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Leucine alters immunoglobulin a secretion and inflammatory cytokine expression induced by lipopolysaccharide via the nuclear factor-κB pathway in intestine of chicken embryos

Published online by Cambridge University Press:  22 December 2017

S. Q. Liu ,
L. Y. Wang ,
G. H. Liu ,
D. Z. Tang ,
X. X. Fan ,
J. P. Zhao ,
H. C. Jiao ,
X. J. Wang ,
S. H. Sun  and
H. Lin
S. Q. Liu
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China School of Basic Medical Sciences, Taishan Medical College, Yingsheng East Road No.2, Taian 271016, China
L. Y. Wang
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
G. H. Liu
Affiliation:
School of Basic Medical Sciences, Taishan Medical College, Yingsheng East Road No.2, Taian 271016, China
D. Z. Tang
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
X. X. Fan
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
J. P. Zhao
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
H. C. Jiao
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
X. J. Wang
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
S. H. Sun*
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
H. Lin*
Affiliation:
Department of Animal Science, Shandong Agricultural University, Daizong Street No.61, Taian, Shandong 271018, China
*
†E-mail: [email protected]; [email protected]
†E-mail: [email protected]; [email protected]
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Abstract

The mammalian target of rapamycin (mTOR) has been shown to be involved in lipopolysaccharide (LPS)-induced immune responses in many mammal cells. Here, we suggest that the mTOR pathway is involved in the intestinal inflammatory responses evoked by LPS treatment in chicken embryos. The intestinal tissue from Specific pathogen free chick embryos was cultured in the presence of LPS for 2 h. Secretory immunoglobulin A (sIgA) concentrations, messenger RNA (mRNA) expression of cytokines, and protein levels of nuclear factor-κB (NF-κB), mitogen-activated protein kinase (MAPK), mTOR and p70 ribosomal S6 kinase (p70S6K) were determined. The results showed that LPS treatment increased sIgA concentrations in a dose-dependent manner. The mRNA levels of interleukine (IL)-6, IL-8, IL-10, tumor necrosis factor-α and Toll-like receptor (TLR) 4 were upregulated by LPS treatment (P<0.05). Lipopolysaccharide increased the phosphorylation of Jun N-terminal kinase (JNK), p38 MAPK and NF-κB (P<0.05) while decreasing the phosphorylation level of mTOR (P<0.05). Supplementation of leucine at doses of 10, 20 and 40 mM dose-dependently decreased sIgA production. Leucine supplementation at 40 mM restored the phosphorylation level of mTOR and p70S6K while suppressing the phosphorylation levels of NF-κB (P<0.05) and partially down-regulating the phosphorylation of p38 MAPK and JNK. The transcription of IL-6 was significantly decreased by leucine supplementation. These results suggested that leucine could alleviate LPS-induced inflammatory responses by down-regulating NF-κB signaling pathway and evoking mTOR/p70S6K signaling pathway, which may involve in the regulation of the intestinal immune system in chicken embryos.

Keywords

inflammatory cytokinesecretory immunoglobulin Anuclear factor-κBleucinemammalian target of rapamycin/p70 ribosomal S6 kinase
Type
Research Article
Information
animal , Volume 12 , Issue 9 , September 2018 , pp. 1903 - 1911
Copyright
© The Animal Consortium 2017 

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References

Austenaa, LM, Carlsen, H, Hollung, K, Blomhoff, HK and Blomhoff, R 2009. Retinoic acid dampens LPS-induced NF-kappa B activity results from human monoblasts and in vivo imaging of NF-kappa B reporter mice. The Journal of Nutritional Biochemistry 20, 726–734.Google Scholar
Baker, AK, Wang, R, Mackman, N and Luyendyk, JP 2009. Rapamycin enhances LPS induction of tissue factor and tumor necrosis factor-alpha expression in macrophages by reducing IL-10 expression. Molecular Immunology 46, 2249–2255.Google Scholar
Cario, E, Rosenberg, M, Brandwein, SL, Beck, PL, Reinecker, HC and Podolsky, DK 2000. Lipopolysaccharide activates distinct signaling pathways in intestinal epithelial cell lines expressing Toll-like receptors. Journal of Immunology 164, 966–972.Google Scholar
Cerutti, A and Rescigno, M 2008. The biology of intestinal immunoglobulin A responses. Immunity 28, 740–750.Google Scholar
Ci, X, Ren, R, Xu, K, Li, H, Yu, Q, Song, Y, Wang, D, Li, R and Deng, X 2010. Schisantherin A exhibits anti-inflammatory properties by down-regulating NF-kappa B and MAPK signaling pathways in lipopolysaccharide-treated RAW 264.7 cells. Inflammation 33, 126–136.Google Scholar
Dos Santos, S, Delattre, AI, De Longueville, F, Bult, H and Raes, M 2007. Gene expression profiling of LPS-stimulated murine macrophages and role of the NF-kappa B and PI3K/mTOR signaling pathways. Annals of the New York Academy of Sciences 1096, 70–77.Google Scholar
Duan, Y, Li, F, Li, Y, Tang, Y, Kong, X, Feng, Z, Anthony, TG, Watford, M, Hou, Y, Wu, G and Yin, Y 2016. The role of leucine and its metabolites in protein and energy metabolism. Amino Acids 48, 41–51.Google Scholar
Duchéne, S, Audouin, E, Crochet, S, Duclos, MJ, Dupont, J and Tesseraud, S 2008. Involvement of the ERK1/2 MAPK pathway in insulin-induced S6K1 activation in avian cells. Domestic Animal Endocrinology 34, 63–73.Google Scholar
Fielhaber, JA, Carroll, SF, Dydensborg, AB, Shourian, M, Triantafillopoulos, A, Harel, S, Hussain, SN, Bouchard, M, Qureshi, ST and Kristof, AS 2012. Inhibition of mammalian target of rapamycin augments lipopolysaccharide-induced lung injury and apoptosis. The Journal of Immunology 188, 4535–4542.Google Scholar
Ghosh, S, Tergaonkar, V, Rothlin, CV, Correa, RG, Bottero, V, Bist, P, Verma, IM and Hunter, T 2006. Essential role of tuberous sclerosis genes TSC1 and TSC2 in NF-kappaB activation and cell survival. Cancer Cell 10, 215–226.Google Scholar
Hou, YC, Chiu, WC, Yeh, CL and Yeh, SL 2012. Glutamine modulates lipopolysaccharide-induced activation of NF-κB via the Akt/mTOR pathway in lung epithelial cells. American Journal of Physiology. Lung Cellular and Molecular Physiology 302, L174–L183.Google Scholar
Huang, B, Xiao, D, Tan, B, Xiao, H, Wang, J, Yin, J, Duan, J, Huang, R, Yang, C and Yin, Y 2016. Chitosan oligosaccharide reduces intestinal inflammation that involves calcium-sensing receptor (CaSR) activation in lipopolysaccharide (LPS) -challenged piglets. Journal of Agricultural and Food Chemistry 64, 245–252.Google Scholar
Kogut, MH, Genovese, KJ, He, H and Arsenault, RJ 2016. AMPK and mTOR, sensors and regulators of immunometabolic changes during Salmonella infection in the chicken. Poultry Science 95, 345–353.Google Scholar
Krämer, S, Wang-Rosenke, Y, Scholl, V, Binder, E, Loof, T, Khadzhynov, D, Kawachi, H, Shimizu, F, Diekmann, F, Budde, K, Neumayer, HH and Peters, H 2008. Low-dose mTOR inhibition by rapamycin attenuates progression in anti-thy1-induced chronic glomerulosclerosis of the rat. American journal of physiology. Renal Physiology 294, F440–F449.Google Scholar
Lebman, DA, Lee, FD and Coffman, RL 1990. Mechanism for transforming growth factor beta and IL-2 enhancement of IgA expression in lipopolysaccharide-stimulated B cell cultures. The Journal of Immunology 144, 952–959.Google Scholar
Lin, HY, Chang, KT, Hung, CC, Kuo, CH, Hwang, SJ, Chen, HC, Hung, CH and Lin, SF 2014. Effects of the mTOR inhibitor Rapamycin on Monocyte-Secreted Chemokines. BMC Immunology 15, 37.Google Scholar
Liu, D, Li, P, Song, S, Liu, Y, Wang, Q, Chang, Y, Wu, Y, Chen, J, Zhao, W, Zhang, L and Wei, W 2012. Pro-apoptotic effect of Epigallo-catechin-3-gallate on B lymphocytes through regulating BAFF/PI3K/Akt/mTOR signaling in rats with collagen-induced arthritis. European Journal of Pharmacology 690, 214–225.Google Scholar
Liu, DY, Wang, S, Jiang, T and Ding, P 2013. TNF-ɑ mediated secretory component is positively regulated by PI3K/AKT/mTOR in CACO-2 cells. Bangladesh Journal of Medical Biochemistry 32, 116–120.Google Scholar
Liu, SQ, Zhao, JP, Fan, XX, Liu, GH, Jiao, HC, Wang, XJ, Sun, SH and Lin, H 2015. Rapamycin, a specific inhibitor of the target of rapamycin complex 1, disrupts intestinal barrier integrity in broiler chicks. Journal of Animal Physiology and Animal Nutrition 100, 323–330.Google Scholar
Lu, YC, Yeh, WC and Ohashi, PS 2008. LPS/TLR4 signaling transduction pathway. Cytokine 42, 145–151.Google Scholar
Macpherson, AJ, Gatto, D, Sainsbury, E, Harriman, GR, Hengartner, H and Zinkernagel, RM 2000. A primitive T cell-independent mechanism of intestinal mucosal IgA responses to commensal bacteria. Science 288, 2222–2226.Google Scholar
Mendes, SD, Candi, A, Vansteenbrugge, M, Pignon, MR, Bult, H, Boudjeltia, KZ, Munaut, C and Raes, M 2009. Microarray analyses of the effects of NF-κB or PI3 K pathway inhibitors on the LPS-induced gene expression profile in RAW264.7 cells Synergistic effects of rapamycin on LPS-induced MMP9-over-expression. Cell Signaling 21, 1109–1122.Google Scholar
Moraes, ML, Ribeiro, AM, Santin, E and Klasing, KC 2016. Effects of conjugated linoleic acid and lutein on the growth performance and immune response of broiler chickens. Poultry Science 95, 237–246.Google Scholar
Nemazee, D, Gavin, A, Hoebe, K and Beutler, B 2006. Immunology, Toll-like receptors and antibody responses. Nature 441, E4.Google Scholar
Rhoads, JM, Corl, BA, Harrell, R, Niu, X, Gatlin, L, Phillips, O, Blikslager, A, Moeser, A, Wu, G and Odle, J 2007. Intestinal ribosomal p70 (S6K) signaling is increased in piglet rotavirus enteritis. American journal of physiology. Gastrointestinal and Liver Physiology 292, G913–G922.Google Scholar
Sampson, LL, Davis, AK, Grogg, MW and Zheng, Y 2016. mTOR disruption causes intestinal epithelial cell defects and intestinal atrophy post injury in mice. FASEB Journal 30, 1263–1275.Google Scholar
Sarbassov, DD, Ali, SM and Sabatini, DM 2005. Growing roles for the mTOR pathway. Current Opinion in Cell Biology 17, 596–603.Google Scholar
Schaeffer, V, Arbabi, S, Garcia, IA, Knoll, ML, Cuschieri, J, Bulger, EM and Maier, RV 2011. Role of the mTOR pathway in LPS-activated monocytes, influence of hypertonic saline. The Journal of Surgical Research 171, 769–776.Google Scholar
Sitia, R, Neuberger, MS and Milstein, C 1987. Regulation of membrane IgM expression in secretory B cells: translational and post-translational events. The EMBO Journal 6, 3969–3977.Google Scholar
Tan, B, Yin, YL, Kong, XF, Li, P, Li, XL, Gao, HJ, Li, XG, Huang, RL and Wu, GY 2010. L-Arginine stimulates proliferation and prevents endotoxin-induced death of intestinal cells. Amino Acids 38, 1227–1235.Google Scholar
To, KK, Lau, CC, Woo, PC, Lau, SK, Chan, JF, Chan, KH, Zhang, AJ, Chen, H and Yuen, KY 2016. Human H7N9 virus induces a more pronounced pro-inflammatory cytokine but an attenuated interferon response in human bronchial epithelial cells when compared with an epidemiologically-linked chicken H7N9 virus. Virology Journal. 13, 42.Google Scholar
Wang, XJ, Yang, X, Wang, RX, Jiao, HC, Song, ZG and Lin, H 2016. Leucine alleviates dexamethasone-induced suppression of muscle protein synthesis via synergy involvement of mTOR and AMPK pathways[J]. Bioscience Reports 36, e00346.Google Scholar
Watanabe, H, Kobayashi, K and Isayama, Y 1975. Peculiar secretory IgA system identified in chickens. II. Identification and distribution of free secretory component and immunoglobulins of IgA, IgM, and IgG in chicken external secretions. The Journal of Immunology 115, 998–1001.Google Scholar
Weichhart, T, Costantino, G, Poglitsch, M, Rosner, M, Zeyda, M, Stuhlmeier, KM, Kolbe, T, Stulnig, TM, Hörl, WH, Hengstschläger, M, Müller, M and Säemann, MD 2008. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 29, 565–577.Google Scholar
Wessels, AG, Kluge, H, Hirche, F, Kiowski, A, Schutkowski, A, Corrent, E, Bartelt, J, König, B and Stangl, G 2016. High leucine diets stimulate cerebral branched-chain amino acid degradation and modify serotonin and ketone body concentrations in a pig model. PloS ONE 11, e0150376.Google Scholar
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