Sex-specific effects of prenatal stress on glucose homoeostasis and peripheral metabolism in rats

Journal of Endocrinology

Volumn 217, Issue 2, 2013, Pages 161-173

  Brunton, Paula J ^a   Sullivan, Katie M ^b   Kerrigan, David ^b   Russell, John A ^c   Seckl, Jonathan R ^b   Drake, Amanda J ^b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

5 reductase; Adipose; Corticosterone metabolism; Early life stress; Liver; Sex difference

Indexed keywords

CHOLESTEROL; DIACYLGLYCEROL ACYLTRANSFERASE 2; GLUCOCORTICOID; GLUCOSE; LIPID; MESSENGER RNA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR ALPHA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TRIACYLGLYCEROL LIPASE;

ARTICLE; BODY WEIGHT; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; FEMALE; GLUCOSE BLOOD LEVEL; GLUCOSE HOMEOSTASIS; GLUCOSE METABOLISM; GLUCOSE TOLERANCE; HYPERINSULINEMIA; INSULIN RESISTANCE; LIPID METABOLISM; MALE; NONHUMAN; ORAL GLUCOSE TOLERANCE TEST; ORGAN WEIGHT; PRENATAL STRESS; PRIORITY JOURNAL; RAT; SEX DIFFERENCE; SUBCUTANEOUS FAT; TRIACYLGLYCEROL BLOOD LEVEL;

ANIMALS; ANIMALS, NEWBORN; FEMALE; GLUCOCORTICOIDS; GLUCOSE; HOMEOSTASIS; INSULIN; INSULIN RESISTANCE; LIPID METABOLISM; MALE; MODELS, ANIMAL; PREGNANCY; PREGNANCY, ANIMAL; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; RATS, SPRAGUE-DAWLEY; SEX FACTORS; STRESS, PHYSIOLOGICAL; STRESS, PSYCHOLOGICAL;

EID: 84877593265     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-12-0540     Document Type: Article

References (57)

1. Akiyama TE, Nicol CJ, Fievet C, Staels B, Ward JM, Auwerx J, Lee SS, Gonzalez FJ & Peters JM 2001 Peroxisome proliferator-activated receptor-a regulates lipid homeostasis, but is not associated with obesity: studies with congenic mouse lines. Journal of Biological Chemistry 276 39088-39093. (doi:10.1074/jbc.M107073200)
2. Atherton HJ, Gulston MK, Bailey NJ, Cheng KK, Zhang W, Clarke K & Griffin JL 2009 Metabolomics of the interaction between PPAR-a and age in the PPAR-a-null mouse. Molecular Systems Biology 5 259. (doi:10.1038/msb.2009.18)
3. Benediktsson R, Lindsay RS, Noble J, Seckl JR & Edwards CRW 1993 Glucocorticoid exposure in utero: new model for adult hypertension. Lancet 341 339-341. (doi:10.1016/0140-6736(93)90138-7)
4. Benediktsson R, Calder AA, Edwards CRW & Seckl JR 1997 Placental 11b-hydroxysteroid dehydrogenase: a key regulator of fetal glucocorticoid exposure. Clinical Endocrinology 46 161-166. (doi:10.1046/ j.1365-2265.1997.1230939.x)
5. Bitran D, Shiekh M & McLeod M 1995 Anxiolytic effect of progesterone is mediated by the neurosteroid allopregnanolone at brain GABA(A) receptors. Journal of Neuroendocrinology 7 171-177. (doi:10.1111/j.1365-2826.1995.tb00744.x)
6. Boden G & Shulman GI 2002 Free fatty acids in obesity and type 2 diabetes: defining their role in the development of insulin resistance and b-cell dysfunction. European Journal of Clinical Investigation 32(Suppl 3) 14-23. (doi:10.1046/j.1365-2362.32.s3.3.x)
7. Boyle KE, CanhamJP, Consitt LA, Zheng D, Koves TR, Gavin TP, Holbert D, Neufer PD, Ilkayeva O, Muoio DM et al. 2011 A high-fat diet elicitsdifferential responses in genes coordinating oxidative metabolism in skeletal muscle of lean and obese individuals. Journal of Clinical Endocrinology and Metabolism 96 775-781. (doi:10.1210/jc.2010-2253)
8. Brunton PJ & Russell JA 2010 Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: sex specific effects. Journal of Neuroendocrinology 22 258-271. (doi:10.1111/j.1365-2826.2010.01969.x)
9. Brunton PJ, McKay AJ, Ochedalski T, Piastowska A, Rebas E, Lachowicz A & Russell JA 2009 Central opioid inhibition of neuroendocrine stress responses in pregnancy in the rat is induced by the neurosteroid allopregnanolone. Journal of Neuroscience 29 6449-6460. (doi:10.1523/ JNEUROSCI.0708-09.2009)
10. Cleasby ME, Kelly PA, Walker BR & Seckl JR 2003 Programming of rat muscle and fat metabolism by in utero overexposure to glucocorticoids. Endocrinology 144 999-1007. (doi:10.1210/en.2002-220559) Cottrell EC & Ozanne SE 2007 Developmental programming of energy balance and the metabolic syndrome. Proceedings of the Nutrition Society 66 198-206. (doi:10.1017/S0029665107005447)
11. Cottrell EC & Ozanne SE 2007 Developmental programming of energy balance and the metabolic syndrome. Proceedings of the Nutrition Society 66 198-206. (doi:10.1017/S0029665107005447)
12. Drake AJ, Walker BR & Seckl JR 2005 Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. American Journal of Physiology. Regulatory, Integrative and Comparative Physiology 288 R34-R38. (doi:10.1152/ajpregu.00106.2004)
13. Drake AJ, Raubenheimer PJ, Kerrigan D, McInnes KJ, Seckl JR & Walker BR 2010 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 151 1581-1587. (doi:10.1210/ en.2009-1088)
14. Edinger KL & Frye CA 2004 Testosterone's analgesic, anxiolytic, and cognitive-enhancing effects may be due in part to actions of its 5a-reduced metabolites in the hippocampus. Behavioral Neuroscience 118 1352-1364. (doi:10.1037/0735-7044.118.6.1352)
15. Edwards CRW, Benediktsson R, Lindsay RS & Seckl JR 1993 Dysfunction of placental glucocorticoid barrier: link between fetal environment and adult hypertension? Lancet 341 355-357. (doi:10.1016/0140-6736(93)90148-A)
16. Entringer S, Wust S, Kumsta R, Layes IM, Nelson EL, Hellhammer DH & Wadhwa PD 2008 Prenatal psychosocial stress exposure is associated with insulin resistance in young adults. American Journal of Obstetrics and Gynecology 199 498e1-498e7. (doi:10.1016/j.ajog.2008.03.006)
17. Estall JL, Kahn M, Cooper MP, Fisher FM, Wu MK, Laznik D, Qu L, Cohen DE, Shulman GI & Spiegelman BM 2009 Sensitivity of lipid metabolism and insulin signaling to genetic alterations in hepatic peroxisome proliferator-activated receptor-gamma coactivator-1a expression. Diabetes 58 1499-1508. (doi:10.2337/db08-1571)
18. Friedman JE, Yun JS, Patel YM, McGrane MM & Hanson RW 1993 Glucocorticoids regulate the induction of phosphoenolpyruvate carboxykinase (GTP) gene transcription during diabetes. Journal of Biological Chemistry 268 12952-12957.
19. Gabory A, Attig L & Junien C 2009 Sexual dimorphism in environmental epigenetic programming.Molecular and Cellular Endocrinology 304 8-18. (doi:10.1016/j.mce.2009.02.015)
20. Granner D, Andreone T, Sasaki K & Beale E 1983 Inhibition of transcription of the phosphoenolpyruvate carboxykinase gene by insulin. Nature 305 549-551. (doi:10.1038/305549a0)
21. Gustafsson JA & Stenberg A 1974 Irreversible androgenic programming at birth of microsomal and soluble rat liver enzymes active on androstene- 3,17-dione and 5a-androstane-3a, 17b-diol. Journal of Biological Chemistry 249 711-718.
22. Handa RJ, Weiser MJ & Zuloaga DG 2009 A role for the androgen metabolite, 5a-androstane-3b, 17b-diol, in modulating oestrogen receptor b-mediated regulation of hormonal stress reactivity. Journal of Neuroendocrinology 21 351-358. (doi:10.1111/j.1365-2826. 2009.01840.x)
23. Hanson RW & Reshef L 2003 Glyceroneogenesis revisited. Biochimie 85 1199-1205. (doi:10.1016/j.biochi.2003.10.022)
24. Harris HJ, Kotelevtsev Y, Mullins JJ, Seckl JR & Holmes MC 2001 Intracellular regeneration of glucocorticoids by 11b-hydroxysteroid dehydrogenase (11b-HSD)-1 plays a key role in regulation of the hypothalamic-pituitary-adrenal axis: analysis of 11b-HSD-1-deficient mice. Endocrinology 142 114-120. (doi:10.1210/en.142.1.114)
25. Huang B, Wu P, Bowker-Kinley MM & Harris RA 2002 Regulation of pyruvate dehydrogenase kinase expression by peroxisome proliferatoractivated receptor-a ligands, glucocorticoids, and insulin. Diabetes 51 276-283. (doi:10.2337/diabetes.51.2.276)
26. Kim JY, Hickner RC, Cortright RL, Dohm GL & Houmard JA 2000 Lipid oxidation is reduced in obese human skeletal muscle. American Journal of Physiology. Endocrinology and Metabolism 279 E1039-E1044.
27. Koletzko B, SymondsME, Olsen SF, for the Early Nutrition Programming P & Early Nutrition Academy 2011 Programming research: where are we and where do we go from here? American Journal of Clinical Nutrition 94 2036S-2043S. (doi:10.3945/ajcn.111.018903)
28. Kotelevtsev Y, Holmes MC, Burchell A, Houston PM, SchmollD, Jamieson P, Best R, Brown R, Edwards CR, Seckl JR et al. 1997 11b-Hydroxysteroid dehydrogenase type 1 knockout mice show attenuated glucocorticoidinducible responses and resist hyperglycemia on obesity or stress. PNAS 94 14924-14929. (doi:10.1073/pnas.94.26.14924)
29. Leone TC, Weinheimer CJ & Kelly DP 1999 A critical role for the peroxisome proliferator-activated receptor a (PPARa) in the cellular fasting response: the PPARa-null mouse as a model of fatty acid oxidation disorders. PNAS 96 7473-7478. (doi:10.1073/pnas.96. 13.7473)
30. Leone TC, Lehman JJ, Finck BN, Schaeffer PJ, Wende AR, Boudina S, Courtois M, Wozniak DF, Sambandam N, Bernal-Mizrachi C et al. 2005 PGC-1a deficiency causes multi-system energy metabolic derangements: muscle dysfunction, abnormal weight control and hepatic steatosis. PLoS Biology 3 e101. (doi:10.1371/journal.pbio.0030101)
31. Lesage J, Del-Favero F, Leonhardt M, Louvart H, Maccari S, Vieau D & Darnaudery M 2004 Prenatal stress induces intrauterine growth restriction and programmes glucose intolerance and feeding behaviour disturbances in the aged rat. Journal of Endocrinology 181 291-296. (doi:10.1677/joe.0.1810291)
32. Li J, Olsen J, Vestergaard M, Obel C, Kristensen JK & Virk J 2012 Prenatal exposure to bereavement and type-2 diabetes: a Danish longitudinal population based study. PLoS ONE 7 e43508. (doi:10.1371/journal. pone.0043508)
33. Lindsay RS, Lindsay RM, Edwards CRW & Seckl JR 1996a Inhibition of 11b-hydroxysteroid dehydrogenase in pregnant rats and the programming of blood pressure in the offspring. Hypertension 27 1200-1204. (doi:10.1161/01.HYP.27.6.1200)
34. Lindsay RS, Lindsay RM, Waddell BJ & Seckl JR 1996b Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: studies with the 11b-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 39 1299-1305. (doi:10.1007/s001250050573)
35. Maccari S & Morley-Fletcher S 2007 Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrinology 32(Suppl 1) S10-S15. (doi:10.1016/j.psyneuen.2007.06.005)
36. Magee TR, Han G, Cherian B, Khorram O, Ross MG & Desai M 2008 Downregulation of transcription factor peroxisome proliferator-activated receptor in programmed hepatic lipid dysregulation and inflammation in intrauterine growth-restricted offspring. American Journal of Obstetrics and Gynecology 271 e271-e275. (doi:10.1016/j.ajog.2008.05.022)
37. Muoio DM, Way JM, Tanner CJ, Winegar DA, Kliewer SA, Houmard JA, KrausWE & DohmGL 2002 Peroxisome proliferator-activated receptora regulates fatty acid utilization in primary human skeletal muscle cells. Diabetes 51 901-909. (doi:10.2337/diabetes.51.4.901)
38. Nechushtan H, Benvenisty N, Brandeis R & Reshef L 1987 Glucocorticoids control phosphoenolpyruvate carboxykinase gene expression in a tissue specific manner. Nucleic Acids Research 15 6405-6417. (doi:10.1093/nar/15.16.6405)
39. Neumann ID, Kromer SA & Bosch OJ 2005 Effects of psycho-social stress during pregnancy on neuroendocrine and behavioural parameters in lactation depend on the genetically determined stress vulnerability. Psychoneuroendocrinology 30 791-806. (doi:10.1016/j.psyneuen.2005. 03.008)
40. Nyirenda MJ, Lindsay RS, Kenyon CJ, Burchell A & Seckl JR 1998 Glucocorticoid exposure in late gestation permanently programs rat hepatic phosphoenolpyruvate carboxykinase and glucocorticoid receptor expression and causes glucose intolerance in adult offspring. Journal of Clinical Investigation 101 2174-2181. (doi:10.1172/JCI1567)
41. Nyirenda MJ, Carter R, Tang JI, de Vries A, Schlumbohm C, Hillier SG, Streit F, Oellerich M, Armstrong VW, Fuchs E et al. 2009 Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11b-hydroxysteroid dehydrogenase type 1. Diabetes 58 2873-2879. (doi:10.2337/db09-0873)
42. Olswang Y, Blum B, Cassuto H, Cohen H, Biberman Y, Hanson RW & Reshef L 2003 Glucocorticoids repress transcription of phosphoenolpyruvate carboxykinase (GTP) gene in adipocytes by inhibiting its C/EBP-mediated activation. Journal of Biological Chemistry 278 12929-12936. (doi:10.1074/jbc.M300263200)
43. Ordyan NE & Pivina SG 2005 Effects of prenatal stress on the activity of an enzyme involved in neurosteroid synthesis during the "critical period" of sexual differentiation of the brain in male rats. Neuroscience and Behavioral Physiology 35 931-935. (doi:10.1007/ s11055-005-0148-4)
44. Paolisso G, Tataranni PA, Foley JE, Bogardus C, Howard BV & Ravussin E 1995 A high concentration of fasting plasma non-esterified fatty acids is a risk factor for the development of NIDDM. Diabetologia 38 1213-1217. (doi:10.1007/BF00422371)
45. Paris JJ, Brunton PJ, Russell JA & Frye CA 2011 Immune stress in late pregnant rats decreases length of gestation, fecundity, and alters later cognitive and affective behaviour of surviving pre-adolescent offspring. Stress 14 652-664. (doi:10.3109/10253890.2011.628719)
46. Patchev VK, Hassan AHS, Holsboer F & Almeida OFX 1996 The neurosteroid tetrahydroprogesterone attenuates the endocrine response to stress and exerts glucocorticoid-like effects on vasopressin gene transcription in the rat hypothalamus. Neuropsychopharmacology 15 533-540. (doi:10.1016/S0893-133X(96)00096-6)
47. Pilkis SJ & Granner DK 1992 Molecular physiology of the regulation of hepatic gluconeogenesis and glycolysis. Annual Review of Physiology 54 885-909. (doi:10.1146/annurev.ph.54.030192.004321)
48. Seckl JR & Holmes MC 2007 Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nature Clinical Practice. Endocrinology & Metabolism 3 479-488. (doi:10.1038/ncpendmet0515)
49. Serr J, Suh Y, Oh SA, Shin S, Kim M, Latshaw JD & Lee K 2011 Acute upregulation of adipose triglyceride lipase and release of non-esterified fatty acids by dexamethasone in chicken adipose tissue. Lipids 46 813-820. (doi:10.1007/s11745-011-3583-8)
50. Tang JI, Kenyon CJ, Seckl JR & Nyirenda MJ 2011 Prenatal overexposure to glucocorticoids programs renal 11b-hydroxysteroid dehydrogenase type 2 expression and salt-sensitive hypertension in the rat. Journal of Hypertension 29 282-289. (doi:10.1097/HJH.0b013e328340aa18)
51. De Vries A, HolmesMC,Heijnis A, Seier JV, Heerden J,Louw J, Wolfe-Coote S, MeaneyMJ, Levitt NS&Seckl JR 2007 Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. Journal of Clinical Investigation 117 1058-1067. (doi:10.1172/JCI30982)
52. Welberg LAM, Seckl JR & Holmes MC 2000 Inhibition of 11b-hydroxysteroid dehydrogenase, the foetoplacental barrier to maternal glucocorticoids, permanently programs amygdala GR mRNA expression and anxiety-like behaviour in the offspring. European Journal of Neuroscience 12 1047-1054. (doi:10.1046/j.1460-9568.2000. 00958.x)
53. Welberg LAM, Seckl JR & Holmes MC 2001 Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophinreleasing hormone: possible implications for behaviour. Neuroscience 104 71-79. (doi:10.1016/S0306-4522(01)00065-3)
54. Westerbacka J, Kolak M, Kiviluoto T,Arkkila P, Siren J, Hamsten A, FisherRM & Yki-Jarvinen H 2007 Genes involved in fatty acid partitioning and binding, lipolysis, monocyte/macrophage recruitment, and inflammation are overexpressed in the human fatty liver of insulin-resistant subjects. Diabetes 56 2759-2765. (doi:10.2337/ db07-0156)
55. Yao-Borengasser A, Varma V, Coker RH, Ranganathan G, Phanavanh B, Rasouli N & Kern PA 2011 Adipose triglyceride lipase expression in human adipose tissue and muscle. Role in insulin resistance and response to training and pioglitazone. Metabolism 60 1012-1020. (doi:10.1016/j.metabol. 2010.10.005)
56. Yehuda R, Bierer LM, Andrew R, Schmeidler J & Seckl JR 2009a Enduring effects of severe developmental adversity, including nutritional deprivation, on cortisol metabolism in aging Holocaust survivors. Journal of Psychiatric Research 43 877-883. (doi:10.1016/j.jpsychires. 2008.12.003)
57. Yehuda R, Bierer LM, Sarapas C, Makotkine I, Andrew R & Seckl JR 2009b Cortisol metabolicpredictors of response to psychotherapy for symptoms of PTSD in survivors of the World Trade Center attacks on September 11, 2001. Psychoneuroendocrinology 34 1304-1313. (doi:10.1016/j.psyneuen.2009.03.018)