Developmental programming in maternal diabetes and obesity
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1 Developmental programming in maternal diabetes and obesity Frans André Van Assche Department of Obstetrics and Gynecology, University Hospital, K. U. Leuven, Herestraat 49, 3000 Leuven, Belgium Corresponding author: Em. Prof. Dr.. Received: Accepted: Published: Abstract Influences in utero and in early neonatal life induce a permanent response in the fetus and the newborn, leading to enhanced susceptibility to later diseases. These effects are transgenerational and are probably due to an epigenetic transmission mediated by the mother. Diabetes and obesity during pregnancy show a marked increased prevalence and induce obesity and diabetes in the next generations. The most important causal factor is fetal hyperinsulinism. It is necessary to detect and control diabetes during pregnancy and to avoid obesitas at preference at adolescent age. Keywords: diabetes, obesity, pregnancy, developmental programming 126
2 INTRODUCTION Even before the discovery of insulin, Dubreuil and Anderodias (1), described giant islets in the pancreas of a newborn of a diabetic mother. It was suggested that the increased glucose level in the mother had an effect on the increased size of the fetal islets. Indeed, the increased transplacental transfer of glucose and other nutrients in the diabetic pregnancy produces B cell hyperplasia in the fetus. It is also important to mention that fetal B cell hyperplasia is only present in asymmetric macrosomia and not in symmetric macrosomia (2, 3). We forwarded the hypothesis at that time that the hyperactivity of the fetal B cells may result in a reduced capacity of insulin secretion in later life. DIABETES AND OBESITY IN PREGNANCY It is clear that diabetes in pregnancy has an effect on the fetus with consequences in later life. This statement is in accordance with the original observations of Doerner et al.: the diabetic intra-uterine environment is an important determinant for the development of diabetes in the offspring (4). These observations were confirmed by several epidemiologic studies and recently summarised. The excess of maternal transmission of diabetes is consistent with an epigenetic effect of hyperglycemia in pregnancy acting in addition to genetic factors to induce diabetes in the next generations.(5, 6). 127 Animal models of diabetes during pregnancy may discover the specific effects of an exposure to an abnormal diabetic intra-uterine environment independent of inherited trails. We have used the rat as experimental model. By inducing mild diabetes in the pregnant rat, the fetal endocrine pancreas showed B cell hyperplasia together with macrosomia and hyperinsulinism, comparable with the findings in humans. Moreover, the first evidence of developmental programming came from this animal research in It was demonstrated that mild diabetes in the pregnant rat induced gestational diabetes in the second generation and as a consequence macrosomia, increased insulin secretion and B cell hyperplasia in the fetuses of the third generation (7). It was postulated that (over)stimulation of the insulin producing B cells in utero leads to a reduced capacity of insulin secretion in conditions of increased demand in later life, such as obesity and pregnancy. The reduced B cell function is not able to meet increased insulin resistance. The effect of a diabetic intra-uterine environment on the next generations has been further explored, and dysfunctional B cells in adult offspring of rats with gestational diabetes has been confirmed (8, 9). Various mechanisms of this dysfunction, originated in utero, have been proposed: B cell exhaustion after chronic overstimulation, direct glucose toxicity on the B cells, or a decrease in insulin gene promoter activity and binding of PDX-1 (pancreatic/duodenal homebox-1) to the
3 insulin promoter, leading to defects in insulin secretion (10). However, it is also possible that fetal hyperinsulinism itself may induce malprogramming through the alterations induced in the hypothalamus. This mechanism may be related to changes in the hypothalamic control of food intake, body weight and glucose metabolism (11). abnormal glucose tolerance. Offspring of these pregnant obese rats remain obese in their further life and have insulin resistance (19). Numerous studies in animals have confirmed that maternal over-nutrition induces a deleterious effect during perinatal life, leading to a metabolic syndrome in the offspring (19-22). EPIGENETIC ADAPTATIONS Obesity in pregnancy shows similar effects as diabetes in pregnancy. Obesity is an important health problem, with even epidemic proportions. In the EU countries more than half of the adult population is overweight, and between 20 and 30 percent are obese (12). Worldwide the combination of diabetes and obesity (diabesity) will become the most important health problem in the next future (13). Obesity in pregnancy (equal to diabetes in pregnancy) is responsible for an increased maternal morbitity and perinatal morbitity and mortality (14-15). Furthermore, the prevalence of congenital malformations in the offspring is increased in these pregnancies (16). Maternal obesity and increased weight gain during pregnancy are associated with increased birth weight independent of genetic factors (17). But even more, obesity in pregnancy has consequences for diseases in the offspring in later life, with a transgenerational effect (18). By inducing obesity in the rat with an obesogenic diet before pregnancy, it has been shown that when pregnant, these animals have insulin resistance and an A diabetic intra-uterine environment induces a transgenerational effect of gestational diabetes. The transgenerational passage is most probably due to epigenetic phenomenons. The alterations on the genome, without changes of the DNA, are characterised as epigenetics. This is a slow process of changing methylgroups on cytosine basis in DNA by methyltransferases. Modifications are identified as demethylation, histone deacetylation and increased histone acetylation, independent from replication (23). Not every newborn with overweight will develop problems in later life. It depends on bad and good adaptation and to the plasticity of his adaptation later on (24). This means that by different environmental influences, alterations are made during intrauterine life on gene expressions, leading to aberrant metabolic phenotypes, such as obesity. Further studies exploring epigenetic mechanisms may understand fetal programming and the transference to future generations (25). 128
4 CONCLUSION In maternal diabetes and in maternal obesity increased transplacental nutrient supply to the fetus induces B cell hyperactivity, hyperinsulinism and increased fetal growth. These B cells have a reduced potential for insulin secretion in later life. Fetal hyperinsulinism is responsible for changes in the hypothalamus, resulting in malprogramming of food intake, body weight and glucose metabolism. These effects are transgenerational and are due to epigenetic phenomenons. From the clinical point of view it is therefore evident that in maternal diabetes and in maternal obesity fetal hyperinsulinism should be avoided. Early detection of gestational diabetes mellitus and strict metabolic control of pregestational and gestational diabetes mellitus are essential. Obesity needs to be prevented at preference at adolescence and certainly before pregnancy. 129
5 LIST OF REFERENCES 1. Dubreuil G, Anderodias J. Ilots de Langerhans géants chez un nouveau né de mère glucosurique. C. R. Soc.Biol. 1920;23: Van Assche FA, Gepts W. The cytological composition of the foetal endocrine pancreas in normal and pathological conditions. Diabetologia. 1971;7: Van Assche FA, Holemans K, et al. Longterm consequences for offspring of diabetes during pregnancy. Br Med Bull. 2001;60: Doerner G, Mohnike A, et al. Zur moegliche Bedeutung eines praenatales hyperinsulismus fuer die postnatale entwicklung eines diabetes mellitus. Endokrinologie. 1973;61: Mc Lean M, Chipps D, Cheung NW. Mother to child transmission of diabetes mellitus. Int J Biochem Cell Biol. 2006;38: Poston L. Developmental programming and diabetes. Best pract Res Clin Endocrinol Metab. 2010;24: Aerts L, Van Assche FA. Is gestational diabetes an acquired condition? J Dev Physiol. 1979;1: Boloker J, Gertz SJ, Simmons RA. Gestational Diabetes leads to the development of diabetes in adulthood in the rat. Diabetes. 2002;51: Aerts L, Van Assche FA. Animal evidence for transgenerational development of diabetes mellitus. Int J Biochem Cell Biol. 2006;38: De Vlieger R, Casteels K, Van Assche FA. Reduced adaptation of the pancreatic B cells during pregnancy. Acta Obst Gyn Scand. 2008;12: Plagemann A, Harder T, et al. Hypothalamic insulin and neuropeptide Y in offspring of gestational diabetic rats. Dev Brain Res. 1998;109: EU report: Promoting healthy diets and physical activity: a European dimension for the prevention of overweight, obesity and chronic diseases. A EU report: Diabesity, a world-wide challenge. February, Sibai BM, Gordon T, et al. Risk factors for preeclampsie in healthy nulliparous women. Am J Obstet Gynecol. 1999;172: Jensen DM, Damm P, et al. Pregnancy outcome and prepregnancy body mass index in 2459 glucose tolerant Danish women. Am J Obstet Gynecol. 2003;188: Watkins ML, Rasmussen SA, et al. Maternal obesity and risk of birth defects. Pediatrics. 2003;111: Ludwig DS, Currie J. The association between pregnancy weight gain and birth weight. The Lancet. 2010;376: Dabela D, Crume T. Maternal environment and the transgenerational cycle of obesity and diabetes. Diabetes. 2011;60: Holemans K, Caluwaerts S, et al. Diet induced obesity in the rat. Am J Obstet Gynecol. 2004;190: Armitage AA, Taylor PD, Poston L. Experimental models of developmental programming. J Physiol. 2005;565: Mcmillen IC, Robinson J. Developmental origin of the metabolic syndrome. Physiol Rev. 2005;85: Nivoit P, Morens C, Van Assche FA, et al. Established diet induced obesity in female rats leads to offspring hyperphagia, adiposity and insulin resistance. Diabetologia. 2009;52: Feng J, Zhou Y, et al. Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult firebrain neurons. Nat Neurosc. 2010;13: Gluckman PD, Hanson MA, et al. Effect of in utero and early life conditions on adult health and disease. N Engl J Med. 2008;359: Waterland RA, Travisano M, et al. Dietinduced hypermethylation at agouti viable yellow is not inherited transgenerationally through the female. FASEB J. 2007;
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