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Effect of Zinc Supplementation on Growth Performance, Intestinal Development, and Intestinal Barrier-Related Gene Expression in Pekin Ducks

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Abstract

The current study was conducted to investigate the effect of zinc supplementation on the growth performance, intestinal morphology, and the transcription of the barrier function related genes in Pekin ducks. Seven-hundred and sixty-eight 1-day-old Pekin ducks were randomly assigned into six dietary treatments. Each treatment had eight replicates with 16 ducks per replicates. The ducks were fed either a corn-soybean meal basal diet or basal diets supplemented with 15, 30, 60, 120, and 240 mg zinc/kg from zinc sulfate. This experiment lasted for 5 weeks, and the jejunum sample were harvested at 14 and 35 days of age. Results have shown that diets supplemented with zinc significantly increased the duck body weight, average daily gain, and average daily feed intake in different period of experiment (P < 0.05); feed to gain ratio was decreased as the zinc level increased (P < 0.05). Zinc supplementation increased the villus height and decreased the crypt depth in jejunum of ducks (P < 0.05) at 14 and 35 days of age. The transcription of tight junction protein CLDN1, OCND, ZO-1, and ZO-3 in jejunum were increased (P < 0.05), and the messenger RNA (mRNA) levels of leak protein CLDN2 were decreased as the dietary zinc level increased (P < 0.05) at 14 and 35 days of age. The mRNA levels of chemical barrier-related genes MUC2 and TFF-2 in jejunum at 14 and 35 days of age were increased (P < 0.05) by zinc supplementation, and so did the transcription of immunological barrier-related genes lgA, pIgR, LYZ, and AvBD2 (P < 0.05). In conclusion, dietary zinc supplementation exhibited growth-promoting effect on Pekin duck, improved intestinal morphology, and enhanced the intestinal barrier integrity.

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References

  1. Andreini C, Banci L, Bertini I et al (2006) Counting the zinc-proteins encoded in the human genome. J Proteome Res 5:196–201

    CAS  PubMed  Google Scholar 

  2. Andreini C, Bertini I (2012) A bioinformatics view of zinc enzymes. J Inorg Biochem 111:150–156

    CAS  PubMed  Google Scholar 

  3. Salim HM, Jo C, Lee BD (2008) Zinc in broiler feeding and nutrition. Avian Biol Res 1:5–18

    Google Scholar 

  4. Feng J, Ma WQ, Niu HH et al (2010) Effects of zinc glycine chelate on growth, hematological, and immunological characteristics in broilers. Biol Trace Elem Res 133:203–211

    CAS  PubMed  Google Scholar 

  5. Liu ZH, Lu L, Li SF et al (2011) Effects of supplemental zinc source and level on growth performance, carcass traits, and meat quality of broilers. Poult Sci 90:1782–1790

    CAS  PubMed  Google Scholar 

  6. Zhang B, Shao Y, Liu D et al (2012) Zinc prevents Salmonella enterica serovar typhimurium-induced loss of intestinal mucosal barrier function in broiler chickens. Avian Pathol 41:361–367

    CAS  PubMed  Google Scholar 

  7. Wu LY, Fang YJ, Guo XY (2011) Dietary L-arginine supplementation beneficially regulates body fat deposition of meat-type ducks. Br Poult Sci 52:221–226

    CAS  PubMed  Google Scholar 

  8. Cui H, ** P, Junliang D et al (2004) Pathology of lymphoid organs in chickens fed a diet deficient in zinc. Avian Pathol 33:519–524

    CAS  PubMed  Google Scholar 

  9. Wight PA, Dewar WA (1976) The histopathology of zinc deficiency in ducks. Avian Pathol 120:183–191

    CAS  Google Scholar 

  10. Cui H, **g F, ** P (2003) Pathology of the thymus, spleen and bursa of Fabricius in zinc-deficient ducklings. Avian Pathol 32:259–264

    PubMed  Google Scholar 

  11. Applegate T, Karcher D, Lilburn M (2005) Comparative development of the small intestine in the turkey poult and Pekin duckling. Poult Sci 84:426–431

    CAS  PubMed  Google Scholar 

  12. Halpern MD, Denning PW (2015) The role of intestinal epithelial barrier function in the development of NEC. Tissue Barriers 3:e1000707

    PubMed  PubMed Central  Google Scholar 

  13. Vereecke L, Beyaert R, Van Loo G (2011) Enterocyte death and intestinal barrier maintenance in homeostasis and disease. Trends Mol Med 17:584–593

    CAS  PubMed  Google Scholar 

  14. Zhu C, Lv H, Chen Z et al (2016) Dietary zinc oxide modulates antioxidant capacity, small intestine development, and jejunal gene expression in weaned piglets. Biol Trace Elem Res 175:331–338

    PubMed  Google Scholar 

  15. Han XY, Ma YF, Lv MY et al (2014) Chitosan-zinc chelate improves intestinal structure and mucosal function and decreases apoptosis in ileal mucosal epithelial cells in weaned pigs. Br J Nutr 111:1405–1411

    CAS  PubMed  Google Scholar 

  16. Shao Y, Lei Z, Yuan J et al (2014) Effect of zinc on growth performance, gut morphometry, and cecal microbial community in broilers challenged with Salmonella enterica serovar typhimurium. J Microbiol 52:1002–1011

    CAS  PubMed  Google Scholar 

  17. Hu CH, Qian ZC, Song J et al (2013) Effects of zinc oxide-montmorillonite hybrid on growth performance, intestinal structure, and function of broiler chicken. Poult Sci 92:143–150

    CAS  PubMed  Google Scholar 

  18. Zhang BK, Guo YM (2009) Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Br J Nutr 102:687

    CAS  PubMed  Google Scholar 

  19. Wang X, Valenzano MC, Mercado JM et al (2013) Zinc supplementation modifies tight junctions and alters barrier function of CACO-2 human intestinal epithelial layers. Dig Dis Sci 58:77–87

    PubMed  Google Scholar 

  20. Wang X, Valenzano MC, Mercado JM et al (2014) Zinc enhancement of LLC-PK(1) renal epithelial barrier function. Clin Nutr 33:280–286

    CAS  PubMed  Google Scholar 

  21. Ranaldi G, Caprini V, Sambuy Y et al (2009) Intracellular zinc stores protect the intestinal epithelium from ochratoxin A toxicity. Toxicol in Vitro 23:1516–1521

    CAS  PubMed  Google Scholar 

  22. Liberato SC, Singh G, Mulholland K (2015) Zinc supplementation in young children: a review of the literature focusing on diarrhoea prevention and treatment. Clin Nutr 34:181–188

    CAS  PubMed  Google Scholar 

  23. Zeng QF, Yang GL, Liu GN et al (2014) Effects of dietary gossypol concentration on growth performance, blood profiles, and hepatic histopathology in meat ducks. Poult Sci 93:2000–2009

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−delta delta C(T)) method. Methods 25:402–408

    CAS  PubMed  Google Scholar 

  25. Wight PA (1977) The ultrastructure of the interdigital web in experimental zinc deficiency of ducks. Avian Pathol 6:111–124

    CAS  PubMed  Google Scholar 

  26. Roberson RH, Schaible PJ (1960) The tolerance of growing chicks for high levels of different forms of zinc. Poult Sci 39:893–896

    CAS  Google Scholar 

  27. Southon S, Livesey G, Gee JM et al (1985) Intestinal cellular proliferation and protein synthesis in zinc-deficient rats. Br J Nutr 53:595

    CAS  PubMed  Google Scholar 

  28. Park JH, Grandjean CJ (1986) Effects of isolated zinc deficiency on the composition of skeletal muscle, liver and bone during growth in rats. J Nutr 116:610–617

    CAS  PubMed  Google Scholar 

  29. Macdonald RS, Hambidge M, Cousins RJ et al (2000) The role of zinc in growth and cell proliferation. J Nutr 130:1500S–1508S

    CAS  PubMed  Google Scholar 

  30. Laron Z (2001) Insulin-like growth factor 1 (IGF-1): a growth hormone. Mol Pathol 54:311–316

    CAS  PubMed  PubMed Central  Google Scholar 

  31. Mcnall AD, Etherton TD, Fosmire GJ (1995) The impaired growth induced by zinc deficiency in rats is associated with decreased expression of the hepatic insulin-like growth factor I and growth hormone receptor genes. J Nutr 125:874–879

    CAS  PubMed  Google Scholar 

  32. Ninh NX, Thissen JP, Maiter D et al (1995) Reduced liver insulin-like growth factor-I gene expression in young zinc-deprived rats is associated with a decrease in liver growth hormone (GH) receptors and serum GH-binding protein. J Endocrinol 144:449–456

    CAS  PubMed  Google Scholar 

  33. Xu ZR, Hu CH, **a MS et al (2003) Effects of dietary fructooligosaccharide on digestive enzyme activities, intestinal microflora and morphology of male broilers. Poult Sci 82:1030–1036

    CAS  PubMed  Google Scholar 

  34. Ma W, Niu H, Feng J et al (2010) Effects of zinc glycine chelate on oxidative stress, contents of trace elements, and intestinal morphology in broilers. Biol Trace Elem Res 142:546–556

    PubMed  Google Scholar 

  35. Lawson MJ, Butler RN, Goland GJ et al (1988) Zinc deficiency is associated with suppression of colonocyte proliferation in the distal large bowel of rats. Biol Trace Elem Res 18:115–121

    CAS  PubMed  Google Scholar 

  36. Duff M, Ettarh R (2002) Crypt cell production rate in the small intestine of the zinc-supplemented mouse. Cells Tissues Organs 172:21

    CAS  PubMed  Google Scholar 

  37. Yegani M, Korver DR (2008) Factors affecting intestinal health in poultry. Poult Sci 87:2052–2063

    CAS  PubMed  Google Scholar 

  38. Anderson RC, Dalziel JE, Gopal PK et al (2012) The role of intestinal barrier function in early life in the development of colitis. INTECH:67–74

  39. Peterson LW, Artis D (2014) Intestinal epithelial cells: regulators of barrier function and immune homeostasis. Nat Rev Immunol 14:141–153

    CAS  PubMed  Google Scholar 

  40. Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cell Mol Life Sci 70:631–659

    CAS  PubMed  Google Scholar 

  41. Hu CH, Song ZH, **ao K et al (2014) Zinc oxide influences intestinal integrity, the expressions of genes associated with inflammation and TLR4-myeloid differentiation factor 88 signaling pathways in weanling pigs. Innate Immun 20:478–486

    PubMed  Google Scholar 

  42. Pearce SC, Sanz Fernandez MV, Torrison J et al (2015) Dietary organic zinc attenuates heat stress-induced changes in pig intestinal integrity and metabolism. J Anim Sci 93:4702

    CAS  PubMed  Google Scholar 

  43. Wada M, Tamura A, Takahashi N et al (2013) Loss of claudins 2 and 15 from mice causes defects in paracellular Na+ flow and nutrient transport in gut and leads to death from malnutrition. Gastroenterology 144:369–380

    CAS  PubMed  Google Scholar 

  44. Rosenthal R, Milatz S, Krug SM et al (2010) Claudin-2, a component of the tight junction, forms a paracellular water channel. J Cell Sci 123:1913

    CAS  PubMed  Google Scholar 

  45. Luettig J, Rosenthal R, Barmeyer C et al (2015) Claudin-2 as a mediator of leaky gut barrier during intestinal inflammation. Tissue Barriers 3:e977176

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Mcguckin MA, Lindén SK, Sutton P et al (2011) Mucin dynamics and enteric pathogens. Nat Rev Microbiol 9:265–278

    CAS  PubMed  Google Scholar 

  47. Johansson ME, Hansson GC (2016) Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol 16:639–649

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Bobíková K, Levkut M, Husáková E et al (2016) Effect of glycine-zinc complex on mucin and IgA expression, secretory IgA concentration and lengths of intestinal villi in chickens. J Comp Pathol 154:81

    Google Scholar 

  49. Jiang Z, Lossie AC, Applegate TJ (2011) Evolution of trefoil factor(s): genetic and spatio-temporal expression of trefoil factor 2 in the chicken (Gallus gallus domesticus). PLoS One 6:e22691

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Tran CP, Cook GA, Yeomans ND et al (1999) Trefoil peptide TFF2 (spasmolytic polypeptide) potently accelerates healing and reduces inflammation in a rat model of colitis. Gut 44:636–642

    CAS  PubMed  PubMed Central  Google Scholar 

  51. Ando K, Fujiya M, Konishi H et al (2015) Heterogeneous nuclear ribonucleoprotein A1 improves the intestinal injury by regulating apoptosis through trefoil factor 2 in mice with anti-CD3-induced enteritis. Inflamm Bowel Dis 21:1541–1552

    PubMed  Google Scholar 

  52. Pabst O (2012) New concepts in the generation and functions of IgA. Nat Rev Immunol 12:821–832

    CAS  PubMed  Google Scholar 

  53. Spencer J, Klavinskis LS, Fraser LD (2012) The human intestinal IgA response; burning questions. Front Immunol 3:108

    PubMed  PubMed Central  Google Scholar 

  54. Shimada S, Kawaguchi-Miyashita M, Kushiro A et al (1999) Generation of polymeric immunoglobulin receptor-deficient mouse with marked reduction of secretory IgA. J Immunol 163:5367–5373

    CAS  PubMed  Google Scholar 

  55. Bevins CL, Salzman NH (2011) Paneth cells, antimicrobial peptides and maintenance of intestinal homeostasis. Nat Rev Microbiol 9:356–368

    CAS  PubMed  Google Scholar 

  56. Sawada M, Takahashi K, Sawada S et al (1991) Selective killing of Paneth cells by intravenous administration of dithizone in rats. Int J Clin Exp Pathol 72:407

    CAS  Google Scholar 

  57. Geiser J, Venken K, De Lisle RC et al (2012) A mouse model of Acrodermatitis enteropathica: loss of intestine zinc transporter ZIP4 (Slc39a4) disrupts the stem cell niche and intestine integrity. PLoS Genet 8:e1002766

    PubMed  PubMed Central  Google Scholar 

  58. Liu P, Pieper R, Tedin L et al (2014) Effect of dietary zinc oxide on jejunal morphological and immunological characteristics in weaned piglets. J Anim Sci 92:5009–5018

    CAS  PubMed  Google Scholar 

  59. Mao X, Qi S, Yu B et al (2013) Zn(2+) and L-isoleucine induce the expressions of porcine beta-defensins in IPEC-J2 cells. Mol Biol Rep 40:1547–1552

    CAS  PubMed  Google Scholar 

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Acknowledgements

The present study was financially supported by the Science and Technology Support Program of Sichuan Province (Grant No. 2013NZ0054), and the research funding was also provided by Sichuan Longda Animal Husbandry Science and Technology Co., Ltd. (No. 009H2200).

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Authors and Affiliations

  1. Animal Nutrition Institute, Sichuan Agricultural University, No. 211 Huimin Road, Wenjiang, Chengdu, Sichuan, 611130, China

    Min Wen, Hua Zhao, Guangmang Liu, **aoling Chen, Gang Tian, **gyi Cai & Gang Jia

  2. Tibet Vocational Technical College, Lasa, 850000, China

    Min Wen

  3. Chelota Group, Guanghan, 618300, China

    Bing Wu

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  1. Min Wen
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  2. Hua Zhao
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  3. Guangmang Liu
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  7. **gyi Cai
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  8. Gang Jia
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Correspondence to Gang Jia.

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Wen, M., Zhao, H., Liu, G. et al. Effect of Zinc Supplementation on Growth Performance, Intestinal Development, and Intestinal Barrier-Related Gene Expression in Pekin Ducks. Biol Trace Elem Res 183, 351–360 (2018). https://doi.org/10.1007/s12011-017-1143-7

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  • DOI: https://doi.org/10.1007/s12011-017-1143-7

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