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Dietary melatonin supplementation alters uteroplacental amino acid flux during intrauterine growth restriction in ewes

Published online by Cambridge University Press:  13 June 2013

C. O. Lemley*
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
L. E. Camacho
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
A. M. Meyer
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
M. Kapphahn
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
J. S. Caton
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
K. A. Vonnahme
Affiliation:
Department of Animal Sciences, Center for Nutrition and Pregnancy, North Dakota State University, Fargo, ND 58108, USA
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Abstract

Dietary melatonin supplementation during mid- to late-gestation increased umbilical artery blood flow and caused disproportionate fetal growth. This melatonin-induced increase in umbilical artery blood flow may alter nutrient availability to the fetus, which may lead to alterations in fetal size. The objectives of the current experiment were to determine amino acid (AA) and glucose concentrations as well as AA and glucose flux across the uteroplacenta using a mid- to late-gestation model of intrauterine growth restriction supplemented with dietary melatonin as a 2 × 2 factorial design. At day 50 of gestation, 32 ewes were supplemented with 5 mg of melatonin (MEL) or no melatonin (CON) and were allocated to receive 100% (adequate; ADQ) or 60% (restricted; RES) of nutrient requirements. On day 130 of gestation, uterine and umbilical blood flows were determined via Doppler ultrasonography during a non-survival surgery. Blood samples were collected under general anesthesia from the maternal saphenous artery, gravid uterine vein, umbilical artery, and umbilical vein for AA analysis and glucose. Total α-AA concentrations in maternal artery and gravid uterine vein were decreased (P < 0.05) in RES v. ADQ fed ewes. Maternal arterial − venous difference in total α-AA was increased (P ⩽ 0.01) in RES v. ADQ fed ewes, while total uterine α-AA flux was not different (P > 0.40) across all treatment groups. Fetal venous − arterial difference in total α-AA as well as uteroplacental flux of total α-AA were decreased (P < 0.05) in CON-RES v. CON-ADQ, and similar (P > 0.20) in MEL-RES v. CON-ADQ. Maternal concentrations and uterine flux of branched-chain AA (BCAA) were not different across all treatment groups; however, fetal uptake of BCAA was decreased (P < 0.05) in CON-RES v. CON-ADQ, and similar (P > 0.20) in MEL-RES v. CON-ADQ. Uterine uptake of glucose was not different (P ⩾ 0.08) across all treatment groups, while uteroplacental uptake of glucose was increased (P ⩽ 0.05) in RES v. ADQ ewes. In conclusion, maternal nutrient restriction increased maternal arterial − venous difference in total α-AA, while total uterine α-AA flux was unaffected by maternal nutrient restriction. Melatonin supplementation did not impact maternal serum concentrations or uterine flux of glucose or AA; however, melatonin did improve fetal BCAA uptake during maternal nutrient restriction.

Type
Physiology and functional biology of systems
Copyright
Copyright © The Animal Consortium 2013 

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References

Battaglia, FC, Regnault, TRH 2001. Placental transport and metabolism of amino acids. Placenta 22, 145161.Google Scholar
Chung, M, Teng, C, Timmerman, M, Meschia, G, Battaglia, FC 1998. Production and utilization of amino acids by ovine placenta in vivo. American Journal of Physiology – Endocrinology and Metabolism 274, E13E22.Google Scholar
Fowden, AL, Ward, JW, Wooding, FPB, Forhead, AJ, Constancia, M 2006. Programming placental nutrient transport capacity. Journal of Physiology 572, 515.Google Scholar
Ford, SP 1995. Control of blood flow to the gravid uterus of domestic livestock species. Journal of Animal Science 73, 18521860.Google Scholar
Hay, WW Jr 2006. Recent observations on the regulation of fetal metabolism of glucose. Journal of Physiology 572, 1724.Google Scholar
Jansson, T 2001. Amino acid transporters in the human placenta. Pediatric Research 49, 141147.Google Scholar
Juaniaux, E, Poston, L, Burton, GJ 2006. Placental-related diseases of pregnancy: involvement of oxidative stress and implications in human evolution. Human Reproduction Update 12, 747755.Google Scholar
Kwon, H, Ford, SP, Bazer, FW, Spencer, TE, Nathanielsz, PW, Nijland, MJ, Hess, BW, Wu, G 2004. Maternal nutrient restriction reduces concentrations of amino acids and polyamines in ovine maternal and fetal plasma and fetal fluids. Biology of Reproduction 71, 901908.Google Scholar
Lekatz, LA, Wu, G, Caton, JS, Taylor, JB, Reynolds, LP, Redmer, DA, Vonnahme, KA 2011. Maternal selenium supplementation and timing of nutrient restriction in pregnant sheep: impacts on nutrient availability to the fetus. Journal of Animal Science 89, 5976.Google Scholar
Lekatz, LA, Ward, MA, Borowicz, PP, Taylor, JB, Redmer, DA, Grazul-Bilska, A, Reynolds, LP, Caton, JS, Vonnahme, KA 2010. Cotyledonary responses to maternal selenium and dietary restriction may influence alterations in fetal weight and fetal liver glycogen in sheep. Animal Reproduction Science 117, 216225.Google Scholar
Lemley, CO, Meyer, AM, Camacho, LE, Neville, TL, Newman, DJ, Caton, JS, Vonnahme, KA 2012. Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 302, R454R467.Google Scholar
Leury, BJ, Bird, AR, Chandler, KD, Bells, AW 1990. Glucose partitioning in the pregnant ewe: effects of undernutrition and exercise. British Journal of Nutrition 64, 449462.Google Scholar
Limesand, SW, Rozance, PJ, Smith, D, Hay, WW Jr 2007. Increased insulin sensitivity and maintenance of glucose utilization rates in fetal sheep with placental insufficiency and intrauterine growth restriction. American Journal of Physiology – Endocrinology and Metabolism 293, E1716E1725.CrossRefGoogle ScholarPubMed
Lynch, CJ, Halle, B, Fujii, H, Vary, TC, Wallin, R, Damuni, Z, Hutson, SM 2003. Potential role of leucine metabolism in the leucine-signaling pathway involving mTOR. American Journal of Physiology – Endocrinology and Metabolism 285, E854E863.CrossRefGoogle ScholarPubMed
Meyer, AM, Reed, JJ, Neville, TL, Taylor, JB, Hammer, CJ, Reynolds, LP, Redmer, DA, Vonnahme, KA, Caton, JS 2010. Effects of plane of nutrition and selemium supply during gestation on ewe and neonatal offspring performance, body composition, and serum selemium. Journal of Animal Science 88, 17861800.Google Scholar
NRC 2007. Nutrient requirements of small ruminants. The National Academic Press, Washington, DC.Google Scholar
Paulis, L, Simko, F 2007. Blood pressure modulation and cardiovascular protection by melatonin: potential mechanisms behind. Physiological Research 56, 671684.Google Scholar
Poeggeler, B, Reiter, RJ, Tan, D, Chen, L, Manchester, L 1993. Melatonin, hydroxyl radical-mediated oxidative damage, and aging: a hypothesis. Journal of Pineal Research 14, 151168.CrossRefGoogle ScholarPubMed
Redmer, DA, Wallace, JM, Reynolds, LP 2004. Effect of nutrient intake during pregnancy on fetal and placental growth and vascular development. Domestic Animal Endocrinology 27, 199217.Google Scholar
Reiter, RJ, Melchiorri, D, Sewerynik, E, Poeggeler, B, Barlow-Walden, L, Chuang, J, Ortiz, GG, AcunaCastroviejo, D 2007. A review of the evidence supporting melatonin's role as an antioxidant. Journal of Pineal Research 18, 111.Google Scholar
Reynolds, LP, Redmer, DA 1995. Utero-placental vascular development and placental function. Journal of Animal Science 73, 18391851.Google Scholar
Reynolds, LP, Borowicz, PP, Vonnahme, KA, Johnson, ML, Grazul-Bilska, AT, Redmer, DA, Caton, JS 2005. Placental angiogenesis in sheep models of compromised pregnancy. Journal of Physiology 565, 4358.Google Scholar
Reynolds, LP, Caton, JS, Redmer, DA, Grazul-Bilska, AT, Vonnahme, KA, Borowicz, PP, Luther, JS, Wallace, JM, Wu, G, Spencer, TE 2006. Evidence for altered placental blood flow and vascularity in compromised pregnancies. Journal of Physiology 572, 5158.Google Scholar
Rigano, S, Bozzo, M, Ferrazzi, E, Belloti, M, Battaglia, FC, Galan, HL 2001. Early and persistent reduction in umbilical vain blood flow in the growth-restricted fetus: a longitudinal study. American Journal of Obstetrics and Gynecology 185, 834838.Google Scholar
Teodoro, GFR, Vianna, D, Torres-Leal, FL, Pantaleao, LC, Matos-Neto, EM, Donato, J Jr, Tirapegui, J 2012. Leucine is essential for attenuating fetal growth restriction caused by a protein-restricted diet in rats. Journal of Nutrition 142, 924930.Google Scholar
Thureen, PJ, Trembler, KA, Meschia, G, Makowski, EL, Wilkening, RB 1992. Placental glucose transport in heat-induced fetal growth retardation. American Journal of Physiology 263, R578R585.Google Scholar
Wallace, JM, Bourke, DA, Aitken, RP, Leitch, N, Hay, WW Jr 2002. Blood flows and nutrient uptakes in growth-restricted pregnancies induced by overnourishing adolescent sheep. American Journal of Physiology – Regulatory, Integrative and Comparative Physiology 282, R1027R1036.CrossRefGoogle ScholarPubMed
Wallace, JM, Luther, JS, Milne, JS, Aitken, RP, Redmer, DA, Reynolds, LP, Hay, WW Jr 2006. Nutritional modulation of adolescent pregnancy outcome – a review. Placenta 27, S61S68.Google Scholar
Wullschleger, S, Loewith, R, Hall, MN 2006. TOR signaling in growth and metabolism. Cell 124, 471484.Google Scholar
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