Epigenetic dysregulation of enhancers in neurons is associated with Alzheimer’s disease pathology and cognitive symptoms
Open accessAbstract
Epigenetic control of enhancers alters neuronal functions and may be involved in Alzheimer’s disease (AD). Here, we identify enhancers in neurons contributing to AD by comprehensive fine-mapping of DNA methylation at enhancers, genome-wide. We examine 1.2 million CpG and CpH sites in enhancers in prefrontal cortex neurons of individuals with no/mild, moderate, and severe AD pathology ( n = 101). We identify 1224 differentially methylated enhancer regions; most of which are hypomethylated at CpH sites in AD neurons. CpH methylation losses occur in normal aging neurons, but are accelerated in AD. Integration of epigenetic and transcriptomic data demonstrates a pro-apoptotic reactivation of the cell cycle in post-mitotic AD neurons. Furthermore, AD neurons have a large cluster of significantly hypomethylated enhancers in the DSCAML1 gene that targets BACE1 . Hypomethylation of these enhancers in AD is associated with an upregulation of BACE1 transcripts and an increase in amyloid plaques, neurofibrillary tangles, and cognitive decline.
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Hypomethylated enhancer regions have been identified in AD neurons, where they may affect expression of AD-relevant genes including tau kinases and BACE1.
“Hypomethylated enhancer regions have been recently identified in AD neurons, where they may affect the expression of AD-relevant genes including tau kinases and BACE1 [512].”
From Molecular and cellular mechanisms underlying the pathogenesis of Alzheimer’s disease (2020) · cites this paper as [512]
Hypomethylation of a large enhancer cluster in CpH sites in prefrontal cortex neurons of severe AD cases, including DSCAML1 enhancers, likely upregulates BACE1 transcripts in AD.
“More recently, a large cluster of significantly hypomethylated enhancers in the CpH sites were identified in prefrontal cortex neurons of individuals with severe AD pathology, and hypomethylation of these enhancers in the DSCAML1 gene likely upregulate BACE1 transcripts in AD (17).”
From The β-Secretase BACE1 in Alzheimer’s Disease (2021) · cites this paper as [17]
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Xu, C., Fu, X.-Y., Qin, H., & Yao, K. (2024) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2024.1499719 · Cited by 17 · see citing works
Ravel‐Godreuil, C., Massiani-Beaudoin, O., Mailly, P., Prochiantz, A., Joshi, R. L., & Fuchs, J. (2021) · iScience · doi:10.1016/j.isci.2021.102756 · Cited by 18 · see citing works
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Neuroepigenetic Mechanisms of Action of Ultrashort Peptides in Alzheimer’s Disease
Ilina, A., Khavinson, V., Linkova, N. S., & Petukhov, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23084259 · Cited by 17 · see citing works
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A unified model of dementias and age‐related neurodegeneration
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- Authors
- Li, P., Marshall, L., Oh, G., Jakubowski, J. L., Groot, D., He, Y., Wang, T., Petronis, A., & Labrie, V.
- Affiliations
- Van Andel Institute (US)
- Centre for Addiction and Mental Health (CA)
- Washington University in St. Louis (US)
- Corresponding author
- Labrie, Viviane
- ORCID
- Venue
- Nature Communications
- Published
- 2019-05-21
- Volume
- 10
- Issue
- 1
- Pages
- 2246-2246
- ISSN
- 2041-1723 (ISSN-L)
- PMC
- PMC6529540
- OpenAlex
- W2945063373
- Cited by
- 234
- References
- 80
- Citations by year
- 2026: 15 · 2025: 22 · 2024: 31 · 2023: 30 · 2022: 41 · 2021: 51 · 2020: 34 · 2019: 10
- FWCI
- 12.73
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Nature Communications (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Digital Commons@Becker (Washington University School of Medicine) (submittedVersion, cc-by)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- Scottish Rite Charitable Foundation of Canada (15110)
- U.S. Department of Defense (PD170089)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Keywords
- Alzheimer's disease, prefrontal cortex neurons, BACE1, amyloid plaques, neurofibrillary tangles, cognitive decline, cell cycle re-entry, apoptosis, fine mapping
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Enhancer Elements, Genetic, Female, Humans, Male, Middle Aged, Neurons, Cohort Studies, Cell Adhesion Molecules, Up-Regulation, Aspartic Acid Endopeptidases, Prefrontal Cortex, CpG Islands, DNA Methylation, Epigenesis, Genetic, Amyloid Precursor Protein Secretases, Cognitive Dysfunction
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