Dietary sodium butyrate protects lipopolysaccharide-induced inflammatory response in lambs through inhibiting TLR4/NF-κB signalling pathway

References

• Aschenbach JR, Ahrens F, Schwelberger HG, Furll B, Roesler U, Hensel A, Gabel G. 2007. Functional characteristics of the porcine colonic epithelium following transportation stress and Salmonella infection. Scand J Gastroenterol. 42(6):708–716.
   PubMed Web of Science ®Google Scholar
• Baumler AJ, Sperandio V. 2016. Interactions between the microbiota and pathogenic bacteria in the gut. Nature. 535(7610):85–93.
   PubMed Web of Science ®Google Scholar
• Biagi G, Piva A, Moschini M, Vezzali E, Roth FX. 2007. Performance, intestinal microflora, and wall morphology of weanling pigs fed sodium butyrate. J Anim Sci. 85(5):1184–1191.
   PubMed Web of Science ®Google Scholar
• Blikslager AT, Moeser AJ, Gookin JL, Jones SL, Odle J. 2007. Restoration of barrier function in injured intestinal mucosa. Physiol Rev. 87(2):545–564.
   PubMed Web of Science ®Google Scholar
• Bruewer M, Luegering A, Kucharzik T, Parkos CA, Madara JL, Hopkins AM, Nusrat A. 2003. Proinflammatory cytokines disrupt epithelial barrier function by apoptosis-independent mechanisms. J Immunol. 171(11):6164–6172.
   PubMed Web of Science ®Google Scholar
• Calderón-Pérez L, Gosalbes M, Yuste S, Valls R, Pedret A, Llauradó E, Jimenez-Hernandez N, Artacho A, Pla-Pagà L, Companys J, et al. 2020. Gut metagenomic and short chain fatty acids signature in hypertension: a cross-sectional study. Sci Rep. 10(1):6436.
   PubMed Web of Science ®Google Scholar
• Chang G, Yan J, Ma N, Liu X, Dai H, Bilal MS, Shen X. 2018. Dietary sodium butyrate supplementation reduces high-concentrate diet feeding-induced apoptosis in mammary cells in dairy goats. J Agric Food Chem. 66(9):2101–2107.
   PubMed Web of Science ®Google Scholar
• Chen J, Vitetta L. 2018. Inflammation-modulating effect of butyrate in the prevention of colon cancer by dietary fiber. Clin Colorectal Canc. 17:541–544.
   PubMed Web of Science ®Google Scholar
• Chen L, Li S, Zheng J, Li W, Jiang X, Zhao X, Li J, Che L, Lin Y, Xu S. 2018. Effects of dietary Clostridium butyricum supplementation on growth performance, intestinal development, and immune response of weaned piglets challenged with lipopolysaccharide. J Anim Sci Biotechnol. 9(1):1–14.
   PubMedGoogle Scholar
• Chen Y, Zhang H, Cheng Y, Li Y, Wen C, Zhou Y. 2018. Dietary l-threonine supplementation attenuates lipopolysaccharide-induced inflammatory responses and intestinal barrier damage of broiler chickens at an early age. Br J Nutr. 119(11):1254–1262.
   PubMed Web of Science ®Google Scholar
• Creevey CJ, Kelly WJ, Henderson G, Leahy SC. 2014. Determining the culturability of the rumen bacterial microbiome. Microb Biotechnol. 7(5):467–479.
   PubMed Web of Science ®Google Scholar
• Crost EH, Tailford LE, Gall GL, Fons M, Henrissat B, Juge N. 2013. Utilisation of mucin glycans by the human gut symbiont Ruminococcus gnavus is strain-dependent. PLoS One. 8(10):e76341.
   PubMed Web of Science ®Google Scholar
• Den Besten G, Van Eunen K, Groen AK, Venema K, Reijngoud D, Bakker BM. 2013. The role of short-chain fatty acids in the interplay between diet, gut microbiota, and host energy metabolism. J Lipid Res. 54(9):2325–2340.
   PubMed Web of Science ®Google Scholar
• Dengler F, Rackwitz R, Benesch F, Pfannkuche H, Gabel G. 2015. Both butyrate incubation and hypoxia upregulate genes involved in the ruminal transport of SCFA and their metabolites. J Anim Physiol Anim Nutr. 99(2):379–390.
   PubMed Web of Science ®Google Scholar
• Feng W, Wu Y, Chen G, Fu S, Li B, Huang B, Wang D, Wang W, Liu J. 2018. Sodium butyrate attenuates diarrhea in weaned piglets and promotes tight junction protein expression in colon in a GPR109A-dependent manner. Cell Physiol Biochem. 47(4):1617–1629.
   PubMedGoogle Scholar
• Gao Q, Zhu H, Dong L, Shi W, Chen R, Song Z, Huang C, Li J, Dong X, Zhou Y, et al. 2019. Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell. 179(5):1240.
   PubMed Web of Science ®Google Scholar
• Gensollen T, Iyer SS, Kasper DL, Blumberg RS. 2016. How colonization by microbiota in early life shapes the immune system. Science. 352(6285):539–544.
   PubMed Web of Science ®Google Scholar
• Ghosh SS, Wang J, Yannie PJ, Ghosh S. 2020. Intestinal barrier dysfunction, LPS translocation, and disease development. J Endocr SoC. 4(2):1–15.
   Web of Science ®Google Scholar
• Gong Q, He L, Wang M, Zuo S, Gao H, Feng Y, Du L, Luo Y, Li J. 2019. Comparison of the TLR4/NFκB and NLRP3 signalling pathways in major organs of the mouse after intravenous injection of lipopolysaccharide. Pharm Biol. 57(1):555–563.
   PubMed Web of Science ®Google Scholar
• Górka P, Śliwiński B, Flaga J, Olszewski J, Nawrocka P, Sobkowiak K, Miltko R, Godlewski MM, Zabielski R, Kowalski ZM. 2018. Effect of exogenous butyrate on the gastrointestinal tract of sheep. II. Hydrolytic activity in the rumen and structure and function of the small intestine. J Anim Sci. 96(12):5325–5335.
   PubMed Web of Science ®Google Scholar
• Guo J, Wang Y, Jiang P, Yao H, Zhao C, Hu X, Cao Y, Zhang N, Fu Y, Shen H. 2019. Sodium butyrate alleviates lipopolysaccharide-induced endometritis in mice through inhibiting inflammatory response. Microb Pathog. 137:103792.
   PubMed Web of Science ®Google Scholar
• Dai H, Liu X, Yan J, Aabdin ZU, Bilal MS, Shen X. 2017. Sodium butyrate ameliorates high-concentrate diet-induced inflammation in the rumen epithelium of dairy goats. J Agric Food Chem. 65(3):596–604.
   PubMed Web of Science ®Google Scholar
• Horioka K, Tanaka H, Isozaki S, Konishi H, Fujiya M, Okuda K, Asari M, Shiono H, Ogawa K, Shimizu K. 2020. Acute colchicine poisoning causes endotoxemia via the destruction of intestinal barrier function: the curative effect of endotoxin prevention in a murine model. Dig Dis Sci. 65(1):132–140.
   PubMed Web of Science ®Google Scholar
• Hou Y, Wang L, Yi D, Ding B, Yang Z, Li J, Chen X, Qiu Y, Wu G. 2013. N-acetylcysteine reduces inflammation in the small intestine by regulating redox, EGF and TLR4 signaling. Amino Acids. 45(3):513–522.
   PubMed Web of Science ®Google Scholar
• Jin X, Zhang M, Yang Y. 2019. Saccharomyces cerevisiae β-glucan-induced SBD-1 expression in ovine ruminal epithelial cells is mediated through the TLR-2-MyD88-NF-κB/MAPK pathway. Vet Res Commun. 43(2):77–89.
   PubMed Web of Science ®Google Scholar
• Ke X, Chen J, Zhang X, Fang W, Yang C, Peng J, Chen Y, Sferra TJ. 2013. Qing Hua Chang Yin attenuates lipopolysaccharide-induced inflammatory response in human intestinal cells by inhibiting NF-κB activation. Exp Ther Med. 6(1):189–193.
   PubMed Web of Science ®Google Scholar
• Li M, Van Esch BCAM, Henricks PAJ, Folkerts G, Garssen J. 2018. The anti-inflammatory effects of short chain fatty acids on lipopolysaccharide- or tumor necrosis factor α-stimulated endothelial cells via activation of GPR41/43 and inhibition of HDACs. Front Pharmacol. 9:533–545.
   PubMed Web of Science ®Google Scholar
• Liu J, Chang G, Huang J, Wang Y, Ma N, Roy A, Shen X. 2019. Sodium butyrate inhibits the inflammation of lipopolysaccharide-induced acute lung injury in mice by regulating the toll-like receptor 4/nuclear factor κB signaling pathway. J Agric Food Chem. 67(6):1674–1682.
   PubMed Web of Science ®Google Scholar
• Lu Y, Yeh W, Ohashi PS. 2008. LPS/TLR4 signal transduction pathway. Cytokine. 42(2):145–151.
   PubMed Web of Science ®Google Scholar
• Luo J, Chen D, Mao X, He J, Yu B, Cheng L, Zeng D. 2019. Purified β-glucans of different molecular weights enhance growth performance of LPS-challenged piglets via improved gut barrier function and microbiota. Animal. 9(9):602.
   Google Scholar
• Marini M, Bamias G, Rivera-Nieves J, Moskaluk C, Hoang S, Ross W, Pizarro T, Cominelli F. 2003. TNF-alpha neutralization ameliorates the severity of murine Crohn’s-like ileitis by abrogation of intestinal epithelial cell apoptosis. PNAS. 100(14):8366–8371.
   PubMed Web of Science ®Google Scholar
• Mercer DW, Smith GS, Cross JM, Russell DH, Chang L, Cacioppo J. 1996. Effects of lipopolysaccharide on intestinal injury; potential role of nitric oxide and lipid peroxidation. J Surg Res. 63(1):185–192.
   PubMed Web of Science ®Google Scholar
• Myer PR, Smith TPL, Wells JE, Kuehn LA, Freetly HC. 2015. Rumen microbiome from steers differing in feed efficiency. PLoS One. 10(6):e0129174.
   PubMed Web of Science ®Google Scholar
• Nayfach S, Shi ZJ, Seshadri R, Pollard KS, Kyrpides NC. 2019. New insights from uncultivated genomes of the global human gut microbiome. Nature. 568(7753):505–510.
   PubMed Web of Science ®Google Scholar
• Perego S, Sansoni V, Banfi G, Lombardi G. 2018. Sodium butyrate has anti-proliferative, pro-differentiating, and immunomodulatory effects in osteosarcoma cells and counteracts the TNFα-induced low-grade inflammation. Int J Immunopathol Pharmacol. 32:394632017752240.
   PubMedGoogle Scholar
• Rigby RJ, Carr J, Orgel K, King SL, Lund PK, Dekaney CM. 2016. Intestinal bacteria are necessary for doxorubicin-induced intestinal damage but not for doxorubicin-induced apoptosis. Gut Microbes. 7(5):414–423.
   PubMed Web of Science ®Google Scholar
• Segain J, Raingeard de la Blétière D, Bourreille A, Leray V, Gervois N, Rosales C, Ferrier L, Bonnet C, Blottière H, Galmiche J. 2000. Butyrate inhibits inflammatory responses through NFkappaB inhibition: implications for Crohn’s disease. Gut. 47(3):397–403.
   PubMed Web of Science ®Google Scholar
• Shyer AE, Huycke TR, Lee CH, Mahadevan L, Tabin CJ. 2015. Bending gradients: how the intestinal stem cell gets its home. Cell. 161(3):569–580.
   PubMed Web of Science ®Google Scholar
• Spence C, Wells WG, Smith CJ. 2006. Characterization of the primary starch utilization operon in the obligate anaerobe bacteroides fragilis: regulation by carbon source and oxygen. J Bacteriol. 188(13):4663–4672.
   PubMed Web of Science ®Google Scholar
• Stuber E, Buschenfeld A, Von FA, Arendt T, Folsch UR. 1999. Intestinal crypt cell apoptosis in murine acute graft versus host disease is mediated by tumour necrosis factor alpha and not by the FasL-Fas interaction: effect of pentoxifylline on the development of mucosal atrophy. Gut. 45(2):229–235.
   PubMed Web of Science ®Google Scholar
• Takao M, Yen H, Tobe T. 2014. LeuO enhances butyrate-induced virulence expression through a positive regulatory loop in enterohaemorrhagic Escherichia coli. Mol Microbiol. 93(6):1302–1313.
   PubMed Web of Science ®Google Scholar
• Tazuke Y, Drongowski RA, Teitelbaum DH, Coran AG. 2003. Interleukin-6 changes tight junction permeability and intracellular phospholipid content in a human enterocyte cell culture model. Pediatr Surg Int. 19(5):321–325.
   PubMed Web of Science ®Google Scholar
• Thoetkiattikul H, Mhuantong W, Laothanachareon T, Tangphatsornruang S, Pattarajinda V, Eurwilaichitr L, Champreda V. 2013. Comparative analysis of microbial profiles in cow rumen fed with different dietary fiber by tagged 16S rRNA gene pyrosequencing. Curr Microbiol. 67(2):130–137.
   PubMed Web of Science ®Google Scholar
• Van Landeghem L, Santoro MA, Mah AT, Krebs AE, Dehmer JJ, Mcnaughton KK, Helmrath MA, Magness ST, Lund PK. 2015. IGF1 stimulates crypt expansion via differential activation of 2 intestinal stem cell populations. FASEB J. 29(7):2828–2842.
   PubMed Web of Science ®Google Scholar
• Venn EC, Barnes AJ, Hansen RJ, Boscan P, Twedt DC, Sullivan LA. 2020. Serum D-lactate concentrations in dogs with parvoviral enteritis. J Vet Intern Med. 34(2):691–699.
   PubMed Web of Science ®Google Scholar
• Wang B, Ma MP, Diao QY, Tu Y. 2019. Saponin-induced shifts in the rumen microbiome and metabolome of young cattle. Front Microbiol. 10:356–370.
   PubMed Web of Science ®Google Scholar
• Wang CC, Wu H, Lin FH, Gong R, Xie F, Peng Y, Feng J, Hu C. 2018. Sodium butyrate enhances intestinal integrity, inhibits mast cell activation, inflammatory mediator production and JNK signaling pathway in weaned pigs. Innate Immun. 24(1):40–46.
   PubMed Web of Science ®Google Scholar
• Whisner CM, Maldonado J, Dente B, Krajmalnik-Brown R, Bruening M. 2018. Diet, physical activity and screen time but not body mass index are associated with the gut microbiome of a diverse cohort of college students living in university housing: a cross-sectional study. BMC Microbiol. 18(1):210–221.
   PubMedGoogle Scholar
• Wijtten PJA, Der Meulen JV, Verstegen MWA. 2011. Intestinal barrier function and absorption in pigs after weaning: a review. Br J Nutr. 105(7):967–981.
   PubMed Web of Science ®Google Scholar
• Wu W, Xiao Z, An W, Dong Y, Zhang B. 2018. Dietary sodium butyrate improves intestinal development and function by modulating the microbial community in broilers. PLoS One. 13(5):e0197762.
   PubMed Web of Science ®Google Scholar
• Xu J, Chen X, Yu S, Su Y, Zhu W. 2016. Effects of early intervention with sodium butyrate on gut microbiota and the expression of inflammatory cytokines in neonatal piglets. PLoS One. 11(9):e0162461.
   PubMed Web of Science ®Google Scholar
• Zhang H, Shao M, Huang H, Wang S, Ma L, Wang H, Hu L, Wei K, Zhu R. 2018. The dynamic distribution of small-tail han sheep microbiota across different intestinal segments. Front Microbiol. 9:32–42.
   PubMed Web of Science ®Google Scholar
• Zhang K, Meng M, Gao L, Tu Y, Bai Y. 2018. Sodium butyrate improves high-concentrate-diet-induced impairment of ruminal epithelium barrier function in goats. J Agric Food Chem. 66(33):8729–8736.
   PubMed Web of Science ®Google Scholar
• Zhang L, Huang X, Xue B, Peng Q, Wang Z, Yan T, Wang L. 2015. Immunization against rumen methanogenesis by vaccination with a new recombinant protein. PLoS One. 10(10):e0140086.
   PubMed Web of Science ®Google Scholar
• Zhang WH, Jiang Y, Zhu QF, Gao F, Dai SF, Chen J, Zhou GH. 2011. Sodium butyrate maintains growth performance by regulating the immune response in broiler chickens. Br Poult Sci. 52(3):292–301.
   PubMed Web of Science ®Google Scholar
• Zhang X, Chen X, Zhang H, Guan S, Wen S, Huang W, Liu Z. 2018. Propofol does not reduce pyroptosis of enterocytes and intestinal epithelial injury after lipopolysaccharide challenge. Dig Dis Sci. 63(1):81–91.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Qin G, Sun Z, Che D, Bao N, Zhang X. 2011. Effects of soybean agglutinin on intestinal barrier permeability and tight junction protein expression in weaned piglets. Int J Mol Sci. 12(12):8502–8512.
   PubMed Web of Science ®Google Scholar
• Zhu H, Liu Y, Xie XL, Huang JJ, Hou Y. 2013. Effect of L-arginine on intestinal mucosal immune barrier function in weaned pigs after Escherichia coli LPS challenge. Innate Immun. 19(3):242–252.
   PubMed Web of Science ®Google Scholar
• Zou X, Ji J, Qu HX, Wang J, Shu DM, Wang Y, Liu TF, Li Y, Luo C. 2019. Effects of sodium butyrate on intestinal health and gut microbiota composition during intestinal inflammation progression in broilers. Poult Sci. 98(10):4449–4456.
   PubMed Web of Science ®Google Scholar