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Volume 159, Issue Pt_8

Exploring the immunomodulatory potential of microbial-associated molecular patterns derived from the enteric bacterial microbiota Free

Abstract

The human intestinal lumen represents one of the most densely populated microbial niches in the biological world and, as a result, the intestinal innate immune system exists in a constant state of stimulation. A key component in the innate defence system is the intestinal epithelial layer, which acts not only as a physical barrier, but also as an immune sensor. The expression of pattern recognition receptors, such as Toll-like receptors, in epithelial cells allows innate recognition of a wide range of highly conserved bacterial moieties, termed microbial-associated molecular patterns (MAMPs), from both pathogenic and non-pathogenic bacteria. To date, studies of epithelial immunity have largely concentrated on inflammatory pathogenic antigens; however, this review discusses the major types of MAMPs likely to be produced by the enteric bacterial microbiota and, using data from studies, animal model systems and clinical observations, speculates on their immunomodulatory potential.

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2013-08-01
2024-04-26
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References

  1. Aderem A., Ulevitch R. J. ( 2000). Toll-like receptors in the induction of the innate immune response. Nature 406:782–787 [View Article][PubMed]
     [Google Scholar]
  2. Akhtar M., Watson J. L., Nazli A., McKay D. M. ( 2003). Bacterial DNA evokes epithelial IL-8 production by a MAPK-dependent, NF-kappaB-independent pathway. FASEB J 17:1319–1321[PubMed]
     [Google Scholar]
  3. Akira S., Uematsu S., Takeuchi O. ( 2006). Pathogen recognition and innate immunity. Cell 124:783–801 [View Article][PubMed]
     [Google Scholar]
  4. Alexander C., Rietschel E. T. ( 2001). Bacterial lipopolysaccharides and innate immunity. J Endotoxin Res 7:167–202[PubMed]
     [Google Scholar]
  5. Artis D. ( 2008). Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat Rev Immunol 8:411–420 [View Article][PubMed]
     [Google Scholar]
  6. Badel S., Bernardi T., Michaud P. ( 2011). New perspectives for Lactobacilli exopolysaccharides. Biotechnol Adv 29:54–66 [View Article][PubMed]
     [Google Scholar]
  7. Bannon C. ( 2008). Molecular basis of the bacterial-epithelial interactions in the gut . PhD thesis, University of Manchester; Manchester, UK:
     [Google Scholar]
  8. Bauer S., Kirschning C. J., Häcker H., Redecke V., Hausmann S., Akira S., Wagner H., Lipford G. B. ( 2001). Human TLR9 confers responsiveness to bacterial DNA via species-specific CpG motif recognition. Proc Natl Acad Sci U S A 98:9237–9242 [View Article][PubMed]
     [Google Scholar]
  9. Bauman S. J., Kuehn M. J. ( 2006). Purification of outer membrane vesicles from Pseudomonas aeruginosa and their activation of an IL-8 response. Microbes Infect 8:2400–2408 [View Article][PubMed]
     [Google Scholar]
  10. Bell J. K., Mullen G. E., Leifer C. A., Mazzoni A., Davies D. R., Segal D. M. ( 2003). Leucine-rich repeats and pathogen recognition in Toll-like receptors. Trends Immunol 24:528–533 [View Article][PubMed]
     [Google Scholar]
  11. Berg H. C. ( 2003). The rotary motor of bacterial flagella. Annu Rev Biochem 72:19–54 [View Article][PubMed]
     [Google Scholar]
  12. Beveridge T. J. ( 1999). Structures of gram-negative cell walls and their derived membrane vesicles. J Bacteriol 181:4725–4733[PubMed]
     [Google Scholar]
  13. Bishop R. E. ( 2005). Fundamentals of endotoxin structure and function. Contrib Microbiol 12:1–27 [View Article][PubMed]
     [Google Scholar]
  14. Bleau C., Monges A., Rashidan K., Laverdure J.-P., Lacroix M., Van Calsteren M.-R., Millette M., Savard R., Lamontagne L. ( 2010). Intermediate chains of exopolysaccharides from Lactobacillus rhamnosus RW-9595M increase IL-10 production by macrophages. J Appl Microbiol 108:666–675 [View Article][PubMed]
     [Google Scholar]
  15. Botos I., Segal D. M., Davies D. R. ( 2011). The structural biology of Toll-like receptors. Structure 19:447–459 [View Article][PubMed]
     [Google Scholar]
  16. Braun V., Wu H. C. 1994; Lipoproteins, structure, function, biosynthesis and model for protein export. Bacterial Cell Wall319–341 Ghuysen J.-M., Hakenbeck R. Amsterdam: Elsevier Science; [View Article]
     [Google Scholar]
  17. Brightbill H. D., Libraty D. H., Krutzik S. R., Yang R.-B., Belisle J. T., Bleharski J. R., Maitland M., Norgard M. V., Plevy S. E. & other authors ( 1999). Host defense mechanisms triggered by microbial lipoproteins through Toll-like receptors. Science 285:732–736 [View Article][PubMed]
     [Google Scholar]
  18. Buckley J. M., Wang J. H., Redmond H. P. ( 2006). Cellular reprogramming by gram-positive bacterial components: a review. J Leukoc Biol 80:731–741 [View Article][PubMed]
     [Google Scholar]
  19. Cario E., Podolsky D. K. ( 2000). Differential alteration in intestinal epithelial cell expression of Toll-like receptor 3 (TLR3) and TLR4 in inflammatory bowel disease. Infect Immun 68:7010–7017 [View Article][PubMed]
     [Google Scholar]
  20. Caroff M., Karibian D. ( 2003). Structure of bacterial lipopolysaccharides. Carbohydr Res 338:2431–2447 [View Article][PubMed]
     [Google Scholar]
  21. Cerning J. ( 1990). Exocellular polysaccharides produced by lactic acid bacteria. FEMS Microbiol Rev 7:113–130[PubMed] [CrossRef]
     [Google Scholar]
  22. Chabot S., Yu H.-L., De Léséleuc L., Cloutier D., Van Calsteren M.-R., Lessard M., Roy D., Lacroix M., Oth D. ( 2001). Exopolysaccharides from Lactobacillus rhamnosus RW-9595M stimulate TNF, IL-6 and IL-12 in human and mouse cultured immunocompetent cells, and IFN-γ in mouse splenocytes. Lait 81:683–697 [View Article]
     [Google Scholar]
  23. Chamaillard M., Hashimoto M., Horie Y., Masumoto J., Qiu S., Saab L., Ogura Y., Kawasaki A., Fukase K. & other authors ( 2003). An essential role for NOD1 in host recognition of bacterial peptidoglycan containing diaminopimelic acid. Nat Immunol 4:702–707 [View Article][PubMed]
     [Google Scholar]
  24. Chatterjee D., Chaudhuri K. ( 2013). Vibrio cholerae O395 outer membrane vesicles modulate intestinal epithelial cells in a NOD1 protein-dependent manner and induce dendritic cell-mediated Th2/Th17 cell responses. J Biol Chem 288:4299–4309 [View Article][PubMed]
     [Google Scholar]
  25. Ciofu O., Beveridge T. J., Kadurugamuwa J. L., Walther-Rasmussen J., Høiby N. ( 2000). Chromosomal β-lactamase is packaged into membrane vesicles and secreted from Pseudomonas aeruginosa . J Antimicrob Chemother 45:9–13 [View Article][PubMed]
     [Google Scholar]
  26. Ciszek-Lenda M., Nowak B., Sróttek M., Gamian A., Marcinkiewicz J. ( 2011). Immunoregulatory potential of exopolysaccharide from Lactobacillus rhamnosus KL37: effects on the production of inflammatory mediators by mouse macrophages. Int J Exp Pathol 92:382–391 [View Article][PubMed]
     [Google Scholar]
  27. Dalpke A., Frank J., Peter M., Heeg K. ( 2006). Activation of toll-like receptor 9 by DNA from different bacterial species. Infect Immun 74:940–946 [View Article][PubMed]
     [Google Scholar]
  28. De Vuyst L., Degeest B. ( 1999). Heteropolysaccharides from lactic acid bacteria. FEMS Microbiol Rev 23:153–177[PubMed] [CrossRef]
     [Google Scholar]
  29. DeSesso J. M., Jacobson C. F. ( 2001). Anatomical and physiological parameters affecting gastrointestinal absorption in humans and rats. Food Chem Toxicol 39:209–228 [View Article][PubMed]
     [Google Scholar]
  30. Dorward D. W., Garon C. F., Judd R. C. ( 1989). Export and intercellular transfer of DNA via membrane blebs of Neisseria gonorrhoeae . J Bacteriol 171:2499–2505[PubMed]
     [Google Scholar]
  31. Durlu-Özkaya F., Aslim B., Ozkaya M. T. ( 2007). Effect of exopolysaccharides (EPSs) produced by Lactobacillus delbrueckii subsp. bulgaricus strains to bacteriophage and nisin sensitivity of the bacteria. LWT-Food Sci Technol 40:564–568 [View Article]
     [Google Scholar]
  32. Dziarski R. ( 2003). Recognition of bacterial peptidoglycan by the innate immune system. Cell Mol Life Sci 60:1793–1804 [View Article][PubMed]
     [Google Scholar]
  33. Dziarski R., Gupta D. ( 2005). Staphylococcus aureus peptidoglycan is a Toll-like receptor 2 activator: a reevaluation. Infect Immun 73:5212–5216 [View Article][PubMed]
     [Google Scholar]
  34. Ellis T. N., Leiman S. A., Kuehn M. J. ( 2010). Naturally produced outer membrane vesicles from Pseudomonas aeruginosa elicit a potent innate immune response via combined sensing of both lipopolysaccharide and protein components. Infect Immun 78:3822–3831 [View Article][PubMed]
     [Google Scholar]
  35. Erridge C., Bennett-Guerrero E., Poxton I. R. ( 2002). Structure and function of lipopolysaccharides. Microbes Infect 4:837–851 [View Article][PubMed]
     [Google Scholar]
  36. Ewaschuk J. B., Backer J. L., Churchill T. A., Obermeier F., Krause D. O., Madsen K. L. ( 2007). Surface expression of Toll-like receptor 9 is upregulated on intestinal epithelial cells in response to pathogenic bacterial DNA. Infect Immun 75:2572–2579 [View Article][PubMed]
     [Google Scholar]
  37. Fenton M. J., Golenbock D. T. ( 1998). LPS-binding proteins and receptors. J Leukoc Biol 64:25–32[PubMed]
     [Google Scholar]
  38. Franchimont D., Vermeire S., El Housni H., Pierik M., Van Steen K., Gustot T., Quertinmont E., Abramowicz M., Van Gossum A. & other authors ( 2004). Deficient host-bacteria interactions in inflammatory bowel disease? The toll-like receptor (TLR)-4 Asp299gly polymorphism is associated with Crohn’s disease and ulcerative colitis. Gut 53:987–992 [View Article][PubMed]
     [Google Scholar]
  39. Furrie E., Macfarlane S., Thomson G., Macfarlane G. T. Microbiology & Gut Biology Group Tayside Tissue & Tumour Bank ( 2005). Toll-like receptors-2, -3 and -4 expression patterns on human colon and their regulation by mucosal-associated bacteria. Immunology 115:565–574 [View Article][PubMed]
     [Google Scholar]
  40. Galanos C., Lüderitz O., Rietschel E. T., Westphal O., Brade H., Brade L., Freudenberg M., Schade U., Imoto M. & other authors ( 1985). Synthetic and natural Escherichia coli free lipid A express identical endotoxic activities. Eur J Biochem 148:1–5 [View Article][PubMed]
     [Google Scholar]
  41. Gewirtz A. T., Navas T. A., Lyons S., Godowski P. J., Madara J. L. ( 2001). Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 167:1882–1885[PubMed] [CrossRef]
     [Google Scholar]
  42. Gill S. R., Pop M., Deboy R. T., Eckburg P. B., Turnbaugh P. J., Samuel B. S., Gordon J. I., Relman D. A., Fraser-Liggett C. M., Nelson K. E. ( 2006). Metagenomic analysis of the human distal gut microbiome. Science 312:1355–1359 [View Article][PubMed]
     [Google Scholar]
  43. Girardin S. E., Boneca I. G., Carneiro L. A., Antignac A., Jéhanno M., Viala J., Tedin K., Taha M. K., Labigne A. & other authors ( 2003a). Nod1 detects a unique muropeptide from Gram-negative bacterial peptidoglycan. Science 300:1584–1587 [View Article][PubMed]
     [Google Scholar]
  44. Girardin S. E., Boneca I. G., Viala J., Chamaillard M., Labigne A., Thomas G., Philpott D. J., Sansonetti P. J. ( 2003b). Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J Biol Chem 278:8869–8872 [View Article][PubMed]
     [Google Scholar]
  45. Granato D., Perotti F., Masserey I., Rouvet M., Golliard M., Servin A., Brassart D. ( 1999). Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl Environ Microbiol 65:1071–1077[PubMed]
     [Google Scholar]
  46. Gribar S. C., Anand R. J., Sodhi C. P., Hackam D. J. ( 2008). The role of epithelial Toll-like receptor signaling in the pathogenesis of intestinal inflammation. J Leukoc Biol 83:493–498 [View Article][PubMed]
     [Google Scholar]
  47. Guarner F., Malagelada J.-R. ( 2003). Gut flora in health and disease. Lancet 361:512–519 [View Article][PubMed]
     [Google Scholar]
  48. Guha M., Mackman N. ( 2001). LPS induction of gene expression in human monocytes. Cell Signal 13:85–94 [View Article][PubMed]
     [Google Scholar]
  49. Hailman E., Lichenstein H. S., Wurfel M. M., Miller D. S., Johnson D. A., Kelley M., Busse L. A., Zukowski M. M., Wright S. D. ( 1994). Lipopolysaccharide (LPS)-binding protein accelerates the binding of LPS to CD14. J Exp Med 179:269–277 [View Article][PubMed]
     [Google Scholar]
  50. Hayashi F., Smith K. D., Ozinsky A., Hawn T. R., Yi E. C., Goodlett D. R., Eng J. K., Akira S., Underhill D. M., Aderem A. ( 2001). The innate immune response to bacterial flagellin is mediated by Toll-like receptor 5. Nature 410:1099–1103 [View Article][PubMed]
     [Google Scholar]
  51. Hemmi H., Takeuchi O., Kawai T., Kaisho T., Sato S., Sanjo H., Matsumoto M., Hoshino K., Wagner H. & other authors ( 2000). A Toll-like receptor recognizes bacterial DNA. Nature 408:740–745 [View Article][PubMed]
     [Google Scholar]
  52. Heumann D., Roger T. ( 2002). Initial responses to endotoxins and Gram-negative bacteria. Clin Chim Acta 323:59–72 [View Article][PubMed]
     [Google Scholar]
  53. Hidalgo-Cantabrana C., López P., Gueimonde M., de los Reyes-Gavilán C. G., Suárez A., Margolles A., Ruas-Madiedo P. ( 2012). Immune modulation capability of exopolysaccharides synthesised by lactic acid bacteria and bifidobacteria. Probiotics Antimicrob Proteins 4:227–237 [View Article]
     [Google Scholar]
  54. Hirschfeld M., Ma Y., Weis J. H., Vogel S. N., Weis J. J. ( 2000). Cutting edge: repurification of lipopolysaccharide eliminates signaling through both human and murine toll-like receptor 2. J Immunol 165:618–622[PubMed] [CrossRef]
     [Google Scholar]
  55. Hoffman W. D., Natanson C. ( 1993). Endotoxin in septic shock. Anesth Analg 77:613–624 [View Article][PubMed]
     [Google Scholar]
  56. Holst O., Ulmer A. J., Brade H., Flad H.-D., Rietschel E. T. ( 1996). Biochemistry and cell biology of bacterial endotoxins. FEMS Immunol Med Microbiol 16:83–104 [View Article][PubMed]
     [Google Scholar]
  57. Hooper L. V. ( 2004). Bacterial contributions to mammalian gut development. Trends Microbiol 12:129–134 [View Article][PubMed]
     [Google Scholar]
  58. Hooper L. V., Littman D. R., Macpherson A. J. ( 2012). Interactions between the microbiota and the immune system. Science 336:1268–1273 [View Article][PubMed]
     [Google Scholar]
  59. Hornung V., Rothenfusser S., Britsch S., Krug A., Jahrsdörfer B., Giese T., Endres S., Hartmann G. ( 2002). Quantitative expression of toll-like receptor 1-10 mRNA in cellular subsets of human peripheral blood mononuclear cells and sensitivity to CpG oligodeoxynucleotides. J Immunol 168:4531–4537[PubMed] [CrossRef]
     [Google Scholar]
  60. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. ( 1999). Cutting edge: Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J Immunol 162:3749–3752[PubMed]
     [Google Scholar]
  61. Huang Y., Li N., Liboni K., Neu J. ( 2003). Glutamine decreases lipopolysaccharide-induced IL-8 production in Caco-2 cells through a non-NF-κB p50 mechanism. Cytokine 22:77–83 [View Article][PubMed]
     [Google Scholar]
  62. Hugot J. P., Chamaillard M., Zouali H., Lesage S., Cézard J. P., Belaiche J., Almer S., Tysk C., O’Morain C. A. & other authors ( 2001). Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 411:599–603 [View Article][PubMed]
     [Google Scholar]
  63. Inohara N., Ogura Y., Fontalba A., Gutierrez O., Pons F., Crespo J., Fukase K., Inamura S., Kusumoto S. & other authors ( 2003). Host recognition of bacterial muramyl dipeptide mediated through NOD2. Implications for Crohn’s disease. J Biol Chem 278:5509–5512 [View Article][PubMed]
     [Google Scholar]
  64. Ismail S., Hampton M. B., Keenan J. I. ( 2003). Helicobacter pylori outer membrane vesicles modulate proliferation and interleukin-8 production by gastric epithelial cells. Infect Immun 71:5670–5675 [View Article][PubMed]
     [Google Scholar]
  65. Iwaki D., Mitsuzawa H., Murakami S., Sano H., Konishi M., Akino T., Kuroki Y. ( 2002). The extracellular Toll-like receptor 2 domain directly binds peptidoglycan derived from Staphylococcus aureus . J Biol Chem 277:24315–24320 [View Article][PubMed]
     [Google Scholar]
  66. Iwasaki A., Medzhitov R. ( 2004). Toll-like receptor control of the adaptive immune responses. Nat Immunol 5:987–995 [View Article][PubMed]
     [Google Scholar]
  67. Kadurugamuwa J. L., Beveridge T. J. ( 1995). Virulence factors are released from Pseudomonas aeruginosa in association with membrane vesicles during normal growth and exposure to gentamicin: a novel mechanism of enzyme secretion. J Bacteriol 177:3998–4008[PubMed]
     [Google Scholar]
  68. Kaparakis M., Turnbull L., Carneiro L., Firth S., Coleman H. A., Parkington H. C., Le Bourhis L., Karrar A., Viala J. & other authors ( 2010). Bacterial membrane vesicles deliver peptidoglycan to NOD1 in epithelial cells. Cell Microbiol 12:372–385 [View Article][PubMed]
     [Google Scholar]
  69. Karched M., Ihalin R., Eneslätt K., Zhong D., Oscarsson J., Wai S. N., Chen C., Asikainen S. E. ( 2008). Vesicle-independent extracellular release of a proinflammatory outer membrane lipoprotein in free-soluble form. BMC Microbiol 8:18 [View Article][PubMed]
     [Google Scholar]
  70. Kesty N. C., Kuehn M. J. ( 2004). Incorporation of heterologous outer membrane and periplasmic proteins into Escherichia coli outer membrane vesicles. J Biol Chem 279:2069–2076 [View Article][PubMed]
     [Google Scholar]
  71. Kesty N. C., Mason K. M., Reedy M., Miller S. E., Kuehn M. J. ( 2004). Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J 23:4538–4549 [View Article][PubMed]
     [Google Scholar]
  72. Kirschning C. J., Wesche H., Merrill Ayres T., Rothe M. ( 1998). Human Toll-like receptor 2 confers responsiveness to bacterial lipopolysaccharide. J Exp Med 188:2091–2097 [View Article][PubMed]
     [Google Scholar]
  73. Kitazawa H., Harata T., Uemura J., Saito T., Kaneko T., Itoh T. ( 1998). Phosphate group requirement for mitogenic activation of lymphocytes by an extracellular phosphopolysaccharide from Lactobacillus delbrueckii ssp. bulgaricus . Int J Food Microbiol 40:169–175 [View Article][PubMed]
     [Google Scholar]
  74. Laws A. P., Gu Y., Marshall V. ( 2001). Biosynthesis, characterisation, and design of bacterial exopolysaccharides from lactic acid bacteria. Biotechnol Adv 19:597–625 [View Article][PubMed]
     [Google Scholar]
  75. Lebeer S., Claes I., Tytgat H. L., Verhoeven T. L. A., Marien E., von Ossowski I., Reunanen J., Palva A., Vos W. M. & other authors ( 2012). Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl Environ Microbiol 78:185–193 [View Article][PubMed]
     [Google Scholar]
  76. Lee J., Mo J.-H., Katakura K., Alkalay I., Rucker A. N., Liu Y.-T., Lee H.-K., Shen C., Cojocaru G. & other authors ( 2006). Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 8:1327–1336 [View Article][PubMed]
     [Google Scholar]
  77. Lee E.-Y., Choi D.-S., Kim K.-P., Gho Y. S. ( 2008). Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom Rev 27:535–555 [View Article][PubMed]
     [Google Scholar]
  78. Lin M.-H., Yang Y.-L., Chen Y.-P., Hua K.-F., Lu C.-P., Sheu F., Lin G.-H., Tsay S.-S., Liang S.-M., Wu S. H. ( 2011). A novel exopolysaccharide from the biofilm of Thermus aquaticus YT-1 induces the immune response through Toll-like receptor 2. J Biol Chem 286:17736–17745 [View Article][PubMed]
     [Google Scholar]
  79. Linder H., Engberg I., Baltzer I. M., Jann K., Svanborg-Edén C. ( 1988). Induction of inflammation by Escherichia coli on the mucosal level: requirement for adherence and endotoxin. Infect Immun 56:1309–1313[PubMed]
     [Google Scholar]
  80. Liu C.-T., Chu F.-J., Chou C. C., Yu R.-C. ( 2011). Antiproliferative and anticytotoxic effects of cell fractions and exopolysaccharides from Lactobacillus casei 01. Mutat Res 721:157–162 [View Article][PubMed]
     [Google Scholar]
  81. Ljungdahl M., Lundholm M., Katouli M., Rasmussen I., Engstrand L., Haglund U. ( 2000). Bacterial translocation in experimental shock is dependent on the strains in the intestinal flora. Scand J Gastroenterol 35:389–397 [View Article][PubMed]
     [Google Scholar]
  82. Lodes M. J., Cong Y., Elson C. O., Mohamath R., Landers C. J., Targan S. R., Fort M., Hershberg R. M. ( 2004). Bacterial flagellin is a dominant antigen in Crohn disease. J Clin Invest 113:1296–1306[PubMed] [CrossRef]
     [Google Scholar]
  83. Looijesteijn P. J., Trapet L., de Vries E., Abee T., Hugenholtz J. ( 2001). Physiological function of exopolysaccharides produced by Lactococcus lactis . Int J Food Microbiol 64:71–80 [View Article][PubMed]
     [Google Scholar]
  84. Lozupone C. A., Stombaugh J. I., Gordon J. I., Jansson J. K., Knight R. ( 2012). Diversity, stability and resilience of the human gut microbiota. Nature 489:220–230 [View Article][PubMed]
     [Google Scholar]
  85. Macho Fernandez E., Valenti V., Rockel C., Hermann C., Pot B., Boneca I. G., Grangette C. ( 2011). Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 60:1050–1059 [View Article][PubMed]
     [Google Scholar]
  86. Macpherson A. J., Harris N. L. ( 2004). Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4:478–485 [View Article][PubMed]
     [Google Scholar]
  87. Manning A. J., Kuehn M. J. ( 2011). Contribution of bacterial outer membrane vesicles to innate bacterial defense. BMC Microbiol 11:258 [View Article][PubMed]
     [Google Scholar]
  88. Mashburn-Warren L. M., Whiteley M. ( 2006). Special delivery: vesicle trafficking in prokaryotes. Mol Microbiol 61:839–846 [View Article][PubMed]
     [Google Scholar]
  89. Maslanik T., Tannura K., Mahaffey L., Loughridge A. B., Benninson L., Ursell L., Greenwood B. N., Knight R., Fleshner M. ( 2012). Commensal bacteria and MAMPs are necessary for stress-induced increases in IL-1β and IL-18 but not IL-6, IL-10 or MCP-1. PLoS ONE 7:e50636 [View Article][PubMed]
     [Google Scholar]
  90. Masumoto J., Yang K., Varambally S., Hasegawa M., Tomlins S. A., Qiu S., Fujimoto Y., Kawasaki A., Foster S. J. & other authors ( 2006). Nod1 acts as an intracellular receptor to stimulate chemokine production and neutrophil recruitment in vivo. J Exp Med 203:203–213 [View Article][PubMed]
     [Google Scholar]
  91. McBroom A. J., Kuehn M. J. ( 2007). Release of outer membrane vesicles by Gram-negative bacteria is a novel envelope stress response. Mol Microbiol 63:545–558 [View Article][PubMed]
     [Google Scholar]
  92. Medzhitov R. ( 2001). Toll-like receptors and innate immunity. Nat Rev Immunol 1:135–145 [View Article][PubMed]
     [Google Scholar]
  93. Melmed G., Thomas L. S., Lee N., Tesfay S. Y., Lukasek K., Michelsen K. S., Zhou Y., Hu B., Arditi M., Abreu M. T. ( 2003). Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: implications for host-microbial interactions in the gut. J Immunol 170:1406–1415[PubMed] [CrossRef]
     [Google Scholar]
  94. Ogura Y., Bonen D. K., Inohara N., Nicolae D. L., Chen F. F., Ramos R., Britton H., Moran T., Karaliuskas R. & other authors ( 2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 411:603–606 [View Article][PubMed]
     [Google Scholar]
  95. Oostenbrug L. E., Drenth J. P., de Jong D. J., Nolte I. M., Oosterom E., van Dullemen H. M., van der Linde K., te Meerman G. J., van der Steege G. & other authors ( 2005). Association between Toll-like receptor 4 and inflammatory bowel disease. Inflamm Bowel Dis 11:567–575 [View Article][PubMed]
     [Google Scholar]
  96. Parker H., Chitcholtan K., Hampton M. B., Keenan J. I. ( 2010). Uptake of Helicobacter pylori outer membrane vesicles by gastric epithelial cells. Infect Immun 78:5054–5061 [View Article][PubMed]
     [Google Scholar]
  97. Poltorak A., He X., Smirnova I., Liu M.-Y., Van Huffel C., Du X., Birdwell D., Alejos E., Silva M. & other authors ( 1998). Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science 282:2085–2088 [View Article][PubMed]
     [Google Scholar]
  98. Poulsen L. V. ( 1999). Microbial biofilm in food processing. LWT-Food Sci Technol 32:321–326 [View Article]
     [Google Scholar]
  99. Rachmilewitz D., Katakura K., Karmeli F., Hayashi T., Reinus C., Rudensky B., Akira S., Takeda K., Lee J. & other authors ( 2004). Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 126:520–528 [View Article][PubMed]
     [Google Scholar]
  100. 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 [View Article][PubMed]
     [Google Scholar]
  101. Ramos H. C., Rumbo M., Sirard J.-C. ( 2004). Bacterial flagellins: mediators of pathogenicity and host immune responses in mucosa. Trends Microbiol 12:509–517 [View Article][PubMed]
     [Google Scholar]
  102. Renelli M., Matias V., Lo R. Y., Beveridge T. J. ( 2004). DNA-containing membrane vesicles of Pseudomonas aeruginosa PAO1 and their genetic transformation potential. Microbiology 150:2161–2169 [View Article][PubMed]
     [Google Scholar]
  103. Rietschel E. T., Kirikae T., Schade F. U., Mamat U., Schmidt G., Loppnow H., Ulmer A. J., Zähringer U., Seydel U. & other authors ( 1994). Bacterial endotoxin: molecular relationships of structure to activity and function. FASEB J 8:217–225[PubMed]
     [Google Scholar]
  104. Roller S., Dea I. C. M. ( 1992). Biotechnology in the production and modification of biopolymers for foods. Crit Rev Biotechnol 12:261–277 [View Article]
     [Google Scholar]
  105. Ruas-Madiedo P., Gueimonde M., Margolles A., de los Reyes-Gavilán C. G., Salminen S. ( 2006). Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J Food Prot 69:2011–2015[PubMed]
     [Google Scholar]
  106. Ruas-Madiedo P., Medrano M., Salazar N., De Los Reyes-Gavilán C. G., Pérez P. F., Abraham A. G. ( 2010). Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. J Appl Microbiol 109:2079–2086 [View Article][PubMed]
     [Google Scholar]
  107. Sanderson I. R., Walker W. A. ( 2006). TLRs in the gut I. The role of TLRs/Nods in intestinal development and homeostasis. Am J Physiol Gastrointest Liver Physiol 292:G6–G10 [View Article][PubMed]
     [Google Scholar]
  108. Schleifer K. H., Kandler O. ( 1972). Peptidoglycan types of bacterial cell walls and their taxonomic implications. Bacteriol Rev 36:407–477[PubMed]
     [Google Scholar]
  109. Schooling S. R., Beveridge T. J. ( 2006). Membrane vesicles: an overlooked component of the matrices of biofilms. J Bacteriol 188:5945–5957 [View Article][PubMed]
     [Google Scholar]
  110. Schuerer-Maly C.-C., Eckmann L., Kagnoff M. F., Falco M. T., Maly F.-E. ( 1994). Colonic epithelial cell lines as a source of interleukin-8: stimulation by inflammatory cytokines and bacterial lipopolysaccharide. Immunology 81:85–91[PubMed]
     [Google Scholar]
  111. Schwandner R., Dziarski R., Wesche H., Rothe M., Kirschning C. J. ( 1999). Peptidoglycan- and lipoteichoic acid-induced cell activation is mediated by Toll-like receptor 2. J Biol Chem 274:17406–17409 [View Article][PubMed]
     [Google Scholar]
  112. Sellati T. J., Bouis D. A., Kitchens R. L., Darveau R. P., Pugin J., Ulevitch R. J., Gangloff S. C., Goyert S. M., Norgard M. V., Radolf J. D. ( 1998). Treponema pallidum and Borrelia burgdorferi lipoproteins and synthetic lipopeptides activate monocytic cells via a CD14-dependent pathway distinct from that used by lipopolysaccharide. J Immunol 160:5455–5464[PubMed]
     [Google Scholar]
  113. Sengül N., Aslím B., Uçar G., Yücel N., Işik S., Bozkurt H., Sakaoğullari Z., Atalay F. ( 2006). Effects of exopolysaccharide-producing probiotic strains on experimental colitis in rats. Dis Colon Rectum 49:250–258 [View Article][PubMed]
     [Google Scholar]
  114. Shen Y., Giardino Torchia M. L., Lawson G. W., Karp C. L., Ashwell J. D., Mazmanian S. K. ( 2012). Outer membrane vesicles of a human commensal mediate immune regulation and disease protection. Cell Host Microbe 12:509–520 [View Article][PubMed]
     [Google Scholar]
  115. Shimazu R., Akashi S., Ogata H., Nagai Y., Fukudome K., Miyake K., Kimoto M. ( 1999). MD-2, a molecule that confers lipopolysaccharide responsiveness on Toll-like receptor 4. J Exp Med 189:1777–1782 [View Article][PubMed]
     [Google Scholar]
  116. Smirnova M. G., Guo L., Birchall J. P., Pearson J. P. ( 2003). LPS up-regulates mucin and cytokine mRNA expression and stimulates mucin and cytokine secretion in goblet cells. Cell Immunol 221:42–49 [View Article][PubMed]
     [Google Scholar]
  117. Soler-Rodriguez A. M., Zhang H., Lichenstein H. S., Qureshi N., Niesel D. W., Crowe S. E., Peterson J. W., Klimpel G. R. ( 2000). Neutrophil activation by bacterial lipoprotein versus lipopolysaccharide: differential requirements for serum and CD14. J Immunol 164:2674–2683[PubMed] [CrossRef]
     [Google Scholar]
  118. Standiford T. J., Arenberg D. A., Danforth J. M., Kunkel S. L., VanOtteren G. M., Strieter R. M. ( 1994). Lipoteichoic acid induces secretion of interleukin-8 from human blood monocytes: a cellular and molecular analysis. Infect Immun 62:119–125[PubMed]
     [Google Scholar]
  119. Steiner T. S., Nataro J. P., Poteet-Smith C. E., Smith J. A., Guerrant R. L. ( 2000). Enteroaggregative Escherichia coli expresses a novel flagellin that causes IL-8 release from intestinal epithelial cells. J Clin Invest 105:1769–1777 [View Article][PubMed]
     [Google Scholar]
  120. Sutcliffe I. C., Russell R. R. B. ( 1995). Lipoproteins of gram-positive bacteria. J Bacteriol 177:1123–1128[PubMed]
     [Google Scholar]
  121. Takeda K., Akira S. ( 2005). Toll-like receptors in innate immunity. Int Immunol 17:1–14 [View Article][PubMed]
     [Google Scholar]
  122. Takeda K., Kaisho T., Akira S. ( 2003). Toll-like receptors. Annu Rev Immunol 21:335–376 [View Article][PubMed]
     [Google Scholar]
  123. Takeuchi O., Hoshino K., Kawai T., Sanjo H., Takada H., Ogawa T., Takeda K., Akira S. ( 1999). Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity 11:443–451 [View Article][PubMed]
     [Google Scholar]
  124. Takeuchi O., Sato S., Horiuchi T., Hoshino K., Takeda K., Dong Z., Modlin R. L., Akira S. ( 2002). Cutting edge: role of Toll-like receptor 1 in mediating immune response to microbial lipoproteins. J Immunol 169:10–14[PubMed] [CrossRef]
     [Google Scholar]
  125. Targan S. R., Landers C. J., Yang H., Lodes M. J., Cong Y., Papadakis K. A., Vasiliauskas E., Elson C. O., Hershberg R. M. ( 2005). Antibodies to CBir1 flagellin define a unique response that is associated independently with complicated Crohn’s disease. Gastroenterology 128:2020–2028 [View Article][PubMed]
     [Google Scholar]
  126. Travassos L. H., Girardin S. E., Philpott D. J., Blanot D., Nahori M.-A., Werts C., Boneca I. G. ( 2004). Toll-like receptor 2-dependent bacterial sensing does not occur via peptidoglycan recognition. EMBO Rep 5:1000–1006 [View Article][PubMed]
     [Google Scholar]
  127. Triantafilou M., Triantafilou K. ( 2002). Lipopolysaccharide recognition: CD14, TLRs and the LPS-activation cluster. Trends Immunol 23:301–304 [View Article][PubMed]
     [Google Scholar]
  128. Ulevitch R. J., Tobias P. S. ( 1999). Recognition of Gram-negative bacteria and endotoxin by the innate immune system. Curr Opin Immunol 11:19–22 [View Article][PubMed]
     [Google Scholar]
  129. Vidal K., Donnet-Hughes A., Granato D. ( 2002). Lipoteichoic acids from Lactobacillus johnsonii strain La1 and Lactobacillus acidophilus strain La10 antagonize the responsiveness of human intestinal epithelial HT29 cells to lipopolysaccharide and gram-negative bacteria. Infect Immun 70:2057–2064 [View Article][PubMed]
     [Google Scholar]
  130. Vijay-Kumar M., Sanders C. J., Taylor R. T., Kumar A., Aitken J. D., Sitaraman S. V., Neish A. S., Uematsu S., Akira S. & other authors ( 2007). Deletion of TLR5 results in spontaneous colitis in mice. J Clin Invest 117:3909–3921[PubMed]
     [Google Scholar]
  131. Vinderola G., Perdigón G., Duarte J., Farnworth E., Matar C. ( 2006). Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine 36:254–260 [View Article][PubMed]
     [Google Scholar]
  132. Wang Q., Dziarski R., Kirschning C. J., Muzio M., Gupta D. ( 2001). Micrococci and peptidoglycan activate TLR2→MyD88→IRAK→TRAF→NIK→IKK→NF-κB signal transduction pathway that induces transcription of interleukin-8. Infect Immun 69:2270–2276 [View Article][PubMed]
     [Google Scholar]
  133. Wang J. H., Doyle M., Manning B. J., Di Wu Q., Blankson S., Redmond H. P. ( 2002). Induction of bacterial lipoprotein tolerance is associated with suppression of Toll-like receptor 2 expression. J Biol Chem 277:36068–36075 [View Article][PubMed]
     [Google Scholar]
  134. Watnick P. I., Kolter R. ( 1999). Steps in the development of a Vibrio cholerae El Tor biofilm. Mol Microbiol 34:586–595 [View Article][PubMed]
     [Google Scholar]
  135. Wu M.-H., Pan T.-M., Wu Y.-J., Chang S.-J., Chang M.-S., Hu C.-Y. ( 2010). Exopolysaccharide activities from probiotic bifidobacterium: immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. Int J Food Microbiol 144:104–110 [View Article][PubMed]
     [Google Scholar]
  136. Yang R. B., Mark M. R., Gray A., Huang A., Xie M. H., Zhang M., Goddard A., Wood W. I., Gurney A. L., Godowski P. J. ( 1998). Toll-like receptor-2 mediates lipopolysaccharide-induced cellular signalling. Nature 395:284–288 [View Article][PubMed]
     [Google Scholar]
  137. Yaron S., Kolling G. L., Simon L., Matthews K. R. ( 2000). Vesicle-mediated transfer of virulence genes from Escherichia coli O157 : H7 to other enteric bacteria. Appl Environ Microbiol 66:4414–4420 [View Article][PubMed]
     [Google Scholar]
  138. Zhang H., Niesel D. W., Peterson J. W., Klimpel G. R. ( 1998). Lipoprotein release by bacteria: potential factor in bacterial pathogenesis. Infect Immun 66:5196–5201[PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.064717-0
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Exploring the immunomodulatory potential of microbial-associated molecular patterns derived from the enteric bacterial microbiota
Microbiology 159, 1535 (2013); https://doi.org/10.1099/mic.0.064717-0
/content/journal/micro/10.1099/mic.0.064717-0
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