Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci
Open accessAbstract
We used a collection of 708 prospectively collected autopsied brains to assess the methylation state of the brain's DNA in relation to Alzheimer's disease (AD). We found that the level of methylation at 71 of the 415,848 interrogated CpGs was significantly associated with the burden of AD pathology, including CpGs in the ABCA7 and BIN1 regions, which harbor known AD susceptibility variants. We validated 11 of the differentially methylated regions in an independent set of 117 subjects. Furthermore, we functionally validated these CpG associations and identified the nearby genes whose RNA expression was altered in AD: ANK1, CDH23, DIP2A, RHBDF2, RPL13, SERPINF1 and SERPINF2. Our analyses suggest that these DNA methylation changes may have a role in the onset of AD given that we observed them in presymptomatic subjects and that six of the validated genes connect to a known AD susceptibility gene network.
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Alterations in DNA methylation levels are involved in many diseases, including AD.
“Alterations of DNA methylation levels have been shown to be involved in many diseases, including AD [19–24].”
From Distinct sex-specific DNA methylation differences in Alzheimer’s disease (2022) · cites this paper as [19]
The Discussion reports replicated associations between altered DNA methylation and AD pathology, supporting the AD portion of the claim. It says the changes suggest a role in AD onset but explicitly cautions that the study cannot establish whether they contribute to the disease or are an early consequence of it. Thus, 'shown to be involved' is stronger than the source establishes. (LLM, conf=0.82)
Experimental — accuracy not yet measuredDNA methylation is an important epigenetic modification that regulates gene transcription and is involved in Alzheimer's disease.
“DNA methylation is an important epigenetic modification that regulates gene transcription and is known to be involved in AD”
From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [18]
The Introduction reports altered DNA methylation at 71 CpGs associated with AD pathology and says transcription of genes in those regions is independently associated with AD pathology. This supports a link between methylation, transcription and AD, but does not establish that the observed methylation changes regulate transcription; the section on cognitively non-impaired subjects says whether they contribute to the disease process remains open. Page numbers were not supplied in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measuredConsistent with previous studies, we observed the majority of these sex-specific differences were hyper-methylated in samples with AD neuropathology, for which methylation levels increased as the AD Braak stage increased.
“Consistent with previous studies [18, 19, 86, 87], we observed the majority of these sex-specific differences were hyper-methylated in samples with AD neuropathology, for which methylation levels increased as the AD Braak stage increased”
From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [18]
In ‘Discovery study to identify differentially methylated chromosomal regions’ (page unavailable), the paper reports that 82% of its differentially methylated regions were more methylated in subjects with a neuropathologic AD diagnosis. ‘Validation of the associated CpG in an independent sample set’ (page unavailable) reports associations using Braak staging, but does not establish that methylation increased with each successive stage. The paper does not identify the citing authors’ sex-specific differences as the regions it studied. (LLM, conf=0.84)
Experimental — accuracy not yet measuredDysregulated DNA methylation is an early feature of AD neuropathology in the brain.
“dysregulated DNAm has been observed as an early feature of AD neuropathology in the brain [19]”
From Distinct sex-specific DNA methylation differences in Alzheimer’s disease (2022) · cites this paper as [19]
Alterations of DNA methylation levels have been implicated in multiple neurological disorders including AD.
“Importantly, alterations of DNA methylation levels have also been implicated in multiple neurological disorders including AD [18–22]”
From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [18]
None of the 14 CpGs detected in our interaction analysis was identified in previous large-scale DNA methylation studies.
“Notably, none of the 14 CpGs detected in our interaction analysis was identified in previous large-scale DNA methylation studies [18–22]”
From Sex-specific DNA methylation differences in Alzheimer’s disease pathology (2021) · cites this paper as [18]
These reference epigenomes, combined with other genomics data, have provided functional and causal insights about several human diseases.
“These reference epigenomes, combined with other genomics data, have provided functional and causal insights about several human disease (De Jager et al., 2014; Farh et al., 2015; Yao, Tak, Berman, & Farnham, 2014).”
From Integrative Analysis of Multi-omics Data for Discovery and Functional Studies of Complex Human Diseases (2016) · cites this paper as De Jager et al., 2014
eQTLs for FURIN, CLCN3, and SNAP91 replicated in ROS/MAP with the same direction of effect; TSNARE1 and CNTN4 had alleles in the same direction but did not reach significance.
“The most significant GWAS SNP was also a significant eQTL with the same direction of effect as in CMC for FURIN (rs4702: P = 1 × 10−6), CLCN3 (rs10520163: P = 9 × 10−6), and SNAP91 (rs3798869: P = 3 × 10−4); TSNARE1 (rs4129585: P = 0.057) and CNTN4 (rs17194490: P = 0.07) also had alleles in the same direction of effect as in CMC but did not reach significance.”
From Gene expression elucidates functional impact of polygenic risk for schizophrenia (2016) · cites this paper as [26]
Two independent genome-wide studies recently identified a differentially methylated region in the ANK1 gene as associated with the burden of AD pathology.
“and two independent genome-wide studies recently identified a differentially methylated region in the ANK1 gene as associated with the burden of AD pathology [198, 199].”
From Genetic architecture of Alzheimer's disease (2020) · cites this paper as [199]
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Microglial Malfunction: The Third Rail in the Development of Alzheimer's Disease
Mhatre, S. D., Tsai, C. A., Rubin, A. J., James, M. L., & Andreasson, K. I. (2015) · Trends in Neurosciences · doi:10.1016/j.tins.2015.08.006 · Cited by 134 · see citing works
Mechanisms and Disease Associations of Haplotype-Dependent Allele-Specific DNA Methylation
Do, C., Lang, C. F., Lin, J. P., Darbary, H. K., Krupska, I., Gaba, A., Petukhova, L., Vonsattel, J., GALLAGHER, M. P., Goland, R., et al. (2016) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2016.03.027 · Cited by 125 · see citing works
- Authors
- De Jager, P. L., Srivastava, G., Lunnon, K., Burgess, J., Schalkwyk, L. C., Yu, L., Eaton, M. L., Keenan, B. T., Ernst, J., McCabe, C., Tang, A., Raj, T., Replogle, J., Brodeur, W., Gabriel, S., Chai, H. S., Younkin, C., Younkin, S. G., Zou, F., Szyf, M., Epstein, C. B., Schneider, J. A., Bernstein, B. E., Meissner, A., Ertekin-Taner, N., Chibnik, L. B., Kellis, M., Mill, J., & Bennett, D. A.
- Affiliations
- Broad Institute (US)
- King's College London (GB)
- Mayo Clinic (US)
- Rush University Medical Center (US)
- Brigham and Women's Hospital (US)
- Corresponding author
- Bennett, David A
- ORCID
- Venue
- Nature Neuroscience
- Published
- 2014-08-17
- Volume
- 17
- Issue
- 9
- Pages
- 1156-1163
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- PMC
- PMC4292795
- OpenAlex
- W2074750860
- Cited by
- 956
- References
- 62
- Citations by year
- 2026: 49 · 2025: 77 · 2024: 74 · 2023: 69 · 2022: 82 · 2021: 94 · 2020: 93 · 2019: 94 · 2018: 93 · 2017: 71 · 2016: 84 · 2015: 59 · 2014: 17
- FWCI
- 31.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Open Access at Essex (University of Essex) (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- eScholarship (California Digital Library) (submittedVersion)
- Figshare (submittedVersion)
- Research Portal (King's College London) (submittedVersion)
- Open Research Exeter (University of Exeter) (submittedVersion)
- Funders
- National Institute on Aging (R01AG017917, P30-AG 10161, K25AG041906, R01AG036039, R01‐AG17917, R01 AG15819, R01AG018023, R01AG036836, U01AG046152, R01-AG18023, AG036039, R01AG036042, R01AG015819, P30AG010161, RC2AG036547, R01AG032990, U01AG046139, RF1AG015819, RF1AG036042, P50AG016574)
- National Human Genome Research Institute (R01HG004037)
- National Institute of Neurological Disorders and Stroke (R01NS080820)
- National Institute of Environmental Health Sciences (U01ES017155)
- National Center for Research Resources (KL2RR024151)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
- Health Sciences › Medicine › Physiology › Alzheimer's disease research and treatments
- Keywords
- Alzheimer's disease, DNA methylation, ANK1, BIN1, RHBDF2, ABCA7, differentially methylated regions, gene expression, preclinical Alzheimer's disease, epigenome-wide association study
- MeSH terms
- Aged, Aged, 80 and over, Alzheimer Disease, Amyloidosis, Brain, Carrier Proteins, Female, Humans, Male, Middle Aged, Nuclear Proteins, Ankyrins, CpG Islands, DNA Methylation, Genetic Predisposition to Disease, Tumor Suppressor Proteins, Intracellular Signaling Peptides and Proteins, Adaptor Proteins, Signal Transducing, Genome-Wide Association Study, Protein Interaction Maps
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