Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS

Abstract Mutations in FUS and TARDBP cause amyotrophic lateral sclerosis (ALS), but the precise mechanisms of selective motor neuron degeneration remain unresolved. To address if pathomechanisms are shared across mutations and related to either gain- or loss-of-function, we performed single-cell RNA...

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Main Authors: Christoph Schweingruber, Jik Nijssen, Jonas Mechtersheimer, Stefan Reber, Mélanie Lebœuf, Niamh L. O’Brien, Irene Mei, Erin Hedges, Michaela Keuper, Julio Aguila Benitez, Vlad Radoi, Martin Jastroch, Marc-David Ruepp, Eva Hedlund
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-59679-1
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author Christoph Schweingruber
Jik Nijssen
Jonas Mechtersheimer
Stefan Reber
Mélanie Lebœuf
Niamh L. O’Brien
Irene Mei
Erin Hedges
Michaela Keuper
Julio Aguila Benitez
Vlad Radoi
Martin Jastroch
Marc-David Ruepp
Eva Hedlund
author_facet Christoph Schweingruber
Jik Nijssen
Jonas Mechtersheimer
Stefan Reber
Mélanie Lebœuf
Niamh L. O’Brien
Irene Mei
Erin Hedges
Michaela Keuper
Julio Aguila Benitez
Vlad Radoi
Martin Jastroch
Marc-David Ruepp
Eva Hedlund
author_sort Christoph Schweingruber
collection DOAJ
description Abstract Mutations in FUS and TARDBP cause amyotrophic lateral sclerosis (ALS), but the precise mechanisms of selective motor neuron degeneration remain unresolved. To address if pathomechanisms are shared across mutations and related to either gain- or loss-of-function, we performed single-cell RNA sequencing across isogenic induced pluripotent stem cell-derived neuron types, harbouring FUS P525L, FUS R495X, TARDBP M337V mutations or FUS knockout. Transcriptional changes were far more pronounced in motor neurons than interneurons. About 20% of uniquely dysregulated motor neuron transcripts were shared across FUS mutations, half from gain-of-function. Most indicated mitochondrial impairments, with attenuated pathways shared with mutant TARDBP M337V as well as C9orf72-ALS patient motor neurons. Mitochondrial motility was impaired in ALS motor axons, even with nuclear localized FUS mutants, demonstrating shared toxic gain-of-function mechanisms across FUS- and TARDBP-ALS, uncoupled from protein mislocalization. These early mitochondrial dysfunctions unique to motor neurons may affect survival and represent therapeutic targets in ALS.
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spelling doaj-art-bd86cec60f18444e9013046c65488efb2025-08-20T02:29:26ZengNature PortfolioNature Communications2041-17232025-05-0116112210.1038/s41467-025-59679-1Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALSChristoph Schweingruber0Jik Nijssen1Jonas Mechtersheimer2Stefan Reber3Mélanie Lebœuf4Niamh L. O’Brien5Irene Mei6Erin Hedges7Michaela Keuper8Julio Aguila Benitez9Vlad Radoi10Martin Jastroch11Marc-David Ruepp12Eva Hedlund13Department of Biochemistry and Biophysics, Stockholm UniversityDepartment of Cell and Molecular Biology, Karolinska Institutet, BiomedicumUK Dementia Research Institute Centre at King’s College London, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Maurice Wohl Clinical Neuroscience InstituteUK Dementia Research Institute Centre at King’s College London, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Maurice Wohl Clinical Neuroscience InstituteDepartment of Biochemistry and Biophysics, Stockholm UniversityUK Dementia Research Institute Centre at King’s College London, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Maurice Wohl Clinical Neuroscience InstituteDepartment of Biochemistry and Biophysics, Stockholm UniversityUK Dementia Research Institute Centre at King’s College London, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Maurice Wohl Clinical Neuroscience InstituteDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm UniversityDepartment of Neuroscience, Karolinska Institutet, BiomedicumDepartment of Biochemistry and Biophysics, Stockholm UniversityDepartment of Molecular Biosciences, The Wenner-Gren Institute, Stockholm UniversityUK Dementia Research Institute Centre at King’s College London, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, Maurice Wohl Clinical Neuroscience InstituteDepartment of Biochemistry and Biophysics, Stockholm UniversityAbstract Mutations in FUS and TARDBP cause amyotrophic lateral sclerosis (ALS), but the precise mechanisms of selective motor neuron degeneration remain unresolved. To address if pathomechanisms are shared across mutations and related to either gain- or loss-of-function, we performed single-cell RNA sequencing across isogenic induced pluripotent stem cell-derived neuron types, harbouring FUS P525L, FUS R495X, TARDBP M337V mutations or FUS knockout. Transcriptional changes were far more pronounced in motor neurons than interneurons. About 20% of uniquely dysregulated motor neuron transcripts were shared across FUS mutations, half from gain-of-function. Most indicated mitochondrial impairments, with attenuated pathways shared with mutant TARDBP M337V as well as C9orf72-ALS patient motor neurons. Mitochondrial motility was impaired in ALS motor axons, even with nuclear localized FUS mutants, demonstrating shared toxic gain-of-function mechanisms across FUS- and TARDBP-ALS, uncoupled from protein mislocalization. These early mitochondrial dysfunctions unique to motor neurons may affect survival and represent therapeutic targets in ALS.https://doi.org/10.1038/s41467-025-59679-1
spellingShingle Christoph Schweingruber
Jik Nijssen
Jonas Mechtersheimer
Stefan Reber
Mélanie Lebœuf
Niamh L. O’Brien
Irene Mei
Erin Hedges
Michaela Keuper
Julio Aguila Benitez
Vlad Radoi
Martin Jastroch
Marc-David Ruepp
Eva Hedlund
Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
Nature Communications
title Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
title_full Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
title_fullStr Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
title_full_unstemmed Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
title_short Single-cell RNA-sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across FUS- and TARDBP-ALS
title_sort single cell rna sequencing reveals early mitochondrial dysfunction unique to motor neurons shared across fus and tardbp als
url https://doi.org/10.1038/s41467-025-59679-1
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