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Evaluation of Anti-colitic Effect of Lactic Acid Bacteria in Mice by cDNA Microarray Analysis

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Abstract

To evaluate the anti-colitic effect of lactic acid bacteria by cDNA microarray analysis, a lactic acid bacteria mixture (LM) consisting of Lactobacillus brevis HY7401, L. suntoryeus HY7801 and Bifidobacterium longum HY8004 was orally administered to dextran sulfate (DSS)-induced colitic mice and the expression profile of numerous genes was assessed. DSS treatment caused colitic outcomes such as inflammation and colon shortening. DSS also up-regulated the expression of inflammation-related genes: pro-inflammatory and chemotactic cytokines, including IL-1β, TNF-α, IL-6, CCL2, CCL4, CCL7, CCL24, CXCL1, CXCL2, CXCL5, CXCL9 and CXCL10, and their receptors CCR3 and CCR7, and other colitis-related genes such as COX-2, PAP, MMP family, S100a8, S100a9 and DEFA1. LM treatment inhibited the mRNA expression of inflammation-related and tissue remodeling genes induced by DSS as well as the colitic symptoms. LM inhibition for the DSS-induced expression of the representative inflammatory markers, IL-1β, TNF-α and COX-2, was supported by quantitative real-time polymerase chain reaction analysis. These findings suggest that LM ameliorates DSS-induced colitis by regulating inflammatory-related cytokines as well as tissue remodeling genes.

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References

  1. Binder, V. 2004. Epidemiology of IBD during the twentieth century: an integrated view. Best Pract. Res. Clin. Gastroenterol. 18:463–79. doi:10.1016/j.bpg.2003.12.002.

    Article  PubMed  Google Scholar 

  2. Shanahan, F. 2002. Crohn’s disease. Lancet. 359:62–9. doi:10.1016/S0140-6736(02)07284-7.

    Article  CAS  PubMed  Google Scholar 

  3. Raffi, F., R. van Embdin, and L. M. C. van Lieshout. 1999. Changes in bacterial enzymes and PCR profiles of fecal bacteria from a patient with ulcerative colitis before and after antimicrobial treatments. Dig. Dis Sci. 44:637–42. doi:10.1023/A:1026634229934.

    Article  Google Scholar 

  4. Atreya, R., J. Multer, S. Fintoo, J. Müllberg, T. Jostock, S. Wirtz, M. Schütz, B. Bartsch, M. Holtmann, C. Becker, D. Strand, J. Czaja, J. F. Schlaak, H. A. Lehr, F. Autschbach, G. Schürmann, N. Nishimoto, K. Yoshizaki, H. Ito, T. Kishimoto, P. R. Galle, S. Rose-John, and M. F. Neurath. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn’s disease and experimental colitis in vivo. Nat. Med. 6:583–8. doi:10.1038/75068.

    Article  CAS  PubMed  Google Scholar 

  5. Salmela, M. T., t. t. MacDonald, D. Black, B. Irvine, T. Zhuma, U. Saarialho-Kere, and S. L. Pender. 2002. Upregulation of matrix metalloproteinases in a model of T cell mediated tissue injury in the gut: analysis by gene array and in situ hybridization. Gut. 51:540–7. doi:10.1136/gut.51.4.540.

    Article  CAS  PubMed  Google Scholar 

  6. Yang, S. K., M. S. Choi, O. H. Kim, S. J. Myung, H. Y. Jung, W. S. Hong, J. H. Kim, and Y. I. Min. 2002. The increased expression of an array of C–X–C and C–C chemokines in the colonic mucosa of patients with ulcerative colitis: regulation by corticosteroids. Am. J. Gastroenterol. 97:126–32. doi:10.1111/j.1572-0241.2002.05431.x.

    Article  CAS  PubMed  Google Scholar 

  7. Lawrance, I. C., c. Fiocchi, and S. Chakravarti. 2001. Ulcerative colitis and Crohn's disease: distinctive gene expression profiles and novel susceptibility candidate genes. Hum. Mol. Genet. 10:445–56. doi:10.1093/hmg/10.5.445.

    Article  CAS  PubMed  Google Scholar 

  8. Costello, C. M., N. Mah, R. Hasler, P. Rosenstiel, G. H. Waetzig, A. Hahn, T. Lu, Y. Gurbuz, S. Nikolaus, M. Albrecht, J. Hampe, R. Lucius, G. Kloppel, H. Eickhoff, H. Lehrach, T. Lengauer, and S. Schreiber. 2005. Dissection of the inflammatory bowel disease transcriptome using genome-wide cDNA microarrays. PLoS Med. 2:e199. doi:10.1371/journal.pmed.0020199.

    Article  PubMed  CAS  Google Scholar 

  9. Collins, M. P., and G. R. Gibson. 1999. Probiotics, prebiotics, and synbiotics: approaches for modulating the microbial ecology of the gut. Am. J. Clin. Nutr. 69:s1052–7.

    Google Scholar 

  10. Perdigon, G., W. E. B. de Jorrat, S. F. de Petrino, and M. Valerde de Budeguer. 1991. Effect of oral administration of Lactobacillus casei on various biological functions of the host. Food Agric. Immunol. 3:93–102. doi:10.1080/09540109109354735.

    Article  Google Scholar 

  11. Taranto, M. P., M. Medici, G. Perdigon, A. P. Ruiz Holgado, and G. F. Valdez. 1998. Evidence for hypoglycemic effect of Lactobacillus reuteri in hypercholesterolemic mice. J. Dairy Sci. 81:2336–40.

    CAS  PubMed  Google Scholar 

  12. Campieri, M., and P. Gionchetti. 1999. Probiotics in inflammatory bowel disease: new insight to pathogenesis or a possible therapeutic alternative. Gastroenterology. 116:1246–60. doi:10.1016/S0016-5085(99)70029-6.

    Article  CAS  PubMed  Google Scholar 

  13. Chung, Y. W., J. H. Choi, T. Y. Oh, C. S. Eun, and D. S. Han. 2007. Lactobacillus casei prevents the development of dextran sulfate sodium-induced colitis in Toll-like receptor 4 mutant mice. Clin. Exp. Immunol. 151:182–9.

    PubMed  Google Scholar 

  14. Grabig, A., D. Pcclik, C. Guzy, A. Dankof, D. C. Baumgart, J. Erckenbrecht, B. Raupach, U. Sonnenborn, J. Eckert, R. R. Schumann, B. Wiedenmann, A. U. Dignass, and A. Sturm. 2006. Escherichia coli strain Nissle 1917 ameliorates experimental colitis via Toll-like receptor 2- and Toll-like receptor 4-dependent pathways. Infect. Immun. 74:4075–82. doi:10.1128/IAI.01449-05.

    Article  CAS  PubMed  Google Scholar 

  15. Peran, L., D. Camuesco, M. Comalada, E. Bailon, A. Henriksson, J. Xaus, A. Zarzuelo, and J. Galvez. 2007. A comparative study of the preventative effects exerted by three probiotics, Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J. Appl. Microbiol. 103:836–44. doi:10.1111/j.1365-2672.2007.03302.x.

    Article  CAS  PubMed  Google Scholar 

  16. Lee, H. S., S. Y. Han, E. A. Bae, C. S. Huh, Y. T. Ahn, J. H. Lee, and D. H. Kim. 2008. Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immunopharmacol. 8:574–80. doi:10.1016/j.intimp.2008.01.009.

    Article  CAS  PubMed  Google Scholar 

  17. Lee, J. H., B. Lee, H. S. Lee, E. A. Bae, H. Lee, Y. T. Ahn, K. S. Lim, C. S. Huh, and D. H. Kim. 2009. Lactobacillus suntoryeus inhibits pro-inflammatory cytokine expression and TLR-4-linked NF-kappa B activation in experimental colitis. Int. J. Colorectal. Dis. 24:231–7. doi:10.1007/s00384-008-0618-6.

    Article  PubMed  Google Scholar 

  18. Lee, B., J. H. Lee, H. S. Lee, E. A. Bae, C. S. Huh, Y. T. Ahn, and D. H. Kim. 2009. Glycosaminoglycan degradation-inhibitory lactic acid bacteria ameliorate 2,4,6-trinitrobenzenesulfonic acid-induced colitis in mice. J. Microbiol. Biotechnol. 19:708–13.

    Google Scholar 

  19. Fukata, M., A. Chen, A. Klepper, S. Krishnareddy, A. S. Vamadevan, L. S. Thomas, R. Xu, H. Inoue, M. Arditi, A. J. Dannenberg, and M. T. Abreu. 2006. Cox-2 is regulated by Toll-like receptor-4 (TLR4) signaling: role in proliferation and apoptosis in the intestine. Gastroenterology. 131:862–77. doi:10.1053/j.gastro.2006.06.017.

    Article  CAS  PubMed  Google Scholar 

  20. Hollenbach, E., M. Vieth, A. Rosessner, M. Neumann, P. Malfertheiner, and M. Naumann. 2005. Inhibition of RICK/Nuclear factor-kB and p38 signalling attenuates the inflammatory response in a murine model of Crohn disease. J. Biol. Chem. 280:14981–8. doi:10.1074/jbc.M500966200.

    Article  CAS  PubMed  Google Scholar 

  21. Lobenhofer, E. K., P. R. Bushel, C. A. Afshari, and H. K. Hamadeh. 2001. Progress in the application of DNA microarrays. Environ. Health Perspect. 109:881–91. doi:10.2307/3454988.

    Article  CAS  PubMed  Google Scholar 

  22. Mudter, J., and M. F. Neurath. 2003. Mucosal T cells: mediators or guardians of inflammatory bowel disease? Curr. Opin. Gastroenterol. 19:343–9. doi:10.1097/00001574-200307000-00004.

    Article  CAS  PubMed  Google Scholar 

  23. Chow, J. C., D. W. Young, D. T. Golenbock, W. J. Christ, and F. Gusovsky. 1999. Toll-like receptor-4 mediates lipopolysaccharide-induced signal transduction. J. Biol. Chem. 274:10689–92. doi:10.1074/jbc.274.16.10689.

    Article  CAS  PubMed  Google Scholar 

  24. Ingalls, R. R., H. Heine, E. Lien, A. Yoshimura, and D. Golenbock. 1999. Lipopolysaccharide recognition, CD14, and lipopolysaccharide receptors. Infect. Dis. Clin. North Am. 13:341–53. doi:10.1016/S0891-5520(05)70078-7.

    Article  CAS  PubMed  Google Scholar 

  25. Kitamura, K., Y. Nakamoto, S. Kaneko, and N. Mukaida. 2004. Pivotal roles of interleukin-6 in transmural inflammation in murine T cell transfer colitis. J. Leukoc. Biol. 76:1111–7. doi:10.1189/jlb.0604328.

    Article  CAS  PubMed  Google Scholar 

  26. Schreiber, S., S. Nikolaus, J. Hampe, J. Hämling, I. Koop, B. Groessner, H. Lochs, and A. Raedler. 1999. Tumour necrosis factor alpha and interleukin 1beta in relapse of Crohn s disease. Lancet. 353:459–61. doi:10.1016/S0140-6736(98)03339-X.

    Article  CAS  PubMed  Google Scholar 

  27. Pallone, F., and G. Monteleone. 1998. Interleukin 12 and Th1 responses in inflammatory bowel disease. Gut. 43:735–6.

    Article  CAS  PubMed  Google Scholar 

  28. McCormack, G., D. Moriarty, D. P. O’Donoghue, P. A. McCormick, K. Sheahan, and A. W. Baird. 2001. Tissue cytokine and chemokine expression in inflammatory bowel disease. Inflamm. Res. 50:491–5. doi:10.1007/PL00000223.

    Article  CAS  PubMed  Google Scholar 

  29. Papadakis, K. A. 2004. Chemokines in inflammatory bowel disease. Curr. Allergy Asthma Rep. 4:83–9. doi:10.1007/s11882-004-0048-7.

    Article  PubMed  Google Scholar 

  30. Cario, E. D. K. P. 2000. Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun. 68:7010–7. doi:10.1128/IAI.68.12.7010-7017.2000.

    Article  CAS  PubMed  Google Scholar 

  31. Dinarello, C. A. 2002. The IL-1 family and inflammatory diseases. Clin. Exp. Rheumatol. 20:S1–13.

    CAS  PubMed  Google Scholar 

  32. Khan, I., F. M. Al-Awadi, N. Thomas, I. Khan, F. M. Al-Awadi, N. Thomas, S. Haridas, and J. T. Anim. 2002. Cyclooxygenase-2 inhibition and experimental colitis: beneficial effects of phosphorothioated antisense oligonucleotide and meloxicam. Scand. J. Gastroenterol. 37:1428–36. doi:10.1080/003655202762671314.

    Article  CAS  PubMed  Google Scholar 

  33. Di Giacinto, C., M. Marinaro, M. Sanchez, W. Strober, M. Boirivant. 2005. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J. Immunol. 174:3237–46.

    CAS  PubMed  Google Scholar 

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Authors and Affiliations

  1. R & D Center, Korea Yakult Co., Ltd., Yongin, Kyunggi-do, 446-901, South Korea

    Hoyong Lee, Young-Tae Ahn, Jung-Hee Lee & Chul-Sung Huh

  2. Department of Life and Nanopharmaceutical Sciences and Department of Pharmaceutical Science, College of Pharmacy, Kyung Hee University, 1, Hoegi, Dongdaemun-ku, Seoul, 130-701, South Korea

    Jung-Hee Lee & Dong-Hyun Kim

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  1. Hoyong Lee
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Lee, H., Ahn, YT., Lee, JH. et al. Evaluation of Anti-colitic Effect of Lactic Acid Bacteria in Mice by cDNA Microarray Analysis. Inflammation 32, 379–386 (2009). https://doi.org/10.1007/s10753-009-9146-y

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