Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability

O-GlcNAcylation is an essential intracellular protein modification mediated by O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA). Recently, missense mutations in OGT have been linked to intellectual disability, indicating that this modification is important for the development and functioning of the...

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Main Authors: Ignacy Czajewski, Bijayalaxmi Swain, Jiawei Xu, Laurin McDowall, Andrew T Ferenbach, Daan MF van Aalten
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-11-01
Series:eLife
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Online Access:https://elifesciences.org/articles/90376
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author Ignacy Czajewski
Bijayalaxmi Swain
Jiawei Xu
Laurin McDowall
Andrew T Ferenbach
Daan MF van Aalten
author_facet Ignacy Czajewski
Bijayalaxmi Swain
Jiawei Xu
Laurin McDowall
Andrew T Ferenbach
Daan MF van Aalten
author_sort Ignacy Czajewski
collection DOAJ
description O-GlcNAcylation is an essential intracellular protein modification mediated by O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA). Recently, missense mutations in OGT have been linked to intellectual disability, indicating that this modification is important for the development and functioning of the nervous system. However, the processes that are most sensitive to perturbations in O-GlcNAcylation remain to be identified. Here, we uncover quantifiable phenotypes in the fruit fly Drosophila melanogaster carrying a patient-derived OGT mutation in the catalytic domain. Hypo-O-GlcNAcylation leads to defects in synaptogenesis and reduced sleep stability. Both these phenotypes can be partially rescued by genetically or chemically targeting OGA, suggesting that a balance of OGT/OGA activity is required for normal neuronal development and function.
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spelling doaj-art-3fab1c97f5ee4c279e3aa895209f4d0d2025-08-20T02:20:15ZengeLife Sciences Publications LtdeLife2050-084X2024-11-011310.7554/eLife.90376Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disabilityIgnacy Czajewski0https://orcid.org/0000-0002-1661-5806Bijayalaxmi Swain1https://orcid.org/0000-0003-0885-0395Jiawei Xu2Laurin McDowall3Andrew T Ferenbach4Daan MF van Aalten5https://orcid.org/0000-0002-1499-6908Division of Molecular, Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dundee, United KingdomSection of Neurobiology and DANDRITE, Department of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkSection of Neurobiology and DANDRITE, Department of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkDivision of Molecular, Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dundee, United KingdomDivision of Molecular, Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dundee, United Kingdom; Section of Neurobiology and DANDRITE, Department of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkDivision of Molecular, Cell and Developmental Biology, School of Life Sciences, University of Dundee, Dundee, United Kingdom; Section of Neurobiology and DANDRITE, Department of Molecular Biology and Genetics, Aarhus University, Aarhus, DenmarkO-GlcNAcylation is an essential intracellular protein modification mediated by O-GlcNAc transferase (OGT) and O-GlcNAcase (OGA). Recently, missense mutations in OGT have been linked to intellectual disability, indicating that this modification is important for the development and functioning of the nervous system. However, the processes that are most sensitive to perturbations in O-GlcNAcylation remain to be identified. Here, we uncover quantifiable phenotypes in the fruit fly Drosophila melanogaster carrying a patient-derived OGT mutation in the catalytic domain. Hypo-O-GlcNAcylation leads to defects in synaptogenesis and reduced sleep stability. Both these phenotypes can be partially rescued by genetically or chemically targeting OGA, suggesting that a balance of OGT/OGA activity is required for normal neuronal development and function.https://elifesciences.org/articles/90376O-GlcNAcylationdevelopmentintellectual disabilitypost-translational modificationsdisease models
spellingShingle Ignacy Czajewski
Bijayalaxmi Swain
Jiawei Xu
Laurin McDowall
Andrew T Ferenbach
Daan MF van Aalten
Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
eLife
O-GlcNAcylation
development
intellectual disability
post-translational modifications
disease models
title Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
title_full Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
title_fullStr Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
title_full_unstemmed Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
title_short Rescuable sleep and synaptogenesis phenotypes in a Drosophila model of O-GlcNAc transferase intellectual disability
title_sort rescuable sleep and synaptogenesis phenotypes in a drosophila model of o glcnac transferase intellectual disability
topic O-GlcNAcylation
development
intellectual disability
post-translational modifications
disease models
url https://elifesciences.org/articles/90376
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