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Periconceptional undernutrition suppresses cortisol response to arginine vasopressin and corticotropin-releasing hormone challenge in adult sheep offspring

Published online by Cambridge University Press:  20 October 2011

M. H. Oliver ,
F. H. Bloomfield ,
A. L. Jaquiery ,
S. E. Todd ,
E. B. Thorstensen  and
J. E. Harding
M. H. Oliver*
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
F. H. Bloomfield
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
A. L. Jaquiery
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
S. E. Todd
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
E. B. Thorstensen
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
J. E. Harding
Affiliation:
Liggins Institute, University of Auckland, Auckland, New Zealand
*
*Address for correspondence: Dr M. H. Oliver, Ngapouri Research Farm, Liggins Institute, University of Auckland, 2739 State Highway 5, RD2, Reporoa 3083, South Waikato, New Zealand. (Email m.oliver@auckland.ac.nz)
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Abstract

Poor maternal nutrition during pregnancy can result in increased disease risk in adult offspring. Many of these effects are proposed to be mediated via altered hypothalamo–pituitary–adrenal axis (HPAA) function, and are sex and age specific. Maternal undernutrition around the time of conception alters HPAA function in foetal and early postnatal life, but there are limited conflicting data about later effects. The aim of this study was to investigate the effect of moderate periconceptional undernutrition on HPAA function of offspring of both sexes longitudinally, from juvenile to adult life. Ewes were undernourished from 61 days before until 30 days after conception or fed ad libitum. HPAA function in offspring was assessed by arginine vasopressin plus corticotropin-releasing hormone challenge at 4, 10 and 18 months. Plasma cortisol response was lower in males than in females, and was not different between singles and twins. Periconceptional undernutrition suppressed offspring plasma cortisol but not adrenocorticotropic hormone responses. In males, this suppression was apparent by 4 months, and was more profound by 10 months, with no further change by 18 months. In females, suppression was first observed at 10 months and became more profound by 18 months. Maternal undernutrition limited to the periconceptional period has a prolonged, sex-dependent effect on adrenal function in the offspring.

Keywords

ACTHcortisolmaternal nutritionpericonceptionalsheep
Type
Original Articles
Information
Journal of Developmental Origins of Health and Disease , Volume 3 , Issue 1 , February 2012 , pp. 52 - 58
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2011

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References

1. Roseboom, T, de Rooij, S, Painter, R. The Dutch famine and its long-term consequences for adult health. Early Hum Dev. 2006; 82, 485–491.CrossRefGoogle ScholarPubMed
2. Kwong, WY, Wild, AE, Roberts, P, Willis, AC, Fleming, TP. Maternal undernutrition during the preimplantation period of rat development causes blastocyst abnormalities and programming of postnatal hypertension. Development. 2000; 127, 4195–4202.Google Scholar
3. Todd, SE, Oliver, MH, Jaquiery, AL, Bloomfield, FH, Harding, JE. Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr Res. 2009; 65, 409–413.Google Scholar
4. Langley-Evans, SC, Gardner, DS, Jackson, AA. Maternal protein restriction influences the programming of the rat hypothalamic–pituitary–adrenal axis. J Nutr. 1996; 126, 1578–1585.Google Scholar
5. Lesage, J, Blondeau, B, Grino, M, Breant, B, Dupouy, JP. Maternal undernutrition during late gestation induces fetal overexposure to glucocorticoids and intrauterine growth retardation, and disturbs the hypothalamo–pituitary–adrenal axis in the newborn rat. Endocrinology. 2001; 142, 1692–1702.CrossRefGoogle ScholarPubMed
6. Dodic, M, Hantzis, V, Duncan, J, et al. . Programming effects of short prenatal exposure to cortisol. FASEB J. 2002; 16, 1017–1026.CrossRefGoogle ScholarPubMed
7. Sloboda, DM, Challis, JR, Moss, TJ, Newnham, JP. Synthetic glucocorticoids: antenatal administration and long-term implications. Curr Pharm Des. 2005; 11, 1459–1472.CrossRefGoogle ScholarPubMed
8. De Blasio, MJ, Gatford, KL, Robinson, JS, Owens, JA. Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R875–R886.Google Scholar
9. Sloboda, DM, Moss, TJ, Li, S, et al. . Prenatal betamethasone exposure results in pituitary–adrenal hyporesponsiveness in adult sheep. Am J Physiol Endocrinol Metab. 2007; 292, E61–E70.CrossRefGoogle ScholarPubMed
10. Sloboda, DM, Moss, TJ, Li, S, et al. . Expression of glucocorticoid receptor, mineralocorticoid receptor, and 11beta-hydroxysteroid dehydrogenase 1 and 2 in the fetal and postnatal ovine hippocampus: ontogeny and effects of prenatal glucocorticoid exposure. J Endocrinol. 2008; 197, 213–220.CrossRefGoogle ScholarPubMed
11. Bloomfield, FH, Oliver, MH, Hawkins, P, et al. . Periconceptional undernutrition in sheep accelerates maturation of the fetal hypothalamic–pituitary–adrenal axis in late gestation. Endocrinology. 2004; 145, 4278–4285.Google Scholar
12. Bloomfield, FH, Oliver, MH, Hawkins, P, et al. . A periconceptional nutritional origin for noninfectious preterm birth. Science. 2003; 300, 606.Google Scholar
13. Jaquiery, AL, Oliver, MH, Bloomfield, FH, Harding, JE. Periconceptional events perturb postnatal growth regulation in sheep. Pediatr Res. 2011; 70, 261–266.Google Scholar
14. Oliver, MH, Hawkins, P, Breier, BH, et al. . Maternal undernutrition during the periconceptual period increases plasma taurine levels and insulin response to glucose but not arginine in the late gestational fetal sheep. Endocrinology. 2001; 142, 4576–4579.CrossRefGoogle Scholar
15. Gardner, DS, Van Bon, BW, Dandrea, J, et al. . Effect of periconceptional undernutrition and gender on hypothalamic–pituitary–adrenal axis function in young adult sheep. J Endocrinol. 2006; 190, 203–212.CrossRefGoogle ScholarPubMed
16. Chadio, SE, Kotsampasi, B, Papadomichelakis, G, et al. . Impact of maternal undernutrition on the hypothalamic–pituitary–adrenal axis responsiveness in sheep at different ages postnatal. J Endocrinol. 2007; 192, 495–503.CrossRefGoogle ScholarPubMed
17. Canny, BJ, O'Farrell, KA, Clarke, IJ, Tilbrook, AJ. The influence of sex and gonadectomy on the hypothalamo–pituitary–adrenal axis of the sheep. J Endocrinol. 1999; 162, 215–225.Google Scholar
18. Poore, KR, Boullin, JP, Cleal, JK, et al. . Sex- and age-specific effects of nutrition in early gestation and early postnatal life on hypothalamo–pituitary–adrenal axis and sympathoadrenal function in adult sheep. J Physiol. 2010; 588, 2219–2237.CrossRefGoogle ScholarPubMed
19. Wallace, JM, Milne, JS, Green, LR, Aitken, RP. Postnatal hypothalamic–pituitary–adrenal function in sheep is influenced by age and sex, but not by prenatal growth restriction. Reprod Fertil Dev. 2011; 23, 275–284.Google Scholar
20. Hawkins, P, Steyn, C, McGarrigle, HH, et al. . Cardiovascular and hypothalamic–pituitary–adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod Fertil Dev. 2000; 12, 443–456.Google Scholar
21. Hernandez, CE, Harding, JE, Oliver, MH, et al. . Effects of litter size, sex and periconceptional ewe nutrition on side preference and cognitive flexibility in the offspring. Behav Brain Res. 2009; 204, 82–87.Google Scholar
22. Hernandez, CE, Matthews, LR, Oliver, MH, Bloomfield, FH, Harding, JE. Effects of sex, litter size and periconceptional ewe nutrition on offspring behavioural and physiological response to isolation. Physiol Behav. 2010; 101, 588–594.Google Scholar
23. Wheaton, JE, Windels, HF, Johnston, LJ. Accelerated lambing using exogenous progesterone and the ram effect. J Anim Sci. 1992; 70, 2628–2635.Google Scholar
24. Jeffray, TM, Matthews, SG, Hammond, GL, Challis, JR. Divergent changes in plasma ACTH and pituitary POMC mRNA after cortisol administration to late-gestation ovine fetus. Am J Physiol. 1998; 274, E417–E425.Google ScholarPubMed
25. Rumball, CW, Oliver, MH, Thorstensen, EB, et al. . Effects of twinning and periconceptional undernutrition on late-gestation hypothalamic–pituitary–adrenal axis function in ovine pregnancy. Endocrinology. 2008; 149, 1163–1172.Google Scholar
26. Hawkins, P, Hanson, MA, Matthews, SG. Maternal undernutrition in early gestation alters molecular regulation of the hypothalamic–pituitary–adrenal axis in the ovine fetus. J Neuroendocrinol. 2001; 13, 855–861.Google Scholar
27. Lesage, J, Hahn, D, Leonhardt, M, et al. . Maternal undernutrition during late gestation-induced intrauterine growth restriction in the rat is associated with impaired placental GLUT3 expression, but does not correlate with endogenous corticosterone levels. J Endocrinol. 2002; 174, 37–43.Google Scholar
28. Jaquiery, AL, Oliver, MH, Bloomfield, FH, et al. . Fetal exposure to excess glucocorticoid is unlikely to explain the effects of periconceptional undernutrition in sheep. J Physiol. 2006; 572, 109–118.Google Scholar
29. Connor, KL, Challis, JR, van Zijl, P, et al. . Do alterations in placental 11beta-hydroxysteroid dehydrogenase (11betaHSD) activities explain differences in fetal hypothalamic–pituitary–adrenal (HPA) function following periconceptional undernutrition or twinning in sheep? Reprod Sci. 2009; 16, 1201–1212.Google Scholar
30. Wintour, EM, Brown, EH, Denton, DA, et al. . The ontogeny and regulation of corticosteroid secretion by the ovine foetal adrenal. Acta Endocrinol (Copenh). 1975; 79, 301–316.Google Scholar
31. Connor, KL, Bloomfield, FH, Oliver, MH, Harding, JE, Challis, JR. Effect of periconceptional undernutrition in sheep on late gestation expression of mRNA and protein from genes involved in fetal adrenal steroidogenesis and placental prostaglandin production. Reprod Sci. 2009; 16, 573–583.Google Scholar
32. Gluckman, PD, Hanson, MA. The consequences of being born small – an adaptive perspective. Horm Res. 2006; 65(Suppl 3), 5–14.Google Scholar
33. Stevens, A, Begum, G, Cook, A, et al. . Epigenetic changes in the hypothalamic proopiomelanocortin and glucocorticoid receptor genes in the ovine fetus after periconceptional undernutrition. Endocrinology. 2010; 151, 3652–3664.Google Scholar
34. Kapoor, A, Petropoulos, S, Matthews, SG. Fetal programming of hypothalamic–pituitary–adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res Rev. 2008; 57, 586–595.CrossRefGoogle ScholarPubMed
35. Liu, L, Li, A, Matthews, SG. Maternal glucocorticoid treatment programs HPA regulation in adult offspring: sex-specific effects. Am J Physiol Endocrinol Metab. 2001; 280, E729–E739.Google Scholar
36. Bo, S, Cavallo-Perin, P, Ciccone, G, Scaglione, L, Pagano, G. The metabolic syndrome in twins: a consequence of low birth weight or of being a twin? Exp Clin Endocrinol Diabetes. 2001; 109, 135–140.Google Scholar
37. Ijzerman, RG, Stehouwer, CD, de Geus, EJ, et al. . The association between low birth weight and high levels of cholesterol is not due to an increased cholesterol synthesis or absorption: analysis in twins. Pediatr Res. 2002; 52, 868–872.Google Scholar
38. Iliadou, A, Cnattingius, S, Lichtenstein, P. Low birthweight and Type 2 diabetes: a study on 11,162 Swedish twins. Int J Epidemiol. 2004; 33, 948–953; discussion 53-4.Google Scholar
39. Levine, RS, Hennekens, CH, Jesse, MJ. Blood pressure in prospective population based cohort of newborn and infant twins. BMJ. 1994; 308, 298–302.Google Scholar
40. Loos, RJ, Fagard, R, Beunen, G, Derom, C, Vlietinck, R. Birth weight and blood pressure in young adults: a prospective twin study. Circulation. 2001; 104, 1633–1638.Google Scholar
41. Poulsen, P, Vaag, AA, Kyvik, KO, Moller Jensen, D, Beck-Nielsen, H. Low birth weight is associated with NIDDM in discordant monozygotic and dizygotic twin pairs. Diabetologia. 1997; 40, 439–446.Google Scholar
42. Williams, S, Poulton, R. Twins and maternal smoking: ordeals for the fetal origins hypothesis? A cohort study. BMJ. 1999; 318, 897–900.Google Scholar
43. Zhang, J, Brenner, RA, Klebanoff, MA. Differences in birth weight and blood pressure at age 7 years among twins. Am J Epidemiol. 2001; 153, 779–782.Google Scholar
44. Gardner, DS, Jamall, E, Fletcher, AJ, Fowden, AL, Giussani, DA. Adrenocortical responsiveness is blunted in twin relative to singleton ovine fetuses. J Physiol. 2004; 557, 1021–1032.Google Scholar
45. Bloomfield, FH, Oliver, MH, Harding, JE. Effects of twinning, birth size, and postnatal growth on glucose tolerance and hypothalamic–pituitary–adrenal function in postpubertal sheep. Am J Physiol Endocrinol Metab. 2007; 292, E231–E237.Google Scholar