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      Fetal Programming of Body Composition, Obesity, and Metabolic Function: The Role of Intrauterine Stress and Stress Biology

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          Abstract

          Epidemiological, clinical, physiological, cellular, and molecular evidence suggests that the origins of obesity and metabolic dysfunction can be traced back to intrauterine life and supports an important role for maternal nutrition prior to and during gestation in fetal programming. The elucidation of underlying mechanisms is an area of interest and intense investigation. In this perspectives paper we propose that in addition to maternal nutrition-related processes it may be important to concurrently consider the potential role of intrauterine stress and stress biology. We frame our arguments in the larger context of an evolutionary-developmental perspective that supports roles for both nutrition and stress as key environmental conditions driving natural selection and developmental plasticity. We suggest that intrauterine stress exposure may interact with the nutritional milieu, and that stress biology may represent an underlying mechanism mediating the effects of diverse intrauterine perturbations, including but not limited to maternal nutritional insults (undernutrition and overnutrition), on brain and peripheral targets of programming of body composition, energy balance homeostasis, and metabolic function. We discuss putative maternal-placental-fetal endocrine and immune/inflammatory candidate mechanisms that may underlie the long-term effects of intrauterine stress. We conclude with a commentary of the implications for future research and clinical practice.

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          Most cited references 181

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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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            The concepts of stress and stress system disorders. Overview of physical and behavioral homeostasis.

             G A Chrousos,  P Gold (1992)
            This article defines stress and related concepts and reviews their historical development. The notion of a stress system as the effector of the stress syndrome is suggested, and its physiologic and pathophysiologic manifestations are described. A new perspective on human disease states associated with dysregulation of the stress system is provided. Published original articles from human and animal studies and selected reviews. Literature was surveyed utilizing MEDLINE and the Index Medicus. Original articles from the basic science and human literature consisted entirely of controlled studies based on verified methodologies and, with the exception of the most recent studies, replicated by more than one laboratory. Many of the basic science and clinical studies had been conducted in our own laboratories and clinical research units. Reviews cited were written by acknowledged leaders in the fields of neurobiology, endocrinology, and behavior. Independent extraction and cross-referencing by the authors. Stress and related concepts can be traced as far back as written science and medicine. The stress system coordinates the generalized stress response, which takes place when a stressor of any kind exceeds a threshold. The main components of the stress system are the corticotropin-releasing hormone and locus ceruleus-norepinephrine/autonomic systems and their peripheral effectors, the pituitary-adrenal axis, and the limbs of the autonomic system. Activation of the stress system leads to behavioral and peripheral changes that improve the ability of the organism to adjust homeostasis and increase its chances for survival. There has been an exponential increase in knowledge regarding the interactions among the components of the stress system and between the stress system and other brain elements involved in the regulation of emotion, cognitive function, and behavior, as well as with the axes responsible for reproduction, growth, and immunity. This new knowledge has allowed association of stress system dysfunction, characterized by sustained hyperactivity and/or hypoactivity, to various pathophysiologic states that cut across the traditional boundaries of medical disciplines. These include a range of psychiatric, endocrine, and inflammatory disorders and/or susceptibility to such disorders. We hope that knowledge from apparently disparate fields of science and medicine integrated into a working theoretical framework will allow generation and testing of new hypotheses on the pathophysiology and diagnosis of, and therapy for, a variety of human illnesses reflecting systematic alterations in the principal effectors of the generalized stress response. We predict that pharmacologic agents capable of altering the central apparatus that governs the stress response will be useful in the treatment of many of these illnesses.
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              High body mass index for age among US children and adolescents, 2003-2006.

              The prevalence of overweight among US children and adolescents increased between 1980 and 2004. To estimate the prevalence of 3 measures of high body mass index (BMI) for age (calculated as weight in kilograms divided by height in meters squared) and to examine recent trends for US children and adolescents using national data with measured heights and weights. Height and weight measurements were obtained from 8165 children and adolescents as part of the 2003-2004 and 2005-2006 National Health and Nutrition Examination Survey (NHANES), nationally representative surveys of the US civilian, noninstitutionalized population. Prevalence of BMI for age at or above the 97th percentile, at or above the 95th percentile, and at or above the 85th percentile of the 2000 sex-specific Centers for Disease Control and Prevention (CDC) BMI-for-age growth charts among US children by age, sex, and racial/ethnic group. Because no statistically significant differences in the prevalence of high BMI for age were found between estimates for 2003-2004 and 2005-2006, data for the 4 years were combined to provide more stable estimates for the most recent time period. Overall, in 2003-2006, 11.3% (95% confidence interval [CI], 9.7%-12.9%) of children and adolescents aged 2 through 19 years were at or above the 97th percentile of the 2000 BMI-for-age growth charts, 16.3% (95% CI, 14.5%-18.1%) were at or above the 95th percentile, and 31.9% (95% CI, 29.4%-34.4%) were at or above the 85th percentile. Prevalence estimates varied by age and by racial/ethnic group. Analyses of the trends in high BMI for age showed no statistically significant trend over the 4 time periods (1999-2000, 2001-2002, 2003-2004, and 2005-2006) for either boys or girls (P values between .07 and .41). The prevalence of high BMI for age among children and adolescents showed no significant changes between 2003-2004 and 2005-2006 and no significant trends between 1999 and 2006.
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                Author and article information

                Journal
                J Nutr Metab
                J Nutr Metab
                JNUME
                Journal of Nutrition and Metabolism
                Hindawi Publishing Corporation
                2090-0724
                2090-0732
                2012
                10 May 2012
                : 2012
                Affiliations
                1Department of Pediatrics, School of Medicine, University of California, Irvine, CA 92697-4260, USA
                2UC Irvine Development, Health and Disease Research Program, School of Medicine, University of California, Irvine, CA 92697-4260, USA
                3Department of Obstetrics & Gynecology, School of Medicine, University of California, Irvine, CA 92697-4260, USA
                4Department of Psychiatry & Human Behavior, School of Medicine, University of California, Irvine, CA 92697-4260, USA
                5Department of Epidemiology, School of Medicine, University of California, Irvine, CA 92697-4260, USA
                Author notes
                *Sonja Entringer: sentring@ 123456uci.edu

                Academic Editor: Barbara Alexander

                Article
                10.1155/2012/632548
                3359710
                22655178
                Copyright © 2012 Sonja Entringer et al.

                This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

                Categories
                Review Article

                Nutrition & Dietetics

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