HORSE SPECIES SYMPOSIUM: Glucocorticoid programming of hypothalamic-pituitary-adrenal axis and metabolic function: Animal studies from mouse to horse

Journal of Animal Science

Volumn 93, Issue 7, 2015, Pages 3245-3260

  Jellyman, J K ^a   Valenzuela, O A ^b   Fowden, A L ^b  

^a HARBOR UCLA MEDICAL CENTER   (United States)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Betamethasone; Cortisol; Dexamethasone; Epigenetics; Glucose; Insulin

Indexed keywords

GLUCOCORTICOID; GLUCOSE; HYDROCORTISONE;

ANIMAL; FEMALE; HORSE; HYPOPHYSIS ADRENAL SYSTEM; HYPOTHALAMUS HYPOPHYSIS SYSTEM; METABOLISM; PHYSIOLOGY; PREGNANCY;

ANIMALS; FEMALE; GLUCOCORTICOIDS; GLUCOSE; HORSES; HYDROCORTISONE; HYPOTHALAMO-HYPOPHYSEAL SYSTEM; PITUITARY-ADRENAL SYSTEM; PREGNANCY;

EID: 84975688020     PISSN: 00218812     EISSN: 15253163     Source Type: Journal    
DOI: 10.2527/jas.2014-8612     Document Type: Review

References (152)

1. Arabadzisz, D., R. Diaz-Heijtz, I. Knuesel, E. Weber, S. Pilloud, A. C. Dettling, J. Feldon, A. J. Law, P. J. Harrison, and C. R. Pryce. 2010. Primate early life stress leads to long-term mild hippocampal decreases in corticosteroid receptor expression. Biol. Psychiatry 67:1106-1109. doi:10.1016/j.biopsych.2009.12.016.
2. Aiken, C. E., A. L. Fowden, and G. C. Smith. 2014. Antenatal glucocorticoids prior to Cesarean delivery at term. JAMA Pediatr. 168:507-508. doi:10.1001/jamapediatrics.2014.9.
3. Arumugam, R., E. Horowitz, D. Lu, J. J. Collier, S. Ronnebaum, D. Fleenor, and M. Freemark. 2008. The interplay of prolactin and the glucocorticoids in the regulation of beta-cell gene expression, fatty acid oxidation, and glucose-stimulated insulin secretion: Implications for carbohydrate metabolism in pregnancy. Endocrinology 149:5401-5414. doi:10.1210/en.2008-0051.
4. Ashcroft, F. M., and P. Rorsman. 1989. Electrophysiology of the pancreatic beta-cell. Prog. Biophys. Mol. Biol. 54:87-143. doi:10.1016/0079-6107(89)90013-8.
5. Ballard, P. L., and R. A. Ballard. 1995. Scientific basis and therapeutic regimens for use of antenatal glucocorticoids. Am. J. Obstet. Gynecol. 173:254-262. doi:10.1016/0002-9378(95)90210-4.
6. Banjanin, S., A. Kapoor, and S. G. Matthews. 2004. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function and blood pressure in mature male guinea pigs. J. Physiol. 558:305-318. doi:10.1113/jphysiol.2004.063669.
7. Barker, D. J., C. Osmond, J. Golding, D. Kuh, and M. E. Wadsworth. 1989a. Growth in utero, blood pressure in childhood and adult life, and mortality from cardiovascular disease. BMJ 298:564-567. doi:10.1136/bmj.298.6673.564.
8. Barker, D. J., P. D. Winter, C. Osmond, B. Margetts, and S. J. Simmonds. 1989b. Weight in infancy and death from ischaemic heart disease. Lancet 334:577-580. doi:10.1016/S0140-6736(89)90710-1.
9. Blanco, C. L., A. G. Moreira, L. L. McGill-Vargas, D. G. Anzueto, P. Nathanielsz, and N. Musi. 2014. Antenatal corticosteroids alter insulin signaling pathways in fetal baboon skeletal muscle. J. Endocrinol. 221:253-260. doi:10.1530/JOE-13-0504.
10. Blencowe, H., S. Cousens, M. Z. Oestergaard, D. Chou, A. B. Moller, R. Narwal, A. Adler, C. Vera Garcia, S. Rohde, L. Say, and J. E. Lawn. 2012. National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: A systematic analysis and implications. Lancet 379:2162-2172. doi:10.1016/S0140-6736(12)60820-4.
11. Blondeau, B., J. Lesage, P. Czernichow, J. P. Dupouy, and B. Bréant. 2001. Glucocorticoids impair fetal beta-cell development in rats. Am. J. Physiol. Endocrinol. Metab. 281:E592-E599.
12. Bloomfield, F. H., M. H. Oliver, C. D. Giannoulias, P. D. Gluckman, J. E. Harding, and J. R. Challis. 2003. Brief undernutrition in late-gestation sheep programs the hypothalamic-pituitary-adrenal axis in adult offspring. Endocrinology 144:2933-2940. doi:10.1210/en.2003-0189.
13. Brissova, M., M. Shiota, W. E. Nicholson, M. Gannon, S. M. Knobel, D. W. Piston, C. V. Wright, and A. C. Powers. 2002. Reduction in pancreatic transcription factor PDX-1 impairs glucose-stimulated insulin secretion. J. Biol. Chem. 277:11225-11232. doi:10.1074/jbc.M111272200.
14. Brunton, P. J., and J. A. Russell. 2010. Prenatal social stress in the rat programmes neuroendocrine and behavioural responses to stress in the adult offspring: Sex-specific effects. J. Neuroendocrinol. 22:258-271. doi:10.1111/j.1365-2826.2010.01969.x.
15. Burdge, G. C., J. Slater-Jefferies, C. Torrens, E. S. Phillips, M. A. Hanson, and K. A. Lillycrop. 2007. 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. 97:435-439. doi:10.1017/S0007114507352392.
16. Cadet, R., P. Pradier, M. Dalle, and P. Delost. 1986. Effects of prenatal maternal stress on the pituitary adrenocortical reactivity in guinea-pig pups. J. Dev. Physiol. 8:467-475.
17. Clarke, A. S., D. J. Wittwer, D. H. Abbott, and M. L. Schneider. 1994. Long-term effects of prenatal stress on HPA axis activity in juvenile rhesus monkeys. Dev. Psychobiol. 27:257-269. doi:10.1002/dev.420270502.
18. Coe, C. L., M. Kramer, B. Czéh, E. Gould, A. J. Reeves, C. Kirschbaum, and E. Fuchs. 2003. Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol. Psychiatry 54:1025-1034. doi:10.1016/S0006-3223(03)00698-X.
19. Crudo, A., S. Petropoulos, V. G. Moisiadis, M. Iqbal, A. Kostaki, Z. Machnes, M. Szyf, and S. G. Matthews. 2012. Prenatal synthetic glucocorticoid treatment changes DNA methylation states in male organ systems: Multigenerational effects. Endocrinology 153:3269-3283. doi:10.1210/en.2011-2160.
20. Dean, F., C. Yu, R. I. Lingas, and S. G. Matthews. 2001. Prenatal glucocorticoid modifies hypothalamo-pituitary-adrenal regulation in prepubertal guinea pigs. Neuroendocrinology 73:194-202. doi:10.1159/000054636.
21. De Blasio, M. J., M. Dodic, A. J. Jefferies, K. M. Moritz, E. M. Wintour, and J. A. Owens. 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. Metab. 293:E75-E82. doi:10.1152/ajpendo.00689.2006.
22. De Loof, A. 2008. Ecdysteroids, juvenile hormone and insect neuropeptides: Recent successes and remaining major challenges. Gen. Comp. Endocrinol. 155:3-13. doi:10.1016/j.ygcen.2007.07.001.
23. Desai, M., J. K. Jellyman, G. Han, M. Beall, R. H. Lane, and M. G. Ross. 2014. Maternal obesity and high-fat diet program offspring metabolic syndrome. Am. J. Obstet. Gynecol. 211:237. e1-237.e13
24. de Vries, A., M. C. Holmes, A. Heijnis, J. V. Seier, J. Heerden, J. Louw, S. Wolfe-Coote, M. J. Meaney, N. S. Levitt, and J. R. Seckl. 2007. Prenatal dexamethasone exposure induces changes in nonhuman primate offspring cardiometabolic and hypothalamic-pituitary-adrenal axis function. J. Clin. Invest. 117:1058-1067. doi:10.1172/JCI30982
25. Drake, A. J., B. R. Walker, and J. R. Seckl. 2005. Intergenerational consequences of fetal programming by in utero exposure to glucocorticoids in rats. Am. J. Physiol. Regul. Integr. Comp. Physiol. 288:R34-R38. doi:10.1152/ajpregu.00106.2004.
26. Enthoven, L., E. R. de Kloet, and M. S. Oitzl. 2008a. Differential development of stress system (re)activity at weaning dependent on time of disruption of maternal care. Brain Res. 1217:62-69. doi:10.1016/j.brainres.2008.04.009.
27. Enthoven, L., M. S. Oitzl, N. Koning, M. van der Mark, and E. R. de Kloet. 2008b. Hypothalamic-pituitary-adrenal axis activity of newborn mice rapidly desensitizes to repeated maternal absence but becomes highly responsive to novelty. Endocrinology 149:6366-6377. doi:10.1210/en.2008-0238.
28. Esguerra, J. L., and L. Eliasson. 2014. Functional implications of long non-coding RNAs in the pancreatic islets of Langerhans. Front. Genet. 5:209. doi:10.3389/fgene.2014.00209.
29. Fernandez-Twinn, D. S., M. Z. Alfaradhi, M. S. Martin-Gronert, D. E. Duque-Guimaraes, A. Piekarz, D. Ferland-McCollough, M. Bushell, and S. E. Ozanne. 2014. Downregulation of IRS- 1 in adipose tissue of offspring of obese mice is programmed cell-autonomously through post-transcriptional mechanisms. Mol. Metab. 3:325-333. doi:10.1016/j.molmet.2014.01.007.
30. Fletcher, A. J., M. R. Goodfellow, A. J. Forhead, D. S. Gardner, H. H. McGarrigle, A. L. Fowden, and D. A. Giussani. 2000. Low doses of dexamethasone suppress pituitary-adrenal function but augment the glycemic response to acute hypoxemia in fetal sheep during late gestation. Pediatr. Res. 47:684-691. doi:10.1203/00006450-200005000-00021.
31. Fletcher, A. J., X. H. Ma, W. X. Wu, P. W. Nathanielsz, H. H. McGarrigle, A. L. Fowden, and D. A. Giussani. 2004. Antenatal glucocorticoids reset the level of baseline and hypoxemia-induced pituitary-adrenal activity in the sheep fetus during late gestation. Am. J. Physiol. Endocrinol. Metab. 286:E311-E319. doi:10.1152/ajpendo.00158.2003.
32. Fowden, A. L., R. K. Barnes, R. S. Comline, and M. Silver. 1980. Pancreatic beta-cell function in the fetal foal and mare. J. Endocrinol. 87:293-301. doi:10.1677/joe.0.0870293.
33. Fowden, A. L., M. Silver, L. Ellis. J. Ousey, and P. D. Rossdale. 1984. Studies on equine prematurity 3: Insulin secretion in the foal during the perinatal period. Equine Vet J. 1984 16:286-91.
34. Forhead, A. J., and A. L. Fowden. 2014. Thyroid hormones in fetal growth and prepartum maturation. J. Endocrinol. 221:R87-R103. doi:10.1530/JOE-14-0025.
35. Fowden, A. L. 1995. Endocrine regulation of fetal growth. Reprod. Fertil. Dev. 7:351-363. doi:10.1071/RD9950351.
36. Fowden, A. L., L. Ellis, and P. D. Rossdale. 1982. Pancreatic beta cell function in the neonatal foal. J. Reprod. Fertil. Suppl. 32:529-535.
37. Fowden, A. L., and A. J. Forhead. 2009. Endocrine regulation of feto-placental growth. Horm. Res. 72:257-265. doi:10.1159/000245927.
38. Fowden, A. L., D. A. Giussani, and A. J. Forhead. 2006. Intrauterine programming of physiological systems: Causes and consequences. Physiology (Bethesda) 21:29-37. doi:10.1152/physiol.00050.2005.
39. Fowden, A. L., D. A. Giussani, and A. J. Forhead. 2005. Endocrine and metabolic programming during intrauterine development. Early Hum. Dev. 81:723-734. doi:10.1016/j.earlhumdev.2005.06.007.
40. Fowden, A. L., and D. J. Hill. 2001. Intra-uterine programming of the endocrine pancreas. Br. Med. Bull. 60:123-142. doi:10.1093/bmb/60.1.123.
41. Fowden, A. L., J. K. Jellyman, O. A. Valenzuela, and A. J. Forhead. 2013. Nutritional programming of intrauterine development: A concept applicable to the horse? J. Equine Vet. Sci. 33:295-304. doi:10.1016/j.jevs.2013.03.005.
42. Fowden, A. L., J. Li, and A. J. Forhead. 1998. Glucocorticoids and the preparation for life after birth: Are there long-term consequences of the life insurance? Proc. Nutr. Soc. 57:113-122. doi:10.1079/PNS19980017.
43. Franko, K. L., A. J. Forhead, and A. L. Fowden. 2010. Differential effects of prenatal stress and glucocorticoid administration on postnatal growth and glucose metabolism in rats. J. Endocrinol. 204:319-329. doi:10.1677/JOE-09-0390.
44. Franko, K. L., D. A. Giussani, A. J. Forhead, and A. L. Fowden. 2007. Effects of dexamethasone on the glucogenic capacity of fetal, pregnant, and non-pregnant adult sheep. J Endocrinol. 192:67-73.
45. Gesina, E., F. Tronche, P. Herrera, B. Duchene, W. Tales, P. Czernichow, and B. Breant. 2004. Dissecting the role of glucocorticoids on pancreas development. Diabetes 53:2322-2329. doi:10.2337/diabetes.53.9.2322.
46. Gray, S., B. S. Stonestreet, S. Thamotharan, G. B. Sadowska, M. Daood, J. Watchko, and S. U. Devaskar. 2006. Skeletal muscle glucose transporter protein responses to antenatal glucocorticoids in the ovine fetus. J. Endocrinol. 189:219-229. doi:10.1677/joe.1.06589.
47. Green, M. K., C. S. Rani, A. Joshi, A. E. Soto-Piña, P. A. Martinez, A. Frazer, R. Strong, and D. A. Morilak. 2011. Prenatal stress induces long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress. Neuroscience 192:438-451. doi:10.1016/j.neuroscience.2011.06.041.
48. Guberman, C., J. K. Jellyman, G. Han, M. G. Ross, and M. Desai. 2013. Maternal high-fat diet programs rat offspring hypertension and activates the adipose renin-angiotensin system. Am. J. Obstet. Gynecol. 209:262. e1-262.e8
49. Hanson, M. A., and P. D. Gluckman. 2005. Developmental processes and the induction of cardiovascular function: Conceptual aspects. J. Physiol. 565:27-34. doi:10.1113/jphysiol.2004.082339.
50. Harris, A., and J. Seckl. 2011. Glucocorticoids, prenatal stress and the programming of disease. Horm. Behav. 59:279-289. doi:10.1016/j.yhbeh.2010.06.007.
51. Hart, K. A., G. L. Heusner, N. A. Norton, and M. H. Barton. 2009. Hypothalamic-pituitary-adrenal axis assessment in healthy term neonatal foals utilizing a paired low dose/high dose ACTH stimulation test. J. Vet. Intern. Med. 23:344-351. doi:10.1111/j.1939-1676.2008.00271.x
52. Hauser, J., J. Feldon, and C. R. Pryce. 2009. Direct and dammediated effects of prenatal dexamethasone on emotionality, cognition and HPA axis in adult Wistar rats. Horm. Behav. 56:364-375. doi:10.1016/j.yhbeh.2009.07.003.
53. Hauser, J., A. Knapman, N. R. Zürcher, S. Pilloud, C. Maier, R. Diaz-Heijtz, H. Forssberg, A. Dettling, J. Feldon, and C. R. Pryce. 2008. Effects of prenatal dexamethasone treatment on physical growth, pituitary-adrenal hormones, and performance of motor, motivational, and cognitive tasks in juvenile and adolescent common marmoset monkeys. Endocrinology 149:6343-6355. doi:10.1210/en.2008-0615.
54. Haussmann, M. F., J. A. Carroll, G. D. Weesner, M. J. Daniels, R. L. Matteri, and D. C. Lay. 2000. Administration of ACTH to restrained, pregnant sows alters their pigs’ hypothalamicpituitary- adrenal (HPA) axis. J. Anim. Sci. 78:2399-2411.
55. Hay, W. W. 1995. Regulation of placental metabolism by glucose supply. Reprod. Fertil. Dev. 7:365-375. doi:10.1071/RD9950365.
56. Henry, C., M. Kabbaj, H. Simon, M. Le Moal, and S. Maccari. 1994. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J. Neuroendocrinol. 6:341-345. doi:10.1111/j.1365-2826.1994.tb00591.x.
57. Hill, D. J., and B. Duvillié. 2000. Pancreatic development and adult diabetes. Pediatr. Res. 48:269-274. doi:10.1203/00006450-200009000-00002.
58. Holdstock, N. B., V. L. Allen, and A. L. Fowden. 2012. Pancreatic endocrine function in newborn pony foals after induced or spontaneous delivery at term. Equine Vet. J. Suppl. 44:30-37. doi:10.1111/j.2042-3306.2011.00447.x.
59. Irvine, C. H., and S. L. Alexander. 1987. Measurement of free cortisol and the capacity and association constant of cortisol- binding proteins in plasma of foals and adult horses. J. Reprod. Fertil. Suppl. 35:19-24.
60. Jarvis, S., C. Moinard, S. K. Robson, E. Baxter, E. Ormandy, A. J. Douglas, J. R. Seckl, J. A. Russell, and A. B. Lawrence. 2006. Programming the offspring of the pig by prenatal social stress: Neuroendocrine activity and behaviour. Horm. Behav. 49:68-80. doi:10.1016/j.yhbeh.2005.05.004.
61. Jellyman, J. K., V. L. Allen, A. J. Forhead, N. B. Holdstock, and A. L. Fowden. 2012b. Hypothalamic-pituitary-adrenal axis function in pony foals after neonatal ACTH-induced glucocorticoid overexposure. Equine Vet. J. Suppl. 44:38-42. doi:10.1111/j.2042-3306.2011.00448.x.
62. Jellyman, J. K., V. L. Allen, N. B. Holdstock, and A. L. Fowden. 2013. Glucocorticoid overexposure in neonatal life alters pancreatic beta-cell function in newborn foals. J. Anim. Sci. 91:104-110. doi:10.2527/jas.2012-5475.
63. Jellyman, J. K., D. S. Gardner, C. M. Edwards, A. L. Fowden, and D. A. Giussani. 2005. Fetal cardiovascular, metabolic and endocrine responses to acute hypoxaemia during and following maternal treatment with dexamethasone in sheep. J. Physiol. 567:673-688. doi:10.1113/jphysiol.2005.089805.
64. Jellyman, J. K., D. S. Gardner, A. L. Fowden, and D. A. Giussani. 2004a. Effects of dexamethasone on the uterine and umbilical vascular beds during basal and hypoxemic conditions in sheep. Am. J. Obstet. Gynecol. 190:825-835. doi:10.1016/j.ajog.2003.09.046.
65. Jellyman, J. K., D. S. Gardner, H. H. McGarrigle, A. L. Fowden, and D. A. Giussani. 2004b. Pituitary-adrenal responses to acute hypoxemia during and after maternal dexamethasone treatment in sheep. Pediatr. Res. 56:864-872. doi:10.1203/01.PDR.0000145253.92052.60.
66. Jellyman, J. K., M. S. Martin-Gronert, R. L. Cripps, D. A. Giussani, S. E. Ozanne, Q. W. Shen, M. Du, A. L. Fowden, and A. J. Forhead. 2012a. Effects of cortisol and dexamethasone on insulin signalling pathways in skeletal muscle of the ovine fetus during late gestation. PLoS ONE 7:E52363. doi:10.1371/journal.pone.0052363.
67. Jellyman, J. K., O. A. Valenzuela, V. L. Allen, A. J. Forhead, N. B. Holdstock, and A. L. Fowden. 2015. Neonatal glucocorticoid overexposure programs pituitary-adrenal function in ponies. Domest. Anim. Endocrinol. 50:45-49. doi:10.1016/j.domaniend.2014.06.006.
68. Jellyman, J. K., O. A. Valenzuela, V. L. Allen, N. B. Holdstock, and A. L. Fowden. 2014. Sex-associated differences in pancreatic β cell function in healthy pre-weaning pony foals. Equine Vet. J. 46:722-728. doi:10.1111/evj.12230.
69. Jeong, I. K., S. H. Oh, B. J. Kim, J. H. Chung, Y. K. Min, M. S. Lee, M. K. Lee, and K. W. Kim. 2001. The effects of dexamethasone on insulin release and biosynthesis are dependent on the dose and duration of treatment. Diabetes Res. Clin. Pract. 51:163-171. doi:10.1016/S0168-8227(00)00229-1.
70. Jia, Y., R. Cong, R. Li, X. Yang, Q. Sun, N. Parvizi, and R. Zhao. 2012. Maternal low-protein diet induces gender-dependent changes in epigenetic regulation of the glucose-6-phosphatase gene in newborn piglet liver. J. Nutr. 142:1659-1665. doi:10.3945/jn.112.160341.
71. Jutapakdeegul, N., S. O. Casalotti, P. Govitrapong, and N. Kotchabhakdi. 2003. Postnatal touch stimulation acutely alters corticosterone levels and glucocorticoid receptor gene expression in the neonatal rat. Dev. Neurosci. 25:26-33. doi:10.1159/000071465.
72. Kapoor, A., J. Leen, and S. G. Matthews. 2008. Molecular regulation of the hypothalamic-pituitary-adrenal axis in adult male guinea pigs after prenatal stress at different stages of gestation. J. Physiol. 586:4317-4326. doi:10.1113/jphysiol.2008.153684.
73. Kapoor, A., and S. G. Matthews. 2005. Short periods of prenatal stress affect growth, behaviour and hypothalamo-pituitaryadrenal axis activity in male guinea pig offspring. J. Physiol. 566:967-977. doi:10.1113/jphysiol.2005.090191.
74. Kapoor, A., and S. G. Matthews. 2008. Prenatal stress modifies behavior and hypothalamic-pituitary-adrenal function in female guinea pig offspring: Effects of timing of prenatal stress and stage of reproductive cycle. Endocrinology 149:6406-6415. doi:10.1210/en.2008-0347.
75. Kay, G., N. Tarcic, T. Poltyrev, and M. Weinstock. 1998. Prenatal stress depresses immune function in rats. Physiol. Behav. 63:397-402. doi:10.1016/S0031-9384(97)00456-3.
76. Koehl, M., M. Darnaudéry, J. Dulluc, O. Van Reeth, M. Le Moal, and S. Maccari. 1999. Prenatal stress alters circadian activity of hypothalamo-pituitary-adrenal axis and hippocampal corticosteroid receptors in adult rats of both gender. J. Neurobiol. 40:302-315. doi:10.1002/(SICI)1097-4695(19990905)40:3<302::AID-NEU3>3.0.CO;2-7
77. Kornfeld, J. W., and J. C. Brüning. 2014. Regulation of metabolism by long, non-coding RNAs. Front. Genet. 5:57. doi:10.3389/fgene.2014.00057.
78. Kranendonk, G., H. Hopster, M. Fillerup, E. D. Ekkel, E. J. Mulder, V. M. Wiegant, and M. A. Taverne. 2006. Lower birth weight and attenuated adrenocortical response to ACTH in offspring from sows that orally received cortisol during gestation. Domest. Anim. Endocrinol. 30:218-238. doi:10.1016/j.domaniend.2005.07.001.
79. Kundakovic, M., and F. A. Champagne. 2011. Epigenetic perspective on the developmental effects of bisphenol A. Brain Behav. Immun. 25:1084-1093. doi:10.1016/j.bbi.2011.02.005.
80. Lambillotte, C., P. Gilon, and J. C. Henquin. 1997. Direct glucocorticoid inhibition of insulin secretion. An in vitro study of dexamethasone effects in mouse islets. J. Clin. Invest. 99:414-423. doi:10.1172/JCI119175.
81. Lavebratt, C., M. Almgren, and T. J. Ekström. 2012. Epigenetic regulation in obesity. Int. J. Obes. (Lond.) 36:757-765. doi:10.1038/ijo.2011.178.
82. Lay, D. C, R. D. Randel, T. H. Friend, O. C. Jenkins, D. A. Neuendorff, D. M. Bushong, E. K. Lanier, and M. K. Bjorge. 1997. Effects of prenatal stress on suckling calves. J. Anim. Sci. 75:3143-3151.
83. Lee, J. R., C. P. Hong, J. W. Moon, Y. D. Jung, D. S. Kim, T. H. Kim, J. A. Gim, J. H. Bae, Y. Choi, J. Eo, Y. J. Kwon, S. Song, J. Ko, Y. M. Yang, H. K. Lee, K. D. Park, K. Ahn, K. T. Do, H. S. Ha, K. Han, J. M. Yi, H. J. Cha, B. W. Cho, J. Bhak, and H. S. Kim. 2014. Genome-wide analysis of DNA methylation patterns in horse. BMC Genomics 15:598. doi:10.1186/1471-2164-15-598.
84. Leonhardt, H., A. W. Page, H. U. Weier, and T. H. Bestor. 1992. A targeting sequence directs DNA methyltransferase to sites of DNA replication in mammalian nuclei. Cell 71:865-873. doi:10.1016/0092-8674(92)90561-P.
85. Levitt, N. S., R. S. Lindsay, M. C. Holmes, and J. R. Seckl. 1996. 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 64:412-418. doi:10.1159/000127146.
86. Li, S., T. J. Moss, I. Nitsos, S. G. Matthews, J. R. Challis, J. P. Newnham, and D. M. Sloboda. 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. doi:10.1017/S2040174412000591.
87. Liggins, G. C. 2000. The role of the hypothalamic-pituitaryadrenal axis in preparing the fetus for birth. Am. J. Obstet. Gynecol. 182:475-477. doi:10.1016/S0002-9378(00)70241-9.
88. Lillycrop, K. A., S. P. Hoile, L. Grenfell, and G. C. Burdge. 2014. DNA methylation, ageing and the influence of early life nutrition. Proc. Nutr. Soc. 73:413-421. doi:10.1017/S0029665114000081.
89. Lindsay, R. S., R. M. Lindsay, B. J. Waddell, and J. R. Seckl. 1996. Prenatal glucocorticoid exposure leads to offspring hyperglycaemia in the rat: Studies with the 11 beta-hydroxysteroid dehydrogenase inhibitor carbenoxolone. Diabetologia 39:1299-1305. doi:10.1007/s001250050573.
90. Liu, D., J. Diorio, B. Tannenbaum, C. Caldji, D. Francis, A. Freedman, S. Sharma, D. Pearson, P. M. Plotsky, and M. J. Meaney. 1997. Maternal care, hippocampal glucocorticoid receptors, and hypothalamic-pituitary-adrenal responses to stress. Science 277:1659-1662. doi:10.1126/science.277.5332.1659.
91. Liu, L., A. Li, and S. G. Matthews. 2001. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: Sex-specific effects. Am. J. Physiol. Endocrinol. Metab. 280:E729-E739.
92. Long, N. M., D. R. Shasa, S. P. Ford, and P. W. Nathanielsz. 2012. Growth and insulin dynamics in two generations of female offspring of mothers receiving a single course of synthetic glucocorticoids. Am. J. Obstet. Gynecol. 207:203. e1-203.e8
93. Long, N. M., D. T. Smith, S. P. Ford, and P. W. Nathanielsz. 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. e1-353.e9.
94. McCance, R. A., and E. M. Widdowson. 1974. The determinants of growth and form. Proc. R. Soc. Lond. B Biol. Sci. 185:1-17. doi:10.1098/rspb.1974.0001.
95. McCormick, C. M., J. W. Smythe, S. Sharma, and M. J. Meaney. 1995. Sex-specific effects of prenatal stress on hypothalamicpituitary- adrenal responses to stress and brain glucocorticoid receptor density in adult rats. Dev. Brain Res. 84:55-61. doi:10.1016/0165-3806(94)00153-Q.
96. McGowan, P. O., and M. Szyf. 2010. Environmental epigenomics: Understanding the effects of parental care on the epigenome. Essays Biochem. 48:275-287. doi:10.1042/bse0480275.
97. Meaney, M. J., and D. H. Aitken. 1985. The effects of early postnatal handling on hippocampal glucocorticoid receptor concentrations: Temporal parameters. Brain Res. 22:301-304. doi:10.1016/0165-3806(85)90183-X.
98. Meaney, M. J., D. H. Aitken, S. R. Bodnoff, L. J. Iny, and R. M. Sapolsky. 1985a. The effects of postnatal handling on the development of the glucocorticoid receptor systems and stress recovery in the rat. Prog. Neuropsychopharmacol. Biol. Psychiatry 9:731-734. doi:10.1016/0278-5846(85)90050-8.
99. Meaney, M. J., D. H. Aitken, L. J. Bodnoff, J. E. Tatarewicz, and R. M. Sapolsky. 1985b. Early postnatal handling alters glucocorticoid receptor concentrations in selected brain regions. Behav. Neurosci. 99:765-770. doi:10.1037/0735-7044.99.4.765.
100. Meaney, M. J., D. H. Aitken, V. Viau, S. Sharma, and A. Sarrieau. 1989. Neonatal handling alters adrenocortical negative feedback sensitivity and hippocampal type II glucocorticoid receptor binding in the rat. Neuroendocrinology 50:597-604. doi:10.1159/000125287.
101. Meaney, M. J., M. Szyf, and J. R. Seckl. 2007. Epigenetic mechanisms of perinatal programming of hypothalamic-pituitaryadrenal function and health. Trends Mol. Med. 13:269-277. doi:10.1016/j.molmed.2007.05.003.
102. Moisiadis, V. G., and S. G. Matthews. 2014a. Glucocorticoids and fetal programming part 1: Outcomes. Nat. Rev. Endocrinol. 10:391-402. doi:10.1038/nrendo.2014.73.
103. Moisiadis, V. G., and S. G. Matthews. 2014b. Glucocorticoids and fetal programming part 2: Mechanisms. Nat. Rev. Endocrinol. 10:403-411. doi:10.1038/nrendo.2014.74.
104. Moss, T. J., D. M. Sloboda, L. C. Gurrin, R. Harding, J. R. Challis, and J. P. Newnham. 2001. Programming effects in sheep of prenatal growth restriction and glucocorticoid exposure. Am. J. Physiol. Regul. Integr. Comp. Physiol. 281:R960-R970.
105. Mueller, B. R., and T. L. Bale. 2008. Sex-specific programming of offspring emotionality after stress early in pregnancy. J. Neurosci. 28:9055-9065. doi:10.1523/JNEUROSCI.1424-08.2008.
106. Nagano, M., H. Ozawa, and H. Suzuki. 2008. Prenatal dexamethasone exposure affects anxiety-like behaviour and neuroendocrine systems in an age-dependent manner. Neurosci. Res. 60:364-371. doi:10.1016/j.neures.2007.12.005.
107. Nijland, M. J., K. Mitsuya, C. Li, S. Ford, T. J. McDonald, P. W. Nathanielsz, and L. A. Cox. 2010. Epigenetic modification of fetal baboon hepatic phosphoenolpyruvate carboxykinase following exposure to moderately reduced nutrient availability. J. Physiol. 588:1349-1359. doi:10.1113/jphysiol.2009.184168.
108. Nilsson, C., E. Jennische, H. P. Ho, E. Eriksson, P. Bjorntorp, and A. Holmang. 2002. Postnatal endotoxin exposure results in increased insulin sensitivity and altered activity of neuroendocrine axes in adult female rats. Eur. J. Endocrinol. 146:251-260. doi:10.1530/eje.0.1460251.
109. Nyirenda, M. J., R. Carter, J. I. Tang, A. de Vries, C. Schlumbohm, S. G. Hillier, F. Streit, M. Oellerich, V. W. Armstrong, E. Fuchs, and J. R. Seckl. 2009. Prenatal programming of metabolic syndrome in the common marmoset is associated with increased expression of 11β-hydroxysteroid dehydrogenase type 1. Diabetes 58:2873-2879. doi:10.2337/db09-0873.
110. Nyirenda, M. J., R. S. Lindsay, C. J. Kenyon, A. Burchell, and J. R. Seckl. 1998. 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. 101:2174-2181. doi:10.1172/JCI1567.
111. Okano, M., D. W. Bell, D. A. Haber, and E. Li. 1999. DNA methyltransferases Dnmt3a and Dnmt3b are essential for de novo methylation and mammalian development. Cell 99:247-257. doi:10.1016/S0092-8674(00)81656-6.
112. Ousey, J. C., A. L. Fowden, S. Wilsher, and W. R. Allen. 2008. The effects of maternal health and body condition on the endocrine responses of neonatal foals. Equine Vet. J. 40:673-679. doi:10.2746/042516408X322175.
113. Ousey, J. C., M. Kölling, H. Kindahl, and W. R. Allen. 2011. Maternal dexamethasone treatment in late gestation induces precocious fetal maturation and delivery in healthy Thoroughbred mares. Equine Vet. J. 43:424-429. doi:10.1111/j.2042-3306.2010.00306.x.
114. Ousey, J. C., P. D. Rossdale, A. L. Fowden, L. Palmer, C. Turnbull, and W. R. Allen. 2004. Effects of manipulating intrauterine growth on post natal adrenocortical development and other parameters of maturity in neonatal foals. Equine Vet. J. 36:616-621. doi:10.2746/0425164044864598.
115. Owen, D., and S. G. Matthews. 2007. Prenatal glucocorticoid exposure alters hypothalamic-pituitary-adrenal function in juvenile guinea pigs. J. Neuroendocrinol. 19:172-180. doi:10.1111/j.1365-2826.2006.01517.x.
116. Ozanne, S. E. 1999. Programming of hepatic and peripheral tissue insulin sensitivity by maternal protein restriction. Biochem. Soc. Trans. 27:94-97.
117. Panzani, S., M. Villani, N. Govoni, H. Kindahl, M. Faustini, G. Romano, and M. C. Veronesi. 2009. 15-Ketodihydro-PGF2α and cortisol plasma concentrations in newborn foals after spontaneous or oxytocin-induced parturition. Theriogenology 71:768-774. doi:10.1016/j.theriogenology.2008.09.053.
118. Petropoulos, S., S. G. Matthews, and M. Szyf. 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. doi:10.1095/biolreprod.113.115899.
119. Raff, H., L. Jacobson, and W. E. Cullinan. 2007. Augmented hypothalamic corticotrophin-releasing hormone mRNA and corticosterone responses to stress in adult rats exposed to perinatal hypoxia. J. Neuroendocrinol. 19:907-912. doi:10.1111/j.1365-2826.2007.01595.x.
120. Reynolds, R. M. 2013. Glucocorticoid excess and the developmental origins of disease: Two decades of testing the hypothesis—2012 Curt Richter Award winner. Psychoneuroendocrinology 38:1-11. doi:10.1016/j.psyneuen.2012.08.012.
121. Rossdale, P. D., J. C. Ousey, M. Silver, and A. L. Fowden. 1984. Studies on equine prematurity 6: Guidelines for assessment of foal maturity. Equine Vet. J. 16:300-302. doi:10.1111/j.2042-3306.1984.tb01931.x.
122. Rossdale, P. D., M. Silver, L. Ellis, and H. Frauenfelder. 1982. Response of the adrenal cortex to tetracosactrin (ACTH1-24) in the premature and full-term foal. J. Reprod. Fertil. Suppl. 32:545-553.
123. Roussel, S., A. Boissy, D. Montigny, P. H. Hemsworth, and C. Duvaux-Ponter. 2005. Gender-specific effects of prenatal stress on emotional reactivity and stress physiology of goat kids. Horm. Behav. 47:256-266. doi:10.1016/j.yhbeh.2004.09.010.
124. Saltiel, A. R., and C. R. Kahn. 2001. Insulin signalling and the regulation of glucose and lipid metabolism. Nature 414:799-806. doi:10.1038/414799a.
125. Schöpper, H., R. Palme, T. Ruf, and S. Huber. 2012. Effects of prenatal stress on hypothalamic-pituitary-adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus). Gen. Comp. Endocrinol. 176:18-27. doi:10.1016/j.ygcen.2011.12.010.
126. Seckl, J. R., and M. J. Meaney. 2004. Glucocorticoid programming. Ann. N. Y. Acad. Sci. 1032:63-84. doi:10.1196/annals.1314.006.
127. Shaltout, H. A., M. C. Chappell, J. C. Rose, and D. I. Diz. 2011. Exaggerated sympathetic mediated responses to behavioral or pharmacological challenges following antenatal betamethasone exposure. Am. J. Physiol. Endocrinol. Metab. 300:E979-E985. doi:10.1152/ajpendo.00636.2010.
128. Shen, C. N., J. R. Seckl, J. M. Slack, and D. Tosh. 2003. Glucocorticoids suppress beta-cell development and induce hepatic metaplasia in embryonic pancreas. Biochem. J. 375:41-50. doi:10.1042/BJ20030140.
129. Silver, M., and A. L. Fowden. 1995. Sympathoadrenal and other endocrine and metabolic responses to hypoglycaemia in the fetal foal during late gestation. Exp. Physiol. 80:651-662. doi:10.1113/expphysiol.1995.sp003875.
130. Silver, M., and A. L. Fowden. 1994. Prepartum adrenocortical maturation in the fetal foal: Responses to ACTH. J. Endocrinol. 142:417-425. doi:10.1677/joe.0.1420417.
131. Silver, M., J. C. Ousey, F. E. Dudan, A. L. Fowden, J. Knox, R. S. Cash, and P. D. Rossdale. 1984. Studies on equine prematurity 2: Post natal adrenocortical activity in relation to plasma adrenocorticotrophic hormone and catecholamine levels in term and premature foals. Equine Vet. J. 16:278-286. doi:10.1111/j.2042-3306.1984.tb01927.x.
132. Simmons, R. A. 2009. Developmental origins of adult disease. Pediatr. Clin. North Am. 56:449-466. doi:10.1016/j.pcl.2009.03.004.
133. Sloboda, D. M., T. J. Moss, L. C. Gurrin, J. P. Newnham, and J. R. Challis. 2002. The effect of prenatal betamethasone administration on postnatal ovine hypothalamic-pituitaryadrenal function. J. Endocrinol. 172:71-81. doi:10.1677/joe.0.1720071.
134. Sloboda, D. M., T. J. Moss, S. Li, D. A. Doherty, I. Nitsos, J. R. Challis, and J. P. Newnham. 2005. Hepatic glucose regulation and metabolism in adult sheep: Effects of prenatal betamethasone. Am. J. Physiol. Endocrinol. Metab. 289:E721-E728. doi:10.1152/ajpendo.00040.2005.
135. Sloboda, D. M., T. J. Moss, S. Li, D. Doherty, I. Nitsos, J. R. Challis, and J. P. Newnham. 2007. Prenatal betamethasone exposure results in pituitary-adrenal hyporesponsiveness in adult sheep. Am. J. Physiol. Endocrinol. Metab. 292:E61-E70. doi:10.1152/ajpendo.00270.2006.
136. Szuran, T. F., V. Pliska, J. Pokorny, and H. Welzl. 2000. Prenatal stress in rats: Effects on plasma corticosterone, hippocampal glucocorticoid receptors, and maze performance. Physiol. Behav. 71:353-362. doi:10.1016/S0031-9384(00)00351-6.
137. Tata, J. R. 1996. Metamorphosis: An exquisite model for hormonal regulation of post-embryonic development. Biochem. Soc. Symp. 62:123-126.
138. Thomassin, H., M. Flavin, M. L. Espinás, and T. Grange. 2001. Glucocorticoid-induced DNA demethylation and gene memory during development. EMBO J. 20:1974-1983. doi:10.1093/emboj/20.8.1974.
139. Uno, H., S. Eisele, A. Sakai, S. Shelton, E. Baker, O. DeJesus, and J. Holden. 1994. Neurotoxicity of glucocorticoids in the primate brain. Horm. Behav. 28:336-348. doi:10.1006/hbeh.1994.1030.
140. Viau, V., S. Sharma, P. M. Plotsky, and M. J. Meaney. 1993. Increased plasma ACTH responses to stress in nonhandled compared with handled rats require basal levels of corticosterone and are associated with increased levels of ACTH secretagogues in the median eminence. J. Neurosci. 13:1097-1105.
141. Waddell, B. J., M. Bollen, C. S. Wyrwoll, T. A. Mori, and P. J. Mark. 2010. Developmental programming of adult adrenal structure and steroidogenesis: effects of fetal glucocorticoid excess and postnatal dietary omega-3 fatty acids. J Endocrinol. 205:171-8.
142. Ward, H. E., E. A. Johnson, A. K. Salm, and D. L. Birkle. 2000. Effects of prenatal stress on defensive withdrawal behavior and corticotropin releasing factor systems in rat brain. Physiol. Behav. 70:359-366. doi:10.1016/S0031-9384(00)00270-5.
143. Weaver, I. C. 2009. Epigenetic effects of glucocorticoids. Semin. Fetal Neonatal Med. 14:143-150. doi:10.1016/j.siny.2008.12.002.
144. Weaver, I. C., N. Cervoni, F. A. Champagne, A. C. D’Alessio, S. Sharma, J. R. Seckl, S. Dymov, M. Szyf, and M. J. Meaney. 2004. Epigenetic programming by maternal behavior. Nat. Neurosci. 7:847-854. doi:10.1038/nn1276.
145. Weaver, I. C., A. C. D’Alessio, S. E. Brown, I. C. Hellstrom, S. Dymov, S. Sharma, M. Szyf, and M. J. Meaney. 2007. The transcription factor nerve growth factor-inducible protein a mediates epigenetic programming: Altering epigenetic marks by immediate-early genes. J. Neurosci. 27:1756-1768. doi:10.1523/JNEUROSCI.4164-06.2007.
146. Weinstock, M., T. Poltyrev, D. Schorer-Apelbaum, D. Men, and R. McCarty. 1998. Effect of prenatal stress on plasma corticosterone and catecholamines in response to footshock in rats. Physiol. Behav. 64:439-444. doi:10.1016/S0031-9384(98)00056-0.
147. Welberg, L. A., J. R. Seckl, and M. C. Holmes. 2001. Prenatal glucocorticoid programming of brain corticosteroid receptors and corticotrophin-releasing hormone: Possible implications for behaviour. Neuroscience 104:71-79. doi:10.1016/S0306-4522(01)00065-3.
148. Wlodek, M. E., A. L. Mibus, A. Tan, A. L. Siebel, J. A. Owens, and K. M. Moritz. 2007. Normal lactational environment restores nephron endowment and prevents hypertension after placental restriction in the rat. J. Am. Soc. Nephrol. 18:1688-1696. doi:10.1681/ASN.2007010015.
149. Wong, D. M., D. T. Vo, C. J. Alcott, A. J. Stewart, A. D. Peterson, B. A. Sponseller, and W. H. Hsu. 2009. Adrenocorticotropic hormone stimulation tests in healthy foals from birth to 12 weeks of age. Can. J. Vet. Res. 73:65-72.
150. Wyrwoll, C. S., D. Kerrigan, M. C. Holmes, J. R. Seckl, and A. J. Drake. 2012. Altered placental methyl donor transport in the dexamethasone programmed rat. Placenta 33:220-223. doi:10.1016/j.placenta.2011.12.017.
151. Yu, H. R., H. C. Kuo, C. C. Chen, J. M. Sheen, M. M. Tiao, Y. C. Chen, K. A. Chang, Y. L. Tain, and L. T. Huang. 2014. Prenatal dexamethasone exposure in rats results in longterm epigenetic histone modifications and tumor necrosis factor-α production decrease. Immunology 143:651-660. doi:10.1111/imm.12346.
152. Zhang, T. Y., B. Labonté, X. L. Wen, G. Turecki, and M. J. Meaney. 2013. Epigenetic mechanisms for the early environmental regulation of hippocampal glucocorticoid receptor gene expression in rodents and humans. Neuropsychopharmacology 38:111-123. doi:10.1038/npp.2012.149.