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Latilactobacillus curvatus BYB3 Isolated from Kimchi Alleviates Dextran Sulfate Sodium (DSS)-Induced Colitis in Mice by Inhibiting IL-6 and TNF-R1 Production

  • Wang, Xing (Division of Animal Science, Chonnam National University) ;
  • Li, Dingyun (Division of Animal Science, Chonnam National University) ;
  • Meng, Ziyao (Division of Animal Science, Chonnam National University) ;
  • Kim, Kiyeop (Division of Animal Science, Chonnam National University) ;
  • Oh, Sejong (Division of Animal Science, Chonnam National University)
  • Received : 2021.09.30
  • Accepted : 2021.12.27
  • Published : 2022.03.28

Abstract

Recent studies have shown that probiotics have health-promoting effects, particularly intestinal immune modulation. In this study, we focused on the immunomodulatory properties of Latilactobacillus curvatus BYB3, formerly called Lactobacillus curvatus, isolated from kimchi. In a mouse model of 14-day dextran sulfate sodium (DSS)-induced colitis, treatment with L. curvatus BYB3 significantly decreased the disease activity index, colon length, and weight loss. Moreover, histological analyses showed that L. curvatus BYB3 protected the structural integrity of the intestinal epithelial layer and mucin-secreting goblet cells from DSS-induced damage, with only slight infiltration by immune cells. To evaluate the molecular mechanisms underlying L. curvatus BYB3-driven inhibition of interleukin 6 production, possible in vivo anti-inflammatory effects of L. curvatus BYB3 were examined in the same mouse model. In addition, significantly lower levels of IL-6 and tumor necrosis factor receptor 1 upregulation were seen in the DSS+BYB3 group (compared to that in the DSS group). These results indicate that L. curvatus BYB3 exhibits health-promoting effects via immune modulation; and therefore, it can be used to treat various inflammatory diseases.

Keywords

Acknowledgement

This work was supported by the National Research Foundation grant (NRF) grant funded by the Korea government (2021R1A4A1031220).

References

  1. Podolsky DK. 1991. Inflammatory bowel disease. N Engl. J. Med. 325: 928-937. https://doi.org/10.1056/NEJM199109263251306
  2. Thia KT, Loftus EVJ, Sandborn WJ, Yang S-K. 2008. An update on the epidemiology of inflammatory bowel disease in Asia. Am. J. Gastroenterol. 103: 3167-3182. https://doi.org/10.1111/j.1572-0241.2008.02158.x
  3. Khor B, Gardet A, Xavier RJ. 2011. Genetics and pathogenesis of inflammatory bowel disease. Nature 474: 307-317. https://doi.org/10.1038/nature10209
  4. Mehta F. 2016. Report: economic implications of inflammatory bowel disease and its management. Am. J. Manag. Care 22: s51-60.
  5. Stevens C, Walz G, Singaram C, Lipman ML, Zanker B, Muggia A, et al. 1992. Tumor necrosis factor-α, interleukin-1β, and interleukin-6 expression in inflammatory bowel disease. Dig. Dis. Sci. 37: 818-826. https://doi.org/10.1007/BF01300378
  6. Albrecht L-J, Tauber SC, Merres J, Kress E, Stope MB, Jansen S, et al. 2016. Lack of proinflammatory cytokine interleukin-6 or tumor necrosis factor receptor-1 results in a failure of the innate immune response after bacterial meningitis. Mediators Inflamm. 2016: 7678542. https://doi.org/10.1155/2016/7678542
  7. Atreya R, Neurath MF. 2005. Involvement of IL-6 in the pathogenesis of inflammatory bowel disease and colon cancer. Clin. Rev. Allergy Immunol. 28: 187-195. https://doi.org/10.1385/CRIAI:28:3:187
  8. Zaidi D, Wine E. 2018. Regulation of nuclear factor kappa-light-chain-enhancer of activated B cells (NF-κβ) in inflammatory bowel diseases. Front. Pediatr. 6: 317. https://doi.org/10.3389/fped.2018.00317
  9. Chassaing B, Aitken JD, Malleshappa M, Vijay-Kumar M. 2014. Dextran sulfate sodium (DSS)-induced colitis in mice. Curr. Protoc. Immunol. 104: 15.25. 1-15.25. 14.
  10. Malhotra S. 1977. Dietary factors in a study of cancer colon from cancer registry, with special reference to the role of saliva, milk and fermented milk products and vegetable fibre. Med. Hypotheses 3: 122-126. https://doi.org/10.1016/0306-9877(77)90024-X
  11. Jacouton E, Chain F, Sokol H, Langella P, Bermudez-Humaran LG. 2017. Probiotic strain Lactobacillus casei BL23 prevents colitis-associated colorectal cancer. Front. Immunol. 8: 1553. https://doi.org/10.3389/fimmu.2017.01553
  12. Mu Q, Tavella VJ, Luo XM. 2018. Role of Lactobacillus reuteri in human health and diseases. Front. Microbiol. 9: 757. https://doi.org/10.3389/fmicb.2018.00757
  13. McFall-Ngai M. 2007. Care for the community. Nature 445: 153-153. https://doi.org/10.1038/445153a
  14. Park J-S, Joe I, Rhee PD, Jeong C-S, Jeong G. 2017. A lactic acid bacterium isolated from kimchi ameliorates intestinal inflammation in DSS-induced colitis. J. Microbiol. 55: 304-310. https://doi.org/10.1007/s12275-017-6447-y
  15. Hogan SP, Seidu L, Blanchard C, Groschwitz K, Mishra A, Karow ML, et al. 2006. Resistin-like molecule β regulates innate colonic function: barrier integrity and inflammation susceptibility. J. Allergy Clin. Immunol. 118: 257-268. https://doi.org/10.1016/j.jaci.2006.04.039
  16. Amer M, Nadeem M, Nazir R, Ur S, Fakhar M, Abid F, et al. 2018. Probiotics and their use in inflammatory bowel disease. Altern. Ther. Health Med. 24: 16-23.
  17. Galvez J, Comalada M, Xaus J. 2010. Prebiotics and probiotics in experimental models of rodent colitis: Lessons in treatment or prevention of inflammatory bowel diseases, pp. 589-610. Bioactive Foods in Promoting Health, Ed. Elsevier,
  18. Lee J-Y, Kim C-J, Kunz B. 2006. Identification of lactic acid bacteria isolated from kimchi and studies on their suitability for application as starter culture in the production of fermented sausages. Meat Sci. 72: 437-445. https://doi.org/10.1016/j.meatsci.2005.08.013
  19. Ikai R, Tanabe K, Shima J. 2020. Lactobacillus curvatus strains specifically show high levels of tolerance to freeze-thaw stress. bioRxiv. 2020.2002.2004.934851.
  20. Solomon L, Mansor S, Mallon P, Donnelly E, Hoper M, Loughrey M, et al. 2010. The dextran sulphate sodium (DSS) model of colitis: an overview. Comp. Clin. Path. 19: 235-239. https://doi.org/10.1007/s00580-010-0979-4
  21. Guimaraes T, Igbaria M, Lu Mt. 1992. The determinants of DSS success: an integrated model. Decis. Sci. 23: 409-430. https://doi.org/10.1111/j.1540-5915.1992.tb00397.x
  22. Oz HS, Chen TS, McClain CJ, de Villiers WJ. 2005. Antioxidants as novel therapy in a murine model of colitis. J. Nutr. Biochem. 16: 297-304. https://doi.org/10.1016/j.jnutbio.2004.09.007
  23. Jo S-G, Noh E-J, Lee J-Y, Kim G, Choi J-H, Lee M-E, et al. 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. https://doi.org/10.1007/s12275-016-6160-2
  24. Song J-L, Choi J-H, Seo J-H, Lim Y-I, Park K-Y. 2014. Anti-colitic effects of kanjangs (fermented soy sauce and sesame sauce) in dextran sulfate sodium-induced colitis in mice. J. Med. Food 17: 1027-1035. https://doi.org/10.1089/jmf.2013.3119
  25. Karmacharya U, Regmi SC, Awasthi BP, Chaudhary P, Kim YE, Lee I-H, et al. 2021. Synthesis and activity of N-(5-hydroxy-3, 4, 6-trimethylpyridin-2-yl) acetamide analogues as anticolitis agents via dual inhibition of TNF-α-and IL-6-induced cell adhesions. Bioorg. Med. Chem. Lett. 43: 128059. https://doi.org/10.1016/j.bmcl.2021.128059
  26. Ren J, Liu Z, Wang Q, Giles J, Greenberg J, Sheibani N, et al. 2016. Andrographolide ameliorates abdominal aortic aneurysm progression by inhibiting inflammatory cell infiltration through downregulation of cytokine and integrin expression. J. Pharmacol. Exp. Ther. 356: 137-147. https://doi.org/10.1124/jpet.115.227934
  27. Gay J, Kokkotou E, O'Brien M, Pothoulakis C, Karalis KP. 2006. Interleukin-6 genetic ablation protects from trinitrobenzene sulfonic acid-induced colitis in mice. Neuroimmunomodulation 13: 114-121. https://doi.org/10.1159/000096656
  28. Mudter J, Neurath MF. 2007. Il-6 signaling in inflammatory bowel disease: pathophysiological role and clinical relevance. Inflamm. Bowel Dis. 13: 1016-1023. https://doi.org/10.1002/ibd.20148
  29. Lin X, Sun Q, Zhou L, He M, Dong X, Lai M, et al. 2018. Colonic epithelial mTORC1 promotes ulcerative colitis through COX-2-mediated Th17 responses. Mucosal Immunol. 11: 1663-1673. https://doi.org/10.1038/s41385-018-0018-3
  30. Akanda MR, Nam H-H, Tian W, Islam A, Choo B-K, Park B-Y. 2018. Regulation of JAK2/STAT3 and NF-κB signal transduction pathways; Veronica polita alleviates dextran sulfate sodium-induced murine colitis. Biomed. Pharmacother. 100: 296-303. https://doi.org/10.1016/j.biopha.2018.01.168