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Influence of nutrient restriction and melatonin supplementation of pregnant ewes on maternal and fetal pancreatic digestive enzymes and insulin-containing clusters

Published online by Cambridge University Press:  09 November 2015

F. E. Keomanivong ,
C. O. Lemley ,
L. E. Camacho ,
R. Yunusova ,
P. P. Borowicz ,
J. S. Caton ,
A. M. Meyer ,
K. A. Vonnahme  and
K. C. Swanson
F. E. Keomanivong
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
C. O. Lemley
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
L. E. Camacho
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
R. Yunusova
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
P. P. Borowicz
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
J. S. Caton
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
A. M. Meyer
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
K. A. Vonnahme
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
K. C. Swanson*
Affiliation:
Animal Sciences Department, North Dakota State University, PO Box 6050, Fargo, ND 58108-6050, USA
*
†E-mail: [email protected]
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Abstract

Primiparous ewes (n=32) were assigned to dietary treatments in a 2×2 factorial arrangement to determine effects of nutrient restriction and melatonin supplementation on maternal and fetal pancreatic weight, digestive enzyme activity, concentration of insulin-containing clusters and plasma insulin concentrations. Treatments consisted of nutrient intake with 60% (RES) or 100% (ADQ) of requirements and melatonin supplementation at 0 (CON) or 5 mg/day (MEL). Treatments began on day 50 of gestation and continued until day 130. On day 130, blood was collected under general anesthesia from the uterine artery, uterine vein, umbilical artery and umbilical vein for plasma insulin analysis. Ewes were then euthanized and the pancreas removed from the ewe and fetus, trimmed of mesentery and fat, weighed and snap-frozen until enzyme analysis. In addition, samples of pancreatic tissue were fixed in 10% formalin solution for histological examination including quantitative characterization of size and distribution of insulin-containing cell clusters. Nutrient restriction decreased (P⩽0.001) maternal pancreatic mass (g) and α-amylase activity (U/g, kU/pancreas, U/kg BW). Ewes supplemented with melatonin had increased pancreatic mass (P=0.03) and α-amylase content (kU/pancreas and U/kg BW). Melatonin supplementation decreased (P=0.002) maternal pancreatic insulin-positive tissue area (relative to section of tissue), and size of the largest insulin-containing cell cluster (P=0.04). Nutrient restriction decreased pancreatic insulin-positive tissue area (P=0.03) and percent of large (32 001 to 512 000 µm2) and giant (⩾512 001 µm2) insulin-containing cell clusters (P=0.04) in the fetus. Insulin concentrations in plasma from the uterine vein, umbilical artery and umbilical vein were greater (P⩽0.01) in animals receiving 100% requirements. When comparing ewes to fetuses, ewes had a greater percentage of medium insulin-containing cell clusters (2001 to 32 000 µm2) while fetuses had more (P<0.001) pancreatic insulin-positive area (relative to section of tissue) and a greater percent of small, large and giant insulin-containing cell clusters (P⩽0.02). Larger insulin-containing clusters were observed in fetuses (P<0.001) compared with ewes. In summary, the maternal pancreas responded to nutrient restriction by decreasing pancreatic weight and activity of digestive enzymes while melatonin supplementation increased α-amylase content. Nutrient restriction decreased the number of pancreatic insulin-containing clusters in fetuses while melatonin supplementation did not influence insulin concentration. This indicated using melatonin as a therapeutic agent to mitigate reduced pancreatic function in the fetus due to maternal nutrient restriction may not be beneficial.

Keywords

developmentewesmelatoninnutrient restrictionpancreas
Type
Research Article
Information
animal , Volume 10 , Issue 3 , March 2016 , pp. 440 - 448
Copyright
© The Animal Consortium 2015 

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References

Borowicz, PP, Arnold, DR, Johnson, ML, Grazul-Bilska, AT, Redmer, DA and Reynolds, LP 2007. Placental growth throughout the last two-thirds of pregnancy in sheep: vascular development and angiogenic factor expression. Biology of Reproduction 76, 259–267.Google Scholar
Bubenik, GA 2008. Thirty four years since the discovery of gastrointestinal melatonin. Journal of Physiology and Pharmacology 58, 33–51.Google Scholar
Chen, L, Yang, W, Zheng, J, Hu, X, Kong, W and Zhang, H 2010. Effect of catch-up growth after food restriction on the entero-insular axis in rats. Nutrition and Metabolism (London) 7, 45.Google Scholar
Corring, T 1980. The adaptation of digestive enzymes to the diet: its physiological significance. Reproduction Nutrition Development 20, 1217–1235.Google Scholar
Dahri, S, Reusen, B, Remacle, C and Hoet, JJ 1995. Nutritional influences on pancreatic development and potential links with non-insulin-dependent diabetes. Proceedings of the Nutrition Society 54, 345–356.CrossRefGoogle ScholarPubMed
Geiger, R and Fritz, H 1986. Trypsin. In Methods of enzymatic analysis (ed. H Bergmeyer), pp. 119–128. Elsevier, New York, USA.Google Scholar
Harmon, DL 1992. Impact of nutrition on pancreatic exocrine and endocrine secretion in ruminants: a review. Journal of Animal Science 70, 1290–1301.Google Scholar
Imamura, S and Misaki, H 1984. A sensitive method for assay of lipase activity by coupling with β-oxidation enzymes of fatty acids. Selected topics in clinical enzymology. Clinical Chemistry 2, 73.Google Scholar
Jaworek, J, Katarzyna, N, Konturek, SJ, Leja-Szpak, A, Thor, P and Pawlik, WW 2004. Melatonin and its precursor, L-tryptophan: influence on pancreatic amylase secretion in vivo and in vitro. Journal of Pineal Research 36, 155–164.Google Scholar
Jaworek, J, Nawrot-Porabka, K, Leja-Szpak, A, Bonior, J, Szklarczyk, J, Kot, M, Konturek, SJ and Pawlik, WW 2007. Melatonin as modulator of pancreatic enzyme secretion and pancreatoprotector. Journal of Physiology and Pharmacology 58 (suppl. 6), 65–80.Google ScholarPubMed
Jaworek, J, Szklarczyk, J, Jaworek, AK, Nawrot-Porąbka, K, Leja-Szpak, A, Bonior, J and Kot, M 2012. Protective effect of melatonin on acute pancreatitis. International Journal of Inflammation 2012, 173675.Google Scholar
Lemley, CO, Camacho, LE, Meyer, AM, Kapphahn, M, Caton, JS and Vonnahme, KA 2013. Dietary melatonin supplementation alters uteroplacental amino acid flux during intrauterine growth restriction in ewes. Animal 7, 1500–1507.Google Scholar
Lemley, CO, Meyer, AM, Camacho, EL, Neville, TL, Newman, DJ, Caton, JS and Vonnahme, KA 2012. Melatonin supplementation alters uteroplacental hemodynamics and fetal development in an ovine model of intrauterine growth restriction (IUGR). American Journal of Physiology, Regulatory, Integrative and Comparative Physiology 302, R454–R467.Google Scholar
Li, G, Hou, G, Lu, W and Kang, J 2011. Melatonin protects mice with intermittent hypoxia from oxidative stress-induced pancreatic injury. Sleep and Biological Rhythms 9, 78–85.Google Scholar
Merkwitz, C, Lochhead, P, Böttger, J, Matz-Soja, M, Sakurai, M, Gebhardt, R and Ricken, AM 2012. Dual origin, development, and fate of bovine pancreatic islets. Journal of Anatomy 222, 358–371.Google Scholar
NRC 2007. Nutrient requirements of small ruminants. National Academies Press, Washington, DC.Google Scholar
Reed, JJ, Ward, MA, Vonnahme, KA, Neville, TL, Julius, SL, Borowicz, PP, Taylor, JB, Redmer, DA, Grazul-Bilska, AT, Reynolds, LP and Caton, JS 2007. Effects of selenium supply and dietary restriction on maternal and fetal BW, visceral organ mass and cellularity estimates, and jejunal vascularity in pregnant ewe lambs. Journal of Animal Science 85, 2721–2733.Google Scholar
Sartori, C, Dessen, P, Mathieu, C, Monney, A, Bloch, J, Nicod, P, Scherrer, U and Duplain, H 2009. Melatonin improves glucose homeostasis and endothelial vascular function in high-fat diet-fed insulin-resistant mice. Endocrinology 150, 5311–5317.Google Scholar
Singer, D 2006. Size relationship of metabolic rate: oxygen availability as the ‘missing link’ between structure and function? Thermochimica Acta 446, 20–28.Google Scholar
Smith, PK, Krohn, RI, Hermanson, GT, Mallia, AK, Gartner, FH, Provenzano, MD, Fujimoto, EK, Goeke, NM, Olson, BJ and Klenk, DC 1985. Measurement of protein using bicinchoninic acid. Analytical Biochemistry 150, 76–85.Google Scholar
Swanson, KC and Harmon, DL 2002. Dietary influences on pancreatic α-amylase expression and secretion in ruminants. In Biology of the intestine in growing animals (ed. R Zabielski, V Lesniewska, PC Gregory and B. Westrom), pp. 515–537. Elsevier, Boston, USA.Google Scholar
Swanson, KC, Kelly, N, Salim, H, Wang, YJ, Holligan, S, Fan, MZ and McBride, BW 2008. Pancreatic mass, cellularity and α-amylase and trypsin activity in feedlot steers fed diets differing in crude protein concentration. Journal of Animal Science 86, 909–915.Google Scholar
Takahashi, H, Kurose, Y, Kobayashi, S, Sugino, T, Kojima, M, Kangawa, K, Hasegawa, Y and Terashima, Y 2006. Ghrelin enhances glucose-induced insulin secretion in scheduled meal-fed sheep. Journal of Endocrinology 189, 67–75.Google Scholar
Wallenfels, K, Fold, P, Niermann, H, Bender, H and Linder, D 1978. The enzymatic synthesis, by transglucosylation of a homologous series of glycosidically substituted malto-oligosaccharides, and their use as amylase substrates. Carbohydrate Research 61, 359–368.Google Scholar
Wang, WB, Ogawa, T, Suda, S, Taniguchi, K, Uike, H, Kumagai, H and Mitani, K 1998. Effects of nutrition level on digestive enzyme activities in the pancreas and small intestine of calves slaughtered at the same body weight. Asian-Australasian Journal of Animal Sciences 11, 375–380.CrossRefGoogle Scholar