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Dietary alanyl-glutamine improves growth performance of weaned piglets through maintaining intestinal morphology and digestion–absorption function

Published online by Cambridge University Press:  21 February 2019

T. D. Zou ,
C. X. Deng ,
Z. R. Wang ,
Y. L. Ye  and
J. M. You
T. D. Zou
Affiliation:
Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China
C. X. Deng
Affiliation:
Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China
Z. R. Wang
Affiliation:
Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China
Y. L. Ye
Affiliation:
Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China
J. M. You*
Affiliation:
Jiangxi Province Key Laboratory of Animal Nutrition, Engineering Research Center of Feed Development, Jiangxi Agricultural University, Nanchang 330045, Jiangxi, China
*
†E-mail: [email protected]
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Abstract

Alanyl-glutamine (Ala-Gln), a highly soluble and stable glutamine dipeptide, is known to improve gut integrity and function. The aim of this study was to evaluate whether dietary Ala-Gln supplementation could improve growth performance, intestinal development and digestive-absorption function in weaned piglets. A total of 100 purebred Yorkshire piglets weaned at 21 days of age were assigned randomly to four dietary treatment groups and fed a basal diet (control group) or a basal diet containing 0.15%, 0.30% and 0.45% Ala-Gln, respectively. Compared with the control group, piglets fed the Ala-Gln diets had higher average daily gain and lower feed : gain and diarrhea rate (P < 0.05). Moreover, dietary Ala-Gln supplementation increased villous height and villous height : crypt depth ratio in duodenum and jejunum (P < 0.05), as well as the activities of maltase and lysozyme in jejunum mucosa (P < 0.05). In addition, a decrease in serum diamine oxidase activity and crypt depth in duodenum and jejunum was observed in piglets fed the Ala-Gln diets (P < 0.05). Serum cytosolic phospholipase A2 (cPLA2) concentration and gene expression of cPLA2, Na+-dependent glucose transporter 1, glucose transporter 2 and peptide transporter 1 in jejunum were increased by feeding Ala-Gln diets relative to control diet (P < 0.05). These results indicated that feeding Ala-Gln diet has beneficial effects on the growth performance of weaned piglets, which associated with maintaining intestinal morphology and digestive-absorption function.

Keywords

alanyl-glutamineintestinal structureintestinal disaccharidase activitiesnutrient transportationmucosal barrier function
Type
Research Article
Information
animal , Volume 13 , Issue 9 , September 2019 , pp. 1826 - 1833
Copyright
© The Animal Consortium 2019 

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Footnotes

a

These two authors contributed equally to this work.

References

Boudry, G, Péron, V, Le, HLI, Lallès, JP and Sève, B 2004. Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. Journal of Nutrition 134, 2256–2262.CrossRefGoogle ScholarPubMed
Boyer, PE, D’Costa, S, Edwards, LL, Milloway, M, Susick, E, Borst, LB, Thakur, S, Campbell, JM, Crenshaw, JD and Polo, J 2015. Early-life dietary spray-dried plasma influences immunological and intestinal injury responses to later-life Salmonella typhimurium challenge. British Journal of Nutrition 113, 783–793.CrossRefGoogle ScholarPubMed
Buyse, M, Berlioz, F, Guilmeau, S, Tsocas, A, Voisin, T, Peranzi, G, Merlin, D, Laburthe, M, Lewin, M and Roze, C 2001. PepT1-mediated epithelial transport of dipeptides and cephalexin is enhanced by luminal leptin in the small intestine. Journal of Clinical Investigation 108, 1483–1494.CrossRefGoogle ScholarPubMed
Carneiro-Filho, BA, Bushen, OY, Brito, GAC, Lima, AAM and Guerrant, RL 2003. Glutamine analogues as adjunctive therapy for infectious diarrhea. Current Infectious Disease Reports 5, 114–119.CrossRefGoogle ScholarPubMed
Cheng, Z 2011. Effects of dietary arginine and glutamine on growth performance, immune responses and intestinal structure of red drum, Sciaenops ocellatus. Aquaculture 319, 247–252.CrossRefGoogle Scholar
Dey, I, Lejeune, M and Chadee, K 2006. Prostaglandin E2 receptor distribution and function in the gastrointestinal tract. British Journal of Pharmacology 149, 611–623.CrossRefGoogle ScholarPubMed
Hou, Y, Wang, L, Zhang, W, Yang, Z, Ding, B, Zhu, H, Liu, Y, Qiu, Y, Yin, Y and Wu, G 2012. Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43, 1233–1242.CrossRefGoogle ScholarPubMed
Ipharraguerre, IR, Tedó, G, Menoyo, D, De, DCN, Holst, JJ, Nofrarías, M, Mereu, A and Burrin, DG 2013. Bile acids induce glucagon-like peptide 2 secretion with limited effects on intestinal adaptation in early weaned pigs. The Journal of Nutrition 143, 1899–1905.CrossRefGoogle ScholarPubMed
Jian, ZM, Cao, JD, Zhu, XG, Zhao, WX, Yu, JC, Ma, EL, Wang, XR, Zhu, MW, Shu, H and Liu, YW 1999. The impact of alanyl-glutamine on clinical safety, nitrogen balance, intestinal permeability, and clinical outcome in postoperative patients: a randomized, double-blind, controlled study of 120 patients. Journal of Parenteral & Enteral Nutrition 23, S62–66.Google ScholarPubMed
Kamei, H, Hachisuka, T, Nakao, M and Takagi, K 2005. Quick recovery of serum diamine oxidase activity in patients undergoing total gastrectomy by oral enteral nutrition. American Journal of Surgery 189, 38–43.CrossRefGoogle ScholarPubMed
Khan, K and Elia, M 1991. Factors affecting the stability of L-glutamine in solution. Clinical Nutrition 10, 186–192.CrossRefGoogle ScholarPubMed
Lima, NL, Soares, AM, Mota, RM, Monteiro, HS, Guerrant, RL and Lima, AA 2007. Wasting and intestinal barrier function in children taking alanyl-glutamine-supplemented enteral formula. Journal of Pediatric Gastroenterology & Nutrition 44, 365–374.CrossRefGoogle ScholarPubMed
Liu, Y, Mao, X, Yu, B, He, J, Zheng, P, Yu, J, Luo, J and Chen, D 2014. Excessive dietary taurine supplementation reduces growth performance, liver and intestinal health of weaned pigs. Livestock Science 168, 109–119.CrossRefGoogle Scholar
Livak, KJ and Schmittgen, TD 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25, 402–408.CrossRefGoogle Scholar
Ma, X, Zhang, S, Pan, L and Piao, X 2017. Effects of lysozyme on the growth performance, nutrient digestibility, intestinal barrier and microbiota of weaned pigs fed diets containing spray-dried whole egg or albumen powder. Canadian Journal of Animal Science 97, 466–475.Google Scholar
Minerwilliams, WM and Moughan, PJ 2016. Intestinal barrier dysfunction: implications for chronic inflammatory conditions of the bowel. Nutrition Research Reviews 29, 40–59.CrossRefGoogle Scholar
Minguetti-Câmara, VC, Marques, AC, Schiavon, FP, Vilela, VR, Bruschi, ML and Bazotte, RB 2014. A comparison of the effects of oral glutamine dipeptide, glutamine, and alanine on blood amino acid availability in rats submitted to insulin-induced hypoglycemia. Nutrients 6, 4520–4530.CrossRefGoogle ScholarPubMed
Moeser, AJ, Klok, CV, Ryan, KA, Wooten, JG, Little, D, Cook, VL and Blikslager, AT 2007. Stress signaling pathways activated by weaning mediate intestinal dysfunction in the pig. American Journal of Physiology Gastrointestinal & Liver Physiology 292, G173–G181.CrossRefGoogle ScholarPubMed
Montagne, L, Pluske, JR and Hampson, DJ 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals [Review]. Animal Feed Science and Technology 108, 95–117.CrossRefGoogle Scholar
Moore, SR, Guedes, MM, Costa, TB, Vallance, J, Maier, EA, Betz, KJ, Aihara, E, Mahe, MM, Lima, AA and Oriá, RB 2015. Glutamine and alanyl-glutamine promote crypt expansion and mTOR signaling in murine enteroids. American Journal of Physiology Gastrointestinal & Liver Physiology 308, G831–G839.CrossRefGoogle ScholarPubMed
Nabuurs, MJ, Hoogendoorn, A, Ej, VDM and van Osta, AL 1993. Villus height and crypt depth in weaned and unweaned pigs, reared under various circumstances in the Netherlands. Research in Veterinary Science 55, 78–84.CrossRefGoogle ScholarPubMed
National Research Council 2012. Nutrient requirement of swine, 11th revised edition. National Academic Press, Washington, DC, USA.Google Scholar
O’Brien, DP, Nelson, LA, Huang, FS and Warner, BW 2001. Intestinal adaptation: structure, function, and regulation. Seminars in Pediatric Surgery 10, 56–64.CrossRefGoogle ScholarPubMed
Oliver, WT and Wells, JE 2013. Lysozyme as an alternative to antibiotics improves growth performance and small intestinal morphology in nursery pigs. Journal of Animal Science 91, 3129–3136.CrossRefGoogle ScholarPubMed
Panel, V, Boëlle, PY and Ayala, J 2006. Cytoplasmic phospholipase A2 expression in human colon adenocarcinoma is correlated with cyclooxygenase-2 expression and contributes to prostaglandin E2 production. Cancer Letters 243, 255–263.CrossRefGoogle ScholarPubMed
Pié, S, Lallès, JP, Blazy, F, Laffitte, J, Sève, B and Oswald, IP 2004. Weaning is associated with an upregulation of expression of inflammatory cytokines in the intestine of piglets. The Journal of Nutrition 134, 641–647.CrossRefGoogle ScholarPubMed
Pluske, JR, Hampson, DJ and Williams, IH 1997. Factors influencing the structure and function of the small intestine in the weaned pig: a review. Livestock Production Science 51, 215–236.CrossRefGoogle Scholar
Röder, PV, Geillinger, KE, Zietek, TS, Thorens, B, Koepsell, H and Daniel, H 2014. The role of SGLT1 and GLUT2 in intestinal glucose transport and sensing. Plos One 9, e89977.CrossRefGoogle Scholar
Rodrigues, RS, Oliveira, RA, Li, Y, Zaja-Milatovic, S, Costa, LB, Braga Neto, MB, Kolling, GL, Lima, AA, Guerrant, RL and Warren, CA 2013. Intestinal epithelial restitution after TcdB challenge and recovery from Clostridium difficile infection in mice with alanyl-glutamine treatment. Journal of Infectious Diseases 207, 1505–1515.CrossRefGoogle ScholarPubMed
Rosa, CV, Azevedo, SC, Bazotte, RB, Peralta, RM, Buttow, NC, Pedrosa, MM, Godoi, VA and Natali, MR 2015. Supplementation with L-glutamine and L-alanyl-L-glutamine changes biochemical parameters and jejunum morphophysiology in type 1 diabetic wistar rats. Plos One 10, e0143005.CrossRefGoogle ScholarPubMed
Santos, AA, Braganeto, MB, Oliveira, MR, Freire, RS, Barros, EB, Santiago, TM, Rebelo, LM, Mermelstein, C, Warren, CA and Guerrant, RL 2013. Glutamine and alanyl-glutamine increase RhoA expression and reduce Clostridium difficile toxin-a-induced intestinal epithelial cell damage. BioMed Research International 2013, 152052.CrossRefGoogle ScholarPubMed
Smith, F, Clark, JE, Overman, BL, Tozel, CC, Huang, JH, Rivier, JE, Blikslager, AT and Moeser, AJ 2010. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. American Journal of Physiology Gastrointestinal & Liver Physiology 298, 352–363.CrossRefGoogle ScholarPubMed
Ueno, PM, Oriá, RB, Maier, EA, Guedes, M, de Azevedo, OG, Wu, D, Willson, T, Hogan, SP, Lima, AA and Guerrant, RL 2011. Alanyl-glutamine promotes intestinal epithelial cell homeostasis in vitro and in a murine model of weanling undernutrition. American Journal of Physiology Gastrointestinal & Liver Physiology 301, G612–G622.CrossRefGoogle Scholar
Wu, G, Meier, SA and Knabe, DA 1996. Dietary glutamine supplementation prevents jejunal atrophy in weaned pigs. Journal of Nutrition 126, 2578–2584.CrossRefGoogle ScholarPubMed
Xi, P, Hong, Y, You, Z, Pei, W and Wang, S 2004. Effects of enteral supplementation with glutamine granules on intestinal mucosal barrier function in severe burned patients. Burns 30, 135–139.Google Scholar
Yi, GF, Carroll, JA, Allee, GL, Gaines, AM, Kendall, DC, Usry, JL, Toride, Y and Izuru, S 2005. Effect of glutamine and spray-dried plasma on growth performance, small intestinal morphology, and immune responses of Escherichia coli K88+-challenged weaned pigs. Journal of Animal Science 83, 634–643.CrossRefGoogle ScholarPubMed
Yin, J, Wu, MM, Xiao, H, Ren, WK, Duan, JL, Yang, G, Li, TJ and Yin, YL 2014. Development of an antioxidant system after early weaning in piglets. Journal of Animal Science 92, 612–619.CrossRefGoogle ScholarPubMed
Zhang, B, Lin, M, Yu, C, Li, J, Zhang, L, Zhou, P, Yang, W, Gao, F and Zhou, G 2016. Alanyl-glutamine supplementation regulates mTOR and ubiquitin proteasome proteolysis signaling pathways in piglets. Nutrition 32, 1123–1131.CrossRefGoogle ScholarPubMed
Zhang, L, Wang, LN, Shi, ZM, Wei, XH, Chen, J and Zhao, RQ 2006. Expression of SGLT1 mRNA in duodenum, jejunum and ileum of weaning piglets and the effect of cysteamine on it. Journal of Agricultural Biotechnology 14, 850–854.Google Scholar
Zhang, S, Yang, Q, Ren, M, Qiao, S, He, P, Li, D and Zeng, X 2016. Effects of isoleucine on glucose uptake through the enhancement of muscular membrane concentrations of GLUT1 and GLUT4 and intestinal membrane concentrations of Na+/glucose co-transporter 1 (SGLT-1) and GLUT2. British Journal of Nutrition 116, 593–602.CrossRefGoogle ScholarPubMed
Zhou, Y, Zhang, P, Deng, G, Liu, X and Lu, D 2012. Improvements of immune status, intestinal integrity and gain performance in the early-weaned calves parenterally supplemented with L-alanyl-L-glutamine dipeptide. Veterinary Immunology & Immunopathology 145, 134–142.CrossRefGoogle ScholarPubMed
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