Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction

Abstract α3β glycine receptor (GlyR) is a subtype of GlyRs that belongs to the Cys-loop receptor superfamily. It is highly expressed in the spinal dorsal horn where sensory information is integrated. Under inflammatory conditions, the large unstructured intracellular M3/M4 loops of the α3 subunit ar...

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Main Authors: Xiaofen Liu, Malgorzata Krezel, Weiwei Wang
Format: Article
Language:English
Published: Nature Portfolio 2025-06-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60516-8
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author Xiaofen Liu
Malgorzata Krezel
Weiwei Wang
author_facet Xiaofen Liu
Malgorzata Krezel
Weiwei Wang
author_sort Xiaofen Liu
collection DOAJ
description Abstract α3β glycine receptor (GlyR) is a subtype of GlyRs that belongs to the Cys-loop receptor superfamily. It is highly expressed in the spinal dorsal horn where sensory information is integrated. Under inflammatory conditions, the large unstructured intracellular M3/M4 loops of the α3 subunit are phosphorylated through the prostaglandin E2 (PGE2) pathway, inhibiting ion conduction, and resulting in elevated pain sensation. A small molecule analgesic analog, 2,6-di-tert-butylphenol (2,6-DTBP) potentiates phosphorylated α3β GlyR through unclear mechanisms and relieves pain. Combining cryo-Electron Microscopy (cryo-EM) structures and single molecule Förster resonance energy transfer (smFRET) experiments, we show compaction of M3/M4 loop towards the ion conduction pore upon phosphorylation and further by 2,6-DTBP binding, which in turn modulates function through changing pore conformations and local electrostatics. We show that simultaneous interactions with the M3/M4 loop and the transmembrane domain (TM) is necessary for the potentiation of heteromeric α3β GlyR by 2,6-DTBP, while TM interaction alone is sufficient to potentiate homomeric α3 GlyR, explaining the mystery of why 2,6-DTBP potentiates only phosphorylated α3β GlyR. These findings show how post-translational modification of the unstructured intracellular M3/M4 loop may regulate Cys-loop receptor function, providing new perspectives in pain control and other pharmaceutical development targeting GlyRs and other Cys-loop receptors.
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spelling doaj-art-a9628f2deadd46ddadc498e4d13544352025-08-20T03:25:19ZengNature PortfolioNature Communications2041-17232025-06-0116111610.1038/s41467-025-60516-8Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interactionXiaofen Liu0Malgorzata Krezel1Weiwei Wang2Departments of Biophysics, University of Texas Southwestern Medical CenterDepartments of Biophysics, University of Texas Southwestern Medical CenterDepartments of Biophysics, University of Texas Southwestern Medical CenterAbstract α3β glycine receptor (GlyR) is a subtype of GlyRs that belongs to the Cys-loop receptor superfamily. It is highly expressed in the spinal dorsal horn where sensory information is integrated. Under inflammatory conditions, the large unstructured intracellular M3/M4 loops of the α3 subunit are phosphorylated through the prostaglandin E2 (PGE2) pathway, inhibiting ion conduction, and resulting in elevated pain sensation. A small molecule analgesic analog, 2,6-di-tert-butylphenol (2,6-DTBP) potentiates phosphorylated α3β GlyR through unclear mechanisms and relieves pain. Combining cryo-Electron Microscopy (cryo-EM) structures and single molecule Förster resonance energy transfer (smFRET) experiments, we show compaction of M3/M4 loop towards the ion conduction pore upon phosphorylation and further by 2,6-DTBP binding, which in turn modulates function through changing pore conformations and local electrostatics. We show that simultaneous interactions with the M3/M4 loop and the transmembrane domain (TM) is necessary for the potentiation of heteromeric α3β GlyR by 2,6-DTBP, while TM interaction alone is sufficient to potentiate homomeric α3 GlyR, explaining the mystery of why 2,6-DTBP potentiates only phosphorylated α3β GlyR. These findings show how post-translational modification of the unstructured intracellular M3/M4 loop may regulate Cys-loop receptor function, providing new perspectives in pain control and other pharmaceutical development targeting GlyRs and other Cys-loop receptors.https://doi.org/10.1038/s41467-025-60516-8
spellingShingle Xiaofen Liu
Malgorzata Krezel
Weiwei Wang
Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
Nature Communications
title Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
title_full Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
title_fullStr Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
title_full_unstemmed Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
title_short Mechanism of human α3β GlyR regulation by intracellular M3/M4 loop phosphorylation and 2,6-di-tert-butylphenol interaction
title_sort mechanism of human α3β glyr regulation by intracellular m3 m4 loop phosphorylation and 2 6 di tert butylphenol interaction
url https://doi.org/10.1038/s41467-025-60516-8
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