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Research article
Clinical Microbiology and Biomedical Sciences
A Mixed Formulation of Lactic Acid Bacteria Inhibits Trinitrobenzene-Sulfonic-Acid-Induced Inflammatory Changes of the Colon Tissue in Mice
1School of Biological Sciences, College of Biomedical Sciences and Engineering, Inje University, Gimhae 621-749, Republic of Korea, 2Research and Development Center, Cell Biotech Co., Ltd., Gimpo 415-871, Republic of Korea
Received: March 31, 2014; Accepted: June 2, 2014
J. Microbiol. Biotechnol. 2014; 24(10): 1438-1444
Published October 28, 2014 https://doi.org/10.4014/jmb.1403.03064
Copyright © The Korean Society for Microbiology and Biotechnology.
Abstract
Lactic acid bacteria (LAB) are probiotics that provide numerous beneficial effects on the host
body, especially on the intestine. Combining several strains of LAB, we prepared a
formulation containing four different LAB and studied its anti-inflammatory activity both in
vitro and in vivo. The formulation significantly reduced NO production from RAW 264.7 cells
treated with bacterial lipopolysaccharide, indicating that the formulation might include antiinflammatory
activity. The formulation also suppressed inflammatory change induced by
trinitrobenzene sulfonic acid (TNBS) in mice, where oral or rectal administration of the
formulation protected the colon tissue from the damage by TNBS. Expressions of the IL-6 and
FasL genes appeared to be down-regulated by the formulation in TNBS-treated colon tissues,
suggesting that the suppression of those genes may be involved in the anti-inflammatory
activity of the formulation.
Keywords
anti-inflammation, probiotics, IBD, IL-6, FasL, Nitric Oxide
References
- Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, et al. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6: 583-588.
- Baumgart DC, Carding SR. 2007. Inflammatory bowel disease: cause and immunobiology. Lancet 369: 1627-1640.
- Baumgart DC, Sandborn WJ. 2007. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 369: 1641-1657.
- Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M. 2013. Probiotics: properties, examples, and specific applications. Cold Spring Harb. Perspect. Med. 3: 1-15.
- Conte MP, Schippa S. Zamboni I, Penta M, Chiarini F, Seganti L, et al. 2006. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut. 55: 1760-1767.
- Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, Roy D. 2008. Immunomodulatory effects of probiotics in the intestinal tract. Curr. Issues Mol. Biol. 10: 37-54.
- Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
- Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR, et al. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126: 131138.
- Hong T, Jin G, Yoshino G, Miura M, Maeda Y, Cho S, Cyong J. 2002. Protective effects of Polygalae root in experimental TNBS-induced colitis in mice. J. Ethnopharmacol. 79: 341-346.
- Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Jarvenpaa S, et al. 2008. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J. Gastroenterol. 14: 2029-2036.
- Larsson A, Melgar S, Rehnström E, Michaëlsson E, Svensson L, Hockings P, et al. 2006. MRI of colon wall thickness - a biomarker in experimental mouse inflammatory disease? Inflamm. Bowel Dis. 12: 478-485.
- LeBlanc JG, de Moreno de Leblanc A, Perdigón G, Miyoshi A, Rochat T, Bermudez-Humaran L, et al. 2008. Antiinflammatory properties of lactic acid bacteria: current knowledge, applications and prospects. Antiinfect. Agents Med. Chem. 7: 148-154.
- Leon F, Smythies LE, Smith PD, Kelsall BL. 2006. Involvement of dendritic cells in the pathogenesis of inflammatory bowel disease. Adv. Exp. Med. Biol. 579: 117-132.
- Lettau M, Paulsen M, Schmidt H, Janssen O. 2011. Insights into the molecular regulation of FasL (CD178) biology. Eur. J. Cell Biol. 90: 456-466.
- Lin WW, Hsieh SL. 2011. Decoy receptor 3: a pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer. Biochem. Pharmacol. 81:838-847.
- Masood MI, Qadir MI, Shirazi JH, Khan IU. 2011. Beneficial effects of lactic acid bacteria on human beings. Crit. Rev. Microbiol. 37: 91-98.
- Mudter J, Amoussina L, Schenk M, Yu J, Brüstle A, Weigmann B, et al. 2008. The transcription factor IFN regulatory factor-4 controls experimental colitis in mice via T cell-derived IL-6. J. Clin. Invest. 118: 2415-2426.
- Nakano K, Saito K, Mine S, Matsushita S, Tanaka Y. 2007. FasL expressed on activated T cell, interact with Fas homeostasis. Apoptosis 12: 45-54.
- Prideaux L, Kamm MA, de Cruz PP, Chan FKL, Ng SC. 2012. Inflammatory bowel disease in Asia: a systematic review. J. Gastroenterol. Hepatol. 27: 1266-1280.
- Purchiaroni F, Tortora A, Gabrielli M, Bertucci F, Gigante G, Ianiro G, et al. 2013. The role of intestinal microbiota and the immune system. Eur. Rev. Med. Pharmacol. Sci. 17: 323333.
- Sacco R, Waters W, Rudolph K, Drew M. 2006. Comparative nitric oxide production by LPS-stimulated monocytederived macrophages from Ovis canadensis and Ovis aries. Comp. Immunol. Microbiol. Infect. Dis. 29: 1-11.
- Schultsz C, Van Den Berg FM, Ten Kate FW, Tytgat GN, Dankert J. 1999. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117: 10891097.
- Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, et al. 2003. Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut 52: 237-242.
- Seo JG, Chung MJ, Lee HG. 2011. Alleviation of atopic dermatitis through probiotic and mixed-probiotic treatments in an atopic dermatitis model. Korean J. Food Sci. Anim. Resour. 31: 420-427.
- Souza HS, Tortori CJ, Castelo-Branco MT, Carvalho AT, Margallo VS, Delgado CF, et al. 2005. Apoptosis in the intestinal mucosa of patients with inflammatory bowel disease: evidence of altered expression of FasL and perforin cytotoxic pathways. Int. J. Colorectal Dis. 20: 277-286.
- Triantafillidis J, Merikas E, Georgopoulos F. 2011. Current and emerging drugs for the treatment of inflammatory bowel disease. Drug Des. Devel. Ther. 5: 185-210.
- Villa-Morales M, Fernández-Piqueras J. 2012. Targeting the Fas/FasL signaling pathway in cancer therapy. Expert Opin. Ther. Targets 16: 85-101.
- Wang K, Yuan CP, Wang W, Yang ZQ, Cui W, Mu LZ, et al. 2010. Expression of interleukin 6 in brain and colon of rats with TNBS-induced colitis. World J. Gastroenterol. 16: 22522259.
- Weigelin B, Krause M, Friedl P. 2011. Cytotoxic T lymphocyte migration and effector function in the tumor microenvironment. Immunol. Lett. 138: 19-21.
- Xavier R, Podolsky D. 2007. Unraveling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
- Yamamoto J, Maeno K, Takada T, Kakutani K, Yurube T, Zhang Z, et al. 2013. Fas ligand plays an important role for the production of pro-inflammatory cytokines in intervertebral disc nucleus pulposus cells. J. Orthop. Res. 31: 608-615.
- Yukawa M, Iizuka M, Horie Y, Yoneyama K, Shirasaka T, Itou H, et al. 2002. Systemic and local evidence of increased Fas-mediated apoptosis in ulcerative colitis. Int. J. Colorectal Dis. 17: 70-76.
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Research article
J. Microbiol. Biotechnol. 2014; 24(10): 1438-1444
Published online October 28, 2014 https://doi.org/10.4014/jmb.1403.03064
Copyright © The Korean Society for Microbiology and Biotechnology.
A Mixed Formulation of Lactic Acid Bacteria Inhibits Trinitrobenzene-Sulfonic-Acid-Induced Inflammatory Changes of the Colon Tissue in Mice
Yeon Suk Cha 1, Jae-Gu Seo 2, Myung-Jun Chung 2, Chung Won Cho 1 and Hyun Joo Youn 1*
1School of Biological Sciences, College of Biomedical Sciences and Engineering, Inje University, Gimhae 621-749, Republic of Korea, 2Research and Development Center, Cell Biotech Co., Ltd., Gimpo 415-871, Republic of Korea
Received: March 31, 2014; Accepted: June 2, 2014
Abstract
Lactic acid bacteria (LAB) are probiotics that provide numerous beneficial effects on the host
body, especially on the intestine. Combining several strains of LAB, we prepared a
formulation containing four different LAB and studied its anti-inflammatory activity both in
vitro and in vivo. The formulation significantly reduced NO production from RAW 264.7 cells
treated with bacterial lipopolysaccharide, indicating that the formulation might include antiinflammatory
activity. The formulation also suppressed inflammatory change induced by
trinitrobenzene sulfonic acid (TNBS) in mice, where oral or rectal administration of the
formulation protected the colon tissue from the damage by TNBS. Expressions of the IL-6 and
FasL genes appeared to be down-regulated by the formulation in TNBS-treated colon tissues,
suggesting that the suppression of those genes may be involved in the anti-inflammatory
activity of the formulation.
Keywords: anti-inflammation, probiotics, IBD, IL-6, FasL, Nitric Oxide
References
- Atreya R, Mudter J, Finotto S, Mullberg J, Jostock T, Wirtz S, et al. 2000. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat. Med. 6: 583-588.
- Baumgart DC, Carding SR. 2007. Inflammatory bowel disease: cause and immunobiology. Lancet 369: 1627-1640.
- Baumgart DC, Sandborn WJ. 2007. Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 369: 1641-1657.
- Behnsen J, Deriu E, Sassone-Corsi M, Raffatellu M. 2013. Probiotics: properties, examples, and specific applications. Cold Spring Harb. Perspect. Med. 3: 1-15.
- Conte MP, Schippa S. Zamboni I, Penta M, Chiarini F, Seganti L, et al. 2006. Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut. 55: 1760-1767.
- Delcenserie V, Martel D, Lamoureux M, Amiot J, Boutin Y, Roy D. 2008. Immunomodulatory effects of probiotics in the intestinal tract. Curr. Issues Mol. Biol. 10: 37-54.
- Fuller R. 1989. Probiotics in man and animals. J. Appl. Bacteriol. 66: 365-378.
- Green LC, Wagner DA, Glogowski J, Skipper PL, Wishnok JS, Tannenbaum SR, et al. 1982. Analysis of nitrate, nitrite, and [15N]nitrate in biological fluids. Anal. Biochem. 126: 131138.
- Hong T, Jin G, Yoshino G, Miura M, Maeda Y, Cho S, Cyong J. 2002. Protective effects of Polygalae root in experimental TNBS-induced colitis in mice. J. Ethnopharmacol. 79: 341-346.
- Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Jarvenpaa S, et al. 2008. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J. Gastroenterol. 14: 2029-2036.
- Larsson A, Melgar S, Rehnström E, Michaëlsson E, Svensson L, Hockings P, et al. 2006. MRI of colon wall thickness - a biomarker in experimental mouse inflammatory disease? Inflamm. Bowel Dis. 12: 478-485.
- LeBlanc JG, de Moreno de Leblanc A, Perdigón G, Miyoshi A, Rochat T, Bermudez-Humaran L, et al. 2008. Antiinflammatory properties of lactic acid bacteria: current knowledge, applications and prospects. Antiinfect. Agents Med. Chem. 7: 148-154.
- Leon F, Smythies LE, Smith PD, Kelsall BL. 2006. Involvement of dendritic cells in the pathogenesis of inflammatory bowel disease. Adv. Exp. Med. Biol. 579: 117-132.
- Lettau M, Paulsen M, Schmidt H, Janssen O. 2011. Insights into the molecular regulation of FasL (CD178) biology. Eur. J. Cell Biol. 90: 456-466.
- Lin WW, Hsieh SL. 2011. Decoy receptor 3: a pleiotropic immunomodulator and biomarker for inflammatory diseases, autoimmune diseases and cancer. Biochem. Pharmacol. 81:838-847.
- Masood MI, Qadir MI, Shirazi JH, Khan IU. 2011. Beneficial effects of lactic acid bacteria on human beings. Crit. Rev. Microbiol. 37: 91-98.
- Mudter J, Amoussina L, Schenk M, Yu J, Brüstle A, Weigmann B, et al. 2008. The transcription factor IFN regulatory factor-4 controls experimental colitis in mice via T cell-derived IL-6. J. Clin. Invest. 118: 2415-2426.
- Nakano K, Saito K, Mine S, Matsushita S, Tanaka Y. 2007. FasL expressed on activated T cell, interact with Fas homeostasis. Apoptosis 12: 45-54.
- Prideaux L, Kamm MA, de Cruz PP, Chan FKL, Ng SC. 2012. Inflammatory bowel disease in Asia: a systematic review. J. Gastroenterol. Hepatol. 27: 1266-1280.
- Purchiaroni F, Tortora A, Gabrielli M, Bertucci F, Gigante G, Ianiro G, et al. 2013. The role of intestinal microbiota and the immune system. Eur. Rev. Med. Pharmacol. Sci. 17: 323333.
- Sacco R, Waters W, Rudolph K, Drew M. 2006. Comparative nitric oxide production by LPS-stimulated monocytederived macrophages from Ovis canadensis and Ovis aries. Comp. Immunol. Microbiol. Infect. Dis. 29: 1-11.
- Schultsz C, Van Den Berg FM, Ten Kate FW, Tytgat GN, Dankert J. 1999. The intestinal mucus layer from patients with inflammatory bowel disease harbors high numbers of bacteria compared with controls. Gastroenterology 117: 10891097.
- Seksik P, Rigottier-Gois L, Gramet G, Sutren M, Pochart P, Marteau P, et al. 2003. Alterations of the dominant faecal bacterial groups in patients with Crohn’s disease of the colon. Gut 52: 237-242.
- Seo JG, Chung MJ, Lee HG. 2011. Alleviation of atopic dermatitis through probiotic and mixed-probiotic treatments in an atopic dermatitis model. Korean J. Food Sci. Anim. Resour. 31: 420-427.
- Souza HS, Tortori CJ, Castelo-Branco MT, Carvalho AT, Margallo VS, Delgado CF, et al. 2005. Apoptosis in the intestinal mucosa of patients with inflammatory bowel disease: evidence of altered expression of FasL and perforin cytotoxic pathways. Int. J. Colorectal Dis. 20: 277-286.
- Triantafillidis J, Merikas E, Georgopoulos F. 2011. Current and emerging drugs for the treatment of inflammatory bowel disease. Drug Des. Devel. Ther. 5: 185-210.
- Villa-Morales M, Fernández-Piqueras J. 2012. Targeting the Fas/FasL signaling pathway in cancer therapy. Expert Opin. Ther. Targets 16: 85-101.
- Wang K, Yuan CP, Wang W, Yang ZQ, Cui W, Mu LZ, et al. 2010. Expression of interleukin 6 in brain and colon of rats with TNBS-induced colitis. World J. Gastroenterol. 16: 22522259.
- Weigelin B, Krause M, Friedl P. 2011. Cytotoxic T lymphocyte migration and effector function in the tumor microenvironment. Immunol. Lett. 138: 19-21.
- Xavier R, Podolsky D. 2007. Unraveling the pathogenesis of inflammatory bowel disease. Nature 448: 427-434.
- Yamamoto J, Maeno K, Takada T, Kakutani K, Yurube T, Zhang Z, et al. 2013. Fas ligand plays an important role for the production of pro-inflammatory cytokines in intervertebral disc nucleus pulposus cells. J. Orthop. Res. 31: 608-615.
- Yukawa M, Iizuka M, Horie Y, Yoneyama K, Shirasaka T, Itou H, et al. 2002. Systemic and local evidence of increased Fas-mediated apoptosis in ulcerative colitis. Int. J. Colorectal Dis. 17: 70-76.
