strain Nissle 1917 ameliorates experimental colitis by modulating intestinal permeability, the inflammatory response and clinical signs in a faecal transplantation model Free

Abstract

Inflammatory bowel diseases (IBDs) are a group of inflammatory conditions of the gut that include ulcerative colitis and Crohn's disease. Probiotics are live micro-organisms that may be used as adjuvant therapy for patients with IBD. The aim of this study was to evaluate the effect of prophylactic ingestion of strain Nissle 1917 (EcN) in a murine model of colitis. For induction of colitis, mice were given a 3.5 % dextran sodium sulfate (DSS) solution for 7 days in drinking water. EcN administration to mice subjected to DSS-induced colitis resulted in significant reduction in clinical and histopathological signs of disease and preservation of intestinal permeability. We observed reduced inflammation, as assessed by reduced levels of neutrophils, eosinophils, chemokines and cytokines. We observed an increase in the number of regulatory T-cells in Peyer's patches. Germ-free mice received faecal content from control or EcN-treated mice and were then subjected to DSS-induced colitis. We observed protection from colitis in animals that were colonized with faecal content from EcN-treated mice. These results suggest that preventative oral administration of EcN or faecal microbiota transplantation with EcN-containing microbiota ameliorates DSS-induced colitis by modifying inflammatory responsiveness to DSS.

Loading

Article metrics loading...

/content/journal/jmm/10.1099/jmm.0.000222
2016-03-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/jmm/65/3/201.html?itemId=/content/journal/jmm/10.1099/jmm.0.000222&mimeType=html&fmt=ahah

References

  1. Abraham C., Medzhitov R. 2011; Interactions between the host innate immune system and microbes in inflammatory bowel disease. Gastroenterology 140:1729–1737 [View Article][PubMed]
    [Google Scholar]
  2. Adar T., Shteingart S., Ben Ya'acov A., Bar-Gil Shitrit A., Goldin E. 2014; From airway inflammation to inflammatory bowel disease: eotaxin-1, a key regulator of intestinal inflammation. Clin Immunol 153:199–208 [View Article][PubMed]
    [Google Scholar]
  3. Al-Haddad S., Riddell R. H. 2005; The role of eosinophils in inflammatory bowel disease. Gut 54:1674–1675 [View Article][PubMed]
    [Google Scholar]
  4. Albert E. J., Duplisea J., Dawicki W., Haidl I. D., Marshall J. S. 2011; Tissue eosinophilia in a mouse model of colitis is highly dependent on TLR2 and independent of mast cells. Am J Pathol 178:150–160 [View Article][PubMed]
    [Google Scholar]
  5. Atarashi K., Tanoue T., Oshima K., Suda W., Nagano Y., Nishikawa H., Fukuda S., Saito T., Narushima S., other authors. 2013; Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature 500:232–236 [View Article][PubMed]
    [Google Scholar]
  6. Baumgart D. C., Sandborn W. J. 2007; Inflammatory bowel disease: clinical aspects and established and evolving therapies. Lancet 369:1641–1657 [View Article][PubMed]
    [Google Scholar]
  7. Bibiloni R., Fedorak R. N., Tannock G. W., Madsen K. L., Gionchetti P., Campieri M., De Simone C., Sartor R. B. 2005; VSL#3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539–1546 [View Article][PubMed]
    [Google Scholar]
  8. Blumberg R. S. 2009; Inflammatory bowel disease: immunologic considerations. In Current Diagnosis & Treatment in Gastroenterology, Hepatology and Endoscopy pp 11–21 Edited by Greenberger N. J., Blumberg R. S., Burakoff R. New York: McGraw-Hill Medical;
    [Google Scholar]
  9. Cerf-Bensussan N., Gaboriau-Routhiau V. 2010; The immune system and the gut microbiota: friends or foes?. Nat Rev Immunol 10:735–744 [View Article][PubMed]
    [Google Scholar]
  10. Chassaing B., Koren O., Goodrich J. K., Poole A. C., Srinivasan S., Ley R. E., Gewirtz A. T. 2015; Dietary emulsifiers impact the mouse gut microbiota promoting colitis and metabolic syndrome. Nature 519:92–96 [View Article][PubMed]
    [Google Scholar]
  11. COBEA 2006 Colégio Brasileiro de Experimentação Animal Legislação e Ética. Available from: http://www.cobea.org.br/. Accessed 30 June, 2011
    [Google Scholar]
  12. Cui H. H., Chen C. L., Wang J. D., Yang Y. J., Cun Y., Wu J. B., Liu Y. H., Dan H. L., Jian Y. T., Chen X. Q. 2004; Effects of probiotic on intestinal mucosa of patients with ulcerative colitis. World J Gastroenterol 10:1521–1525 [View Article][PubMed]
    [Google Scholar]
  13. Dongarrà M. L., Rizzello V., Muccio L., Fries W., Cascio A., Bonaccorsi I., Ferlazzo G. 2013; Mucosal immunology and probiotics. Curr Allergy Asthma Rep 13:19–26 [View Article][PubMed]
    [Google Scholar]
  14. Elian S. D., Souza E. L., Vieira A. T., Teixeira M. M., Arantes R. M., Nicoli J. R., Martins F. S. 2015; Bifidobacterium longum subsp. infantis BB-02 attenuates acute murine experimental model of inflammatory bowel disease. Benef Microbes 6:277–286 [View Article][PubMed]
    [Google Scholar]
  15. FAO/WHO Report 2002 Guidelines for the Evaluation of Probiotics in Food London/Ontario: Food and Agricultural Organization/World Health Organization Working Group;
    [Google Scholar]
  16. Fedorak R. N., Madsen K. L. 2004; Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis 10:286–299 [View Article][PubMed]
    [Google Scholar]
  17. Furusawa Y., Obata Y., Fukuda S., Endo T. A., Nakato G., Takahashi D., Nakanishi Y., Uetake C., Kato K., other authors. 2013; Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature 504:446–450 [View Article][PubMed]
    [Google Scholar]
  18. Geem D., Harusato A., Flannigan K., Denning T. L. 2015; Harnessing regulatory T cells for the treatment of inflammatory bowel disease. Inflamm Bowel Dis 21:1409–1418[PubMed]
    [Google Scholar]
  19. Ghouri Y. A., Richards D. M., Rahimi E. F., Krill J. T., Jelinek K. A., DuPont A. W. 2014; Systematic review of randomized controlled trials of probiotics, prebiotics, and synbiotics in inflammatory bowel disease. Clin Exp Gastroenterol 7:473–487[PubMed]
    [Google Scholar]
  20. Grant C. R., Liberal R., Mieli-Vergani G., Vergani D., Longhi M. S. 2015; Regulatory T-cells in autoimmune diseases: challenges, controversies and yet–unanswered questions. Autoimmun Rev 14:105–116 [View Article][PubMed]
    [Google Scholar]
  21. Himmel M. E., Hardenberg G., Piccirillo C. A., Steiner T. S., Levings M. K. 2008; The role of T-regulatory cells and Toll-like receptors in the pathogenesis of human inflammatory bowel disease. Immunology 125:145–153 [View Article][PubMed]
    [Google Scholar]
  22. Huttenhower C., Kostic A. D., Xavier R. J. 2014; Inflammatory bowel disease as a model for translating the microbiome. Immunity 40:843–854 [View Article][PubMed]
    [Google Scholar]
  23. Johnson-Henry K. C., Donato K. A., Shen-Tu G., Gordanpour M., Sherman P. M. 2008; Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157 : H7-induced changes in epithelial barrier function. Infect Immun 76:1340–1348 [View Article][PubMed]
    [Google Scholar]
  24. Kaser A., Zeissig S., Blumberg R. S. 2010; Inflammatory bowel disease. Annu Rev Immunol 28:573–621 [View Article][PubMed]
    [Google Scholar]
  25. Kelly D., Mulder I. E. 2012; Microbiome and immunological interactions. Nutr Rev 70:(Suppl 1)S18–S30 [View Article][PubMed]
    [Google Scholar]
  26. Klingberg T. D., Pedersen M. H., Cencic A., Budde B. B. 2005; Application of measurements of transepithelial electrical resistance of intestinal epithelial cell monolayers to evaluate probiotic activity. Appl Environ Microbiol 71:7528–7530 [View Article][PubMed]
    [Google Scholar]
  27. Kobayashi Y. 2008; The role of chemokines in neutrophil biology. Front Biosci 13:2400–2407 [View Article][PubMed]
    [Google Scholar]
  28. Kruger P., Saffarzadeh M., Weber A.N.R., Rieber N., Radsak M., von Bernuth H., Benarafa C., Roos D., Skokowa J., Hartl D. 2015; Neutrophils: between host defence, immune modulation, and tissue injury. PLoS Pathog 11:e1004651 [View Article][PubMed]
    [Google Scholar]
  29. Kruis W., Frič P., Pokrotnieks J., Lukás M., Fixa B., Kascák M., Kamm M. A., Weismueller J., Beglinger C., other authors. 2004; Maintaining remission of ulcerative colitis with the probiotic Escherichia coli Nissle 1917 is as effective as with standard mesalazine. Gut 53:1617–1623 [View Article][PubMed]
    [Google Scholar]
  30. Lepage P., Häsler R., Spehlmann M. E., Rehman A., Zvirbliene A., Begun A., Ott S., Kupcinskas L., Doré J., other authors. 2011; Twin study indicates loss of interaction between microbiota and mucosa of patients with ulcerative colitis. Gastroenterology 141:227–236 [View Article][PubMed]
    [Google Scholar]
  31. Loftus E. V. Jr., Sandborn W. J. 2002; Epidemiology of inflammatory bowel disease. Gastroenterol Clin North Am 31:1–20 [View Article][PubMed]
    [Google Scholar]
  32. Logan I., Bowlus C. L. 2010; The geoepidemiology of autoimmune intestinal diseases. Autoimmun Rev 9:A372–A378 [View Article][PubMed]
    [Google Scholar]
  33. Maloy K. J., Powrie F. 2011; Intestinal homeostasis and its breakdown in inflammatory bowel disease. Nature 474:298–306 [View Article][PubMed]
    [Google Scholar]
  34. Manichanh C., Borruel N., Casellas F., Guarner F. 2012; The gut microbiota in IBD. Nat Rev Gastroenterol Hepatol 9:599–608 [View Article][PubMed]
    [Google Scholar]
  35. Martins F. S., Elian S. D., Vieira A. T., Tiago F. C., Martins A. K., Silva F. C., Souza E.L.S., Sousa L. P., Araújo H. R., other authors. 2011; Oral treatment with Saccharomyces cerevisiae strain UFMG 905 modulates immune responses and interferes with signal pathways involved in the activation of inflammation in a murine model of typhoid fever. Int J Med Microbiol 301:359–364 [View Article][PubMed]
    [Google Scholar]
  36. Martins F. S., Vieira A. T., Elian S. D., Arantes R. M., Tiago F. C., Sousa L. P., Araújo H. R., Pimenta P. F., Bonjardim C. A., other authors. 2013; Inhibition of tissue inflammation and bacterial translocation as one of the protective mechanisms of Saccharomyces boulardii against Salmonella infection in mice. Microbes Infect 15:270–279 [View Article][PubMed]
    [Google Scholar]
  37. Molodecky N. A., Soon I. S., Rabi D. M., Ghali W. A., Ferris M., Chernoff G., Benchimol E. I., Panaccione R., Ghosh S., other authors. 2012; Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology 142:46–54 e42, quiz e30 [View Article][PubMed]
    [Google Scholar]
  38. Neuman M. G. 2007; Immune dysfunction in inflammatory bowel disease. Translational Research 149:173–186 [View Article][PubMed]
    [Google Scholar]
  39. Neurath M. F. 2014; Cytokines in inflammatory bowel disease. Nat Rev Immunol 14:329–342 [View Article][PubMed]
    [Google Scholar]
  40. Ordás I., Eckmann L., Talamini M., Baumgart D. C., Sandborn W. J. 2012; Ulcerative colitis. Lancet 380:1606–1619 [View Article][PubMed]
    [Google Scholar]
  41. Orel R., Kamhi Trop T. 2014; Intestinal microbiota, probiotics and prebiotics in inflammatory bowel disease. World J Gastroenterol 20:11505–11524 [View Article][PubMed]
    [Google Scholar]
  42. Perše M., Cerar A. 2012; Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotechnol 2012:1–13 [View Article][PubMed]
    [Google Scholar]
  43. Powrie F., Leach M. W., Mauze S., Caddie L. B., Coffman R. L. 1993; Phenotypically distinct subsets of CD4+T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int Immunol 5:1461–1471 [View Article][PubMed]
    [Google Scholar]
  44. Raphael I., Nalawade S., Eagar T. N., Forsthuber T. G. 2015; T cell subsets and their signature cytokines in autoimmune and inflammatory diseases. Cytokine 74:5–17 [View Article][PubMed]
    [Google Scholar]
  45. Rigottier-Gois L. 2013; Dysbiosis in inflammatory bowel diseases: the oxygen hypothesis. ISME J 7:1256–1261 [View Article][PubMed]
    [Google Scholar]
  46. Rogler G. 2011; Prebiotics and probiotics in ulcerative colitis: where do we stand?. Digestion 84:126–127 [View Article][PubMed]
    [Google Scholar]
  47. Rudensky A. Y. 2011; Regulatory T cells and Foxp3. Immunol Rev 241:260–268 [View Article][PubMed]
    [Google Scholar]
  48. Satokari R. 2015; Contentious host-microbiota relationship in inflammatory bowel disease – can foes become friends again?. Scand J Gastroenterol 50:34–42 [View Article][PubMed]
    [Google Scholar]
  49. Schneider C. A., Rasband W. S., Eliceiri K. W. 2012; NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675 [View Article][PubMed]
    [Google Scholar]
  50. Schultz M., Strauch U. G., Linde H. J., Watzl S., Obermeier F., Göttl C., Dunger N., Grunwald N., Schölmerich J., Rath H. C. 2004; Preventive effects of Escherichia coli strain Nissle 1917 on acute and chronic intestinal inflammation in two different murine models of colitis. Clin Diagn Lab Immunol 11:372–378[PubMed]
    [Google Scholar]
  51. Sha S., Xu B., Kong X., Wei N., Liu J., Wu K. 2014; Preventive effects of Escherichia coli strain Nissle 1917 with different courses and different doses on intestinal inflammation in murine model of colitis. Inflamm Res 63:873–883 [View Article][PubMed]
    [Google Scholar]
  52. Smith P. M., Howitt M. R., Panikov N., Michaud M., Gallini C. A., Bohlooly-Y M., Glickman J. N., Garrett W. S. 2013; The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 341:569–573 [View Article][PubMed]
    [Google Scholar]
  53. Strath M., Warren D. J., Sanderson C. J. 1985; Detection of eosinophils using an eosinophil peroxidase assay. Its use as an assay for eosinophil differentiation factors. J Immunol Methods 83:209–215 [View Article][PubMed]
    [Google Scholar]
  54. Talley N. J., Abreu M. T., Achkar J. P., Bernstein C. N., Dubinsky M. C., Hanauer S. B., Kane S. V., Sandborn W. J., Ullman T. A., other authors. 2011; An evidence-based systematic review on medical therapies for inflammatory bowel disease. Am J Gastroenterol 106:(Suppl 1)S2–S25 quiz S26 [View Article][PubMed]
    [Google Scholar]
  55. Tiago F. C., Porto B. A., Ribeiro N. S., Moreira L. M., Arantes R. M., Vieira A. T., Teixeira M. M., Generoso S. V., Nascimento V. N., other authors. 2015; Effect of Saccharomyces cerevisiae strain UFMG A-905 in experimental model of inflammatory bowel disease. Benef Microbes 6:807–815 [View Article][PubMed]
    [Google Scholar]
  56. Travers J., Rothenberg M. E. 2015; Eosinophils in mucosal immune responses. Mucosal Immunol 8:464–475 [View Article][PubMed]
    [Google Scholar]
  57. Triantafillidis J. K., Merikas E., Georgopoulos F. 2011; Current and emerging drugs for the treatment of inflammatory bowel disease. Drug Des Devel Ther 5:185–210 [View Article][PubMed]
    [Google Scholar]
  58. Valatas V., Bamias G., Kolios G. 2015; Experimental colitis models: insights into the pathogenesis of inflammatory bowel disease and translational issues. Eur J Pharmacol 759:253–264 [View Article][PubMed]
    [Google Scholar]
  59. Venturi A., Gionchetti P., Rizzello F., Johansson R., Zucconi E., Brigidi P., Matteuzzi D., Campieri M. 1999; Impact on the composition of the faecal flora by a new probiotic preparation: preliminary data on maintenance treatment of patients with ulcerative colitis. Aliment Pharmacol Ther 13:1103–1108 [View Article][PubMed]
    [Google Scholar]
  60. Vieira A. T., Pinho V., Lepsch L. B., Scavone C., Ribeiro I. M., Tomassini T., Ribeiro-dos-Santos R., Soares M. B., Teixeira M. M., Souza D. G. 2005; Mechanisms of the anti-inflammatory effects of the natural secosteroids physalins in a model of intestinal ischaemia and reperfusion injury. Br J Pharmacol 146:244–251 [View Article][PubMed]
    [Google Scholar]
  61. Vieira A. T., Fagundes C. T., Alessandri A. L., Castor M. G., Guabiraba R., Borges V. O., Silveira K. D., Vieira E. L., Gonçalves J. L., other authors. 2009; Treatment with a novel chemokine-binding protein or eosinophil lineage-ablation protects mice from experimental colitis. Am J Pathol 175:2382–2391 [View Article][PubMed]
    [Google Scholar]
  62. Vieira A. T., Teixeira M. M., Martins F. S. 2013; The role of probiotics and prebiotics in inducing gut immunity. Front Immunol 4:1–12 [View Article]
    [Google Scholar]
  63. Wang L., Ray A., Jiang X., Wang J. Y., Basu S., Liu X., Qian T., He R., Dittel B. N., Chu Y. 2015; T regulatory cells and B cells cooperate to form a regulatory loop that maintains gut homeostasis and suppresses dextran sulfate sodium-induced colitis. Mucosal Immunol 8:1297–1312 [View Article][PubMed]
    [Google Scholar]
  64. Woodruff S. A., Masterson J. C., Fillon S., Robinson Z. D., Furuta G. T. 2011; Role of eosinophils in inflammatory bowel and gastrointestinal diseases. J Pediatr Gastroenterol Nutr 52:650–661 [View Article][PubMed]
    [Google Scholar]
  65. Yan Y., Kolachala V., Dalmasso G., Nguyen H., Laroui H., Sitaraman S. V., Merlin D. 2009; Temporal and spatial analysis of clinical and molecular parameters in dextran sodium sulfate induced colitis. PLoS One 4:e6073 [View Article][PubMed]
    [Google Scholar]
  66. Zocco M. A., dal Verme L. Z., Cremonini F., Piscaglia A. C., Nista E. C., Candelli M., Novi M., Rigante D., Cazzato I. A., other authors. 2006; Efficacy of Lactobacillus GG in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 23:1567–1574 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jmm/10.1099/jmm.0.000222
Loading
/content/journal/jmm/10.1099/jmm.0.000222
Loading

Data & Media loading...

Most cited Most Cited RSS feed