Journal of Microbiology

, Volume 55, Issue 4, pp 304–310 | Cite as

A lactic acid bacterium isolated from kimchi ameliorates intestinal inflammation in DSS-induced colitis

Microbial Pathogenesis and Host-Microbe Interaction

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.

Keywords

lactic acid bacteria kimchi inflammatory bowel disease dextran sulfate sodium 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Supplementary material

12275_2017_6447_MOESM1_ESM.pdf (184 kb)
Supplementary material, approximately 184 KB.

References

  1. Atreya, R. and Neurath, M.F. 2008. New therapeutic strategies for treatment of inflammatory bowel disease. Mucosal. Immunol. 1, 175–182.CrossRefPubMedGoogle Scholar
  2. 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.CrossRefPubMedGoogle Scholar
  3. Bouma, G. and Strober, W. 2003. The immunological and genetic basis of inflammatory bowel disease. Nat. Rev. Immunol. 3, 521–533.CrossRefPubMedGoogle Scholar
  4. 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.CrossRefGoogle Scholar
  5. 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.CrossRefPubMedGoogle Scholar
  6. 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.CrossRefGoogle Scholar
  7. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  9. Fiocchi, C. 1998. Inflammatory bowel disease: etiology and pathogenesis. Gastroenterology 115, 182–205.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedGoogle Scholar
  11. Hibi, T. and Ogata, H. 2006. Novel pathophysiological concepts of inflammatory bowel disease. J. Gastroenterol. 41, 10–16.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Kopp-Hoolihan, L. 2001. Prophylactic and therapeutic uses of probiotics: a review. J. Am. Diet. Assoc. 101, 229–241.CrossRefPubMedGoogle Scholar
  16. Krawisz, J.E., Sharon, P., and Stenson, W.F. 1984. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Gastroenterology 87, 1344–1350.PubMedGoogle Scholar
  17. 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.Google Scholar
  18. 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.CrossRefPubMedGoogle Scholar
  19. 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.PubMedPubMedCentralGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedGoogle Scholar
  22. O’Shea, J.J., Ma, A., and Lipsky, P. 2002. Cytokines and autoimmunity. Nat. Rev. Immunol. 2, 37–45.CrossRefPubMedGoogle Scholar
  23. 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.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 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.Google Scholar
  27. Podolsky, D.K. 1991. Inflammatory bowel disease. New Engl. J. Med. 325, 928–937.CrossRefPubMedGoogle Scholar
  28. Sanders, M.E. 2003. Probiotics: considerations for human health. Nutr. Rev. 61, 91–99.CrossRefPubMedGoogle Scholar
  29. 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.CrossRefPubMedGoogle Scholar
  30. Saraiva, M. and O’Garra, A. 2010. The regulation of IL-10 production by immune cells. Nat. Rev. Immunol. 10, 170–181.CrossRefPubMedGoogle Scholar
  31. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  32. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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.CrossRefPubMedGoogle Scholar
  34. 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.CrossRefPubMedGoogle Scholar
  35. Strober, W., Fuss, I.J., and Blumberg, R.S. 2002. The immunology of mucosal models of inflammation 1. Annu. Rev. Immunol. 20, 495–549.CrossRefPubMedGoogle Scholar
  36. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  37. Tanoue, T., Atarashi, K., and Honda, K. 2016. Development and maintenance of intestinal regulatory T cells. Nat. Rev. Immunol. 16, 295–309.CrossRefPubMedGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. 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.CrossRefPubMedGoogle Scholar
  40. Wirtz, S., Neufert, C., Weigmann, B., and Neurath, M.F. 2007. Chemically induced mouse models of intestinal inflammation. Nat. Protoc. 2, 541–546.CrossRefPubMedGoogle Scholar

Copyright information

© The Microbiological Society of Korea and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of Biological ScienceUniversity of UlsanUlsanRepublic of Korea
  2. 2.Franklin W. Olin College of EngineeringNeedhamUSA
  3. 3.School of Biological Sciences, College of Natural ScienceSeoul National UniversitySeoulRepublic of Korea

Personalised recommendations