Decreased epigenetic age of PBMCs from Italian semi-supercentenarians and their offspring
Open accessAbstract
Given the dramatic increase in ageing populations, it is of great importance to understand the genetic and molecular determinants of healthy ageing and longevity. Semi-supercentenarians (subjects who reached an age of 105-109 years) arguably represent the gold standard of successful human ageing because they managed to avoid or postpone the onset of major age-related diseases. Relatively few studies have looked at epigenetic determinants of extreme longevity in humans. Here we test whether families with extreme longevity are epigenetically distinct from controls according to an epigenetic biomarker of ageing which is known as "epigenetic clock". We analyze the DNA methylation levels of peripheral blood mononuclear cells (PBMCs) from Italian families constituted of 82 semi-supercentenarians (mean age: 105.6 ± 1.6 years), 63 semi-supercentenarians' offspring (mean age: 71.8 ± 7.8 years), and 47 age-matched controls (mean age: 69.8 ± 7.2 years). We demonstrate that the offspring of semi-supercentenarians have a lower epigenetic age than age-matched controls (age difference=5.1 years, p=0.00043) and that centenarians are younger (8.6 years) than expected based on their chronological age. By contrast, no significant difference could be observed for estimated blood cell counts (such as naïve or exhausted cytotoxic T cells or helper T cells). Future studies will be needed to replicate these findings in different populations and to extend them to other tissues. Overall, our results suggest that epigenetic processes might play a role in extreme longevity and healthy human ageing.
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Attempts to both remove and exploit confounding by cell composition changes have not altered the weak associations with mortality and other health outcomes.
“However, attempts to both remove and exploit the confounding by cell composition changes have not altered the weak associations with mortality and other health outcomes60.”
From Measuring biological age using omics data (2022) · cites this paper as [60]
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An epigenetic biomarker of aging for lifespan and healthspan
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Self-citationInflammaging: a new immune–metabolic viewpoint for age-related diseases
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Self-citationDNA methylation-based biomarkers and the epigenetic clock theory of ageing
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Self-citationDNA methylation GrimAge strongly predicts lifespan and healthspan
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Self-citationImmunosenescence and Inflamm-Aging As Two Sides of the Same Coin: Friends or Foes?
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Self-citationThe Continuum of Aging and Age-Related Diseases: Common Mechanisms but Different Rates
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Self-citationEpigenetic clock analysis of diet, exercise, education, and lifestyle factors
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Self-citationAn epigenetic clock analysis of race/ethnicity, sex, and coronary heart disease
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Self-citationDNA Methylation Clocks in Aging: Categories, Causes, and Consequences
Field, A. E., Robertson, N., Wang, T., Havas, A. P., Ideker, T., & Adams, P. D. (2018) · Molecular Cell · doi:10.1016/j.molcel.2018.08.008 · Cited by 622 · see citing works
Immunosenescence and inflammaging in the aging process: age-related diseases or longevity?
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Measuring biological age using omics data
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Menopause accelerates biological aging
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Self-citationBiological Versus Chronological Aging
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Self-citationUsing DNA methylation profiling to evaluate biological age and longevity interventions
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Multi-tissue DNA methylation age predictor in mouse
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Physical Activity and Brain Health
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The integration of inflammaging in age-related diseases
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Biomarkers of Aging: From Function to Molecular Biology
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Interconnections between Inflammageing and Immunosenescence during Ageing
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An epigenetic clock for gestational age at birth based on blood methylation data
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Self-citationThe Healthy Immigrant Effect and Aging in the United States and Other Western Countries
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Self-citationGut microbiota changes in the extreme decades of human life: a focus on centenarians
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Self-citationTraumatic stress and accelerated DNA methylation age: a meta-analysis
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Underlying features of epigenetic aging clocks in vivo and in vitro.
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Huntington's disease accelerates epigenetic aging of human brain and disrupts DNA methylation levels
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Self-citationMaintenance of age in human neurons generated by microRNA-based neuronal conversion of fibroblasts
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Self-citationGWAS of epigenetic aging rates in blood reveals a critical role for TERT
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Self-citationA multi-tissue full lifespan epigenetic clock for mice
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Self-citationLong-term exposure to air pollution is associated with biological aging
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Self-citationObesity accelerates epigenetic aging in middle-aged but not in elderly individuals
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Inflammaging and human longevity in the omics era
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Self-citationAn epigenetic aging clock for dogs and wolves
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Self-citationDetermination of Biological Age: Geriatric Assessment vs Biological Biomarkers
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Cell‐free DNA as a biomarker of aging
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Self-citationAccelerated epigenetic aging in Werner syndrome
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Self-citationAge-related DNA methylation changes are sex-specific: a comprehensive assessment
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Self-citationGenetic and epigenetic regulation of human aging and longevity
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Methylation across the central dogma in health and diseases: new therapeutic strategies
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DNA Methylation Clocks and Their Predictive Capacity for Aging Phenotypes and Healthspan
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Simplified Assay for Epigenetic Age Estimation in Whole Blood of Adults
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Systematic underestimation of the epigenetic clock and age acceleration in older subjects
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Self-citationInflammaging 2018: An update and a model
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Self-citationBack to the future: Epigenetic clock plasticity towards healthy aging
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Forensic individual age estimation with DNA: From initial approaches to methylation tests.
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Abnormal Epigenetic Regulation of Immune System during Aging
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Maintained memory in aging is associated with young epigenetic age
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Self-citationPerinatally acquired HIV infection accelerates epigenetic aging in South African adolescents
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Self-citationAging, exceptional longevity and comparisons of the Hannum and Horvath epigenetic clocks
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Nutrition and Inflammation: Are Centenarians Similar to Individuals on Calorie-Restricted Diets?
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Self-citationIschemic stroke patients are biologically older than their chronological age
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Epigenetic clock analysis in long-term meditators
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Castration delays epigenetic aging and feminizes DNA methylation at androgen-regulated loci
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Self-citationAnalysis of Epigenetic Age Acceleration and Healthy Longevity Among Older US Women
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Self-citationThe epigenetic aging, obesity, and lifestyle
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A longitudinal study of DNA methylation as a potential mediator of age-related diabetes risk
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The Aging Thyroid: A Reappraisal Within the Geroscience Integrated Perspective
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Self-citationGenetic variants near MLST8 and DHX57 affect the epigenetic age of the cerebellum
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Self-citationDNA methylation signatures in panic disorder
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- Authors
- Horvath, S., Pirazzini, C., Bacalini, M. G., Gentilini, D., Di Blasio, A. M., Delledonne, M., Mari, D., Arosio, B., Monti, D., Passarino, G., De Rango, F., D'Aquila, P., Giuliani, C., Marasco, E., Collino, S., Descombes, P., Garagnani, P., & Franceschi, C.
- Affiliations
- University of California, Los Angeles (US)
- University of Bologna (IT)
- Istituto di Genomica Applicata (IT)
- IRCCS Istituto Auxologico Italiano (IT)
- Istituto Auxologico Italiano IRCCS, Cusano Milanino, 20095 Milan, Italy
- University of Verona (IT)
- University of Milan (IT)
- University of Florence (IT)
- University of Calabria (IT)
- Department of Cell Biology, University of Calabria, 87036 Rende, Italy
- École Polytechnique Fédérale de Lausanne (CH)
- IRCCS Azienda Ospedliero-Universitaria di Bologna Policlinico di Sant'Orsola (IT)
- Institute of Organic Synthesis and Photoreactivity (IT)
- ORCID
- Venue
- Aging
- Publisher
- Impact Journals, LLC
- Published
- 2015-12-15
- Volume
- 7
- Issue
- 12
- Pages
- 1159-1170
- ISSN
- 1945-4589 (ISSN-L)
- PMC
- PMC4712339
- OpenAlex
- W2333822468
- Cited by
- 316
- References
- 83
- Citations by year
- 2026: 11 · 2025: 16 · 2024: 21 · 2023: 31 · 2022: 38 · 2021: 37 · 2020: 29 · 2019: 32 · 2018: 44 · 2017: 34 · 2016: 22 · 2015: 1
- FWCI
- 14.61
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- cc-by
- Locations
- Aging (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion, cc-by)
- Florence Research (University of Florence) (submittedVersion, other-oa)
- Funders
- European Commission (305522, 602757, 259679, 634821)
- National Institutes of Health (PRIN 2009)
- National Institute on Aging (U34AG051425, R01AG042511)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Aging › Genetics, Aging, and Longevity in Model Organisms
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Keywords
- exceptional longevity, epigenetic clocks, DNA methylation, epigenetic age, peripheral blood mononuclear cells, healthy aging, T cell subsets
- MeSH terms
- Aged, 80 and over, Aging, Biological Clocks, Female, Humans, Italy, Leukocytes, Mononuclear, Male, Models, Biological, DNA Methylation, Epigenesis, Genetic
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