Developmental origins of obesity and type 2 diabetes: Molecular aspects and role of chemicals

Environmental Health and Preventive Medicine

Volumn 18, Issue 3, 2013, Pages 185-197

  Inadera, Hidekuni ^a  

^a UNIVERSITY OF TOYAMA   (Japan)

Author keywords

Chemicals; Developmental origins of health and disease; Epigenetics; Obesity; Type 2 diabetes

Indexed keywords

DNA METHYLATION; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL FACTOR; EPIDEMIC; EPIGENETICS; GENETIC TRANSCRIPTION; HUMAN; MALNUTRITION; METABOLIC DISORDER; MOLECULAR MECHANICS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OBESITY; PREGNANCY; REVIEW; WEIGHT GAIN; CHEMICALLY INDUCED; DIABETES MELLITUS, TYPE 2; FEMALE; GENETIC EPIGENESIS; GENETICS; METABOLISM; NUTRITION; PHYSIOLOGICAL STRESS; POLLUTANT; PRENATAL EXPOSURE; PREVENTION AND CONTROL; RISK FACTOR; TOXICITY;

POLLUTANT; STEROID;

DIABETES MELLITUS, TYPE 2; ENVIRONMENTAL EXPOSURE; ENVIRONMENTAL POLLUTANTS; EPIGENESIS, GENETIC; FEMALE; HUMANS; NUTRITIONAL PHYSIOLOGICAL PHENOMENA; OBESITY; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RISK FACTORS; STEROIDS; STRESS, PHYSIOLOGICAL;

EID: 84877757578     PISSN: 1342078X     EISSN: 13474715     Source Type: Journal    
DOI: 10.1007/s12199-013-0328-8     Document Type: Review

References (170)

1. Zimmet P, Alberti KG, Shaw J. Global and societal implications of the diabetes epidemic. Nature. 2001;414:782-7.
2. Finucane MM, Stevens GA, Cowan MJ, Danaei G, Lin JK, Paciorek CJ, et al. National, regional, and global trends in body-mass index since 1980: systematic analysis of health examination surveys and epidemiological studies with 960 country-years and 9.1 million participants. Lancet. 2011;377:557-67.
3. Alexander CM, Landsman PB, Teutsch SM, Haffner SM. NCEP-defined metabolic syndrome, diabetes, and prevalence of coronary heart disease among NHANES III participants age 50 years and older. Diabetes. 2003;52:1210-4.
4. 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;359:61-73.
5. Godfrey KM, Barker DJ. Fetal programming and adult health. Public Health Nutr. 2001;4:611-24.
6. Ravelli GP, Stein ZA, Susser MW. Obesity in young men after famine exposure in utero and early infancy. N Engl J Med. 1976;295:349-53.
7. Hofman PL, Regan F, Jackson WE, Jefferies C, Knight DB, Robinson EM, et al. Premature birth and later insulin resistance. N Engl J Med. 2004;351:2179-86.
8. Gluckman PD, Hanson MA, editors. Developmental origins of health and disease. Cambridge: Cambridge University Press; 2006.
9. Huxley R, Neil A, Collins R. Unravelling the fetal origins hypothesis: is there really an inverse association between birthweight and subsequent blood pressure? Lancet. 2002;360:659-65.
10. Newsome CA, Shiell AW, Fall CH, Phillips DI, Shier R, Law CM. Is birth weight related to later glucose and insulin metabolism? - a systematic review. Diabet Med. 2003;20:339-48.
11. Huxley R, Owen CG, Whincup PH, Cook DG, Colman S, Collins R. Birth weight and subsequent cholesterol levels: exploration of the "fetal origins" hypothesis. JAMA. 2004;292:2755-64.
12. Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004;305:1733-6.
13. Barker DJ, Osmond C. Infant mortality, childhood nutrition, and ischemic heart disease in England and Wales. Lancet. 1986;1:1077-81.
14. Barker DJ, Winter PD, Osmond C, Margetts B, Simmonds SJ. Weight in infancy and death from ischemic heart disease. Lancet. 1989;2:577-80.
15. Hales CN, Barker DJ. Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis. Diabetologia. 1992;35:595-601.
16. Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS. Fetal nutrition and cardiovascular disease in adult life. Lancet. 1993;341:938-41.
17. Barker DJ, Hales CN, Fall CH, Osmond C, Phipps K, Clark PM. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993;36:62-7.
18. Phillips DI, Barker DJ, Hales CN, Hirst S, Osmond C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994;37:150-4.
19. Frankel S, Elwood P, Sweetnam P, Yarnell J, Smith GD. Birthweight, body-mass index in middle age, and incident coronary heart disease. Lancet. 1996;348:1478-80.
20. Stein CE, Fall CH, Kumaran K, Osmond C, Cox V, Barker DJ. Fetal growth and coronary heart disease in south India. Lancet. 1996;48:1269-73.
21. Benyshek DC, Martin JF, Johnston CS. A reconsideration of the origins of the type 2 diabetes epidemic among Native Americans and the implications for intervention policy. Med Anthropol. 2001;20:25-64.
22. Kajantie E, Osmond C, Barker DJ, Forsen T, Phillips DI, Eriksson JG. Size at birth as a predictor of mortality in adulthood: a follow-up of 350000 person-years. Int J Epidemiol. 2005;34:655-63.
23. Leon DA, Lithell HO, Vagero D, Koupilova I, Mohsen R, Berglund L, et al. Reduced fetal growth rate and increased risk of death from ischemic heart disease: cohort study of 15000 Swedish men and women born 1915-29. Br Med J. 1998;317:241-5.
24. Slomko H, Heo HJ, Einstein FH. Epigenetics of obesity and diabetes in humans. Endocrinology. 2012;153:1025-30.
25. Lumey LH, Stein AD, Kahn HS, van der Pal-de Bruin KM, Blauw GJ, Zybert PA, et al. Cohort profile: the Dutch Hunger Winter families study. Int J Epidemiol. 2007;36:1196-204.
26. 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;70:811-6.
27. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP. Perceived health of adults after prenatal exposure the Dutch famine. Paediatr Perinat Epidemiol. 2003;17:391-7.
28. Ravelli AC, van der Meulen JH, Michels RP, Osmond C, Barker DJ, Hales CN, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351:173-7.
29. Painter RC, Roseboom TJ, Bleker OP. Prenatal exposure to the Dutch famine and disease in later life: an overview. Reprod Toxicol. 2005;20:345-52.
30. Phillips DI. Insulin resistance as a programmed response to fetal undernutrition. Diabetologia. 1996;39:1119-22.
31. Curhan GC, Willett WC, Rimm EB, Spiegelman D, Ascherio AL, Stampfer MJ. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996;94:3246-50.
32. Nobili V, Alisi A, Panera N, Agostoni C. Low birth weight and catch-up-growth associated with metabolic syndrome: a ten year systematic review. Pediatr Endocrinol Rev. 2008;6:241-7.
33. Dufour S, Petersen KF. Disassociation of liver and muscle insulin resistance from ectopic lipid accumulation in low-birth-weight individuals. J Clin Endocrinol Metab. 2011;96:3873-80.
34. Barouki R, Gluckman PD, Grandjean P, Hanson M, Heindel JJ. Developmental origins of non-communicable disease: implications for research and public health. Environ Health. 2012;11:42.
35. Wang Y, Wang X, Kong Y, Zhang JH, Zeng Q. The Great Chinese Famine leads to shorter and overweight females in Chongqing Chinese population after 50 years. Obesity. 2010;18:588-92.
36. Hult M, Tornhammar P, Ueda P, Chima C, Bonamy AK, Ozumba B, et al. Hypertension, diabetes and overweight: looming legacies of the Biafran famine. PLoS One. 2010;5:e13582.
37. Stein AD, Lumey LH. The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: the Dutch famine Birth Cohort Study. Hum Biol. 2000;72:641-54.
38. Eriksson JG, Forsen TJ, Osmond C, Barker DJ. Pathways of infant and childhood growth that lead to type 2 diabetes. Diabetes Care. 2003;26:3006-10.
39. Eriksson JG, Osmond C, Kajantie E, Forsen TJ, Barker DJ. Patterns of growth among children who later develop type 2 diabetes or its risk factors. Diabetologia. 2006;49:2853-8.
40. Dai Y, Thamotharan S, Garg M, Shin BC, Devakar SU. Superimposition of postnatal calorie restriction protects the aging male intrauterine growth-restricted offspring from metabolic maladaptations. Endocrinology. 2012;153:4216-26.
41. Garg M, Thamotharan M, Dai Y, Thamotharan S, Shin BC, Stout D, et al. Early postnatal caloric restriction protects adult male intrauterine growth-restricted offspring from obesity. Diabetes. 2012;61:1391-8.
42. Pinney SE, Simmons RA. Metabolic programming, epigenetics, and gestational diabetes mellitus. Curr Diab Rep. 2012;12:67-74.
43. Barker DJ, Osmond C, Simmonds SJ, Wield GA. The relation of small head circumference and thinness at birth to death from cardiovascular disease in adult life. Br Med J. 1993;306:422-6.
44. Phillips DI. Programming of the stress response: a fundamental mechanism underlying the long-term effects of the fetal environment? J Intern Med. 2007;261:453-60.
45. Benediktsson R, Lindsay RS, Noble J, Seckl JR, Edwards CR. Glucocorticoid exposure in utero: new model for adult hypertension. Lancet. 1993;341:339-41.
46. Levitt NS, Lindsay RS, Holmes MC, Seckl JR. Dexamethasone in the last week of pregnancy attenuates hippocampal glucocorticoid receptor gene expression and elevates blood pressure in the adult offspring in the rat. Neuroendocrinology. 1996;64:412-8.
47. 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;101:2174-81.
48. Buhl ES, Neschen S, Yonemitsu S, Rossbacher J, Zhang D, Morino K, et al. Increased hypothalamic-pituitary-adrenal axis activity and hepatic insulin resistance in low-birth weight rats. Am J Physiol Endocrinol Metab. 2007;293:E1451-8.
49. 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;19:1-19.
50. Dalziel SR, Walker NK, Parag V, Mantell C, Rea HH, Rodgers A, et al. Cardiovascular risk factors after antenatal exposure to betamethasone: 30-year follow-up of a randomised controlled trial. Lancet. 2005;365:1856-62.
51. Langley-Evans SC. Hypertension induced by foetal exposure to a maternal low-protein diet, in the rat, is prevented by pharmacological blockade of maternal glucocorticoid synthesis. J Hypertens. 1997;15:537-44.
52. Bourque SL, Komolova M, McCabe K, Adams MA, Nakatsu K. Perinatal iron deficiency combined with a high-fat diet causes obesity and cardiovascular dysregulation. Endocrinology. 2012;153:1174-82.
53. Godfrey KM, Sheppard A, Gluckman PD, Lillycrop KA, Burdge GC, McLean C, et al. Epigenetic gene promoter methylation at birth is associated with child's later adiposity. Diabetes. 2011;60:1528-34.
54. 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:E83-7.
55. Shiell AW, Campbell-Brown M, Haselden S, Robinson S, Godfrey KM, Barker DJ. High-meat, low-carbohydrate diet in pregnancy: relation to adult blood pressure in the offspring. Hypertension. 2001;38:1282-8.
56. Langley-Evans SC, Phillips GJ, Jackson AA. In utero exposure to maternal low protein diets induces hypertension in weanling rats, independently of maternal blood pressure changes. Clin Nutr. 1994;13:319-24.
57. Maloney CA, Gosby AK, Phuyal JL, Denyer GS, Bryson JM, Caterson ID. Site-specific changes in the expression of fat-partitioning genes in weanling rats exposed to a low-protein diet in utero. Obes Res. 2003;11:461-8.
58. Langley-Evans SC. Critical differences between two low protein diet protocols in the programming of hypertension in the rat. Int J Food Sci Nutr. 2005;51:11-7.
59. Kwong WY, Wild AE, Roberts P, Willis AC, Fleming TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000;127:4195-202.
60. McMillen IC, Robinson JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005;85:571-633.
61. Alexander BT. Fetal programming of hypertension. Am J Physiol Regul Integr Comp Physiol. 2006;290:R1-10.
62. 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;57:107-18.
63. Gheorghe CP, Goyal R, Holweger JD, Longo LD. Placental gene expression responses to maternal protein restriction in the mouse. Placenta. 2009;30:411-7.
64. Lillycrop KA, Rodford J, Garratt ES, Slater-Jefferies JL, Godfrey KM, Gluckman PD, et al. Maternal protein restriction with or without folic acid supplementation during pregnancy alters the hepatic transcriptome in adult male rats. Br J Nutr. 2010;103:1711-9.
65. Jones PA, Takai D. The role of DNA methylation in mammalian epigenetics. Science. 2001;293:1068-70.
66. Bird A. DNA methylation patterns and epigenetic memory. Genes Dev. 2002;16:6-21.
67. Drake AJ, Walker BR, Seckl JR. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am J Physiol Regul Integr Comp Physiol. 2005;288:R34-8.
68. 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;97:435-9.
69. Burdge GC, Lillycrop KA. Nutrition, epigenetics, and developmental plasticity: implications for understanding human disease. Annu Rev Nutr. 2010;30:315-39.
70. Ooki S. Life course genetic epidemiologic study based on longitudinal twin-family data: a new perspective (in Japanese). Nihon Eiseigaku Zasshi. 2011;66:31-8.
71. Drong AW, Lindgren CM, McCarthy MI. The genetic and epigenetic basis of type 2 diabetes and obesity. Clin Pharmacol Ther. 2012;92:707-15.
72. Waterland RA, Jirtle RL. Early nutrition, epigenetic changes at transposons and imprinted genes, and enhanced susceptibility to adult chronic diseases. Nutrition. 2004;20:63-8.
73. Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr Res. 2007;61:5R-10R.
74. Dolinoy DC, Huang D, Jirtle RL. Maternal nutrient supplementation counteracts bisphenol A-induced DNA hypomethylation in early development. Proc Natl Acad Sci USA. 2007;104:13056-61.
75. Ling C, Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes. 2009;58:2718-25.
76. Heindel JJ, vom Saal FS. Role of nutrition and environmental endocrine disrupting chemicals during the perinatal period on the aetiology of obesity. Mol Cell Endocrinol. 2009;304:90-6.
77. 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;135:1382-6.
78. 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;100:520-6.
79. 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 Pdx 1. J Clin Invest. 2008;118:2316-24.
80. Waterland RA, Jirtle RL. Transposable elements: targets for early nutritional effects on epigenetic gene regulation. Mol Cell Biol. 2003;23:5293-300.
81. Sinclair KD, Allegrucci C, Singh R, Gardner DS, Sebastian S, Bispham J, 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;104:19351-6.
82. Lillycrop KA, Phillips ES, Torrens C, Hanson MA, Jackson AA, Burdge GC. Feeding pregnant rats a protein-restricted diet persistently alters the methylation of specific cytosines in the hepatic PPAR alpha promoter of the offspring. Br J Nutr. 2008;100:278-82.
83. 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;99:540-9.
84. Heijmans BT, Tobi EW, Stein AD, Putter H, Blauw GJ, Susser ES, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci USA. 2008;105:17046-9.
85. Tobi EW, Lumey LH, Talens RP, Kremer D, Putter H, Stein AD, et al. DNA methylation differences after exposure to prenatal famine are common and timing- and sex-specific. Hum Mol Genet. 2009;18:4046-53.
86. Baillie-Hamilton PF. Chemical toxins: a hypothesis to explain the global obesity epidemic. J Altern Complement Med. 2002;8:185-92.
87. Heindel JJ. Endocrine disruptors and the obesity epidemic. Toxicol Sci. 2003;76:247-9.
88. Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS, Soto AM, et al. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr Rev. 2009;30:293-342.
89. Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. Environ Health Perspect. 2008;116:39-44.
90. Vandenberg LN, Hauser R, Marcus M, Olea N, Welshons WV. Human exposure to bisphenol A. Reprod Toxicol. 2007;24:139-77.
91. Mullerova D, Kopecky J. White adipose tissue: storage and effector site for environmental pollutants. Physiol Res. 2007;56:375-81.
92. Toschke AM, Koletzko B, Slikker W Jr, Hermann M, von Kries R. Childhood obesity is associated with maternal smoking in pregnancy. Eur J Pediatr. 2002;161:445-8.
93. Power C, Jefferis BJ. Fetal environment and subsequent obesity: a study of maternal smoking. Int J Epidemiol. 2002;31:413-9.
94. Al Mamun A, Lawlor DA, Alati R, O'Callaghan MJ, Williams GM, Najman JM. Does maternal smoking during pregnancy have a direct effect on future offspring obesity? Evidence from a prospective birth cohort study. Am J Epidemiol. 2006;164:317-25.
95. Wang SL, Tsai PC, Yang CY, Leon Guo Y. Increased risk of diabetes and polychlorinated biphenyls and dioxins: a 24-year follow-up study of the Yucheng cohort. Diabetes Care. 2008;31:1574-9.
96. Park JS, Bergman A, Linderholm L, Athanasiadou M, Kocan A, Petrik J, et al. Placental transfer of polychlorinated biphenyls, their hydroxylated metabolites and pentachlorophenol in pregnant women from eastern Slovakia. Chemosphere. 2008;70:1676-84.
97. Smink A, Ribas-Fito N, Garcia R, Torrent M, Mendez MA, Grimalt JO, et al. Exposure to hexachlorobenzene during pregnancy increases the risk of overweight in children aged 6 years. Acta Paediatr. 2008;97:1465-9.
98. Karmaus W, Osuch JR, Eneli I, Mudd LM, Zhang J, Mikucki D, et al. Maternal level of dichlorodiphenyl-dichloroethylene (DDE) may increase weight and body mass index in adult female offspring. Occup Environ Med. 2009;66:143-9.
99. Janesick A, Blumberg B. Endocrine disrupting chemicals and the developmental programming of adipogenesis and obesity. Birth Defects Res C Embryo Today. 2011;93:34-50.
100. Lee DH, Lee IK, Song K, Steffes M, Toscano W, Baker BA, et al. A strong dose-response relation between serum concentration of persistent organic pollutants and diabetes: results from the National Health and Examination Survey 1999-2002. Diabetes Care. 2006;29:1638-44.
101. Porta M. Persistent organic pollutants and the burden of diabetes. Lancet. 2006;368:558-9.
102. Vasiliu O, Cameron L, Gardiner J, Deguire P, Karmaus W. Polybrominated biphenyls, polychlorinated biphenyls, body weight, and incidence of adult-onset diabetes mellitus. Epidemiology. 2006;17:352-9.
103. Verhulst SL, Nelen V, Hond ED, Deguire P, Karmaus W. Intrauterine exposure to environmental pollutants and body mass index during the first 3 years of life. Environ Health Perspect. 2009;117:122-6.
104. Halldorsson TI, Rytter D, Haug LS, Bech BH, Danielsen I, Becher G, et al. Prenatal exposure to perfluorooctanoate and risk of overweight at 20 years of age: a prospective cohort study. Environ Health Perspect. 2012;120:668-73.
105. Moreno-Aliaga MJ, Matsumura F. Effects of 1,1,1-trichloro-2,2-bis(p- chlorophenyl)-ethane (p, p′-DDT) on 3T3-L1 and 3T3 F442A adipocyte differentiation. Biochem Pharmacol. 2002;63:997-1007.
106. Newbold RR, Padilla-Banks E, Snyder RJ, Jefferson WN. Developmental exposure to estrogenic compounds and obesity. Birth Defects Res A Clin Mol Teratol. 2005;73:478-80.
107. Howdeshell KL, Hotchkiss AK, Thayer KA, Vandenberg JG, vom Saal FS. Exposure to bisphenol A advances puberty. Nature. 1999;401:763-4.
108. Somm E, Schwitzgebel VM, Toulotte A, Cederroth CR, Combescure C, Nef S, et al. Perinatal exposure to bisphenol a alters early adipogenesis in the rat. Environ Health Perspect. 2009;117:1549-55.
109. Wei J, Lin Y, Li Y, Ying C, Chen J, Song L, et al. Perinatal exposure to bisphenol A at reference dose predisposes offspring to metabolic syndrome in adult rats on a high-fat diet. Endocrinology. 2011;152:3049-61.
110. Newbold RR, Padilla-Banks E, Jefferson WN. Perinatal exposure to environmental estrogens and the development of obesity. Mol Nutr Food Res. 2007;51:912-7.
111. Newbold RR, Padilla-Banks E, Jefferson WN. Environmental estrogens and obesity. Mol Cell Endocrinol. 2009;304:84-9.
112. Wright C, Evans AC, Evans NP, Duffy P, Fox J, Boland MP, et al. Effect of maternal exposure to the environmental estrogen, octylphenol, during fetal and/or postnatal life on onset of puberty, endocrine status, and ovarian follicular dynamics in ewe lambs. Biol Reprod. 2002;67:1734-40.
113. Cook PS, Naaz A. Role of estrogens in adipocyte development and function. Exp Biol Med. 2004;229:1127-35.
114. Rantakokko P, Turunen A, Verkasalo PK, Kiviranta H, Mannisto S, Vartiainen T. Blood levels of organotin compounds and their relation to fish consumption in Finland. Sci Total Environ. 2008;399:90-5.
115. Inadera H, Shimomura A. Environmental chemical tributyltin augments adipocyte differentiation. Toxicol Lett. 2005;74:226-34.
116. Kanayama T, Kobayashi N, Mamiya T, Nakanishi T, Nishikawa J. Organotin compounds promote adipocyte differentiation as agonists of the peroxisome proliferators-activated receptor gamma/retinoid X receptor pathway. Mol Pharmacol. 2005;67:766-74.
117. Grun F, Watanabe H, Zamanian Z, Maeda L, Arima K, Cubacha R, et al. Endocrine-disrupting organotin compounds are potent inducers of adipogenesis in vertebrates. Mol Endocrinol. 2006;20:2141-55.
118. Kirchner S, Kieu T, Chow C, Casey S, Blumberg B. Prenatal exposure to the environmental obesogen tributyltin predisposes multipotent stem cells to become adipocytes. Mol Endocrinol. 2010;24:526-39.
119. Penza M, Jeremic M, Marrazzo E, Maggi A, Ciana P, Rando G, et al. The environmental chemical tributyltin chloride (TBT) shows both estrogenic and adipogenic activities in mice which might depend on the exposure dose. Toxicol Appl Pharmacol. 2011;255:65-75.
120. Feige JN, Gelman L, Rossi D, Zoete V, Metivier R, Tudor C, et al. The endocrine disruptor monoethyl-hexyl-phthalate is a selective peroxisome proliferator-activated receptor gamma modulator that promotes adipogenesis. J Biol Chem. 2007;282:19152-66.
121. Anway MD, Cupp AS, Uzumcu M, Skinner MK. Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science. 2005;308:1466-9.
122. Jirtle RL, Skinner MK. Environmental epigenomics and disease susceptibility. Nat Rev Genet. 2007;8:253-62.
123. Skinner MK, Anway MD, Savenkova MI, Gore AC, Crews D. Transgenerational epigenetic programming of the brain transcriptome and anxiety behavior. PLoS One. 2008;3:e3745.
124. Casals-Casas C, Desvergne B. Endocrine disruptors: from endocrine to metabolic disruption. Annu Rev Physiol. 2011;73:135-62.
125. Vandenberg LN, Colborn T, Hayes TB, Heindel JJ, Jacobs DR Jr, Lee DH, et al. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr Rev. 2012;33:378-455.
126. Woodruff TJ, Zota AR, Schwartz JM. Environmental chemicals in pregnant women in the US: NHANES 2003-2004. Environ Health Perspect. 2011;119:878-85.
127. de Rooij SR, Painter RC, Roseboom TJ, Phillips DI, Osmond C, Barker DJ, et al. Glucose tolerance at age 58 and the decline of glucose tolerance in comparison with age 50 in people prenatally exposed to the Dutch famine. Diabetologia. 2006;49:637-43.
128. de Rooij SR, Painter RC, Phillips DI, Osmond C, Michels RP, Godsland IF, et al. Impaired insulin secretion after prenatal exposure to the Dutch famine. Diabetes Care. 2006;29:1897-901.
129. de Rooij SR, Painter RC, Phillips DI, Osmond C, Tanck NW, Defesche JC, et al. The effects of the Pro12Ala polymorphism of the peroxisome proliferators-activated receptor-gamma2 gene on glucose/insulin metabolism interact with prenatal exposure to famine. Diabetes Care. 2006;29:1052-7.
130. Stein AD, Kahn HS, Rundle A, Zybert PA, van der Pal-de Bruin K, Lumey LH. Anthropometric measures in middle age after exposure to famine during gestation: evidence from the Dutch Famine. Am J Clin Nutr. 2007;85:869-76.
131. de Rooij SR, Painter RC, Holleman F, Bossuyt PM, Roseboom TJ. The metabolic syndrome in adults prenatally exposed to the Dutch famine. Am J Clin Nutr. 2007;86:1219-24.
132. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Bleker OP. Plasma lipid profiles in adults after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2000;72:1101-6.
133. Lumey LH, Stein AD, Kahn HS, Romijn JA. Lipid profiles in middle-aged men and women after famine exposure during gestation: the Dutch Hunger Winter Families Study. Am J Clin Nutr. 2009;89:1737-43.
134. Roseboom TJ, van der Meulen JH, Ravelli AC, van Montfrans GA, Osmond C, Barker DJ, et al. Blood pressure in adults after prenatal exposure to famine. J Hypertens. 1999;17:325-30.
135. Roseboom TJ, van der Meulen JH, van Montfrans GA, Ravelli AC, Osmond C, Barker DJ, et al. Maternal nutrition during gestation and blood pressure in later life. J Hypertens. 2001;19:29-34.
136. Stein AD, Zybert PA, van der Pal-de Bruin K, Lumey LH. Exposure to famine during gestation, size at birth, and blood pressure at age 59 years: evidence from the Dutch Famine. Eur J Epidemiol. 2006;21:759-65.
137. Painter RC, de Rooij SR, Bossuyt PM, Phillips DI, Osmond C, Barker DJ, et al. Blood pressure response to psychological stressors in adults after prenatal exposure to the Dutch famine. J Hypertens. 2006;24:1771-8.
138. Roseboom TJ, van der Meulen JH, Osmond C, Barker DJ, Ravelli AC, Schroeder-Tanka JM, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944-45. Heart. 2000;84:595-8.
139. Painter RC, de Rooij SR, Bossuyt PM, Simmers TA, Osmond C, Barker DJ, et al. Early onset of coronary artery disease after prenatal exposure to the Dutch famine. Am J Clin Nutr. 2006;84:322-7.
140. Painter RC, Roseboom TJ, Bossuyt PM, Osmond C, Barker DJ, Bleker OP. Adult mortality at age 57 after prenatal exposure to the Dutch famine. Eur J Epidemiol. 2005;20:673-6.
141. Painter RC, de Rooij SR, Hutten BA, Bossuyt PM, de Groot E, Osmond C, et al. Reduced intima media thickness in adults after prenatal exposure to the Dutch famine. Atherosclerosis. 2007;193:421-7.
142. van Abeelen AF, Veenendaal MV, Painter RC, de Rooij SR, Dijkgraaf MG, Bossuyt PM, et al. Survival effects of prenatal famine exposure. Am J Clin Nutr. 2012;95:179-83.
143. Susser E, Neugebauer R, Hoek HW, Brown AS, Lin S, Labovitz D, et al. Schizophrenia after prenatal famine. Further evidence. Arch Gen Psychiatry. 1996;53:25-31.
144. Roseboom TJ, van der Meulen JH, Ravelli AC, Osmond C, Barker DJ, Bleker OP, et al. Plasma fibrinogen and factor VII concentrations in adults after prenatal exposure to famine. Br J Haematol. 2000;111:112-7.
145. Lopuhaa CE, Roseboom TJ, Osmond C, Barker DJ, Ravelli AC, Bleker OP, et al. Atopy, lung function, and obstructive airways disease after prenatal exposure to famine. Thorax. 2000;55:555-61.
146. de Rooij SR, Painter RC, Phillips DI, Osmond C, Michels RP, Bossuyt PM, et al. Hypothalamic-pituitary-adrenal axis activity in adults who were prenatally exposed to the Dutch famine. Eur J Endocrinol. 2006;155:153-60.
147. Lai MS, Hsueh YM, Chen CJ, Shyu MP, Chen SY, Kuo TL, et al. Ingested inorganic arsenic and prevalence of diabetes mellitus. Am J Epidemiol. 1994;139:484-92.
148. Henriksen GL, Ketchum NS, Michalek JE, Swaby JA. Serum dioxin and diabetes mellitus in veterans of Operation Ranch Hand. Epidemiology. 1997;8:252-8.
149. Longnecker MP, Michalek JE. Serum dioxin level in relation to diabetes mellitus among Air Force veterans with background levels of exposure. Epidemiology. 2000;11:44-8.
150. Gladen BC, Ragan NB, Rogan WJ. Pubertal growth and development and prenatal and lactational exposure to polychlorinated biphenyls and dichlorodiphenyl dichloroethene. J Pediatr. 2000;136:490-6.
151. Cox S, Niskar AS, Narayan KM, Marcus M. Prevalence of self-reported diabetes and exposure to organochlorine pesticides among Mexican Americans: Hispanic health and nutrition examination survey, 1982-1984. Environ Health Perspect. 2007;115:1747-52.
152. Codru N, Schymura MJ, Negoita S, Akwesasne Task Force on Environment, Rei R, Carpenter DO. Diabetes in relation to serum levels of polychlorinated biphenyls and chlorinated pesticides in adult Native Americans. Environ Health Perspect. 2007;115:1442-7.
153. Lee DH, Lee IK, Porta M, Steffes M, Jacobs DR Jr. Relationship between serum concentrations of persistent organic pollutants and the prevalence of metabolic syndrome among non-diabetic adults: results from the National Health and Nutrition Examination Survey 1999-2002. Diabetologia. 2007;50:1841-51.
154. Hanswell-Elkins M, Satarug S, O'Rourke P, Moore M, Ng J, McGrath V, et al. Striking association between urinary cadmium level and albuminuria among Torres Strait Islander people with diabetes. Environ Res. 2008;106:379-83.
155. Michalek JE, Pavuk M. Diabetes and cancer in veterans of Operation Ranch Hand after adjustment for calendar period, days of spraying, and time spent in Southeast Asia. J Occup Environ Med. 2008;50:330-40.
156. Rignell-Hydbom A, Lidfeldt J, Kiviranta H, Rantakokko P, Samsioe G, Agardh CD, et al. Exposure to p, p′-DDE: a risk factor for type 2 diabetes. PLoS One. 2009;4:e7503.
157. Lundin JI, Alexander BH, Olsen GW, Church TR. Ammonium perfluorooctanoate production and occupational mortality. Epidemiology. 2009;20:921-8.
158. Turyk M, Anderson H, Knobeloch L, Imm P, Persky V. Organochlorine exposure and incidence of diabetes in a cohort of Great Lakes sport fish consumers. Environ Health Perspect. 2009;117:1076-82.
159. Lopez-Espinosa MJ, Freire C, Arrebola JP, Navea N, Taoufiki J, Fernandez MF, et al. Nonylphenol and octylphenol in adipose tissue of women in Southern Spain. Chemosphere. 2009;76:847-52.
160. Ukropec J, Radikova Z, Huckova M, Koska J, Kocan A, Sebokova E, et al. High prevalence of prediabetes and diabetes in a population exposed to high levels of an organochlorine cocktail. Diabetologia. 2010;53:899-906.
161. Son HK, Kim SA, Kang JH, Chang YS, Park SK, Lee SK, et al. Strong associations between low-dose organochlorine pesticides and type 2 diabetes in Korea. Environ Int. 2010;36:410-4.
162. Lee DH, Steffes MW, Sjodin A, Jones RS, Needham LL, Jacobs DR Jr. Low dose of some persistent organic pollutants predicts type 2 diabetes: a nested case-control study. Environ Health Perspect. 2010;118:1235-42.
163. Park SK, Son HK, Lee SK, Kang JH, Chang YS, Jacobs DR, et al. Relationship between serum concentrations of organochlorine pesticides and metabolic syndrome among non-diabetic adults. J Prev Med Public Health. 2010;43:1-8.
164. Mendez MA, Garcia-Esteban R, Guxens M, Vrijheid M, Kogevinas M, Goni F, et al. Prenatal organochlorine compound exposure, rapid weight gain, and overweight in infancy. Environ Health Perspect. 2011;119:272-8.
165. Carwile JL, Michels KB. Urinary bisphenol A and obesity: NHANES 2003-2006. Environ Res. 2011;111:825-30.
166. Gasull M, Pumarega J, Tellez-Plaza M, Castell C, Tresserras R, Lee DH, et al. Blood concentrations of persistent organic pollutants and prediabetes and diabetes in the general population of Catalonia. Environ Sci Technol. 2012;46:7799-810.
167. Merali Z, Singhal RL. Diabetogenic effects of chronic oral cadmium administration to neonatal rats. Br J Pharmacol. 1980;69:151-7.
168. Rubin BS, Murray MK, Damassa DA, King JC, Soto AM. Perinatal exposure to low doses of bisphenol A affects body weight, patterns of estrous cyclicity, and plasma LH levels. Environ Health Perspect. 2001;109:657-80.
169. Miyawaki J, Sakayama K, Kato H, Yamamoto H, Masuno H. Perinatal and postnatal exposure to bisphenol a increases adipose tissue mass and serum cholesterol level in mice. J Atheroscler Thromb. 2007;14:245-52.
170. Hines EP, White SS, Stanko JP, Gibbs-Flournoy EA, Lau C, Fenton SE. Phenotypic dichotomy following developmental exposure to perfluorooctanoic acid (PFOA) in female CD-1 mice: low doses induce elevated serum leptin and insulin, and overweight in mid-life. Mol Cell Endocrinol. 2009;304:97-105.