Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)

With the objective of finding new classes of cognitive enhancers with potential for the treatment of neurodegenerative disorders, such as Alzheimer's disease, small molecule inhibitors of insulin-regulated aminopeptidase (IRAP) were designed and synthesized. IRAP is a member of the M1 family of...

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Main Authors: Julia Beveridge, Marcus Söderström, Rubén Prieto-Díaz, Hugo Gutierrez-de-Teran, Luke R. Odell, Mathias Hallberg, Mats Larhed, Johan Gising
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:European Journal of Medicinal Chemistry Reports
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Online Access:http://www.sciencedirect.com/science/article/pii/S2772417424000876
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author Julia Beveridge
Marcus Söderström
Rubén Prieto-Díaz
Hugo Gutierrez-de-Teran
Luke R. Odell
Mathias Hallberg
Mats Larhed
Johan Gising
author_facet Julia Beveridge
Marcus Söderström
Rubén Prieto-Díaz
Hugo Gutierrez-de-Teran
Luke R. Odell
Mathias Hallberg
Mats Larhed
Johan Gising
author_sort Julia Beveridge
collection DOAJ
description With the objective of finding new classes of cognitive enhancers with potential for the treatment of neurodegenerative disorders, such as Alzheimer's disease, small molecule inhibitors of insulin-regulated aminopeptidase (IRAP) were designed and synthesized. IRAP is a member of the M1 family of zinc aminopeptidases and is abundantly expressed in areas of the brain associated with cognition, such as the amygdala, hippocampus and cerebral cortex. IRAP inhibitors were previously shown to enhance memory and learning in animal models. A comprehensive high throughput screening of 400,000 small molecules from the European Lead Factory library provided a series of 50 promising compounds in a qualified hit list (QHL). More than 30 IRAP inhibitors with an IC50 below 3.5 μM were identified. Herein, selected compounds from this QHL were assayed for solubility and permeability. Most of the selected compounds displayed good solubility, but further permeability studies on the best compounds revealed low blood brain barrier (BBB) permeability and high efflux in cells overexpressing P-gp pumps, rendering them less promising as starting points in drug discovery processes. Two compounds from the QHL were prioritized for further structural optimization; the pyridyl-substituted isoxazole 1a (QHL27) and the benzylhydroxamic acid derivative 1b (QHL1), both demonstrating fair BBB permeability and no indication of efflux. While our attempts to improve the isoxazole derivative 1a were not fruitful, a structural modification of 1b to provide the chloro-substituted benzylhydroxamic acid 14b resulted in a ten-fold improvement of the IRAP inhibition with an IC50 value of 60 nM. The binding modes of 1b and 14b were determined by free energy perturbation (FEP) analysis performed on candidate docking poses, determining a binding mode that accurately explained the experimental SAR. Further FEP studies of compound 14b suggested that it exhibits selectivity towards IRAP over Aminopeptidase N (APN), indicating its potential for targeted therapeutic applications.
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spelling doaj-art-2b4f75b325c64fd7b9368d76b8f085c02024-12-05T05:21:56ZengElsevierEuropean Journal of Medicinal Chemistry Reports2772-41742024-12-0112100215Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)Julia Beveridge0Marcus Söderström1Rubén Prieto-Díaz2Hugo Gutierrez-de-Teran3Luke R. Odell4Mathias Hallberg5Mats Larhed6Johan Gising7The Beijer Laboratory, Science for Life Laboratory, Department of Medicinal Chemistry, Biomedical Centre, Uppsala University, P.O. Box 574, SE-751 23, Uppsala, SwedenThe Beijer Laboratory, Science for Life Laboratory, Department of Medicinal Chemistry, Biomedical Centre, Uppsala University, P.O. Box 574, SE-751 23, Uppsala, SwedenDepartment of Cell and Molecular Biology, Biomedical Centre, Uppsala University, P.O. Box 596, SE-751 24, Uppsala, SwedenDepartment of Cell and Molecular Biology, Biomedical Centre, Uppsala University, P.O. Box 596, SE-751 24, Uppsala, SwedenDepartment of Medicinal Chemistry, Biomedical Centre, Uppsala University, P.O. Box 574, SE-751 23, Uppsala, SwedenThe Beijer Laboratory, Department of Pharmaceutical Biosciences, Neuropharmacology and Addiction Research, Biomedical Centre, Uppsala University, P.O. Box 591, SE-751 24, Uppsala, SwedenThe Beijer Laboratory, Science for Life Laboratory, Department of Medicinal Chemistry, Biomedical Centre, Uppsala University, P.O. Box 574, SE-751 23, Uppsala, Sweden; Corresponding author.The Beijer Laboratory, Science for Life Laboratory, Department of Medicinal Chemistry, Biomedical Centre, Uppsala University, P.O. Box 574, SE-751 23, Uppsala, Sweden; Corresponding author.With the objective of finding new classes of cognitive enhancers with potential for the treatment of neurodegenerative disorders, such as Alzheimer's disease, small molecule inhibitors of insulin-regulated aminopeptidase (IRAP) were designed and synthesized. IRAP is a member of the M1 family of zinc aminopeptidases and is abundantly expressed in areas of the brain associated with cognition, such as the amygdala, hippocampus and cerebral cortex. IRAP inhibitors were previously shown to enhance memory and learning in animal models. A comprehensive high throughput screening of 400,000 small molecules from the European Lead Factory library provided a series of 50 promising compounds in a qualified hit list (QHL). More than 30 IRAP inhibitors with an IC50 below 3.5 μM were identified. Herein, selected compounds from this QHL were assayed for solubility and permeability. Most of the selected compounds displayed good solubility, but further permeability studies on the best compounds revealed low blood brain barrier (BBB) permeability and high efflux in cells overexpressing P-gp pumps, rendering them less promising as starting points in drug discovery processes. Two compounds from the QHL were prioritized for further structural optimization; the pyridyl-substituted isoxazole 1a (QHL27) and the benzylhydroxamic acid derivative 1b (QHL1), both demonstrating fair BBB permeability and no indication of efflux. While our attempts to improve the isoxazole derivative 1a were not fruitful, a structural modification of 1b to provide the chloro-substituted benzylhydroxamic acid 14b resulted in a ten-fold improvement of the IRAP inhibition with an IC50 value of 60 nM. The binding modes of 1b and 14b were determined by free energy perturbation (FEP) analysis performed on candidate docking poses, determining a binding mode that accurately explained the experimental SAR. Further FEP studies of compound 14b suggested that it exhibits selectivity towards IRAP over Aminopeptidase N (APN), indicating its potential for targeted therapeutic applications.http://www.sciencedirect.com/science/article/pii/S2772417424000876Insulin Regulated AminopeptidaseInhibitorsHydroxamic acidsFree energy perturbationsStructure activity relationships
spellingShingle Julia Beveridge
Marcus Söderström
Rubén Prieto-Díaz
Hugo Gutierrez-de-Teran
Luke R. Odell
Mathias Hallberg
Mats Larhed
Johan Gising
Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
European Journal of Medicinal Chemistry Reports
Insulin Regulated Aminopeptidase
Inhibitors
Hydroxamic acids
Free energy perturbations
Structure activity relationships
title Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
title_full Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
title_fullStr Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
title_full_unstemmed Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
title_short Benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase (IRAP)
title_sort benzylhydroxamic acids as inhibitors of insulin regulated aminopeptidase irap
topic Insulin Regulated Aminopeptidase
Inhibitors
Hydroxamic acids
Free energy perturbations
Structure activity relationships
url http://www.sciencedirect.com/science/article/pii/S2772417424000876
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