Prenatal stress-immune programming of sex differences in comorbidity of depression and obesity/metabolic syndrome

Dialogues in Clinical Neuroscience

Volumn 18, Issue 4, 2016, Pages 425-436

  Goldstein, Jill M ^a,b   Holsen, Laura ^a,b   Huang, Grace ^a   Hammond, Bradley D ^c,d   James Todd, Tamarra ^a,e   Cherkerzian, Sara ^a,b   Hale, Taben M ^c   Handa, Robert J ^c,d  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^d Department of Ecosystem Science and Sustainability   (United States)

^e HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Depression; Depression cardiometabolic comorbidity; Fetal programming; Inflammation; Obesity metabolic syndrome; Prenatal stress model; Sex difference

Indexed keywords

STEROID HORMONE;

ARTICLE; BRAIN DEVELOPMENT; CAUSE OF DEATH; CELL DIFFERENTIATION; COMORBIDITY; DISEASE ASSOCIATION; FEMALE; FETUS BRAIN; FOOD INTAKE; HUMAN; HYPERTENSION; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; IMPAIRED GLUCOSE TOLERANCE; LIPID STORAGE; MAJOR DEPRESSION; MALE; MATERNAL STRESS; MENTAL PATIENT; METABOLIC SYNDROME X; MORBIDITY; MORTALITY; POSTMENOPAUSE; PREDICTION; PRENATAL STRESS; PREVALENCE; SEX DIFFERENCE; SOCIAL STRESS; DEPRESSIVE DISORDER, MAJOR; GONAD; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; IMMUNOLOGY; MENTAL STRESS; OBESITY; PATHOPHYSIOLOGY; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PREGNANCY; PRENATAL EXPOSURE; SEXUAL DEVELOPMENT;

COMORBIDITY; DEPRESSIVE DISORDER, MAJOR; FEMALE; GONADS; HUMANS; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; MALE; METABOLIC SYNDROME X; OBESITY; PITUITARY-ADRENAL SYSTEM; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; SEX CHARACTERISTICS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 85012986133     PISSN: 12948322     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (158)

1. World Health Organization. Global health estimates 2014 summary tables: YLD by cause, age, and sex, 2000-2012. Available at: http://www. who.int/healthinfo/global_burden_disease/estimates/en/index2.html. Published June 2014. Accessed October 2016.
2. Roberts RE, Deleger S, Strawbridge WJ, Kaplan GA. Prospective association between obesity and depression: evidence from the Alameda County Study. Int J Obes Relat Metab Disord. 2003;27(4):514-521.
3. Yang L, Colditz GA. Prevalence of overweight and obesity in the United States, 2007-2012. JAMA Intern Med. 2015;175(8):1412-1413.
4. Gilman SE, Cherkerzian S, Buka SL, Hahn J, Hornig M, Goldstein JM. Prenatal immune programming of sex-dependent risk for major depression. Transl Psychiatry. 2016;6(5):e822.
5. Goldstein JM, Cherkerzian S, Buka SL, et al. Sex-specific impact of maternal-fetal risk factors on depression and cardiovascular risk 40 years later. J Dev Orig Health Dis. 2011;6(2):353-364.
6. van Os J, Jones P, Lewis G, Wadsworth M, Murray R. Developmental precursors of affective illness in a general population birth cohort. Arch Gen Psychiatry. 1997;54(7):625-631.
7. Salam RA, Das JK, Bhutta ZA. Impact of intrauterine growth restriction on long-term health. Curr Opin Clin Nutr Metab Care. 2014;17(3):249-254.
8. McEwen BS. Gonadal steroid influences on brain development and sexual differentiation. In: Greep R, ed. Reproductive Physiology IV: International Review of Physiology. Vol 27. Baltimore, MD: University Park Press; 1983:99-145.
9. Tobet S, Knoll JG, Hartshorn C, et al. Brain sex differences and hormone influences: a moving experience? J Neuroendocrinol. 2009;21(4):387-392.
10. Giedd JN, Vaituzis AC, Hamburger SD, et al. Quantitative MRI of the temporal lobe, amygdala, and hippocampus in normal human development: ages 4-18 years. J Comp Neurol. 1996;366(2):223-230.
11. Goldstein JM, Seidman LJ, Horton NJ, et al. Normal sexual dimorphism of the adult human brain assessed by in vivo magnetic resonance imaging. Cereb Cortex. 2001;11(6):490-497.
12. Makris N, Swaab DF, van der Kouwe A, et al. Volumetric parcellation methodology of the human hypothalamus in neuroimaging: normative data and sex differences. Neuroimage. 2013;69:1-10.
13. Goldstein JM, Handa RJ, Tobet SA. Disruption of fetal hormonal programming (prenatal stress) implicates shared risk for sex differences in depression and cardiovascular disease. Front Neuroendocrinol. 2014;35(1):140-158.
14. Tobet S, Handa R, Goldstein JM. Sex-dependent pathophysiology as predictors of comorbidity of major depressive disorder and cardiovascular disease. Pflugers Arch. 2013;465(5):585-594.
15. Needham BL, Epel ES, Adler NE, Kiefe C. Trajectories of change in obesity and symptoms of depression: the CARDIA study. Am J Public Health. 2010;100(6):1040-1046.
16. Murphy JM, Horton NJ, Burke JD Jr, et al. Obesity and weight gain in relation to depression: findings from the Stirling County Study. Int J Obes (Lond). 2009;33(3):335-341.
17. Kloiber S, Ising M, Reppermund S, et al. Overweight and obesity affect treatment response in major depression. Biol Psychiatry. 2007;62(4):321-326.
18. Heo M, Pietrobelli A, Fontaine KR, Sirey JA, Faith MS. Depressive mood and obesity in US adults: comparison and moderation by sex, age, and race. Int J Obes (Lond). 2006;30(3):513-519.
19. Hasler G, Pine DS, Kleinbaum DG, et al. Depressive symptoms during childhood and adult obesity: the Zurich Cohort Study. Mol Psychiatry. 2005;10(9):842-850.
20. Mozaffarian D, Benjamin EJ, Go AS, et al. Heart disease and stroke statistics-2015 update: a report from the American Heart Association. Circulation. 2015;131(4):e29-322.
21. DeFronzo RA, Ferrannini E. Insulin resistance. A multifaceted syndrome responsible for NIDDM, obesity, hypertension, dyslipidemia, and atherosclerotic cardiovascular disease. Diabetes Care. 1991;14(3):173-194.
22. James-Todd TM, Huang T, Seely EW, Saxena AR. The association between phthalates and metabolic syndrome: the National Health and Nutrition Examination Survey 2001-2010. Environ Health. 2016;15:52.
23. Beltran-Sanchez H, Harhay MO, Harhay MM, McElligott S. Prevalence and trends of metabolic syndrome in the adult U.S. population, 1999-2010. J Am Coll Cardiol. 2013;62(8):697-703.
24. Bose M, Olivan B, Laferrere B. Stress and obesity: the role of the hypothalamic-pituitary-adrenal axis in metabolic disease. Curr Opin Endocrinol Diabetes Obes. 2009;16(5):340-346.
25. Vicennati V, Ceroni L, Genghini S, Patton L, Pagotto U, Pasquali R. Sex difference in the relationship between the hypothalamic-pituitary-adrenal axis and sex hormones in obesity. Obesity (Silver Spring). 2006;14(2):235-243.
26. Bujalska IJ, Kumar S, Hewison M, Stewart PM. Differentiation of adipose stromal cells: the roles of glucocorticoids and 11β-hydroxysteroid dehydrogenase. Endocrinology. 1999;140(7):3188-3196.
27. Gelernter-Yaniv L, Feng N, Sebring NG, Hochberg Z, Yanovski JA. Associations between a polymorphism in the 11 beta hydroxysteroid dehydrogenase type I gene and body composition. Int J Obes Relat Metab Disord. 2003;27(8):983-986.
28. Rivera M, Cohen-Woods S, Kapur K, et al. Depressive disorder moderates the effect of the FTO gene on body mass index. Mol Psychiatry. 2012;17(6):604-611.
29. Rask E, Olsson T, Soderberg S, et al. Tissue-specific dysregulation of cortisol metabolism in human obesity. J Clin Endocrinol Metab. 2001;86(3):1418-1421.
30. Mystkowski P, Schwartz MW. Gonadal steroids and energy homeostasis in the leptin era. Nutrition. 2000;16(10):937-946.
31. Vicennati V, Ceroni L, Gagliardi L, Gambineri A, Pasquali R. Comment: response of the hypothalamic-pituitary-adrenocortical axis to high-protein/fat and high-carbohydrate meals in women with different obesity phenotypes. J Clin Endocrinol Metab. 2002;87(8):3984-3988.
32. Benson S, Arck PC, Tan S, et al. Effects of obesity on neuroendocrine, cardiovascular, and immune cell responses to acute psychosocial stress in premenopausal women. Psychoneuroendocrinology. 2009;34(2):181-189.
33. McEwen BS, De Kloet ER, Rostene W. Adrenal steroid receptors and actions in the nervous system. Physiol Rev. 1986;66(4):1121-1188.
34. McClellan KM, Stratton MS, Tobet SA. Roles for gamma-aminobutyric acid in the development of the paraventricular nucleus of the hypothalamus. J Comp Neurol. 2010;518(14):2710-2728.
35. Frahm KA, Schow MJ, Tobet SA. The vasculature within the paraventricular nucleus of the hypothalamus in mice varies as a function of development, subnuclear location, and GABA signaling. Horm Metab Res. 2012;44(8):619-624.
36. Bao AM, Hestiantoro A, Van Someren EJ, Swaab DF, Zhou JN. Colocalization of corticotropin-releasing hormone and oestrogen receptor-a in the paraventricular nucleus of the hypothalamus in mood disorders. Brain. 2005;128(pt 6):1301-1313.
37. Goldstein JM, Jerram M, Abbs B, Whitfield-Gabrieli S, Makris N. Sex differences in stress response circuitry activation dependent on female hormonal cycle. J Neurosci. 2010;30(2):431-438.
38. Jacobs EG, Holsen LM, Lancaster K, et al. 17β-Estradiol differentially regulates stress circuitry activity in healthy and depressed women. Neuropsychopharmacology. 2015;40(3):566-576.
39. De Pergola G, Maldera S, Tartagni M, Pannacciulli N, Loverro G, Giorgino R. Inhibitory effect of obesity on gonadotropin, estradiol, and inhibin B levels in fertile women. Obesity (Silver Spring). 2006;14(11):1954-1960.
40. Fernandez-Real JM, Sanchis D, Ricart W, et al. Plasma oestrone-fatty acid ester levels are correlated with body fat mass in humans. Clin Endocrinol (Oxf). 1999;50(2):253-260.
41. Kruijver FP, Balesar R, Espila AM, Unmehopa UA, Swaab DF. Estrogen receptor-a distribution in the human hypothalamus in relation to sex and endocrine status. J Comp Neurol. 2002;454(2):115-139.
42. Kruijver FP, Balesar R, Espila AM, Unmehopa UA, Swaab DF. Estrogenreceptor-β distribution in the human hypothalamus: similarities and differences with ERα distribution. J Comp Neurol. 2003;466(2):251-277.
43. österlund MK, Gustafsson JA, Keller E, Hurd YL. Estrogen receptor β (ERβ) messenger ribonucleic acid (mRNA) expression within the human forebrain: distinct distribution pattern to ER mRNA. J Clin Endocrinol Metab. 2000;85(10):3840-3846.
44. Osterlund MK, Keller E, Hurd YL. The human forebrain has discrete estrogen receptor α messenger RNA expression: high levels in the amygdaloid complex. Neuroscience. 2000;95(2):333-342.
45. Janssen I, Powell LH, Kazlauskaite R, Dugan SA. Testosterone and visceral fat in midlife women: the Study of Women's Health Across the Nation (SWAN) fat patterning study. Obesity. 2010;18(3):604-610.
46. Derby CA, Zilber S, Brambilla D, Morales KH, McKinlay JB. Body mass index, waist circumference and waist to hip ratio and change in sex steroid hormones: the Massachusetts Male Ageing Study. Clin Endocrinol (Oxf). 2006;65(1):125-131.
47. Eskola PJ, Jokelainen J, Jarvelin MR, et al. Depression and insulin resistance: additional support for the novel heuristic model in perimenopausal depression. Am J Psychiatry. 2015;172(8):796-797.
48. Holsboer F, Gerken A, Stalla GK, Muller OA. Blunted aldosterone and ACTH release after human CRH administration in depressed patients. Am J Psychiatry. 1987;144(2):229-231.
49. Nemeroff CB, Widerlov E, Bissette G, et al. Elevated concentrations of CSF corticotropin-releasing factor-like immunoreactivity in depressed patients. Science. 1984;226(4680):1342-1344.
50. Plotsky PM, Owens MJ, Nemeroff CB. Psychoneuroendocrinology of depression. Hypothalamic-pituitary-adrenal axis. Psychiatr Clin North Am. 1998;21(2):293-307.
51. Raison CL, Miller AH. When not enough is too much: the role of insufficient glucocorticoid signaling in the pathophysiology of stress-related disorders. Am J Psychiatry. 2003;160(9):1554-1565.
52. Goldstein JM, Holsen L, Handa R, Tobet S. Fetal hormonal programming of sex differences in depression: linking women's mental health with sex differences in the brain across the lifespan. Front Neurosci. 2014;8:247.
53. Kelly WF, Checkley SA, Bender DA. Cushing's syndrome, tryptophan and depression. Br J Psychiatry. 1980;136:125-132.
54. Ling MH, Perry PJ, Tsuang MT. Side effects of corticosteroid therapy. Psychiatric aspects. Arch Gen Psychiatry. 1981;38(4):471-477.
55. Young EA, Midgley AR, Carlson NE, Brown MB. Alteration in the hypothalamic-pituitary-ovarian axis in depressed women. Arch Gen Psychiatry. 2000;57(12):1157-1162.
56. Epperson CN, Wisner KL, Yamamoto B. Gonadal steroids in the treatment of mood disorders. Psychosom Med. 1999;61(5):676-697.
57. Payne JL, Palmer JT, Joffe H. A reproductive subtype of depression: conceptualizing models and moving toward etiology. Harv Rev Psychiatry. 2009;17(2):72-86.
58. Harlow BL, Wise LA, Otto MW, Soares CN, Cohen LS. Depression and its influence on reproductive endocrine and menstrual cycle markers associated with perimenopause: the Harvard Study of Moods and Cycles. Arch Gen Psychiatry. 2003;60(1):29-36.
59. Rubinow DR, Schmidt PJ. Androgens, brain, and behavior. Am J Psychiatry. 1996;153(8):974-984.
60. Roca CA, Schmidt PJ, Altemus M, et al. Differential menstrual cycle regulation of hypothalamic-pituitary-adrenal axis in women with premenstrual syndrome and controls. J Clin Endocrinol Metab. 2003;88(7):3057-3063.
61. Angold A, Costello EJ. Puberty and depression. Child Adolesc Psychiatr Clin N Am. 2006;15(4):919-937, ix.
62. Steiner M. Female-specific mood disorders. Clin Obstet Gynecol. 1992;35(3):599-611.
63. Young EA, Kornstein SG, Harvey AT, et al. Influences of hormonebased contraception on depressive symptoms in premenopausal women with major depression. Psychoneuroendocrinology. 2007;32(7):843-853.
64. Brummelte S, Galea LA. Depression during pregnancy and postpartum: contribution of stress and ovarian hormones. Prog Neuropsychopharmacol Biol Psychiatry. 2010;34(5):766-776.
65. Graziottin A, Serafini A. Depression and the menopause: why antidepressants are not enough? Menopause Int. 2009;15(2):76-81.
66. Daly RC, Danaceau MA, Rubinow DR, Schmidt PJ. Concordant restoration of ovarian function and mood in perimenopausal depression. Am J Psychiatry. 2003;160(10):1842-1846.
67. Dougherty D, Rauch SL. Neuroimaging and neurobiological models of depression. Harv Rev Psychiatry. 1997;5(3):138-159.
68. Drevets WC, Price JL, Bardgett ME, Reich T, Todd RD, Raichle ME. Glucose metabolism in the amygdala in depression: relationship to diagnostic subtype and plasma cortisol levels. Pharmacol Biochem Behav. 2002;71(3):431-447.
69. Mayberg HS. Limbic-cortical dysregulation: a proposed model of depression. J Neuropsychiatry Clin Neurosci. 1997;9(3):471-481.
70. Sheline YI, Mittler BL, Mintun MA. The hippocampus and depression. Eur Psychiatry. 2002;17(suppl 3):300-305.
71. Handa RJ, Burgess LH, Kerr JE, O'Keefe JA. Gonadal steroid hormone receptors and sex differences in the hypothalamo-pituitary-adrenal axis. Horm Behav. 1994;28(4):464-476.
72. Kawata M. Roles of steroid hormones and their receptors in structural organization in the nervous system. Neurosci Res. 1995;24(1):1-46.
73. Ostlund H, Keller E, Hurd YL. Estrogen receptor gene expression in relation to neuropsychiatric disorders. Ann N Y Acad Sci. 2003;1007:54-63.
74. Koolschijn PC, van Haren NE, Lensvelt-Mulders GJ, Hulshoff Pol HE, Kahn RS. Brain volume abnormalities in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Hum Brain Mapp. 2009;30(11):3719-3735.
75. Schmaal L, Hibar DP, Samann PG, et al. Cortical abnormalities in adults and adolescents with major depression based on brain scans from 20 cohorts worldwide in the ENIGMA Major Depressive Disorder Working Group. Mol Psychiatry. 2016 May 3. Epub ahead of print. doi:10.1038/mp.2016.60.
76. Arnone D, Job D, Selvaraj S, et al. Computational meta-analysis of statistical parametric maps in major depression. Hum Brain Mapp. 2016;37(4):1393-1404.
77. Campbell S, Marriott M, Nahmias C, MacQueen GM. Lower hippocampal volume in patients suffering from depression: a meta-analysis. Am J Psychiatry. 2004;161(4):598-607.
78. Hamilton JP, Siemer M, Gotlib IH. Amygdala volume in major depressive disorder: a meta-analysis of magnetic resonance imaging studies. Mol Psychiatry. 2008;13(11):993-1000.
79. Cole J, Costafreda SG, McGuffin P, Fu CH. Hippocampal atrophy in first episode depression: a meta-analysis of magnetic resonance imaging studies. J Affect Disord. 2011;134(1-3):483-487.
80. Kempton MJ, Salvador Z, Munafo MR, et al. Structural neuroimaging studies in major depressive disorder. Meta-analysis and comparison with bipolar disorder. Arch Gen Psychiatry. 2011;68(7):675-690.
81. McKinnon MC, Yucel K, Nazarov A, MacQueen GM. A meta-analysis examining clinical predictors of hippocampal volume in patients with major depressive disorder. J Psychiatry Neurosci. 2009;34(1):41-54.
82. Videbech P, Ravnkilde B. Hippocampal volume and depression: a meta-analysis of MRI studies. Am J Psychiatry. 2004;161(11):1957-1966.
83. Saper CB, Chou TC, Elmquist JK. The need to feed: homeostatic and hedonic control of eating. Neuron. 2002;36(2):199-211.
84. Cummings DE, Purnell JQ, Frayo RS, Schmidova K, Wisse BE, Weigle DS. A preprandial rise in plasma ghrelin levels suggests a role in meal initiation in humans. Diabetes. 2001;50(8):1714-1719.
85. Nakazato M, Murakami N, Date Y, et al. A role for ghrelin in the central regulation of feeding. Nature. 2001;409(6817):194-198.
86. Malik S, McGlone F, Bedrossian D, Dagher A. Ghrelin modulates brain activity in areas that control appetitive behavior. Cell Metab. 2008;7(5):400-409.
87. Soriano-Guillén L, Ortega L, Navarro P, Riestra P, Gavela-Pérez T, Garcés C. Sex-related differences in the association of ghrelin levels with obesity in adolescents. Clin Chem Lab Med. 2016;54(8):1371-1376.
88. Karim R, Stanczyk FZ, Brinton RD, Rettberg J, Hodis HN, Mack WJ. Association of endogenous sex hormones with adipokines and ghrelin in postmenopausal women. J Clin Endocrinol Metab. 2014;100(2):508-515.
89. Barim AO, Aydin S, Colak R, Dag E, Deniz O, Sahin I. Ghrelin, paraoxonase and arylesterase levels in depressive patients before and after citalopram treatment. Clin Biochem. 2009;42(10-11):1076-1081.
90. Kluge M, Schussler P, Schmid D, et al. Ghrelin plasma levels are not altered in major depression. Neuropsychobiology. 2009;59(4):199-204.
91. Ahmed ML, Ong KK, Morrell DJ, et al. Longitudinal study of leptin concentrations during puberty: sex differences and relationship to changes in body composition. J Clin Endocrinol Metab. 1999;84(3):899-905.
92. Saad MF, Damani S, Gingerich RL, et al. Sexual dimorphism in plasma leptin concentration. J Clin Endocrinol Metab. 1997;82(2):579-584.
93. Garza JC, Guo M, Zhang W, Lu XY. Leptin increases adult hippocampal neurogenesis in vivo and in vitro. J Biol Chem. 2008;283(26):18238-18247.
94. Korbonits M, Trainer PJ, Little JA, et al. Leptin levels do not change acutely with food administration in normal or obese subjects, but are negatively correlated with pituitary-adrenal activity. Clin Endocrinol (Oxf). 1997;46(6):751-757.
95. Hryhorczuk C, Sharma S, Fulton SE. Metabolic disturbances connecting obesity and depression. Front Neurosci. 2013;7:177.
96. Briana DD, Malamitsi-Puchner A. The role of adipocytokines in fetal growth. Ann N Y Acad Sci. 2010;1205:82-87.
97. Zhu W, Cheng KK, Vanhoutte PM, Lam KS, Xu A. Vascular effects of adiponectin: molecular mechanisms and potential therapeutic intervention. Clin Sci (Lond). 2008;114(5):361-374.
98. Boyne MS, Bennett NR, Cooper RS, et al. Sex-differences in adiponectin levels and body fat distribution: longitudinal observations in Afro-Jamaicans. Diabetes Res Clin Pract. 2010;90(2):e33-e36.
99. Donahue RP, Rejman K, Rafalson LB, Dmochowski J, Stranges S, Trevisan M. Sex differences in endothelial function markers before conversion to pre-diabetes: does the clock start ticking earlier among women? The Western New York Study. Diabetes Care. 2007;30(2):354-359.
100. Liu J, Guo M, Zhang D, et al. Adiponectin is critical in determining susceptibility to depressive behaviors and has antidepressant-like activity. Proc Natl Acad Sci U S A. 2012;109(30):12248-12253.
101. Ravelli AC, van der Meulen JH, Michels RP, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998;351(9097):173-177.
102. Haggerty CL, Ferrell RE, Hubel CA, Markovic N, Harger G, Ness RB. Association between allelic variants in cytokine genes and preeclampsia. Am J Obstet Gynecol. 2005;193(1):209-215.
103. Sanchez SE, Zhang C, Williams MA, et al. Tumor necrosis factor-a soluble receptor p55 (sSex Difp55) and risk of preeclampsia in Peruvian women. J Reprod Immunol. 2000;47(1):49-63.
104. Naghavi M, Wyde P, Litovsky S, et al. Influenza infection exerts prominent inflammatory and thrombotic effects on the atherosclerotic plaques of apolipoprotein E-deficient mice. Circulation. 2003;107(5):762-768.
105. Libby P, Ridker PM, Maseri A. Inflammation and atherosclerosis. Circulation. 2002;105(9):1135-1143.
106. Mirhafez SR, Pasdar A, Avan A, et al. Cytokine and growth factor profiling in patients with the metabolic syndrome. Br J Nutr. 2015;113(12):1911-1919.
107. Cottrell EC, Seckl JR, Holmes MC, Wyrwoll CS. Foetal and placental 11β-HSD2: a hub for developmental programming. Acta Physiol (Oxf). 2014;210(2):288-295.
108. Holmes MC, Wyrwoll C, Seckl J. Fetal programming of adult behaviour by stress and glucocorticoids. Psychoneuroendocrinology. 2015;61:9.
109. Handa RJ, Weiser MJ. Gonadal steroid hormones and the hypothalamo-pituitary-adrenal axis. Front Neuroendocrinol. 2014;35(2):197-220.
110. Workman AD, Charvet CJ, Clancy B, Darlington RB, Finlay BL. Modeling transformations of neurodevelopmental sequences across mammalian species. J Neurosci. 2013;33(17):7368-7383.
111. Bayer SA, Altman J, Russo RJ, Zhang X. Timetables of neurogenesis in the human brain based on experimentally determined patterns in the rat. Neurotoxicology. 1993;14(1):83-144.
112. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC. Prenatal dexamethasone 'programmes' hypotension, but stress-induced hypertension in adult offspring. J Endocrinol. 2008;196(2):343-352.
113. Hadoke PW, Lindsay RS, Seckl JR, Walker BR, Kenyon CJ. Altered vascular contractility in adult female rats with hypertension programmed by prenatal glucocorticoid exposure. J Endocrinol. 2006;188(3):435-442.
114. Igosheva N, Taylor PD, Poston L, Glover V. Prenatal stress in the rat results in increased blood pressure responsiveness to stress and enhanced arterial reactivity to neuropeptide Y in adulthood. J Physiol. 2007;582(pt 2):665-674.
115. Moritz KM, Dodic M, Jefferies AJ, et al. Haemodynamic characteristics of hypertension induced by prenatal cortisol exposure in sheep. Clin Exp Pharmacol Physiol. 2009;36(10):981-987.
116. Rogers JM, Ellis-Hutchings RG, Grey BE, et al. Elevated blood pressure in offspring of rats exposed to diverse chemicals during pregnancy. Toxicol Sci. 2014;137(2):436-446.
117. Gwathmey TM, Shaltout HA, Rose JC, Diz DI, Chappell MC. Glucocorticoid-induced fetal programming alters the functional complement of angiotensin receptor subtypes within the kidney. Hypertension. 2011;57(3):620-626.
118. O'Sullivan L, Cuffe JS, Koning A, Singh RR, Paravicini TM, Moritz KM. Excess prenatal corticosterone exposure results in albuminuria, sex-specific hypotension, and altered heart rate responses to restraint stress in aged adult mice. Am J Physiol Renal Physiol. 2015;308(10):F1065-F1073.
119. Lee JH, Zhang J, Flores L, Rose JC, Massmann GA, Figueroa JP. Antenatal betamethasone has a sex-dependent effect on the in vivo response to endothelin in adult sheep. Am J Physiol Regul Integr Comp Physiol. 2013;304(8):R581-R587.
120. Shaltout HA, Rose JC, Chappell MC, Diz DI. Angiotensin-(1-7) deficiency and baroreflex impairment precede the antenatal betamethasone exposure-induced elevation in blood pressure. Hypertension. 2012;59(2):453-458.
121. Tang JI, Kenyon CJ, Seckl JR, Nyirenda MJ. Prenatal overexposure to glucocorticoids programs renal 11-hydroxysteroid dehydrogenase type 2 expression and salt-sensitive hypertension in the rat. J Hypertens. 2011;29(2):282-289.
122. Igosheva N, Klimova O, Anishchenko T, Glover V. Prenatal stress alters cardiovascular responses in adult rats. J Physiol. 2004;557(pt 1):273-285.
123. Samuelsson AM, Ohrn I, Dahlgren J, et al. Prenatal exposure to interleukin-6 results in hypertension and increased hypothalamic-pituitary-adrenal axis activity in adult rats. Endocrinology. 2004;145(11):4897-4911.
124. Crudo A, Petropoulos S, Moisiadis VG, et al. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: multigenerational effects. Endocrinology. 2012;153(7):3269-3283.
125. Cuffe JS, Burgess DJ, O'Sullivan L, Singh RR, Moritz KM. Maternal corticosterone exposure in the mouse programs sex-specific renal adaptations in the renin-angiotensin-aldosterone system in 6-month offspring. Physiol Rep. 2016;4(8). doi:10.14814/phy2.12754.
126. Dagan A, Gattineni J, Habib S, Baum M. Effect of prenatal dexamethasone on postnatal serum and urinary angiotensin II levels. Am J Hypertens. 2010;23(4):420-424.
127. O'Regan D, Kenyon CJ, Seckl JR, Holmes MC. Glucocorticoid exposure in late gestation in the rat permanently programs gender-specific differences in adult cardiovascular and metabolic physiology. Am J Physiol Endocrinol Metab. 2004;287(5):E863-E870.
128. Bogdarina I, Haase A, Langley-Evans S, Clark AJ. Glucocorticoid effects on the programming of AT1b angiotensin receptor gene methylation and expression in the rat. PLoS One. 2010;5(2):e9237.
129. Dodic M, McAlinden AT, Jefferies AJ, et al. Differential effects of prenatal exposure to dexamethasone or cortisol on circulatory control mechanisms mediated by angiotensin II in the central nervous system of adult sheep. J Physiol. 2006;571(pt 3):651-660.
130. Marshall AC, Shaltout HA, Nautiyal M, Rose JC, Chappell MC, Diz DI. Fetal betamethasone exposure attenuates angiotensin-(1-7)-Mas receptor expression in the dorsal medulla of adult sheep. Peptides. 2013;44:25-31.
131. Cottrell EC, Seckl JR. Prenatal stress, glucocorticoids and the programming of adult disease. Front Behav Neurosci. 2009;3:19.
132. Harris A, Seckl J. Glucocorticoids, prenatal stress and the programming of disease. Horm Behav. 2011;59(3):279-289.
133. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A, Seckl JR. Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. J Clin Invest. 1998;101(10):2174-2181.
134. Dumortier O, Theys N, Ahn MT, Remacle C, Reusens B. Impairment of rat fetal beta-cell development by maternal exposure to dexamethasone during different time-windows. PLoS One. 2011;6(10):e25576. doi:10.1371/journal.pone.0025576.
135. Drake AJ, Raubenheimer PJ, Kerrigan D, McInnes KJ, Seckl JR, Walker BR. Prenatal dexamethasone programs expression of genes in liver and adipose tissue and increased hepatic lipid accumulation but not obesity on a high-fat diet. Endocrinology. 2010;151(4):1581-1587.
136. Cleasby ME, Kelly PA, Walker BR, Seckl JR. Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology. 2003;144(3):999-1007.
137. Carbone DL, Zuloaga DG, Hiroi R, Foradori CD, Legare ME, Handa RJ. Prenatal dexamethasone exposure potentiates diet-induced hepatosteatosis and decreases plasma IGF-I in a sex-specific fashion. Endocrinology. 2012;153:295-306.
138. Nugent BM, Bale TL. The omniscient placenta: metabolic and epigenetic regulation of fetal programming. Front Neuroendocrinol. 2015;39:28-37.
139. Howerton CL, Bale TL. Targeted placental deletion of OGT recapitulates the prenatal stress phenotype including hypothalamic mitochondrial dysfunction. Proc Natl Acad Sci U S A. 2014;111(26):9639-9644.
140. Howerton CL, Morgan CP, Fischer DB, Bale TL. O-GlcNAc transferase (OGT) as a placental biomarker of maternal stress and reprogramming of CNS gene transcription in development. Proc Natl Acad Sci U S A. 2013;110(13):5169-5174.
141. Bouret SG. Early life origins of obesity: role of hypothalamic programming. J Pediatr Gastroenterol Nutr. 2009;48(suppl 1):S31-S38.
142. Bouret SG, Draper SJ, Simerly RB. Formation of projection pathways from the arcuate nucleus of the hypothalamus to hypothalamic regions implicated in the neural control of feeding behavior in mice. J Neurosci. 2004;24(11):2797-2805.
143. Croizier S, Prevot V, Bouret SG. Leptin controls parasympathetic wiring of the pancreas during embryonic life. Cell Rep. 2016;15(1):36-44.
144. Smith JT, Waddell BJ. Developmental changes in plasma leptin and hypothalamic leptin receptor expression in the rat: peripubertal changes and the emergence of sex differences. J Endocrinol. 2003;176(3):313-319.
145. Yura S, Itoh H, Sagawa N, et al. Role of premature leptin surge in obesity resulting from intrauterine undernutrition. Cell Metab. 2005;1(6):371-378.
146. Attig L, Solomon G, Ferezou J, et al. Early postnatal leptin blockage leads to a long-term leptin resistance and susceptibility to diet-induced obesity in rats. Int J Obes (Lond). 2008;32(7):1153-1160.
147. Shin BC, Dai Y, Thamotharan M, Gibson LC, Devaskar SU. Pre-and postnatal calorie restriction perturbs early hypothalamic neuropeptide and energy balance. J Neurosci Res. 2012;90(6):1169-1182.
148. Mela V, Diaz F, Lopez-Rodriguez AB, et al. Blockage of the neonatal leptin surge affects the gene expression of growth factors, glial proteins, and neuropeptides involved in the control of metabolism and reproduction in peripubertal male and female rats. Endocrinology. 2015;156(7):2571-2581.
149. Maccari S, Darnaudery M, Morley-Fletcher S, Zuena AR, Cinque C, Van Reeth O. Prenatal stress and long-term consequences: implications of glucocorticoid hormones. Neurosci Biobehav Rev. 2003;27(1-2):119-127.
150. Takahashi LK, Kalin NH. Early developmental and temporal characteristics of stress-induced secretion of pituitary-adrenal hormones in prenatally stressed rat pups. Brain Res. 1991;558(1):75-78.
151. Henry C, Kabbaj M, Simon H, Le Moal M, Maccari S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol. 1994;6(3):341-345.
152. Shoener JA, Baig R, Page KC. Prenatal exposure to dexamethasone alters hippocampal drive on hypothalamic-pituitary-adrenal axis activity in adult male rats. Am J Physiol Regul Integr Comp Physiol. 2006;290(5):R1366-R1373.
153. Richardson HN, Zorrilla EP, Mandyam CD, Rivier CL. Exposure to repetitive versus varied stress during prenatal development generates two distinct anxiogenic and neuroendocrine profiles in adulthood. Endocrinology. 2006;147(5):2506-2517.
154. McCormick CM, Smythe JW, Sharma S, Meaney MJ. Sex-specific effects of prenatal stress on hypothalamic-pituitary-adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Brain Res Dev Brain Res. 1995;84(1):55-61.
155. Bhatnagar S, Lee TM, Vining C. Prenatal stress differentially affects habituation of corticosterone responses to repeated stress in adult male and female rats. Horm Behav. 2005;47(4):430-438.
156. Tobe I, Ishida Y, Tanaka M, Endoh H, Fujioka T, Nakamura S. Effects of repeated maternal stress on FOS expression in the hypothalamic paraventricular nucleus of fetal rats. Neuroscience. 2005;134(2):387-395.
157. Hiroi R, Carbone DL, Zuloaga DG, Bimonte-Nelson HA, Handa RJ. Sexdependent programming effects of prenatal glucocorticoid treatment on the developing serotonin system and stress-related behaviors in adulthood. Neuroscience. 2016;320:43-56.
158. Brunton PJ, Donadio MV, Yao ST, et al. 5a-Reduced neurosteroids sexdependently reverse central prenatal programming of neuroendocrine stress responses in rats. J Neurosci. 2015;35(2):666-677.