Myelin dysfunction drives amyloid-β deposition in models of Alzheimer's disease.
Journal
Nature
ISSN: 1476-4687
Titre abrégé: Nature
Pays: England
ID NLM: 0410462
Informations de publication
Date de publication:
Jun 2023
Jun 2023
Historique:
received:
30
07
2021
accepted:
21
04
2023
medline:
9
6
2023
pubmed:
1
6
2023
entrez:
31
5
2023
Statut:
ppublish
Résumé
The incidence of Alzheimer's disease (AD), the leading cause of dementia, increases rapidly with age, but why age constitutes the main risk factor is still poorly understood. Brain ageing affects oligodendrocytes and the structural integrity of myelin sheaths
Identifiants
pubmed: 37258678
doi: 10.1038/s41586-023-06120-6
pii: 10.1038/s41586-023-06120-6
pmc: PMC10247380
doi:
Substances chimiques
Amyloid beta-Peptides
0
APP protein, mouse
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
349-357Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023. The Author(s).
Références
Bowley, M. P., Cabral, H., Rosene, D. L. & Peters, A. Age changes in myelinated nerve fibers of the cingulate bundle and corpus callosum in the rhesus monkey. J. Comp. Neurol. 518, 3046–3064 (2010).
pubmed: 20533359
pmcid: 2889619
doi: 10.1002/cne.22379
Safaiyan, S. et al. Age-related myelin degradation burdens the clearance function of microglia during aging. Nat. Neurosci. 19, 995–998 (2016).
pubmed: 27294511
pmcid: 7116794
doi: 10.1038/nn.4325
Safaiyan, S. et al. White matter aging drives microglial diversity. Neuron 109, 1100–1117.e10 (2021).
pubmed: 33606969
doi: 10.1016/j.neuron.2021.01.027
Griffiths, I. et al. Axonal swellings and degeneration in mice lacking the major proteolipid of myelin. Science 280, 1610–1613 (1998).
pubmed: 9616125
doi: 10.1126/science.280.5369.1610
Fünfschilling, U. et al. Glycolytic oligodendrocytes maintain myelin and long-term axonal integrity. Nature 485, 517–521 (2012).
pubmed: 22622581
pmcid: 3613737
doi: 10.1038/nature11007
Lee, Y. et al. Oligodendroglia metabolically support axons and contribute to neurodegeneration. Nature 487, 443–448 (2012).
pubmed: 22801498
pmcid: 3408792
doi: 10.1038/nature11314
Saab, A. S. et al. Oligodendroglial NMDA receptors regulate glucose import and axonal energy metabolism. Neuron 91, 119–132 (2016).
pubmed: 27292539
pmcid: 9084537
doi: 10.1016/j.neuron.2016.05.016
Toyama, B. H. et al. Identification of long-lived proteins reveals exceptional stability of essential cellular structures. Cell 154, 971–982 (2013).
pubmed: 23993091
pmcid: 3788602
doi: 10.1016/j.cell.2013.07.037
Ando, S., Tanaka, Y., Toyoda, Y. & Kon, K. Turnover of myelin lipids in aging brain. Neurochem. Res. 28, 5–13 (2003).
pubmed: 12587659
doi: 10.1023/A:1021635826032
Yeung, M. S. et al. Dynamics of oligodendrocyte generation and myelination in the human brain. Cell 159, 766–774 (2014).
pubmed: 25417154
doi: 10.1016/j.cell.2014.10.011
Ringman, J. M. et al. Diffusion tensor imaging in preclinical and presymptomatic carriers of familial Alzheimer’s disease mutations. Brain 130, 1767–1776 (2007).
pubmed: 17522104
doi: 10.1093/brain/awm102
Dean, D. C. et al. Association of amyloid pathology with myelin alteration in preclinical Alzheimer disease. JAMA Neurol. 74, 41–49 (2017).
pubmed: 27842175
pmcid: 5195903
doi: 10.1001/jamaneurol.2016.3232
Wang, Q. et al. Quantification of white matter cellularity and damage in preclinical and early symptomatic Alzheimer’s disease. NeuroImage Clin. 22, 101767 (2019).
pubmed: 30901713
pmcid: 6428957
doi: 10.1016/j.nicl.2019.101767
Araque Caballero, M. Á. et al. White matter diffusion alterations precede symptom onset in autosomal dominant Alzheimer’s disease. Brain 141, 3065–3080 (2018).
pubmed: 30239611
pmcid: 6158739
doi: 10.1093/brain/awy229
Snaidero, N. et al. Antagonistic functions of MBP and CNP establish cytosolic channels in CNS myelin. Cell Rep. 18, 314–323 (2017).
pubmed: 28076777
pmcid: 5263235
doi: 10.1016/j.celrep.2016.12.053
Edgar, J. M. et al. Early ultrastructural defects of axons and axon–glia junctions in mice lacking expression of Cnp1. Glia 57, 1815–1824 (2009).
pubmed: 19459211
doi: 10.1002/glia.20893
Trevisiol, A. et al. Structural myelin defects are associated with low axonal ATP levels but rapid recovery from energy deprivation in a mouse model of spastic paraplegia. PLoS Biol. 18, e3000943 (2020).
pubmed: 33196637
pmcid: 7704050
doi: 10.1371/journal.pbio.3000943
Bush, A. I. et al. Rapid induction of Alzheimer Aβ amyloid formation by zinc. Science 265, 1464–1467 (1994).
pubmed: 8073293
doi: 10.1126/science.8073293
Jankowsky, J. L. et al. Rodent Aβ modulates the solubility and distribution of amyloid deposits in transgenic mice. J. Biol. Chem. 282, 22707–22720 (2007).
pubmed: 17556372
doi: 10.1074/jbc.M611050200
Chen, J.-F. et al. Enhancing myelin renewal reverses cognitive dysfunction in a murine model of Alzheimer’s disease. Neuron 109, 2292–2307.e5 (2021).
pubmed: 34102111
pmcid: 8298291
doi: 10.1016/j.neuron.2021.05.012
Zhang, X. et al. Oligodendroglial glycolytic stress triggers inflammasome activation and neuropathology in Alzheimer’s disease. Sci. Adv. 6, eabb8680 (2020).
pubmed: 33277246
pmcid: 7717916
doi: 10.1126/sciadv.abb8680
Chung, J. A. & Cummings, J. L. Neurobehavioral and neuropsychiatric symptoms in Alzheimer’s disease: characteristics and treatment. Neurol. Clin. 18, 829–846 (2000).
pubmed: 11072263
doi: 10.1016/S0733-8619(05)70228-0
Cherny, R. A. et al. Treatment with a copper–zinc chelator markedly and rapidly inhibits β-amyloid accumulation in Alzheimer’s disease transgenic mice. Neuron 30, 665–676 (2001).
pubmed: 11430801
doi: 10.1016/S0896-6273(01)00317-8
Frenkel, D., Maron, R., Burt, D. S. & Weiner, H. L. Nasal vaccination with a proteosome-based adjuvant and glatiramer acetate clears β-amyloid in a mouse model of Alzheimer disease. J. Clin. Invest. 115, 2423–2433 (2005).
pubmed: 16100572
pmcid: 1184038
doi: 10.1172/JCI23241
Schoenemann, P. T., Sheehan, M. J. & Glotzer, L. D. Prefrontal white matter volume is disproportionately larger in humans than in other primates. Nat. Neurosci. 8, 242–252 (2005).
pubmed: 15665874
doi: 10.1038/nn1394
Stokin, G. B. et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer’s disease. Science 307, 1282–1288 (2005).
pubmed: 15731448
doi: 10.1126/science.1105681
Gowrishankar, S., Wu, Y. & Ferguson, S. M. Impaired JIP3-dependent axonal lysosome transport promotes amyloid plaque pathology. J. Cell Biol. 216, 3291–3305 (2017).
pubmed: 28784610
pmcid: 5626538
doi: 10.1083/jcb.201612148
Vagnoni, A. et al. Calsyntenin-1 mediates axonal transport of the amyloid precursor protein and regulates Aβ production. Hum. Mol. Genet. 21, 2845–2854 (2012).
pubmed: 22434822
pmcid: 3373235
doi: 10.1093/hmg/dds109
Niederst, E. D., Reyna, S. M. & Goldstein, L. S. Axonal amyloid precursor protein and its fragments undergo somatodendritic endocytosis and processing. Mol. Biol. Cell 26, 205–217 (2015).
pubmed: 25392299
pmcid: 4294669
doi: 10.1091/mbc.E14-06-1049
Buxbaum, J. D. et al. Alzheimer amyloid protein precursor in the rat hippocampus: transport and processing through the perforant path. J. Neurosci. 18, 9629–9637 (1998).
pubmed: 9822724
pmcid: 6793291
doi: 10.1523/JNEUROSCI.18-23-09629.1998
Lazarov, O., Lee, M., Peterson, D. A. & Sisodia, S. S. Evidence that synaptically released β-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J. Neurosci. 22, 9785–9793 (2002).
pubmed: 12427834
pmcid: 6757836
doi: 10.1523/JNEUROSCI.22-22-09785.2002
Gowrishankar, S. et al. Massive accumulation of luminal protease-deficient axonal lysosomes at Alzheimer’s disease amyloid plaques. Proc. Natl Acad. Sci USA. 112, E3699–E3708 (2015).
pubmed: 26124111
pmcid: 4507205
doi: 10.1073/pnas.1510329112
Sadleir, K. R. et al. Presynaptic dystrophic neurites surrounding amyloid plaques are sites of microtubule disruption, BACE1 elevation, and increased Aβ generation in Alzheimer’s disease. Acta Neuropathol. 132, 235–256 (2016).
pubmed: 26993139
pmcid: 4947125
doi: 10.1007/s00401-016-1558-9
Yuan, P. et al. TREM2 haplodeficiency in mice and humans impairs the microglia barrier function leading to decreased amyloid compaction and severe axonal dystrophy. Neuron 90, 724–739 (2016).
pubmed: 27196974
pmcid: 4898967
doi: 10.1016/j.neuron.2016.05.003
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
Parhizkar, S. et al. Loss of TREM2 function increases amyloid seeding but reduces plaque-associated ApoE. Nat. Neurosci. 22, 191–204 (2019).
pubmed: 30617257
pmcid: 6417433
doi: 10.1038/s41593-018-0296-9
Keren-Shaul, H. et al. A unique microglia type associated with restricting development of Alzheimer’s disease. Cell 169, 1276–1290.e17 (2017).
pubmed: 28602351
doi: 10.1016/j.cell.2017.05.018
Hammond, T. R. et al. Single-cell RNA sequencing of microglia throughout the mouse lifespan and in the injured brain reveals complex cell-state changes. Immunity 50, 253–271.e6 (2019).
pubmed: 30471926
doi: 10.1016/j.immuni.2018.11.004
Deming, Y. et al. The MS4A gene cluster is a key modulator of soluble TREM2 and Alzheimer’s disease risk. Sci. Transl. Med. 11, eaau2291 (2019).
pubmed: 31413141
pmcid: 6697053
doi: 10.1126/scitranslmed.aau2291
Huynh, T.-P. V., Davis, A. A., Ulrich, J. D. & Holtzman, D. M. Apolipoprotein E and Alzheimer’s disease: the influence of apolipoprotein E on amyloid-β and other amyloidogenic proteins: thematic review series: ApoE and lipid homeostasis in Alzheimer’s disease. J. Lipid Res. 58, 824–836 (2017).
pubmed: 28246336
pmcid: 5408619
doi: 10.1194/jlr.R075481
Schmued, L. C., Raymick, J., Paule, M. G., Dumas, M. & Sarkar, S. Characterization of myelin pathology in the hippocampal complex of a transgenic mouse model of Alzheimer’s disease. Curr. Alzheimer Res. 10, 30–37 (2013).
pubmed: 23157338
Mitew, S. et al. Focal demyelination in Alzheimer’s disease and transgenic mouse models. Acta Neuropathol. 119, 567–577 (2010).
pubmed: 20198482
doi: 10.1007/s00401-010-0657-2
Behrendt, G. et al. Dynamic changes in myelin aberrations and oligodendrocyte generation in chronic amyloidosis in mice and men. Glia 61, 273–286 (2013).
pubmed: 23090919
doi: 10.1002/glia.22432
Chen, W.-T. et al. Spatial transcriptomics and in situ sequencing to study Alzheimer’s disease. Cell 182, 976–991.e19 (2020).
pubmed: 32702314
doi: 10.1016/j.cell.2020.06.038
Kenigsbuch, M. et al. A shared disease-associated oligodendrocyte signature among multiple CNS pathologies. Nat. Neurosci. 25, 876–886 (2022).
pubmed: 35760863
pmcid: 9724210
doi: 10.1038/s41593-022-01104-7
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
Janova, H. et al. Microglia ablation alleviates myelin-associated catatonic signs in mice. J. Clin. Invest. 128, 734–745 (2018).
pubmed: 29252214
doi: 10.1172/JCI97032
Jendresen, C. et al. Systemic LPS-induced Aβ-solubilization and clearance in AβPP-transgenic mice is diminished by heparanase overexpression. Sci. Rep. 9, 4600 (2019).
pubmed: 30872722
pmcid: 6418119
doi: 10.1038/s41598-019-40999-4
Wendeln, A.-C. et al. Innate immune memory in the brain shapes neurological disease hallmarks. Nature 556, 332–338 (2018).
pubmed: 29643512
pmcid: 6038912
doi: 10.1038/s41586-018-0023-4
Sheng, J. G. et al. Lipopolysaccharide-induced-neuroinflammation increases intracellular accumulation of amyloid precursor protein and amyloid β peptide in APPswe transgenic mice. Neurobiol. Dis. 14, 133–145 (2003).
pubmed: 13678674
doi: 10.1016/S0969-9961(03)00069-X
Knopp, R. C., Baumann, K. K., Wilson, M. L., Banks, W. A. & Erickson, M. A. Amyloid beta pathology exacerbates weight loss and brain cytokine responses following low-dose lipopolysaccharide in aged female Tg2576 mice. Int. J. Mol. Sci. 23, 2377 (2022).
pubmed: 35216491
pmcid: 8879430
doi: 10.3390/ijms23042377
Mahmoudi, E. et al. Diagnosis of Alzheimer’s disease and related dementia among people with multiple sclerosis: large cohort study, USA. Mult. Scler. Relat. Disord. 57, 103351 (2022).
pubmed: 35158460
doi: 10.1016/j.msard.2021.103351
Luczynski, P., Laule, C., Hsiung, G.-Y. R., Moore, G. W. & Tremlett, H. Coexistence of multiple sclerosis and Alzheimer’s disease: a review. Mult. Scler. Relat. Disord. 27, 232–238 (2019).
pubmed: 30415025
doi: 10.1016/j.msard.2018.10.109
Bartzokis, G. Age-related myelin breakdown: a developmental model of cognitive decline and Alzheimer’s disease. Neurobiol. Aging 25, 5–18 (2004).
pubmed: 14675724
doi: 10.1016/j.neurobiolaging.2003.03.001
Braak, H. & Braak, E. Development of Alzheimer-related neurofibrillary changes in the neocortex inversely recapitulates cortical myelogenesis. Acta Neuropathol. 92, 197–201 (1996).
pubmed: 8841666
doi: 10.1007/s004010050508
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
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
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
Klugmann, M. et al. Assembly of CNS myelin in the absence of proteolipid protein. Neuron 18, 59–70 (1997).
pubmed: 9010205
doi: 10.1016/S0896-6273(01)80046-5
Lüders, K. A., Patzig, J., Simons, M., Nave, K. A. & Werner, H. B. Genetic dissection of oligodendroglial and neuronal Plp1 function in a novel mouse model of spastic paraplegia type 2. Glia 65, 1762–1776 (2017).
pubmed: 28836307
doi: 10.1002/glia.23193
Meschkat, M. et al. White matter integrity in mice requires continuous myelin synthesis at the inner tongue. Nat. Commun. 13, 1–18 (2022).
doi: 10.1038/s41467-022-28720-y
Gorski, J. A. et al. Cortical excitatory neurons and glia, but not GABAergic neurons, are produced in the Emx1-expressing lineage. J. Neurosci. 22, 6309–6314 (2002).
pubmed: 12151506
pmcid: 6758181
doi: 10.1523/JNEUROSCI.22-15-06309.2002
Kawaguchi, D., Sahara, S., Zembrzycki, A. & O’Leary, D. D. Generation and analysis of an improved Foxg1-IRES-Cre driver mouse line. Dev. Biol. 412, 139–147 (2016).
pubmed: 26896590
pmcid: 5895454
doi: 10.1016/j.ydbio.2016.02.011
Berghoff, S. A. et al. Microglia facilitate repair of demyelinated lesions via post-squalene sterol synthesis. Nat. Neurosci. 24, 47–60 (2021).
pubmed: 33349711
doi: 10.1038/s41593-020-00757-6
Singmann, H. et al. afex: analysis of factorial experiments. R package version 0.16-1 (2016).
Liebmann, T. et al. Three-dimensional study of Alzheimer’s disease hallmarks using the iDISCO clearing method. Cell Rep. 16, 1138–1152 (2016).
pubmed: 27425620
pmcid: 5040352
doi: 10.1016/j.celrep.2016.06.060
Wirths, O. et al. N-truncated Aβ
doi: 10.1186/s13195-017-0309-z
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
Weil, M.-T., Ruhwedel, T., Meschkat, M., Sadowski, B. & Möbius, W. in Oligodendrocytes: Methods and Protocols (eds Lyons, D. A. & Kegel, L.) 343–375 (Springer, 2019).
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).
pubmed: 23104886
doi: 10.1093/bioinformatics/bts635
Liao, Y., Smyth, G. K. & Shi, W. featureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).
pubmed: 24227677
doi: 10.1093/bioinformatics/btt656
Love, M. I., Huber, W. & Anders, S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 15, 550 (2014).
pubmed: 25516281
pmcid: 4302049
doi: 10.1186/s13059-014-0550-8
Kolberg, L., Raudvere, U., Kuzmin, I., Vilo, J. & Peterson, H. gprofiler2—an R package for gene list functional enrichment analysis and namespace conversion toolset g: Profiler. F1000Res. 9, ELIXIR-709 (2020).
pubmed: 33564394
pmcid: 7859841
doi: 10.12688/f1000research.24956.2
Liao, Y., Wang, J., Jaehnig, E. J., Shi, Z. & Zhang, B. WebGestalt 2019: gene set analysis toolkit with revamped UIs and APIs. Nucleic Acids Res. 47, W199–W205 (2019).
pubmed: 31114916
pmcid: 6602449
doi: 10.1093/nar/gkz401
Gu, Z. & Hübschmann, D. Simplify enrichment: a Bioconductor package for clustering and visualizing functional enrichment results. Genomics Proteomics Bioinformatics https://doi.org/10.1016/j.gpb.2022.04.008 (2022).
Corces, M. R. et al. An improved ATAC-seq protocol reduces background and enables interrogation of frozen tissues. Nat. Methods 14, 959–962 (2017).
pubmed: 28846090
pmcid: 5623106
doi: 10.1038/nmeth.4396
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902.e21 (2019).
pubmed: 31178118
pmcid: 6687398
doi: 10.1016/j.cell.2019.05.031
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573–3587.e29 (2021).
pubmed: 34062119
pmcid: 8238499
doi: 10.1016/j.cell.2021.04.048
McInnes, L., Healy, J. & Melville, J. UMAP: uniform manifold approximation and projection for dimension reduction. Preprint at https://arxiv.org/abs/1802.03426 (2018).
Finak, G. et al. MAST: a flexible statistical framework for assessing transcriptional changes and characterizing heterogeneity in single-cell RNA sequencing data. Genome Biol. 16, 278 (2015).
pubmed: 26653891
pmcid: 4676162
doi: 10.1186/s13059-015-0844-5
Barrett, T. et al. NCBI GEO: archive for functional genomics data sets—update. Nucleic Acids Res. 41, D991–D995 (2012).
pubmed: 23193258
pmcid: 3531084
doi: 10.1093/nar/gks1193