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An epigenome-wide association study of sex-specific chronological ageing
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Abstract
Background: Advanced age is associated with cognitive and physical decline and is a major risk factor for a multitude of disorders. There is also a gap in life expectancy between males and females. DNA methylation differences have been shown to be associated with both age and sex. Here, we investigate age-by-sex differences in blood-based DNA methylation in an unrelated cohort of 2586 individuals between the ages of 18 and 87 years, with replication in a further 4450 individuals between the ages of 18 and 93 years. Methods: Linear regression models were applied, with stringent genome-wide significance thresholds ( p < 3.6 × 10 −8 ) used in both the discovery and replication data. A second, highly conservative mixed linear model method that better controls the false-positive rate was also applied, using the same genome-wide significance thresholds. Results: Using the linear regression method, 52 autosomal and 597 X-linked CpG sites, mapping to 251 unique genes, replicated with concordant effect size directions in the age-by-sex interaction analysis. The site with the greatest difference mapped to GAGE10 , an X-linked gene. Here, DNA methylation levels remained stable across the male adult age range (DNA methylation by age r = 0.02) but decreased across female adult age range (DNA methylation by age r = − 0.61). One site (cg23722529) with a significant age-by-sex interaction also had a quantitative trait locus (rs17321482) that is a genome-wide significant variant for prostate cancer. The mixed linear model method identified 11 CpG sites associated with the age-by-sex interaction. Conclusion: The majority of differences in age-associated DNA methylation trajectories between sexes are present on the X chromosome. Several of these differences occur within genes that have been implicated in sexually dimorphic traits.
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“As advanced aging is the strongest factor for AD, we also compared our results with those from Yusipov et al. [94] and McCartney et al. [35], which identified 8 and 52 autosomal CpGs differentially affected by aging, but we did not find any overlap with these previous studies.”
From Distinct sex-specific DNA methylation differences in Alzheimer’s disease (2022) · cites this paper as [35]
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Additional file 4 of Blood-based epigenome-wide analyses of cognitive abilities
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Self-citationAdditional file 3 of Blood-based epigenome-wide analyses of cognitive abilities
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Self-citationAdditional file 1 of Blood-based epigenome-wide analyses of cognitive abilities
McCartney, D. L., Hillary, R. F., Conole, E. L. S., Banos, D. T., Gadd, D. A., Walker, R. M., Nangle, C., Flaig, R., Campbell, A., Murray, A. D., et al. (2022) · Figshare · doi:10.6084/m9.figshare.18585799
Self-citationAdditional file 1 of Distinct sex-specific DNA methylation differences in Alzheimer’s disease
C. Silva, T., Zhang, W., Young, J. I., Gomez, L., Schmidt, M. A., Varma, A., Chen, X. S., Martin, E. R., & Wang, L. (2022) · Figshare · doi:10.6084/m9.figshare.21129953
Additional file 2 of Refining epigenetic prediction of chronological and biological age
Bernabeu, E., McCartney, D. L., Gadd, D. A., Hillary, R. F., Lu, A. T., Murphy, L., Wrobel, N., Campbell, A., Harris, S. E., Liewald, D. C. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26571943
Self-citationAdditional file 3 of Refining epigenetic prediction of chronological and biological age
Bernabeu, E., McCartney, D. L., Gadd, D. A., Hillary, R. F., Lu, A. T., Murphy, L., Wrobel, N., Campbell, A., Harris, S. E., Liewald, D. C. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26571946
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Self-citationAdditional file 4 of Refining epigenetic prediction of chronological and biological age
Bernabeu, E., McCartney, D. L., Gadd, D. A., Hillary, R. F., Lu, A. T., Murphy, L., Wrobel, N., Campbell, A., Harris, S. E., Liewald, D. C. M., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26571949
Self-citationAdditional file 5 of Ageing-associated changes in DNA methylation in X and Y chromosomes
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Additional file 2 of Sex-biased genetic regulation of inflammatory proteins in the Dutch population
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Additional file 2 of Blood-based epigenome-wide analyses of cognitive abilities
McCartney, D. L., Hillary, R. F., Conole, E. L. S., Banos, D. T., Gadd, D. A., Walker, R. M., Nangle, C., Flaig, R., Campbell, A., Murray, A. D., et al. (2022) · Figshare · doi:10.6084/m9.figshare.18585802
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Metadata
- Authors
- McCartney, D. L., Zhang, F., Hillary, R. F., Zhang, Q., Stevenson, A. J., Walker, R. M., Bermingham, M. L., Boutin, T., Morris, S. W., Campbell, A., Murray, A. D., Whalley, H. C., Porteous, D. J., Hayward, C., Evans, K. L., Chandra, T., Deary, I. J., McIntosh, A. M., Yang, J., Visscher, P. M., McRae, A. F., & Marioni, R. E.
- Affiliations
- Institute of Genetics and Cancer (GB)
- The University of Queensland (AU)
- University of Aberdeen (GB)
- Royal Edinburgh Hospital (GB)
- University of Edinburgh (GB)
- Corresponding author
- Marioni, Riccardo E.
- ORCID
- McCartney, Daniel L.
- Zhang, Futao
- Hillary, Robert F.
- Zhang, Qian
- Stevenson, Anna J.
- Walker, Rosie M.
- Bermingham, Mairead L.
- Boutin, Thibaud
- Campbell, Archie
- Murray, Alison D.
- Whalley, Heather C.
- Porteous, David J.
- Hayward, Caroline
- Evans, Kathryn L.
- Chandra, Tamir
- Deary, Ian J.
- McIntosh, Andrew M.
- Yang, Jian
- Visscher, Peter M.
- McRae, Allan F.
- Marioni, Riccardo E.
- Venue
- Genome Medicine
- Published
- 2019-12-31
- Volume
- 12
- Issue
- 1
- Pages
- 1-1
- ISSN
- 1756-994X (ISSN-L)
- PMC
- PMC6938636
- OpenAlex
- W2992920781
- Cited by
- 152
- References
- 63
- Citations by year
- 2026: 7 · 2025: 32 · 2024: 26 · 2023: 17 · 2022: 26 · 2021: 40 · 2020: 4
- FWCI
- 6.12
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Genome Medicine (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Aberdeen University Research Archive (Aberdeen University) (submittedVersion)
- Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Funders
- Wellcome Trust (104036/Z/14/Z, 108890/Z/15/Z)
- Alzheimer’s Research UK (ARUK-PG2017B-10)
- National Health and Medical Research Council (1078037, 1083656)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- DNA methylation, chronological aging, sex differences, X chromosome, epigenome-wide association study, sexually dimorphic traits, blood DNA methylation, linear mixed models
- MeSH terms
- Adult, Aged, Aging, Female, Gene Expression Regulation, Humans, Male, Middle Aged, Sex Characteristics, Linear Models, CpG Islands, DNA Methylation, Quantitative Trait Loci, Chromosomes, Human, X, Genome-Wide Association Study
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