Autophagy flux in CA1 neurons of Alzheimer hippocampus: Increased induction overburdens failing lysosomes to propel neuritic dystrophy
Open accessAbstract
Defective autophagy contributes to Alzheimer disease (AD) pathogenesis although evidence is conflicting on whether multiple stages are impaired. Here, for the first time, we have comprehensively evaluated the entire autophagic process specifically in CA1 pyramidal neurons of hippocampus from early and late-stage AD subjects and nondemented controls. CA1 neurons aspirated by laser capture microdissection were analyzed using a custom-designed microarray comprising 578 neuropathology- and neuroscience-associated genes. Striking upregulation of autophagy-related genes, exceeding that of other gene ontology groups, reflected increases in autophagosome formation and lysosomal biogenesis beginning at early AD stages. Upregulated autophagosome formation was further indicated by elevated gene and protein expression levels for autophagosome components and increased LC3-positive puncta. Increased lysosomal biogenesis was evidenced by activation of MiTF/TFE family transcriptional regulators, particularly TFE3 (transcription factor binding to IGHM enhancer 3) and by elevated expression of their target genes and encoded proteins. Notably, TFEB (transcription factor EB) activation was associated more strongly with glia than neurons. These findings establish that autophagic sequestration is both competent and upregulated in AD. Autophagosome-lysosome fusion is not evidently altered. Despite this early disease response, however, autophagy flux is progressively impeded due to deficient substrate clearance, as reflected by autolysosomal accumulation of LC3-II and SQSTM1/p62 and expansion of autolysosomal size and total area. We propose that sustained induction of autophagy in the face of progressively declining lysosomal clearance of substrates explains the uncommonly robust autophagic pathology and neuritic dystrophy implicated in AD pathogenesis.
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Gene set enrichment analyses were performed according to standard procedures on two published RNA-seq datasets.
“Gene set enrichment analyses were performed according to standard procedures [39, 40] on two published RNA-seq datasets [31, 48]”
From A gene toolbox for monitoring autophagy transcription (2021) · cites this paper as [48]
The citation identifies this paper as one of two published RNA-seq datasets. In Materials and methods, “Single population microarray” describes custom-designed arrays and array hybridization, not RNA sequencing; the “Gene Ontology (GO) analysis” section says its input genes were detected by that microarray. Page numbers are unavailable in our copy. (LLM, conf=0.88)
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Experimental — accuracy not yet measuredDisruption of autophagic flux and failure of autophagosomes to fuse with lysosomes leads to a build-up of vesicles seen in dystrophic neurites and cell bodies in AD, CBD and PSP, as well as in tauopathy models.
“Disruption of autophagic flux and a failure of autophagosomes to fuse with lysosomes leads to a build-up of vesicles, which can be seen in dystrophic neurites and cell bodies in AD, CBD and PSP, as well as in tauopathy models73–76.”
From Tau-targeting therapies for Alzheimer disease (2018) · cites this paper as [75]
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- Authors
- Bordi, M., Berg, M. J., Mohan, P. S., Peterhoff, C. M., Alldred, M. J., Che, S., Ginsberg, S. D., & Nixon, R. A.
- Affiliations
- Nathan Kline Institute for Psychiatric Research (US)
- Corresponding author
- Nixon, Ralph A.
- Venue
- Autophagy
- Publisher
- Informa UK Limited
- Published
- 2016-11-04
- Volume
- 12
- Issue
- 12
- Pages
- 2467-2483
- ISSN
- 1554-8627 (ISSN-L)
- 1554-8635
- PMC
- PMC5173282
- OpenAlex
- W2547593615
- Cited by
- 353
- References
- 101
- Citations by year
- 2026: 23 · 2025: 37 · 2024: 41 · 2023: 38 · 2022: 37 · 2021: 42 · 2020: 48 · 2019: 34 · 2018: 30 · 2017: 22 · 2013: 1
- FWCI
- 26.84
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Autophagy (publishedVersion, cc-by-nc)
- PubMed Central (publishedVersion, cc-by-nc)
- PubMed (publishedVersion)
- Funders
- Emory University
- National Institute on Aging (P01AG014449, R01AG043375, P50AG025688, P01AG017617)
- National Institute of Neurological Disorders and Stroke (P30NS055077)
- Topics
- Health Sciences › Medicine › Epidemiology › Autophagy in Disease and Therapy
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Calcium signaling and nucleotide metabolism
- Keywords
- Alzheimer's disease, autophagic flux, CA1 pyramidal neurons, hippocampus, autophagosome formation, lysosomal biogenesis, TFE3, TFEB, p62, LC3-II, neuritic dystrophy, autophagosome-lysosome fusion
- MeSH terms
- Autophagosomes, Aged, Aged, 80 and over, Alzheimer Disease, Autophagy, Cathepsin D, Demography, Female, Gene Expression Regulation, Humans, Lysosomes, Male, Microtubule-Associated Proteins, Middle Aged, Neurites, Basic Helix-Loop-Helix Leucine Zipper Transcription Factors, CA1 Region, Hippocampal
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