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Research article

Food Microbiology and Biotechnology

Effect of Probiotics Lactobacillus and Bifidobacterium on Gut-Derived Lipopolysaccharides and Inflammatory Cytokines: An In Vitro Study Using a Human Colonic Microbiota Model

Laetitia Rodes 1, Afshan Khan 1, Arghya Paul 1, Michael Coussa-Charley 1, Daniel Marinescu 1, Catherine Tomaro-Duchesneau 1, Wei Shao 1, Imen Kahouli 1, 2 and Satya Prakash 1*

1Biomedical Technology and Cell Therapy Research Laboratory, Department of Biomedical Engineering and Artificial Cells and Organs Research Centre, Faculty of Medicine, McGill University, Quebec, H3A 2B4, Canada, 1Department of Experimental Medicine, McGill University, H3A 2B4, Canada

Received: May 9, 2012; Accepted: December 2, 2012

J. Microbiol. Biotechnol. 2013; 23(4): 518-526

Published April 28, 2013 https://doi.org/10.4014/jmb.1205.05018

Copyright © The Korean Society for Microbiology and Biotechnology.

Abstract

Gut-derived lipopolysaccharides (LPS) are critical to the development and progression of chronic low-grade inflammation and metabolic diseases. In this study, the effects of probiotics Lactobacillus and Bifidobacterium on gut-derived lipopolysaccharide and inflammatory cytokine concentrations were evaluated using a human colonic microbiota model. Lactobacillus reuteri, L. rhamnosus, L. plantarum, Bifidobacterium animalis, B. bifidum, B. longum, and B. longum subsp. infantis were identified from the literature for their anti-inflammatory potential. Each bacterial culture was administered daily to a human colonic microbiota model during 14 days. Colonic lipopolysaccharides, and Gram-positive and negative bacteria were quantified. RAW 264.7 macrophage cells were stimulated with supernatant from the human colonic microbiota model. Concentrations of TNF-α, IL-1β, and IL-4 cytokines were measured. Lipopolysaccharide concentrations were significantly reduced with the administration of B. bifidum (-46.45 ± 5.65%), L. rhamnosus (-30.40 ± 5.08%), B. longum (-42.50 ± 1.28%), and B. longum subsp. infantis (-68.85 ± 5.32%) (p < 0.05). Cell counts of Gram-negative and positive bacteria were distinctly affected by the probiotic administered. There was a probiotic strain-specific effect on immunomodulatory responses of RAW 264.7 macrophage cells. B. longum subsp. infantis demonstrated higher capacities to reduce TNF-α concentrations (-69.41 ± 2.78%; p < 0.05) and to increase IL-4 concentrations (+16.50 ± 0.59%; p < 0.05). Colonic lipopolysaccharides were significantly correlated with TNF-α and IL-1β concentrations (p < 0.05). These findings suggest that specific probiotic bacteria, such as B. longum subsp. infantis, might decrease colonic lipopolysaccharide concentrations, which might reduce the proinflammatory tone. This study has noteworthy applications in the field of biotherapeutics for the prevention and/or treatment of inflammatory and metabolic diseases.

Keywords

Lactobacilli, Cytokines, Bifidobacteria, Colonic model, Inflammation, Lipopolysaccharide

References

  1. Alisi, A., M. Manco, R. Devito, F. Piemonte, and V. Nobili. 2010. Endotoxin and plasminogen activator inhibitor-1 serum levels associated with nonalcoholic steatohepatitis in children. J. Pediatr. Gastroenterol. Nutr. 50: 645-649.
    Pubmed CrossRef
  2. Bahrami, B., M. W. Child, S. Macfarlane, and G. T. Macfarlane. 2011. Adherence and cytokine induction in Caco-2 cells by bacterial populations from a three-stage continuous-culture model of the large intestine. Appl. Environ. Microbiol. 77: 29342942.
    Pubmed PMC CrossRef
  3. Bispo, P. J., G. B. de Melo, A. L. Hofling-Lima, and A. C. Pignatari. 2011. Detection and Gram discrimination of bacterial pathogens from aqueous and vitreous humor using real-time PCR assays. Invest. Ophthalmol. Vis. Sci. 52: 873-881.
    Pubmed CrossRef
  4. Borthakur, A., A. N. Anbazhagan, A. Kumar, G. Raheja, V. Singh, K. Ramaswamy, and P. K. Dudeja. 2010. The probiotic Lactobacillus plantarum counteracts TNF-{alpha}-induced downregulation of SMCT1 expression and function. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G928-G934.
    Pubmed PMC CrossRef
  5. Cani, P. D., J. Amar, M. A. Iglesias, M. Poggi, C. Knauf, D. Bastelica, et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772.
    Pubmed CrossRef
  6. Cani, P. D., R. Bibiloni, C. Knauf, A. Waget, A. M. Neyrinck, N. M. Delzenne, and R. Burcelin. 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481.
    Pubmed CrossRef
  7. Cani, P. D., A. M. Neyrinck, F. Fava, C. Knauf, R. G. Burcelin, K. M. Tuohy, et al. 2007. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50: 2374-2383.
    Pubmed CrossRef
  8. Cani, P. D., S. Possemiers, T. Van de Wiele, Y. Guiot, A. Everard, O. Rottier, et al. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103.
    Pubmed PMC CrossRef
  9. Chawla, A., K. D. Nguyen, and Y. P. Goh. 2011. Macrophagemediated inflammation in metabolic disease. Nat. Rev. Immunol. 11: 738-749.
    Pubmed PMC CrossRef
  10. Chon, H. and B. Choi. 2010. The effects of a vegetable-derived probiotic lactic acid bacterium on the immune response. Microbiol. Immunol. 54: 228-236.
    Pubmed CrossRef
  11. Chon, H., B. Choi, E. Lee, S. Lee, and G. Jeong. 2009. Immunomodulatory effects of specific bacterial components of Lactobacillus plantarum KFCC11389P on the murine macrophage cell line RAW 264.7. J. Appl. Microbiol. 107: 1588-1597.
    Pubmed CrossRef
  12. Coombes, J. L. and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435-446.
    Pubmed PMC CrossRef
  13. De, P. G., J. Cinova, R. Stepankova, L. Tuckova, and Y. Sanz. 2009. Pivotal advance: Bifidobacteria and Gram-negative bacteria differentially influence immune responses in the proinflammatory milieu of celiac disease. J. Leukoc. Biol. 87: 765-778.
  14. Ewaschuk, J. B., H. Diaz, L. Meddings, B. Diederichs, A. Dmytrash, J. Backer, et al. 2008. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G1025-G1034.
    Pubmed CrossRef
  15. Forsyth, C. B., A. Farhadi, S. M. Jakate, Y. Tang, M. Shaikh, and A. Keshavarzian. 2009. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43: 163-172.
    Pubmed PMC CrossRef
  16. Gordon, S. 2007. The macrophage: Past, present and future. Eur. J. Immunol. 37 (Suppl 1): S9-S17.
    Pubmed CrossRef
  17. Goris, H., S. Daenen, M. R. Halie, and D. van der Waaij. 1986. Effect of intestinal flora modulation by oral polymyxin treatment on hemopoietic stem cell kinetics in mice. Acta Haematol. 76:44-49.
    Pubmed CrossRef
  18. Goris, H., F. de Boer, and D. van der Waaij. 1985. Myelopoiesis in experimentally contaminated specific-pathogen-free and germfree mice during oral administration of polymyxin. Infect. Immun. 50: 437-441.
    Pubmed PMC
  19. Gosselink, M. P., W. R. Schouten, L. M. van Lieshout, W. C. Hop, J. D. Laman, and J. G. Ruseler-Van Embden. 2004. Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis. Colon Rectum 47: 876-884.
    Pubmed CrossRef
  20. Grimm, M. C., W. E. Pullman, G. M. Bennett, P. J. Sullivan, P. Pavli, and W. F. Doe. 1995. Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J. Gastroenterol. Hepatol. 10: 387-395.
    Pubmed CrossRef
  21. Kamada, N., T. Hisamatsu, S. Okamoto, H. Chinen, T. Kobayashi, T. Sato, et al. 2008. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFNgamma axis. J. Clin. Invest. 118: 2269-2280.
    Pubmed PMC
  22. Karimi, K., M. D. Inman, J. Bienenstock, and P. Forsythe. 2009. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179: 186-193.
    Pubmed CrossRef
  23. Kawai, T. and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
    Pubmed CrossRef
  24. Kim, D. W., S. B. Cho, H. J. Lee, W. T. Chung, K. H. Kim, J. Hwangbo, et al. 2007. Comparison of cytokine and nitric oxide induction in murine macrophages between whole cell and enzymatically digested Bifidobacterium sp. obtained from monogastric animals. J. Microbiol. 45: 305-310.
    Pubmed
  25. Larsen, N., F. K. Vogensen, F. W. van den Berg, D. S. Nielsen, A. S. Andreasen, B. K. Pedersen, et al. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5: e9085.
    Pubmed PMC CrossRef
  26. Leeson, M. C., Y. Fujihara, and D. C. Morrison. 1994. Evidence for lipopolysaccharide as the predominant proinflammatory mediator in supernatants of antibiotic-treated bacteria. Infect. Immun. 62: 4975-4980.
    Pubmed PMC
  27. Lopez, P., M. Gueimonde, A. Margolles, and A. Suarez. 2010. Distinct Bifidobacterium strains drive different immune responses in vitro. Int. J. Food Microbiol. 138: 157-165.
    Pubmed CrossRef
  28. Lu, Y. C., W. C. Yeh, and P. S. Ohashi. 2008. LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151.
    Pubmed CrossRef
  29. Ma, D., P. Forsythe, and J. Bienenstock. 2004. Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect. Immun. 72: 5308-5314.
    Pubmed PMC CrossRef
  30. Madsen, K. L., J. S. Doyle, L. D. Jewell, M. M. Tavernini, and R. N. Fedorak. 1999. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 11071114.
    CrossRef
  31. Maitra, U., H. Deng, T. Glaros, B. Baker, D. G. Capelluto, Z. Li, and L. Li. 2012. Molecular mechanisms responsible for the selective and low-grade induction of proinflammatory mediators in murine macrophages by lipopolysaccharide. J. Immunol. 189:1014-1023.
    Pubmed CrossRef
  32. Mao, Y., S. Nobaek, B. Kasravi, D. Adawi, U. Stenram, G. Molin, and B. Jeppsson. 1996. The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 111: 334-344.
    Pubmed CrossRef
  33. Mehta, N. N., F. C. McGillicuddy, P. D. Anderson, C. C. Hinkle, R. Shah, L. Pruscino, et al. 2010. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59: 172-181.
    Pubmed PMC CrossRef
  34. Mutlu, E., A. Keshavarzian, P. Engen, C. B. Forsyth, M. Sikaroodi, and P. Gillevet. 2009. Intestinal dysbiosis: A possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin. Exp. Res. 33: 1836-1846.
    Pubmed CrossRef
  35. O’Mahony, C., P. Scully, D. O’Mahony, S. Murphy, F. O’Brien, A. Lyons, et al. 2008. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog. 4: e1000112.
    Pubmed PMC CrossRef
  36. Pena, J. A., A. B. Rogers, Z. Ge, V. Ng, S. Y. Li, J. G. Fox, and J. Versalovic. 2005. Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect. Immun. 73: 912-920.
    Pubmed PMC CrossRef
  37. Prakash, S., L. Rodes, M. Coussa-Charley, and C. TomaroDuchesneau. 2011. Gut microbiota: Next frontier in understanding human health and development of biotherapeutics. Biologics 5:71-86.
    Pubmed PMC CrossRef
  38. Rodes, L., A. Paul, M. Coussa-Charley, H. Al-Salami, C. Tomaro-Duchesneau, M. Fakhoury, and S. Prakash. 2011. Transit time affects the community stability of Lactobacillus and Bifidobacterium species in an in vitro model of human colonic microbiotia. Artif. Cells Blood Substit. Immobil. Biotechnol. 39: 351-356.
    Pubmed CrossRef
  39. Roselli, M., A. Finamore, M. S. Britti, and E. Mengheri. 2006. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br. J. Nutr. 95: 1177-1184.
    Pubmed CrossRef
  40. Schiffrin, E. J., A. Parlesak, C. Bode, J. C. Bode, M. A. van’t Hof, D. Grathwohl, and Y. Guigoz. 2009. Probiotic yogurt in the elderly with intestinal bacterial overgrowth: Endotoxaemia and innate immune functions. Br. J. Nutr. 101: 961-966.
    Pubmed CrossRef
  41. Schultz, M., C. Veltkamp, L. A. Dieleman, W. B. Grenther, P. B. Wyrick, S. L. Tonkonogy, and R. B. Sartor. 2002. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8:71-80.
    Pubmed CrossRef
  42. Smith, P. D., L. E. Smythies, M. Mosteller-Barnum, D. A. Sibley, M. W. Russell, M. Merger, et al. 2001. Intestinal macrophages lack CD14 and CD89 and consequently are downregulated for LPS- and IgA-mediated activities. J. Immunol. 167: 2651-2656.
    Pubmed
  43. Smith, P. D., L. E. Smythies, R. Shen, T. Greenwell-Wild, M. Gliozzi, and S. M. Wahl. 2011. Intestinal macrophages and response to microbial encroachment. Mucosal Immunol. 4: 3142.
    Pubmed CrossRef
  44. Smythies, L. E., M. Sellers, R. H. Clements, M. MostellerBarnum, G. Meng, W. H. Benjamin, et al. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115: 66-75.
    Pubmed PMC
  45. Stagg, A. J., A. L. Hart, S. C. Knight, and M. A. Kamm. 2003. The dendritic cell: Its role in intestinal inflammation and relationship with gut bacteria. Gut 52: 1522-1529.
    Pubmed PMC CrossRef
  46. Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457: 480-484.
    Pubmed PMC CrossRef
  47. Veiga, P., C. A. Gallini, C. Beal, M. Michaud, M. L. Delaney, A. DuBois, et al. 2010. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl. Acad. Sci. USA 107:18132-18137.
    Pubmed PMC CrossRef
  48. Xia, Y., H. Q. Chen, M. Zhang, Y. Q. Jiang, X. M. Hang, and H. L. Qin. 2011. Effect of Lactobacillus plantarum LP-Onlly on gut flora and colitis in interleukin-10 knockout mice. J. Gastroenterol. Hepatol. 26: 405-411.
    Pubmed CrossRef
  49. Zeuthen, L. H., H. R. Christensen, and H. Frokiaer. 2006. Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with Gramnegative bacteria. Clin. Vaccine Immunol. 13: 365-375.
    Pubmed PMC CrossRef
  50. Zhang, W., Y. Gu, Y. Chen, H. Deng, L. Chen, S. Chen, G. Zhang, and Z. Gao. 2010. Intestinal flora imbalance results in altered bacterial translocation and liver function in rats with experimental cirrhosis. Eur. J. Gastroenterol. Hepatol. 22:1481-1486.
    Pubmed

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Article

Research article

J. Microbiol. Biotechnol. 2013; 23(4): 518-526

Published online April 28, 2013 https://doi.org/10.4014/jmb.1205.05018

Copyright © The Korean Society for Microbiology and Biotechnology.

Effect of Probiotics Lactobacillus and Bifidobacterium on Gut-Derived Lipopolysaccharides and Inflammatory Cytokines: An In Vitro Study Using a Human Colonic Microbiota Model

Laetitia Rodes 1, Afshan Khan 1, Arghya Paul 1, Michael Coussa-Charley 1, Daniel Marinescu 1, Catherine Tomaro-Duchesneau 1, Wei Shao 1, Imen Kahouli 1, 2 and Satya Prakash 1*

1Biomedical Technology and Cell Therapy Research Laboratory, Department of Biomedical Engineering and Artificial Cells and Organs Research Centre, Faculty of Medicine, McGill University, Quebec, H3A 2B4, Canada, 1Department of Experimental Medicine, McGill University, H3A 2B4, Canada

Received: May 9, 2012; Accepted: December 2, 2012

Abstract

Gut-derived lipopolysaccharides (LPS) are critical to
the development and progression of chronic low-grade
inflammation and metabolic diseases. In this study, the
effects of probiotics Lactobacillus and Bifidobacterium on
gut-derived lipopolysaccharide and inflammatory cytokine
concentrations were evaluated using a human colonic
microbiota model. Lactobacillus reuteri, L. rhamnosus, L.
plantarum, Bifidobacterium animalis, B. bifidum, B. longum,
and B. longum subsp. infantis were identified from the
literature for their anti-inflammatory potential. Each
bacterial culture was administered daily to a human colonic
microbiota model during 14 days. Colonic lipopolysaccharides,
and Gram-positive and negative bacteria were quantified.
RAW 264.7 macrophage cells were stimulated with
supernatant from the human colonic microbiota model.
Concentrations of TNF-α, IL-1β, and IL-4 cytokines
were measured. Lipopolysaccharide concentrations were
significantly reduced with the administration of B. bifidum
(-46.45 ± 5.65%), L. rhamnosus (-30.40 ± 5.08%), B. longum
(-42.50 ± 1.28%), and B. longum subsp. infantis (-68.85 ±
5.32%) (p < 0.05). Cell counts of Gram-negative and
positive bacteria were distinctly affected by the probiotic
administered. There was a probiotic strain-specific effect on
immunomodulatory responses of RAW 264.7 macrophage
cells. B. longum subsp. infantis demonstrated higher
capacities to reduce TNF-α concentrations (-69.41 ± 2.78%;
p < 0.05) and to increase IL-4 concentrations (+16.50 ± 0.59%;
p < 0.05). Colonic lipopolysaccharides were significantly
correlated with TNF-α and IL-1β concentrations (p < 0.05).
These findings suggest that specific probiotic bacteria,
such as B. longum subsp. infantis, might decrease colonic
lipopolysaccharide concentrations, which might reduce
the proinflammatory tone. This study has noteworthy
applications in the field of biotherapeutics for the prevention
and/or treatment of inflammatory and metabolic diseases.

Keywords: Lactobacilli, Cytokines, Bifidobacteria, Colonic model, Inflammation, Lipopolysaccharide

References

  1. Alisi, A., M. Manco, R. Devito, F. Piemonte, and V. Nobili. 2010. Endotoxin and plasminogen activator inhibitor-1 serum levels associated with nonalcoholic steatohepatitis in children. J. Pediatr. Gastroenterol. Nutr. 50: 645-649.
    Pubmed CrossRef
  2. Bahrami, B., M. W. Child, S. Macfarlane, and G. T. Macfarlane. 2011. Adherence and cytokine induction in Caco-2 cells by bacterial populations from a three-stage continuous-culture model of the large intestine. Appl. Environ. Microbiol. 77: 29342942.
    Pubmed KoreaMed CrossRef
  3. Bispo, P. J., G. B. de Melo, A. L. Hofling-Lima, and A. C. Pignatari. 2011. Detection and Gram discrimination of bacterial pathogens from aqueous and vitreous humor using real-time PCR assays. Invest. Ophthalmol. Vis. Sci. 52: 873-881.
    Pubmed CrossRef
  4. Borthakur, A., A. N. Anbazhagan, A. Kumar, G. Raheja, V. Singh, K. Ramaswamy, and P. K. Dudeja. 2010. The probiotic Lactobacillus plantarum counteracts TNF-{alpha}-induced downregulation of SMCT1 expression and function. Am. J. Physiol. Gastrointest. Liver Physiol. 299: G928-G934.
    Pubmed KoreaMed CrossRef
  5. Cani, P. D., J. Amar, M. A. Iglesias, M. Poggi, C. Knauf, D. Bastelica, et al. 2007. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 56: 1761-1772.
    Pubmed CrossRef
  6. Cani, P. D., R. Bibiloni, C. Knauf, A. Waget, A. M. Neyrinck, N. M. Delzenne, and R. Burcelin. 2008. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes 57: 1470-1481.
    Pubmed CrossRef
  7. Cani, P. D., A. M. Neyrinck, F. Fava, C. Knauf, R. G. Burcelin, K. M. Tuohy, et al. 2007. Selective increases of bifidobacteria in gut microflora improve high-fat-diet-induced diabetes in mice through a mechanism associated with endotoxaemia. Diabetologia 50: 2374-2383.
    Pubmed CrossRef
  8. Cani, P. D., S. Possemiers, T. Van de Wiele, Y. Guiot, A. Everard, O. Rottier, et al. 2009. Changes in gut microbiota control inflammation in obese mice through a mechanism involving GLP-2-driven improvement of gut permeability. Gut 58: 1091-1103.
    Pubmed KoreaMed CrossRef
  9. Chawla, A., K. D. Nguyen, and Y. P. Goh. 2011. Macrophagemediated inflammation in metabolic disease. Nat. Rev. Immunol. 11: 738-749.
    Pubmed KoreaMed CrossRef
  10. Chon, H. and B. Choi. 2010. The effects of a vegetable-derived probiotic lactic acid bacterium on the immune response. Microbiol. Immunol. 54: 228-236.
    Pubmed CrossRef
  11. Chon, H., B. Choi, E. Lee, S. Lee, and G. Jeong. 2009. Immunomodulatory effects of specific bacterial components of Lactobacillus plantarum KFCC11389P on the murine macrophage cell line RAW 264.7. J. Appl. Microbiol. 107: 1588-1597.
    Pubmed CrossRef
  12. Coombes, J. L. and F. Powrie. 2008. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8: 435-446.
    Pubmed KoreaMed CrossRef
  13. De, P. G., J. Cinova, R. Stepankova, L. Tuckova, and Y. Sanz. 2009. Pivotal advance: Bifidobacteria and Gram-negative bacteria differentially influence immune responses in the proinflammatory milieu of celiac disease. J. Leukoc. Biol. 87: 765-778.
  14. Ewaschuk, J. B., H. Diaz, L. Meddings, B. Diederichs, A. Dmytrash, J. Backer, et al. 2008. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 295: G1025-G1034.
    Pubmed CrossRef
  15. Forsyth, C. B., A. Farhadi, S. M. Jakate, Y. Tang, M. Shaikh, and A. Keshavarzian. 2009. Lactobacillus GG treatment ameliorates alcohol-induced intestinal oxidative stress, gut leakiness, and liver injury in a rat model of alcoholic steatohepatitis. Alcohol 43: 163-172.
    Pubmed KoreaMed CrossRef
  16. Gordon, S. 2007. The macrophage: Past, present and future. Eur. J. Immunol. 37 (Suppl 1): S9-S17.
    Pubmed CrossRef
  17. Goris, H., S. Daenen, M. R. Halie, and D. van der Waaij. 1986. Effect of intestinal flora modulation by oral polymyxin treatment on hemopoietic stem cell kinetics in mice. Acta Haematol. 76:44-49.
    Pubmed CrossRef
  18. Goris, H., F. de Boer, and D. van der Waaij. 1985. Myelopoiesis in experimentally contaminated specific-pathogen-free and germfree mice during oral administration of polymyxin. Infect. Immun. 50: 437-441.
    Pubmed KoreaMed
  19. Gosselink, M. P., W. R. Schouten, L. M. van Lieshout, W. C. Hop, J. D. Laman, and J. G. Ruseler-Van Embden. 2004. Delay of the first onset of pouchitis by oral intake of the probiotic strain Lactobacillus rhamnosus GG. Dis. Colon Rectum 47: 876-884.
    Pubmed CrossRef
  20. Grimm, M. C., W. E. Pullman, G. M. Bennett, P. J. Sullivan, P. Pavli, and W. F. Doe. 1995. Direct evidence of monocyte recruitment to inflammatory bowel disease mucosa. J. Gastroenterol. Hepatol. 10: 387-395.
    Pubmed CrossRef
  21. Kamada, N., T. Hisamatsu, S. Okamoto, H. Chinen, T. Kobayashi, T. Sato, et al. 2008. Unique CD14 intestinal macrophages contribute to the pathogenesis of Crohn disease via IL-23/IFNgamma axis. J. Clin. Invest. 118: 2269-2280.
    Pubmed KoreaMed
  22. Karimi, K., M. D. Inman, J. Bienenstock, and P. Forsythe. 2009. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am. J. Respir. Crit. Care Med. 179: 186-193.
    Pubmed CrossRef
  23. Kawai, T. and S. Akira. 2011. Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34: 637-650.
    Pubmed CrossRef
  24. Kim, D. W., S. B. Cho, H. J. Lee, W. T. Chung, K. H. Kim, J. Hwangbo, et al. 2007. Comparison of cytokine and nitric oxide induction in murine macrophages between whole cell and enzymatically digested Bifidobacterium sp. obtained from monogastric animals. J. Microbiol. 45: 305-310.
    Pubmed
  25. Larsen, N., F. K. Vogensen, F. W. van den Berg, D. S. Nielsen, A. S. Andreasen, B. K. Pedersen, et al. 2010. Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS One 5: e9085.
    Pubmed KoreaMed CrossRef
  26. Leeson, M. C., Y. Fujihara, and D. C. Morrison. 1994. Evidence for lipopolysaccharide as the predominant proinflammatory mediator in supernatants of antibiotic-treated bacteria. Infect. Immun. 62: 4975-4980.
    Pubmed KoreaMed
  27. Lopez, P., M. Gueimonde, A. Margolles, and A. Suarez. 2010. Distinct Bifidobacterium strains drive different immune responses in vitro. Int. J. Food Microbiol. 138: 157-165.
    Pubmed CrossRef
  28. Lu, Y. C., W. C. Yeh, and P. S. Ohashi. 2008. LPS/TLR4 signal transduction pathway. Cytokine 42: 145-151.
    Pubmed CrossRef
  29. Ma, D., P. Forsythe, and J. Bienenstock. 2004. Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect. Immun. 72: 5308-5314.
    Pubmed KoreaMed CrossRef
  30. Madsen, K. L., J. S. Doyle, L. D. Jewell, M. M. Tavernini, and R. N. Fedorak. 1999. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116: 11071114.
    CrossRef
  31. Maitra, U., H. Deng, T. Glaros, B. Baker, D. G. Capelluto, Z. Li, and L. Li. 2012. Molecular mechanisms responsible for the selective and low-grade induction of proinflammatory mediators in murine macrophages by lipopolysaccharide. J. Immunol. 189:1014-1023.
    Pubmed CrossRef
  32. Mao, Y., S. Nobaek, B. Kasravi, D. Adawi, U. Stenram, G. Molin, and B. Jeppsson. 1996. The effects of Lactobacillus strains and oat fiber on methotrexate-induced enterocolitis in rats. Gastroenterology 111: 334-344.
    Pubmed CrossRef
  33. Mehta, N. N., F. C. McGillicuddy, P. D. Anderson, C. C. Hinkle, R. Shah, L. Pruscino, et al. 2010. Experimental endotoxemia induces adipose inflammation and insulin resistance in humans. Diabetes 59: 172-181.
    Pubmed KoreaMed CrossRef
  34. Mutlu, E., A. Keshavarzian, P. Engen, C. B. Forsyth, M. Sikaroodi, and P. Gillevet. 2009. Intestinal dysbiosis: A possible mechanism of alcohol-induced endotoxemia and alcoholic steatohepatitis in rats. Alcohol Clin. Exp. Res. 33: 1836-1846.
    Pubmed CrossRef
  35. O’Mahony, C., P. Scully, D. O’Mahony, S. Murphy, F. O’Brien, A. Lyons, et al. 2008. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog. 4: e1000112.
    Pubmed KoreaMed CrossRef
  36. Pena, J. A., A. B. Rogers, Z. Ge, V. Ng, S. Y. Li, J. G. Fox, and J. Versalovic. 2005. Probiotic Lactobacillus spp. diminish Helicobacter hepaticus-induced inflammatory bowel disease in interleukin-10-deficient mice. Infect. Immun. 73: 912-920.
    Pubmed KoreaMed CrossRef
  37. Prakash, S., L. Rodes, M. Coussa-Charley, and C. TomaroDuchesneau. 2011. Gut microbiota: Next frontier in understanding human health and development of biotherapeutics. Biologics 5:71-86.
    Pubmed KoreaMed CrossRef
  38. Rodes, L., A. Paul, M. Coussa-Charley, H. Al-Salami, C. Tomaro-Duchesneau, M. Fakhoury, and S. Prakash. 2011. Transit time affects the community stability of Lactobacillus and Bifidobacterium species in an in vitro model of human colonic microbiotia. Artif. Cells Blood Substit. Immobil. Biotechnol. 39: 351-356.
    Pubmed CrossRef
  39. Roselli, M., A. Finamore, M. S. Britti, and E. Mengheri. 2006. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br. J. Nutr. 95: 1177-1184.
    Pubmed CrossRef
  40. Schiffrin, E. J., A. Parlesak, C. Bode, J. C. Bode, M. A. van’t Hof, D. Grathwohl, and Y. Guigoz. 2009. Probiotic yogurt in the elderly with intestinal bacterial overgrowth: Endotoxaemia and innate immune functions. Br. J. Nutr. 101: 961-966.
    Pubmed CrossRef
  41. Schultz, M., C. Veltkamp, L. A. Dieleman, W. B. Grenther, P. B. Wyrick, S. L. Tonkonogy, and R. B. Sartor. 2002. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm. Bowel Dis. 8:71-80.
    Pubmed CrossRef
  42. Smith, P. D., L. E. Smythies, M. Mosteller-Barnum, D. A. Sibley, M. W. Russell, M. Merger, et al. 2001. Intestinal macrophages lack CD14 and CD89 and consequently are downregulated for LPS- and IgA-mediated activities. J. Immunol. 167: 2651-2656.
    Pubmed
  43. Smith, P. D., L. E. Smythies, R. Shen, T. Greenwell-Wild, M. Gliozzi, and S. M. Wahl. 2011. Intestinal macrophages and response to microbial encroachment. Mucosal Immunol. 4: 3142.
    Pubmed CrossRef
  44. Smythies, L. E., M. Sellers, R. H. Clements, M. MostellerBarnum, G. Meng, W. H. Benjamin, et al. 2005. Human intestinal macrophages display profound inflammatory anergy despite avid phagocytic and bacteriocidal activity. J. Clin. Invest. 115: 66-75.
    Pubmed KoreaMed
  45. Stagg, A. J., A. L. Hart, S. C. Knight, and M. A. Kamm. 2003. The dendritic cell: Its role in intestinal inflammation and relationship with gut bacteria. Gut 52: 1522-1529.
    Pubmed KoreaMed CrossRef
  46. Turnbaugh, P. J., M. Hamady, T. Yatsunenko, B. L. Cantarel, A. Duncan, R. E. Ley, et al. 2009. A core gut microbiome in obese and lean twins. Nature 457: 480-484.
    Pubmed KoreaMed CrossRef
  47. Veiga, P., C. A. Gallini, C. Beal, M. Michaud, M. L. Delaney, A. DuBois, et al. 2010. Bifidobacterium animalis subsp. lactis fermented milk product reduces inflammation by altering a niche for colitogenic microbes. Proc. Natl. Acad. Sci. USA 107:18132-18137.
    Pubmed KoreaMed CrossRef
  48. Xia, Y., H. Q. Chen, M. Zhang, Y. Q. Jiang, X. M. Hang, and H. L. Qin. 2011. Effect of Lactobacillus plantarum LP-Onlly on gut flora and colitis in interleukin-10 knockout mice. J. Gastroenterol. Hepatol. 26: 405-411.
    Pubmed CrossRef
  49. Zeuthen, L. H., H. R. Christensen, and H. Frokiaer. 2006. Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with Gramnegative bacteria. Clin. Vaccine Immunol. 13: 365-375.
    Pubmed KoreaMed CrossRef
  50. Zhang, W., Y. Gu, Y. Chen, H. Deng, L. Chen, S. Chen, G. Zhang, and Z. Gao. 2010. Intestinal flora imbalance results in altered bacterial translocation and liver function in rats with experimental cirrhosis. Eur. J. Gastroenterol. Hepatol. 22:1481-1486.
    Pubmed