Ligand-Specific Allosteric Coupling Controls G-Protein-Coupled Receptor Signaling

J. Holze, M. Bermudez, E.M. Pfeil, M. Kauk, T. Bödefeld, M. Irmen, C. Matera, C. Dallanoce, M. De Amici, U. Holzgrabe, G.M. König, C. Tränkle, G. Wolber, R. Schrage, K. Mohr, C. Hoffmann, E. Kostenis, A. Bock

Research output: Contribution to JournalArticleAcademicpeer-review

Abstract

Copyright © 2020 American Chemical Society.Allosteric coupling describes a reciprocal process whereby G-protein-coupled receptors (GPCRs) relay ligand-induced conformational changes from the extracellular binding pocket to the intracellular signaling surface. Therefore, GPCR activation is sensitive to both the type of extracellular ligand and intracellular signaling protein. We hypothesized that ligand-specific allosteric coupling may result in preferential (i.e., biased) engagement of downstream effectors. However, the structural basis underlying ligand-dependent control of this essential allosteric mechanism is poorly understood. Here, we show that two sets of extended muscarinic acetylcholine receptor M1 agonists, which only differ in linker length, progressively constrain receptor signaling. We demonstrate that stepwise shortening of their chemical linker gradually hampers binding pocket closure, resulting in divergent coupling to distinct G-protein families. Our data provide an experimental strategy for the design of ligands with selective G-protein recognition and reveal a potentially general mechanism of ligand-specific allosteric coupling.
Original languageEnglish
Pages (from-to)859-867
JournalACS Pharmacology and Translational Science
Volume3
Issue number5
DOIs
Publication statusPublished - 9 Oct 2020
Externally publishedYes

Funding

We thank Arthur Christopoulos (Monash University, Melbourne, Australia) for providing the stable CHO-M1 W400A cell line, and Iris Jusen and Dieter Baumert (both University of Bonn) for technical assistance. M.B. acknowledges funding by the Deutsche Forschungsgemeinschaft (German Research Foundation, Project Number 407626949) and support by the Joachim Herz Stiftung. E.P. is funded by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation), 214362475/GRK1873/2. E.K. and G.M.K. gratefully acknowledge support of this work by the DFG-funded Research Unit FOR2372 with the Grants KO 1582/10-1 and KO 1582/10-2 (to E.K), as well as KO 902/17-1 and KO 902/17-2 (to G.M.K.). A.B. acknowledges funding by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation) through SFB1423, Project Number 421152132, subproject C05. 7.35

FundersFunder number
DFG-funded7.35, SFB1423, 421152132, KO 1582/10-1, KO 1582/10-2, KO 902/17-2, KO 902/17-1
Joachim Herz Stiftung214362475/GRK1873/2
Deutsche Forschungsgemeinschaft407626949

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