ALSPAC; Aging; DNA methylation; Pace of Ageing; biological pathways; epigenome-wide association studies; financial issues
Abstract :
[en] Early-life adversity as neglect or low socioeconomic status is associated with negative physical/mental health outcomes and plays an important role in health trajectories through life. The early-life environment has been shown to be encoded as changes in epigenetic markers that are retained for many years.We investigated the effect of maternal major financial problems (MFP) and material deprivation (MD) on their children's epigenome in the Avon Longitudinal Study of Parents and Children (ALSPAC) cohort. Epigenetic aging, measured with epigenetic clocks, was weakly accelerated with increased MFP. In subsequent EWAS, MFP, and MD showed strong, independent programing effects on children's genomes. MFP in the period from birth to age seven was associated with genome-wide epigenetic modifications on children's genome visible at age 7 and partially remaining at age 15.These results support the hypothesis that physiological processes at least partially explain associations between early-life adversity and health problems later in life. Both maternal stressors (MFP/MD) had similar effects on biological pathways, providing preliminary evidence for the mechanisms underlying the effects of low socioeconomic status in early life and disease outcomes later in life. Understanding these associations is essential to explain disease susceptibility, overall life trajectories and the transition from health to disease.
Disciplines :
Genetics & genetic processes
Author, co-author :
Holuka, Cyrielle ✱; Department of Infection and Immunity, Immune Endocrine Epigenetics Research Group, Luxembourg Institute of Health, Esch-sur-Alzette, Luxembourg ; Faculty of Science, University of Luxembourg, Belval, Luxembourg
Menta, Giorgia; Luxembourg Institute of Socio-Economic Research (LISER), Esch-sur-Alzette, Luxembourg
Caro, Juan Carlos; Department of Industrial Engineering, Universidad de Concepcion, Talcahuano, Chile
VÖGELE, Claus ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Health and Behaviour
D'AMBROSIO, Conchita ; University of Luxembourg > Faculty of Humanities, Education and Social Sciences (FHSE) > Department of Behavioural and Cognitive Sciences (DBCS) > Health and Behaviour
Turner, Jonathan D ✱; Department of Infection and Immunity, Immune Endocrine Epigenetics Research Group, Luxembourg Institute of Health, Esch-sur-Alzette, Luxembourg
✱ These authors have contributed equally to this work.
External co-authors :
yes
Language :
English
Title :
Developmental epigenomic effects of maternal financial problems.
Alegría-Torres, J. A., Baccarelli, A., & Bollati, V. (2011). Epigenetics and lifestyle. Epigenomics, 3 (3), 267-277. https://doi.org/10.2217/epi.11.22
Alfano, R., Guida, F., Galobardes, B., Chadeau-Hyam, M., Delpierre, C., Ghantous, A., Henderson, J., Herceg, Z., Jain, P., Nawrot, T. S., Relton, C., Vineis, P., Castagné R. B., & Plusquin, M. (2019). Socioeconomic position during pregnancy and DNA methylation signatures at three stages across early life: Epigenome-wide association studies in the ALSPAC birth cohort. International Journal of Epidemiology, 48 (1), 30-44. https://doi.org/10.1093/ije/dyy259
Bachmann, M. D. C., Bellalta, S. D., Basoalto, R., Gómez-Valenzuela, F., Jalil, Y., Lépez, M., Matamoros, A., & von Bernhardi, R. (2020). The challenge by multiple environmental and biological factors induce inflammation in aging: Their role in the promotion of chronic disease. Frontiers in Immunology, 11, 570083. https://doi.org/10.3389/fimmu.2020.570083
Batten, S. V., Aslan, M., Maciejewski, P. K., & Mazure, C. M. (2004). Childhood maltreatment as a risk factor for adult cardiovascular disease and depression. The Journal of Clinical Psychiatry, 65 (2), 249-254. https://doi.org/10.4088/jcp.v65n0217
Belsky, D. W., Caspi, A., Arseneault, L., Baccarelli, A., Corcoran, D. L., Gao, X., Hannon, E., Harrington, H. L., Rasmussen, L. J. H., Houts, R., Huffman, K., Kraus, W. E., Kwon, D., Mill, J., Pieper, C. F., Prinz, J. A., Poulton, R., Schwartz, J., Sugden, K., Vokonas, P., Williams, B. S., & Moffitt, T. E. (2020). Quantification of the pace of biological aging in humans through a blood test, the DunedinPoAm DNA methylation algorithm. Elife, 9, e54870. https://doi.org/10.7554/eLife.54870
Belsky, D. W., Caspi, A., Houts, R., Cohen, H. J., Corcoran, D. L., Danese, A., Harrington, H. L., Israel, S., Levine, M. E., Schaefer, J. D., Sugden, K., Williams, B., Yashin, A. I., Poulton, R., & Moffitt, T. E. (2015). Quantification of biological aging in young adults. Proceedings of the National Academy of Sciences, 112 (30), E4104-4110. https://doi.org/10.1073/pnas.1506264112
Belsky, J., & Shalev, I. (2016). Contextual adversity, telomere erosion, pubertal development, and health: Two models of accelerated aging, or one? Development and Psychopathology, 28 (4pt2), 1367-1383. https://doi.org/10.1017/S0954579416000900
Borsche, M., Pereira, S. L., Klein, C., & Grünewald, A. (2021). Mitochondria and parkinson's disease: Clinical, molecular, and translational aspects. J Parkinsons Dis, 11 (1), 45-60. https://doi.org/10.3233/jpd-201981
Bossert, W., Chakravarty, S. R., & D'Ambrosio, C. (2013). Multidimensional poverty and material deprivation with discrete data. Review of Income and Wealth, 59 (1), 29-43. https://doi.org/10.1111/j.1475-4991.2012.00519.x
Boyd, A., Golding, J., Macleod, J., Lawlor, D. A., Fraser, A., Henderson, J., Molloy, L., Ness, A., Ring, S., & Davey Smith, G. (2013). Cohort profile: The 'children of the 90s' - the index offspring of the avon longitudinal study of parents and children. International Journal of Epidemiology, 42 (1), 111-127. https://doi.org/10.1093/ije/dys064
Butterfield, D. A., & Halliwell, B. (2019). Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nature Reviews Neuroscience, 20 (3), 148-160. https://doi.org/10.1038/s41583-019-0132-6
Caro, J. C., Holuka, C., Menta, G., Turner, J. D., Vögele, C., & D'Ambrosio, C. (2023). Children's internalizing behavior development is heterogeneously associated with the pace of epigenetic aging. Biological Psychology, 176, 108463. https://doi.org/10.1016/j.biopsycho.2022.108463
Clark, A. E., D'Ambrosio, C., & Barazzetta, M. (2021). Childhood circumstances and young adulthood outcomes: The role of mothers' financial problems. Health Economics, 30 (2), 342-357. https://doi.org/10.1002/hec.4194
Clark, A. E., D'Ambrosio, C., & Rohde, N. (2021). Prenatal economic shocks and birth outcomes in UK cohort data. Economics & Human Biology, 41, 100964. https://doi.org/10.1016/j.ehb.2020.100964
Dalmer, T. R. A., & Clugston, R. D. (2019). Gene ontology enrichment analysis of congenital diaphragmatic hernia-associated genes. Pediatric Research, 85 (1), 13-19. https://doi.org/10.1038/s41390-018-0192-8
Elwenspoek M. M. C., Hengesch X., Leenen F. A. D., Schritz A., Sias K., Schaan V. K., Mériaux S. B., Schmitz S., Bonnemberger F., Schächinger H., Vögele C., Turner J. D., & Muller C. P. (2017). Proinflammatory T cell status associated with early life adversity. Journal of Immunology, 199 (12), 4046-4055. https://doi.org/10.4049/jimmunol.1701082
Fernandes, S. B., Patil, N. D., Meriaux, S., Theresine, M., Muller, C. P., Leenen, F. A. D., Elwenspoek, M. M. C., Zimmer, J., & Turner, J. D. (2021). Unbiased screening identifies functional differences in NK cells after early life psychosocial stress. Frontiers in Immunology, 12, 674532. https://doi.org/10.3389/fimmu.2021.674532
Fiorito, G., McCrory, C., Robinson, O., Carmeli, C., Rosales, C. O., Zhang, Y., Colicino, E., Dugué P.-A., Artaud, F., McKay, G. J., Jeong, A., Mishra, P. P., Nøst, T. H., Krogh, V., Panico, S., Sacerdote, C., Tumino, R., Palli, D., Matullo, G., Guarrera, S.,... the BIOS Consortiumthe Lifepath consortium (2019). Socioeconomic position, lifestyle habits and biomarkers of epigenetic aging: A multi-cohort analysis. Aging (Albany NY), 11 (7), 2045-2070. https://doi.org/10.18632/aging.101900
Fraser, A., Macdonald-Wallis, C., Tilling, K., Boyd, A., Golding, J., Davey Smith, G., Henderson, J., Macleod, J., Molloy, L., Ness, A., Ring, S., Nelson, S. M., & Lawlor, D. A. (2013). Cohort profile: The avon longitudinal study of parents and children: ALSPAC mothers cohort. International Journal of Epidemiology, 42 (1), 97-110. https://doi.org/10.1093/ije/dys066
Galobardes, B., Smith, G. D., & Lynch, J. W. (2006). Systematic review of the influence of childhood socioeconomic circumstances on risk for cardiovascular disease in adulthood. Annals of Epidemiology, 16 (2), 91-104. https://doi.org/10.1016/j.annepidem.2005.06.053
Girchenko, P., Lahti, J., Czamara, D., Knight, A. K., Jones, M. J., Suarez, A., Hämäläinen, E., Kajantie, E., Laivuori, H., Villa, P. M., Reynolds, R. M., Kobor, M. S., Smith, A. K., Binder, E. B., & Räikkönen, K. (2017). Associations between maternal risk factors of adverse pregnancy and birth outcomes and the offspring epigenetic clock of gestational age at birth. Clinical Epigenetics, 9 (1), 49. https://doi.org/10.1186/s13148-017-0349-z
Goldsmith, D. R., Bekhbat, M., Mehta, N. D., & Felger, J. C. (2023). Inflammation-related functional and structural dysconnectivity as a pathway to psychopathology. Biol Psychiatry, 93 (5), 405-418. https://doi.org/10.1016/j.biopsych.2022.11.003
Gunnar, M. R., DePasquale, C. E., Reid, B. M., Donzella, B., & Miller, B. S. (2019). Pubertal stress recalibration reverses the effects of early life stress in postinstitutionalized children. Proceedings of the National Academy of Sciences, 116 (48), 23984-23988. https://doi.org/10.1073/pnas.1909699116
Hannum, G., Guinney, J., Zhao, L., Zhang, L., Hughes, G., Sadda, S. V., Klotzle, B., Bibikova, M., Fan, J.-B., Gao, Y., Deconde, R., Chen, M., Rajapakse, I., Friend, S., Ideker, T., & Zhang, K. (2013). Genome-wide methylation profiles reveal quantitative views of human aging rates. Molecular Cell, 49 (2), 359-367. https://doi.org/10.1016/j.molcel.2012.10.016
Hassamal, S. (2023). Chronic stress, neuroinflammation, and depression: An overview of pathophysiological mechanisms and emerging anti-inflammatories. Front Psychiatry, 14, 1130989. https://doi.org/10.3389/fpsyt.2023.1130989
Hayward, M. D., & Gorman, B. K. (2004). The long arm of childhood: The influence of early-life social conditions on men's mortality. Demography, 41 (1), 87-107. https://doi.org/10.1353/dem.2004.0005
Horvath, S. (2013). DNA methylation age of human tissues and cell types. Genome Biology, 14 (10), R115. https://doi.org/10.1186/gb-2013-14-10-r115
Horvath, S., & Raj, K. (2018). DNA methylation-based biomarkers and the epigenetic clock theory of ageing. Nature Reviews Genetics, 19 (6), 371-384. https://doi.org/10.1038/s41576-018-0004-3
Jylhava, J., Pedersen, N. L., & Hagg, S. (2017). Biological age predictors. EBioMedicine, 21, 29-36. https://doi.org/10.1016/j.ebiom.2017.03.046
Kaeberlein, M. (2013). Longevity and aging. F1000Prime Rep, 5, 5. https://doi.org/10.12703/P5-5
Kirkwood, T. B. (2005). Understanding the odd science of aging. Cell, 120 (4), 437-447. https://doi.org/10.1016/j.cell.2005.01.027
Knight, A. K., Craig, J. M., Theda, C., Bækvad-Hansen, M., Bybjerg-Grauholm, J., Hansen, C. S., Hollegaard, M. V., Hougaard, D. M., Mortensen, P. B., Weinsheimer, S. M., Werge, T. M., Brennan, P. A., Cubells, J. F., Newport, D. J., Stowe, Z. N., Cheong, J. L. Y., Dalach, P., Doyle, L. W., Loke, Y. J., Baccarelli, A. A.,... Smith, A. K. (2016). An epigenetic clock for gestational age at birth based on blood methylation data. Genome Biology, 17 (1), 206. https://doi.org/10.1186/s13059-016-1068-z
Laubach, Z. M., Perng, W., Cardenas, A., Rifas-Shiman, S. L., Oken, E., DeMeo, D., Litonjua, A. A., Duca, R.-C., Godderis, L., Baccarelli, A., & Hivert, M.-F. (2019). Socioeconomic status and DNA methylation from birth through mid-childhood: A prospective study in project viva. Epigenomics, 11 (12), 1413-1427. https://doi.org/10.2217/epi-2019-0040
Lo, Y. H., & Lin, W. Y. (2022). Cardiovascular health and four epigenetic clocks. Clinical Epigenetics, 14 (1), 73. https://doi.org/10.1186/s13148-022-01295-7
Lopez-Otin, C., Blasco, M. A., Partridge, L., Serrano, M., & Kroemer, G. (2013). The hallmarks of aging. Cell, 153 (6), 1194-1217. https://doi.org/10.1016/j.cell.2013.05.039
Lynch, J. W., Kaplan, G. A., & Salonen, J. T. (1997). Why do poor people behave poorly? Variation in adult health behaviours and psychosocial characteristics by stages of the socioeconomic lifecourse. Social Science & Medicine, 44 (6), 809-819. https://doi.org/10.1016/s0277-9536(96)00191-8
Marini, S., Davis, K. A., Soare, T. W., Zhu, Y., Suderman, M. J., Simpkin, A. J., Smith, A. D. A. C., Wolf, E. J., Relton, C. L., & Dunn, E. C. (2020). Adversity exposure during sensitive periods predicts accelerated epigenetic aging in children. Psychoneuroendocrinology, 113, 104484. https://doi.org/10.1016/j.psyneuen.2019.104484
McLaughlin, K. A., Breslau, J., Green, J. G., Lakoma, M. D., Sampson, N. A., Zaslavsky, A. M., & Kessler, R. C. (2011). Childhood socio-economic status and the onset, persistence, and severity of DSM-IV mental disorders in a US national sample. Social Science & Medicine, 73 (7), 1088-1096. https://doi.org/10.1016/j.socscimed.2011.06.011
Mposhi, A., & Turner, J. D. (2023). How can early life adversity still exert an effect decades later? A question of timing, tissues and mechanisms. Frontiers in Immunology, 14, 1215544. https://doi.org/10.3389/fimmu.2023.1215544
Naumova, O. Y., Lee, M., Koposov, R., Szyf, M., Dozier, M., & Grigorenko, E. L. (2012). Differential patterns of whole-genome DNA methylation in institutionalized children and children raised by their biological parents. Development and Psychopathology, 24 (1), 143-155. https://doi.org/10.1017/S0954579411000605
Naumova, O. Y., Rychkov, S. Y., Kornilov, S. A., Odintsova, V. V., Anikina, VO, Solodunova, M. Y., Arintcina, I. A., Zhukova, M. A., Ovchinnikova, I. V., Burenkova, O. V., Zhukova, O. V., Muhamedrahimov, R. J., Grigorenko, E. L., & El-Maarri, O. (2019). Effects of early social deprivation on epigenetic statuses and adaptive behavior of young children: A study based on a cohort of institutionalized infants and toddlers. PLoS One, 14 (3), e0214285. https://doi.org/10.1371/journal.pone.0214285
Noroozi, R., Ghafouri-Fard, S., Pisarek, A., Rudnicka, J., Spólnicka, M., Branicki, W., Taheri, M., & Pośpiech, E. (2021). DNA methylation-based age clocks: From age prediction to age reversion. Ageing Research Reviews, 68, 101314. https://doi.org/10.1016/j.arr.2021.101314
Pearce, E. E., Alsaggaf, R., Katta, S., Dagnall, C., Aubert, G., Hicks, B. D., Spellman, S. R., Savage, S. A., Horvath, S., & Gadalla, S. M. (2022). Telomere length and epigenetic clocks as markers of cellular aging: A comparative study. Geroscience, 44 (3), 1861-1869. https://doi.org/10.1007/s11357-022-00586-4
Peters, T. J., Buckley, M. J., Statham, A. L., Pidsley, R., Samaras, K., Lord, R. V., Clark, S. J., & Molloy, P. L. (2015). De novo identification of differentially methylated regions in the human genome. Epigenetics & Chromatin, 8, 6. https://doi.org/10.1186/1756-8935-8-6
Pidsley, R., Zotenko, E., Peters, T. J., Lawrence, M. G., Risbridger, G. P., Molloy, P., Van Djik, S., Muhlhausler, B., Stirzaker, C., & Clark, S. J. (2016). Critical evaluation of the illumina methylationEPIC beadChip microarray for whole-genome DNA methylation profiling. Genome Biology, 17 (1), 208. https://doi.org/10.1186/s13059-016-1066-1
Pollak, S. D. (2015). Developmental psychopathology: Recent advances and future challenges. World Psychiatry, 14 (3), 262-269. https://doi.org/10.1002/wps.20237
Raffington, L., Belsky, D. W., Kothari, M., Malanchini, M., Tucker-Drob, E. M., & Harden, K. P. (2021). Socioeconomic disadvantage and the pace of biological aging in children. Pediatrics, 147 (6), e2020024406. https://doi.org/10.1542/peds.2020-024406
Reid, B. M., Coe, C. L., Doyle, C. M., Sheerar, D., Slukvina, A., Donzella, B., & Gunnar, M. R. (2019). Persistent skewing of the T-cell profile in adolescents adopted internationally from institutional care. Brain Behavior and Immunity, 77, 168-177. https://doi.org/10.1016/j.bbi.2019.01.001
Relton, C. L., Gaunt, T., McArdle, W., Ho, K., Duggirala, A., Shihab, H., Woodward, G., Lyttleton, O., Evans, D. M., Reik, W., Paul, Y.-L., Ficz, G., Ozanne, S. E., Wipat, A., Flanagan, K., Lister, A., Heijmans, B. T., Ring, S. M., & Davey Smith, G. (2015). Data resource profile: Accessible resource for integrated epigenomic studies (ARIES). International Journal of Epidemiology, 44 (4), 1181-1190. https://doi.org/10.1093/ije/dyv072
Rodriguez-Miguelez, P., Looney, J., Blackburn, M., Thomas, J., Pollock, J. S., & Harris, R. A. (2022). The link between childhood adversity and cardiovascular disease risk: Role of cerebral and systemic vasculature. Function (Oxf), 3 (4), zqac029. https://doi.org/10.1093/function/zqac029
Sabbatinelli, J., Prattichizzo, F., Olivieri, F., Procopio, A. D., Rippo, M. R., & Giuliani, A. (2019). Where metabolism meets senescence: Focus on endothelial cells. Frontiers in Physiology, 10, 1523. https://doi.org/10.3389/fphys.2019.01523
Shin, S. H., & Kim, Y. K. (2023). Early life stress, neuroinflammation, and psychiatric illness of adulthood. Yeast Membrane Transport, 1411, 105-134. https://doi.org/10.1007/978-981-19-7376-5_6
Smith, K. E., & Pollak, S. D. (2020). Early life stress and development: Potential mechanisms for adverse outcomes. Journal of Neurodevelopmental Disorders, 12 (1), 34. https://doi.org/10.1186/s11689-020-09337-y
Spurrier, G. F., Shulman, K., Dibich, S., Benoit, L., Duckworth, K., & Martin, A. (2022). Physical symptoms as psychiatric manifestations in medical spaces: A qualitative study. Front Psychiatry, 13, 1074424. https://doi.org/10.3389/fpsyt.2022.1074424
Sun, Y., Fang, J., Wan, Y., Su, P., & Tao, F. (2020). Association of early-life adversity with measures of accelerated biological aging among children in China. JAMA Netw Open, 3 (9), e2013588. https://doi.org/10.1001/jamanetworkopen.2020.13588
Turecki, G., Ota, V. K., Belangero, S. I., Jackowski, A., & Kaufman, J. (2014). Early life adversity, genomic plasticity, and psychopathology. Lancet Psychiatry, 1 (6), 461-466. https://doi.org/10.1016/s2215-0366(14)00022-4
Unnikrishnan, A., Freeman, W. M., Jackson, J., Wren, J. D., Porter, H., & Richardson, A. (2019). The role of DNA methylation in epigenetics of aging. Pharmacology & Therapeutics, 195, 172-185. https://doi.org/10.1016/j.pharmthera.2018.11.001
van Lenthe, F. J., Kamphuis, C. B., Beenackers, M. A., Jansen, T., Looman, C. W., Nusselder, W. J., & Mackenbach, J. P. (2014). Cohort profile: Understanding socioeconomic inequalities in health and health behaviours: The GLOBE study. International Journal of Epidemiology, 43 (3), 721-730. https://doi.org/10.1093/ije/dyt040
Yan, Q., Paul, K. C., Lu, A. T., Kusters, C., Binder, A. M., Horvath, S., & Ritz, B. (2020). Epigenetic mutation load is weakly correlated with epigenetic age acceleration. Aging (Albany NY), 12 (18), 17863-17894. https://doi.org/10.18632/aging.103950