Abstract
Some species of lactic acid bacteria have been shown to be beneficial in inflammatory bowel disease (IBD). In the present study, a strain of lactic acid bacterium (Lactobacillus paracasei LS2) was isolated from the Korean food, kimchi, and was shown to inhibit the development of experimental colitis induced by dextran sulfate sodium (DSS). To investigate the role of LS2 in IBD, mice were fed DSS in drinking water for seven days along with LS2 bacteria which were administered intragastrically to some of the mice, while phosphate-buffered saline (PBS) was administered to others (the controls). The administration of LS2 reduced body weight loss and increased survival, and disease activity indexes (DAI) and histological scores indicated that the severity of colitis was significantly reduced. The production of inflammatory cytokines and myeloperoxidase (MPO) activity also decreased. Flow cytometry analysis showed that the number of Th1 (IFN-γ) population cells was significantly reduced in the LS2-administered mice compared with the controls. The administration of LS2 induced the increase of CD4+FOXP3+ Treg cells, which are responsible for IL-10. Numbers of macrophages (CD11b+ F4/80+), and neutrophils (CD11b+ Gr-1+) among lamina propria lymphocytes (LPL) were also reduced. These results indicate that LS2 has an anti-inflammatory effect and ameliorates DSS-induced colitis.
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Atreya, R. and Neurath, M.F. 2008. New therapeutic strategies for treatment of inflammatory bowel disease. Mucosal. Immunol. 1, 175–182.
Blumberg, R.S., Saubermann, L.J., and Strober, W. 1999. Animal models of mucosal inflammation and their relation to human inflammatory bowel disease. Curr. Opin. Immunol. 11, 648–656.
Bouma, G. and Strober, W. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3, 521–533.
Cho, Y.H., Hong, S.M., and Kim, C.H. 2013. Isolation and characterization of lactic acid bacteria from kimchi, korean traditional fermented food to apply into fermented dairy products. Korean J. Food Sci. An. 33, 75–82.
Couper, K.N., Blount, D.G., and Riley, E.M. 2008. IL-10: the master regulator of immunity to infection. J. Immunol. 180, 5771–5777.
Daniel, C., Poiret, S., Goudercourt, D., Dennin, V., Leyer, G., and Pot, B. 2006. Selecting lactic acid bacteria for their safety and functionality by use of a mouse colitis model. Environ. Microb. 72, 5799–5805.
de Moreno de LeBlanc, A., Del Carmen, S., Zurita-Turk, M., Santos Rocha, C., Van de Guchte, M., Azevedo, V., Miyoshi, A., and Le-Blanc, J.G. 2011. Importance of IL-10 modulation by probiotic microorganisms in gastrointestinal inflammatory diseases. ISRN Gastroenterol. 2011, 892971.
Dohi, T., Fujihashi, K., Rennert, P.D., Iwatani, K., Kiyono, H., and McGhee, J.R. 1999. Hapten-induced colitis is associated with colonic patch hypertrophy and T helper cell 2-type responses. J. Exp. Med. 189, 1169–1180.
Fiocchi, C. 1998. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115, 182–205.
Foligne, B., Nutten, S., Steidler, L., Dennin, V., Goudercourt, D., Mercenier, A., and Pot, B. 2006. Recommendations for improved use of the murine TNBS-induced colitis model in evaluating antiinflammatory properties of lactic acid bacteria: technical and microbiological aspects. Digest. Dis. Sci. 51, 390–400.
Hibi, T. and Ogata, H. 2006. Novel pathophysiological concepts of inflammatory bowel disease. J. Gastroenterol. 41, 10–16.
Jo, S.G., Noh, E.J., Lee, J.Y., Kim, G., Choi, J.H., Lee, M.E., Song, J.H., Chang, J.Y., and Park, J.H. 2016. Lactobacillus curvatus WiKim38 isolated from kimchi induces IL-10 production in dendritic cells and alleviates DSS-induced colitis in mice. J. Microbiol. 54, 503–509.
Kim, H.Y., Song, J.L., Chang, H.K., Kang, S.A., and Park, K.Y. 2014. Kimchi protects against azoxymethane/dextran sulfate sodiuminduced colorectal carcinogenesis in mice. J. Med. Food. 17, 833–841.
Kinoshita, K., Hori, M., Fujisawa, M., Sato, K., Ohama, T., Momotani, E., and Ozaki, H. 2006. Role of TNF-α in muscularis inflammation and motility disorder in a TNBS-induced colitis model: clues from TNF-α-deficient mice. Neurogastroent. Motil. 18, 578–588.
Kopp-Hoolihan, L. 2001. Prophylactic and therapeutic uses of probiotics: a review. J. Am. Diet. Assoc. 101, 229–241.
Krawisz, J.E., Sharon, P., and Stenson, W.F. 1984. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Gastroenterology 87, 1344–1350.
Lahtinen, S., Ouwehand, A.C., Salminen, S., and von Wright, A. 2011. Lactic acid bacteria: microbiological and functional aspects. pp. 187–212. CRC Press, USA.
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 antiinflammatory and immunomodulatory activities. Int. Immunopharmacol. 11, 2159–2166.
Masoodi, I., Tijjani, B.M., Wani, H., Hassan, N.S., Khan, A.B., and Hussain, S. 2011. Biomarkers in the management of ulcerative colitis: a brief revie. Ger. Med. Sci. 9, Doc03.
Moore, K.W., de Waal Malefyt, R., Coffman, R.L., and O’Garra, A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu. Rev. Immunol. 19, 683–765.
Murthy, S.N.S., Cooper, H.S., Shim, H., Shah, R.S., Ibrahim, S.A., and Sedergran, D.J. 1993. Treatment of dextran sulfate sodiuminduced murine colitis by intracolonic cyclosporin. Digest. Dis. Sci. 38, 1722–1734.
O’Shea, J.J., Ma, A., and Lipsky, P. 2002. Cytokines and autoimmunity. Nat. Rev. Immunol. 2, 37–45.
Okayasu, I., Hatakeyama, S., Yamada, M., Ohkusa, T., Inagaki, Y., and Nakaya, R. 1990. A novel method in the induction of reliable experimental acute and chronic ulcerative colitis in mice. Gastroenterology 98, 694–702.
Pagnini, C., Saeed, R., Bamias, G., Arseneau, K.O., Pizarro, T.T., and Cominelli, F. 2010. Probiotics promote gut health through stimulation of epithelial innate immunity. Proc. Natl. Acad. Sci. USA 107, 454–459.
Palmen, M., Dijkstra, C.D., Ende, M.B., Pena, A.S., and Rees, E.P. 1995. Anti-CD11b/CD18 antibodies reduce inflammation in acute colitis in rats. Clin. Exp. Immunol. 101, 351–356.
Pelinescu, D.R., Sasarman, E., Chifiriuc, M.C., Stoica, I., Nohit, A.M., Avram, I., Serbancea, F., and Dimov, T.V. 2009. Isolation and identification of some Lactobacillus and Enterococcus strains by a polyphasic taxonomical approach. Rom. Biotech. Lett. 14, 4225–4233.
Podolsky, D.K. 1991. Inflammatory bowel disease. New Engl. J. Med. 325, 928–937.
Sanders, M.E. 2003. Probiotics: considerations for human health. Nutr. Rev. 61, 91–99.
Santucci, L., Agostini, M., Bruscoli, S., Mencarelli, A., Ronchetti, S., Ayroldi, E., Morelli, A., Baldoni, M., and Riccardi, C. 2007. GITR modulates innate and adaptive mucosal immunity during the development of experimental colitis in mice. Gut 56, 52–60.
Saraiva, M. and O’Garra, A. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170–181.
Schaer, C., Hiltbrunner, S., Ernst, B., Mueller, C., Kurrer, M., Kopf, M., and Harris, N.L. 2011. HVEM signalling promotes colitis. PLoS One 6, e18495.
Schenk, M., Bouchon, A., Seibold, F., and Mueller, C. 2007. TREM-1-expressing intestinal macrophages crucially amplify chronic inflammation in experimental colitis and inflammatory bowel diseases. J. Clin. Invest. 117, 3097–3106.
Schultz, M., Veltkamp, C., Dieleman, L.A., Grenther, W.B., Wyrick, P.B., Tonkonogy, S.L., and Sartor, R.B. 2002. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8, 71–80.
Stow, J.L., Low, P.C., Offenhauser, C., and Sangermani, D. 2009. Cytokine secretion in macrophages and other cells: pathways and mediators. Immunobiology 214, 601–612.
Strober, W., Fuss, I.J., and Blumberg, R.S. 2002. The immunology of mucosal models of inflammation 1. Annu. Rev. Immunol. 20, 495–549.
Takamura, T., Harama, D., Fukumoto, S., Nakamura, Y., Shimokawa, N., Ishimaru, K., Ikegami, S., Makino, S., Kitamura, M., and Nakao, A. 2011. Lactobacillus bulgaricus OLL1181 activates the aryl hydrocarbon receptor pathway and inhibits colitis. Immunol. Cell Biol. 89, 817–822.
Tanoue, T., Atarashi, K., and Honda, K. 2016. Development and maintenance of intestinal regulatory T cells. Nat. Rev. Immunol. 16, 295–309.
Wang, J., Anders, R.A., Wang, Y., Turner, J.R., Abraham, C., Pfeffer, K., and Fu, Y.X. 2005. The critical role of LIGHT in promoting intestinal inflammation and Crohn’s disease. J. Immunol. 174, 8173–8182.
Wang, Y., Liu, X.P., Zhao, Z.B., Chen, J.H., and Yu, C.G. 2011. Expression of CD4+ forkhead box P3 (FOXP3)+ regulatory T cells in inflammatory bowel disease. J. Dig. Dis. 12, 286–294.
Wirtz, S., Neufert, C., Weigmann, B., and Neurath, M.F. 2007. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541–546.
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Park, JS., Joe, I., Rhee, P.D. et al. A lactic acid bacterium isolated from kimchi ameliorates intestinal inflammation in DSS-induced colitis. J Microbiol. 55, 304–310 (2017). https://doi.org/10.1007/s12275-017-6447-y
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DOI: https://doi.org/10.1007/s12275-017-6447-y