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RESEARCH ARTICLE

Protective effects of taurine on growth performance and intestinal epithelial barrier function in weaned piglets challenged without or with lipopolysaccharide

Zhiru Tang A B C , Jinyan Liu A , Zhihong Sun A , Jinlong Li A , Weizhong Sun A , Junxia Mao A and Yao Wang A
+ Author Affiliations
- Author Affiliations

A Key Laboratory for Bio-feed and Animal Nutrition, Southwest University, Chongqing 400715, P. R. China.

B College of Animal Science and Technology, Southwest University, Tiansheng Road 2, Beibei District, Chongqing, 400715, P. R. China.

C Corresponding author. Email: tangzhiru2326@sina.com.cn

Animal Production Science 58(11) 2011-2020 https://doi.org/10.1071/AN16249
Submitted: 19 April 2016  Accepted: 28 May 2017   Published: 23 October 2017

Abstract

We evaluated whether weaned piglets were protected from bacterial endotoxins by placing the animals on a taurine-supplemented diet. A total of 40 weaned Landrace × Yorkshire piglets (5.75 ± 0.58 kg, weaned at 21 days) were allocated to four groups with 10 barrows per group, following a 2 × 2 factorial design with two inclusion levels of lipopolysaccharide (LPS) (no or one time peritoneal injection by the dose of 100 µg/kg bodyweight on Day 7 of the trial) and two inclusion levels of dietary taurine (no or 0.1% taurine in a basal diet in the whole trial). There was a significant interaction between LPS and taurine with regard to growth and small intestinal mucosal membrane integrity, morphology, immune parameters, and antioxidant capacity (P < 0.05). Feed conversion, daily weight gain, daily feed intake, villus height, and the villus to crypt ratio, vascular endothelial growth factor, regenerating islet-derived protein 3 gamma, trefoil factor-3, transforming growth factor β-1 expression, number of goblet cells and the least amount of claudin-1, occludin, zonula occludens-1, serum glutathione peroxidase, nitrogen oxide synthase, superoxide dismutase, peroxidase, and total antioxidant was lowest in LPS-challenged animals. Furthermore, animals in the LPS group had the highest serum diamine oxidase concentration, number of lymphocytes, concentrations of calprotectin, sIgA, toll-like receptor-4, mRNA levels of interleukin-1β, interleukin-8, toll-like receptor-4, and tumour necrosis factor-α (P < 0.05). These data suggested that the peritoneal injection administration of LPS decreased growth performance and disrupted small intestinal mucosal membrane integrity and triggered an inflammatory response in the small intestinal mucosal membrane. Dietary administration of taurine improved growth performance, increased small intestinal villus height, stimulated immune and antioxidant function and improved small intestinal mucosal membrane integrity in weaned piglets challenged without or with LPS (P < 0.05). The beneficial effects of taurine were likely due to decreased stimulation of the immune response to LPS and an improvement in intestinal epithelial barrier function. Dietary administration of taurine could prevent weaned piglets from intestinal damage by LPS of Gram-negative bacteria.

Additional keywords: anti-inflammatory response, antioxidant function, functional amino acid, intestinal health, intestinal mucous membrane integrity.


References

Abraham C, Medzhitov R (2011) Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140, 1729–1737.
Interactions between the host innate immune system and microbes in inflammatory bowel disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlsVGhsL4%3D&md5=b6b57b98ca793f5d8671368a68e4176aCAS |

Berkes J, Viswanathan VK, Savkovic SD, Hecht G (2003) Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation. Gut 52, 439–451.
Intestinal epithelial responses to enteric pathogens: effects on the tight junction barrier, ion transport, and inflammation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1ygurg%3D&md5=72f7b5214ededac161bf77f85ab51a97CAS |

Boudry G, Péron V, Huërou-Luron I, Lallès JP, Sève B (2004) Weaning induces both transient and long-lasting modifications of absorptive, secretory, and barrier properties of piglet intestine. The Journal of Nutrition 134, 2256–2262.

Bustin SA, Benes V, Garson JA, Hellemans J, Huggett J, Kubista M, Mueller R, Nolan T, Pfaffl MW, Shipley GL, Vandesompele J, Wittwer CT (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clinical Chemistry 55, 611–622.
The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXktVWqs7g%3D&md5=ba1d3529679588933be21dd6d4cb6b25CAS |

Cash HL, Whitham CV, Behrendt CL, Hooper LV (2006) Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126–1130.
Symbiotic bacteria direct expression of an intestinal bactericidal lectin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XotlCgtLc%3D&md5=2debe7d2c15f861bc0c984a6a05479a1CAS |

Chen DW, Zhang KY, Wu CY (2008) Influences of lipopolysaccharides-induced immune challenge on performance and whole-body protein turnover in weanling pigs. Livestock Science 113, 291–295.
Influences of lipopolysaccharides-induced immune challenge on performance and whole-body protein turnover in weanling pigs.Crossref | GoogleScholarGoogle Scholar |

Costa F, Mumolo MG, Ceccarelli L, Bellini M, Romano MR, Sterpi C, Ricchiuti A, Marchi S, Bottai M (2005) Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn’s disease. Gut 54, 364–368.
Calprotectin is a stronger predictive marker of relapse in ulcerative colitis than in Crohn’s disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXisFCqtbY%3D&md5=80d31a179b2c4533cf4c8ec19e15c79fCAS |

Deng H, Xu L, Tang ZR, Lai X, Xiao DH, Shi BS, Zhang XL, Sun ZH, Zhang Z, Sun WZ (2014) Effects of orally administered Escherichia coli Nissle 1917 on growth performance and jejunal mucosal membrane integrity, morphology, immune parameters and antioxidant capacity in early weaned piglets. Animal Feed Science and Technology 198, 286–294.
Effects of orally administered Escherichia coli Nissle 1917 on growth performance and jejunal mucosal membrane integrity, morphology, immune parameters and antioxidant capacity in early weaned piglets.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhvVGisbvK&md5=95573fbe96ffd3d61f4c91141f16330bCAS |

Desaldeleer C, Ferret-Bernard S, de Quelen F, Le Normand L, Perrier C, Savary G, Romé V, Michel C, Mourot J, Le Huërou-Luron I, Boudry G (2014) Maternal 18:3n-3 favors piglet intestinal passage of LPS and promotes intestinal-anti-inflammatory response to this bacterial ligand. The Journal of Nutritional Biochemistry 25, 1090–1098.
Maternal 18:3n-3 favors piglet intestinal passage of LPS and promotes intestinal-anti-inflammatory response to this bacterial ligand.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Oqs7nP&md5=6cef0128188ad9244371cfdbe4baae4fCAS |

Ferrara N, Gerber HP, LeCouter J (2003) The biology of VEGF and its receptors. Nature Medicine 9, 669–676.
The biology of VEGF and its receptors.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXktFOnur4%3D&md5=0f3010469f5e4d403d3387c8cf5fc947CAS |

Gironella M, Iovanna JL, Sans M, Gil F, Peñalva M, Closa D, Piqué JM, Panés J (2005) Anti-inflammatory effects of pancreatitis associated protein in inflammatory bowel disease. Gut 54, 1244–1253.
Anti-inflammatory effects of pancreatitis associated protein in inflammatory bowel disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVegsrvJ&md5=3ec6f097e41629140df1ad60e00d9ba9CAS |

Gu X, Li D, She R (2002) Effect of weaning on small intestinal structure and function in the piglet. Archives of Animal Nutrition 56, 275–286.

Gurujeyalakshmi G, Wang YJ, Giri SN (2000) Suppression of bleomycin-induced nitric oxide production in mice by taurine and niacin. Nitric Oxide 4, 399–411.
Suppression of bleomycin-induced nitric oxide production in mice by taurine and niacin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXls1CnsLc%3D&md5=fb29d19e2805ec9d6a6c067714e1d567CAS |

Heuer OE, Hammerum AM, Collignon P, Wegener HC (2006) Human health hazard from antimicrobial-resistant enterococci in animals and food. Clinical Infectious Diseases 43, 911–916.
Human health hazard from antimicrobial-resistant enterococci in animals and food.Crossref | GoogleScholarGoogle Scholar |

Jeon SH, Lee MY, Rahman MM, Kim SJ, Kim GB, Park SY, Hong CU, Kim SZ, Kim JS, Kang HS (2009) The antioxidant, taurine reduced lipopolysaccharide (LPS)-induced genera of ROS, and activation of MAPKs and Bax in cultured pneumocytes. Pulmonary Pharmacology & Therapeutics 22, 562–566.
The antioxidant, taurine reduced lipopolysaccharide (LPS)-induced genera of ROS, and activation of MAPKs and Bax in cultured pneumocytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlCnu7nJ&md5=fb123562992bbe945ac51dd8e8fa125cCAS |

Jepson MM, Pell JM, Bates PC, Millward DJ (1986) The effects of endotoxameia on protein metabolism in skeletal muscle and liver of fed and fasted rats. The Biochemical Journal 235, 329–336.
The effects of endotoxameia on protein metabolism in skeletal muscle and liver of fed and fasted rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XhvVChtr8%3D&md5=d644a6e678d4443263195b08c346bb07CAS |

Kido J, Kido R, Suryono KM, Fagerhol MK, Nagata T (2003) Calprotectin release from human neutrophils is induced by porphyromonas gingivalis lipopolysaccharide via the CD14-Toll-like receptor-nuclear factor kappa B pathway. Journal of Periodontal Research 38, 557–563.
Calprotectin release from human neutrophils is induced by porphyromonas gingivalis lipopolysaccharide via the CD14-Toll-like receptor-nuclear factor kappa B pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtVSqsL%2FF&md5=ccc10781ad3c8ec55ae991fe88184e62CAS |

Kim JW, Kim C (2005) Inhibition of LPS-induced NO production by taurine chloramine in macrophages is mediated though Ras-ERK-NF-kB. Biochemical Pharmacology 70, 1352–1360.
Inhibition of LPS-induced NO production by taurine chloramine in macrophages is mediated though Ras-ERK-NF-kB.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVKjs7bN&md5=8d8b0a038d6682867583e08ff636920fCAS |

Lackeyram D, Archbold T, Shoveller AK, Mine Y, Fan MZ (2007) Gut carbohydrate digestive enzymes respond differentially to oxidative stress induced by in vivo infusion of hydrogen peroxide (H2O2) in formula-fed piglets. The FASEB Journal 21, A1076

Lee DN, Cheng YH, Chuang YS, Shiv J, Lian YM, Wei HW, Weng CF (2004) Effects of dietary taurine supplementation on growth performance, serum constituents and antibody production of broilers. Asian Aust. Journal of Animal Science 17, 109–115.

Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. British Journal of Nutrition 98, 237–252.
Amino acids and immune function.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsFentrg%3D&md5=b2fa74ba78aa0430b8b843b9354d6119CAS |

Liu Y, Huang J, Hou Y, Zhu H, Zhao S, Ding B, Yin Y, Yi G, Shi J, Fan W (2008) Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. British Journal of Nutrition 100, 552–560.
Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht1Snt77F&md5=756ab8b4eda3a7009d79b82b75045c5bCAS |

Liu Y, Mao XB, Yu B, He J, Zheng P, Yu J, Luo JQ, Chen DW (2014) Excessive dietary taurine supplementation reduces growth performance, liver and intestinal health of weaned pigs. Livestock Science 168, 109–119.
Excessive dietary taurine supplementation reduces growth performance, liver and intestinal health of weaned pigs.Crossref | GoogleScholarGoogle Scholar |

Ma TY (1997) Intestinal epithelial barrier dysfunction in Crohn’s disease. Proceedings of the Society for Experimental Biology and Medicine 214, 318–327.
Intestinal epithelial barrier dysfunction in Crohn’s disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXislynu7s%3D&md5=e52cb472aab0ce12e4d10ad84a8cf7e4CAS |

McLamb BL, Gibson AJ, Overman EL, Stahl C, Moeser AJ (2013) Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli Challenge and exacerbates intestinal injury and clinical disease. PLoS One 8, e59838
Early weaning stress in pigs impairs innate mucosal immune responses to enterotoxigenic E. coli Challenge and exacerbates intestinal injury and clinical disease.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFalt78%3D&md5=e928bcc41f30671a6cec39b90449c768CAS |

Mochizuki T, Satsu H, Nakano T, Shimizu M (2004) Regulation of the human taurine transporter by TNF-α and an anti-inflammatory function of taurine in human intestinal Caco-2 cells. Biology Factors 21, 141–144.

Montagne L, Pluske JR, 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. Animal Feed Science and Technology 108, 95–117.
A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals.Crossref | GoogleScholarGoogle Scholar |

NRC (2012) ‘Nutrient requirements of swine.’ 11th edn. (National Academies Press: Washington, DC)

Sies H (1993) Strategies of antioxidant defense. European Journal of Biochemistry 215, 213–219.
Strategies of antioxidant defense.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXltlKms7w%3D&md5=25388b7f853aea2aeb8a1a69a62bea32CAS |

Simonovic I, Rosenberg J, Koutsouris A, Hecht G (2000) Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cellular Microbiology 2, 305–315.
Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXmtFOrsr8%3D&md5=bdd3221d67189f69439a765ee2c549f1CAS |

Son MW, Ko J, Doh HM, Kim WB, Park TS, Shim MJ, Kim BK (1998) Protective effect of taurine on TNBS-induced inflammatory bowel disease in rats. Archive Pharmacology Reseach 21, 531–536.
Protective effect of taurine on TNBS-induced inflammatory bowel disease in rats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXms1ekt7o%3D&md5=e7e6e40856d10d2b0a07e8c22906514eCAS |

Šplíchal I, Fagerhol MK, Trebichavský I, Šplíchalová A, Schulze J (2005) The effect of intestinal colonization of germ-free pigs with Escherichia coli on calprotectin levels in plasma, intestinal and bronchoalveolar lavages. Immunity 209, 681–687.

Tsuchioka T, Fujiwara T, Sunagawa M (2006) Effects of glutamic acid and taurine on total parenteral nutrition. Journal of Pediatric Surgery 41, 1566–1572.
Effects of glutamic acid and taurine on total parenteral nutrition.Crossref | GoogleScholarGoogle Scholar |

Venkatesha S, Toporsian M, Lam C, Hanai J, Mammoto T, Kim YM, Bdolah Y, Lim KH, Yuan HT, Libermann TA, Stillman IE, Roberts D, D’Amore PA, Epstein FH, Sellke FW, Romero R, Sukhatme VP, Letarte M, Karumanchi SA (2006) Soluble endoglin contributes to the pathogenesis of preeclampsia. Nature Medicine 12, 642–649.
Soluble endoglin contributes to the pathogenesis of preeclampsia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltlOjtrs%3D&md5=00f01a6d1a991397c71810df4369ef60CAS |

Wang J, Chen L, Li P, Li X, Zhou H, Wang F, Li D, Yin Y, Wu G (2008) Gene expression is altered in piglet small intestine by weaning and dietary glutamine supplementation. The Journal of Nutrition 138, 1025–1032.

Wannemacher RW (1977) Key role of various individual amino acids in host response to infection. Journal of Clinic Nutrition 30, 1269–1280.

Xiao DF, Wang YF, Liu G, He JH, Qiu W, Hu XG, Feng ZM, Ran ML, Charles MN, Sung WK, Tang ZR, Yin YL (2014) Effects of chitosan on intestinal inflammation in weaned pigs challenged by enterotoxigenic Escherichia coli. PLoS One 9, e104192
Effects of chitosan on intestinal inflammation in weaned pigs challenged by enterotoxigenic Escherichia coli.Crossref | GoogleScholarGoogle Scholar |

Yamachika T, Werther JL, Bodian C, Babyatsky M, Tatematsu M, Yamamura Y, Chen A, Itzkowitz S (2002) Intestinal trefoil factor: a marker of poor prognosis in gastric carcinoma. Clinical Cancer Research 8, 1092–1099.