Impact of paternal education on epigenetic ageing in adolescence and mid-adulthood: a multi-cohort study in the USA and Mexico

Author:

Joyce Brian T12ORCID,Gao Tao12,Koss Kalsea3,Zheng Yinan12,Cardenas Andres4,Heiss Jonathan5,Just Allan5ORCID,Zhang Kai6,van Horn Linda1ORCID,Allen Norrina Bai1,Greenland Philip1,Cohen Sheldon7,Gordon-Larsen Penny8,Mitchell Colter9,McLanahan Sara10,Schneper Lisa11,Notterman Daniel11,Rifas-Shiman Sheryl L12,Oken Emily12ORCID,Hivert Marie-France1213,Wright Robert5,Baccarelli Andrea14,Lloyd-Jones Donald1,Hou Lifang12

Affiliation:

1. Department of Preventive Medicine, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

2. Center for Global Oncology, Institute for Global Health, Northwestern University Feinberg School of Medicine, Chicago, IL, USA

3. Department of Human Development and Family Science, University of Georgia, Athens, GA, USA

4. Division of Environmental Health Sciences, School of Public Health, University of California, Berkeley, CA, USA

5. Department of Environmental Medicine and Public Health, Icahn School of Medicine at Mt. Sinai, New York, NY, USA

6. Department of Epidemiology, Human Genetics, and Environmental Sciences, School of Public Health, The University of Texas Health Science Center at Houston, Houston, TX, USA

7. Department of Psychology, Carnegie Mellon University, Pittsburgh, PA, USA

8. Department of Nutrition, Gillings School of Global Public Health, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA

9. Center for Human Growth and Development, University of Michigan, Ann Arbor, MI, USA

10. Department of Sociology, Princeton University, Princeton, NJ, USA

11. Department of Molecular Biology, Princeton University, Princeton, NJ, USA

12. Division of Chronic Disease Research Across the Lifecourse, Department of Population Medicine, Harvard Medical School and Harvard Pilgrim Health Care Institute, Boston, MA, USA

13. Department of Endocrinology, Diabetes Unit, Massachusetts General Hospital, Boston, MA, USA

14. Department of Environmental Health Sciences, Columbia University, New York, NY, USA

Abstract

Abstract Background Both parental and neighbourhood socio-economic status (SES) are linked to poorer health independently of personal SES measures, but the biological mechanisms are unclear. Our objective was to examine these influences via epigenetic age acceleration (EAA)—the discrepancy between chronological and epigenetic ages. Methods We examined three USA-based [Coronary Artery Risk Disease in Adults (CARDIA) study, Fragile Families and Child Wellbeing Study (FFCWS) and Programming Research in Obesity, Growth, Environment and Social Stressors (PROGRESS)] and one Mexico-based (Project Viva) cohort. DNA methylation was measured using Illumina arrays, personal/parental SES by questionnaire and neighbourhood disadvantage from geocoded address. In CARDIA, we examined the most strongly associated personal, parental and neighbourhood SES measures with EAA (Hannum’s method) at study years 15 and 20 separately and combined using a generalized estimating equation (GEE) and compared with other EAA measures (Horvath’s EAA, PhenoAge and GrimAge calculators, and DunedinPoAm). Results EAA was associated with paternal education in CARDIA [GEEs: βsome college = −1.01 years (−1.91, −0.11) and β<high school = 1.05 (0.09, 2.01) vs college graduates] and FFCWS [GEEs: β<high school = 0.62 (0.00, 1.24)]. We found stronger associations for some paternal education categories among White adults (for GEE, βsome college = −1.39 (−2.41, −0.38)], men (βsome college = −1.76 (−3.16, −0.35)] and women [β<high school = 1.77 (0.42, 3.11)]. Conclusions These findings suggest that EAA captures epigenetic impacts of paternal education independently of personal SES later in life. Longitudinal studies should explore these associations at different life stages and link them to health outcomes. EAA could be a useful biomarker of SES-associated health and provide important insight into the pathogenesis and prevention of chronic disease.

Funder

National Heart, Lung, and Blood Institute (NHLBI) in collaboration with the University of Alabama at Birmingham

Northwestern University

University of Minnesota

Kaiser Foundation Research Institute

Intramural Research Program of the National Institute on Aging (NIA) and an intra-agency agreement between NIA and NHLBI

American Heart Association

Northwestern University and Lurie Children’s Hospital

National Institutes of Health

NIH-NIEHS

Leaves of Grass Foundation and the Klarman Scholars Program at Beth Israel Deaconess Medical Center

Publisher

Oxford University Press (OUP)

Subject

General Medicine,Epidemiology

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