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Review

Prenatal nutritional influences on obesity risk in offspring

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Pages 137-149 | Published online: 10 Dec 2010

References

  • Seidell JC. Prevention of obesity: the role of the food industry. Nutr Metab Cardiovasc Dis. 1999;9(1):45–50.
  • Seidell JC. Obesity, insulin resistance and diabetes – a worldwide epidemic. Br J Nutr. 2000;83 Suppl 1:S5–S8.
  • Bell CG, Walley AJ, Froguel P. The genetics of human obesity. Nat Rev Genet. 2005;6(3):221–234.
  • Ravelli AC, van Der Meulen JH, Osmond C, Barker DJ, Bleker OP Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999;70(5):811–816.
  • Godfrey KM, Barker DJ. Fetal nutrition and adult disease. Am J Clin Nutr. 2000;71 Suppl 5:1344S–1352S.
  • Breier BH, Vickers MH, Ikenasio BA, Chan KY, Wong WP Fetal programming of appetite and obesity. Mol Cell Endocrinol. 2001; 185(1–2):73–79.
  • Hanson MA, Gluckman PD. Developmental origins of health and disease: new insights. Basic Clin Pharmacol Toxicol. 2008;102(2):90–93.
  • Gluckman PD, Hanson MA, Spencer HG. Predictive adaptive responses and human evolution. Trends Ecol Evol. 2005;20(10):527–533.
  • Godfrey KM, Gluckman PD, Hanson MA. Developmental origins of metabolic disease: life course and intergenerational perspectives. Trends Endocrinol Metab. 2010;21(4):199–205.
  • Gluckman PD, Hanson MA, Beedle AS. Early life events and their consequences for later disease: a life history and evolutionary perspective. Am J Hum Biol. 2007;19(1):1–19.
  • Gluckman PD, Hanson MA, Beedle AS. Non-genomic transgenerational inheritance of disease risk. Bioessays. 2007;29(2):145–154.
  • Stettler N, Iotova V. Early growth patterns and long-term obesity risk. Curr Opin Clin Nutr Metab Care. 2010;13(3):294–299.
  • Barker DJP, Osmond C. Infant mortality, childhood nutrition, and ischaemic heart disease in England and Wales. Lancet. 1986;1(8489): 1077–1081.
  • Barker DJP, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989;8663:577–580.
  • Barker DJP, Bull AR, Osmond C, Simmonds SJ. Fetal and placental size and risk of hypertension in adult life. Br Med J. 1990;301(6746): 259–262.
  • Osmond C, Barker DJ, Slattery JM. Risk of death from cardiovascular disease and chronic bronchitis determined by place of birth in England and Wales. J Epidemiol Community Health. 1990;44(2):139–141.
  • Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976;295(7): 349–353.
  • Roseboom TJ, van der Meulen JH, Ravelli AC, et al. Blood pressure in adults after prenatal exposure to famine. J Hypertens. 1999;17(3):325–330.
  • Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Effects of prenatal exposure to the Dutch famine on adult disease in later life: an overview. Mol Cell Endocrinol. 2001;185(1–2):93–98.
  • Stanner SA, Yudkin JS. Fetal programming and the Leningrad Siege study. Twin res. 2001;4(5):287–292.
  • Barker DJ. Low intelligence. Its relation to length of gestation and rate of foetal growth. Br J Prev Soc Med. 1966;20(2):58–66.
  • Hales CN, Ozanne SE. For debate: fetal and early postnatal growth restriction lead to diabetes, the metabolic syndrome and renal failure. Diabetologia. 2003;46(7):1013–1019.
  • Ong KK, Ahmed ML, Emmett PM, Preece MA, Dunger DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000;320(7240):967–971.
  • Ibanez L, Ong K, Dunger DB, de Zegher F. Early development of adiposity and insulin resistance after catch-up weight gain in small- for-gestational-age children. J Clin Endocrinol Metab. 2006;91(6): 2153–2158.
  • Ibanez L, Suarez L, Lopez-Bermejo A, Diaz M, Valls C, de Zegher F Early development of visceral fat excess after spontaneous catch-up growth in children with low birth weight. J Clin Endocrinol Metab. 2008;93(3):925–928.
  • Eriksson JG. Early growth, and coronary heart disease and type 2 diabetes: experiences from the Helsinki Birth Cohort Studies. Int J Obes (Lond). 2006;30 Suppl 4:S18–S22.
  • Yajnik C. Interactions of perturbations in intrauterine growth and growth during childhood on the risk of adult-onset disease. Proc Nutr Soc. 2000;59(2):257–265.
  • Eriksson JG, Forsen T, Tuomilehto J, Winter PD, Osmond C, Barker DJ. Catch-up growth in childhood and death from coronary heart disease: longitudinal study, BMJ. 1999;318(7181):427–431.
  • Parsons TJ, Power C, Manor O. Fetal and early life growth and body mass index from birth to early adulthood in 1958 British cohort: longitudinal study. BMJ. 2001;323(7325):1331–1335.
  • Eriksson J, Forsen T, Osmond C, Barker D. Obesity from cradle to grave. Int j obes relat metab disord. 2003;27(6):722–727.
  • Fetita LS, Sobngwi E, Serradas P, Calvo F, Gautier JF. Consequences of fetal exposure to maternal diabetes in offspring. J Clin Endocrinol Metab. 2006;91(10):3718–3724.
  • Gillman MW, Rifas-Shiman S, Berkey CS, Field AE, Colditz GA. Maternal gestational diabetes, birth weight, and adolescent obesity. Pediatrics. 2003;111(3):e221–e226.
  • Lampl M, Jeanty P. Exposure to maternal diabetes is associated with altered fetal growth patterns: a hypothesis regarding metabolic allocation to growth under hyperglycemic-hypoxemic conditions. Am J Hum Biol. 2004;16(3):237–263.
  • Silverman BL, Metzger BE, Cho NH, Loeb CA. Impaired glucose tolerance in adolescent offspring of diabetic mothers. Relationship to fetal hyperinsulinism. Diabetes Care. 1995;18(5):611–617.
  • Catalano PM. Increasing maternal obesity and weight gain during pregnancy: the obstetric problems of plentitude. Obstet Gynecol. 2007; 110(4):743–744.
  • Jonathan R, Jennifer B, Mark M. Maternal obesity and pregnancy complications: a review. Aust N Z J Obstet Gynaecol. 2008;48(3): 228–235.
  • Catalano PM, Farrell K, Thomas A, et al. Perinatal risk factors for childhood obesity and metabolic dysregulation. Am J Clin Nutr. 2009; 90(5):1303–1313.
  • Boney CM, Verma A, Tucker R, Vohr BR. Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus. Pediatrics. 2005;115(3):e290–e296.
  • Kristensen J, Vestergaard H, Wisborg K, Kesmodel U, Secher U. Pre-pregnancy weight and the risk of stillbirth and neonatal death. BJOG. 2005;112(4):403–408.
  • Shankar K, Harrell A, Liu X, Gilchrist JM, Ronis MJ, Badger TM. Maternal obesity at conception programs obesity in the offspring. Am J Physiol Regul Integr Comp Physiol. 2008;294(2):R528–R538.
  • Armitage JA, Poston L, Taylor PD. Developmental origins of obesity and the metabolic syndrome: the role of maternal obesity. Front Horm Res. 2008;36:73–84.
  • Crozier SR, Inskip HM, Godfrey KM, et al. Weight gain in pregnancy and childhood body composition: findings from the Southampton Women’s Survey. Am J Clin Nutr. 2010;91(6):1745–1751.
  • Barker DJ. Obesity and early life. Obes Rev. 2007;8 Suppl 1:45–49.
  • Barker DJ. The origins of the developmental origins theory. J Intern Med. 2007;261(5):412–417.
  • McArdle HJ, Andersen HS, Jones H, Gambling L. Fetal programming: causes and consequences as revealed by studies of dietary manipulation in rats – a review. Placenta. 2006;27 Suppl A:S56-S60.
  • Vickers MH, Breier BH, Cutfield WS, Hofman PL, Gluckman PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol Endocrinol Metab. 2000;279(1):E83–E87.
  • Vickers MH, Breier BH, McCarthy D, Gluckman PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol. 2003;285(1):R271–R273.
  • Vickers MH, Reddy S, Ikenasio BA, Breier BH. Dysregulation of the adipoinsular axis – a mechanism for the pathogenesis of hyperleptinemia and adipogenic diabetes induced by fetal programming. J Endocrinol. 2001;170(2):323–332.
  • Woodall SM, Johnston BM, Breier BH, Gluckman PD. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res. 1996;40(3):438–443.
  • Woodall SM, Breier BH, Johnston BM, Gluckman PD. A model of intrauterine growth retardation caused by chronic maternal undernutrition in the rat: effects on the somatotrophic axis and postnatal growth. J Endocrinol. 1996;150(2):231–242.
  • Langley-Evans SC, Welham SJ, Jackson AA. Fetal exposure to a maternal low protein diet impairs nephrogenesis and promotes hypertension in the rat. Life Sci. 1999;64(11):965–974.
  • Langley-Evans SC. Metabolic programming in pregnancy: studies in animal models. Genes Nutr. 2007;2(1):33–38.
  • Lillycrop KA, Slater-Jefferies JL, Hanson MA, Godfrey KM, Jackson AA, Burdge GC. Induction of altered epigenetic regulation of the hepatic glucocorticoid receptor in the offspring of rats fed a protein- restricted diet during pregnancy suggests that reduced DNA methyl- transferase-1 expression is involved in impaired DNA methylation and changes in histone modifications. Br J Nutr. 2007;97(6):1064–1073.
  • Rajakumar PA, He J, Simmons RA, Devaskar SU. Effect of uteroplacental insufficiency upon brain neuropeptide Y and corticotropin- releasing factor gene expression and concentrations. Pediatr Res. 1998;44(2):168–174.
  • Simmons RA, Templeton LJ, Gertz SJ. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes. 2001; 50(10):2279–2286.
  • Simmons RA. Role of metabolic programming in the pathogenesis of beta-cell failure in postnatal life. Rev Endocr Metab Disord. 2007; 8(2):95–104.
  • Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest. 1998;101(10):2174–2181.
  • Lewis RM, Forhead AJ, Petry CJ, Ozanne SE, Hales CN. Long-term programming of blood pressure by maternal dietary iron restriction in the rat. Br J Nutr. 2002;88(3):283–290.
  • Dahlgren J, Nilsson C, Jennische E, et al. Prenatal cytokine exposure results in obesity and gender-specific programming. Am J Physiol Endocrinol Metab. 2001;281(2):E326–E334.
  • Barker DJ, Osmond C, Golding J, Kuh D, Wadsworth ME. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ. 1989;298(6673):564–567.
  • Snoeck A, Remacle C, Reusens B, Hoet JJ. Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biol Neonate. 1990;57(2):107–118.
  • Langley SC, Jackson AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond). 1994;86(2):217–222; discussion 121.
  • Desai M, Crowther NJ, Lucas A, Hales CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr. 1996;76(4):591–603.
  • Ozanne SE, Constancia M. Mechanisms of disease: the developmental origins of disease and the role of the epigenotype. Nat Clin Pract Endocrinol Metab. 2007;3(7):539–546.
  • Petry CJ, Ozanne SE, Hales CN. Programming of intermediary metabolism. Mol Cell Endocrinol. 2001;185(1–2):81–91.
  • Burdge GC, Slater-Jefferies J, Torrens C, Phillips ES, Hanson MA, Lillycrop KA. Dietary protein restriction of pregnant rats in the F0 generation induces altered methylation of hepatic gene promoters in the adult male offspring in the F1 and F2 generations. Br J Nutr. 2007;97(3):435–439.
  • Langley-Evans SC. Critical differences between two low protein diet protocols in the programming of hypertension in the rat. Int J Food Sci Nutr. 2000;51(1):11–17.
  • Jennings BJ, Ozanne SE, Dorling MW, Hales CN. Early growth determines longevity in male rats and may be related to telomere shortening in the kidney. FEBS Lett. 1999;448(1):4–8.
  • Cottrell EC, Ozanne SE. Developmental programming of energy balance and the metabolic syndrome. Proc Nutr Soc. 2007;66(2):198–206.
  • Ozanne SE, Dorling MW, Wang CL, Nave BT. Impaired PI 3-kinase activation in adipocytes from early growth-restricted male rats. Am J Physiol Endocrinol Metab. 2001;280(3):E534–E539.
  • Ozaki T, Nishina H, Hanson MA, Poston L. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol. 2001;530(Pt 1):141–152.
  • Krechowec SO, Vickers M, Gertler A, Breier BH. Prenatal influences on leptin sensitivity and susceptibility to diet-induced obesity. J Endocrinol 2006;189(2):355–363.
  • Desai M, Gayle D, Babu J, Ross MG. Programmed obesity in intrauterine growth-restricted newborns: modulation by newborn nutrition. Am J Physiol Regul Integr Comp Physiol. 2005;288(1):R91–R96.
  • Padmavathi IJ, Kishore YD, Venu L, et al. Prenatal and perinatal zinc restriction: effects on body composition, glucose tolerance and insulin response in rat offspring. Exp Physiol. 2009;94(6):761–769.
  • Venu L, Padmavathi IJ, Kishore YD, et al. Long-term effects of maternal magnesium restriction on adiposity and insulin resistance in rat pups. Obesity (Silver Spring). 2008;16(6):1270–1276.
  • Venu L, Kishore YD, Raghunath M. Maternal and perinatal magnesium restriction predisposes rat pups to insulin resistance and glucose intolerance. J Nutr. 2005;135(6):1353–1358.
  • Venu L, Harishankar N, Prasanna Krishna T, Raghunath M. Maternal dietary vitamin restriction increases body fat content but not insulin resistance in WNIN rat offspring up to 6 months of age. Diabetologia. 2004;47(9):1493–1501.
  • Padmavathi IJN, Rao KR, Venu L, et al. Chronic maternal dietary chromium restriction modulates visceral adiposity. Diabetes. 2010;59(1): 98–104.
  • Lewis RM, Petry CJ, Ozanne SE, Hales CN. Effects of maternal iron restriction in the rat on blood pressure, glucose tolerance, and serum lipids in the 3-month-old offspring. Metabolism. 2001;50(5): 562–567.
  • Armitage JA, Khan IY, Taylor PD, Nathanielsz PW, Poston L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals?. J Physiol. 2004;561(Pt 2):355–377.
  • Bayol SA, Simbi BH, Fowkes RC, Stickland NC. A maternal “junk food” diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring. Endocrinology. 2010;151(4):1451–1461.
  • Szeto IMY, Das PJ, Aziz A, Anderson GH. Multivitamin supplementation of Wistar rats during pregnancy accelerates the development of obesity in offspring fed an obesogenic diet. Int J Obes (Lond). 2009; 33(3):364–372.
  • Giraudo SQ, Della-Fera MA, Proctor L, Wickwire K, Ambati S, Baile CA. Maternal high fat feeding and gestational dietary restriction: effects on offspring body weight, food intake and hypothalamic gene expression over three generations in mice. Pharmacol Biochem Behav. In press 2010.
  • Howie GJ, Sloboda DM, Kamal T, Vickers MH. Maternal nutritional history predicts obesity in adult offspring independent of postnatal diet. J Physiol. 2009;587(Pt 4):905–915.
  • Holemans K, Caluwaerts S, Poston L, van Assche FA. Diet-induced obesity in the rat: a model for gestational diabetes mellitus. Am J Obstet Gynecol. 2004;190(3):858–865.
  • Armitage JA, Taylor PD, Poston L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005;565(Pt 1):3–8.
  • McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85(2):571–633.
  • Samuelsson AM, Matthews PA, Argenton M, et al. Diet-induced obesity in female mice leads to offspring hyperphagia, adiposity, hypertension, and insulin resistance: a novel murine model of developmental programming. Hypertension. 2008;51(2):383–392.
  • Morris MJ, Chen H. Established maternal obesity in the rat reprograms hypothalamic appetite regulators and leptin signaling at birth. Int J Obes (Lond). 2009;33(1):115–122.
  • Horvath TL, Bruning JC. Developmental programming of the hypothalamus: a matter of fat. Nat Med. 2006;12(1):52–53; discussion 53.
  • Bouret SG, Draper SJ, Simerly RB. Trophic action of leptin on hypothalamic neurons that regulate feeding. Science. 2004;304(5667):108–110.
  • Bouret SG, Draper SJ, Simerly RB. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci. 2004;24(11):2797–2805.
  • Iniguez G, Soto N, Avila A, et al. Adiponectin levels in the first two years of life in a prospective cohort: relations with weight gain, leptin levels and insulin sensitivity. J Clin Endocrinol Metab. 2004; 89(11):5500–5503.
  • Elmquist JK, Ahima RS, Elias CF, Flier JS, Saper CB. Leptin activates distinct projections from the dorsomedial and ventromedial hypothalamic nuclei. Proc Natl Acad Sci U S A. 1998;95(2):741–746.
  • Bouret SG, Simerly RB. Development of leptin-sensitive circuits. J Neuroendocrinol. 2007;19(8):575–582.
  • Vickers MH, Gluckman PD, Coveny AH, et al. Neonatal leptin treatment reverses developmental programming. Endocrinology. 2005; 146(10):4211–4216.
  • Gluckman PD, Lillycrop KA, Vickers MH, et al. Metabolic plasticity during mammalian development is directionally dependent on early nutritional status. Proc Natl Acad Sci U S A. 2007;104(31):12796–12800.
  • Ahima RS, Prabakaran D, Flier JS. Postnatal leptin surge and regulation of circadian rhythm of leptin by feeding. Implications for energy homeostasis and neuroendocrine function. J Clin Invest. 1998;101(5): 1020–1027.
  • Attig L, Djiane J, Gertler A, et al. Study of hypothalamic leptin receptor expression in low-birth-weight piglets and effects of leptin supplementation on neonatal growth and development. Am J Physiol Endocrinol Metab. 2008;295(5):E1117–E1125.
  • Vickers MH, Ikenasio BA, Breier BH. Adult growth hormone treatment reduces hypertension and obesity induced by an adverse prenatal environment. J Endocrinol. 2002;175(3):615–623.
  • Sas T, Mulder P, Hokken-Koelega A. Body composition, blood pressure, and lipid metabolism before and during long-term growth hormone (GH) treatment in children with short stature born small for gestational age either with or without GH deficiency. J Clin Endocrinol Metab. 2000;85(10):3786–3792.
  • Vickers MH, Ikenasio BA, Breier BH. IGF-I treatment reduces hyper- phagia, obesity, and hypertension in metabolic disorders induced by fetal programming. Endocrinology. 2001;142(9):3964–3973.
  • Stoffers DA, Desai BM, DeLeon DD, Simmons RA. Neonatal exendin-4 prevents the development of diabetes in the intrauterine growth retarded rat. Diabetes. 2003;52(3):734–740.
  • Park JH, Stoffers DA, Nicholls RD, Simmons RA. Development of type 2 diabetes following intrauterine growth retardation in rats is associated with progressive epigenetic silencing of Pdx1. J Clin Invest. 2008;118(6):2316–2324.
  • Raab EL, Vuguin PM, Stoffers DA, Simmons RA. Neonatal exendin-4 treatment reduces oxidative stress and prevents hepatic insulin resistance in intrauterine growth retarded rats. Am J Physiol Regul Integr Comp Physiol. 2009;297(6):R1785–R1794.
  • Freeman JS. Role of the incretin pathway in the pathogenesis of type 2 diabetes mellitus. Cleve Clin J Med. 2009;76 Suppl 5:S12–S19.
  • Wyrwoll CS, Mark PJ, Mori TA, Puddey IB, Waddell BJ. Prevention of programmed hyperleptinemia and hypertension by postnatal dietary omega-3 fatty acids. Endocrinology. 2006;147(1):599–606.
  • Gluckman PD, Beedle AS, Hanson MA, Yap EP. Developmental perspectives on individual variation: implications for understanding nutritional needs. Nestle Nutr Workshop Ser Pediatr Program. 2008; 62:1–9; disucssion 9–12.
  • Gicquel C, El-Osta A, Le Bouc Y. Epigenetic regulation and fetal programming. Best Pract Res Clin Endocrinol Metab. 2008;22(1):1–16.
  • Szyf M. Epigenetics, DNA methylation, and chromatin modifying drugs. Annu Rev Pharmacol Toxicol. 2009;49:243–263.
  • Gluckman PD, Hanson MA, Cooper C, Thornburg KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008;359(1):61–73.
  • Tang WY, Ho SM. Epigenetic reprogramming and imprinting in origins of disease. Rev Endocr Metab Disord. 2007;8(2):173–182.
  • Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8(4):253–262.
  • Lillycrop KA, Phillips ES, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction of pregnant rats induces and folic acid supplementation prevents epigenetic modification of hepatic gene expression in the offspring. J Nutr. 2005;135(6):1382–1386.
  • Burdge GC, Lillycrop KA, Jackson AA, Gluckman PD, Hanson MA. The nature of the growth pattern and of the metabolic response to fasting in the rat are dependent upon the dietary protein and folic acid intakes of their pregnant dams and post-weaning fat consumption. Br J Nutr. 2008;99(3):540–549.
  • Pham TD, MacLennan NK, Chiu CT, Laksana GS, Hsu JL, Lane RH. Uteroplacental insufficiency increases apoptosis and alters p53 gene methylation in the full-term IUGR rat kidney. Am J Physiol Regul Integr Comp Physiol. 2003;285(5):R962–R970.
  • Bogdarina I, Welham S, King PJ, Burns SP, Clark AJ. Epigenetic modification of the renin-angiotensin system in the fetal programming of hypertension. Circ Res. 2007;100(4):520–526.
  • Weaver IC, Diorio J, Seckl JR, Szyf M, Meaney MJ. Early environmental regulation of hippocampal glucocorticoid receptor gene expression: characterization of intracellular mediators and potential genomic target sites. Ann N Y Acad Sci. 2004;1024:182–212.
  • Weaver IC, Cervoni N, Champagne FA, et al. Epigenetic programming by maternal behavior. Nat Neurosci. 2004;7(8):847–854.
  • Sinclair KD, Allegrucci C, Singh R, et al. DNA methylation, insulin resistance, and blood pressure in offspring determined by maternal periconceptional B vitamin and methionine status. Proc Natl Acad Sci USA. 2007;104(49):19351–19356.
  • Poulsen P, Esteller M, Vaag A, Fraga MF The epigenetic basis of twin discordance in age-related diseases. PediatrRes. 2007;61(5 Pt 2): 38R–2R.
  • Fraga MF, Ballestar E, Paz MF, et al. Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A. 2005;102(30):10604–10609.
  • Doherty AS, Mann MR, Tremblay KD, Bartolomei MS, Schultz RM. Differential effects of culture on imprinted H19 expression in the preimplantation mouse embryo. Biol Reprod. 2000;62(6):1526–1535.
  • Kwong WY, Miller DJ, Ursell E, et al. Imprinted gene expression in the rat embryo-fetal axis is altered in response to periconceptional maternal low protein diet. Reproduction. 2006;132(2):265–277.
  • MacLennan NK, James SJ, Melnyk S, et al. Uteroplacental insufficiency alters DNA methylation, one-carbon metabolism, and histone acetylation in IUGR rats. Physiol Genomics. 2004;18(1):43–50.
  • Meaney MJ, Brake W, Gratton A. Environmental regulation of the development of mesolimbic dopamine systems: a neurobiological mechanism for vulnerability to drug abuse? sychoneuroendocrinology. 2002;27(1–2):127–138.
  • Meaney MJ, Szyf M. Environmental programming of stress responses through DNA methylation: life at the interface between a dynamic environment and a fixed genome. Dialogues Clin Neurosci. 2005;7(2):103–123.
  • Champagne DL, Bagot RC, van Hasselt F, et al. Maternal care and hippocampal plasticity: evidence for experience-dependent structural plasticity, altered synaptic functioning, and differential responsiveness to glucocorticoids and stress. J Neurosci. 2008;28(23):6037–6045.
  • Cameron NM, Shahrokh D, Del Corpo A, et al. Epigenetic programming of phenotypic variations in reproductive strategies in the rat through maternal care. J Neuroendocrinology. 2008;20(6):795–801.
  • Champagne FA, Francis DD, Mar A, Meaney MJ. Variations in maternal care in the rat as a mediating influence for the effects of environment on development. PhysiolBehav. 2003;79(3):359–371.
  • Waterland RA, Michels KB. Epigenetic epidemiology of the developmental origins hypothesis. Annu Rev Nutr. 2007;27:363–388.
  • Waterland RA, Dolinoy DC, Lin JR, Smith CA, Shi X, Tahiliani KG. Maternal methyl supplements increase offspring DNA methylation at Axin Fused. Genesis. 2006;44(9):401–406.
  • Lillycrop KA, Jackson AA, Hanson MA, Burdge GC. Dietary protein restriction in the pregnant rat induces altered covalent modifications to histones at the glucocorticoid receptor promoter in the liver of the offspring after weaning. Proc Nutr Soc. 2006;65:108A.
  • Silva AJ, White R. Inheritance of allelic blueprints for methylation patterns. Cell. 1988;54(2):145–152.
  • Iliopoulos D, Malizos KN, Tsezou A. Epigenetic regulation of leptin affects MMP-13 expression in osteoarthritic chondrocytes: possible molecular target for osteoarthritis therapeutic intervention. Ann Rheum Dis. 2007;66(12):1616–1621.
  • Melzner I, Scott V, Dorsch K, et al. Leptin gene expression in human preadipocytes is switched on by maturation-induced demethyla- tion of distinct CpGs in its proximal promoter. J Biol Chem. 2002; 277(47):45420–45427.
  • Stoger R. In vivo methylation patterns of the leptin promoter in human and mouse. Epigenetics. 2006;1(4):155–162.
  • Yokomori N, Tawata M, Onaya T. DNA demethylation modulates mouse leptin promoter activity during the differentiation of 3T3-L1 cells. Diabetologia. 2002;45(1):140–148.
  • Yokomori N, Tawata M, Onaya T. DNA demethylation during the differentiation of 3T3-L1 cells affects the expression of the mouse GLUT4 gene. Diabetes. 1999;48(4):685–690.
  • Carretero MV Torres L, Latasa U, et al. Transformed but not normal hepatocytes express UCP2. FEBS Lett. 1998;439(1–2):55–58.
  • Holness MJ, Caton PW, Sugden MC. Acute and long-term nutrient-led modifications of gene expression: potential role of SIRT1 as a central co-ordinator of short and longer-term programming of tissue function. Nutrition. 2010;26(5):491–501.
  • Chen JH, Martin-Gronert MS, Tarry-Adkins J, Ozanne SE. Maternal protein restriction affects postnatal growth and the expression of key proteins involved in lifespan regulation in mice. PLoS ONE. 2009; 4(3):e4950.
  • Martin-Gronert MS, Tarry-Adkins JL, Cripps RL, Chen JH, Ozanne SE. Maternal protein restriction leads to early life alterations in the expression of key molecules involved in the aging process in rat offspring. Am J Physiol Regul Integr Comp Physiol. 2008;294(2):R494–R500.
  • Ho SM, Tang WY. Techniques used in studies of epigenome dysregulation due to aberrant DNA methylation: an emphasis on fetal-based adult diseases. Reprod Toxicol. 2007;23(3):267–282.
  • Ptak C, Petronis A. Epigenetics and complex disease: from etiology to new therapeutics. Annu Rev Pharmacol Toxicol. 2008;48:257–276.
  • Catalano PM, Presley L, Minium J, Hauguel-de Mouzon S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care. 2009;32(6):1076–1080.