Type 2 diabetes mellitus (T2DM) is a multifactorial disease, and its aetiology involves a complex interplay between genetic, epigenetic, and environmental factors. In recent years, evidences from both human and animal experiments have correlated early life factors with programming diabetes risk in adult life. Fetal and neonatal period is crucial for organ development. Many maternal factors during pregnancy may increase the risk of diabetes of offsprings in later life, which include malnutrition, healthy (hyperglycemia and obesity), behavior (smoking, drinking, and junk food diet), hormone administration, and even stress. In neonates, catch-up growth, lactation, glucocorticoids administration, and stress have all been found to increase the risk of insulin resistance or T2DM. Unfavorable environments (socioeconomic situation and famine) or obesity also has long-term negative effects on children by causing increased susceptibility to T2DM in adults. We also address the potential mechanisms that may underlie the developmental programming of T2DM. Therefore, it might be possible to prevent or delay the risk for T2DM by improving pre- and/or postnatal factors. 1. Introduction Type 2 diabetes (T2DM) is a metabolic disease caused by genetic and multiple environmental factors. Epidemical and experimental studies have found that detrimental early life factors may predispose high incidence of cardiovascular disease and metabolic diseases in later life, which is also termed as “barker hypothesis.” Organs are under development and functional maturation from fetal stage to childhood; disturbance of the homeostasis during crucial periods might predispose increased risk of insulin resistance and even T2DM in late life. 2. Part I: Prenatal Factors (Figure 1) 2.1. Diet and Nutrition It has been suggested that the quality and quantity of the nutrition during pregnancy may cause strong and permanent effects on the fetus. The altered structure of chromosome during this procedure might be the cause of cell dysfunction and increased susceptibility to diseases through altered gene expression [1]. Figure 1: Prenatal factors mentioned in recent years that might correlate with insulin resistance and/or T2DM. Data from human and animal studies have shown that malnutrition or overnutrition, metabolic disorders, exposure to hypoxia, some chemicals and hormones, and unhealthy lifestyle such as smoking and alcohol drinking during pregnancy might predispose detrimental long-term effects on offspring, leading to increased risk of insulin resistance or T2DM. TFA: transfatty acids; BPA:
References
[1]
J. C. Mathers, “Early nutrition: impact on epigenetics,” Forum of Nutrition, vol. 60, pp. 42–48, 2007.
[2]
F. Portrait, E. Teeuwiszen, and D. Deeg, “Early life undernutrition and chronic diseases at older ages: the effects of the Dutch famine on cardiovascular diseases and diabetes,” Social Science and Medicine, vol. 73, no. 5, pp. 711–718, 2011.
[3]
C. S. Yajnik, “Early life origins of insulin resistance and type 2 diabetes in india and other Asian countries,” Journal of Nutrition, vol. 134, no. 1, pp. 205–210, 2004.
[4]
R. Orozco-Solís, R. J. B. Matos, O. Guzmán-Quevedo et al., “Nutritional programming in the rat is linked to long-lasting changes in nutrient sensing and energy homeostasis in the hypothalamus,” PLoS ONE, vol. 5, no. 10, Article ID e13537, 2010.
[5]
J. L. Tarry-Adkins, J. Chen, R. H. Jones, N. H. Smith, and S. E. Ozanne, “Poor maternal nutrition leads to alterations in oxidative stress, antioxidant defense capacity, and markers of fibrosis in rat islets: potential underlying mechanisms for development of the diabetic phenotype in later life,” FASEB Journal, vol. 24, no. 8, pp. 2762–2771, 2010.
[6]
I. Sandovici, N. H. Smith, M. D. Nitert et al., “Maternal diet and aging alter the epigenetic control of a promoter-enhancer interaction at the Hnf4a gene in rat pancreatic islets,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 13, pp. 5449–5454, 2011.
[7]
N. Theys, M. Ahn, T. Bouckenooghe, B. Reusens, and C. Remacle, “Maternal malnutrition programs pancreatic islet mitochondrial dysfunction in the adult offspring,” Journal of Nutritional Biochemistry, vol. 22, no. 10, pp. 985–994, 2011.
[8]
A. Rodriguez-Trejo, M. G. Ortiz-Lopez, E. Zambrano et al., “Developmental programming of neonatal pancreatic β-cells by a maternal low-protein diet in rats involves a switch from proliferation to differentiation,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 302, no. 11, pp. E1431–E1439, 2012.
[9]
A. D. Maurer and R. A. Reimer, “Maternal consumption of high-prebiotic fibre or -protein diets during pregnancy and lactation differentially influences satiety hormones and expression of genes involved in glucose and lipid metabolism in offspring in rats,” The British Journal of Nutrition, vol. 105, no. 3, pp. 329–338, 2011.
[10]
Sadashiv, S. Tiwari, B. N. Paul et al., “Resistin gene expression in visceral adipose tissue of postmenopausal women and its association with insulin resistance,” Women's Health, vol. 8, no. 5, pp. 521–528, 2012.
[11]
T. Matsubara, A. Mita, K. Minami et al., “PGRN is a key adipokine mediating high fat diet-induced insulin resistance and obesity through IL-6 in adipose tissue,” Cell Metabolism, vol. 15, no. 1, pp. 38–50, 2012.
[12]
K. M. Lee, S. J. Yang, Y. D. Kim et al., “Disruption of the cereblon gene enhances hepatic AMPK activity and prevents high-fat diet-induced obesity and insulin resistance in mice,” Diabetes, vol. 62, no. 6, pp. 1855–1864, 2013.
[13]
M. H. Black, R. M. Watanabe, E. Trigo et al., “High-fat diet is associated with obesity-mediated insulin resistance and β-cell dysfunction in Mexican Americans,” Journal of Nutrition, vol. 143, no. 4, pp. 479–485, 2013.
[14]
H. Masuyama and Y. Hiramatsu, “Effects of a high-fat diet exposure in utero on the metabolic syndrome-like phenomenon in mouse offspring through epigenetic changes in adipocytokine gene expression,” Endocrinology, vol. 153, no. 6, pp. 2823–2830, 2012.
[15]
C. Liang, M. E. Oest, and M. R. Prater, “Intrauterine exposure to high saturated fat diet elevates risk of adult-onset chronic diseases in C57BL/6 mice,” Birth Defects Research B, vol. 86, no. 5, pp. 377–384, 2009.
[16]
S. Rajia, H. Chen, and M. J. Morris, “Maternal overnutrition impacts offspring adiposity and brain appetite markers-modulation by postweaning diet,” Journal of Neuroendocrinology, vol. 22, no. 8, pp. 905–914, 2010.
[17]
N. Briancon, D. E. McNay, E. Maratos-Flier, and J. S. Flier, “Combined neural inactivation of suppressor of cytokine signaling-3 and protein-tyrosine phosphatase-1B reveals additive, synergistic, and factor-specific roles in the regulation of body energy balance,” Diabetes, vol. 59, no. 12, pp. 3074–3084, 2010.
[18]
N. G. Ashino, K. N. Saito, F. D. Souza et al., “Maternal high-fat feeding through pregnancy and lactation predisposes mouse offspring to molecular insulin resistance and fatty liver,” Journal of Nutritional Biochemistry, vol. 23, no. 4, pp. 341–348, 2012.
[19]
K. F. Yang, X. H. Shen, and W. Cai, “Prenatal and early postnatal exposure to high-saturated-fat diet represses Wnt signaling and myogenic genes in offspring rats,” Experimental Biology and Medicine, vol. 237, no. 8, pp. 912–918, 2012.
[20]
M. Abiola, M. Favier, E. Christodoulou-Vafeiadou, A. Pichard, I. Martelly, and I. Guillet-Deniau, “Activation of Wnt/β-catenin signaling increases insulin sensitivity through a reciprocal regulation of Wnt10b and SREBP-1c in skeletal muscle cells,” PLoS ONE, vol. 4, no. 12, Article ID e8509, 2009.
[21]
A. K. Thompson, A.-M. Minihane, and C. M. Williams, “Trans fatty acids, insulin resistance and diabetes,” European Journal of Clinical Nutrition, vol. 65, no. 5, pp. 553–564, 2011.
[22]
R. Micha and D. Mozaffarian, “Trans fatty acids: effects on metabolic syndrome, heart disease and diabetes,” Nature Reviews Endocrinology, vol. 5, no. 6, pp. 335–344, 2009.
[23]
S. E. Dorfman, D. Laurent, J. S. Gounarides et al., “Metabolic implications of dietary trans-fatty acids,” Obesity, vol. 17, no. 6, pp. 1200–1207, 2009.
[24]
K. Kavanagh, S. Sajadian, K. A. Jenkins et al., “Neonatal and fetal exposure to trans-fatty acids retards early growth and adiposity while adversely affecting glucose in mice,” Nutrition Research, vol. 30, no. 6, pp. 418–426, 2010.
[25]
S. A. Bayol, B. H. Simbi, R. C. Fowkes, and N. C. Stickland, “A maternal “junk food” diet in pregnancy and lactation promotes nonalcoholic fatty liver disease in rat offspring,” Endocrinology, vol. 151, no. 4, pp. 1451–1461, 2010.
[26]
T. Ramirez, M. Tong, W. C. Chen, Q. G. Nguyen, J. R. Wands, and S. M. de la Monte, “Chronic alcohol-induced hepatic insulin resistance and endoplasmic reticulum stress ameliorated by peroxisome-proliferator activated receptor-delta agonist treatment,” Journal of Gastroenterology and Hepatology, vol. 28, no. 1, pp. 179–187, 2013.
[27]
F. Yue, X. Zhang, H. Zhang, X. Jiang, L. Gao, and J. Zhao, “Association of alcohol consumption with the impaired β-cell function independent of body mass index among Chinese men,” Endocrine Journal, vol. 59, no. 5, pp. 425–433, 2012.
[28]
L. Chen and B. L. G. Nyomba, “Effects of prenatal alcohol exposure on glucose tolerance in the rat offspring,” Metabolism, vol. 52, no. 4, pp. 454–462, 2003.
[29]
L. Chen, T. Zhang, and B. L. G. Nyomba, “Insulin resistance of gluconeogenic pathways in neonatal rats after prenatal ethanol exposure,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 286, no. 3, pp. R554–R559, 2004.
[30]
L. Chen, X. H. Yao, and B. L. G. Nyomba, “In vivo insulin signaling through PI3-kinase is impaired in skeletal muscle of adult rat offspring exposed to ethanol in utero,” Journal of Applied Physiology, vol. 99, no. 2, pp. 528–534, 2005.
[31]
X. H. Yao, L. Chen, and B. L. G. Nyomba, “Adult rats prenatally exposed to ethanol have increased gluconeogenesis and impaired insulin response of hepatic gluconeogenic genes,” Journal of Applied Physiology, vol. 100, no. 2, pp. 642–648, 2006.
[32]
X. H. Yao and B. L. G. Nyomba, “Hepatic insulin resistance induced by prenatal alcohol exposure is associated with reduced PTEN and TRB3 acetylation in adult rat offspring,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 294, no. 6, pp. R1797–R1806, 2008.
[33]
X. H. Yao and B. L. G. Nyomba, “Abnormal glucose homeostasis in adult female rat offspring after intrauterine ethanol exposure,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 292, no. 5, pp. R1926–R1933, 2007.
[34]
F. Beguinot, “Tribbles homologue 3 (TRIB3) and the insulin-resistance genes in type 2 diabetes,” Diabetologia, vol. 53, no. 9, pp. 1831–1834, 2010.
[35]
A. Gupta and C. S. Dey, “PTEN, a widely known negative regulator of insulin/PI3K signaling, positively regulates neuronal insulin resistance,” Molecular Biology of the Cell, vol. 23, no. 19, pp. 3882–3898, 2012.
[36]
S. Nammi, K. Dembele, and B. L. G. Nyomba, “Increased 11β-hydroxysteroid dehydrogenase type-1 and hexose-6-phosphate dehydrogenase in liver and adipose tissue of rat offspring exposed to alcohol in utero,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 292, no. 3, pp. R1101–R1109, 2007.
[37]
T. Groff, “Bisphenol A: invisible pollution,” Current Opinion in Pediatrics, vol. 22, no. 4, pp. 524–529, 2010.
[38]
P. Alonso-Magdalena, S. Morimoto, C. Ripoll, E. Fuentes, and A. Nadal, “The estrogenic effect of bisphenol a disrupts pancreatic β-cell function in vivo and induces insulin resistance,” Environmental Health Perspectives, vol. 114, no. 1, pp. 106–112, 2006.
[39]
A. Nadal, P. Alonso-Magdalena, S. Soriano, I. Quesada, and A. B. Ropero, “The pancreatic β-cell as a target of estrogens and xenoestrogens: implications for blood glucose homeostasis and diabetes,” Molecular and Cellular Endocrinology, vol. 304, no. 1-2, pp. 63–68, 2009.
[40]
P. Alonso-Magdalena, A. B. Ropero, S. Soriano, I. Quesada, and A. Nadal, “Bisphenol-A: a new diabetogenic factor?” Hormones, vol. 9, no. 2, pp. 118–126, 2010.
[41]
E. Makaji, S. Raha, M. G. Wade, and A. C. Holloway, “Effect of environmental contaminants on β cell function,” International Journal of Toxicology, vol. 30, no. 4, pp. 410–418, 2011.
[42]
I. A. Lang, T. S. Galloway, A. Scarlett et al., “Association of Urinary Bisphenol A concentration with medical disorders and laboratory abnormalities in adults,” The Journal of the American Medical Association, vol. 300, no. 11, pp. 1303–1310, 2008.
[43]
J. Wei, Y. Lin, Y. Li et al., “Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet,” Endocrinology, vol. 152, no. 8, pp. 3049–3061, 2011.
[44]
P. Alonso-Magdalena, E. Vieira, S. Soriano et al., “Bisphenol a exposure during pregnancy disrupts glucose homeostasis in mothers and adult male offspring,” Environmental Health Perspectives, vol. 118, no. 9, pp. 1243–1250, 2010.
[45]
K. K. Ryan, A. M. Haller, J. E. Sorrell, S. C. Woods, R. J. Jandacek, and R. J. Seeley, “Perinatal exposure to bisphenol-A and the development of metabolic syndrome in CD-1 mice,” Endocrinology, vol. 151, no. 6, pp. 2603–2612, 2010.
[46]
L. Cao, C. Mao, S. Li et al., “Hepatic insulin signaling changes: possible mechanism in prenatal hypoxia-increased susceptibility of fatty liver in adulthood,” Endocrinology, vol. 153, no. 10, pp. 4955–4965, 2012.
[47]
E. J. Camm, M. S. Martin-Gronert, N. L. Wright, J. A. Hansell, S. E. Ozanne, and D. A. Giussani, “Prenatal hypoxia independent of undernutrition promotes molecular markers of insulin resistance in adult offspring,” FASEB Journal, vol. 25, no. 1, pp. 420–427, 2011.
[48]
S. A. Chang, “Smoking and type 2 diabetes mellitus,” Diabetes and Metabolism Journal, vol. 36, no. 6, pp. 399–403, 2012.
[49]
B. C. Bergman, L. Perreault, D. Hunerdosse et al., “nd reversible mechanisms of smoking-induced insulin resistance in humans,” Diabetes, vol. 61, no. 12, pp. 3156–3166, 2012.
[50]
E. Thiering, I. Brüske, J. Kratzsch et al., “Prenatal and postnatal tobacco smoke exposure and development of insulin resistance in 10 year old children,” International Journal of Hygiene and Environmental Health, vol. 214, no. 5, pp. 361–368, 2011.
[51]
J. E. Bruin, L. D. Kellenberger, H. C. Gerstein, K. M. Morrison, and A. C. Holloway, “Fetal and neonatal nicotine exposure and postnatal glucose homeostasis: identifying critical windows of exposure,” Journal of Endocrinology, vol. 194, no. 1, pp. 171–178, 2007.
[52]
A. C. Holloway, D. Q. Cuu, K. M. Morrison, H. C. Gerstein, and M. A. Tarnopolsky, “Transgenerational effects of fetal and neonatal exposure to nicotine,” Endocrine, vol. 31, no. 3, pp. 254–259, 2007.
[53]
E. Somm, V. M. Schwitzgebel, D. M. Vauthay et al., “Prenatal nicotine exposure alters early pancreatic islet and adipose tissue development with consequences on the control of body weight and glucose metabolism later in life,” Endocrinology, vol. 149, no. 12, pp. 6289–6299, 2008.
[54]
H. Chen, S. Saad, S. L. Sandow, and P. P. Bertrand, “Cigarette smoking and brain regulation of energy homeostasis,” Frontiers in Pharmacology, vol. 3, article 147, 2012.
[55]
C. L. Coe, G. R. Lubach, and E. A. Shirtcliff, “Maternal stress during pregnancy predisposes for iron deficiency in infant monkeys impacting innate immunity,” Pediatric Research, vol. 61, no. 5, part 1, pp. 520–524, 2007.
[56]
J. Lesage, F. Del-Favero, M. Leonhardt et al., “Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat,” Journal of Endocrinology, vol. 181, no. 2, pp. 291–296, 2004.
[57]
J. Li, J. Olsen, M. Vestergaard, C. Obel, J. K. Kristensen, and J. Virk, “Prenatal exposure to bereavement and type-2 diabetes: a Danish longitudinal population based study,” PLoS ONE, vol. 7, no. 8, Article ID e43508, 2012.
[58]
S. Entringer, S. Wüst, R. Kumsta et al., “Prenatal psychosocial stress exposure is associated with insulin resistance in young adults,” The American Journal of Obstetrics and Gynecology, vol. 199, no. 5, pp. 498.e1–498.e7, 2008.
[59]
S. Entringer, E. S. Epel, R. Kumsta et al., “Stress exposure in intrauterine life is associated with shorter telomere length in young adulthood,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 33, pp. E513–E518, 2011.
[60]
K. D. Salpea, P. J. Talmud, J. A. Cooper et al., “Association of telomere length with type 2 diabetes, oxidative stress and UCP2 gene variation,” Atherosclerosis, vol. 209, no. 1, pp. 42–50, 2010.
[61]
J. L. Buxton, R. G. Walters, S. Visvikis-Siest, D. Meyre, P. Froguel, and A. I. F. Blakemore, “Childhood obesity is associated with shorter leukocyte telomere length,” Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 5, pp. 1500–1505, 2011.
[62]
D. S. Fernandez-Twinn, H. L. Blackmore, L. Siggens et al., “The programming of cardiac hypertrophy in the offspring by maternal obesity is associated with hyperinsulinemia, AKT, ERK, and mTOR activation,” Endocrinology, vol. 153, no. 12, pp. 5961–5971, 2012.
[63]
J. R. O'Reilly and R. M. Reynolds, “The risk of maternal obesity to the long-term health of the offspring,” Clinical Endocrinology, vol. 78, no. 1, pp. 9–16, 2013.
[64]
M. Obregon, “Maternal obesity results in offspring prone to metabolic syndrome,” Endocrinology, vol. 151, no. 8, pp. 3475–3476, 2010.
[65]
C. M. Boney, A. Verma, R. Tucker, and B. R. Vohr, “Metabolic syndrome in childhood: association with birth weight, maternal obesity, and gestational diabetes mellitus,” Pediatrics, vol. 115, no. 3, pp. e290–e296, 2005.
[66]
K. Shankar, P. Kang, A. Harrell et al., “Maternal overweight programs insulin and adiponectin signaling in the offspring,” Endocrinology, vol. 151, no. 6, pp. 2577–2589, 2010.
[67]
L. Zhang, N. M. Long, S. M. Hein, Y. Ma, P. W. Nathanielsz, and S. P. Ford, “Maternal obesity in ewes results in reduced fetal pancreatic β-cell numbers in late gestation and decreased circulating insulin concentration at term,” Domestic Animal Endocrinology, vol. 40, no. 1, pp. 30–39, 2011.
[68]
S. P. Ford, L. Zhang, M. Zhu et al., “Maternal obesity accelerates fetal pancreatic β-cell but not α-cell development in sheep: prenatal consequences,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 297, no. 3, pp. R835–R843, 2009.
[69]
J. A. Oben, A. Mouralidarane, A. Samuelsson et al., “Maternal obesity during pregnancy and lactation programs the development of offspring non-alcoholic fatty liver disease in mice,” Journal of Hepatology, vol. 52, no. 6, pp. 913–920, 2010.
[70]
S. J. Borengasser, F. Lau, P. Kang et al., “Maternal obesity during gestation impairs fatty acid oxidation and mitochondrial SIRT3 expression in rat offspring at weaning,” PLoS ONE, vol. 6, no. 8, Article ID e24068, 2011.
[71]
H. Boerschmann, M. Pflüger, L. Henneberger, A. Ziegler, and S. Hummel, “Prevalence and predictors of overweight and insulin resistance in offspring of mothers with gestational diabetes mellitus,” Diabetes Care, vol. 33, no. 8, pp. 1845–1849, 2010.
[72]
N. C. Bush, P. C. Chandler-Laney, D. J. Rouse, W. M. Granger, R. A. Oster, and B. A. Gower, “Higher maternal gestational glucose concentration is associated with lower offspring insulin sensitivity and altered β-cell function,” Journal of Clinical Endocrinology and Metabolism, vol. 96, no. 5, pp. E803–E809, 2011.
[73]
Y. Song, J. Li, Y. Zhao et al., “Severe maternal hyperglycemia exacerbates the development of insulin resistance and fatty liver in the offspring on high fat diet,” Experimental Diabetes Research, vol. 2012, Article ID 254976, 8 pages, 2012.
[74]
J. M. Ma, C. J. Zeng, L. Zhang, C. Shou, and H. X. Yang, “Increased hepatic peroxisome proliferator-activated receptor coactivator-1α expression precedes the development of insulin resistance in offspring of rats from severe hyperglycemic mothers,” Chinese Medical Journal, vol. 125, no. 7, pp. 1224–1229, 2012.
[75]
A. Natali, E. Muscelli, A. Mari et al., “Insulin sensitivity and β-cell function in the offspring of type 2 diabetic patients: impact of line of inheritance,” Journal of Clinical Endocrinology and Metabolism, vol. 95, no. 10, pp. 4703–4711, 2010.
[76]
A. J. King, N. B. Olivier, P. S. Mohankumar, J. S. Lee, V. Padmanabhan, and G. D. Fink, “Hypertension caused by prenatal testosterone excess in female sheep,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 292, no. 6, pp. E1837–E1841, 2007.
[77]
S. E. Recabarren, V. Padmanabhan, E. Codner et al., “Postnatal developmental consequences of altered insulin sensitivity in female sheep treated prenatally with testosterone,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 289, no. 5, pp. E801–E806, 2005.
[78]
V. Padmanabhan, A. Veiga-Lopez, D. H. Abbott, S. E. Recabarren, and C. Herkimer, “Developmental programming: impact of prenatal testosterone excess and postnatal weight gain on insulin sensitivity index and transfer of traits to offspring of overweight females,” Endocrinology, vol. 151, no. 2, pp. 595–605, 2010.
[79]
S. E. Nada, R. C. Thompson, and V. Padmanabhan, “Developmental programming: differential effects of prenatal testosterone excess on insulin target tissues,” Endocrinology, vol. 151, no. 11, pp. 5165–5173, 2010.
[80]
A. V. Roland, C. S. Nunemaker, S. R. Keller, and S. M. Moenter, “Prenatal androgen exposure programs metabolic dysfunction in female mice,” Journal of Endocrinology, vol. 207, no. 2, pp. 213–223, 2010.
[81]
S. Amalfi, L. M. Velez, M. F. Heber et al., “Prenatal hyperandrogenization induces metabolic and endocrine alterations which depend on the levels of testosterone exposure,” PLoS ONE, vol. 7, no. 5, Article ID e37658, 2012.
[82]
M. Sun, M. Maliqueo, A. Benrick et al., “Maternal androgen excess reduces placental and fetal weights, increases placental steroidogenesis, and leads to long-term health effects in their female offspring,” The American Journal of Physiology—Endocrinology and Metabolism, vol. 303, no. 11, pp. E1373–E1385, 2012.
[83]
C. M. Bruns, S. T. Baum, R. J. Colman et al., “Insulin resistance and impaired insulin secretion in prenatally androgenized male rhesus monkeys,” Journal of Clinical Endocrinology and Metabolism, vol. 89, no. 12, pp. 6218–6223, 2004.
[84]
K. Hogg, C. Wood, A. S. McNeilly, and W. C. Duncan, “The in utero programming effect of increased maternal androgens and a direct fetal intervention on liver and metabolic function in adult sheep,” PLoS ONE, vol. 6, no. 9, Article ID e24877, 2011.
[85]
M. J. Nyirenda, S. Dean, V. Lyons, K. E. Chapman, and J. R. Seckl, “Prenatal programming of hepatocyte nuclear factor 4α in the rat: a key mechanism in the “foetal origins of hyperglycaemia”?” Diabetologia, vol. 49, no. 6, pp. 1412–1420, 2006.
[86]
M. J. Nyirenda, R. S. Lindsay, C. J. Kenyon, A. Burchell, and J. R. Seckl, “Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring,” Journal of Clinical Investigation, vol. 101, no. 10, pp. 2174–2181, 1998.
[87]
K. L. Franko, D. A. Giussani, A. J. Forhead, and A. L. Fowden, “Effects of dexamethasone on the glucogenic capacity of fetal, pregnant, and non-pregnant adult sheep,” Journal of Endocrinology, vol. 192, no. 1, pp. 67–73, 2007.
[88]
M. J. Nyirenda, R. Carter, J. I. Tang et al., “Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11β-hydroxysteroid dehydrogenase type 1,” Diabetes, vol. 58, no. 12, pp. 2873–2879, 2009.
[89]
G. Li, A. Hernandez-Ono, R. M. Crooke, M. J. Graham, and H. N. Ginsberg, “Antisense reduction of 11β-hydroxysteroid dehydrogenase type 1 enhances energy expenditure and insulin sensitivity independent of food intake in C57BL/6J mice on a Western-type diet,” Metabolism, vol. 61, no. 6, pp. 823–835, 2012.
[90]
D. Xu, G. Liang, Y. E. Yan et al., “Nicotine-induced over-exposure to maternal glucocorticoid and activated glucocorticoid metabolism causes hypothalamic-pituitary-adrenal axis-associated neuroendocrine metabolic alterations in fetal rats,” Toxicology Letters, vol. 209, no. 3, pp. 282–290, 2012.
[91]
B. Valtat, C. Dupuis, D. Zenaty et al., “Genetic evidence of the programming of β cell mass and function by glucocorticoids in mice,” Diabetologia, vol. 54, no. 2, pp. 350–359, 2011.
[92]
G. Liang, M. Chen, X. L. Pan, J. Zheng, and H. Wang, “Ethanol-induced inhibition of fetal hypothalamic-pituitary-adrenal axis due to prenatal overexposure to maternal glucocorticoid in mice,” Experimental and Toxicologic Pathology, vol. 63, no. 7-8, pp. 607–611, 2011.
[93]
K. D. Bruce and M. A. Hanson, “The developmental origins, mechanisms, and implications of metabolic syndrome,” Journal of Nutrition, vol. 140, no. 3, pp. 648–652, 2010.
[94]
D. S. Fernandez-Twinn and S. E. Ozanne, “Mechanisms by which poor early growth programs type-2 diabetes, obesity and the metabolic syndrome,” Physiology and Behavior, vol. 88, no. 3, pp. 234–243, 2006.
[95]
M. S. Martin-Gronert and S. E. Ozanne, “Mechanisms linking suboptimal early nutrition and increased risk of type 2 diabetes and obesity,” Journal of Nutrition, vol. 140, no. 3, pp. 662–666, 2010.
[96]
H. Z. Deng, H. Deng, Z. Su et al., “Insulin resistance and adiponectin levels are associated with height catch-up growth in pre-pubertal Chinese individuals born small for gestational age,” Nutrition and Metabolism, vol. 9, no. 1, article 107, 2012.
[97]
N. J. Crowther, N. Cameron, J. Trusler, M. Toman, S. A. Norris, and I. P. Gray, “Influence of catch-up growth on glucose tolerance and β-cell function in 7-year-old children: results from the birth to twenty study,” Pediatrics, vol. 121, no. 6, pp. e1715–e1722, 2008.
[98]
K. K. Ong, C. J. Petry, P. M. Emmett et al., “Insulin sensitivity and secretion in normal children related to size at birth, postnatal growth, and plasma insulin-like growth factor-I levels,” Diabetologia, vol. 47, no. 6, pp. 1064–1070, 2004.
[99]
P. Cettour-Rose, S. Samec, A. P. Russell et al., “Redistribution of glucose from skeletal muscle to adipose tissue during catch-up fat: a link between catch-up growth and later metabolic syndrome,” Diabetes, vol. 54, no. 3, pp. 751–756, 2005.
[100]
A. G. Dulloo, “Thrifty energy metabolism in catch-up growth trajectories to insulin and leptin resistance,” Best Practice and Research in Clinical Endocrinology and Metabolism, vol. 22, no. 1, pp. 155–171, 2008.
[101]
A. G. Dulloo, J. Jacquet, J. Seydoux, and J.-. Montani, “The thrifty “catch-up fat” phenotype: its impact on insulin sensitivity during growth trajectories to obesity and metabolic syndrome,” International Journal of Obesity, vol. 30, supplement 4, pp. S23–S35, 2006.
[102]
N. S. Lima, E. G. de Moura, M. C. F. Passos et al., “Early weaning causes undernutrition for a short period and programmes some metabolic syndrome components and leptin resistance in adult rat offspring,” The British Journal of Nutrition, vol. 105, no. 9, pp. 1405–1413, 2011.
[103]
T. Pentinat, M. Ramon-Krauel, J. Cebria, R. Diaz, and J. C. Jimenez-Chillaron, “Transgenerational inheritance of glucose intolerance in a mouse model of neonatal overnutrition,” Endocrinology, vol. 151, no. 12, pp. 5617–5623, 2010.
[104]
H. Davidowa and A. Plagemann, “Insulin resistance of hypothalamic arcuate neurons in neonatally overfed rats,” NeuroReport, vol. 18, no. 5, pp. 521–524, 2007.
[105]
A. Plagemann, K. Roepke, T. Harder et al., “Epigenetic malprogramming of the insulin receptor promoter due to developmental overfeeding,” Journal of Perinatal Medicine, vol. 38, no. 4, pp. 393–400, 2010.
[106]
E. P. Conceicao, J. G. Franco, E. Oliveira et al., “Oxidative stress programming in a rat model of postnatal early overnutrition—role of insulin resistance,” Journal of Nutritional Biochemistry, vol. 24, no. 1, pp. 81–87, 2013.
[107]
D. Kaufman, M. A. Banerji, I. Shorman et al., “Early-life stress and the development of obesity and insulin resistance in juvenile bonnet macaques,” Diabetes, vol. 56, no. 5, pp. 1382–1386, 2007.
[108]
J. N. Gorski, A. A. Dunn-Meynell, T. G. Hartman, and B. E. Levin, “Postnatal environment overrides genetic and prenatal factors influencing offspring obesity and insulin resistance,” The American Journal of Physiology—Regulatory Integrative and Comparative Physiology, vol. 291, no. 3, pp. R768–R778, 2006.
[109]
E. de Oliveira, E. G. Moura, A. P. Santos-Silva et al., “Neonatal nicotine exposure causes insulin and leptin resistance and inhibits hypothalamic leptin signaling in adult rat offspring,” Journal of Endocrinology, vol. 206, no. 1, pp. 55–63, 2010.
[110]
S. Loizzo, G. Campana, S. Vella et al., “Post-natal stress-induced endocrine and metabolic alterations in mice at adulthood involve different pro-opiomelanocortin-derived peptides,” Peptides, vol. 31, no. 11, pp. 2123–2129, 2010.
[111]
A. Loizzo, S. Loizzo, G. Galietta et al., “Overweight and metabolic and hormonal parameter disruption are induced in adult male mice by manipulations during lactation period,” Pediatric Research, vol. 59, no. 1, pp. 111–115, 2006.
[112]
D. B. Baxi, P. K. Singh, K. D. Vachhrajani, and A. V. Ramachandran, “Plasticity changes in adult metabolic homeostasis and tissue oxidative stress: neonatal programming by corticosterone and melatonin as deprogrammer,” Journal of Maternal-Fetal and Neonatal Medicine, vol. 25, no. 6, pp. 831–844, 2012.
[113]
C. Alexanderson, E. Eriksson, E. Stener-Victorin, M. L？nn, and A. Holmáng, “Early postnatal oestradiol exposure causes insulin resistance and signs of inflammation in circulation and skeletal muscle,” Journal of Endocrinology, vol. 201, no. 1, pp. 49–58, 2009.
[114]
C. Nilsson, M. Niklasson, E. Eriksson, P. Bj？rntorp, and A. Holm？ng, “Imprinting of female offspring with testosterone results in insulin resistance and changes in body fat distribution at adult age in rats,” Journal of Clinical Investigation, vol. 101, no. 1, pp. 74–78, 1998.
[115]
E. G. Kuznetsova, T. G. Amstislavskaya, V. V. Bulygina, S. I. Il'nitskaya, M. A. Tibeikina, and Y. A. Skrinskaya, “Effects of administration of sodium glutamate during the neonatal period on behavior and blood corticosterone levels in male mice,” Neuroscience and Behavioral Physiology, vol. 37, no. 8, pp. 827–833, 2007.
[116]
B. Rácz, A. Tamás, P. Kiss et al., “Involvement of ERK and CREB signaling pathways in the protective effect of PACAP in monosodium glutamate-induced retinal lesion,” Annals of the New York Academy of Sciences, vol. 1070, pp. 507–511, 2006.
[117]
V. Chaparro-Huerta, M. C. Rivera-Cervantes, M. E. Flores-Soto, U. Gómez-Pinedo, and C. Beas-Zárate, “Proinflammatory cytokines and apoptosis following glutamate-induced excitotoxicity mediated by p38 MAPK in the hippocampus of neonatal rats,” Journal of Neuroimmunology, vol. 165, no. 1-2, pp. 53–62, 2005.
[118]
A. E. Hirata, I. S. Andrade, P. Vaskevicius, and M. S. Dolnikoff, “Monosodium glutamate (MSG)-obese rats develop glucose intolerance and insulin resistance to peripheral glucose uptake,” Brazilian Journal of Medical and Biological Research, vol. 30, no. 5, pp. 671–674, 1997.
[119]
R. Roman-Ramos, J. C. Almanza-Perez, R. Garcia-Macedo et al., “Monosodium glutamate neonatal intoxication associated with obesity in adult stage is characterized by chronic inflammation and increased mRNA expression of peroxisome proliferator-activated receptors in mice,” Basic and Clinical Pharmacology and Toxicology, vol. 108, no. 6, pp. 406–413, 2011.
[120]
Y. Sasaki, W. Suzuki, T. Shimada et al., “Dose dependent development of diabetes mellitus and non-alcoholic steatohepatitis in monosodium glutamate-induced obese mice,” Life Sciences, vol. 85, no. 13-14, pp. 490–498, 2009.
[121]
A. E. Andreazzi, D. X. Scomparin, F. P. Mesquita et al., “Swimming exercise at weaning improves glycemic control and inhibits the onset of monosodium L-glutamate-obesity in mice,” Journal of Endocrinology, vol. 201, no. 3, pp. 351–359, 2009.
[122]
Y. Sasaki, T. Shimada, S. Iizuka et al., “Effects of bezafibrate in nonalcoholic steatohepatitis model mice with monosodium glutamate-induced metabolic syndrome,” European Journal of Pharmacology, vol. 662, no. 1–3, pp. 1–8, 2011.
[123]
S. C. Maty, J. W. Lynch, T. E. Raghunathan, and G. A. Kaplan, “Childhood socioeconomic position, gender, adult body mass index, and incidence of type 2 diabetes mellitus over 34 years in the Alameda county study,” The American Journal of Public Health, vol. 98, no. 8, pp. 1486–1494, 2008.
[124]
T. Tamayo, H. Christian, and W. Rathmann, “Impact of early psychosocial factors (childhood socioeconomic factors and adversities) on future risk of type 2 diabetes, metabolic disturbances and obesity: a systematic review,” BMC Public Health, vol. 10, article 525, 2010.
[125]
A. F. van Abeelen, S. G. Elias, P. M. Bossuyt et al., “Famine exposure in the young and the risk of type 2 diabetes in adulthood,” Diabetes, vol. 61, no. 9, pp. 2255–2260, 2012.
[126]
F. M. Biro and M. Wien, “Childhood obesity and adult morbidities,” The American Journal of Clinical Nutrition, vol. 91, no. 5, pp. 1499S–1505S, 2010.
[127]
P. W. Franks, R. L. Hanson, W. C. Knowler, M. L. Sievers, P. H. Bennett, and H. C. Looker, “Childhood obesity, other cardiovascular risk factors, and premature death,” The New England Journal of Medicine, vol. 362, no. 6, pp. 485–493, 2010.
[128]
M. Caceres, C. G. Teran, S. Rodriguez, and M. Medina, “Prevalence of insulin resistance and its association with metabolic syndrome criteria among Bolivian children and adolescents with obesity,” BMC Pediatrics, vol. 8, article 31, 2008.
