Skip to main content
Log in

Commensal bacteria and epithelial cross talk in the developing intestine

  • Published:
Current Gastroenterology Reports Aims and scope Submit manuscript

Abstract

Indigenous intestinal microbes have co-evolved with the intestinal immune system to form a symbiotic ecosystem. In the postnatal period, intestinal microbes provide the developing gut with stimuli that are necessary for healthy maturation of the intestinal immune system. Cross talk between the host and commensal microbes is an essential component of gut homeostasis mechanisms also in later life. During recent years, innovative research has shed light on the molecular mechanisms of these interactions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References and Recommended Reading

  1. Rautava S, Kalliomaki M, Isolauri E: New therapeutic strategy for combating the increasing burden of allergic disease: Probiotics-A Nutrition, Allergy, Mucosal Immunology and Intestinal Microbiota (NAMI) Research Group report. J Allergy Clin Immunol 2005, 116:31–37.

    Article  PubMed  Google Scholar 

  2. Zhang G, Ghosh S: Toll-like receptor-mediated NF-kappaB activation: a phylogenetically conserved paradigm in innate immunity. J Clin Invest 2001, 107:13–19.

    Article  PubMed  CAS  Google Scholar 

  3. Schnare M, Barton GM, Holt AC, et al.: Toll-like receptors control activation of adaptive immune responses. Nat Immunol 2001, 2:947–950.

    Article  PubMed  CAS  Google Scholar 

  4. Kaisho T, Akira S: Toll-like receptor function and signaling. J Allergy Clin Immunol 2006, 117:979–987.

    Article  PubMed  CAS  Google Scholar 

  5. Akira S, Uematsu S, Takeuchi O: Pathogen recognition and innate immunity. Cell 2006, 124:783–801.

    Article  PubMed  CAS  Google Scholar 

  6. Cario E: Bacterial interactions with cells of the intestinal mucosa: Toll-like receptors and NOD2. Gut 2005, 54:1182–1193.

    Article  PubMed  CAS  Google Scholar 

  7. Hausmann M, Kiessling S, Mestermann S, et al.: Toll-like receptors 2 and 4 are up-regulated during intestinal inflammation. Gastroenterology 2002, 122:1987–2000.

    Article  PubMed  CAS  Google Scholar 

  8. Hart AL, Al-Hassi HO, Rigby RJ, et al.: Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 2005, 129:50–65.

    Article  PubMed  CAS  Google Scholar 

  9. Kawai T, Akira S: TLR signaling. Semin Immunol 2007, 19:24–32.

    Article  PubMed  CAS  Google Scholar 

  10. Hayden MS, Ghosh S: Signaling to NF-kappaB. Genes Dev 2004, 18:2195–2224.

    Article  PubMed  CAS  Google Scholar 

  11. O’Neill LA, Fitzgerald KA, Bowie AG: The Toll-IL-1 receptor adaptor family grows to five members. Trends Immunol 2003, 24:286–290.

    Article  PubMed  CAS  Google Scholar 

  12. Otte JM, Cario E, Podolsky DK: Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 2004, 126:1054–1070.

    Article  PubMed  CAS  Google Scholar 

  13. Haller D, Jobin C: Interaction between resident luminal bacteria and the host: can a healthy relationship turn sour? J Pediatr Gastroenterol Nutr 2004, 38:123–136.

    Article  PubMed  Google Scholar 

  14. Ogura Y, Bonen DK, Inohara N, et al.: A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 2001, 411:603–606.

    Article  PubMed  CAS  Google Scholar 

  15. Girardin SE, Boneca IG, Carneiro LA, et al.: Nod1 detects a unique muropeptide from gram-negative bacterial peptidoglycan. Science 2003, 300:1584–1587.

    Article  PubMed  CAS  Google Scholar 

  16. Chin AI, Dempsey PW, Bruhn K, et al.: Involvement of receptor-interacting protein 2 in innate and adaptive immune responses. Nature 2002, 416:190–194.

    Article  PubMed  CAS  Google Scholar 

  17. Eder W, Klimecki W, Yu L, et al.: Toll-like receptor 2 as a major gene for asthma in children of European farmers. J Allergy Clin Immunol 2004, 113:482–488.

    Article  PubMed  CAS  Google Scholar 

  18. Ley RE, Peterson DA, Gordon JI: Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell. 2006, 124:837–848.

    Article  PubMed  CAS  Google Scholar 

  19. Tannock GW: What immunologists should know about bacterial communities of the human bowel. Semin Immunol 2006, 19:94–105

    Article  PubMed  CAS  Google Scholar 

  20. Matsumiya Y, Kato N, Watanabe K, Kato H: Molecular epidemiological study of vertical transmission of vaginal Lactobacillus species from mothers to newborn infants in Japanese, by arbitrarily primed polymerase chain reaction. J Infect Chemother 2002, 8:43–49.

    PubMed  CAS  Google Scholar 

  21. Gronlund MM, Lehtonen OP, Eerola E, Kero P: Fecal microflora in healthy infants born by different methods of delivery: permanent changes in intestinal flora after cesarean delivery. J Pediatr Gastroenterol Nutr 1999, 28:19–25.

    Article  PubMed  CAS  Google Scholar 

  22. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, et al.: Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J Pediatr Gastroenterol Nutr 2000, 30:61–67.

    Article  PubMed  CAS  Google Scholar 

  23. Bennet R, Eriksson M, Nord CE, Zetterstrom R: Fecal bacterial microflora of newborn infants during intensive care management and treatment with five antibiotic regimens. Pediatr Infect Dis 1986, 5:533–539.

    Article  PubMed  CAS  Google Scholar 

  24. de la Cochetiere MF, Piloquet H, des Robert C, et al.: Early intestinal bacterial colonization and necrotizing enterocolitis in premature infants: the putative role of Clostridium. Pediatr Res 2004, 56:366–370.

    Article  PubMed  Google Scholar 

  25. Rautava S: Potential uses of probiotics in the neonate. Semin Fetal Neonatal Med 2007, 12:45–53.

    Article  PubMed  Google Scholar 

  26. Hooper LV: Bacterial contributions to mammalian gut development. Trends Microbiol 2004, 12:129–134.

    Article  PubMed  CAS  Google Scholar 

  27. Hooper LV, Wong MH, Thelin A, et al.: Molecular analysis of commensal host-microbial relationships in the intestine. Science 2001, 291:881–884.

    Article  PubMed  CAS  Google Scholar 

  28. Bron PA, Marco M, Hoffer SM, et al.: Genetic characterization of the bile salt response in Lactobacillus plantarum and analysis of responsive promoters in vitro and in situ in the gastrointestinal tract. J Bacteriol 2004, 186:7829–7835.

    Article  PubMed  CAS  Google Scholar 

  29. Sudo N, Sawamura S, Tanaka K, et al.: The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 1997, 159:1739–1745.

    PubMed  CAS  Google Scholar 

  30. Bashir ME, Louie S, Shi HN, et al.: Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J Immunol 2004, 172:6978–6987.

    PubMed  CAS  Google Scholar 

  31. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL: An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 2005, 122:107–118.

    Article  PubMed  CAS  Google Scholar 

  32. Liu PT, Stenger S, Li H, et al.: Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 2006, 311:1770–1773.

    Article  PubMed  CAS  Google Scholar 

  33. Lee JY, Zhao L, Youn HS, et al.: Saturated fatty acid activates but polyunsaturated fatty acid inhibits Toll-like receptor 2 dimerized with Toll-like receptor 6 or 1. J Biol Chem 2004, 279:16971–16979.

    Article  PubMed  CAS  Google Scholar 

  34. Ruiz PA, Hoffmann M, Szcesny S, et al.: Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats. Immunology 2005, 115:441–450.

    Article  PubMed  CAS  Google Scholar 

  35. Savidge TC, Newman PG, Pan WH, et al.: Lipopolysaccharide-induced human enterocyte tolerance to cytokine-mediated interleukin-8 production may occur independently of TLR-4/MD-2 signaling. Pediatr Res 2006, 59:89–95.

    Article  PubMed  CAS  Google Scholar 

  36. Lee J, Mo JH, Katakura K, et al.: Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 2006, 8:1327–1336.

    Article  PubMed  CAS  Google Scholar 

  37. Melmed G, Thomas LS, Lee N, et al.: 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 2003, 170:1406–1415.

    PubMed  CAS  Google Scholar 

  38. Gewirtz AT, Navas TA, Lyons S, et al.: Cutting edge: bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J Immunol 2001, 167:1882–1885.

    PubMed  CAS  Google Scholar 

  39. Malin M, Isolauri E, Pikkarainen P, et al.: Enhanced absorption of macromolecules. A secondary factor in Crohn’s disease. Dig Dis Sci 1996, 41:1423–1428.

    Article  PubMed  CAS  Google Scholar 

  40. Collier-Hyams LS, Zeng H, Sun J, et al.: Cutting edge: Salmonella AvrA effector inhibits the key proinflammatory, anti-apoptotic NF-kappa B pathway. J Immunol 2002, 169:2846–2850.

    PubMed  CAS  Google Scholar 

  41. Neish AS, Gewirtz AT, Zeng H, et al.: Prokaryotic regulation of epithelial responses by inhibition of IkappaB-alpha ubiquitination. Science 2000, 289:1560–1563.

    Article  PubMed  CAS  Google Scholar 

  42. Kelly D, Campbell JI, King TP, et al.: Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-gamma and RelA. Nat Immunol Jan 2004, 5:104–112.

    Article  CAS  Google Scholar 

  43. Kanneganti TD, Lamkanfi M, Kim YG, et al.: Pannexin-1-mediated recognition of bacterial molecules activates the cryopyrin inflammasome independent of Toll-like receptor signaling. Immunity 2007, 26:433–443.

    Article  PubMed  CAS  Google Scholar 

  44. Nenci A, Becker C, Wullaert A, et al.: Epithelial NEMO links innate immunity to chronic intestinal inflammation. Nature 2007, 446:557–561.

    Article  PubMed  CAS  Google Scholar 

  45. Rakoff-Nahoum S, Paglino J, Eslami-Varzaneh F, et al.: Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229–241.

    Article  PubMed  CAS  Google Scholar 

  46. Rescigno M, Urbano M, Valzasina B, et al.: Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2001, 2:361–367.

    Article  PubMed  CAS  Google Scholar 

  47. Michelsen KS, Aicher A, Mohaupt M, et al.: The role of toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS). Peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J Biol Chem 2001, 276:25680–25686.

    Article  PubMed  CAS  Google Scholar 

  48. Turnbull EL, Yrlid U, Jenkins CD, Macpherson GG: Intestinal dendritic cell subsets: differential effects of systemic TLR4 stimulation on migratory fate and activation in vivo. J Immunol 2005, 174:1374–1384.

    PubMed  CAS  Google Scholar 

  49. An H, Yu Y, Zhang M, et al.: Involvement of ERK, p38 and NF-kappaB signal transduction in regulation of TLR2, TLR4 and TLR9 gene expression induced by lipopolysaccharide in mouse dendritic cells. Immunology 2002, 106:38–45.

    Article  PubMed  CAS  Google Scholar 

  50. Macpherson AJ, Uhr T: Induction of protective IgA by intestinal dendritic cells carrying commensal bacteria. Science 2004, 303:1662–1665.

    Article  PubMed  CAS  Google Scholar 

  51. Niess JH, Reinecker HC: Dendritic cells: the commanders-inchief of mucosal immune defenses. Curr Opin Gastroenterol 2006, 22:354–360.

    Article  PubMed  Google Scholar 

  52. Uematsu S, Jang MH, Chevrier N, et al.: Detection of pathogenic intestinal bacteria by Toll-like receptor 5 on intestinal CD11c+ lamina propria cells. Nat Immunol 2006, 7:868–874.

    Article  PubMed  CAS  Google Scholar 

  53. Wang Q, McLoughlin RM, Cobb BA, et al.: A bacterial carbohydrate links innate and adaptive responses through Toll-like receptor 2. J Exp Med 2006, 203:2853–2863.

    Article  PubMed  CAS  Google Scholar 

  54. Moseman EA, Liang X, Dawson AJ, et al.: Human plasmacytoid dendritic cells activated by CpG oligodeoxynucleotides induce the generation of CD4+CD25+ regulatory T cells. J Immunol 2004, 173:4433–4442.

    PubMed  CAS  Google Scholar 

  55. Pasare C, Medzhitov R: Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells. Science 2003, 299:1033–1036.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to W. Allan Walker.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Rautava, S., Walker, W.A. Commensal bacteria and epithelial cross talk in the developing intestine. Curr Gastroenterol Rep 9, 385–392 (2007). https://doi.org/10.1007/s11894-007-0047-7

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11894-007-0047-7

Keywords

Navigation