Aspartate attenuates intestinal injury and inhibits TLR4 and NODs/NF-κB and p38 signaling in weaned pigs after LPS challenge

European Journal of Nutrition

Volumn 56, Issue 4, 2017, Pages 1433-1443

  Wang, Haibo ^a   Liu, Yulan ^a   Shi, Haifeng ^a   Wang, Xiuying ^a   Zhu, Huiling ^a   Pi, Dingan ^a   Leng, Weibo ^a   Li, Shuang ^a  

^a WUHAN POLYTECHNIC UNIVERSITY   (China)

Author keywords

Aspartate; Inflammatory response; Intestine injury; Lipopolysaccharide; Weaned piglets

Indexed keywords

AMINE OXIDASE (COPPER CONTAINING); ASPARTIC ACID; BETA ACTIN; CASPASE 3; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CASPASE RECRUITMENT DOMAIN PROTEIN 4; CLAUDIN 1; COMPLEMENTARY DNA; ESCHERICHIA COLI LIPOPOLYSACCHARIDE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MYELOID DIFFERENTIATION FACTOR 88; NUCLEOTIDE BINDING OLIGOMERIZATION DOMAIN PROTEIN; OCCLUDIN; RECEPTOR INTERACTING PROTEIN SERINE THREONINE KINASE 2; SUPPRESSOR OF CYTOKINE SIGNALING 1; TIGHT JUNCTION PROTEIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; LIPOPOLYSACCHARIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD SAMPLING; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEEDING; ILEUM; IMMUNE RESPONSE; INFLAMMATION; INTESTINE INJURY; INTESTINE MUCOSA; INTRACELLULAR SIGNALING; JEJUNUM; MORPHOLOGY; NONHUMAN; PORCINE MODEL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; SUPPLEMENTATION; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; DRUG EFFECTS; GENETICS; INTESTINE; METABOLISM; PATHOLOGY; PHOSPHORYLATION; PIG; SIGNAL TRANSDUCTION; WEANING;

AMINE OXIDASE (COPPER-CONTAINING); ANIMALS; ASPARTIC ACID; CASPASE 3; DOWN-REGULATION; INTESTINES; LIPOPOLYSACCHARIDES; NF-KAPPA B; NOD SIGNALING ADAPTOR PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RNA, MESSENGER; SIGNAL TRANSDUCTION; SWINE; TOLL-LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR-ALPHA; WEANING;

EID: 84959174382     PISSN: 14366207     EISSN: 14366215     Source Type: Journal    
DOI: 10.1007/s00394-016-1189-x     Document Type: Article

References (44)

1. Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J (2007) Restoration of barrier function in injured intestinal mucosa. Physiol Rev 87:545–564
2. Mitsui T, Fukatsu K, Yanagawa M, Amenomori S, Ogawa E, Fukuda T, Murakoshi S, Moriya T, Yasuhara H, Seto Y (2014) Truncal vagotomy temporarily decreases the pro- and anti-inflammatory cytokine levels in the small intestine. Surg Today 44:1123–1127
3. Wu G, Bazer FW, Davis TA, Jaeger LA, Johnson GA, Kim SW, Knabe DA, Meininger CJ, Spencer TE, Yin Y (2007) Important roles for the arginine family of amino acids in swine nutrition and production. Livest Sci 112:8–22
4. Flynn NE, Knabe DA, Mallick BK, Wu G (2000) Postnatal changes of plasma amino acids in suckling pigs. J Anim Sci 78:2369–2375
5. Pi D, Liu Y, Shi H, Li S, Odle J, Lin X, Zhu H, Chen F, Hou Y, Leng W (2014) Dietary supplementation of Aspartate enhances intestinal integrity and energy status in weanling piglets after lipopolysaccharide challenge. J Nutr Biochem 25:456–462
6. Li P, Yin YL, Li D, Kim SW, Wu G (2007) Amino acids and immune function. Br J Nutr 98:237–252
7. Wu GY, Brosnan JT (1992) Macrophages can convert citrulline into arginine. Biochem J 281:45–48
8. Sukhotnik I, Helou H, Mogilner J, Lurie M, Bernsteyn A, Coran AG, Shiloni E (2005) Oral arginine improves intestinal recovery following ischemia-reperfusion injury in rat. Pediatr Surg Int 21:191–196
9. Zhou X, Wu X, Yin Y, Zhang C, He L (2012) Preventive oral supplementation with glutamine and arginine has beneficial effects on the intestinal mucosa and inflammatory cytokines in endotoxemic rats. Amino Acids 43:813–821
10. Fukata M, Vamadevan AS, Abreu MT (2009) Toll-like receptors (TLRs) and Nod-like receptors (NLRs) in inflammatory disorders. Semin Immunol 21:242–253
11. Uddin MJ, Kaewmala K, Tesfaye D, Tholen E, Looft C, Hoelker M, Schellander K, Cinar MU (2013) Expression patterns of porcine Toll-like receptors family set of genes (TLR1-10) in gut-associated lymphoid tissues alter with age. Res Vet Sci 95:92–102
12. Parlato M, Yeretssian G (2014) NOD-like receptors in intestinal homeostasis and epithelial tissue repair. Int J Mol Sci 15:9594–9627
13. Becker CE, O’Neill LA (2007) Inflammasomes in inflammatory disorders: the role of TLRs and their interactions with NLRs. Semin Immunopathol 29:239–248
14. Xu Y, Liu XD, Gong X, Eissa NT (2008) Signaling pathway of autophagy associated with innate immunity. Autophagy 4:110–112
15. Inohara Chamaillard, McDonald C, Nuñez G (2005) NOD-LRR proteins: role in host-microbial interactions and inflammatory disease. Annu Rev Biochem 74:355–383
16. Doyle A, Zhang G, Abdel Fattah EA, Eissa NT, Li YP (2011) Toll-like receptor 4 mediates lipopolysaccharide-induced muscle catabolism via coordinate activation of ubiquitin-proteasome and autophagy-lysosome pathways. FASEB J 25:99–110
17. 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. Br J Nutr 100:552–560
18. Mair KH, Sedlak C, Käser T, Pasternak A, Levast B, Gerner W, Saalmüller A, Summerfield A, Gerdts V, Wilson HL, Meurens F (2014) The porcine innate immune system: an update. Dev Comp Immunol 45:321–343
19. NRC (1998) Nutrient requirements of swine. 10th edn. National Academic Press, Washington
20. Shi HF, Liu YL, Li S, Zhu HL, Cheng F, Hou YQ, Ding BY, Pi DA, Leng WB (2013) Effect of Aspartic acid on growth performance, blood cell differential count, and blood biochemical measurements of weaned piglets after lipopolysaccharide challenge. China J Anim Sci 7:38–43
21. Liu YL, Li DF, Gong LM, Yi GF, Gaines AM, Carroll JA (2003) Effects of fish oil supplementation on the performance and the immunological, adrenal, and somatotropic responses of weaned pigs after an Escherichia coli lipopolysaccharide challenge. J Anim Sci 81:2758–2765
22. Mercer DW, Smith GS, Cross JM, Russell DH, Chang L, Cacioppo J (1996) Effects of lipopolysaccharide on intestinal injury: potential role of nitricoxide and lipid peroxidation. J Surg Res 63:185–192
23. Luna LG (1968) Manual of histologic staining methods of the armed forces institute of pathology. In: McGraw-Hill Book Company, 3rd edn. New York, pp 258
24. Liu YL, Han J, Huang JJ, Wang XQ, Wang FL, Wang JJ (2009) Dietary l-arginine supplementation improves intestinal function in weaned pigs after an Escherichia coli lipopolysaccharide challenge. Asian-Aust J Anim Sci 22:1667–1675
25. 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
26. Xun W, Shi L, Zhou H, Hou G, Cao T, Zhao C (2015) Effects of curcumin on growth performance, jejunal mucosal membrane integrity, morphology and immune status in weaned piglets challenged with enterotoxigenic Escherichia coli. Int Immunopharmacol 27:46–52
27. Peng X, Yan H, You Z, Wang P, Wang S (2004) Effects of enteral supplementation with glutamine granules on intestinal mucosal barrier function in severe burned patients. Burns 30:135–139
28. Anderson JM, Van Itallie CM (2009) Physiology and function of the tight junction. Cold Spring Harb Perspect Biol 1:a002584
29. Fukudome I, Kobayashi M, Dabanaka K, Maeda H, Okamoto K, Okabayashi T, Baba R, Kumagai N, Oba K, Fujita M, Hanazaki K (2014) Diamine oxidase as a marker of intestinal mucosal injury and the effect of soluble dietary fiber on gastrointestinal tract toxicity after intravenous 5-fluorouracil treatment in rats. Med Mol Morphol 47:100–107
30. Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293
31. Tan B, Yin Y, Kong X, Li P, Li X, Gao H, Li X, Huang R, Wu G (2010) L-Arginine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids 38:1227–1235
32. Hou Y, Wang L, Zhang W, Yang Z, Ding B, Zhu H, Liu Y, Qiu Y, Yin Y, Wu G (2012) Protective effects of N-acetylcysteine on intestinal functions of piglets challenged with lipopolysaccharide. Amino Acids 43:1233–1242
33. Al-Sayeqh AF, Loughlin MF, Dillon E, Mellits KH, Connerton IF (2010) Campylobacter jejuni activates NF-kappaB independently of TLR2, TLR4, Nod1 and Nod2 receptors. Microb Pathog 49:294–304
34. Sabroe I, Parker LC, Dower SK, Whyte MK (2008) The role of TLR activation in inflammation. J Pathol 214:126–135
35. Chen Y, Chen D, Tian G, He J, Mao X, Mao Q, Yu B (2012) Dietary arginine supplementation alleviates immune challenge induced by Salmonella enterica serovar Choleraesuis bacterin potentially through the Toll-like receptor 4-myeloid differentiation factor 88 signalling pathway in weaned piglets. Br J Nutr 108:1069–1076
36. Coll RC, O’Neill LA (2010) New insights into the regulation of signalling by toll-like receptors and nod-like receptors. J Innate Immun 2:406–421
37. Zhang G, Ghosh S (2002) Negative regulation of toll-like receptor-mediated signaling by Tollip. J Biol Chem 277:7059–7065
38. Divanovic S, Trompette A, Atabani SF, Madan R, Golenbock DT, Visintin A, Finberg RW, Tarakhovsky A, Vogel SN, Belkaid Y, Kurt-Jones EA, Karp CL (2005) Negative regulation of Toll-like receptor 4 signaling by the Toll-like receptor homolog RP105. Nat Immunol 6:571–578
39. Mansell A, Smith R, Doyle SL, Gray P, Fenner JE, Crack PJ, Nicholson SE, Hilton DJ, O’Neill LA, Hertzog PJ (2006) Suppressor of cytokine signaling 1 negatively regulates Toll-like receptor signaling by mediating Mal degradation. Nat Immunol 7:148–155
40. McDonald C, Chen FF, Ollendorff V, Ogura Y, Marchetto S, Lécine P, Borg JP, Nuñez G (2005) A role for Erbin in the regulation of Nod2-dependent NF-kappaB signaling. J Biol Chem 280:40301–40309
41. Eitel J, Krüll M, Hocke AC, N’Guessan PD, Zahlten J, Schmeck B, Slevogt H, Hippenstiel S, Suttorp N, Opitz B (2008) Beta-PIX and Rac1 GTPase mediate trafficking and negative regulation of NOD2. J Immunol 181:2664–2671
42. Kondo T, Kawai T, Akira S (2012) Dissecting negative regulation of Toll-like receptor signaling. Trends Immunol 33:449–458
43. Ren W, Chen S, Yin J, Duan J, Li T, Liu G, Feng Z, Tan B, Yin Y, Wu G (2014) Dietary arginine supplementation of mice alters the microbial population and activates intestinal innate immunity. J Nutr 144:988–995
44. Anderson L, Seilhamer J (1997) A comparison of selected mRNA and protein abundances in human liver. Electrophoresis 18:533–537