Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression

Alzheimer's disease (AD) exhibits imbalance between neuronal excitation and inhibition, likely secondary to interneuron dysfunction. To reveal underlying mediators, we spatially profiled the transcriptome of neuronal subtypes in 5XFAD versus control mice at early- and late-stage disease. Pooled...

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Main Authors: Kevin S. Chen, Mohamed H. Noureldein, Diana M. Rigan, John M. Hayes, Kyle J. Loi, Junguk Hur, Masha G. Savelieff, Eva L. Feldman
Format: Article
Language:English
Published: Elsevier 2025-09-01
Series:Neurobiology of Disease
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Online Access:http://www.sciencedirect.com/science/article/pii/S0969996125002281
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author Kevin S. Chen
Mohamed H. Noureldein
Diana M. Rigan
John M. Hayes
Kyle J. Loi
Junguk Hur
Masha G. Savelieff
Eva L. Feldman
author_facet Kevin S. Chen
Mohamed H. Noureldein
Diana M. Rigan
John M. Hayes
Kyle J. Loi
Junguk Hur
Masha G. Savelieff
Eva L. Feldman
author_sort Kevin S. Chen
collection DOAJ
description Alzheimer's disease (AD) exhibits imbalance between neuronal excitation and inhibition, likely secondary to interneuron dysfunction. To reveal underlying mediators, we spatially profiled the transcriptome of neuronal subtypes in 5XFAD versus control mice at early- and late-stage disease. Pooled analysis of neuron types showed expected pathways at early-stage (RNA and protein processing pathways) versus late-stage (neurodegenerative pathways) disease. Early-stage interneurons exhibited alterations in AD-related RNA and protein pathways along with canonical neurodegenerative pathways. Early-stage excitatory neurons, however, showed changes in axon guidance and synapse pathways, without representation of neurodegenerative pathways. Classical neurodegenerative pathways were represented only in late-stage excitatory neurons. Late-stage interneurons instead featured neuronal and synapse pathways along with cellular, cancer, and infection pathways. Our results suggest earlier neurodegenerative pathway involvement in interneurons, represented in excitatory neurons only at later stages, possibly indicating earlier inhibitory neuron involvement. These transcriptomic profiles offer insight into potential AD pathophysiology and therapeutic targets.
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institution Kabale University
issn 1095-953X
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publishDate 2025-09-01
publisher Elsevier
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series Neurobiology of Disease
spelling doaj-art-7417ffbea7d64764b7f8a77046b782002025-08-20T03:32:23ZengElsevierNeurobiology of Disease1095-953X2025-09-0121310701210.1016/j.nbd.2025.107012Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progressionKevin S. Chen0Mohamed H. Noureldein1Diana M. Rigan2John M. Hayes3Kyle J. Loi4Junguk Hur5Masha G. Savelieff6Eva L. Feldman7Department of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; Department of Neurosurgery, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USADepartment of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USADepartment of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USADepartment of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USADepartment of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USADepartment of Biomedical Sciences, University of North Dakota, Grand Forks, ND, 58202, USADepartment of Biomedical Sciences, University of North Dakota, Grand Forks, ND, 58202, USADepartment of Neurology, University of Michigan, Ann Arbor, MI, 48109, USA; Department of Neurosurgery, University of Michigan, Ann Arbor, MI, 48109, USA; NeuroNetwork for Emerging Therapies, University of Michigan, Ann Arbor, MI, 48109, USA; Corresponding author at: 5017 AAT-BSRB, 109 Zina Pitcher Place, Ann Arbor, MI 48109, USA.Alzheimer's disease (AD) exhibits imbalance between neuronal excitation and inhibition, likely secondary to interneuron dysfunction. To reveal underlying mediators, we spatially profiled the transcriptome of neuronal subtypes in 5XFAD versus control mice at early- and late-stage disease. Pooled analysis of neuron types showed expected pathways at early-stage (RNA and protein processing pathways) versus late-stage (neurodegenerative pathways) disease. Early-stage interneurons exhibited alterations in AD-related RNA and protein pathways along with canonical neurodegenerative pathways. Early-stage excitatory neurons, however, showed changes in axon guidance and synapse pathways, without representation of neurodegenerative pathways. Classical neurodegenerative pathways were represented only in late-stage excitatory neurons. Late-stage interneurons instead featured neuronal and synapse pathways along with cellular, cancer, and infection pathways. Our results suggest earlier neurodegenerative pathway involvement in interneurons, represented in excitatory neurons only at later stages, possibly indicating earlier inhibitory neuron involvement. These transcriptomic profiles offer insight into potential AD pathophysiology and therapeutic targets.http://www.sciencedirect.com/science/article/pii/S09699961250022815XFADExcitatoryHyperexcitabilityInhibitoryMouseSpatial transcriptomics
spellingShingle Kevin S. Chen
Mohamed H. Noureldein
Diana M. Rigan
John M. Hayes
Kyle J. Loi
Junguk Hur
Masha G. Savelieff
Eva L. Feldman
Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
Neurobiology of Disease
5XFAD
Excitatory
Hyperexcitability
Inhibitory
Mouse
Spatial transcriptomics
title Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
title_full Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
title_fullStr Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
title_full_unstemmed Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
title_short Interneuron transcriptomics reveals pathologic markers of Alzheimer's disease progression
title_sort interneuron transcriptomics reveals pathologic markers of alzheimer s disease progression
topic 5XFAD
Excitatory
Hyperexcitability
Inhibitory
Mouse
Spatial transcriptomics
url http://www.sciencedirect.com/science/article/pii/S0969996125002281
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