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      Transgenerational impact of intimate partner violence on methylation in the promoter of the glucocorticoid receptor

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          Abstract

          Prenatal exposure to maternal stress can have lifelong implications for psychological function, such as behavioral problems and even the development of mental illness. Previous research suggests that this is due to transgenerational epigenetic programming of genes operating in the hypothalamic–pituitary–adrenal axis, such as the glucocorticoid receptor (GR). However, it is not known whether intrauterine exposure to maternal stress affects the epigenetic state of these genes beyond infancy. Here, we analyze the methylation status of the GR gene in mothers and their children, at 10–19 years after birth. We combine these data with a retrospective evaluation of maternal exposure to intimate partner violence (IPV). Methylation of the mother's GR gene was not affected by IPV. For the first time, we show that methylation status of the GR gene of adolescent children is influenced by their mother's experience of IPV during pregnancy. As these sustained epigenetic modifications are established in utero, we consider this to be a plausible mechanism by which prenatal stress may program adult psychosocial function.

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          Most cited references20

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          Epigenetic programming by maternal behavior.

          Here we report that increased pup licking and grooming (LG) and arched-back nursing (ABN) by rat mothers altered the offspring epigenome at a glucocorticoid receptor (GR) gene promoter in the hippocampus. Offspring of mothers that showed high levels of LG and ABN were found to have differences in DNA methylation, as compared to offspring of 'low-LG-ABN' mothers. These differences emerged over the first week of life, were reversed with cross-fostering, persisted into adulthood and were associated with altered histone acetylation and transcription factor (NGFI-A) binding to the GR promoter. Central infusion of a histone deacetylase inhibitor removed the group differences in histone acetylation, DNA methylation, NGFI-A binding, GR expression and hypothalamic-pituitary-adrenal (HPA) responses to stress, suggesting a causal relation among epigenomic state, GR expression and the maternal effect on stress responses in the offspring. Thus we show that an epigenomic state of a gene can be established through behavioral programming, and it is potentially reversible.
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            Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress.

            Variations in maternal care affect the development of individual differences in neuroendocrine responses to stress in rats. As adults, the offspring of mothers that exhibited more licking and grooming of pups during the first 10 days of life showed reduced plasma adrenocorticotropic hormone and corticosterone responses to acute stress, increased hippocampal glucocorticoid receptor messenger RNA expression, enhanced glucocorticoid feedback sensitivity, and decreased levels of hypothalamic corticotropin-releasing hormone messenger RNA. Each measure was significantly correlated with the frequency of maternal licking and grooming (all r's > -0.6). These findings suggest that maternal behavior serves to "program" hypothalamic-pituitary-adrenal responses to stress in the offspring.
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              Nongenomic transmission across generations of maternal behavior and stress responses in the rat.

              In the rat, variations in maternal care appear to influence the development of behavioral and endocrine responses to stress in the offspring. The results of cross-fostering studies reported here provide evidence for (i) a causal relationship between maternal behavior and stress reactivity in the offspring and (ii) the transmission of such individual differences in maternal behavior from one generation of females to the next. Moreover, an environmental manipulation imposed during early development that alters maternal behavior can then affect the pattern of transmission in subsequent generations. Taken together, these findings indicate that variations in maternal care can serve as the basis for a nongenomic behavioral transmission of individual differences in stress reactivity across generations.
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                Author and article information

                Journal
                Transl Psychiatry
                Transl Psychiatry
                Translational Psychiatry
                Nature Publishing Group
                2158-3188
                July 2011
                19 July 2011
                1 July 2011
                : 1
                : 7
                : e21
                Affiliations
                [1 ]simpleDepartment of Psychology, University of Konstanz and Center for Psychiatry Reichenau , Konstanz, Germany
                [2 ]simpleLehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz , Konstanz, Germany
                [3 ]simpleZukunftskolleg, University of Konstanz , Konstanz, Germany
                Author notes
                [* ]simpleDepartment of Psychology, University of Konstanz and Center for Psychiatry Reichenau , 78457 Konstanz, Germany. E-mail: thomas.elbert@ 123456uni-konstanz.de
                [* ]simpleLehrstuhl für Zoologie und Evolutionsbiologie, Department of Biology, University of Konstanz , 78457 Konstanz, Germany. E-mail: axel.meyer@ 123456uni-konstanz.de
                [4]

                These authors contributed equally to this work.

                Article
                tp201121
                10.1038/tp.2011.21
                3309516
                22832523
                f541b493-a456-432d-ab89-8fedc4756048
                Copyright © 2011 Macmillan Publishers Limited

                This work is licensed under the Creative Commons Attribution-NonCommercial-No Derivative Works 3.0 Unported License. To view a copy of this license, visit http://creativecommons.org/licenses/by-nc-nd/3.0/

                History
                : 06 June 2011
                : 07 June 2011
                Categories
                Original Article

                Clinical Psychology & Psychiatry
                epigenetics,prenatal stress,methylation,hypothalamic–pituitary–adrenal axis,glucocorticoid receptor,intimate partner violence

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