A group of cationic amphiphilic drugs activates MRGPRX2 and induces scratching behavior in mice.


Journal

The Journal of allergy and clinical immunology
ISSN: 1097-6825
Titre abrégé: J Allergy Clin Immunol
Pays: United States
ID NLM: 1275002

Informations de publication

Date de publication:
08 2021
Historique:
received: 28 04 2020
revised: 10 11 2020
accepted: 28 12 2020
pubmed: 23 2 2021
medline: 21 10 2021
entrez: 22 2 2021
Statut: ppublish

Résumé

Mas gene-related G protein-coupled receptors (MRGPRs) are a G protein-coupled receptor family responsive to various exogenous and endogenous agonists, playing a fundamental role in pain and itch sensation. The primate-specific family member MRGPRX2 and its murine orthologue MRGPRB2 are expressed by mast cells mediating IgE-independent signaling and pseudoallergic drug reactions. Our aim was to increase knowledge about the function and regulation of MRGPRX2/MRGPRB2, which is of major importance in prevention of drug hypersensitivity reactions and drug-induced pruritus. To identify novel MRGPR (ant)agonists, we screened a library of pharmacologically active compounds by utilizing a high-throughput calcium mobilization assay. The identified hit compounds were analyzed for their pseudoallergic and pruritogenic effects in mice and human. We found a class of commonly used drugs activating MRGPRX2 that, to a large extent, consists of antidepressants, antiallergic drugs, and antipsychotics. Three-dimensional pharmacophore modeling revealed structural similarities of the identified agonists, classifying them as cationic amphiphilic drugs. Mast cell activation was investigated by using the 3 representatively selected antidepressants clomipramine, paroxetine, and desipramine. Indeed, we were able to show a concentration-dependent activation and MRGPRX2-dependent degranulation of the human mast cell line LAD2 (Laboratory of Allergic Diseases-2). Furthermore, clomipramine, paroxetine, and desipramine were able to induce degranulation of human skin and murine peritoneal mast cells. These substances elicited dose-dependent scratching behavior following intradermal injection into C57BL/6 mice but less so in MRGPRB2-mutant mice, as well as wheal-and-flare reactions following intradermal injections in humans. Our results contribute to the characterization of structure-activity relationships and functionality of MRGPRX2 ligands and facilitate prediction of adverse reactions such as drug-induced pruritus to prevent severe drug hypersensitivity reactions.

Sections du résumé

BACKGROUND
Mas gene-related G protein-coupled receptors (MRGPRs) are a G protein-coupled receptor family responsive to various exogenous and endogenous agonists, playing a fundamental role in pain and itch sensation. The primate-specific family member MRGPRX2 and its murine orthologue MRGPRB2 are expressed by mast cells mediating IgE-independent signaling and pseudoallergic drug reactions.
OBJECTIVES
Our aim was to increase knowledge about the function and regulation of MRGPRX2/MRGPRB2, which is of major importance in prevention of drug hypersensitivity reactions and drug-induced pruritus.
METHODS
To identify novel MRGPR (ant)agonists, we screened a library of pharmacologically active compounds by utilizing a high-throughput calcium mobilization assay. The identified hit compounds were analyzed for their pseudoallergic and pruritogenic effects in mice and human.
RESULTS
We found a class of commonly used drugs activating MRGPRX2 that, to a large extent, consists of antidepressants, antiallergic drugs, and antipsychotics. Three-dimensional pharmacophore modeling revealed structural similarities of the identified agonists, classifying them as cationic amphiphilic drugs. Mast cell activation was investigated by using the 3 representatively selected antidepressants clomipramine, paroxetine, and desipramine. Indeed, we were able to show a concentration-dependent activation and MRGPRX2-dependent degranulation of the human mast cell line LAD2 (Laboratory of Allergic Diseases-2). Furthermore, clomipramine, paroxetine, and desipramine were able to induce degranulation of human skin and murine peritoneal mast cells. These substances elicited dose-dependent scratching behavior following intradermal injection into C57BL/6 mice but less so in MRGPRB2-mutant mice, as well as wheal-and-flare reactions following intradermal injections in humans.
CONCLUSION
Our results contribute to the characterization of structure-activity relationships and functionality of MRGPRX2 ligands and facilitate prediction of adverse reactions such as drug-induced pruritus to prevent severe drug hypersensitivity reactions.

Identifiants

pubmed: 33617860
pii: S0091-6749(21)00229-3
doi: 10.1016/j.jaci.2020.12.655
pii:
doi:

Substances chimiques

Antidepressive Agents 0
MRGPRX2 protein, human 0
Mrgprx2 protein, mouse 0
Nerve Tissue Proteins 0
Receptors, G-Protein-Coupled 0
Receptors, Neuropeptide 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

506-522.e8

Informations de copyright

Copyright © 2021 American Academy of Allergy, Asthma & Immunology. Published by Elsevier Inc. All rights reserved.

Auteurs

Katharina Wolf (K)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany. Electronic address: katharina.b.wolf@fau.de.

Helen Kühn (H)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Felicitas Boehm (F)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Lisa Gebhardt (L)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Markus Glaudo (M)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Konstantin Agelopoulos (K)

Center for Chronic Pruritus, Department of Dermatology, University of Münster, Munich, Germany.

Sonja Ständer (S)

Center for Chronic Pruritus, Department of Dermatology, University of Münster, Munich, Germany.

Philipp Ectors (P)

Computer Chemistry Center, Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Dirk Zahn (D)

Computer Chemistry Center, Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Yvonne K Riedel (YK)

PharmaCenter Bonn, Pharmaceutical Institute, Pharmaceutical & Medicinal Chemistry, University of Bonn, Bonn, Germany.

Dominik Thimm (D)

PharmaCenter Bonn, Pharmaceutical Institute, Pharmaceutical & Medicinal Chemistry, University of Bonn, Bonn, Germany.

Christa E Müller (CE)

PharmaCenter Bonn, Pharmaceutical Institute, Pharmaceutical & Medicinal Chemistry, University of Bonn, Bonn, Germany.

Sascha Kretschmann (S)

Department of Medicine 5, Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Anita N Kremer (AN)

Department of Medicine 5, Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Daphne Chien (D)

Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Md.

Nathachit Limjunyawong (N)

Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Md.

Qi Peng (Q)

Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Md.

Xinzhong Dong (X)

Solomon H. Snyder Department of Neuroscience, The Johns Hopkins University School of Medicine, Baltimore, Md.

Pavel Kolkhir (P)

I.M. Sechenov First Moscow State Medical University (Sechenov University), Division of Immune-Mediated Skin Diseases, Moscow, Russia; Dermatological Allergology, Allergie-Centrum-Charité, Department of Dermatology and Allergology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.

Jörg Scheffel (J)

Dermatological Allergology, Allergie-Centrum-Charité, Department of Dermatology and Allergology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.

Mia Lykke Søgaard (ML)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Benno Weigmann (B)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany.

Markus F Neurath (MF)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany; German Center for Immunotherapy-Deutsches Zentrum Immuntherapie (DZI), Erlangen, Germany.

Tomasz Hawro (T)

Dermatological Allergology, Allergie-Centrum-Charité, Department of Dermatology and Allergology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.

Martin Metz (M)

Dermatological Allergology, Allergie-Centrum-Charité, Department of Dermatology and Allergology, Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, and Berlin Institute of Health, Berlin, Germany.

Michael J M Fischer (MJM)

Center for Physiology and Pharmacology, University of Vienna, Vienna, Austria.

Andreas E Kremer (AE)

Department of Medicine 1, University Hospital Erlangen and Friedrich-Alexander-University Erlangen-Nürnberg, Nuremberg, Germany. Electronic address: andreas.kremer@uk-erlangen.de.

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Classifications MeSH