Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.

Glycosphingolipids (GSL) are important bioactive membrane components. GSLs containing sialic acids, known as gangliosides, are highly abundant in the brain and diseases of ganglioside metabolism cause severe early-onset neurodegeneration. The ganglioside GM2 is processed by β-hexosaminidase A and wh...

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Main Authors: Alex S Nicholson, David A Priestman, Robin Antrobus, James C Williamson, Reuben Bush, Shannon J McKie, Henry G Barrow, Emily Smith, Kostantin Dobrenis, Nicholas A Bright, Frances M Platt, Janet E Deane
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2025-07-01
Series:PLoS Biology
Online Access:https://doi.org/10.1371/journal.pbio.3003265
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author Alex S Nicholson
David A Priestman
Robin Antrobus
James C Williamson
Reuben Bush
Shannon J McKie
Henry G Barrow
Emily Smith
Kostantin Dobrenis
Nicholas A Bright
Frances M Platt
Janet E Deane
author_facet Alex S Nicholson
David A Priestman
Robin Antrobus
James C Williamson
Reuben Bush
Shannon J McKie
Henry G Barrow
Emily Smith
Kostantin Dobrenis
Nicholas A Bright
Frances M Platt
Janet E Deane
author_sort Alex S Nicholson
collection DOAJ
description Glycosphingolipids (GSL) are important bioactive membrane components. GSLs containing sialic acids, known as gangliosides, are highly abundant in the brain and diseases of ganglioside metabolism cause severe early-onset neurodegeneration. The ganglioside GM2 is processed by β-hexosaminidase A and when non-functional GM2 accumulates causing Tay-Sachs and Sandhoff diseases. We have developed i3Neuron-based disease models demonstrating storage of GM2 and severe endolysosomal dysfunction. Additionally, the plasma membrane (PM) is significantly altered in its lipid and protein composition. These changes are driven in part by lysosomal exocytosis causing inappropriate accumulation of lysosomal proteins on the cell surface. There are also significant changes in synaptic protein abundances with direct functional impact on neuronal activity. Lysosomal proteins are also enriched at the PM in GM1 gangliosidosis supporting that lysosomal exocytosis is a conserved mechanism of PM proteome change in these diseases. This work provides mechanistic insights into neuronal dysfunction in gangliosidoses highlighting that these are severe PM disorders with implications for other lysosomal and neurodegenerative diseases.
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issn 1544-9173
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publishDate 2025-07-01
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spelling doaj-art-9c39efa0a0e64c5587e349177be697ac2025-08-20T03:27:43ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852025-07-01237e300326510.1371/journal.pbio.3003265Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.Alex S NicholsonDavid A PriestmanRobin AntrobusJames C WilliamsonReuben BushShannon J McKieHenry G BarrowEmily SmithKostantin DobrenisNicholas A BrightFrances M PlattJanet E DeaneGlycosphingolipids (GSL) are important bioactive membrane components. GSLs containing sialic acids, known as gangliosides, are highly abundant in the brain and diseases of ganglioside metabolism cause severe early-onset neurodegeneration. The ganglioside GM2 is processed by β-hexosaminidase A and when non-functional GM2 accumulates causing Tay-Sachs and Sandhoff diseases. We have developed i3Neuron-based disease models demonstrating storage of GM2 and severe endolysosomal dysfunction. Additionally, the plasma membrane (PM) is significantly altered in its lipid and protein composition. These changes are driven in part by lysosomal exocytosis causing inappropriate accumulation of lysosomal proteins on the cell surface. There are also significant changes in synaptic protein abundances with direct functional impact on neuronal activity. Lysosomal proteins are also enriched at the PM in GM1 gangliosidosis supporting that lysosomal exocytosis is a conserved mechanism of PM proteome change in these diseases. This work provides mechanistic insights into neuronal dysfunction in gangliosidoses highlighting that these are severe PM disorders with implications for other lysosomal and neurodegenerative diseases.https://doi.org/10.1371/journal.pbio.3003265
spellingShingle Alex S Nicholson
David A Priestman
Robin Antrobus
James C Williamson
Reuben Bush
Shannon J McKie
Henry G Barrow
Emily Smith
Kostantin Dobrenis
Nicholas A Bright
Frances M Platt
Janet E Deane
Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
PLoS Biology
title Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
title_full Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
title_fullStr Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
title_full_unstemmed Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
title_short Plasma membrane remodeling in GM2 gangliosidoses drives synaptic dysfunction.
title_sort plasma membrane remodeling in gm2 gangliosidoses drives synaptic dysfunction
url https://doi.org/10.1371/journal.pbio.3003265
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