Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood

IntroductionThe proportion of older adults within society is sharply increasing and a better understanding of how we age starts to be critical. However, given the paucity of longitudinal studies with both neuroimaging and epigenetic data, it remains largely unknown whether the speed of the epigeneti...

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Main Authors: Klara Mareckova, Anna Pacinkova, Radek Marecek, Ludmila Sebejova, Lydie Izakovicova Holla, Jana Klanova, Milan Brazdil, Yuliya S. Nikolova
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-08-01
Series:Frontiers in Aging Neuroscience
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fnagi.2023.1215957/full
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author Klara Mareckova
Klara Mareckova
Anna Pacinkova
Anna Pacinkova
Radek Marecek
Ludmila Sebejova
Lydie Izakovicova Holla
Jana Klanova
Milan Brazdil
Milan Brazdil
Yuliya S. Nikolova
Yuliya S. Nikolova
author_facet Klara Mareckova
Klara Mareckova
Anna Pacinkova
Anna Pacinkova
Radek Marecek
Ludmila Sebejova
Lydie Izakovicova Holla
Jana Klanova
Milan Brazdil
Milan Brazdil
Yuliya S. Nikolova
Yuliya S. Nikolova
author_sort Klara Mareckova
collection DOAJ
description IntroductionThe proportion of older adults within society is sharply increasing and a better understanding of how we age starts to be critical. However, given the paucity of longitudinal studies with both neuroimaging and epigenetic data, it remains largely unknown whether the speed of the epigenetic clock changes over the life course and whether any such changes are proportional to changes in brain aging and cognitive skills. To fill these knowledge gaps, we conducted a longitudinal study of a prenatal birth cohort, studied epigenetic aging across adolescence and young adulthood, and evaluated its relationship with brain aging and cognitive outcomes.MethodsDNA methylation was assessed using the Illumina EPIC Platform in adolescence, early and late 20 s, DNA methylation age was estimated using Horvath’s epigenetic clock, and epigenetic age gap (EpiAGE) was calculated as DNA methylation age residualized for batch, chronological age and the proportion of epithelial cells. Structural magnetic resonance imaging (MRI) was acquired in both the early 20 s and late 20 s using the same 3T Prisma MRI scanner and brain age was calculated using the Neuroanatomical Age Prediction using R (NAPR) platform. Cognitive skills were assessed using the Wechsler Adult Intelligence Scale (WAIS) in the late 20 s.ResultsThe EpiAGE in adolescence, the early 20 s, and the late 20 s were positively correlated (r = 0.34–0.47), suggesting that EpiAGE is a relatively stable characteristic of an individual. Further, a faster pace of aging between the measurements was positively correlated with EpiAGE at the end of the period (r = 0.48–0.77) but negatively correlated with EpiAGE at the earlier time point (r = −0.42 to −0.55), suggesting a compensatory mechanism where late matures might be catching up with the early matures. Finally, higher positive EpiAGE showed small (Adj R2 = 0.03) but significant relationships with a higher positive brain age gap in all participants and lower full-scale IQ in young adult women in the late 20 s.DiscussionWe conclude that the EpiAGE is a relatively stable characteristic of an individual across adolescence and early adulthood, but that it shows only a small relationship with accelerated brain aging and a women-specific relationship with worse performance IQ.
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spelling doaj.art-0ed6036ef6e548e3a1fe1253132c0ce02023-08-01T09:10:34ZengFrontiers Media S.A.Frontiers in Aging Neuroscience1663-43652023-08-011510.3389/fnagi.2023.12159571215957Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthoodKlara Mareckova0Klara Mareckova1Anna Pacinkova2Anna Pacinkova3Radek Marecek4Ludmila Sebejova5Lydie Izakovicova Holla6Jana Klanova7Milan Brazdil8Milan Brazdil9Yuliya S. Nikolova10Yuliya S. Nikolova11Brain and Mind Research, Central European Institute of Technology (CEITEC), Masaryk University (MU), Brno, Czechia1St Department of Neurology, St. Anne’s University Hospital and Faculty of Medicine, Masaryk University, Brno, CzechiaBrain and Mind Research, Central European Institute of Technology (CEITEC), Masaryk University (MU), Brno, CzechiaFaculty of Informatics, Masaryk University, Brno, CzechiaBrain and Mind Research, Central European Institute of Technology (CEITEC), Masaryk University (MU), Brno, CzechiaRECETOX, Faculty of Science, Masaryk University, Brno, CzechiaDepartment of Stomatology, St. Anne’s Univ. Hospital and Faculty of Medicine, Masaryk University, Brno, CzechiaRECETOX, Faculty of Science, Masaryk University, Brno, CzechiaBrain and Mind Research, Central European Institute of Technology (CEITEC), Masaryk University (MU), Brno, Czechia1St Department of Neurology, St. Anne’s University Hospital and Faculty of Medicine, Masaryk University, Brno, CzechiaCampbell Family Mental Health Research Institute, Centre for Addiction and Mental Health (CAMH), Toronto, ON, CanadaDepartment of Psychiatry, University of Toronto, Toronto, ON, CanadaIntroductionThe proportion of older adults within society is sharply increasing and a better understanding of how we age starts to be critical. However, given the paucity of longitudinal studies with both neuroimaging and epigenetic data, it remains largely unknown whether the speed of the epigenetic clock changes over the life course and whether any such changes are proportional to changes in brain aging and cognitive skills. To fill these knowledge gaps, we conducted a longitudinal study of a prenatal birth cohort, studied epigenetic aging across adolescence and young adulthood, and evaluated its relationship with brain aging and cognitive outcomes.MethodsDNA methylation was assessed using the Illumina EPIC Platform in adolescence, early and late 20 s, DNA methylation age was estimated using Horvath’s epigenetic clock, and epigenetic age gap (EpiAGE) was calculated as DNA methylation age residualized for batch, chronological age and the proportion of epithelial cells. Structural magnetic resonance imaging (MRI) was acquired in both the early 20 s and late 20 s using the same 3T Prisma MRI scanner and brain age was calculated using the Neuroanatomical Age Prediction using R (NAPR) platform. Cognitive skills were assessed using the Wechsler Adult Intelligence Scale (WAIS) in the late 20 s.ResultsThe EpiAGE in adolescence, the early 20 s, and the late 20 s were positively correlated (r = 0.34–0.47), suggesting that EpiAGE is a relatively stable characteristic of an individual. Further, a faster pace of aging between the measurements was positively correlated with EpiAGE at the end of the period (r = 0.48–0.77) but negatively correlated with EpiAGE at the earlier time point (r = −0.42 to −0.55), suggesting a compensatory mechanism where late matures might be catching up with the early matures. Finally, higher positive EpiAGE showed small (Adj R2 = 0.03) but significant relationships with a higher positive brain age gap in all participants and lower full-scale IQ in young adult women in the late 20 s.DiscussionWe conclude that the EpiAGE is a relatively stable characteristic of an individual across adolescence and early adulthood, but that it shows only a small relationship with accelerated brain aging and a women-specific relationship with worse performance IQ.https://www.frontiersin.org/articles/10.3389/fnagi.2023.1215957/fullepigenetic agebrain ageIQlongitudinalmagnetic resonance imaging (MRI)
spellingShingle Klara Mareckova
Klara Mareckova
Anna Pacinkova
Anna Pacinkova
Radek Marecek
Ludmila Sebejova
Lydie Izakovicova Holla
Jana Klanova
Milan Brazdil
Milan Brazdil
Yuliya S. Nikolova
Yuliya S. Nikolova
Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
Frontiers in Aging Neuroscience
epigenetic age
brain age
IQ
longitudinal
magnetic resonance imaging (MRI)
title Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
title_full Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
title_fullStr Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
title_full_unstemmed Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
title_short Longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
title_sort longitudinal study of epigenetic aging and its relationship with brain aging and cognitive skills in young adulthood
topic epigenetic age
brain age
IQ
longitudinal
magnetic resonance imaging (MRI)
url https://www.frontiersin.org/articles/10.3389/fnagi.2023.1215957/full
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