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      Epigenetic Programming of Stress Responses through Variations in Maternal Care

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          Abstract

          Early life experiences shape an individual's physical and mental health across the lifespan. Not surprisingly, an upbringing that is associated with adversity can produce detrimental effects on health. A central theme that arises from studies in human and nonhuman species is that the effects of adversity are mediated by the interactions between a mother and her young. In this review we describe some of the long-term effects of maternal care on the offspring and we focus on the impact of naturally occurring variations in the behavior of female rats. Of particular interest are mothers that engage in high or low amounts of licking/grooming (LG) and arched-back nursing (ABN) of their pups, but do so within the normal range for this species. Such variations in LG-ABN can alter the function of the hypothalamic-pituitary-adrenal (HPA) axis, and cognitive and emotional development by directly affecting the underlying neural mechanisms. At the heart of these mechanisms is gene expression. By studying the hippocampal glucocorticoid receptor gene, we have identified that maternal care regulates its expression by changing two processes: the acetylation of histones H3-K9, and the methylation of the NGFI-A consensus sequence on the exon 1(7) promoter. Sustained "maternal effects" appear elsewhere in biology, including plants, insects, and lizards, and may have evolved to program advantages in the environments that the offspring will likely face as adults. Given the importance of early life and parent-child interactions to later behavior, prevention and intervention programs should target this critical phase of development.

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          Most cited references62

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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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            Place navigation impaired in rats with hippocampal lesions

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              Economic stress, coercive family process, and developmental problems of adolescents.

              We propose a model of family conflict and coercion that links economic stress in family life to adolescent symptoms of internalizing and externalizing emotions and behaviors. The 180 boys and 198 girls in the study were living in intact families in the rural Midwest, an area characterized by economic decline and uncertainty. Theoretical constructs in the model were measured using both trained observer and family member reports. These adolescents and their parents were interviewed each year for 3 years during the seventh, eighth, and ninth grades. Our theoretical model proposes that economic pressure experienced by parents increases parental dysphoria and marital conflict as well as conflicts between parents and children over money. High levels of spousal irritability, coupled with coercive exchanges over money matters, were expected to be associated with greater hostility in general by parents toward their children. These hostile/coercive exchanges were expected to increase the likelihood of adolescent emotional and behavioral problems. Overall, results were consistent with the proposed model. Moreover, the hypothesized processes applied equally well to the behavior of mothers and fathers, as well as sons and daughters.
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                Author and article information

                Journal
                Annals of the New York Academy of Sciences
                Wiley
                00778923
                17496632
                December 2004
                January 12 2006
                : 1036
                : 1
                : 167-180
                Article
                10.1196/annals.1330.011
                15817737
                81c8cbd6-fbf1-4802-8e6c-573b1018b6dd
                © 2006

                http://doi.wiley.com/10.1002/tdm_license_1.1

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