Modulation of Immune System by Probiotics to Protect Against Enteric Disorders

Chapter

Abstract

Emerging diseases of the immune system are increasing with socio-economic and sanitary conditions. This is evidenced by the high incidences of allergic and autoimmune diseases in Western countries than in developing countries. Evidence is accumulating that disruption of normal microbiota and their associated beneficial effects on intestinal mucosal immunity is pivotal to occurrence of these disorders. Their pathogeneses appear to revolve around impaired ability of the intestinal microbiota to effectively modulate and thus balance the body immune responses. As a result the immune system reacts excessively to antigens that would otherwise be tolerated and thus result in allergic reactions, or reacts to self antigens to cause autoimmune diseases. Some of these disorders are characterised by persistent production of inflammatory mediators leading to chronic inflammation and tissue damage. Several reports have indicated that oral administration of excessive numbers of selected members of microbiota, so called probiotic bacteria, prevents, treats, and improves the conditions of patients with immune-mediated disorders like allergy, inflammatory bowel diseases, and type 1 diabetes. Current knowledge suggests that probiotic bacteria mediate their beneficial effects via modulation of the immune system to balance its responses and institute protection. Herein the current knowledge on the pathogenesis of some of the immune mediated diseases and the beneficial effect of probiotic bacteria to such patients are described. The chapter also explores the role of probiotic bacteria in modulating the immune system and confer protection to the host.

Keywords

Irritable Bowel Syndrome Tight Junction Celiac Disease Food Allergy Probiotic Bacterium 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Bach JF (2002) The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med 347:911–920PubMedCrossRefGoogle Scholar
  2. Backhed F, Ley RE, Sonnenburg JL, Peterson DA, Gordon JI (2005) Host-bacterial mutualism in the human intestine. Science 307:1915–1920PubMedCrossRefGoogle Scholar
  3. Ball TM, Castro-Rodriguez JA, Griffith KA, Holberg CJ, Martinez FD, Wright AL (2000) Siblings, day-care attendance, and the risk of asthma and wheezing during childhood. N Engl J Med 343:538–543PubMedCrossRefGoogle Scholar
  4. Baumgart DC, Dignass AU (2002) Intestinal barrier function. Curr Opin Clin Nutr Met Care 5:685–694CrossRefGoogle Scholar
  5. Behera AK, Kumar M, Lockey RF, Mohapatra SS (2002) Adenovirus-mediated interferon g gene therapy for allergic asthma: involvement of interleukin 12 and STAT4 signaling. Hum Gene Ther 13:1697–1709PubMedCrossRefGoogle Scholar
  6. Bixquert Jiménez M (2009) Treatment of irritable bowel syndrome with probiotics. An etiopathogenic approach at last? Rev Esp Enferm Dig 101:553–564Google Scholar
  7. Braun-Fahrlander C, Gassner M, Grize L, Neu U, Sennhauser FH, Varonier HS, Vuille JC, Wüthrich B (1999) Prevalence of hay fever and allergic sensitization in farmer’s children and their peers living in the same rural community. SCARPOL team. Swiss study on childhood allergy and respiratory symptoms with respect to air pollution. Clin Exp Allergy 29:28–34PubMedCrossRefGoogle Scholar
  8. Broide DH, Stachnick G, Castaneda D, Nayar J, Miller M, Cho J, Rodriquez M, Roman M, Raz E (2001) Immunostimulatory DNA mediates inhibition of eosinophilic inflammation and airway hyperreactivity independent of natural killer cells in vivo. J Allergy Clin Immunol 108:759–763PubMedCrossRefGoogle Scholar
  9. Buning J, Schmitz M, Repenning B, Ludwig D, Schmidt MA, Strobel S, Zimmer K-Ph (2005) Interferon γ mediates antigen trafficking to MHC class II positive late endosomes of enterocytes. E J Immunol 35:831–842CrossRefGoogle Scholar
  10. Caballero-Franco C, Keller K, De Simona C, Chadee K (2007) The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 292:G315–G322Google Scholar
  11. Caicedo RA, Li N, Des Robert C, Scumpia PO, Hubsher CP, Wasserfall CH, Schatz DA, Atkinson MA, Neu J (2008) Neonatal formula feeding leads to immunological alterations in an animal model of type 1 diabetes. Pediatr Res 63:303–307PubMedCrossRefGoogle Scholar
  12. Catassi C, Fasano A (2008) Celiac disease. Curr Opin Gastroenterol 24:687–691PubMedCrossRefGoogle Scholar
  13. Christensen HR, Frokiaer H, Pestka JJ (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168:171–178PubMedGoogle Scholar
  14. Clemente MG, De Virgiliis S, Kang JS, Macatagney R, Musu MP, Di Pierro MR, Drago S, Congia M, Fasano A (2003) Early effects of gliadin on enterocyte intracellular signalling involved in intestinal barrier function. Gut 52:218–223PubMedCrossRefGoogle Scholar
  15. Courtois P, Nsimba G, Jijakli H, Sener A, Scott FW, Malaisse WJ (2005) Gut permeability and intestinal mucins, invertase, and peroxidase in control and diabetes-prone BB rats fed either a protective or a diabetogenic diet. Dig Dis Sci 50:266–275PubMedCrossRefGoogle Scholar
  16. D’Arienzo R, Maurano F, Lavermicocca P, Ricca E, Rossi M (2009) Modulation of the immune response by probiotic strains in a mouse model of gluten sensitivity. Cytokine 48:254–259PubMedCrossRefGoogle Scholar
  17. Darfeuille-Michaud A, Boudeau J, Bulois P, Neut C, Glasser AL, Barnich N, Bringer MA, Swidsinski A, Beaugerie L, Colombel JF (2004) High prevalence of adherent-invasive Escherichia coli associated with ileal mucosa in Crohn’s disease. Gastroenterology 127:412–421PubMedCrossRefGoogle Scholar
  18. D’Eufemia P, Celli M, Finocchiaro R, Pacifico L, Viozzi L, Zaccagnini M, Cardi E, Giardini O (1996) Abnormal intestinal permeability in children with autism. Acta Paediatr 85:1076–1079PubMedCrossRefGoogle Scholar
  19. Di Pierro M, Lu R, Uzzau S, Wang W, Margaretten K, Pazzani C, Maimone F, Fasano A (2001) Zonula occludens toxin structure-function analysis. Identification of the fragment biologically active on tight junctions and of the zonulin receptor binding domain. J Biol Chem 276:19160–19165PubMedCrossRefGoogle Scholar
  20. Dogi CA, Galdeano CM, Perdigón G (2008) Gut immune stimulation by non pathogenic Gram(+) and Gram(−) bacteria. Comparison with a probiotic strain. Cytokine 41:223–231PubMedCrossRefGoogle Scholar
  21. Drakes M, Blanchard T, Czinn S (2004) Bacterial probiotic modulation of dendritic cells. Infect Immun 72:3299–3309PubMedCrossRefGoogle Scholar
  22. Duchmann R, May E, Heike M (1999) T cell specificity and cross reactivity towards Enterobacteria, Bacteroides, Bifidobacterium, and antigens from resident intestinal flora in humans. Gut 44:812–818PubMedCrossRefGoogle Scholar
  23. Ewaschuk JB, Backer JL, Churchill TA, Obermeir F, Krause DO, Madsen KL (2007) Surface expression of Toll-like receptor 9 is upregulated on intestinal epithelial cells in response to pathogenic bacterial DNA. Infect Immun 75:2572–2579PubMedCrossRefGoogle Scholar
  24. Fasano A, Shea-Donohue T (2005) Mechanisms of disease: the role of intestinal barrier function in the pathogenesis of gastrointestinal autoimmune diseases. Nat Clin Pract Gastroenterol Hepatol 2:416–422PubMedCrossRefGoogle Scholar
  25. Flinterman AE, Knol EF, van Ieperen-van Dijk AG, Timmerman HM, Knulst AC, Bruijnzeel-Koomen CA, Pasmans SG, van Hoffen E (2007) Probiotics have a different immunomodulatory potential in vitro versus ex vivo upon oral administration in children with food allergy. Int Arch Allergy Immunol 143:237–244PubMedCrossRefGoogle Scholar
  26. Freitas M, Axelsson LG, Cayuela E (2005) Indigenous microbes and their soluble factors differentially modulate intestinal glycosylation steps in vivo. Use of a “lectin assay” to survey in vivo glycosylation changes. Histochem Cell Biol 124:423–433PubMedCrossRefGoogle Scholar
  27. Furrie E (2005) Probiotics and allergy. Proc Nutr Soc 64:465–469PubMedCrossRefGoogle Scholar
  28. Gaboriau-Routhiau V, Moreau MC (1996) Gut flora allows recovery of oral tolerance to ovalbumin in mice after transient breakdown mediated by cholera toxin or Escherichia coli heat-labile enterotoxin. Pediatr Res 39:625–629PubMedCrossRefGoogle Scholar
  29. Ghadimi D, Fölster-Holst R, de Vrese M, Winkler P, Heller KJ, Schrezenmeir J (2008) Effects of probiotic bacteria and their genomic DNA on TH1/TH2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunology 213:6677–6692Google Scholar
  30. Gonzalez-Mariscal L, Betanzos A, Nava P, Jaramillo BE (2003) Tight junction proteins. Prog Biophys Mol Biol 81:1–44PubMedCrossRefGoogle Scholar
  31. Grabig A, Paclik D, Guzy C, Dankof A, Baumgart DC, Erckenbrecht J, Raupach B, Sonnenborn U, Eckert J, Schumann RR, Wiedenmann B, Dignass AU, Sturm A (2006) Escherichia coli strain Nissle 1917 ameliorates experimental colitis via toll-like receptor 2- and toll-like receptor 4-dependent pathways. Infect Immun 74:4075–4082PubMedCrossRefGoogle Scholar
  32. Graham S, Courtois P, Malaisse WJ, Rozing J, Scott FW, Mowat AM (2004) Enteropathy precedes type 1 diabetes in the BB rat. Gut 53:1437–1444PubMedCrossRefGoogle Scholar
  33. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, Pot B, Hartung T, Hols P, Mercenier A (2005) Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci U S A 102:10321–10326PubMedCrossRefGoogle Scholar
  34. He F, Morita H, Hashimoto H, Hosoda M, Kurisaki J, Ouwehand AC, Isolauri E, Benno Y, Salminen S (2002) Intestinal Bifidobacterium species induce varying cytokine production. J Allergy Clin Immunol 109:1035–1036PubMedCrossRefGoogle Scholar
  35. Hecht G (2001) Microbial pathogens that affect tight junctions in tight junctions, 2nd ed. CRC Press, Boca Raton, pp 493–516Google Scholar
  36. Hemmings WA (1978) The entry into the brain of large molecules derived from dietary protein. Proc R Soc Lond B Biol Sci 200:175–192PubMedCrossRefGoogle Scholar
  37. Hessle C, Andersson B, Wold AE (2000) Gram-positive bacteria are potent inducers of monocytic interleukin-12 (IL-12) while Gram-negative bacteria preferentially stimulate IL-10 production. Infect Immun 68:3581–3586PubMedCrossRefGoogle Scholar
  38. Heuvelin E, Lebreton C, Grangette C, Pot B, Cerf-Bensussan H, Heyman M (2009) Mechanisms involved in alleviation of intestinal inflammation by Bifidobacterium breve soluble factors. PLoS One 4:e5184CrossRefGoogle Scholar
  39. Hisamatsu T, Suzuki M, Reinecker HC, Nadeau WJ, McCormick BA, Podolsky DK (2003) CARD15/NOD2 functions as an anti-bacterial factor in human intestinal epithelial cells. Gastroenterology 124:993–1000PubMedCrossRefGoogle Scholar
  40. Hoffmann M, Rath E, Hölzlwimmer G, Quintanilla-Martinez L, Loach D, Tannock G, Haller D (2008) Lactobacillus reuteri 100-23 transiently activates intestinal epithelial cells of mice that have a complex microbiota during early stages of colonization. J Nutr 138:1684–1691Google Scholar
  41. Hollander D (2002) Crohn’s disease, TNF-alpha, and the leaky gut. The chicken or the egg? Am J Gastroenterol 97:1867–1868PubMedGoogle Scholar
  42. Hugot JP, Chamaillard M, Zouali H, Lesage S, Cézard JP, Belaiche J, Almer S, Tysk C, O’Morain CA, Gassull M, Binder V, Finkel Y, Cortot A, Modigliani R, Laurent-Puig P, Gower-Rousseau C, Macry J, Colombel JF, Sahbatou M, Thomas G (2001) Association of NOD2 leucine-rich repeat variants with susceptibility to Crohn’s disease. Nature 411:599–603CrossRefGoogle Scholar
  43. Hussain I, Jain VV, Kitagaki K, Businga TR, O’Shaughnessy P, Kline JN (2002) Modulation of murine allergic rhinosinusitis by CpG oligodeoxynucleotides. Laryngoscope 112:1819–1826PubMedCrossRefGoogle Scholar
  44. Isolauri E, Salminen S (2008) Probiotics: use in allergic disorders. J Clin Gastroenterol 42:S91–S96PubMedCrossRefGoogle Scholar
  45. Jabri B, Sollid LM (2006) Mechanisms of disease: immunopathogenesis of celiac disease. Nat Clin Pract Gastroenterol Hepatol 3:516–525PubMedCrossRefGoogle Scholar
  46. Jiang WG, Bryce RP, Horrobin DF, Mansel RE (1998) Regulation of tight junction permeability and occludin expression by polyunsaturated fatty acids. Biochem Biophys Res Commun 244:414–420PubMedCrossRefGoogle Scholar
  47. Jijon H, Backer J, Diaz H, Yeung H, Thiel D, McKaigney C, De Simone C, Madsen K (2004) DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology 126:1358–1373PubMedCrossRefGoogle Scholar
  48. Kalimo K, Lammintausta K, Klemi P (1988) Mast cells and IgE in intestinal mucosa in adult atopic dermatitis patients. Br J Dermatol 86:101–104Google Scholar
  49. Kalliomaki M, Kirjavainen P, Eerola E, Kero P, Salminen S, Isolauri E (2001) Distinct patterns of neonatal gut microflora in infants in whom atopy was and was not developing. J Allergy Clin Immunol 107:129–134PubMedCrossRefGoogle Scholar
  50. Kitagaki K, Jain VV, Businga TR, Hussain I, Kline JN (2002) Immunomodulatory effects of CpG oligodeoxynucleotides on established Th2 responses. Clin Diagn Lab Immunol 9:1260–1269PubMedGoogle Scholar
  51. Kline JN, Krieg AM, Waldschmidt TJ, Ballas ZK, Jain V, Busing TR (1999) CpG oligodeoxynucleotides do not require TH1 cytokines to prevent eosinophilic airway inflammation in a murine model of asthma. J Allergy Clin Immunol 104:1258–1264PubMedCrossRefGoogle Scholar
  52. Lefebvre DE, Powell KL, Strom A, Scott FW (2006) Dietary proteins as environmental modifiers of type 1 diabetes mellitus. Ann Rev Nutr 26:175–202CrossRefGoogle Scholar
  53. Lin YP, Thibodeaux CH, Peña JA, Ferry GD, Versalovic J (2008) Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm Bowel Dis 14:1068–1083PubMedCrossRefGoogle Scholar
  54. Lutgendorff F, Akkermans LM, Söderholm JD (2008) The role of microbiota and probiotics in stress-induced gastro-intestinal damage. Curr Mol Med 8:282–298PubMedCrossRefGoogle Scholar
  55. Lynch NR, Hagel I, Perez M, Di Prisco MC, Lopez R, Alvarez N (1993) Effect of anthelmintic treatment on the allergic reactivity of children in a tropical slum. J Allergy Clin Immunol 92:404–411PubMedCrossRefGoogle Scholar
  56. Maassen CB, van Holten-Neelen C, Balk F, den Bak-Glashouwer MJ, Leer RJ, Laman JD, Boersma WJ, Claassen E (2000) Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18:2615–2623CrossRefGoogle Scholar
  57. Macintire DK, Bellhorn TL (2002) Bacterial translocation: clinical implications and prevention. Vet Clin North Am Small Anim Pract 32:1165–1178PubMedCrossRefGoogle Scholar
  58. Maeda S, Hsu LC, Liu H, Bankston LA, Iimura M, Kagnoff MF, Eckmann L, Karin M (2005) Nod2 mutation in Crohn’s disease potentiates NF-kappaB activity and IL-1beta processing. Science 307:734–738PubMedCrossRefGoogle Scholar
  59. Malago JJ, Koninkx JFJG, van Dijk JE (2002) The heat shock response and cytoprotection of the intestinal epithelium. Cell Stress Chaperones 7:191–199PubMedCrossRefGoogle Scholar
  60. Malago JJ, Koninkx JFJG, Douma PM, Dirkzwager A, Veldman A, Hendriks HGCJM, van Dijk JE (2003) Differential modulation of enterocyte-like Caco-2 cells after exposure to short chain fatty acids. Food Addit Contam 20:427–437PubMedCrossRefGoogle Scholar
  61. Malago JJ, Tooten PCJ, Koninkx JFJG (2010) Anti-inflammatory properties of probiotic bacteria on Salmonella-induced IL-8 synthesis in enterocyte-like Caco-2 cells. Benef Microbe 1(2):121–130CrossRefGoogle Scholar
  62. Matricardi PM, Rosmini F, Ferrigno L, Pannetta V, Bonini S (1997) Cross sectional retrospective study of prevalence of atopy among Italian military students with antibodies against hepatitis A virus. Br Med J 314:999–1003CrossRefGoogle Scholar
  63. Mennigen R, Bruewer M (2009) Effect of probiotics on intestinal barrier function. Ann N Y Acad Sci 1165:183–189PubMedCrossRefGoogle Scholar
  64. Michelsen KS, Arditi M (2007) Toll-like receptors and innate immunity in gut homeostasis and pathology. Curr Opin Hematol 14:48–54PubMedCrossRefGoogle Scholar
  65. Miettinen M, Veckman V, Latvala S, Sareneva T, Matikainen S, Julkunen I (2008) Live Lactobacillus rhamnosus and Streptococcus pyogenes differentially regulate Toll-like receptor (TLR) gene expression in human primary macrophages. J Leukoc Biol 84:1092–1100PubMedCrossRefGoogle Scholar
  66. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, Bavari S, Klaenhammer TR (2005) Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A 102:2880–2885PubMedCrossRefGoogle Scholar
  67. Molberg O, McAdam SN, Korner R, Quarsten H, Kristiansen C, Madsen L, Fugger L, Scott H, Norén O, Roepstorff P, Lundin KE, Sjöström H, Sollid LM (1998) Tissue transglutaminase selectively modifies gliadin peptides that are recognized by gut-derived T cells in celiac disease. Nat Med 4:713–717PubMedCrossRefGoogle Scholar
  68. Mordes JP, Bortell R, Blankenhorn EP, Rossini AA, Greiner DL (2004) Rat models of type 1 diabetes: genetics, environment, and autoimmunity. ILAR J 45:278–291PubMedCrossRefGoogle Scholar
  69. Mowat AM, Parker LA, Beacock-Sharp H, Millington OR, Chirdo F (2004) Oral tolerance: overview and historical perspectives. Ann N Y Acad Sci 1029:1–8PubMedCrossRefGoogle Scholar
  70. Munakata K, Yamamoto M, Anjiki N (2008) Importance of the interferon-alpha system in murine large intestine indicated by microarray analysis of commensal bacteria-induced immunological changes. BMC Genomics 9:192PubMedCrossRefGoogle Scholar
  71. Nemeth E, Fajdiga S, Malago JJ, Koninkx JFJG, Tooten PCJ, van Dijk JE (2006) Inhibition of Salmonella-induced IL-8 synthesis and expression of Hsp70 in enterocyte-like Caco-2 cells after exposure to non-starter lactobacilli. Int J Food Microbiol 112:266–274PubMedCrossRefGoogle Scholar
  72. Netea MG, Kullberg BJ, de Jong DJ, Franke B, Sprong T, Naber TH, Drenth JP, Van der Meer JW (2004) NOD2 mediates anti-inflammatory signals induced by TLR2 ligands: implications for Crohn’s disease. Eur J Immunol 34:2052–2059PubMedCrossRefGoogle Scholar
  73. Nobaek S, Johansson ML, Molin G, Ahrne S, Jeppsson B (2000) Alteration of intestinal microflora is associated with reduction in abdominal bloating and pain in patients with irritable bowel syndrome. Am J Gastroenterol 95:1231–1238PubMedCrossRefGoogle Scholar
  74. Noverr MC, Huffnagle GB (2004) Does the microbiota regulate immune responses outside the gut? Trends Microbiol 12:562–568Google Scholar
  75. Nusrat A, von Eichel-Streiber C, Turner JR, Verkade P, Madara JL, Parkos CA (2001) Clostridium difficile toxins disrupt epithelial barrier function by altering membrane microdomain localization of tight junction proteins. Infect Immun 69:1329–1336PubMedCrossRefGoogle Scholar
  76. O’Byrne PM (2006) Cytokines or their antagonists for the treatment of asthma. Chest 130:244–250PubMedCrossRefGoogle Scholar
  77. Ogata H, Hibi T (2003) Cytokine and anti-cytokine therapies for inflammatory bowel disease. Curr Pharm Des 9:1107–1113PubMedCrossRefGoogle Scholar
  78. Ogura Y, Bonen DK, Inohara N, Nicolae DL, Chen FF, Ramos R, Britton H, Moran T, Karaliuskas R, Duerr RH, Achkar JP, Brant SR, Bayless TM, Kirschner BS, Hanauer SB, Nuñez G, Cho JH (2001) A frameshift mutation in NOD2 associated with susceptibility to Crohn’s disease. Nature 411:603–606CrossRefGoogle Scholar
  79. Ouwehand AC, Isolauri E, He F, Hashimoto H, Benno Y, Salminen S (2001) Differences in Bifidobacterium flora composition in allergic and healthy infants. J Allergy Clin Immunol 108:144–145PubMedCrossRefGoogle Scholar
  80. Ouwehand AC, Bergsma N, Parhiala R, Lahtinen S, Gueimonde M, Finne-Soveri H, Strandberg T, Ptikälä K, Salminen S (2008) Bifidobacterium microbiota and parameters of immune function in elderly subjects. FEMS Immunol Med Microbiol 53:18–25PubMedCrossRefGoogle Scholar
  81. Pessi T, Sütas Y, Marttinen A, Isolauri E (1998) Probiotics reinforce mucosal degradation of antigens in rats: implications for therapeutic use of probiotics. J Nutr 128:2313–2318PubMedGoogle Scholar
  82. Petrof EO, Kojima K, Ropeleski MJ, Musch MW, Tao Y, De Simone C, Chang EB (2004) Probiotics inhibit nuclear factor-kappaB and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 127:1474–1487PubMedCrossRefGoogle Scholar
  83. Pochard P, Gosset P, Grangette C, Andre C, Tonnel AB, Pestel J, Mercenier A (2002) Lactic acid bacteria inhibit TH2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 110:617–623PubMedCrossRefGoogle Scholar
  84. Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, Savilahti E (2004) Lactobacillus GG effect in increasing IFN-g production in infants with cow’s milk allergy J Allergy Clin Immunol 114:131–136Google Scholar
  85. Qin HL, Shen TY, Gao ZG, Fan XB, Hang XM, Jiang YQ, Zhang HZ (2005) Effect of lactobacillus on the gut microflora and barrier function of the rats with abdominal infection. World J Gastroenterol 11:2591–2596PubMedGoogle Scholar
  86. Rautava S, Kalliomäki M, Isolauri E (2005) New therapeutic strategy for combating the increasing burden of allergic disease: probiotics. J Allergy Clin Immunol 116:31–37PubMedCrossRefGoogle Scholar
  87. Riedler J, Braun-Fahrlander C, Eder W, Schreuer M, Waser M, Maisch S, Carr D, Schierl R, Nowak D, von Mutius E (2001) Exposure to farming in early life and development of asthma and allergy: a crosssectional survey. Lancet 358:1129–1133PubMedCrossRefGoogle Scholar
  88. Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, Pærregaard A (2003) Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 11:389–395CrossRefGoogle Scholar
  89. Salvatore S, Hauser B, Vandenplas Y (2007) Chronic enteropathy and feeding. Nestle Nutr Workshop Ser Pediatr Program 59:115–126PubMedGoogle Scholar
  90. Sartor RB (2007) Bacteria in Crohn’s disease: mechanisms of inflammation and therapeutic implications. J Clin Gastroenterol 41:S37–S43CrossRefGoogle Scholar
  91. Schiffrin EJ, Brassart D, Servin AL, Rochat F, Donnet-Hughes A (1997) Immune modulation of blood leukocytes in humans by lactic acid bacteria: criteria for strain selection. Am J Clin Nutr 66:515S–20SPubMedGoogle Scholar
  92. Shaheen SO, Aaby P, Hall AJ, Barker DJ, Heyes CB, Shiell AW, Goudiaby A (1996) Measles and atopy in Guinea-Bissau. Lancet 347:1792–1796Google Scholar
  93. Simonovic I, Rosenberg J, Koutsouris A, Hecht G (2000) Enteropathogenic Escherichia coli dephosphorylates and dissociates occludin from intestinal epithelial tight junctions. Cell Microbiol 2:305–315PubMedCrossRefGoogle Scholar
  94. Söderholm JD, Peterson KH, Olaison G, Franzén LE, Westrom B, Magnusson KE, Sjödahl R (1999) Epithelial permeability to proteins in the noninflamed ileum of Crohn’s disease? Gastroenterology 117:65–72PubMedCrossRefGoogle Scholar
  95. Sporik R, Holgate ST, Platts-Mills TA, Cogswell JJ (1990) Exposure to house-dust mite allergen (Der p I) and the development of asthma in childhood. A prospective study. N Engl J Med 323:502–507PubMedCrossRefGoogle Scholar
  96. Strachan DP (1989) Hay fever, hygiene, and household size. Br Med J 299:1259–1260CrossRefGoogle Scholar
  97. Tafazoli F, Zeng CQ, Estes MK, Magnusson KE, Svensson L (2001) NSP4 enterotoxin of rotavirus induces paracellular leakage in polarized epithelial cells. J Virol 75:1540–1546PubMedCrossRefGoogle Scholar
  98. Talley NJ (2008) Functional gastrointestinal disorders as a public health problem. Neurogastroenterol Motil 20(Suppl 1):121–129PubMedCrossRefGoogle Scholar
  99. Tlaskalová-Hogenová H, Stepánková R, Hudcovic T, Tucková L, Cukrowska B, Lodinová-Zádníková R, Kozáková H, Rossmann P, Bártová J, Sokol D, Funda DP, Borovská D, Reháková Z, Sinkora J, Hofman J, Drastich P, Kokesová A (2004) Commensal bacteria (normalmicroflora), mucosal immunity, and chronic inflammatory and autoimmune diseases. Immunol Lett 93:97–108PubMedCrossRefGoogle Scholar
  100. Trevisi P, De Filippi S, Minieri L, Mazzoni M, Modesto M, Biavati B, Bosi P (2008) Effect of fructo-oligosaccharides and different doses of Bifidobacterium animalis in a weaning diet on bacterial translocation and Toll-like receptor gene expression in pigs. Nutrition 24:1023–1029PubMedCrossRefGoogle Scholar
  101. Vaarala O, Atkinson MA, Neu J (2008) The “perfect storm” for type 1 diabetes: the complex interplay between intestinal microbiota, gut permeability, and mucosal immunity. Diabetes 57:2555–2562PubMedCrossRefGoogle Scholar
  102. Vaishnava S, Behrendt CL, Ismail AS, Eckmann L, Hooper LV (2008) Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci U S A 105:20858–20863PubMedCrossRefGoogle Scholar
  103. van de Wal Y, Kooy Y, van Veelen P, Peña S, Mearin L, Papadopoulos G, Koning F (1998) Selective deamidation by tissue transglutaminase strongly enhances gliadin-specific T cell reactivity. J Immunol 161:1585–1588Google Scholar
  104. van der Velden VH, Laan MP, Baert MR, de Waal Malefyt R, Neijens HJ, Savelkoul HF (2001) Selective development of a strong Th2 cytokine profile in high-risk children who develop atopy: risk factors and regulatory role of IFN-g, IL-4, IL-10. Clin Exp Allergy 31:997–1006CrossRefGoogle Scholar
  105. Vizoso Pinto MG, Rodriguez Gómez M, Seifert S, Watzl B, Holzapfel WH, Franz CM (2009) Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 133:86–93PubMedCrossRefGoogle Scholar
  106. Voltan S, Castagliuolo I, Elli M, Longo S, Brun P, D’Incà R, Porzionato A, Macchi V, Palù G, Sturniolo GC, Morelli L, Martines D (2007) Aggregating phenotype in Lactobacillus crispatus determines intestinal colonization and TLR2 and TLR4 modulation in murine colonic mucosa. Clin Vaccine Immunol 14:1138–1148PubMedCrossRefGoogle Scholar
  107. von Mutius E, Braun-Fahrlander C, Schierl R, Riedler J, Ehlermann S, Maisch S, Waser M, Nowak D (2000) Exposure to endotoxin or other bacterial components might protect against the development of atopy. Clin Exp Allergy 30:1230–1234CrossRefGoogle Scholar
  108. Wang WL, Lu RL, DiPierro M, Fasano A (2000) Zonula occluding toxin, a microtubule binding protein. World J Gastroenterol 6:330–334PubMedGoogle Scholar
  109. Watanabe S, Narisawa Y, Arase S, Okamatsu H, Ikenaga T, Tajiri Y, Kumemura M (2003) Differences in faecal microflora between patients with atopic dermatitis and healthy control subjects. J Allergy Clin Immunol 111:587–591PubMedCrossRefGoogle Scholar
  110. Watts T, Berti I, Sapone A, Gerarduzzi T, Not T, Zielke R, Fasano A (2005) Role of the intestinal tight junction modulator zonulin in the pathogenesis of type I diabetes in BB diabetic-prone rats. Proc Natl Acad Sci U S A 102:2916–2921PubMedCrossRefGoogle Scholar
  111. Wehkamp J, Salzman NH, Porter E, Nuding S, Weichenthal M, Petras RE, Shen B, Schaefferler E, Schwab M, Linzmeier R, Feathers RW, Chu H, Lima H Jr, Fellermann K, Ganz T, Stange EF, Bevins CL (2005) Reduced Paneth cell alpha-defensins in ileal Crohn’s disease. Proc Natl Acad Sci U S A 102:18129–18134PubMedCrossRefGoogle Scholar
  112. Werner T, Haller D (2007) Intestinal epithelial cell signalling and chronic inflammation: from the proteome to specific molecular mechanisms. Mutat Res 622:42–57PubMedCrossRefGoogle Scholar
  113. Westerholm-Ormio M, Vaarala O, Pihkala P, Ilonen J, Savilahti E (2003) Immunologic activity in the small intestinal mucosa of pediatric patients with type 1 diabetes. Diabetes 52:2287–2295PubMedCrossRefGoogle Scholar
  114. Wills-Karp M, Santeliz J, Karp CL (2001) The germless theory of allergic disease: revisiting the hygiene hypothesis. Nat Rev Immunol 1:69–75PubMedCrossRefGoogle Scholar
  115. Winkler P, Ghadimi D, Schrezenmeir J, Kraehenbuhl JP (2007) Molecular and cellular basis of microflora-host interactions. J Nutr 137:756S–772SPubMedGoogle Scholar
  116. Xystrakis E, Boswell SE, Hawrylowicz CM (2006) T regulatory cells and the control of allergic disease. Expert Opin Biol Ther 6:121–133PubMedCrossRefGoogle Scholar
  117. Yasui H, Shida K, Matsuzaki T, Yokokura T (1999) Immunomodulatory function of lactic acid bacteria. Antonie Van Leeuwenhoek 76:383–389PubMedCrossRefGoogle Scholar

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© Springer Science+Business Media B.V. 2011

Authors and Affiliations

  1. 1.Department of Veterinary Pathology, Faculty of Veterinary MedicineSokoine University of AgricultureMorogoroTanzania

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