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References

  1. Barthold SW, Coleman GL, Jacoby RO, Livestone EM, Jonas AM. 1978. Transmissible murine colonic hyperplasia. Vet. Pathol. 15: 223-236.
    Pubmed CrossRef
  2. Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, et al. 2012. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut 61: 829-838.
    Pubmed PMC CrossRef
  3. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742.
    Pubmed CrossRef
  4. Deng W, Li Y, Vallance BA, Finlay BB. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69: 6323-6335.
    Pubmed PMC CrossRef
  5. Dogi CA, Galdeano CM, Perdigón G. 2008. Gut immune stimulation by non pathogenic gram (+) and gram (−) bacteria. Comparison with a probiotic strain. Cytokine 41:223-231.
    Pubmed CrossRef
  6. Dong L, Li J, Liu Y, Yue W, Luo X. 2012. Toll-like receptor 2 monoclonal antibody or/and Toll-like receptor 4 monoclonal antibody increase counts of lactobacilli and bifidobacteria in dextran sulfate sodium-induced colitis in mice. J. Gastroenterol. Hepatol. 27: 110-119.
    Pubmed CrossRef
  7. Dorner BG, Scheffold A, Rolph MS, Huser MB, Kaufmann SH, Radbruch A, et al. 2002 MIP-1α, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines. Proc. Natl. Acad. Sci. USA 99: 6181-6186.
    Pubmed PMC CrossRef
  8. Doron S, Snydman DR, Gorbach SL. 2005. Lactobacillus GG:bacteriology and clinical applications. Gastroenterol. Clin. North Am. 34: 483-498.
    Pubmed CrossRef
  9. Gibson DL, Ma C, Rosenberger CM, Bergstrom KS, Valdez Y, Huang JT, et al. 2008. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10: 388-403.
    Pubmed
  10. Hartland EL, Batchelor M, Delahay RM, Hale C, Matthews S, Dougan G, et al. 1999. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol. Microbiol. 32: 151-158.
    Pubmed CrossRef
  11. Higgins LM, Frankel G, Connerton I, Gonçalves NS, Dougan G, MacDonald TT. 1999. Role of bacterial intimin in colonic hyperplasia and inflammation. Science 285: 588-591.
    Pubmed CrossRef
  12. Higgins LM, Frankel G, Douce G, Dougan G, MacDonald TT. 1996. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67:3031-3039.
  13. Johansson ML, Nobaek S, Berggren A, Nyman M, Björck I, Ahrné S, et al. 1998. Survival of Lactobacillus plantarum DSM 9843 (299v), and effect on the short-chain fatty acid content of faeces after ingestion of a rose-hip drink with fermented oats. Int. J. Food Microbiol. 42: 29-38.
    CrossRef
  14. Johnson-Henry KC, Nadjafi M, Avitzur Y, Mitchell DJ, Ngan BY, Galindo-Mata E, et al. 2005. Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J. Infect. Dis. 191: 2106-2117.
    Pubmed CrossRef
  15. Kerr AR, Irvine JJ, Search JJ, Gingles NA, Kadioglu A, Andrew PW, et al. 2002. Role of inflammatory mediators in resistance and susceptibility to pneumococcal infection. Infect. Immun. 70: 1547-1557.
    Pubmed PMC CrossRef
  16. Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, et al. 2006. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect. Immun. 74: 2522-2536.
    Pubmed PMC CrossRef
  17. Kim M, Ashida H, Ogawa M, Yoshikawa Y, Mimuro H, Sasakawa C. 2010. Bacterial interactions with the host epithelium. Cell Host Microbe 8: 20-35.
    Pubmed CrossRef
  18. Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, et al. 2004. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53: 1617-1623.
    Pubmed PMC CrossRef
  19. Luperchio SA, Newman JV, Dangler CA, Schrenzel MD, Brenner DJ, Steigerwalt AG, Schauer DB. 2000. Citrobacter rodentium, the causative agent of transmissible murine colonic hyperplasia, exhibits clonality: synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J. Clin. Microbiol. 38:4343-4350.
    Pubmed PMC
  20. Luperchio SA, Schauer DB. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3: 333-340.
    CrossRef
  21. Moayyedi P, Ford AC, Talley NJ, Cremonini F, FoxxOrenstein AE, Brandt LJ, Quigley EM. 2010. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 59: 325-332.
    Pubmed CrossRef
  22. Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H. 2002. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol. Med. Microbiol. 32: 105-110.
    Pubmed CrossRef
  23. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7: 1697-1706.
    Pubmed CrossRef
  24. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
    Pubmed PMC
  25. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
    Pubmed CrossRef
  26. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, et al. 1996. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 98: 945-953.
    Pubmed PMC CrossRef
  27. Rodrigues DM, Sousa AJ, Johnson-Henry KC, Sherman PM, Gareau MG. 2012. Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. J. Infect. Dis. 206: 99-109.
    Pubmed CrossRef
  28. Sartor RB. 2006. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3: 390-407.
    Pubmed CrossRef
  29. Sartor RB. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
    Pubmed CrossRef
  30. Schauer DB, Zabel BA, Pedraza IF, O’Hara CM, Steigerwalt AG, Brenner DJ. 1995. Genetic and biochemical characterization of Citrobacter rodentium sp. nov. J. Clin. Microbiol. 33: 20642068.
  31. Takeda K, Akira S. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
    Pubmed CrossRef
  32. Wei OL, Hilliard A, Kalman D, Sherman M. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 73: 19781985.
    Pubmed PMC CrossRef
  33. Williams MD, Ha CY, Ciorba MA. 2010. Probiotics as therapy in gastroenterology: a study of physician opinions and recommendations. J. Clin. Gastroenterol. 44: 631-636.
    CrossRef
  34. Williams NT. 2010. Probiotics. Am. J. Health Syst. Pharm. 67:449-458.
    Pubmed CrossRef
  35. Xu LL, Warren MK, Rose WL, Gong W, Wang JM. 1996. Human recombinant monocyte chemotactic protein and other CC chemokines bind and induce directional migration of dendritic cells in vitro. J. Leukoc. Biol. 60: 365-371.
    Pubmed
  36. Yan F, Polk DB. 2012. Lactobacillus rhamnosus GG: an updated strategy to use microbial products to promote health. Funct. Food Rev. 4: 77-84.
    Pubmed PMC

Article

Research article

J. Microbiol. Biotechnol. 2016; 26(7): 1333-1340

Published online July 28, 2016 https://doi.org/10.4014/jmb.1602.02004

Copyright © The Korean Society for Microbiology and Biotechnology.

The Probiotic Lactobacillus Prevents Citrobacter rodentium-Induced Murine Colitis in a TLR2-Dependent Manner

Seung-Hyun Ryu 1, Jong-Hyung Park 1, Soo-Young Choi 1, Hee-Yeon Jeon 1, Jin-Il Park 1, Jun-Young Kim 1, Seung-Hoon Ham 1 and Yang-Kyu Choi 1*

Department of Laboratory Animal Medicine, College of Veterinary Medicine, Konkuk University, Seoul 05029, Republic of Korea

Received: February 3, 2016; Accepted: April 5, 2016

Abstract

The main objective of this study was to investigate whether Lactobacillus rhamnosus GG (LGG)
ameliorated the effects of Citrobactor rodentium infection in Toll-like receptor 2 (TLR2)
knockout (KO) and TLR4 KO mice, as well as in wild-type C57BL/6 (B6) mice. TLR2 KO, TLR4
KO, and B6 mice were divided into three groups per each strain. Each group had an
uninfected control group (n = 5), C. rodentium-infected group (n = 8), and LGG-pretreated
C. rodentium-infected group (n = 8). The survival rate of B6 mice infected with C. rodentium
was higher when pretreated with LGG. Pretreatment with LGG ameliorated C. rodentiuminduced
mucosal hyperplasia in B6 and TLR4 KO mice. However, in C-rodentium-infected
TLR2 KO mice, mucosal hyperplasia persisted, regardless of pretreatment with LGG. In
addition, LGG-pretreated B6 and TLR4 KO mice showed a decrease in spleen weight and
downregulation of tumor necrosis factor alpha, interferon gamma, and monocyte chemotactic
protein 1 mRNA expression compared with the non-pretreated group. In contrast, such
changes were not observed in TLR2 KO mice, regardless of pretreatment with LGG. From the
above results, we conclude that pretreatment with LGG ameliorates C. rodentium-induced
colitis in B6 and TLR4 KO mice, but not in TLR2 KO mice. Therefore, LGG protects mice from
C. rodentium-induced colitis in a TLR2-dependent manner.

Keywords: Citrobacter rodentium, colitis, Lactobacillus rhamnosus, probiotic, toll-like receptor

References

  1. Barthold SW, Coleman GL, Jacoby RO, Livestone EM, Jonas AM. 1978. Transmissible murine colonic hyperplasia. Vet. Pathol. 15: 223-236.
    Pubmed CrossRef
  2. Ciorba MA, Riehl TE, Rao MS, Moon C, Ee X, Nava GM, et al. 2012. Lactobacillus probiotic protects intestinal epithelium from radiation injury in a TLR-2/cyclo-oxygenase-2-dependent manner. Gut 61: 829-838.
    Pubmed KoreaMed CrossRef
  3. Dalton DK, Pitts-Meek S, Keshav S, Figari IS, Bradley A, Stewart TA. 1993. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259:1739-1742.
    Pubmed CrossRef
  4. Deng W, Li Y, Vallance BA, Finlay BB. 2001. Locus of enterocyte effacement from Citrobacter rodentium: sequence analysis and evidence for horizontal transfer among attaching and effacing pathogens. Infect. Immun. 69: 6323-6335.
    Pubmed KoreaMed CrossRef
  5. Dogi CA, Galdeano CM, Perdigón G. 2008. Gut immune stimulation by non pathogenic gram (+) and gram (−) bacteria. Comparison with a probiotic strain. Cytokine 41:223-231.
    Pubmed CrossRef
  6. Dong L, Li J, Liu Y, Yue W, Luo X. 2012. Toll-like receptor 2 monoclonal antibody or/and Toll-like receptor 4 monoclonal antibody increase counts of lactobacilli and bifidobacteria in dextran sulfate sodium-induced colitis in mice. J. Gastroenterol. Hepatol. 27: 110-119.
    Pubmed CrossRef
  7. Dorner BG, Scheffold A, Rolph MS, Huser MB, Kaufmann SH, Radbruch A, et al. 2002 MIP-1α, MIP-1β, RANTES, and ATAC/lymphotactin function together with IFN-γ as type 1 cytokines. Proc. Natl. Acad. Sci. USA 99: 6181-6186.
    Pubmed KoreaMed CrossRef
  8. Doron S, Snydman DR, Gorbach SL. 2005. Lactobacillus GG:bacteriology and clinical applications. Gastroenterol. Clin. North Am. 34: 483-498.
    Pubmed CrossRef
  9. Gibson DL, Ma C, Rosenberger CM, Bergstrom KS, Valdez Y, Huang JT, et al. 2008. Toll-like receptor 2 plays a critical role in maintaining mucosal integrity during Citrobacter rodentium-induced colitis. Cell. Microbiol. 10: 388-403.
    Pubmed
  10. Hartland EL, Batchelor M, Delahay RM, Hale C, Matthews S, Dougan G, et al. 1999. Binding of intimin from enteropathogenic Escherichia coli to Tir and to host cells. Mol. Microbiol. 32: 151-158.
    Pubmed CrossRef
  11. Higgins LM, Frankel G, Connerton I, Gonçalves NS, Dougan G, MacDonald TT. 1999. Role of bacterial intimin in colonic hyperplasia and inflammation. Science 285: 588-591.
    Pubmed CrossRef
  12. Higgins LM, Frankel G, Douce G, Dougan G, MacDonald TT. 1996. Citrobacter rodentium infection in mice elicits a mucosal Th1 cytokine response and lesions similar to those in murine inflammatory bowel disease. Infect. Immun. 67:3031-3039.
  13. Johansson ML, Nobaek S, Berggren A, Nyman M, Björck I, Ahrné S, et al. 1998. Survival of Lactobacillus plantarum DSM 9843 (299v), and effect on the short-chain fatty acid content of faeces after ingestion of a rose-hip drink with fermented oats. Int. J. Food Microbiol. 42: 29-38.
    CrossRef
  14. Johnson-Henry KC, Nadjafi M, Avitzur Y, Mitchell DJ, Ngan BY, Galindo-Mata E, et al. 2005. Amelioration of the effects of Citrobacter rodentium infection in mice by pretreatment with probiotics. J. Infect. Dis. 191: 2106-2117.
    Pubmed CrossRef
  15. Kerr AR, Irvine JJ, Search JJ, Gingles NA, Kadioglu A, Andrew PW, et al. 2002. Role of inflammatory mediators in resistance and susceptibility to pneumococcal infection. Infect. Immun. 70: 1547-1557.
    Pubmed KoreaMed CrossRef
  16. Khan MA, Ma C, Knodler LA, Valdez Y, Rosenberger CM, Deng W, et al. 2006. Toll-like receptor 4 contributes to colitis development but not to host defense during Citrobacter rodentium infection in mice. Infect. Immun. 74: 2522-2536.
    Pubmed KoreaMed CrossRef
  17. Kim M, Ashida H, Ogawa M, Yoshikawa Y, Mimuro H, Sasakawa C. 2010. Bacterial interactions with the host epithelium. Cell Host Microbe 8: 20-35.
    Pubmed CrossRef
  18. Kruis W, Fric P, Pokrotnieks J, Lukás M, Fixa B, Kascák M, et al. 2004. Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53: 1617-1623.
    Pubmed KoreaMed CrossRef
  19. Luperchio SA, Newman JV, Dangler CA, Schrenzel MD, Brenner DJ, Steigerwalt AG, Schauer DB. 2000. Citrobacter rodentium, the causative agent of transmissible murine colonic hyperplasia, exhibits clonality: synonymy of C. rodentium and mouse-pathogenic Escherichia coli. J. Clin. Microbiol. 38:4343-4350.
    Pubmed KoreaMed
  20. Luperchio SA, Schauer DB. 2001. Molecular pathogenesis of Citrobacter rodentium and transmissible murine colonic hyperplasia. Microbes Infect. 3: 333-340.
    CrossRef
  21. Moayyedi P, Ford AC, Talley NJ, Cremonini F, FoxxOrenstein AE, Brandt LJ, Quigley EM. 2010. The efficacy of probiotics in the treatment of irritable bowel syndrome: a systematic review. Gut 59: 325-332.
    Pubmed CrossRef
  22. Mukai T, Asasaka T, Sato E, Mori K, Matsumoto M, Ohori H. 2002. Inhibition of binding of Helicobacter pylori to the glycolipid receptors by probiotic Lactobacillus reuteri. FEMS Immunol. Med. Microbiol. 32: 105-110.
    Pubmed CrossRef
  23. Mundy R, MacDonald TT, Dougan G, Frankel G, Wiles S. 2005. Citrobacter rodentium of mice and man. Cell. Microbiol. 7: 1697-1706.
    Pubmed CrossRef
  24. Nataro JP, Kaper JB. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11: 142-201.
    Pubmed KoreaMed
  25. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, Edberg S, Medzhitov R. 2004. Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118: 229-241.
    Pubmed CrossRef
  26. Rath HC, Herfarth HH, Ikeda JS, Grenther WB, Hamm TE Jr, Balish E, et al. 1996. Normal luminal bacteria, especially Bacteroides species, mediate chronic colitis, gastritis, and arthritis in HLA-B27/human beta2 microglobulin transgenic rats. J. Clin. Invest. 98: 945-953.
    Pubmed KoreaMed CrossRef
  27. Rodrigues DM, Sousa AJ, Johnson-Henry KC, Sherman PM, Gareau MG. 2012. Probiotics are effective for the prevention and treatment of Citrobacter rodentium-induced colitis in mice. J. Infect. Dis. 206: 99-109.
    Pubmed CrossRef
  28. Sartor RB. 2006. Mechanisms of disease: pathogenesis of Crohn's disease and ulcerative colitis. Nat. Clin. Pract. Gastroenterol. Hepatol. 3: 390-407.
    Pubmed CrossRef
  29. Sartor RB. 2008. Microbial influences in inflammatory bowel diseases. Gastroenterology 134: 577-594.
    Pubmed CrossRef
  30. Schauer DB, Zabel BA, Pedraza IF, O’Hara CM, Steigerwalt AG, Brenner DJ. 1995. Genetic and biochemical characterization of Citrobacter rodentium sp. nov. J. Clin. Microbiol. 33: 20642068.
  31. Takeda K, Akira S. 2005. Toll-like receptors in innate immunity. Int. Immunol. 17: 1-14.
    Pubmed CrossRef
  32. Wei OL, Hilliard A, Kalman D, Sherman M. 2005. Mast cells limit systemic bacterial dissemination but not colitis in response to Citrobacter rodentium. Infect. Immun. 73: 19781985.
    Pubmed KoreaMed CrossRef
  33. Williams MD, Ha CY, Ciorba MA. 2010. Probiotics as therapy in gastroenterology: a study of physician opinions and recommendations. J. Clin. Gastroenterol. 44: 631-636.
    CrossRef
  34. Williams NT. 2010. Probiotics. Am. J. Health Syst. Pharm. 67:449-458.
    Pubmed CrossRef
  35. Xu LL, Warren MK, Rose WL, Gong W, Wang JM. 1996. Human recombinant monocyte chemotactic protein and other CC chemokines bind and induce directional migration of dendritic cells in vitro. J. Leukoc. Biol. 60: 365-371.
    Pubmed
  36. Yan F, Polk DB. 2012. Lactobacillus rhamnosus GG: an updated strategy to use microbial products to promote health. Funct. Food Rev. 4: 77-84.
    Pubmed KoreaMed