Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide

Abstract Ionotropic glycine receptors (GlyRs) are chloride-permeable ligand-gated ion channels expressed in the nervous system. Alterations to glycinergic inhibition and the generation of dysfunctional GlyRs have been linked to chronic pain, a widely prevalent disease. Positive allosteric modulators...

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Main Authors: César O. Lara, Carlos F. Burgos, Katherine Fariña-Oliva, Ana M. Marileo, Victoria P. San Martín, David Flaig, Paul Soto-Ortega, Omayra V. Contreras, Anggelo Sazo, Krishna Gaete-Riquelme, Jeremías Corradi, Carola Muñoz-Montesino, Jorge Fuentealba, Patricio A. Castro, Luis G. Aguayo, Cecilia Bouzat, Gustavo Moraga-Cid, Gonzalo E. Yévenes
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Language:English
Published: Nature Portfolio 2025-02-01
Series:Scientific Reports
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Online Access:https://doi.org/10.1038/s41598-025-90209-7
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author César O. Lara
Carlos F. Burgos
Katherine Fariña-Oliva
Ana M. Marileo
Victoria P. San Martín
David Flaig
Paul Soto-Ortega
Omayra V. Contreras
Anggelo Sazo
Krishna Gaete-Riquelme
Jeremías Corradi
Carola Muñoz-Montesino
Jorge Fuentealba
Patricio A. Castro
Luis G. Aguayo
Cecilia Bouzat
Gustavo Moraga-Cid
Gonzalo E. Yévenes
author_facet César O. Lara
Carlos F. Burgos
Katherine Fariña-Oliva
Ana M. Marileo
Victoria P. San Martín
David Flaig
Paul Soto-Ortega
Omayra V. Contreras
Anggelo Sazo
Krishna Gaete-Riquelme
Jeremías Corradi
Carola Muñoz-Montesino
Jorge Fuentealba
Patricio A. Castro
Luis G. Aguayo
Cecilia Bouzat
Gustavo Moraga-Cid
Gonzalo E. Yévenes
author_sort César O. Lara
collection DOAJ
description Abstract Ionotropic glycine receptors (GlyRs) are chloride-permeable ligand-gated ion channels expressed in the nervous system. Alterations to glycinergic inhibition and the generation of dysfunctional GlyRs have been linked to chronic pain, a widely prevalent disease. Positive allosteric modulators (PAMs) targeting GlyRs exerted analgesic effects, motivating research on glycinergic PAMs as potential pain therapies. Rationally designed tricyclic sulfonamides are novel glycinergic PAMs with analgesic activity. However, detailed electrophysiological studies on these PAMs are still limited, and the GlyR binding site structural data has not been yet validated by mutational studies. Here, we combined electrophysiology and bioinformatics to systematically study the AM-1488 actions, a prototypical tricyclic sulfonamide, on recombinant GlyRs. We determined that AM-1488 is a potent, non-selective PAM of mammalian GlyR subtypes. In addition, the compound displayed agonistic activity, with partial preference for α1GlyRs. Single channel assays revealed that the compound increased the channel open probability without changing conductance. Mutational analyses on the tricyclic sulfonamide site confirm the molecular determinants contributing to functional activity. Our findings further define the mechanistic framework underlying the GlyR modulation by this PAM class, suggesting that further structure-driven exploration within the tricyclic sulfonamide site may originate novel glycinergic modulators for future development.
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spelling doaj-art-119d8e99c6764f98b3ee4d3d7bf8dccd2025-08-20T02:13:02ZengNature PortfolioScientific Reports2045-23222025-02-0115111510.1038/s41598-025-90209-7Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamideCésar O. Lara0Carlos F. Burgos1Katherine Fariña-Oliva2Ana M. Marileo3Victoria P. San Martín4David Flaig5Paul Soto-Ortega6Omayra V. Contreras7Anggelo Sazo8Krishna Gaete-Riquelme9Jeremías Corradi10Carola Muñoz-Montesino11Jorge Fuentealba12Patricio A. Castro13Luis G. Aguayo14Cecilia Bouzat15Gustavo Moraga-Cid16Gonzalo E. Yévenes17Department of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartament of Biology, Biochemistry and Pharmacy, Instituto de Investigaciones Bioquímicas de Bahía Blanca (INIBIBB), Universidad Nacional del Sur-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Department of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartament of Biology, Biochemistry and Pharmacy, Instituto de Investigaciones Bioquímicas de Bahía Blanca (INIBIBB), Universidad Nacional del Sur-Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET)Department of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionDepartment of Physiology, Faculty of Biological Sciences, Universidad de ConcepcionAbstract Ionotropic glycine receptors (GlyRs) are chloride-permeable ligand-gated ion channels expressed in the nervous system. Alterations to glycinergic inhibition and the generation of dysfunctional GlyRs have been linked to chronic pain, a widely prevalent disease. Positive allosteric modulators (PAMs) targeting GlyRs exerted analgesic effects, motivating research on glycinergic PAMs as potential pain therapies. Rationally designed tricyclic sulfonamides are novel glycinergic PAMs with analgesic activity. However, detailed electrophysiological studies on these PAMs are still limited, and the GlyR binding site structural data has not been yet validated by mutational studies. Here, we combined electrophysiology and bioinformatics to systematically study the AM-1488 actions, a prototypical tricyclic sulfonamide, on recombinant GlyRs. We determined that AM-1488 is a potent, non-selective PAM of mammalian GlyR subtypes. In addition, the compound displayed agonistic activity, with partial preference for α1GlyRs. Single channel assays revealed that the compound increased the channel open probability without changing conductance. Mutational analyses on the tricyclic sulfonamide site confirm the molecular determinants contributing to functional activity. Our findings further define the mechanistic framework underlying the GlyR modulation by this PAM class, suggesting that further structure-driven exploration within the tricyclic sulfonamide site may originate novel glycinergic modulators for future development.https://doi.org/10.1038/s41598-025-90209-7Glycine receptorsAllosteric modulationElectrophysiologyMolecular modellingPharmacologyChronic pain
spellingShingle César O. Lara
Carlos F. Burgos
Katherine Fariña-Oliva
Ana M. Marileo
Victoria P. San Martín
David Flaig
Paul Soto-Ortega
Omayra V. Contreras
Anggelo Sazo
Krishna Gaete-Riquelme
Jeremías Corradi
Carola Muñoz-Montesino
Jorge Fuentealba
Patricio A. Castro
Luis G. Aguayo
Cecilia Bouzat
Gustavo Moraga-Cid
Gonzalo E. Yévenes
Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
Scientific Reports
Glycine receptors
Allosteric modulation
Electrophysiology
Molecular modelling
Pharmacology
Chronic pain
title Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
title_full Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
title_fullStr Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
title_full_unstemmed Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
title_short Allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
title_sort allosteric modulation and direct activation of glycine receptors by a tricyclic sulfonamide
topic Glycine receptors
Allosteric modulation
Electrophysiology
Molecular modelling
Pharmacology
Chronic pain
url https://doi.org/10.1038/s41598-025-90209-7
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