Prenatal Steroids and Metabolic Dysfunction: Lessons from Sheep

Literature Cited

1. 1.  Barker D 2004. The developmental origins of adult disease. J. Am. Coll. Nutr. 23:588S–95S
   [Google Scholar]
2. 2.  Fowden AL, Forhead AJ 2004. Endocrine mechanisms of intrauterine programming. Reproduction 127:515–26
   [Google Scholar]
3. 3.  Padmanabhan V, Cardoso RC, Puttabyatappa M 2016. Developmental programming, a pathway to disease. Endocrinology 157:1328–40
   [Google Scholar]
4. 4.  Hanson MA, Gluckman P 2014. Early developmental conditioning of later health and disease: Physiology or pathophysiology?. Physiol. Rev. 94:1027–76
   [Google Scholar]
5. 5.  Barker DJ 2007. The origins of the developmental origins theory. J. Intern. Med. 261:412–17
   [Google Scholar]
6. 6.  Ravelli GP, Stein ZA, Susser MW 1976. Obesity in young men after famine exposure in utero and early infancy. N. Engl. J. Med. 295:349–53
   [Google Scholar]
7. 7.  Gluckman PD, Hanson MA 2004. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr. Res. 56:311–17
   [Google Scholar]
8. 8.  Nijland MJ, Ford SP, Nathanielsz PW 2008. Prenatal origins of adult disease. Curr. Opin. Obstet. Gynecol. 20:132–38
   [Google Scholar]
9. 9.  Ganu RS, Harris RA, Collins K, Aagaard KM 2012. Maternal diet: a modulator for epigenomic regulation during development in nonhuman primates and humans. Int. J. Obes. Suppl. 2:S14–S18
   [Google Scholar]
10. 10.  Trevino LS, Wang Q, Walker CL 2015. Phosphorylation of epigenetic “readers, writers and erasers”: implications for developmental reprogramming and the epigenetic basis for health and disease. Prog. Biophys. Mol. Biol. 118:8–13
    [Google Scholar]
11. 11.  Markey CM, Coombs MA, Sonnenschein C, Soto AM 2003. Mammalian development in a changing environment: Exposure to endocrine disruptors reveals the developmental plasticity of steroid‐hormone target organs. Evol. Dev 5:67–75
    [Google Scholar]
12. 12.  McEwen B 1992. Steroid hormones: effect on brain development and function. Hormone Res. Paediatr. 37:1–10
    [Google Scholar]
13. 13.  Gore AC 2008. Developmental programming and endocrine disruptor effects on reproductive neuroendocrine systems. Front. Neuroendocrinol. 29:358–74
    [Google Scholar]
14. 14.  Puttabyatappa M, Cardoso RC, Padmanabhan V 2015. Effect of maternal PCOS and PCOS-like phenotype on the offspring's health. Mol. Cell. Endocrinol. 435:29–39
    [Google Scholar]
15. 15.  Frye C, Bo E, Calamandrei G, Calza L, Dessì‐Fulgheri F et al. 2012. Endocrine disrupters: a review of some sources, effects, and mechanisms of actions on behaviour and neuroendocrine systems. J. Neuroendocrinol. 24:144–59
    [Google Scholar]
16. 16.  Hakim C, Padmanabhan V, Vyas AK 2016. Gestational hyperandrogenism in developmental programming. Endocrinology 158:199–212
    [Google Scholar]
17. 17.  Diamanti-Kandarakis E, Bourguignon JP, Giudice LC, Hauser R, Prins GS et al. 2009. Endocrine-disrupting chemicals: an Endocrine Society scientific statement. Endocr. Rev. 30:293–342
    [Google Scholar]
18. 18.  Cardoso RC, Puttabyatappa M, Padmanabhan V 2015. Steroidogenic versus metabolic programming of reproductive neuroendocrine, ovarian and metabolic dysfunctions. Neuroendocrinology 102:226–37
    [Google Scholar]
19. 19.  Abbott DH, Nicol LE, Levine JE, Xu N, Goodarzi MO, Dumesic DA 2013. Nonhuman primate models of polycystic ovary syndrome. Mol. Cell. Endocrinol. 373:21–28
    [Google Scholar]
20. 20.  Padmanabhan V, Veiga-Lopez A 2013. Animal models of the polycystic ovary syndrome phenotype. Steroids 78:734–40
    [Google Scholar]
21. 21.  Padmanabhan V, Veiga-Lopez A 2013. Sheep models of polycystic ovary syndrome phenotype. Mol. Cell. Endocrinol. 373:8–20
    [Google Scholar]
22. 22.  Wood RI, Foster DL 1998. Sexual differentiation of reproductive neuroendocrine function in sheep. Rev. Reprod. 3:130–40
    [Google Scholar]
23. 23.  Lizneva D, Suturina L, Walker W, Brakta S, Gavrilova-Jordan L, Azziz R 2016. Criteria, prevalence, and phenotypes of polycystic ovary syndrome. Fertil. Steril. 106:6–15
    [Google Scholar]
24. 24.  Veiga-Lopez A, Steckler TL, Abbott DH, Welch KB, MohanKumar PS et al. 2011. Developmental programming: impact of excess prenatal testosterone on intrauterine fetal endocrine milieu and growth in sheep. Biol. Reprod. 84:87–96
    [Google Scholar]
25. 25.  Abi Salloum B, Veiga-Lopez A, Abbott DH, Burant CF, Padmanabhan V 2015. Developmental programming: Exposure to testosterone excess disrupts steroidal and metabolic environment in pregnant sheep. Endocrinology 156:2323–37
    [Google Scholar]
26. 26.  Beck-Peccoz P, Padmanabhan V, Baggiani AM, Cortelazzi D, Buscaglia M et al. 1991. Maturation of hypothalamic-pituitary-gonadal function in normal human fetuses: circulating levels of gonadotropins, their common α-subunit and free testosterone, and discrepancy between immunological and biological activities of circulating follicle-stimulating hormone. J. Clin. Endocrinol. Metabol. 73:525–32
    [Google Scholar]
27. 27.  Morton G, Cummings D, Baskin D, Barsh G, Schwartz M 2006. Central nervous system control of food intake and body weight. Nature 443:289–95
    [Google Scholar]
28. 28.  Livingstone C, Collison M 2002. Sex steroids and insulin resistance. Clin. Sci. 102:151–66
    [Google Scholar]
29. 29.  Polderman KH, Gooren L, Asscheman H, Bakker A, Heine RJ 1994. Induction of insulin resistance by androgens and estrogens. J. Clin. Endocrinol. Metabol. 79:265–71
    [Google Scholar]
30. 30.  Crespi EJ, Steckler TL, Mohankumar PS, Padmanabhan V 2006. Prenatal exposure to excess testosterone modifies the developmental trajectory of the insulin-like growth factor system in female sheep. J. Physiol. 572:119–30
    [Google Scholar]
31. 31.  Steckler T, Wang J, Bartol FF, Roy SK, Padmanabhan V 2005. Fetal programming: Prenatal testosterone treatment causes intrauterine growth retardation, reduces ovarian reserve and increases ovarian follicular recruitment. Endocrinology 146:3185–93
    [Google Scholar]
32. 32.  Manikkam M, Crespi EJ, Doop DD, Herkimer C, Lee JS et al. 2004. Fetal programming: Prenatal testosterone excess leads to fetal growth retardation and postnatal catch-up growth in sheep. Endocrinology 145:790–98
    [Google Scholar]
33. 33.  Myatt L 2006. Placental adaptive responses and fetal programming. J. Physiol. 572:25–30
    [Google Scholar]
34. 34.  Braun T, Challis JR, Newnham JP, Sloboda DM 2013. Early-life glucocorticoid exposure: the hypothalamic-pituitary-adrenal axis, placental function, and long-term disease risk. Endocr. Rev. 34:885–916
    [Google Scholar]
35. 35.  Beckett EM, Astapova O, Steckler TL, Veiga-Lopez A, Padmanabhan V 2014. Developmental programing: impact of testosterone on placental differentiation. Reproduction 148:199–209
    [Google Scholar]
36. 36.  Recabarren SE, Padmanabhan V, Codner E, Lobos A, Durán C et al. 2005. Postnatal developmental consequences of altered insulin sensitivity in female sheep treated prenatally with testosterone. Am. J. Physiol. Endocrinol. Metabol 289:E801–6
    [Google Scholar]
37. 37.  Padmanabhan V, Veiga-Lopez A, Abbott D, Recabarren S, Herkimer C 2010. 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 151:595–605
    [Google Scholar]
38. 38.  Handa RJ, Pak TR, Kudwa AE, Lund TD, Hinds L 2008. An alternate pathway for androgen regulation of brain function: activation of estrogen receptor beta by the metabolite of dihydrotestosterone, 5α-androstane-3β, 17β-diol. Horm. Behav. 53:741–52
    [Google Scholar]
39. 39.  Cardoso RC, Veiga-Lopez A, Moeller J, Beckett E, Pease A et al. 2015. Developmental programming: impact of gestational steroid and metabolic milieus on adiposity and insulin sensitivity in prenatal testosterone-treated female sheep. Endocrinology 157:522–35
    [Google Scholar]
40. 40.  Veiga-Lopez A, Moeller J, Patel D, Ye W, Pease A et al. 2013. Developmental programming: impact of prenatal testosterone excess on insulin sensitivity, adiposity, and free fatty acid profile in postpubertal female sheep. Endocrinology 154:1731–42
    [Google Scholar]
41. 41.  Lu C, Cardoso RC, Puttabyatappa M, Padmanabhan V 2016. Developmental programming: prenatal testosterone excess and insulin signaling disruptions in female sheep. Biol. Reprod. 94:113
    [Google Scholar]
42. 42.  Nada SE, Thompson RC, Padmanabhan V 2010. Developmental programming: differential effects of prenatal testosterone excess on insulin target tissues. Endocrinology 151:5165–73
    [Google Scholar]
43. 43.  Dunaif A, Wu X, Lee A, Diamanti-Kandarakis E 2001. Defects in insulin receptor signaling in vivo in the polycystic ovary syndrome (PCOS). Am. J. Physiol. Endocrinol. Metab. 281:E392–99
    [Google Scholar]
44. 44.  Corbould A, Kim YB, Youngren JF, Pender C, Kahn BB et al. 2005. Insulin resistance in the skeletal muscle of women with PCOS involves intrinsic and acquired defects in insulin signaling. Am. J. Physiol. Endocrinol. Metab. 288:E1047–54
    [Google Scholar]
45. 45.  Hojlund K, Glintborg D, Andersen NR, Birk JB, Treebak JT et al. 2008. Impaired insulin-stimulated phosphorylation of Akt and AS160 in skeletal muscle of women with polycystic ovary syndrome is reversed by pioglitazone treatment. Diabetes 57:357–66
    [Google Scholar]
46. 46.  Puttabyatappa M, Andriessen V, Mesquitta M, Zeng L, Pennathur S, Padmanabhan V 2017. Developmental programming: impact of gestational steroid and metabolic milieus on mediators of insulin sensitivity in prenatal testosterone–treated female sheep. Endocrinology 158:2783–98
    [Google Scholar]
47. 47.  Sheppard KM, Padmanabhan V, Coolen LM, Lehman MN 2011. Prenatal programming by testosterone of hypothalamic metabolic control neurones in the ewe. J. Neuroendocrinol. 23:401–11
    [Google Scholar]
48. 48.  Varela L, Horvath TL 2012. Leptin and insulin pathways in POMC and AgRP neurons that modulate energy balance and glucose homeostasis. EMBO Rep 13:1079–86
    [Google Scholar]
49. 49.  Weyer C, Foley J, Bogardus C, Tataranni P, Pratley R 2000. Enlarged subcutaneous abdominal adipocyte size, but not obesity itself, predicts type II diabetes independent of insulin resistance. Diabetologia 43:1498–506
    [Google Scholar]
50. 50.  Salans LB, Knittle JL, Hirsch J 1968. The role of adipose cell size and adipose tissue insulin sensitivity in the carbohydrate intolerance of human obesity. J. Clin. Investig. 47:153–65
    [Google Scholar]
51. 51.  McLaughlin T, Deng A, Yee G, Lamendola C, Reaven G et al. 2010. Inflammation in subcutaneous adipose tissue: relationship to adipose cell size. Diabetologia 53:369–77
    [Google Scholar]
52. 52.  McLaughlin T, Sherman A, Tsao P, Gonzalez O, Yee G et al. 2007. Enhanced proportion of small adipose cells in insulin-resistant versus insulin-sensitive obese individuals implicates impaired adipogenesis. Diabetologia 50:1707–15
    [Google Scholar]
53. 53.  Müller G 2011. Let's shift lipid burden—from large to small adipocytes. Eur. J. Pharmacol. 656:1–4
    [Google Scholar]
54. 54.  Virtue S, Vidal-Puig A 2010. Adipose tissue expandability, lipotoxicity and the metabolic syndrome—an allostatic perspective. Biochim. Biophys. Acta 1801:338–49
    [Google Scholar]
55. 55.  Lee Y-H, Pratley RE 2005. The evolving role of inflammation in obesity and the metabolic syndrome. Curr. Diabetes Rep. 5:70–75
    [Google Scholar]
56. 56.  Sørensen TI, Virtue S, Vidal-Puig A 2010. Obesity as a clinical and public health problem: Is there a need for a new definition based on lipotoxicity effects?. Biochim. Biophys. Acta 1801:400–4
    [Google Scholar]
57. 57.  King AJ, Olivier NB, MohanKumar PS, Lee JS, Padmanabhan V, Fink GD 2007. Hypertension caused by prenatal testosterone excess in female sheep. Am. J. Physiol. Endocrinol. Metabol. 292:E1837–E41
    [Google Scholar]
58. 58.  Vyas AK, Hoang V, Padmanabhan V, Gilbreath E, Mietelka KA 2016. Prenatal programming: adverse cardiac programming by gestational testosterone excess. Sci. Rep. 6:28335
    [Google Scholar]
59. 59.  Malcolm KD, Jackson LM, Bergeon C, Lee TM, Padmanabhan V, Foster DL 2006. Long-term exposure of female sheep to physiologic concentrations of estradiol: effects on the onset and maintenance of reproductive function, pregnancy, and social development in female offspring. Biol. Reprod. 75:844–52
    [Google Scholar]
60. 60.  Puttabyatappa M, Cardoso RC, Herkimer C, Veiga-Lopez A, Padmanabhan V 2016. Developmental programming: postnatal estradiol modulation of prenatally organized reproductive neuroendocrine function in sheep. Reproduction 152:139–50
    [Google Scholar]
61. 61.  Lea-Currie YR, Monroe D, Mcintosh MK 1999. Dehydroepiandrosterone and related steroids alter 3T3-L1 preadipocyte proliferation and differentiation. Comp. Biochem. Physiol. C 123:17–25
    [Google Scholar]
62. 62.  Cooke PS, Naaz A 2004. Role of estrogens in adipocyte development and function. Exp. Biol. Med. 229:1127–35
    [Google Scholar]
63. 63.  Jellyman J, Valenzuela O, Fowden A 2015. Horse species symposium: glucocorticoid programming of hypothalamic-pituitary-adrenal axis and metabolic function: animal studies from mouse to horse. J. Anim. Sci. 93:3245–60
    [Google Scholar]
64. 64.  Fowden AL, Giussani DA, Forhead AJ 2006. Intrauterine programming of physiological systems: causes and consequences. Physiology 21:29–37
    [Google Scholar]
65. 65.  Fowden AL, Forhead AJ 2009. Hormones as epigenetic signals in developmental programming. Exp. Physiol. 94:607–25
    [Google Scholar]
66. 66.  Moisiadis VG, Matthews SG 2014. Glucocorticoids and fetal programming part 1: outcomes. Nat. Rev. Endocrinol. 10:391–402
    [Google Scholar]
67. 67.  Cottrell EC, Seckl J 2009. Prenatal stress, glucocorticoids and the programming of adult disease. Front. Behav. Neurosci. 3:19
    [Google Scholar]
68. 68.  Maccari S, Darnaudery M, Morley-Fletcher S, Zuena A, Cinque C, Van Reeth O 2003. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci. Biobehav. Rev. 27:119–27
    [Google Scholar]
69. 69.  Harris A, Seckl J 2011. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 59:279–89
    [Google Scholar]
70. 70.  Fowden AL, Valenzuela O, Vaughan O, Jellyman J, Forhead AJ 2016. Glucocorticoid programming of intrauterine development. Domest. Anim. Endocrinol. 56:S121–S32
    [Google Scholar]
71. 71.  Moisiadis VG, Matthews SG 2014. Glucocorticoids and fetal programming part 2: mechanisms. Nat. Rev. Endocrinol. 10:403–11
    [Google Scholar]
72. 72.  Seckl JR 2004. Prenatal glucocorticoids and long-term programming. Eur. J. Endocrinol. 151:U49–U62
    [Google Scholar]
73. 73.  Jensen E, Gallaher B, Breier B, Harding J 2002. The effect of a chronic maternal cortisol infusion on the late-gestation fetal sheep. J. Endocrinol. 174:27–36
    [Google Scholar]
74. 74.  Fowden A, Szemere J, Hughes P, Gilmour R, Forhead A 1996. The effects of cortisol on the growth rate of the sheep fetus during late gestation. J. Endocrinol. 151:97–105
    [Google Scholar]
75. 75.  Kutzler MA, Ruane EK, Coksaygan T, Vincent SE, Nathanielsz PW 2004. Effects of three courses of maternally administered dexamethasone at 0.7, 0.75, and 0.8 of gestation on prenatal and postnatal growth in sheep. Pediatrics 113:313–19
    [Google Scholar]
76. 76.  Newnham JP, Evans SF, Godfrey M, Huang W, Ikegami M, Jobe A 1999. Maternal, but not fetal, administration of corticosteroids restricts fetal growth. J. Matern. Fetal Med. 8:81–87
    [Google Scholar]
77. 77.  Fowden AL, Forhead AJ, Sferruzzi-Perri AN, Burton GJ, Vaughan OR 2015. Endocrine regulation of placental phenotype. Placenta 36:S50–S59
    [Google Scholar]
78. 78.  Braun T, Meng W, Shang H, Li S, Sloboda DM et al. 2015. Early dexamethasone treatment induces placental apoptosis in sheep. Reprod. Sci. 22:47–59
    [Google Scholar]
79. 79.  Ward J, Forhead A, Wooding F, Fowden A 2006. Functional significance and cortisol dependence of the gross morphology of ovine placentomes during late gestation. Biol. Reprod. 74:137–45
    [Google Scholar]
80. 80.  Braun T, Li S, Moss TJ, Newnham JP, Challis JR et al. 2007. Maternal betamethasone administration reduces binucleate cell number and placental lactogen in sheep. J. Endocrinol. 194:337–47
    [Google Scholar]
81. 81.  De Blasio MJ, Dodic M, Jefferies AJ, Moritz KM, Wintour EM, Owens JA 2007. Maternal exposure to dexamethasone or cortisol in early pregnancy differentially alters insulin secretion and glucose homeostasis in adult male sheep offspring. Am. J. Physiol. Endocrinol. Metabol. 293:E75–E82
    [Google Scholar]
82. 82.  Roghair RD, Miller FJ Jr, Scholz TD, Lamb FS, Segar JL 2008. Endothelial superoxide production is altered in sheep programmed by early gestation dexamethasone exposure. Neonatology 93:19–27
    [Google Scholar]
83. 83.  Sloboda D, Moss T, Gurrin L, Newnham J 2002. The effect of prenatal betamethasone administration on postnatal ovine hypothalamic-pituitary-adrenal function. J. Endocrinol. 172:71–81
    [Google Scholar]
84. 84.  Sloboda DM, Moss TJ, Li S, Doherty DA, Nitsos I et al. 2005. Hepatic glucose regulation and metabolism in adult sheep: effects of prenatal betamethasone. Am. J. Physiol. Endocrinol. Metabol. 289:E721–E28
    [Google Scholar]
85. 85.  Moss TJ, Sloboda DM, Gurrin LC, Harding R, Challis JR, Newnham JP 2001. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R960–R70
    [Google Scholar]
86. 86.  Long NM, Smith DT, Ford SP, Nathanielsz PW 2013. Elevated glucocorticoids during ovine pregnancy increase appetite and produce glucose dysregulation and adiposity in their granddaughters in response to ad libitum feeding at 1 year of age. Am. J. Obstet. Gynecol. 209:353.e1–53.e9
    [Google Scholar]
87. 87.  Sloboda D, Newnham J 2000. Effects of repeated maternal betamethasone administration on growth and hypothalamic-pituitary-adrenal function of the ovine fetus at term. J. Endocrinol. 165:79–91
    [Google Scholar]
88. 88.  Rakers F, Frauendorf V, Rupprecht S, Schiffner R, Bischoff SJ et al. 2013. Effects of early- and late-gestational maternal stress and synthetic glucocorticoid on development of the fetal hypothalamus–pituitary–adrenal axis in sheep. Stress 16:122–29
    [Google Scholar]
89. 89.  Long NM, Ford SP, Nathanielsz PW 2013. Multigenerational effects of fetal dexamethasone exposure on the hypothalamic–pituitary–adrenal axis of first- and second-generation female offspring. Am. J. Obstet. Gynecol. 208:217.e1–17.e8
    [Google Scholar]
90. 90.  Huang W, Beazley L, Quinlivan J, Evans S, Newnham J, Dunlop S 1999. Effect of corticosteroids on brain growth in fetal sheep. Obstet. Gynecol. 94:213–18
    [Google Scholar]
91. 91.  Li S, Moss T, Nitsos I, Matthews S, Challis J et al. 2013. The impact of maternal synthetic glucocorticoid administration in late pregnancy on fetal and early neonatal hypothalamic–pituitary–adrenal axes regulatory genes is dependent upon dose and gestational age at exposure. J. Dev. Orig. Health Dis. 4:77–89
    [Google Scholar]
92. 92.  Andrews RC, Walker BR 1999. Glucocorticoids and insulin resistance: old hormones, new targets. Clin. Sci. 96:513–23
    [Google Scholar]
93. 93.  Berry MJ, Jaquiery AL, Oliver MH, Harding JE, Bloomfield FH 2013. Antenatal corticosteroid exposure at term increases adult adiposity: an experimental study in sheep. Acta Obstet. Gynecol. Scand. 92:862–65
    [Google Scholar]
94. 94.  Whorwood C, Firth K, Budge H, Symonds M 2001. Maternal undernutrition during early to mid-gestation programs tissue-specific alterations in the expression of the glucocorticoid receptor, 11β-hydroxysteroid dehydrogenase isoforms, and type 1 angiotensin II receptor in neonatal sheep. Endocrinology 142:2854–64
    [Google Scholar]
95. 95.  Reynolds RM 2010. Corticosteroid-mediated programming and the pathogenesis of obesity and diabetes. J. Steroid Biochem. Mol. Biol. 122:3–9
    [Google Scholar]
96. 96.  Moritz KM, De Matteo R, Dodic M, Jefferies AJ, Arena D et al. 2011. Prenatal glucocorticoid exposure in the sheep alters renal development in utero: implications for adult renal function and blood pressure control. Am. J. Physiol. Regul. Integr. Comp. Physiol. 301:R500–9
    [Google Scholar]
97. 97.  Wintour E, Moritz K, Johnson K, Ricardo S, Samuel C, Dodic M 2003. Reduced nephron number in adult sheep, hypertensive as a result of prenatal glucocorticoid treatment. J. Physiol. 549:929–35
    [Google Scholar]
98. 98.  Casals-Casas C, Desvergne B 2011. Endocrine disruptors: from endocrine to metabolic disruption. Annu. Rev. Physiol. 73:135–62
    [Google Scholar]
99. 99.  Gore A, Chappell V, Fenton S, Flaws J, Nadal A et al. 2015. Executive summary to EDC-2: the Endocrine Society's second scientific statement on endocrine-disrupting chemicals. Endocr. Rev. 36:593–602
    [Google Scholar]
100. 100.  Padmanabhan V, Veiga-Lopez A 2014. Reproduction symposium: developmental programming of reproductive and metabolic health. J. Anim. Sci. 92:3199–210
     [Google Scholar]
101. 101.  Vandenberg LN, Maffini MV, Sonnenschein C, Rubin BS, Soto AM 2009. Bisphenol-A and the great divide: a review of controversies in the field of endocrine disruption. Endocr. Rev. 30:75–95
     [Google Scholar]
102. 102.  Ranjit N, Siefert K, Padmanabhan V 2010. Bisphenol-A and disparities in birth outcomes: a review and directions for future research. J. Perinatol. 30:2–9
     [Google Scholar]
103. 103.  Nadal A 2013. Obesity: Fat from plastics? Linking bisphenol A exposure and obesity. Nat. Rev. Endocrinol. 9:9–10
     [Google Scholar]
104. 104.  Savabieasfahani M, Kannan K, Astapova O, Evans NP, Padmanabhan V 2006. Developmental programming: differential effects of prenatal exposure to bisphenol-A or methoxychlor on reproductive function. Endocrinology 147:5956–66
     [Google Scholar]
105. 105.  Veiga-Lopez A, Moeller J, Sreedharan R, Singer K, Lumeng C et al. 2015. Developmental programming: interaction between prenatal BPA exposure and postnatal adiposity on metabolic variables in female sheep. Am. J. Physiol. Endocrinol. Metabol. 310:E238–E47
     [Google Scholar]
106. 106.  Puttabyatappa M, Cardoso RC, Padmanabhan V 2016. Effect of maternal PCOS and PCOS-like phenotype on the offspring's health. Mol. Cell. Endocrinol. 435:29–39
     [Google Scholar]
107. 107.  Prins GS, Birch L, Tang W-Y, Ho S-M 2007. Developmental estrogen exposures predispose to prostate carcinogenesis with aging. Reprod. Toxicol 23:374–82
     [Google Scholar]
108. 108.  Despres J 1993. Abdominal obesity as important component of insulin-resistance syndrome. Nutrition 9:452–59
     [Google Scholar]
109. 109.  Veiga-Lopez A, Pennathur S, Kannan K, Patisaul HB, Dolinoy DC et al. 2015. Impact of gestational bisphenol A on oxidative stress and free fatty acids: human association and interspecies animal testing studies. Endocrinology 156:911–22
     [Google Scholar]
110. 110.  Ceriello A, Motz E 2004. Is oxidative stress the pathogenic mechanism underlying insulin resistance, diabetes, and cardiovascular disease? The common soil hypothesis revisited. Arterioscler. Thromb. Vasc. Biol. 24:816–23
     [Google Scholar]
111. 111.  Nunez A, Kannan K, Giesy J, Fang J, Clemens L 2001. Effects of bisphenol A on energy balance and accumulation in brown adipose tissue in rats. Chemosphere 42:917–22
     [Google Scholar]
112. 112.  MohanKumar SM, Rajendran TD, Vyas AK, Hoang V, Asirvatham-Jeyaraj N et al. 2017. Effects of prenatal bisphenol-A exposure and postnatal overfeeding on cardiovascular function in female sheep. J. Dev. Orig. Health Dis. 8:65–74
     [Google Scholar]
113. 113.  Koneva L, Vyas A, McEachin R, Puttabyatappa M, Wang HS et al. 2017. Developmental programming: interaction between prenatal BPA and postnatal overfeeding on cardiac tissue gene expression in female sheep. Environ. Mol. Mutagen. 58:4–18
     [Google Scholar]
114. 114.  Liao C, Kannan K 2013. Concentrations and profiles of bisphenol A and other bisphenol analogues in foodstuffs from the United States and their implications for human exposure. J. Agric. Food Chem. 61:4655–62
     [Google Scholar]
115. 115.  Rochester JR, Bolden AL 2015. Bisphenol S and F: a systematic review and comparison of the hormonal activity of bisphenol A substitutes. Environ. Health Perspect. 123:643–50
     [Google Scholar]
116. 116.  Liao C, Liu F, Alomirah H, Loi VD, Mohd MA et al. 2012. Bisphenol S in urine from the United States and seven Asian countries: occurrence and human exposures. Environ. Sci. Technol. 46:6860–66
     [Google Scholar]
117. 117.  Ye X, Wong L-Y, Kramer J, Zhou X, Jia T, Calafat AM 2015. Urinary concentrations of bisphenol A and three other bisphenols in convenience samples of US adults during 2000–2014. Environ. Sci. Technol. 49:11834–39
     [Google Scholar]
118. 118.  Liu J, Li J, Wu Y, Zhao Y, Luo F et al. 2017. Bisphenol A metabolites and bisphenol S in paired maternal and cord serum. Environ. Sci. Technol. 51:2456–63
     [Google Scholar]
119. 119.  Gingrich J, Pu Y, Roberts J, Karthikraj R, Kannan K et al. 2018. Gestational bisphenol S impairs placental endocrine function and the fusogenic trophoblast signaling pathway. Arch. Toxicol. 92:1861–76
     [Google Scholar]
120. 120.  Wallace RM, Pohler KG, Smith MF, Green JA 2015. Placental PAGs: gene origins, expression patterns, and use as markers of pregnancy. Reproduction 149:R115–R26
     [Google Scholar]
121. 121.  Pu Y, Gingrich JD, Steibel JP, Veiga-Lopez A 2017. Sex-specific modulation of fetal adipogenesis by gestational bisphenol A and bisphenol S exposure. Endocrinology 158:3844–58
     [Google Scholar]
122. 122.  Howard P, Michalenko E, Jarvis W, Basu D, Sage G et al. 1991. Handbook of Environmental Fate and Exposure Data for Organic Chemicals, Vol. 2: Solvents Boca Raton, FL: CRC Press
     [Google Scholar]
123. 123.  Oropeza-Hernández LF, López-Romero R, Albores A 2003. Hepatic CYP1A, 2B, 2C, 2E and 3A regulation by methoxychlor in male and female rats. Toxicol. Lett. 144:93–103
     [Google Scholar]
124. 124.  Hiort O 2013. The differential role of androgens in early human sex development. BMC Med 11:152
     [Google Scholar]
125. 125.  Forhead AJ, Fowden AL 2009. The hungry fetus? Role of leptin as a nutritional signal before birth. J. Physiol. 587:1145–52
     [Google Scholar]
126. 126.  Wood CE 2014. Estrogen in the fetus. Advances in Fetal and Neonatal Physiology L Zhang, CA Ducsay 217–28 New York: Springer
     [Google Scholar]
127. 127.  Bondesson M, Hao R, Lin C-Y, Williams C, Gustafsson J-Å 2015. Estrogen receptor signaling during vertebrate development. Biochim. Biophys. Acta 1849:142–51
     [Google Scholar]
128. 128.  Seckl JR, Holmes MC 2007. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal “programming” of adult pathophysiology. Nat. Rev. Endocrinol. 3:479–88
     [Google Scholar]
129. 129.  Bispham J, Gopalakrishnan G, Dandrea J, Wilson V, Budge H et al. 2003. Maternal endocrine adaptation throughout pregnancy to nutritional manipulation: consequences for maternal plasma leptin and cortisol and the programming of fetal adipose tissue development. Endocrinology 144:3575–85
     [Google Scholar]
130. 130.  Whyte J, Alexenko A, Davis A, Ellersieck M, Fountain E, Rosenfeld C 2007. Maternal diet composition alters serum steroid and free fatty acid concentrations and vaginal pH in mice. J. Endocrinol. 192:75–81
     [Google Scholar]
131. 131.  Takahashi LK, Turner JG, Kalin NH 1998. Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies. Psychoneuroendocrinology 23:571–81
     [Google Scholar]
132. 132.  Barrett ES, Swan SH 2015. Stress and androgen activity during fetal development. Endocrinology 156:3435–41
     [Google Scholar]
133. 133.  Godfrey KM, Lillycrop KA, Burdge GC, Gluckman PD, Hanson MA 2007. Epigenetic mechanisms and the mismatch concept of the developmental origins of health and disease. Pediatr. Res. 61:5R–10R
     [Google Scholar]
134. 134.  Vickers MH, Sloboda DM 2012. Strategies for reversing the effects of metabolic disorders induced as a consequence of developmental programming. Front. Physiol. 3:242
     [Google Scholar]
135. 135.  Jirtle RL, Skinner MK 2007. Environmental epigenomics and disease susceptibility. Nat. Rev. Genet. 8:253–62
     [Google Scholar]
136. 136.  Thomassin H, Flavin M, Espinás ML, Grange T 2001. Glucocorticoid‐induced DNA demethylation and gene memory during development. EMBO J 20:1974–83
     [Google Scholar]
137. 137.  Crudo A, Petropoulos S, Moisiadis VG, Iqbal M, Kostaki A et al. 2012. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology 153:3269–83
     [Google Scholar]
138. 138.  Petropoulos S, Matthews SG, Szyf M 2014. Adult glucocorticoid exposure leads to transcriptional and DNA methylation changes in nuclear steroid receptors in the hippocampus and kidney of mouse male offspring. Biol. Reprod. 90:43
     [Google Scholar]
139. 139.  Xu N, Kwon S, Abbott DH, Geller DH, Dumesic DA et al. 2011. Epigenetic mechanism underlying the development of polycystic ovary syndrome (PCOS)-like phenotypes in prenatally androgenized rhesus monkeys. PLOS ONE 6:e27286
     [Google Scholar]
140. 140.  Skinner MK, Manikkam M, Guerrero-Bosagna C 2010. Epigenetic transgenerational actions of environmental factors in disease etiology. Trends Endocrinol. Metab. 21:214–22
     [Google Scholar]
141. 141.  Thompson LP, Al-Hasan Y 2012. Impact of oxidative stress in fetal programming. J. Pregnancy 2012:582748
     [Google Scholar]
142. 142.  Mutsaers HA, To R 2012. Dexamethasone enhances oxidative stress-induced cell death in murine neural stem cells. Neurotox. Res. 22:127–37
     [Google Scholar]
143. 143.  Lakshmy R 2013. Metabolic syndrome: role of maternal undernutrition and fetal programming. Rev. Endocr. Metab. Disord. 14:229–40
     [Google Scholar]
144. 144.  Neier K, Marchlewicz EH, Dolinoy DC, Padmanabhan V 2015. Assessing human health risk to endocrine disrupting chemicals: a focus on prenatal exposures and oxidative stress. Endocr. Disrupt. 3:e1069916
     [Google Scholar]
145. 145.  Sen S, Simmons RA 2010. Maternal antioxidant supplementation prevents adiposity in the offspring of Western diet–fed rats. Diabetes 59:3058–65
     [Google Scholar]
146. 146.  Xu N, Chua AK, Jiang H, Liu N-A, Goodarzi MO 2014. Early embryonic androgen exposure induces transgenerational epigenetic and metabolic changes. Mol. Endocrinol. 28:1329–36
     [Google Scholar]
147. 147.  Xin F, Susiarjo M, Bartolomei MS 2015. Multigenerational and transgenerational effects of endocrine disrupting chemicals: A role for altered epigenetic regulation?. Semin. Cell Dev. Biol. 43:66–75
     [Google Scholar]
148. 148.  Walker DM, Gore AC 2011. Transgenerational neuroendocrine disruption of reproduction. Nat. Rev. Endocrinol. 7:197–207
     [Google Scholar]
149. 149.  Ibáñez L, de Zegher F 2003. Low‐dose combination of flutamide, metformin and an oral contraceptive for non‐obese, young women with polycystic ovary syndrome. Hum. Reprod. 18:57–60
     [Google Scholar]