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Maternal supplementation with fishmeal protects against late gestation endotoxin-induced fetal programming of the ovine hypothalamic-pituitary-adrenal axis

Published online by Cambridge University Press:  01 May 2014

R. E. Fisher
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
M. Or’Rashid
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
M. Quinton
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
O. AlZahal
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
H. J. Boermans
Affiliation:
Department of Biomedical Sciences, University of Guelph, Guelph, Ontario, Canada
B. W. McBride
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
N. A. Karrow*
Affiliation:
Department of Animal and Poultry Science, University of Guelph, Guelph, Ontario, Canada
*
*Address for correspondence: N. A. Karrow, Animal and Poultry Science, University of Guelph, 50 Stone Road East, Guelph, Ontario, Canada N1G2W1. (Email nkarrow@uoguelph.ca)

Abstract

Adverse uterine environments caused by maternal stress (such as bacterial endotoxin) can alter programming of the fetal hypothalamic–pituitary–adrenal axis (HPAA) rendering offspring susceptible to various adulthood diseases. Thus, protection against this type of stress may be critical for ensuring offspring health. The present study was designed to determine if maternal supplementation with omega-3 polyunsaturated fatty acids (n-3 PUFAs) during pregnancy helps to protect against stress-induced fetal programming. Briefly, 53 ewes were fed a diet supplemented with fishmeal (FM) or soybean meal (SM) from day 100 of gestation (gd100) through lactation. On gd135, half the ewes from each dietary group were challenged with either 1.2 μg/kg Escherichia coli lipopolysaccharide (LPS) endotoxin, or saline as the control. The offspring’s cortisol response to weaning stress was assessed 50 days postpartum by measuring serum cortisol concentrations 0, 6 and 24 h post weaning. Twenty-four hours post-weaning, lambs were subjected to an adrenocorticotropic hormone (ACTH) challenge (0.5 μg/kg) and serum cortisol concentrations were measured 0, 0.25, 0.5, 1 and 2 h post injection. At 5.5 months of age, offspring were also challenged with 400 ng/kg of LPS, and serum cortisol concentrations were measured 0, 2, 4 and 6 h post challenge. Interestingly, female offspring born to FM+LPS mothers had a greater cortisol response to weaning and endotoxin challenge compared with the other treatments, while female offspring born to SM+LPS mothers had a faster cortisol response to the ACTH stressor. Additionally, males born to FM+LPS mothers had a greater cortisol response to the ACTH challenge than the other treatments. Overall, FM supplementation during gestation combined with LPS challenge alters HPAA responsiveness of the offspring into adulthood.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2014 

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References

1. Harris, A, Seckl, J. Glucocorticoids prenatal stress and the programming of disease. Horm Behav. 2011; 59, 279289.CrossRefGoogle ScholarPubMed
2. Rakers, F, Frauendorf, V, Rupprecht, S, et al. Effects of early- and late-gestational maternal stress and synthetic glucocorticoid on development of the fetal hypothalamus-pituitary-adrenal axis in sheep. Stress. 2013; 16, 122129.Google Scholar
3. Sloboda, DM, Newnham, JP, Challis, JR. Repeated maternal glucocorticoid administration and the developing liver in fetal sheep. J Endocrinol. 2002; 175, 535543.Google Scholar
4. 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, E61E70.Google Scholar
5. 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, 443456.CrossRefGoogle Scholar
6. Reynolds, RM. Glucocorticoid excess and the developmental origins of disease: two decades of testing the hypothesis – 2012 Curt Richter Award Winner. Psychoneuroendocrinology. 2013; 38, 111.Google Scholar
7. Karrow, NA. Activation of the hypothalamic-pituitary-adrenal axis and autonomic nervous system during inflammation and altered programming of the neuroendocrine-immune axis during fetal and neonatal development: lessons learned from the model inflammagen, lipopolysaccharide. Brain Behav Immun. 2006; 20, 144158.Google Scholar
8. Fisher, RE, Karrow, NA, Quinton, M, et al. Endotoxin exposure during late pregnancy alters ovine offspring febrile and hypothalamic-pituitary-adrenal axis responsiveness later in life. Stress. 2010; 13, 334342.Google Scholar
9. Silverman, MN, Sternberg, EM. Glucocorticoid regulation of inflammation and its functional correlates: from HPA axis to glucocorticoid receptor dysfunction. Ann N Y Acad Sci. 2012; 1261, 5563.Google Scholar
10. Silverman, MN, Sternberg, EM. Neuroendocrine-immune interactions in rheumatoid arthritis: mechanisms of glucocorticoid resistance. Neuroimmunomodulation. 2008; 15, 1928.Google Scholar
11. Stasi, C, Orlandelli, E. Role of the brain-gut axis in the pathophysiology of Crohn’s disease. Dig Dis. 2008; 26, 156166.Google Scholar
12. Gold, SM, Mohr, DC, Huitinga, I, et al. The role of stress-response systems for the pathogenesis and progression of MS. Trends Immunol. 2005; 26, 644652.Google Scholar
13. Adcock, IM, Ford, PA, Bhavsar, P, Ahmad, T, Chung, KF. Steroid resistance in asthma: mechanisms and treatment options. Curr Allergy Asthma Rep. 2008; 8, 171178.Google Scholar
14. Simopoulos, AP. Human requirement for N-3 polyunsaturated fatty acids. Poult Sci. 2000; 79, 961970.Google Scholar
15. Laye, S. Polyunsaturated fatty acids, neuroinflammation and well being. Prostaglandins Leukot Essent Fatty Acids. 2010; 82, 295303.CrossRefGoogle ScholarPubMed
16. Calder, PC. N-3 Polyunsaturated fatty acids, inflammation, and inflammatory diseases. Am J Clin Nutr. 2006; 83, 1505S1519S.CrossRefGoogle ScholarPubMed
17. Weylandt, KH, Kang, JX. Rethinking lipid mediators. Lancet. 2005; 366, 618620.Google Scholar
18. Block, RC, Dier, U, Calderonartero, P, et al. The effects of EPA+DHA and aspirin on inflammatory cytokines and angiogenesis factors. World J Cardiovasc Dis. 2012; 2, 1419.Google Scholar
19. Lee, CH. Resolvins as new fascinating drug candidates for inflammatory diseases. Arch Pharm Res. 2012; 35, 37.Google Scholar
20. Cleland, LG, French, JK, Betts, WH, Murphy, GA, Elliott, MJ. Clinical and biochemical effects of dietary fish oil supplements in rheumatoid arthritis. J Rheumatol. 1988; 15, 14711475.Google Scholar
21. Shimizu, T, Fujii, T, Suzuki, R, et al. Effects of highly purified eicosapentaenoic acid on erythrocyte fatty acid composition and leukocyte and colonic mucosa leukotriene B4 production in children with ulcerative colitis. J Pediatr Gastroenterol Nutr. 2003; 37, 581585.Google Scholar
22. Trebble, TM, Arden, NK, Wootton, SA, et al. Fish oil and antioxidants alter the composition and function of circulating mononuclear cells in Crohn disease. Am J Clin Nutr. 2004; 80, 11371144.Google Scholar
23. Stenson, WF, Cort, D, Rodgers, J, et al. Dietary supplementation with fish oil in ulcerative colitis. Ann Intern Med. 1992; 116, 609614.Google Scholar
24. Payan, DG, Wong, MY, Chernov-Rogan, T, et al. Alterations in human leukocyte function induced by ingestion of eicosapentaenoic acid. J Clin Immunol. 1986; 6, 402410.Google Scholar
25. Arm, JP, Horton, CE, Mencia-Huerta, JM, et al. Effect of dietary supplementation with fish oil lipids on mild asthma. Thorax. 1988; 43, 8492.CrossRefGoogle ScholarPubMed
26. Mickleborough, TD, Lindley, MR, Ionescu, AA, Fly, AD. Protective effect of fish oil supplementation on exercise-induced bronchoconstriction in asthma. Chest. 2006; 129, 3949.Google Scholar
27. Stryker, JA, Fisher, R, You, Q, et al. Effects of dietary fish meal and soybean meal on the ovine innate and acquired immune response during pregnancy and lactation. Animal. 2013; 7, 151159.Google Scholar
28. Or-Rashid, MM, Fisher, R, Karrow, N, AlZahal, O, McBride, BW. Plasma fatty acid profile of gestating ewes supplemented with fishmeal. Am J Anim Vet Sci. 2012; 7, 6774.Google Scholar
29. Matthews, SG, Challis, JR. Regulation of the hypothalamo-pituitary-adrenocortical axis in fetal sheep. Trends Endocrinol Metab. 1996; 7, 239246.Google Scholar
30. Wang, Z, Goonewardene, LA. The use of MIXED models in the analysis of animal experiments with repeated measures data. Canadian J Anim Sci. 2004; 84, 111.Google Scholar
31. Block, RC, Dier, U, Calderonartero, P, et al. The effects of EPA+DHA and aspirin on inflammatory cytokines and angiogenesis factors. World J Cardiovasc Dis. 2012; 2, 1419.Google Scholar
32. Rhen, T, Cidlowski, JA. Antiinflammatory action of glucocorticoids--new mechanisms for old drugs. N Engl J Med. 2005; 353, 17111723.Google Scholar
33. Barnes, PJ. Glucocorticosteroids: current and future directions. Br J Pharmacol . 2011; 163, 2943.Google Scholar
34. Waddell, BJ, Bollen, M, Wyrwoll, CS, Mori, TA, Mark, PJ. Developmental programming of adult adrenal structure and steroidogenesis: effects of fetal glucocorticoid excess and postnatal dietary omega-3 fatty acids. J Endocrinol. 2010; 205, 171178.CrossRefGoogle ScholarPubMed
35. Ganga, R, Tort, L, Acerete, L, Montero, D, Izquierdo, MS. Modulation of ACTH-induced cortisol release by polyunsaturated fatty acids in interrenal cells from gilthead seabream, Sparus aurata. J Endocrinol. 2006; 190, 3945.Google Scholar
36. Rapoport, SI, Chang, MC, Spector, AA. Delivery and turnover of plasma-derived essential PUFAs in mammalian brain. J Lipid Res. 2001; 42, 678685.Google Scholar
37. Song, JH, Fujimoto, K, Miyazawa, T. Polyunsaturated (n-3) fatty acids susceptible to peroxidation are increased in plasma and tissue lipids of rats fed docosahexaenoic acid-containing oils. J Nutr. 2000; 130, 30283033.Google Scholar
38. Schopper, H, Palme, R, Ruf, T, Huber, S. Chronic stress in pregnant guinea pigs (Cavia aperea f. porcellus) attenuates long-term stress hormone levels and body weight gain, but not reproductive output. J Comp Physiol B. 2011; 181, 10891100.Google Scholar
39. Kapoor, A, Matthews, SG. 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. 2008; 149, 64066415.CrossRefGoogle ScholarPubMed
40. Hodyl, NA, Walker, FR, Krivanek, KM, Clifton, V, Hodgson, DM. Modelling prenatal bacterial infection: functional consequences of altered hypothalamic pituitary adrenal axis development. Behav Brain Res. 2007; 178, 108114.Google Scholar
41. McCabe, L, Marash, D, Li, A, Matthews, SG. Repeated antenatal glucocorticoid treatment decreases hypothalamic corticotropin releasing hormone mRNA but not corticosteroid receptor mRNA expression in the fetal guinea-pig brain. J Neuroendocrinol. 2001; 13, 425431.Google Scholar
42. Schopper, H, Palme, R, Ruf, T, Huber, S. Effects of prenatal stress on hypothalamic-pituitary-adrenal (HPA) axis function over two generations of guinea pigs (Cavia aperea f. porcellus). Gen Comp Endocrinol. 2012; 176, 1827.Google Scholar
43. 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, 495503.Google Scholar
44. 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, 203212.Google Scholar
45. 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, 22192237.Google Scholar
46. 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, 464476.Google Scholar
47. Kapoor, A, Matthews, SG. Testosterone is involved in mediating the effects of prenatal stress in male guinea pig offspring. J Physiol. 2011; 589, 755766.Google Scholar
48. Shanks, N, McCormick, CM, Meaney, MJ. Sex differences in hypothalamic-pituitary-adrenal responding to endotoxin challenge in the neonate: reversal by gonadectomy. Brain Res Dev Brain Res. 1994; 79, 260266.Google Scholar
49. Collier, CT, Williams, PN, Carroll, JA, Welsh, TH Jr, Laurenz, JC. Effect of maternal restraint stress during gestation on temporal lipopolysaccharide-induced neuroendocrine and immune responses of progeny. Domest Anim Endocrinol. 2011; 40, 4050.Google Scholar
50. Puder, JJ, Freda, PU, Goland, RS, Wardlaw, SL. Estrogen modulates the hypothalamic-pituitary-adrenal and inflammatory cytokine responses to endotoxin in women. J Clin Endocrinol Metab. 2001; 86, 24032408.Google ScholarPubMed