Article

Effects of site-directed mutagenesis of GLP-1 and glucagon receptors on signal transduction activated by dual and triple agonists

Sanaz Darbalaei1,2, Ru-lue Chang3, Qing-tong Zhou4, Yan Chen4, An-tao Dai1, Ming-wei Wang3,4,5,6, De-hua Yang1,2,5
1 The National Center for Drug Screening and CAS Key Laboratory of Receptor Research, Shanghai Institute of Materia Medica, Chinese Academy of Sciences (CAS), Shanghai 201203, China
2 University of Chinese Academy of Sciences, Beijing 100049, China
3 School of Pharmacy, Fudan University, Shanghai 201203, China
4 Department of Pharmacology, School of Basic Medical Sciences, Fudan University, Shanghai 200032, China
5 Research Center for Deepsea Bioresources, Sanya 572025, China
6 Department of Chemistry, School of Science, The University of Tokyo, Tokyo 113-0033, Japan
Correspondence to: Ming-wei Wang: mwwang@simm.ac.cn, De-hua Yang: dhyang@simm.ac.cn,
DOI: 10.1038/s41401-022-00962-y
Received: 21 April 2022
Accepted: 17 July 2022
Advance online: 11 August 2022

Abstract

The paradigm of one drug against multiple targets, known as unimolecular polypharmacology, offers the potential to improve efficacy while overcoming some adverse events associated with the treatment. This approach is best exemplified by targeting two or three class B1 G protein-coupled receptors, namely, glucagon-like peptide-1 receptor (GLP-1R), glucagon receptor (GCGR) and glucose-dependent insulinotropic polypeptide receptor for treatment of type 2 diabetes and obesity. Some of the dual and triple agonists have already shown initial successes in clinical trials, although the molecular mechanisms underlying their multiplexed pharmacology remain elusive. In this study we employed structure-based site-directed mutagenesis together with pharmacological assays to compare agonist efficacy across two key signaling pathways, cAMP accumulation and ERK1/2 phosphorylation (pERK1/2). Three dual agonists (peptide 15, MEDI0382 and SAR425899) and one triple agonist (peptide 20) were evaluated at GLP-1R and GCGR, relative to the native peptidic ligands (GLP-1 and glucagon). Our results reveal the existence of residue networks crucial for unimolecular agonist-mediated receptor activation and their distinct signaling patterns, which might be useful to the rational design of biased drug leads.
Keywords: glucagon-like peptide-1 receptor; glucagon receptor; dual and triple agonist; cAMP; pERK1/2; unimolecular polypharmacology

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