Abstract
Inflammatory bowel disease (IBD) is a chronic lifelong disease characterized by inflammation of the gastrointestinal tract. Although more and more treatment options serve IBD, there is still no cure. It is important to find an effective treatment for IBD. This study aims to investigate whether Lactobacillus plantarum (L. plantarum) could alleviate colitis induced by dextran sulfate sodium (DSS). Following the DSS challenge, L. plantarum on DSS-mediated inflammatory colon lesions in mice, and L. plantarum therapy heightened the relative abundance of the colon-resident Actinobacteria. Analysis of serum metabolomics also indicated that the content of MG (18:4 (6Z, 9Z, 12Z, 15Z)/0:0/0:0) was increased in response to L. plantarum therapy, and this was also the case for indolepyruvate and 1-hydroxyibuprofen. However, 13-oxooctadecadienoic acid (13-oxoODE) and indolylacryloylglycine content fell following the DSS challenge. Based on these results, the study elucidates the mitigatory effects of L. plantarum in colitis, which depend on its regulation of the colonic microbial community and its modification of serum metabolites. The results revealed that L. plantarum mitigated inflammatory colon lesions, reprogrammed the microbial community and altered the level of serum metabolites in a murine model challenged with DSS. The study may present a potential therapeutic strategy for colitis.
Similar content being viewed by others
References
Anderson, J.L., Edney, R.J., and Whelan, K. (2012). Systematic review: Faecal microbiota transplantation in the management of inflammatory bowel disease. Aliment Pharmacol Ther 36, 503–516.
Bai, M., Liu, H., Xu, K., Zhang, X., Deng, B., Tan, C., Deng, J., Bing, P., and Yin, Y. (2019). Compensation effects of coated cysteamine on meat quality, amino acid composition, fatty acid composition, mineral content in dorsal muscle and serum biochemical indices in finishing pigs offered reduced trace minerals diet. Sci China Life Sci 62, 1550–1553.
Bernstein, C.N. (2015). Treatment of ibd: Where we are and where we are going. Am J Gastroenterol 110, 114–126.
Bull, G., Shattock, P., Whiteley, P., Anderson, R., Groundwater, P.W., Lough, J.W., and Lees, G. (2003). Indolyl-3-acryloylglycine (IAG) is a putative diagnostic urinary marker for autism spectrum disorders. Med Sci Monit 9, CR422–425.
Cai, Y.H., Aguilar, Y.M., Yu, L., Wang, Y., Liu, H.B., Liu, G., Zhong, J., Jiang, Y.B., and Yin, Y.L. (2014). Effects of dietary supplementation of Lactobacillus plantarum on growth performance and serum concentration of amino acids in weaned piglets. Anim Nutr Feed Tech 14, 411–420.
Choi, S.H., Lee, S.H., Kim, M.G., Lee, H.J., and Kim, G.B. (2019). Lactobacillus plantarum CAU1055 ameliorates inflammation in lipopolysaccharide-induced RAW264.7 cells and a dextran sulfate sodium-induced colitis animal model. J Dairy Sci 102, 6718–6725.
Cui, Y., Wei, H., Lu, F., Liu, X., Liu, D., Gu, L., and Ouyang, C. (2016). Different effects of three selected lactobacillus strains in dextran sulfate sodium-induced colitis in balb/c mice. PLoS ONE 11, e0148241.
Currò, D., Ianiro, G., Pecere, S., Bibbò, S., and Cammarota, G. (2017). Probiotics, fibre and herbal medicinal products for functional and inflammatory bowel disorders. British J Pharmacol 174, 1426–1449.
Dalton, N.R., Chandler, S., Turner, C., Charman, T., Pickles, A., Simonoff, E., and Baird, G. (2017). Measurement of urine indolylacroylglycine is not useful in the diagnosis or dietary management of autism. Autism Res 10, 408–413.
Di Sabatino, A., Biancheri, P., Rovedatti, L., Macdonald, T.T., and Corazza, G.R. (2012). Recent advances in understanding ulcerative colitis. Intern Emerg Med 7, 103–111.
Ding, S., Ma, Y., Liu, G., Yan, W., Jiang, H., and Fang, J. (2019). Lactobacillus brevis alleviates DSS-induced colitis by reprograming intestinal microbiota and influencing serum metabolome in murine model. Front Physiol 10, 1152.
Gibson, G.R., Hutkins, R., Sanders, M.E., Prescott, S.L., Reimer, R.A., Salminen, S.J., Scott, K., Stanton, C., Swanson, K.S., Cani, P.D., et al. (2017). Expert consensus document: The international scientific association for probiotics and prebiotics (ISAPP) consensus statement on the definition and scope of prebiotics. Nat Rev Gastroenterol Hepatol 14, 491–502.
Gonzalez-Rey, E., Anderson, P., González, M.A., Rico, L., Büscher, D., and Delgado, M. (2009). Human adult stem cells derived from adipose tissue protect against experimental colitis and sepsis. Gut 58, 929–939.
Gronbach, K., Flade, I., Holst, O., Lindner, B., Ruscheweyh, H.J., Wittmann, A., Menz, S., Schwiertz, A., Adam, P., Stecher, B., et al. (2014). Endotoxicity of lipopolysaccharide as a determinant of T-cell-mediated colitis induction in mice. Gastroenterology 146, 765–775.
Guan, G., Ding, S., Yin, Y., Duraipandiyan, V., Al-Dhabi, N.A., and Liu, G. (2019). Macleaya cordata extract alleviated oxidative stress and altered innate immune response in mice challenged with enterotoxigenic Escherichia coli. Sci China Life Sci 62, 1019–1027.
Guan, G., Wang, H., Chen, S., Liu, G., Xiong, X., Tan, B., Duraipandiyan, V., Al-Dhabi, N.A., and Fang, J. (2016). Dietary chitosan supplementation increases microbial diversity and attenuates the severity of citrobacter rodentium infection in mice. Mediat Inflamm 2016, 9236196.
Guo, Q., Li, F., Duan, Y., Wen, C., Wang, W., Zhang, L., Huang, R., and Yin, Y. (2020). Oxidative stress, nutritional antioxidants and beyond. Sci China Life Sci 63, 866–874.
He, B., Li, T., Wang, W., Gao, H., Bai, Y., Zhang, S., Zang, J., Li, D., and Wang, J. (2019). Metabolic characteristics and nutrient utilization in high-feed-efficiency pigs selected using different feed conversion ratio models. Sci China Life Sci 62, 959–970.
Heinecke, J.W., Li, W., Daehnke, H.L., 3rd, and Goldstein, J.A. (1993). Dityrosine, a specific marker of oxidation, is synthesized by the myeloperoxidase-hydrogen peroxide system of human neutrophils and macrophages. J Biol Chem 268, 4069–4077.
Jalanka, J., Cheng, J., Hiippala, K., Ritari, J., Salojärvi, J., Ruuska, T., Kalliomäki, M., and Satokari, R. (2020). Colonic mucosal microbiota and association of bacterial taxa with the expression of host antimicrobial peptides in pediatric ulcerative colitis. IJMS 21, 6044.
Kim, D.H., Kim, S., Ahn, J.B., Kim, J.H., Ma, H.W., Seo, D.H., Che, X., Park, K.C., Jeon, J.Y., Kim, S.Y., et al. (2020). Lactobacillus plantarum CBT LP3 ameliorates colitis via modulating T cells in mice. Int J Med Microbiol 310, 151391.
Kim, M., Lim, S.J., Kang, S.W., Um, B.H., and Nho, C.W. (2014). Aceriphyllum rossii extract and its active compounds, quercetin and kaempferol inhibit IgE-mediated mast cell activation and passive cutaneous anaphylaxis. J Agric Food Chem 62, 3750–3758.
Knutson, C.G., Mangerich, A., Zeng, Y., Raczynski, A.R., Liberman, R.G., Kang, P., Ye, W., Prestwich, E.G., Lu, K., Wishnok, J.S., et al. (2013). Chemical and cytokine features of innate immunity characterize serum and tissue profiles in inflammatory bowel disease. Proc Natl Acad Sci USA 110, E2332–E2341.
Lang, M., Baumgartner, M., Rożalska, A., Frick, A., Riva, A., Jarek, M., Berry, D., and Gasche, C. (2020). Crypt residing bacteria and proximal colonic carcinogenesis in a mouse model of lynch syndrome. Int J Cancer 147, 2316–2326.
Levit, R., Savoy de Giori, G., de Moreno de LeBlanc, A., and LeBlanc, J.G. (2018). Effect of riboflavin-producing bacteria against chemically induced colitis in mice. J Appl Microbiol 124, 232–240.
Liu, Y.W., Su, Y.W., Ong, W.K., Cheng, T.H., and Tsai, Y.C. (2011). Oral administration of lactobacillus plantarum k68 ameliorates DSS-induced ulcerative colitis in balb/c mice via the anti-inflammatory and immunomodulatory activities. Int Immunopharmacol 11, 2159–2166.
Machiels, K., Joossens, M., Sabino, J., De Preter, V., Arijs, I., Eeckhaut, V., Ballet, V., Claes, K., Van Immerseel, F., Verbeke, K., et al. (2014). A decrease of the butyrate-producing species Roseburia hominis and Faecalibacterium prausnitzii defines dysbiosis in patients with ulcerative colitis. Gut 63, 1275–1283.
Mao, R., and Hu, P.J. (2016). The future of IBD therapy: Where are we and where should we go next? Dig Dis 34, 175–179.
Ohland, C.L., and Macnaughton, W.K. (2010). Probiotic bacteria and intestinal epithelial barrier function. Am J Physiol-Gastrointest Liver Physiol 298, G807–G819.
Pace, F., Pace, M. and Quartarone, G. (2015). Probiotics in digestive diseases: Focus on lactobacillus GG. Minerva Gastroenterol Dietol 61, 273–292.
Plaza-Díaz, J., Ruiz-Ojeda, F.J., Vilchez-Padial, L.M., and Gil, A. (2017). Evidence of the anti-inflammatory effects of probiotics and synbiotics in intestinal chronic diseases. Nutrients 9, 555.
Round, J.L., and Mazmanian, S.K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 9, 313–323.
Ryman, V.E., Packiriswamy, N., and Sordillo, L.M. (2016). Apoptosis of endothelial cells by 13-hpode contributes to impairment of endothelial barrier integrity. Mediators Inflammation 2016, 1–13.
Sánchez, B., Delgado, S., Blanco-Míguez, A., Lourenço, A., Gueimonde, M., and Margolles, A. (2017). Probiotics, gut microbiota, and their influence on host health and disease. Mol Nutr Food Res 61, 1600240.
Scheijen, J.L.J.M., Hanssen, N.M.J., van de Waarenburg, M.P.H., Jonkers, D.M.A.E., Stehouwer, C.D.A., and Schalkwijk, C.G. (2012). L(+) and D(−) lactate are increased in plasma and urine samples of type 2 diabetes as measured by a simultaneous quantification of L(+) and D(−) lactate by reversed-phase liquid chromatography tandem mass spectrometry. Exp Diabetes Res 2012, 1–10.
Schicho, R., Nazyrova, A., Shaykhutdinov, R., Duggan, G., Vogel, H.J., and Storr, M. (2010). Quantitative metabolomic profiling of serum and urine in DSS-induced ulcerative colitis of mice by 1H NMR spectroscopy. J Proteome Res 9, 6265–6273.
Sheehan, D., Moran, C., and Shanahan, F. (2015). The microbiota in inflammatory bowel disease. J Gastroenterol 50, 495–507.
Shiomi, Y., Nishiumi, S., Ooi, M., Hatano, N., Shinohara, M., Yoshie, T., Kondo, Y., Furumatsu, K., Shiomi, H., Kutsumi, H., et al. (2011). GCMS-based metabolomic study in mice with colitis induced by dextran sulfate sodium. Inflamm Bowel Dis 17, 2261–2274.
Tamboli, C.P., Neut, C., Desreumaux, P., and Colombel, J.F. (2004). Dysbiosis in inflammatory bowel disease. Gut 53, 1–4.
Tian, T., Wang, Z., and Zhang, J. (2017). Pathomechanisms of oxidative stress in inflammatory bowel disease and potential antioxidant therapies. Oxidative Med Cellular Longevity 2017, 1–18.
Wang, G., Liu, Y., Lu, Z., Yang, Y., Xia, Y., Lai, P.F.H., and Ai, L. (2019). The ameliorative effect of a Lactobacillus strain with good adhesion ability against dextran sulfate sodium-induced murine colitis. Food Funct 10, 397–409.
Wang, L., Angley, M.T., Gerber, J.P., Young, R.L., Abarno, D.V., McKinnon, R.A., and Sorich, M.J. (2009). Is urinary indolyl-3-acryloylglycine a biomarker for autism with gastrointestinal symptoms? Biomarkers 14, 596–603.
Wang, L., Zhu, F., Yang, H., Li, J., Li, Y., Ding, X., Xiong, X., Ji, F., Zhou, H., and Yin, Y. (2020). Epidermal growth factor improves intestinal morphology by stimulating proliferation and differentiation of enterocytes and mTOR signaling pathway in weaning piglets. Sci China Life Sci 63, 259–268.
Wang, T., Teng, K., Liu, G., Liu, Y., Zhang, J., Zhang, X., Zhang, M., Tao, Y., and Zhong, J. (2018a). Lactobacillusreuteri HCM2 protects mice against enterotoxigenic Escherichia coli through modulation of gut microbiota. Sci Rep 8, 17485.
Wang, Y., Guo, Y., Chen, H., Wei, H., and Wan, C. (2018b). Potential of Lactobacillus plantarum ZDY2013 and Bifidobacterium bifidum WBIN03 in relieving colitis by gut microbiota, immune, and anti-oxidative stress. Can J Microbiol 64, 327–337.
Wang, Y., Liu, Y., Sidhu, A., Ma, Z., McClain, C., and Feng, W. (2012). Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am J Physiol-Gastrointest Liver Physiol 303, G32–G41.
Weingarden, A.R., and Vaughn, B.P. (2017). Intestinal microbiota, fecal microbiota transplantation, and inflammatory bowel disease. Gut Microbes 8, 238–252.
Wysoczanski, R., Kendall, A., Motwani, M., Vega, R., Rahman, F., McCartney, S., Bloom, S., Nicolaou, A., Gilroy, D., Segal, A., et al. (2019). Ulcerative colitis is characterized by amplified acute inflammation with delayed resolution. https://doi.org/10.1101/870139.
Zhang, F., Li, Y., Wang, X., Wang, S., and Bi, D. (2019). The impact of Lactobacillus plantarum on the gut microbiota of mice with DSS-induced colitis. Biomed Res Int 2019, 1–10.
Zou, L., Xiong, X., Yang, H., Wang, K., Zhou, J., Lv, D., and Yin, Y. (2019). Identification of microRNA transcriptome reveals that miR-100 is involved in the renewal of porcine intestinal epithelial cells. Sci China Life Sci 62, 816–828.
Acknowledgements
This study was supported by the National Natural Science Foundation of China (31772642, 31672457), Hunan Provincial Science and Technology Department (2019TP2004, 2017NK2322, 2016WK2008, 2016TP2005), Double first-class construction project of Hunan Agricultural University (SYL201802003), and China Postdoctoral Science Foundation (2018M632963, 2019T120705).
Author information
Authors and Affiliations
Corresponding author
Additional information
Compliance and ethics
The author(s) declare that they have no conflict of interest. All aspects of this research were conducted in accordance with the Chinese Guidelines for Animal Welfare and Experimental Protocols. The Hunan Agricultural University’s Animal Ethics Committee granted approval for the animal procedures used in this study.
Rights and permissions
About this article
Cite this article
Ding, S., Yan, W., Fang, J. et al. Potential role of Lactobacillus plantarum in colitis induced by dextran sulfate sodium through altering gut microbiota and host metabolism in murine model. Sci. China Life Sci. 64, 1906–1916 (2021). https://doi.org/10.1007/s11427-020-1835-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-020-1835-4