Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment

Abstract Best1 and Best2 are two members of the bestrophin family of anion channels critically involved in the prevention of retinal degeneration and maintenance of intraocular pressure, respectively. Here, we solved glutamate- and γ-aminobutyric acid (GABA)-bound Best2 structures, which delineate a...

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Main Authors: Aaron P. Owji, Jingyun Dong, Alec Kittredge, Jiali Wang, Yu Zhang, Tingting Yang
Format: Article
Language:English
Published: Nature Portfolio 2024-12-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-54938-z
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author Aaron P. Owji
Jingyun Dong
Alec Kittredge
Jiali Wang
Yu Zhang
Tingting Yang
author_facet Aaron P. Owji
Jingyun Dong
Alec Kittredge
Jiali Wang
Yu Zhang
Tingting Yang
author_sort Aaron P. Owji
collection DOAJ
description Abstract Best1 and Best2 are two members of the bestrophin family of anion channels critically involved in the prevention of retinal degeneration and maintenance of intraocular pressure, respectively. Here, we solved glutamate- and γ-aminobutyric acid (GABA)-bound Best2 structures, which delineate an intracellular glutamate binding site and an extracellular GABA binding site on Best2, respectively, identified extracellular GABA as a permeable activator of Best2, and elucidated the co-regulation of Best2 by glutamate, GABA and glutamine synthetase in vivo. We further identified multiple small molecules as activators of the bestrophin channels. Extensive analyses were carried out for a potent activator, 4-aminobenzoic acid (PABA): PABA-bound Best1 and Best2 structures are solved and illustrate the same binding site as in GABA-bound Best2; PABA treatment rescues the functional deficiency of patient-derived Best1 mutations. Together, our results demonstrate the mechanism and potential of multiple small molecule candidates as clinically applicable drugs for bestrophin-associated diseases/conditions.
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issn 2041-1723
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record_format Article
series Nature Communications
spelling doaj-art-b5bf1810ca514d98bba32bc385eccbf72025-08-20T02:53:50ZengNature PortfolioNature Communications2041-17232024-12-0115111010.1038/s41467-024-54938-zNeurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatmentAaron P. Owji0Jingyun Dong1Alec Kittredge2Jiali Wang3Yu Zhang4Tingting Yang5Department of Ophthalmology, Columbia UniversityDepartment of Ophthalmology, Columbia UniversityDepartment of Ophthalmology, Columbia UniversityDepartment of Ophthalmology, Columbia UniversityDepartment of Ophthalmology, Columbia UniversityDepartment of Ophthalmology, Columbia UniversityAbstract Best1 and Best2 are two members of the bestrophin family of anion channels critically involved in the prevention of retinal degeneration and maintenance of intraocular pressure, respectively. Here, we solved glutamate- and γ-aminobutyric acid (GABA)-bound Best2 structures, which delineate an intracellular glutamate binding site and an extracellular GABA binding site on Best2, respectively, identified extracellular GABA as a permeable activator of Best2, and elucidated the co-regulation of Best2 by glutamate, GABA and glutamine synthetase in vivo. We further identified multiple small molecules as activators of the bestrophin channels. Extensive analyses were carried out for a potent activator, 4-aminobenzoic acid (PABA): PABA-bound Best1 and Best2 structures are solved and illustrate the same binding site as in GABA-bound Best2; PABA treatment rescues the functional deficiency of patient-derived Best1 mutations. Together, our results demonstrate the mechanism and potential of multiple small molecule candidates as clinically applicable drugs for bestrophin-associated diseases/conditions.https://doi.org/10.1038/s41467-024-54938-z
spellingShingle Aaron P. Owji
Jingyun Dong
Alec Kittredge
Jiali Wang
Yu Zhang
Tingting Yang
Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
Nature Communications
title Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
title_full Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
title_fullStr Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
title_full_unstemmed Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
title_short Neurotransmitter-bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
title_sort neurotransmitter bound bestrophin channel structures reveal small molecule drug targeting sites for disease treatment
url https://doi.org/10.1038/s41467-024-54938-z
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