Oligodendrocytes produce amyloid-β and contribute to plaque formation alongside neurons in Alzheimer's disease model mice.
Journal
Nature neuroscience
ISSN: 1546-1726
Titre abrégé: Nat Neurosci
Pays: United States
ID NLM: 9809671
Informations de publication
Date de publication:
05 Aug 2024
05 Aug 2024
Historique:
received:
28
09
2023
accepted:
12
07
2024
medline:
6
8
2024
pubmed:
6
8
2024
entrez:
5
8
2024
Statut:
aheadofprint
Résumé
Amyloid-β (Aβ) is thought to be neuronally derived in Alzheimer's disease (AD). However, transcripts of amyloid precursor protein (APP) and amyloidogenic enzymes are equally abundant in oligodendrocytes (OLs). By cell-type-specific deletion of Bace1 in a humanized knock-in AD model, APP
Identifiants
pubmed: 39103558
doi: 10.1038/s41593-024-01730-3
pii: 10.1038/s41593-024-01730-3
doi:
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2024. The Author(s).
Références
Zhao, J. et al. β-secretase processing of the β-amyloid precursor protein in transgenic mice is efficient in neurons but inefficient in astrocytes. J. Biol. Chem. 271, 31407–31411 (1996).
pubmed: 8940150
doi: 10.1074/jbc.271.49.31407
Veeraraghavalu, K., Zhang, C., Zhang, X., Tanzi, R. E. & Sisodia, S. S. Age-dependent, non-cell-autonomous deposition of amyloid from synthesis of β-amyloid by cells other than excitatory neurons. J. Neurosci. 34, 3668–3673 (2014).
pubmed: 24599465
pmcid: 3942582
doi: 10.1523/JNEUROSCI.5079-13.2014
Rice, H. C. et al. Contribution of GABAergic interneurons to amyloid-β plaque pathology in an APP knock-in mouse model. Mol. Neurodegener. 15, 3 (2020).
pubmed: 31915042
pmcid: 6950898
doi: 10.1186/s13024-019-0356-y
Skaper, S. D., Evans, N. A., Rosin, C., Facci, L. & Richardson, J. C. Oligodendrocytes are a novel source of amyloid peptide generation. Neurochem. Res. 34, 2243–2250 (2009).
pubmed: 19557514
doi: 10.1007/s11064-009-0022-9
Walter, S. et al. The metalloprotease ADAMTS4 generates N-truncated Aβ4–x species and marks oligodendrocytes as a source of amyloidogenic peptides in Alzheimer’s disease. Acta Neuropathol. 137, 239–257 (2019).
pubmed: 30426203
doi: 10.1007/s00401-018-1929-5
Gazestani, V. et al. Early Alzheimer’s disease pathology in human cortex involves transient cell states. Cell 186, 4438–4453.e23 (2023).
pubmed: 37774681
doi: 10.1016/j.cell.2023.08.005
Chen, J. F. et al. Enhancing myelin renewal reverses cognitive dysfunction in a murine model of Alzheimer’s disease. Neuron 109, 2292–2307 (2021).
pubmed: 34102111
pmcid: 8298291
doi: 10.1016/j.neuron.2021.05.012
Mathys, H. et al. Single-cell transcriptomic analysis of Alzheimer’s disease. Nature 570, 332–337 (2019).
pubmed: 31042697
pmcid: 6865822
doi: 10.1038/s41586-019-1195-2
Depp, C. et al. Myelin dysfunction drives amyloid-β deposition in models of Alzheimer’s disease. Nature 618, 349–357 (2023).
pubmed: 37258678
pmcid: 10247380
doi: 10.1038/s41586-023-06120-6
Ximerakis, M. et al. Single-cell transcriptomic profiling of the aging mouse brain. Nat. Neurosci. 22, 1696–1708 (2019).
pubmed: 31551601
doi: 10.1038/s41593-019-0491-3
Zeisel, A. et al. Molecular architecture of the mouse nervous system. Cell 174, 999–1014 (2018).
pubmed: 30096314
pmcid: 6086934
doi: 10.1016/j.cell.2018.06.021
Zhou, Y. et al. Human and mouse single-nucleus transcriptomics reveal TREM2-dependent and TREM2-independent cellular responses in Alzheimer’s disease. Nat. Med. 26, 131–142 (2020).
pubmed: 31932797
pmcid: 6980793
doi: 10.1038/s41591-019-0695-9
Jäkel, S. et al. Altered human oligodendrocyte heterogeneity in multiple sclerosis. Nature 566, 543–547 (2019).
pubmed: 30747918
pmcid: 6544546
doi: 10.1038/s41586-019-0903-2
Lake, B. B. et al. Integrative single-cell analysis of transcriptional and epigenetic states in the human adult brain. Nat. Biotechnol. 36, 70–80 (2018).
pubmed: 29227469
doi: 10.1038/nbt.4038
Tognatta, R. et al. Transient Cnp expression by early progenitors causes Cre-Lox-based reporter lines to map profoundly different fates. Glia 65, 342–359 (2017).
pubmed: 27807896
doi: 10.1002/glia.23095
Jo, Y. R. et al. Potential neuron-autonomous Purkinje cell degeneration by 2′,3′-cyclic nucleotide 3′-phosphodiesterase promoter/Cre-mediated autophagy impairments. FASEB J. 35, e21225 (2021).
pubmed: 33337568
doi: 10.1096/fj.202001366RR
Lam, M. et al. CNS myelination requires VAMP2/3-mediated membrane expansion in oligodendrocytes. Nat. Commun. 13, 5583 (2022).
pubmed: 36151203
pmcid: 9508103
doi: 10.1038/s41467-022-33200-4
Hu, X., Hu, J., Dai, L., Trapp, B. & Yan, R. Axonal and Schwann cell BACE1 is equally required for remyelination of peripheral nerves. J. Neurosci. 35, 3806–3814 (2015).
pubmed: 25740511
pmcid: 4348183
doi: 10.1523/JNEUROSCI.5207-14.2015
Blackwell, J. M., Lesicko, A. M., Rao, W., De Biasi, M. & Geffen, M. N. Auditory cortex shapes sound responses in the inferior colliculus. eLife 9, e51890 (2020).
pubmed: 32003747
pmcid: 7062464
doi: 10.7554/eLife.51890
Lee, C. C., Nayak, A., Sethuraman, A., Belfort, G. & McRae, G. J. A three-stage kinetic model of amyloid fibrillation. Biophys. J. 92, 3448–3458 (2007).
pubmed: 17325005
pmcid: 1853138
doi: 10.1529/biophysj.106.098608
Burgold, S., Filser, S., Dorostkar, M. M., Schmidt, B. & Herms, J. In vivo imaging reveals sigmoidal growth kinetic of β-amyloid plaques. Acta Neuropathol. Commun. 2, 30 (2014).
pubmed: 24678659
pmcid: 4050984
doi: 10.1186/2051-5960-2-30
Herculano-Houzel, S. The glia/neuron ratio: how it varies uniformly across brain structures and species and what that means for brain physiology and evolution. Glia 62, 1377–1391 (2014).
pubmed: 24807023
doi: 10.1002/glia.22683
Kamenetz, F. et al. APP processing and synaptic function. Neuron 37, 925–937 (2003).
pubmed: 12670422
doi: 10.1016/S0896-6273(03)00124-7
Sevigny, J. et al. The antibody aducanumab reduces Aβ plaques in Alzheimer’s disease. Nature 537, 50–56 (2016).
pubmed: 27582220
doi: 10.1038/nature19323
Tucker, S. et al. The murine version of BAN2401 (mAb158) selectively reduces amyloid-β protofibrils in brain and cerebrospinal fluid of tg-ArcSwe mice. J. Alzheimers Dis. 43, 575–588 (2015).
pubmed: 25096615
doi: 10.3233/JAD-140741
Chatila, Z. K. et al. BACE1 regulates proliferation and neuronal differentiation of newborn cells in the adult hippocampus in mice. eNeuro 5, ENEURO.0067-18.2018 (2018).
Sur, C. et al. BACE inhibition causes rapid, regional and non-progressive volume reduction in Alzheimer’s disease brain. Brain 143, 3816–3826 (2020).
pubmed: 33253354
pmcid: 8453290
doi: 10.1093/brain/awaa332
Wessels, A. M. et al. Cognitive outcomes in trials of two BACE inhibitors in Alzheimer’s disease. Alzheimers Dement. 16, 1483–1492 (2020).
pubmed: 33049114
doi: 10.1002/alz.12164
Satir, T. M. et al. Partial reduction of amyloid β production by β-secretase inhibitors does not decrease synaptic transmission. Alzheimers Res. Ther. 12, 63 (2020).
pubmed: 32456694
pmcid: 7251689
doi: 10.1186/s13195-020-00635-0
Peters, F. et al. BACE1 inhibition more effectively suppresses initiation than progression of β-amyloid pathology. Acta Neuropathol. 135, 695–710 (2018).
pubmed: 29327084
pmcid: 5904228
doi: 10.1007/s00401-017-1804-9
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587 (2021).
pubmed: 34062119
pmcid: 8238499
doi: 10.1016/j.cell.2021.04.048
Allen, M., Poggiali, D., Whitaker, K., Marshall, T. R. & Kievit, R. A. Raincloud plots: a multi-platform tool for robust data visualization. Wellcome Open Res. 4, 63 (2019).
pubmed: 31069261
doi: 10.12688/wellcomeopenres.15191.1
Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer, 2009).
Saito, T. et al. Single App knock-in mouse models of Alzheimer’s disease. Nat. Neurosci. 17, 661–663 (2014).
pubmed: 24728269
doi: 10.1038/nn.3697
Hu, X., Das, B., Hou, H., He, W. & Yan, R. BACE1 deletion in the adult mouse reverses preformed amyloid deposition and improves cognitive functions. J. Exp. Med. 215, 927–940 (2018).
pubmed: 29444819
pmcid: 5839766
doi: 10.1084/jem.20171831
Lappe-Siefke, C. et al. Disruption of Cnp1 uncouples oligodendroglial functions in axonal support and myelination. Nat. Genet. 33, 366–374 (2003).
pubmed: 12590258
doi: 10.1038/ng1095
Goebbels, S. et al. Genetic targeting of principal neurons in neocortex and hippocampus of NEX-Cre mice. Genesis 44, 611–621 (2006).
pubmed: 17146780
doi: 10.1002/dvg.20256
Madisen, L. et al. A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci. 13, 133–140 (2010).
pubmed: 20023653
doi: 10.1038/nn.2467
Oakley, H. et al. Intraneuronal β-amyloid aggregates, neurodegeneration and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J. Neurosci. 26, 10129–10140 (2006).
pubmed: 17021169
pmcid: 6674618
doi: 10.1523/JNEUROSCI.1202-06.2006
Weil, M. T. et al. Isolation and culture of oligodendrocytes. Methods Mol. Biol. 1936, 79–95 (2019).
pubmed: 30820894
doi: 10.1007/978-1-4939-9072-6_5
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
doi: 10.1038/nmeth.2019
Wirths, O. Extraction of soluble and insoluble protein fractions from mouse brains and spinal cords. Bio Protoc. 7, e2422 (2017).
pubmed: 34541150
pmcid: 8413590
Oh, S. W. et al. A mesoscale connectome of the mouse brain. Nature 508, 207–214 (2014).
pubmed: 24695228
pmcid: 5102064
doi: 10.1038/nature13186