The signature of maternal rearing in the methylome in rhesus macaque prefrontal cortex and T cells

Early-life adversity is associated with a broad scope of life-long health and behavioral disorders. Particularly critical is the role of the mother. A possible mechanism is that these effects are mediated by "epigenetic" mechanisms. Studies in rodents suggest a causal relationship between...

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Published inThe Journal of neuroscience Vol. 32; no. 44; pp. 15626 - 15642
Main Authors Provençal, Nadine, Suderman, Matthew J, Guillemin, Claire, Massart, Renaud, Ruggiero, Angela, Wang, Dongsha, Bennett, Allyson J, Pierre, Peter J, Friedman, David P, Côté, Sylvana M, Hallett, Michael, Tremblay, Richard E, Suomi, Stephen J, Szyf, Moshe
Format Journal Article
LanguageEnglish
Published United States Society for Neuroscience 31.10.2012
Subjects
Animals
Base Sequence
Chromosomes - genetics
DNA Methylation - physiology
DNA, Complementary - metabolism
Immunoprecipitation
In Situ Hybridization
Macaca mulatta
Male
Maternal Deprivation
Microarray Analysis
Molecular Sequence Data
Prefrontal Cortex - metabolism
Real-Time Polymerase Chain Reaction
RNA - biosynthesis
RNA - isolation & purification
Social Environment
T-Lymphocytes - metabolism
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Summary:Early-life adversity is associated with a broad scope of life-long health and behavioral disorders. Particularly critical is the role of the mother. A possible mechanism is that these effects are mediated by "epigenetic" mechanisms. Studies in rodents suggest a causal relationship between early-life adversity and changes in DNA methylation in several "candidate genes" in the brain. This study examines whether randomized differential rearing (maternal vs surrogate-peer rearing) of rhesus macaques is associated with differential methylation in early adulthood. The data presented here show that differential rearing leads to differential DNA methylation in both prefrontal cortex and T cells. These differentially methylated promoters tend to cluster by both chromosomal region and gene function. The broad impact of maternal rearing on DNA methylation in both the brain and T cells supports the hypothesis that the response to early-life adversity is system-wide and genome-wide and persists to adulthood. Our data also point to the feasibility of studying the impact of the social environment in peripheral T-cell DNA methylation.
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Author contributions: N.P., M.J.S., S.J.S., and M.S. designed research; N.P., M.J.S., C.G., R.M., A.R., D.W., and A.J.B. performed research; A.J.B., P.J.P., D.P.F., S.M.C., M.H., R.E.T., S.J.S., and M.S. contributed unpublished reagents/analytic tools; N.P., M.J.S., S.J.S., and M.S. analyzed data; N.P., M.J.S., A.J.B., P.J.P., D.P.F., M.H., R.E.T., S.J.S., and M.S. wrote the paper.
N.P. and M.J.S. contributed equally to this work.
ISSN:0270-6474
1529-2401
DOI:10.1523/JNEUROSCI.1470-12.2012