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Single-Cell Chromatin Modification Profiling Reveals Increased Epigenetic Variations with Aging
Open accessAbstract
Post-translational modifications of histone proteins and exchanges of histone variants of chromatin are central to the regulation of nearly all DNA-templated biological processes. However, the degree and variability of chromatin modifications in specific human immune cells remain largely unknown. Here, we employ a highly multiplexed mass cytometry analysis to profile the global levels of a broad array of chromatin modifications in primary human immune cells at the single-cell level. Our data reveal markedly different cell-type- and hematopoietic-lineage-specific chromatin modification patterns. Differential analysis between younger and older adults shows that aging is associated with increased heterogeneity between individuals and elevated cell-to-cell variability in chromatin modifications. Analysis of a twin cohort unveils heritability of chromatin modifications and demonstrates that aging-related chromatin alterations are predominantly driven by non-heritable influences. Together, we present a powerful platform for chromatin and immunology research. Our discoveries highlight the profound impacts of aging on chromatin modifications.
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“Reduced levels of H3K122ac extend the lifespan of budding yeast (Sen et al., 2015) and levels of H3K27ac and H3K56ac decrease in many human immune cell types (Cheung et al., 2018; Dang et al., 2009).”
From Loss of epigenetic information as a cause of mammalian aging (2023) · cites this paper as Cheung et al., 2018
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“In line with these findings, increased variation of chromatin modifications was recently observed in immune cells from elderly individuals (18).”
From Aging promotes reorganization of the CD4 T cell landscape toward extreme regulatory and effector phenotypes (2019) · cites this paper as [18]
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ACSS2 upregulation enhances neuronal resilience to aging and tau-associated neurodegeneration
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Crosstalk of Histone Modifications in the Healthy Human Immune SystemPreprint
Đermadi, D., Kalesinskas, L., Ganesan, A., Kuo, A. J., Cheung, P., Cheng, S., Dvorak, M., Scriba, T. J., Habtezion, A., Donato, M., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.01.21.477300 · Cited by 1
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Cell type-specific epigenomic variation and its association with genotype in the human breastPreprint
Hauduc, A., Steif, J., Bilenky, M., Moksa, M., Cao, Q., Ding, S., Eaves, C. J., & Hirst, M. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.16.648998 · Cited by 2
Jagannathan, P., Ty, M., Sun, S., Callaway, P. C., Rek, J. C., Press, K. D., van der Ploeg, K., Nideffer, J., Hu, Z., Klemm, S. L., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-1820334/v1 · Cited by 2
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Assessing Human Treg Suppression at Single-Cell Resolution Using Mass Cytometry
Søndergaard, J. N., Tulyeu, J., Priest, D., Sakaguchi, S., & Wing, J. B. (2025) · BIO-PROTOCOL · doi:10.21769/bioprotoc.5424 · Cited by 1
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“We characterized this landscape in Meg3 + HSCs and identified increased H3K23ac, a mark elevated in aged human haematopoietic stem and progenitor cells (HSPCs) 155 and associated with several cancers 122,156 , but whose function in HSCs was unknown.”
Choudhury, A., Burry, M. J., Kwon, W. J., Yin, X., Rallistan, A., Presti, S., Ndakwah, G. S., Cheng, E. Q., Kalaycıoğlu, M., Harris, M., et al. (2026) · EBioMedicine · doi:10.1016/j.ebiom.2026.106455 · Cited by 1
Self-citationRole of Mitochondria in Generation of Phenotypic Heterogeneity in Yeast
Dhar, R. (2020) · Journal of the Indian Institute of Science · doi:10.1007/s41745-020-00176-3 · Cited by 2
Prospects for assessing the biological and immunological age of a person by blood factors
Kurgan, N. D., Panova, E. I., Silakova, L. V., Каганский, А. М., & Александрович, Р. С. (2021) · Science and Innovations in Medicine · doi:10.35693/2500-1388-2021-6-4-19-39 · Cited by 2
Linking Aging to Cancer: The Role of Chromatin Biology
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Lan, H., Xu, S., Li, H., Guo, R., Feng, Z., & Wang, Y. (2025) · Clinical Interventions in Aging · doi:10.2147/cia.s519438
“33 It is also noteworthy that DNA methylation has recently gained increasing attention.”
Computational approaches for the systematic analysis of aging-associated molecular alterations
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EPIGENETIC ALTERATIONS IN GENE EXPRESSION IN THE AGING IMMUNE SYSTEM
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Oxidative Stress Induced Senescence Gives Rise to Transcriptionally Distinct Physiological StatesPreprint
Burnaevskiy, N., Oshima, J., & Mendenhall, A. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.05.18.492555 · Cited by 1
Memory Th1 cells modulate heterologous diseases through innate functionPreprint
Rakebrandt, N., Yassini, N., Kolz, A., Schorer, M., Lambert, K., Rauld, C., Balázs, Z., Krauthammer, M. O., Carballido, J. M., Peters, A., et al. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.03.22.533799 · Cited by 1
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“29,30 To adopt this powerful method for epigenetic studies of human brain development, we have established a custom Epi-CyTOF antibody panel consisting of >30 epigenetic readouts and 10 neural cell-type markers for the identification of major neural cell populations in the human developing…”
InfluentialTranslational traffic jam in aging brains
Dionne, O., & Laurent, B. (2025) · Science · doi:10.1126/science.adz4995 · Cited by 1
Hubbard, B. (2017) · Materials and Methods · doi:10.13070/mm.en.7.2261
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Identification of age and ethnicity specific gene expression biomarkers for immune agingPreprint
Hu, Y., Xu, Y., Mao, L., Wen, L., Xiang, J., Zhu, G., Hu, Y., Niu, H., Gao, F., Gao, L., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.02.22.432179
Characterization of aging-related changes in human hematopoietic stem cells
Amoah, A. (2021) · OPen Access Repositorium der Universität Ulm (OPARU) (Ulm University) · doi:10.18725/oparu-38410
Faculty Opinions recommendation of Understanding intrinsic hematopoietic stem cell aging.
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Ganesan, A., Đermadi, D., Kalesinskas, L., Donato, M., Sowers, R., Utz, P. J., & Khatri, P. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.07.21.501033
“57 Such subject-specific models are advantageous since individuals are exposed to different environments that are known 58 to have different effects on epigenetics and HPTMs[13, 17].”
BackgroundMethodInfluentialSelf-citationEpigenetic aging and its reversal
de la Parte, C., & Guallar, D. (2022) · Elsevier eBooks · doi:10.1016/b978-0-323-91617-2.00006-7 · Cited by 1
Nadeau, K. C., Movassagh, H., Prunicki, M. M., Kaushik, A., Zhou, X., Dunham, D., Smith, E. M., He, Z., Muench, G. R. A., Shi, M., et al. (2022) · doi:10.22541/au.166806366.68188863/v1
Single cell suppression profiling of human regulatory T cellsPreprint
Søndergaard, J. N., Tulyeu, J., Priest, D., Sakaguchi, S., & Wing, J. B. (2024) · Research Square · doi:10.21203/rs.3.rs-4327429/v1
Riccardi, F., Romano, G., Licastro, D., & Pagani, F. (2024) · PLoS ONE · doi:10.1371/journal.pone.0298965
Spatial quantification of cellular metabolism in tissues by metabolic regulome profiling
Glauner, T. A., Truxa, S., Cetin, M., Schlüter, K., Calafato, D., & Hartmann, F. J. (2024) · Elsevier eBooks · doi:10.1016/b978-0-12-822213-3.00006-1
Emerging Technologies for Epigenetic Drug Discovery
(2024) · Royal Society of Chemistry eBooks · doi:10.1039/9781837674916-part2
Metadata
- Authors
- Cheung, P., Vallania, F., Warsinske, H. C., Donato, M., Schaffert, S., Chang, S. E., Dvorak, M., Dekker, C. L., Davis, M. M., Utz, P. J., Khatri, P., & Kuo, A. J.
- Affiliations
- Stanford Medicine (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Utz, Paul J.
- Khatri, Purvesh
- Kuo, Alex J.
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2018-05
- Volume
- 173
- Issue
- 6
- Pages
- 1385-1397.e14
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC5984186
- OpenAlex
- W2801503232
- Cited by
- 323
- References
- 66
- Citations by year
- 2026: 21 · 2025: 27 · 2024: 31 · 2023: 40 · 2022: 40 · 2021: 47 · 2020: 56 · 2019: 35 · 2018: 25
- FWCI
- 14.85
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 395 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Cooperative Center for Human Immunology (U19AI057229)
- NIH (S10RR025518-01, S10RR027431-01, S10OD016318-01, 5U19AI109662-05, 5R01AI125197-02, 5U19AI057229-15, U19AI090019, 2T32AR050942-06A1, 5K12HL120001-02, 5T32AI07290-31, 5T32AI007290-29)
- Autoimmunity Center of Excellence (5U19AI110491-04, 5UM1A110498-04)
- NIAID/NIH
- Bill & Melinda Gates Foundation
- Donald E. and Delia B. Baxter Foundation
- Elizabeth F. Adler
- Henry Gustav Floren Trust
- NIH Clinical and Translational Science Award (UL1 RR025744)
- Novo Nordisk
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- chromatin modification, histone modifications, histone variants, aging, immune cells, single-cell profiling, mass cytometry, hematopoietic lineage, cellular heterogeneity, heritability, twin cohort, epigenetic variation
- MeSH terms
- Adolescent, Adult, Aged, Aging, Cell Separation, Chromatin, Diseases in Twins, Female, Flow Cytometry, Histones, Humans, Immune System, Leukocytes, Mononuclear, Male, Middle Aged, Monocytes, Protein Processing, Post-Translational, Registries, Immunophenotyping, Cell Lineage, Principal Component Analysis, Epigenesis, Genetic, Young Adult
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