Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease

Abstract Oligodendrocyte dysfunction, myelin degeneration, and white matter changes are critical events in the cognitive decline of Alzheimer’s disease (AD). Amyloid-β peptide (Aβ), a hallmark of AD, disrupts oligodendrocyte and myelin homeostasis, through mechanisms that remain poorly understood. H...

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Main Authors: Adhara Gaminde-Blasco, Rodrigo Senovilla-Ganzo, Uxue Balantzategi, Maialen Martinez-Preciado, Estibaliz Capetillo-Zarate, Fernando García-Moreno, Carlos Matute, Jimena Baleriola, Elena Alberdi
Format: Article
Language:English
Published: Springer 2025-08-01
Series:Cellular and Molecular Life Sciences
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Online Access:https://doi.org/10.1007/s00018-025-05823-5
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author Adhara Gaminde-Blasco
Rodrigo Senovilla-Ganzo
Uxue Balantzategi
Maialen Martinez-Preciado
Estibaliz Capetillo-Zarate
Fernando García-Moreno
Carlos Matute
Jimena Baleriola
Elena Alberdi
author_facet Adhara Gaminde-Blasco
Rodrigo Senovilla-Ganzo
Uxue Balantzategi
Maialen Martinez-Preciado
Estibaliz Capetillo-Zarate
Fernando García-Moreno
Carlos Matute
Jimena Baleriola
Elena Alberdi
author_sort Adhara Gaminde-Blasco
collection DOAJ
description Abstract Oligodendrocyte dysfunction, myelin degeneration, and white matter changes are critical events in the cognitive decline of Alzheimer’s disease (AD). Amyloid-β peptide (Aβ), a hallmark of AD, disrupts oligodendrocyte and myelin homeostasis, through mechanisms that remain poorly understood. Here, transcriptomic profiling of Aβ-exposed oligodendrocytes revealed widespread gene expression changes, particularly in RNA-related processes. Among these, hnRNP A2, a key regulator of RNA transport and myelin protein regulation, was aberrantly upregulated in hippocampal oligodendrocytess from AD patients with high Aβ levels, from AD mouse models, and in Aβ-treated oligodendrocytes. RNA-immunoprecipitation sequencing of the hnRNP A2 interactome revealed Aβ-induced changes in mRNA interactions, particularly enriched binding to Mbp and Mobp, indicating impaired RNA metabolism of myelin components. Furthermore, Aβ, through hnRNP A2 disruption, increased the number, cargo and dynamics of Mbp- and Mobp-containing granules, enhanced MBP and MOBP synthesis, and decreased oligodendroglial voltage-gated Ca2+ influx in an MBP-dependent manner. These findings suggest that Aβ-induced dysregulation of hnRNP A2 impairs RNA metabolism and myelin protein synthesis, altering the intracellular Ca2+ homeostasis critical for oligodendrocyte function. Graphical abstract
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spelling doaj-art-d4014b2182484073bbfefa73c4369fb92025-08-20T03:45:52ZengSpringerCellular and Molecular Life Sciences1420-90712025-08-0182112210.1007/s00018-025-05823-5Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s diseaseAdhara Gaminde-Blasco0Rodrigo Senovilla-Ganzo1Uxue Balantzategi2Maialen Martinez-Preciado3Estibaliz Capetillo-Zarate4Fernando García-Moreno5Carlos Matute6Jimena Baleriola7Elena Alberdi8Department of Neuroscience, University of the Basque Country (UPV/EHU)Achucarro Basque Center for NeuroscienceDepartment of Neuroscience, University of the Basque Country (UPV/EHU)Department of Neuroscience, University of the Basque Country (UPV/EHU)Department of Neuroscience, University of the Basque Country (UPV/EHU)Department of Neuroscience, University of the Basque Country (UPV/EHU)Department of Neuroscience, University of the Basque Country (UPV/EHU)Achucarro Basque Center for NeuroscienceDepartment of Neuroscience, University of the Basque Country (UPV/EHU)Abstract Oligodendrocyte dysfunction, myelin degeneration, and white matter changes are critical events in the cognitive decline of Alzheimer’s disease (AD). Amyloid-β peptide (Aβ), a hallmark of AD, disrupts oligodendrocyte and myelin homeostasis, through mechanisms that remain poorly understood. Here, transcriptomic profiling of Aβ-exposed oligodendrocytes revealed widespread gene expression changes, particularly in RNA-related processes. Among these, hnRNP A2, a key regulator of RNA transport and myelin protein regulation, was aberrantly upregulated in hippocampal oligodendrocytess from AD patients with high Aβ levels, from AD mouse models, and in Aβ-treated oligodendrocytes. RNA-immunoprecipitation sequencing of the hnRNP A2 interactome revealed Aβ-induced changes in mRNA interactions, particularly enriched binding to Mbp and Mobp, indicating impaired RNA metabolism of myelin components. Furthermore, Aβ, through hnRNP A2 disruption, increased the number, cargo and dynamics of Mbp- and Mobp-containing granules, enhanced MBP and MOBP synthesis, and decreased oligodendroglial voltage-gated Ca2+ influx in an MBP-dependent manner. These findings suggest that Aβ-induced dysregulation of hnRNP A2 impairs RNA metabolism and myelin protein synthesis, altering the intracellular Ca2+ homeostasis critical for oligodendrocyte function. Graphical abstracthttps://doi.org/10.1007/s00018-025-05823-5OligodendrocytesMBPHnRNP A2Calcium homeostasisAmyloid-β peptideAlzheimer´s disease
spellingShingle Adhara Gaminde-Blasco
Rodrigo Senovilla-Ganzo
Uxue Balantzategi
Maialen Martinez-Preciado
Estibaliz Capetillo-Zarate
Fernando García-Moreno
Carlos Matute
Jimena Baleriola
Elena Alberdi
Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
Cellular and Molecular Life Sciences
Oligodendrocytes
MBP
HnRNP A2
Calcium homeostasis
Amyloid-β peptide
Alzheimer´s disease
title Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
title_full Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
title_fullStr Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
title_full_unstemmed Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
title_short Disruption of hnRNP A2-mediated RNA dynamics by amyloid-β drives MBP increase in Alzheimer’s disease
title_sort disruption of hnrnp a2 mediated rna dynamics by amyloid β drives mbp increase in alzheimer s disease
topic Oligodendrocytes
MBP
HnRNP A2
Calcium homeostasis
Amyloid-β peptide
Alzheimer´s disease
url https://doi.org/10.1007/s00018-025-05823-5
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