobilka, B. K. Structures of the M
pubmed: 31073061
pmcid: 7034192
doi: 10.1126/science.aaw5188
Kofuku, Y. et al. Efficacy of the β
pubmed: 22948827
doi: 10.1038/ncomms2046
Solt, A. S. et al. Insight into partial agonism by observing multiple equilibria for ligand-bound and Gs-mimetic nanobody-bound β
pubmed: 29176642
pmcid: 5702606
doi: 10.1038/s41467-017-02008-y
Okude, J. et al. Identification of a conformational equilibrium that determines the efficacy and functional selectivity of the μ-opioid receptor. Angew. Chem. Int. Ed. 54, 15771–15776 (2015).
doi: 10.1002/anie.201508794
Wu, F.-J. et al. Probing the correation between ligand efficacy and conformaitonal diversity at the α
pubmed: 32303636
pmcid: 7247315
doi: 10.1074/jbc.RA120.012842
Xu, J. et al. Conformational complexity and dynamics in a muscarinic receptor revealed by NMR spectroscopy. Mol. Cell 75, 1–15 (2019).
doi: 10.1016/j.molcel.2019.04.028
Wingler, L. M. et al. Angiotensin analogs with divergent bias stabilize distinct receptor conformations. Cell 176, 468–478 (2019).
pubmed: 30639099
pmcid: 6475118
doi: 10.1016/j.cell.2018.12.005
Mahalingam, M., Martínez-Mayorga, K., Brown, M. & Vogel, R. Two protonation switches control rhodopsin activation in membranes. Proc. Natl Acad. Sci. USA 105, 17795–17800 (2008).
pubmed: 18997017
pmcid: 2584695
doi: 10.1073/pnas.0804541105
Zaitseva, E., Brown, M. F. & Vogel, R. Sequential rearrangement of interhelical networks upon rhodopsin activation in membranes: The Meta IIa conformational substate. J. Am. Chem. Soc. 132, 4815–4821 (2010).
pubmed: 20230054
pmcid: 2859452
doi: 10.1021/ja910317a
Furutani, Y., Shichida, Y. & Kandori, H. Sturctural changes of water molecules during the photoactivation processes in bovine rhodopsin. Biochemistry 42, 9619–9625 (2003).
pubmed: 12911303
doi: 10.1021/bi034592k
Kumar, S. & Barth, A. Following enzyme activity with infrared spectroscopy. Sensors 10, 2626–2637 (2010).
pubmed: 22319264
pmcid: 3274194
doi: 10.3390/s100402626
Iwaki, M., Cotton, N. P. J., Quirk, P. G., Rich, P. R. & Baz Jackson, J. Molecular recognition between protein and nicotinamide dinucleotide in intact, proton-translocating transhydrogenase studied by ATR-FTIR spectroscopy. J. Am. Chem. Soc. 128, 2621–2629 (2006).
pubmed: 16492047
doi: 10.1021/ja0556272
Kitade, Y., Furutani, Y., Kamo, N. & Kandori, H. Proton release group of pharaonic phoborhodopsin revealed by ATR-FTIR spectroscopy. Biochemistry 48, 1595–1603 (2009).
pubmed: 19178155
doi: 10.1021/bi801984u
Jiang, X. et al. Resolving voltage-dependent structural changes of a membrane photoreceptor by surface-enhanced IR difference spectroscopy. Proc. Natl Acad. Sci. USA 105, 12113–12117 (2008).
pubmed: 18719097
pmcid: 2527874
doi: 10.1073/pnas.0802289105
Doki, S. et al. Structural basis for dynamic mechanism of proton-coupled symport by the peptide transporter POT. Proc. Natl. Acad. Sci. USA 110, 11343–11348 (2013).
Furutani, Y., Murata, T. & Kandori, H. Sodium or lithium ion-binding-induced structural changes in the K-ring of V-ATPase from Enterococcus hirae revealed by ATR-FTIR spectroscopy. J. Am. Chem. Soc. 133, 2860–2863 (2011).
pubmed: 21319823
doi: 10.1021/ja1116414
Katayama, K. et al. “In situ” observation of the role of chloride ion binding to monkey green sensitive visual pigment by ATR-FTIR spectroscopy. Phys. Chem. Chem. Phys. 20, 3381–3387 (2018).
pubmed: 29297909
doi: 10.1039/C7CP07277E
Katayama, K., Nakamura, S., Sasaki, T., Imai, H. & Kandori, H. Role of Gln114 in spectral tuning of a long-wavelength sensitive visual pigment. Biochemistry 58, 2944–2952 (2019).
pubmed: 31144811
doi: 10.1021/acs.biochem.9b00340
Katayama, K. et al. Ligand binding-induced structural changes in the M
pubmed: 31692352
doi: 10.1021/acs.jpclett.9b02942
Ballesteros, J. A. & Weinstein, H. Integrated methods for the construction of three-dimensional models and computational probing of structure-function relationships in G protein-coupled receptors. Methods Neurosci. 25, 336–428 (1995).
Langmead, C. J. & Christopoulos, A. Supra-physiological efficacy at GPCRs: superstition or super agonists? Br. J. Pharmacol. 169, 353–356 (2013).
pubmed: 23441648
pmcid: 3651661
doi: 10.1111/bph.12142
Heitz, F. et al. Site-directed mutagenesis of the putative human muscarinic M
pubmed: 10513578
doi: 10.1016/S0014-2999(99)00439-2
Inoue, A. et al. Illuminating G-protein-coupling selectivity of GPCRs. Cell 177, 1933–1947 (2019).
pubmed: 31160049
pmcid: 6773469
doi: 10.1016/j.cell.2019.04.044
Goormaghtign, E., Cabiaux, V. & Ruysschaert, J. M. Determination of soluble and membrane protein structure by Fourier transform infrared spectroscopy. Subcell. Biochem. 23, 405–450 (1994).
doi: 10.1007/978-1-4615-1863-1_10
Suzuki, K. et al. Vibrational analysis of acetylcholine binding to the M
pubmed: 35423811
pmcid: 8696876
doi: 10.1039/D1RA01030A
Cheng, K. et al. Lithocholylcholine, a bile acid/acetylcholine hybrid, is a muscarinic receptor antagonist. J. Pharmacol. Exp. Ther. 303, 29–35 (2002).
pubmed: 12235229
doi: 10.1124/jpet.102.036376
Kashihara, K., Varga, E. V., Waite, S. L., Roeske, W. R. & Yamamura, H. I. Cloning of the rat m3, m4 and m5 muscarinic acetylcholine receptor genes by the Polymerase Chain Reaction (PCR) and the pharmacological characterization of the expressed genes. Life Sci. 51, 955–971 (1992).
pubmed: 1325587
doi: 10.1016/0024-3205(92)90403-C
Kovacs, I., Yamamura, H. I., Waite, S. L., Varga, E. V. & Roeske, W. R. Pharmacological comparison of the cloned human and rat M
pubmed: 9454790
Shannon, H. E. et al. Xanomeline: a novel muscarinic receptor agonist with functional selectivity for M
pubmed: 7909557
Jakubík, J., El-Fakahany, E. E. & Dolezal, V. Differences in kinetics of xanomeline binding and selectivity of activation of G proteins at M
pubmed: 16675658
doi: 10.1124/mol.106.023762
Maeda, S. et al. Structure and selectivity engineering of the M
pubmed: 32646996
pmcid: 7954660
doi: 10.1126/science.aax2517
Thal, D. M. et al. Crystal structures of the M1 and M4 muscarinic acetylcholine receptors. Nature 531, 335–340 (2016).
pubmed: 26958838
pmcid: 4915387
doi: 10.1038/nature17188
Yin, W. et al. Crystal structure of the human 5-HT
doi: 10.1038/s41421-018-0009-2
Katayama, K. et al. Vibrational spectroscopy analysis of ligand efficacy in human M2 muscarinic acetylcholine receptor (M2R).xlsx. figshare. Dataset. https://doi.org/10.6084/m9.figshare.16608511.v1 (2021).