Skip to main content

Advertisement

SpringerLink
Log in
Menu
Find a journal Publish with us Track your research
Search
Cart
  1. Home
  2. Journal of Gastroenterology
  3. Article

Probiotics and immunity

  • Review
  • Published: 22 January 2009
  • Volume 44, pages 26–46, (2009)
  • Cite this article
Download PDF
Journal of Gastroenterology Aims and scope Submit manuscript
Probiotics and immunity
Download PDF
  • Andrea T. Borchers1,
  • Carlo Selmi2,3,
  • Frederick J. Meyers4,
  • Carl L. Keen1 &
  • …
  • M. Eric Gershwin2 

  • 8623 Accesses

  • 340 Citations

  • 21 Altmetric

  • 2 Mentions

  • Explore all metrics

Abstract

Probiotics are defined as live microorganisms that, when administered in adequate amounts, confer a health benefit on the host, including the gastrointestinal tract. While this beneficial effect was originally thought to stem from improvements in the intestinal microbial balance, there is now substantial evidence that probiotics can also provide benefits by modulating immune functions. In animal models, probiotic supplementation is able to provide protection from spontaneous and chemically induced colitis by downregulating inflammatory cytokines or inducing regulatory mechanisms in a strain-specific manner. In animal models of allergen sensitization and murine models of asthma and allergic rhinitis, orally administered probiotics can strain-dependently decrease allergen-specific IgE production, in part by modulating systemic cytokine production. Certain probiotics have been shown to decrease airway hyperresponsiveness and inflammation by inducing regulatory mechanisms. Promising results have been obtained with probiotics in the treatment of human inflammatory diseases of the intestine and in the prevention and treatment of atopic eczema in neonates and infants. However, the findings are too variable to allow firm conclusions as to the effectiveness of specific probiotics in these conditions.

Article PDF

Download to read the full article text

Similar content being viewed by others

Role of Probiotics in Allergic Diseases

Chapter © 2022

Probiotics for Allergic Airway Infection and Inflammations

Chapter © 2021

Can probiotics be used in the prevention and treatment of bronchial asthma?

Article Open access 01 July 2024
Use our pre-submission checklist

Avoid common mistakes on your manuscript.

References

  1. Hahn BH, Grossman J, Chen W, McMahon M. The pathogenesis of atherosclerosis in autoimmune rheumatic diseases: roles of inflammation and dyslipidemia. J Autoimmun 2007;28:69–75.

    Article  PubMed  CAS  Google Scholar 

  2. Blank M, Gershwin ME. Autoimmunity: from the mosaic to the kaleidoscope. J Autoimmun 2008;30:1–4.

    Article  PubMed  Google Scholar 

  3. Escarcega RO, Garcia-Carrasco M, Fuentes-Alexandro S, Jara LJ, Rojas-Rodriguez J, Escobar-Linares LE, et al. Insulin resistance, chronic inflammatory state and the link with systemic lupus erythematosus-related coronary disease. Autoimmun Rev 2006;6:48–53.

    Article  PubMed  CAS  Google Scholar 

  4. Belizna CC, Richard V, Thuillez C, Levesque H, Shoenfeld Y. Insights into atherosclerosis therapy in antiphospholipid syndrome. Autoimmun Rev 2007;7:46–51.

    Article  PubMed  CAS  Google Scholar 

  5. Food and Agriculture Organization of the United Nations, World Health Organization. Guidelines for evaluation of probiotics in food. London, Ontario: Canada; 2002. ftp://ftp.fao.org/es/esn/food/wgreport2.pdf, accessed 18 April 2008.

  6. Mowat AM. Anatomical basis of tolerance and immunity to intestinal antigens. Nat Rev Immunol 2003;3:331–341.

    Article  PubMed  CAS  Google Scholar 

  7. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, Bonasio R, 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 

  8. Niess JH, Brand S, Gu X, Landsman L, Jung S, McCormick BA, et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005;307:254–258.

    Article  PubMed  CAS  Google Scholar 

  9. Chieppa M, Rescigno M, Huang AY, Germain RN. Dynamic imaging of dendritic cell extension into the small bowel lumen in response to epithelial cell TLR engagement. J Exp Med 2006;203:2841–2852.

    Article  PubMed  CAS  Google Scholar 

  10. Steffen EK, Berg RD. Relationship between cecal population levels of indigenous bacteria and translocation to the mesenteric lymph nodes. Infect Immun 1983;39:1252–1259.

    PubMed  CAS  Google Scholar 

  11. Ibnou-Zekri N, Blum S, Schiffrin EJ, von der Weid T. Divergent patterns of colonization and immune response elicited from two intestinal Lactobacillus strains that display similar properties in vitro. Infect Immun 2003;71:428–436.

    Article  PubMed  CAS  Google Scholar 

  12. 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 

  13. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, Liu YJ, et al. Immunobiology of dendritic cells. Annu Rev Immunol 2000;18:767–811.

    Article  PubMed  CAS  Google Scholar 

  14. Bilsborough J, Viney JL. Gastrointestinal dendritic cells play a role in immunity, tolerance, and disease. Gastroenterology 2004;127:300–309.

    Article  PubMed  CAS  Google Scholar 

  15. Steinman RM, Hawiger D, Nussenzweig MC. Tolerogenic dendritic cells. Annu Rev Immunol 2003;21:685–711.

    Article  PubMed  CAS  Google Scholar 

  16. Peng Y, Martin DA, Kenkel J, Zhang K, Ogden CA, Elkon KB. Innate and adaptive immune response to apoptotic cells. J Autoimmun 2007;29:303–309.

    Article  PubMed  CAS  Google Scholar 

  17. Lan RY, Mackay IR, Gershwin ME. Regulatory T cells in the prevention of mucosal inflammatory diseases: patrolling the border. J Autoimmun 2007;29:272–280.

    Article  PubMed  CAS  Google Scholar 

  18. Bamias G, Okazawa A, Rivera-Nieves J, Arseneau KO, De La Rue SA, Pizarro TT, et al. Commensal bacteria exacerbate intestinal inflammation but are not essential for the development of murine ileitis. J Immunol 2007;178:1809–1818.

    PubMed  CAS  Google Scholar 

  19. Liu Z, Jiu J, Liu S, Fa X, Li F, Du Y. Blockage of tumor necrosis factor prevents intestinal mucosal inflammation through downregulation of interleukin-23 secretion. J Autoimmun 2007;29:187–194.

    Article  PubMed  CAS  Google Scholar 

  20. Nakagome Y, Ueno Y, Kogure T, Fukushima K, Moritoki Y, Ridgway WM, et al. Autoimmune cholangitis in NOD.c3c4 mice is associated with cholangiocyte-specific Fas antigen deficiency. J Autoimmun 2007;29:20–29.

    Article  PubMed  CAS  Google Scholar 

  21. Glaysher BR, Mabbott NA. Role of the GALT in scrapie agent neuroinvasion from the intestine. J Immunol 2007;178:3757–3766.

    PubMed  CAS  Google Scholar 

  22. Song F, Wardrop RM, Gienapp IE, Stuckman SS, Meyer AL, Shawler T, et al. The Peyer’s patch is a critical immunoregulatory site for mucosal tolerance in experimental autoimmune encephalomylelitis (EAE). J Autoimmun 2008;30:230–237.

    Article  PubMed  CAS  Google Scholar 

  23. Kristof K, Erdei A, Bajtay Z. Set a thief to catch a thief: self-reactive innate lymphocytes and self tolerance. Autoimmun Rev 2008;7:278–283.

    Article  PubMed  CAS  Google Scholar 

  24. Wan EC, Gordon TP, Jackson MW. Autoantibodies to calcium channels in type 1 diabetes mediate autonomic dysfunction by different mechanisms in colon and bladder and are neutralized by antiidiotypic antibodies. J Autoimmun 2008;31:66–72.

    Article  PubMed  CAS  Google Scholar 

  25. Briani C, Samaroo D, Alaedini A. Celiac disease: from gluten to autoimmunity. Autoimmun Rev 2008.

  26. O’Mahony L, O’Callaghan L, McCarthy J, Shilling D, Scully P, Sibartie S, et al. Differential cytokine response from dendritic cells to commensal and pathogenic bacteria in different lymphoid compartments in humans. Am J Physiol Gastrointest Liver Physiol 2006;290:G839–G845.

    Article  PubMed  CAS  Google Scholar 

  27. Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, Gionchetti P, et al. Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 2004;53:1602–1609.

    Article  PubMed  CAS  Google Scholar 

  28. Fink LN, Zeuthen LH, Ferlazzo G, Frøkiær H. Human antigen-presenting cells respond differently to gut-derived probiotic bacteria but mediate similar strain-dependent NK and T cell activation. FEMS Immunol Med Microbiol 2007;51:535–546.

    Article  PubMed  CAS  Google Scholar 

  29. Young SL, Simon MA, Baird MA, Tannock GW, Bibiloni R, Spencely K, et al. Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clin Diagn Lab Immunol 2004;11:686–690.

    Article  PubMed  Google Scholar 

  30. Zeuthen LH, Christensen HR, Frøkiær H. Lactic acid bacteria inducing a weak interleukin-12 and tumor necrosis factor alpha response in human dendritic cells inhibit strongly stimulating lactic acid bacteria but act synergistically with Gram-negative bacteria. Clin Vaccine Immunol 2006;13:365–375.

    Article  PubMed  CAS  Google Scholar 

  31. Fink LN, Zeuthen LH, Christensen HR, Morandi B, Frøkiær H, Ferlazzo G. Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. Int Immunol 2007;19:1319–1327.

    Article  PubMed  CAS  Google Scholar 

  32. Gackowska L, Michalkiewicz J, Krotkiewski M, Helmin-Basa A, Kubiszewska I, Dzierzanowska D. Combined effect of different lactic acid bacteria strains on the mode of cytokines pattern expression in human peripheral blood mononuclear cells. J Physiol Pharmacol 2006;57Suppl 9:13–21.

    PubMed  Google Scholar 

  33. Kekkonen RA, Kajasto E, Miettinen M, Veckman V, Korpela R, Julkunen I. Probiotic Leuconostoc mesenteroides ssp. cremoris and Streptococcus thermophilus induce IL-12 and IFN-g production. World J Gastroenterol 2008;14:1192–1203.

    Article  PubMed  CAS  Google Scholar 

  34. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, Warfield KL, et al. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci USA 2005;102:2880–2885.

    Article  PubMed  CAS  Google Scholar 

  35. Braat H, de Jong EC, van den Brande JM, Kapsenberg ML, Peppelenbosch MP, van Tol EA, et al. Dichotomy between Lactobacillus rhamnosus and Klebsiella pneumoniae on dendritic cell phenotype and function. J Mol Med 2004;82:197–205.

    Article  PubMed  CAS  Google Scholar 

  36. Drakes M, Blanchard T, Czinn S. Bacterial probiotic modulation of dendritic cells. Infect Immun 2004;72:3299–3309.

    Article  PubMed  CAS  Google Scholar 

  37. Niers LE, Hoekstra MO, Timmerman HM, van Uden NO, de Graaf PM, Smits HH, et al. Selection of probiotic bacteria for prevention of allergic diseases: immunomodulation of neonatal dendritic cells. Clin Exp Immunol 2007;149:344–352.

    PubMed  CAS  Google Scholar 

  38. Braat H, van den Brande J, van Tol E, Hommes D, Peppelenbosch M, van Deventer S. Lactobacillus rhamnosus induces peripheral hyporesponsiveness in stimulated CD4+ T cells via modulation of dendritic cell function. Am J Clin Nutr 2004;80:1618–1625.

    PubMed  CAS  Google Scholar 

  39. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, van Capel TM, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol 2005;115:1260–1267.

    Article  PubMed  CAS  Google Scholar 

  40. von der Weid T, Bulliard C, J. SE. Induction by a lactic acid bacterium of a population of CD4+ T cells with low proliferative capacity that produce transforming growth factor b and interleukin-10. Clin Diagn Lab Immunol 2001;8:695–701.

    Article  PubMed  Google Scholar 

  41. Rimoldi M, Chieppa M, Larghi P, Vulcano M, Allavena P, Rescigno M. Monocyte-derived dendritic cells activated by bacteria or by bacteria-stimulated epithelial cells are functionally different. Blood 2005;106:2818–2826.

    Article  PubMed  CAS  Google Scholar 

  42. Zeuthen LH, Fink LN, Frøkiær H. Epithelial cells prime the immune response to an array of gut-derived commensals towards a tolerogenic phenotype through distinct actions of thymic stromal lymphopoietin and transforming growth factor-β. Immunology 2008;123:197–208.

    PubMed  CAS  Google Scholar 

  43. Roselli M, Finamore A, Britti MS, Mengheri E. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammationassociated response induced by enterotoxigenic Escherichia coli K88. Br J Nutr 2006;95:1177–1184.

    Article  PubMed  CAS  Google Scholar 

  44. Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, et al. Adhesion of lactic acid bacteria to Caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 2002;46:293–297.

    PubMed  CAS  Google Scholar 

  45. Otte JM, Podolsky DK. Functional modulation of enterocytes by Gram-positive and Gram-negative microorganisms. Am J Physiol Gastrointest Liver Physiol 2004;286:G613–G626.

    Article  PubMed  CAS  Google Scholar 

  46. O’Hara AM, O’Regan P, Fanning A, O’Mahony C, Macsharry J, Lyons A, et al. Functional modulation of human intestinal epithelial cell responses by Bifidobacterium infantis and Lactobacillus salivarius. Immunology 2006;118:202–215.

    Article  PubMed  CAS  Google Scholar 

  47. Zhang L, Li N, Caicedo R, Neu J. Alive and dead Lactobacillus rhamnosus GG decrease tumor necrosis factor-alpha-induced interleukin-8 production in Caco-2 cells. J Nutr 2005;135:1752–1756.

    PubMed  CAS  Google Scholar 

  48. Jijon H, Backer J, Diaz H, Yeung H, Thiel D, McKaigney C, et al. DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology 2004;126:1358–1373.

    Article  PubMed  CAS  Google Scholar 

  49. Haller D, Bode C, Hammes WP, Pfeifer AM, Schiffrin EJ, Blum S. Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 2000;47:79–87.

    Article  PubMed  CAS  Google Scholar 

  50. Rimoldi M, Chieppa M, Salucci V, Avogadri F, Sonzogni A, Sampietro GM, et al. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat Immunol 2005;6:507–514.

    Article  PubMed  CAS  Google Scholar 

  51. Li HS, Ligons DL, Rose NR. Genetic complexity of autoimmune myocarditis. Autoimmun Rev 2008;7:168–173.

    Article  PubMed  CAS  Google Scholar 

  52. Baschal EE, Eisenbarth GS. Extreme genetic risk for type 1A diabetes in the post-genome era. J Autoimmun 2008;31:1–6.

    Article  PubMed  CAS  Google Scholar 

  53. Gleicher N, Barad DH. Gender as risk factor for autoimmune diseases. J Autoimmun 2007;28:1–6.

    Article  PubMed  CAS  Google Scholar 

  54. Jordan MA, Baxter AG. The genetics of immunoregulatory T cells. J Autoimmun 2008.

  55. Rieger R, Gershwin ME. The X and why of xenobiotics in primary biliary cirrhosis. J Autoimmun 2007;28:76–84.

    Article  PubMed  CAS  Google Scholar 

  56. Smith P, Mangan NE, Walsh CM, Fallon RE, McKenzie AN, van Rooijen N, et al. Infection with a helminth parasite prevents experimental colitis via a macrophage-mediated mechanism. J Immunol 2007;178:4557–4566.

    PubMed  CAS  Google Scholar 

  57. Frazer IH. Autoimmunity and persistent viral infection: two sides of the same coin? J Autoimmun 2008.

  58. Praprotnik S, Sodin-Semrl S, Tomsic M, Shoenfeld Y. The curiously suspicious: infectious disease may ameliorate an ongoing autoimmune destruction in systemic lupus erythematosus patients. J Autoimmun 2008;30:37–41.

    Article  PubMed  CAS  Google Scholar 

  59. Stojanovich L, Marisavljevich D. Stress as a trigger of autoimmune disease. Autoimmun Rev 2008;7:209–213.

    Article  PubMed  Google Scholar 

  60. Tozzoli R, Barzilai O, Ram M, Villalta D, Bizzaro N, Sherer Y, et al. Infections and autoimmune thyroid diseases: parallel detection of antibodies against pathogens with proteomic technology. Autoimmun Rev 2008 Aug 9 [Epub ahead of print].

  61. Sheasley-O’Neill SL, Brinkman CC, Ferguson AR, Dispenza MC, Engelhard VH. Dendritic cell immunization route determines integrin expression and lymphoid and nonlymphoid tissue distribution of CD8 T cells. J Immunol 2007;178:1512–1522.

    PubMed  CAS  Google Scholar 

  62. Abbas AK, Lohr J, Knoechel B. Balancing autoaggressive and protective T cell responses. J Autoimmun 2007;28:59–61.

    Article  PubMed  CAS  Google Scholar 

  63. Atzeni F, Doria A, Carrabba M, Turiel M, Sarzi-Puttini P. Potential target of infliximab in autoimmune and inflammatory diseases. Autoimmun Rev 2007;6:529–536.

    Article  PubMed  CAS  Google Scholar 

  64. Lleo A, Invernizzi P, Selmi C, Coppel RL, Alpini G, Podda M, et al. Autophagy: highlighting a novel player in the autoimmunity scenario. J Autoimmun 2007;29:61–68.

    Article  PubMed  CAS  Google Scholar 

  65. Bai AP, Ouyang Q, Xiao XR, Li SF. Probiotics modulate inflammatory cytokine secretion from inflamed mucosa in active ulcerative colitis. Int J Clin Pract 2006;60:284–288.

    Article  PubMed  Google Scholar 

  66. Rachmilewitz D, Karmeli F, Shteingart S, Lee J, Takabayashi K, Raz E. Immunostimulatory oligonucleotides inhibit colonic proinflammatory cytokine production in ulcerative colitis. Inflamm Bowel Dis 2006;12:339–345.

    Article  PubMed  Google Scholar 

  67. Borruel N, Casellas F, Antolín M, Llopis M, Carol M, Espíin E, et al. Effects of nonpathogenic bacteria on cytokine secretion by human intestinal mucosa. Am J Gastroenterol 2003;98:865–870.

    Article  PubMed  CAS  Google Scholar 

  68. Borruel N, Carol M, Casellas F, Antolín M, de Lara F, Espín E, et al. Increased mucosal tumour necrosis factor a production in Crohn’s disease can be downregulated ex vivo by probiotic bacteria. 51 2002;5.

    Google Scholar 

  69. Carol M, Borruel N, Antolín M, Llopis M, Casellas F, Guarner F, et al. Modulation of apoptosis in intestinal lymphocytes by a probiotic bacteria in Crohn’s disease. J Leukoc Biol 2006;79:917–922.

    Article  PubMed  CAS  Google Scholar 

  70. Ardesjo B, Hansson CM, Bruder CE, Rorsman F, Betterle C, Dumanski JP, et al. Autoantibodies to glutathione S-transferase theta 1 in patients with primary sclerosing cholangitis and other autoimmune diseases. J Autoimmun 2008;30:273–282.

    Article  PubMed  CAS  Google Scholar 

  71. Reinecker HC, Steffen M, Witthoeft T, Pflueger I, Schreiber S, MacDermott RP, et al. Enhanced secretion of tumour necrosis factor-alpha, IL-6, and IL-1β by isolated lamina propria mononuclear cells from patients with ulcerative colitis and Crohn’s disease. Clin Exp Immunol 1993;94:174–181.

    PubMed  CAS  Google Scholar 

  72. Atreya R, Mudter J, Finotto S, Müllberg J, Jostock T, Wirtz S, et al. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in Crohn disease and experimental colitis in vivo. Nat Med 2000;6:583–588.

    Article  PubMed  CAS  Google Scholar 

  73. Jonkers D, R. S. Review article: probiotics in gastrointestinal and liver diseases. Aliment Pharmacol Ther 2007;26Suppl 2:133–148.

    PubMed  CAS  Google Scholar 

  74. Holmén N, Lundgren A, Lundin S, Bergin AM, Rudin A, Sjövall H, et al. Functional CD4+CD25high regulatory T cells are enriched in the colonic mucosa of patients with active ulcerative colitis and increase with disease activity. Inflamm Bowel Dis 2006;12:447–456.

    Article  PubMed  Google Scholar 

  75. Saruta M, Yu QT, Fleshner PR, Mantel PY, Schmidt-Weber CB, Banham AH, et al. Characterization of FOXP3+CD4+ regulatory T cells in Crohn’s disease. Clin Immunol 2007;125:281–290.

    Article  PubMed  CAS  Google Scholar 

  76. Yu QT, Saruta M, Avanesyan A, Fleshner PR, Banham AH, Papadakis KA. Expression and functional characterization of FOXP3+ CD4+ regulatory T cells in ulcerative colitis. Inflamm Bowel Dis 2007;13:191–199.

    Article  PubMed  Google Scholar 

  77. Sitohy B, Hammarström S, Danielsson A, Hammarström ML. Basal lymphoid aggregates in ulcerative colitis colon: a site for regulatory T cell action. Clin Exp Immunol 2008;151:326–333.

    PubMed  CAS  Google Scholar 

  78. Muratov V, Ulfgren AK, Engström M, Elvin K, Winqvist O, Löfberg R, et al. Decreased numbers of FoxP3-positive and TLR-2-positive cells in intestinal mucosa are associated with improvement in patients with active inflammatory bowel disease following selective leukocyte apheresis. J Gastroenterol 2008;43:277–282.

    Article  PubMed  Google Scholar 

  79. Shaoul R, Lerner A. Associated autoantibodies in celiac disease. Autoimmun Rev 2007;6:559–565.

    Article  PubMed  CAS  Google Scholar 

  80. Burek CL, Rose NR. Autoimmune thyroiditis and ROS. Autoimmun Rev 2008;7:530–537.

    Article  PubMed  CAS  Google Scholar 

  81. Crane FL, Low H. Reactive oxygen species generation at the plasma membrane for antibody control. Autoimmun Rev 2008;7:518–522.

    Article  PubMed  CAS  Google Scholar 

  82. Davies AJ. Immunological tolerance and the autoimmune response. Autoimmun Rev 2008;7:538–543.

    Article  PubMed  CAS  Google Scholar 

  83. Dimitrov JD, Vassilev TL, Andre S, Kaveri SV, Lacroix-Desmazes S. Functional variability of antibodies upon oxidative processes. Autoimmun Rev 2008;7:574–578.

    Article  PubMed  CAS  Google Scholar 

  84. Griffiths HR. Is the generation of neo-antigenic determinants by free radicals central to the development of autoimmune rheumatoid disease? Autoimmun Rev 2008;7:544–549.

    Article  PubMed  CAS  Google Scholar 

  85. Kurien BT, Scofield RH. Autoimmunity and oxidatively modified autoantigens. Autoimmun Rev 2008;7:567–573.

    Article  PubMed  CAS  Google Scholar 

  86. Ortona E, Margutti P, Matarrese P, Franconi F, Malorni W. Redox state, cell death and autoimmune diseases: a gender perspective. Autoimmun Rev 2008;7:579–584.

    Article  PubMed  CAS  Google Scholar 

  87. Salunga TL, Cui ZG, Shimoda S, Zheng HC, Nomoto K, Kondo T, et al. Oxidative stress-induced apoptosis of bile duct cells in primary biliary cirrhosis. J Autoimmun 2007;29:78–86.

    Article  PubMed  CAS  Google Scholar 

  88. Sasaki M, Ikeda H, Nakanuma Y. Activation of ATM signaling pathway is involved in oxidative stress-induced expression of mito-inhibitory p21WAF1/Cip1 in chronic non-suppurative destructive cholangitis in primary biliary cirrhosis: an immunohistochemical study. J Autoimmun 2008;31:73–78.

    Article  PubMed  CAS  Google Scholar 

  89. Rolfe VE, Fortun PJ, Hawkey CJ, Bath-Hextall F. Probiotics for maintenance of remission in Crohn’s disease. Cochrane Database Syst Rev 2006 Oct 18;(4):CD004826.

  90. Mallon P, McKay D, Kirk S, Gardiner K. Probiotics for induction of remission in ulcerative colitis. Cochrane Database Syst Rev 2007 Oct 17;(4):CD005573.

  91. Zigra PI, Maipa VE, Alamanos YP. Probiotics and remission of ulcerative colitis: a systematic review. Neth J Med 2007;65:411–418.

    PubMed  CAS  Google Scholar 

  92. Furrie E, Macfarlane S, Kennedy A, Cummings JH, Walsh SV, O’Neil DA, et al. Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: a randomised controlled pilot trial. Gut 2005;54:242–249.

    Article  PubMed  CAS  Google Scholar 

  93. Ulisse S, Gionchetti P, D’Alò S, Russo FP, Pesce I, Ricci G, et al. Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatment. Am J Gastroenterol 2001;96:2691–2699.

    Article  PubMed  CAS  Google Scholar 

  94. O’Mahony L, McCarthy J, Kelly P, Hurley G, Luo F, Chen K, et al. Lactobacillus and Bifidobacterium in irritable bowel syndrome: symptom responses and relationship to cytokine profiles. Gastroenterology 2005;128:541–551.

    Article  PubMed  Google Scholar 

  95. Lorea Baroja M, Kirjavainen PV, Hekmat S, Reid G. Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clin Exp Immunol 2007;149:470–479.

    PubMed  CAS  Google Scholar 

  96. Pronio A, Montesani C, Butteroni C, Vecchione S, Mumolo G, Vestri A, et al. Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells. Inflamm Bowel Dis 2008;14:662–668.

    Article  PubMed  Google Scholar 

  97. Schultz M, Linde HJ, Lehn N, Zimmermann K, Grossmann J, Falk W, et al. Immunomodulatory consequences of oral administration of Lactobacillus rhamnosus strain GG in healthy volunteers. J Dairy Res 2003;70:165–173.

    Article  PubMed  CAS  Google Scholar 

  98. Hvas CL, Kelsen J, Agnholt J, Höllsberg P, Tvede M, Møller JK, et al. Crohn’s disease intestinal CD4+ T cells have impaired interleukin-10 production which is not restored by probiotic bacteria. Scand J Gastroenterol 2007;42:592–601.

    Article  PubMed  CAS  Google Scholar 

  99. Mudter J, Wirtz S, Galle PR, Neurath MF. A new model of chronic colitis in SCID mice induced by adoptive transfer of CD 62L+ CD4+ T cells: insights into the regulatory role of interleukin-6 on apoptosis. Pathobiology 2002–2003;70:170–176.

    Article  PubMed  CAS  Google Scholar 

  100. Peran L, Camuesco D, Comalada M, Bailon E, Henriksson A, Xaus J, et al. A comparative study of the preventative effects exerted by three probiotics, Bifidobacterium lactis, Lactobacillus casei and Lactobacillus acidophilus, in the TNBS model of rat colitis. J Appl Microbiol 2007;103:836–844.

    Article  PubMed  CAS  Google Scholar 

  101. Peran L, Sierra S, Comalada M, Lara-Villoslada F, Bailón E, Nieto Á, et al. A comparative study of the preventative effects exerted by two probiotics, Lactobacillus reuteri and Lactobacillus fermentum, in the trinitrobenzenesulfonic acid model of rat colitis. Br J Nutr 2007;97:96–103.

    Article  PubMed  CAS  Google Scholar 

  102. Dieleman LA, Goerres MS, Arends A, Sprengers D, Torrice C, Hoentjen F, et al. Lactobacillus GG prevents recurrence of colitis in HLA-B27 transgenic rats after antibiotic treatment. Gut 2003;52:370–376.

    Article  PubMed  CAS  Google Scholar 

  103. McCarthy J, O’Mahony L, O’Callaghan L, Sheil B, Vaughan EE, Fitzsimons N, et al. Double blind, placebo controlled trial of two probiotic strains in interleukin 10 knockout mice and mechanistic link with cytokine balance. Gut 2003;52:975–980.

    Article  PubMed  CAS  Google Scholar 

  104. Schultz M, Veltkamp C, Dieleman LA, Grenther WB, Wyrick PB, Tonkonogy SL, et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis 2002;8:71–80.

    Article  PubMed  Google Scholar 

  105. Schultz M, Strauch UG, Linde HJ, Watzl S, Obermeier F, Göttl C, et al. 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 2004;11:372–378.

    Article  PubMed  Google Scholar 

  106. Møller PL, Pærregaard A, Gad M, Kristensen NN, Claesson MH. Colitic SCID mice fed Lactobacillus spp. show an ameliorated gut histopathology and an altered cytokine profile by local T cells. Inflamm Bowel Dis 2005;11:814–819.

    Article  PubMed  Google Scholar 

  107. Foligne B, Zoumpopoulou G, Dewulf J, Ben Younes A, Chareyre F, Sirard JC, et al. A key role of dendritic cells in probiotic functionality. PLoS ONE 2007;2:e313; accessed 18 Apr 2008.

    Article  PubMed  CAS  Google Scholar 

  108. Foligne B, Nutten S, Grangette C, Dennin V, Goudercourt D, Poiret S, et al. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J Gastroenterol 2007;13:236–243.

    PubMed  Google Scholar 

  109. Zoumpopoulou G, Foligne B, Christodoulou K, Grangette C, Pot B, Tsakalidou E. Lactobacillus fermentum ACA-DC 179 displays probiotic potential in vitro and protects against trinitrobenzene sulfonic acid (TNBS)-induced colitis and Salmonella infection in murine models. Int J Food Microbiol 2008;121:18–26.

    Article  PubMed  CAS  Google Scholar 

  110. Grangette C, Nutten S, Palumbo E, Morath S, Hermann C, Dewulf J, et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci USA 2005;102:10321–10326.

    Article  PubMed  CAS  Google Scholar 

  111. Di Giacinto C, Marinaro M, Sanchez M, Strober W, Boirivant M. Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-b-bearing regulatory cells. J Immunol 2005;174:3237–3246.

    PubMed  Google Scholar 

  112. Joetham A, Takeda K, Taube C, Miyahara N, Matsubara S, Koya T, et al. Naturally occurring lung CD4+CD25+ T cell regulation of airway allergic responses depends on IL-10 induction of TGF-β. J Immunol 2007;178:1433–1442.

    PubMed  CAS  Google Scholar 

  113. Rachmilewitz D, Katakura K, Karmeli F, Hayashi T, Reinus C, Rudensky B, et al. Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology 2004;126:520–528.

    Article  PubMed  CAS  Google Scholar 

  114. Katakura K, Lee J, Rachmilewitz D, Li G, Eckmann L, Raz E. Toll-like receptor 9-induced type I IFN protects mice from experimental colitis. J Clin Invest 2005;115:695–702.

    PubMed  CAS  Google Scholar 

  115. Mantovani A, Garlanda C, Locati M, Rodriguez TV, Feo SG, Savino B, et al. Regulatory pathways in inflammation. Autoimmun Rev 2007;7:8–11.

    Article  PubMed  CAS  Google Scholar 

  116. Askenasy N, Kaminitz A, Yarkoni S. Mechanisms of T regulatory cell function. Autoimmun Rev 2008;7:370–375.

    Article  PubMed  CAS  Google Scholar 

  117. Penders J, Stobberingh EE, van den Brandt PA, Thijs C. The role of the intestinal microbiota in the development of atopic disorders. Allergy 2007;62:1223–1236.

    Article  PubMed  CAS  Google Scholar 

  118. Adlerberth I, Strachan DP, Matricardi PM, Ahrné S, Orfei L, Åberg N, et al. Gut microbiota and development of atopic eczema in 3 European birth cohorts. J Allergy Clin Immunol 2007;120:343–350.

    Article  PubMed  CAS  Google Scholar 

  119. Taylor AL, Dunstan JA, Prescott SL. Probiotic supplementation for the first 6 months of life fails to reduce the risk of atopic dermatitis and increases the risk of allergen sensitization in high-risk children: a randomized controlled trial. J Allergy Clin Immunol 2007;119:184–191.

    Article  PubMed  Google Scholar 

  120. Abrahamsson TR, Jakobsson T, Böttcher MF, Fredrikson M, Jenmalm MC, Björkstén B, et al. Probiotics in prevention of IgEassociated eczema: a double-blind, randomized, placebo-controlled trial. J Allergy Clin Immunol 2007;119:1174–1180.

    Article  PubMed  CAS  Google Scholar 

  121. Kalliomäki M, Salminen S, Arvilommi H, Kero P, Koskinen P, Isolauri E. Probiotics in primary prevention of atopic disease: a randomised placebo-controlled trial. Lancet 2001;357:1076–1079.

    Article  PubMed  Google Scholar 

  122. Kalliomäki M, Salminen S, Poussa T, Arvilommi H, Isolauri E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomized placebo-controlled trial. Lancet 2003;361:1869–1871.

    Article  PubMed  Google Scholar 

  123. Kalliomäki M, Salminen S, Poussa T, Isolauri E. Probiotics during the first 7 years of life: a cumulative risk reduction of eczema in a randomized, placebo-controlled trial. J Allergy Clin Immunol 2007;119:1019–1021.

    Article  PubMed  Google Scholar 

  124. Kukkonen K, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. Probiotics and prebiotic gala-ctooligosaccharides in the prevention of allergic diseases: a randomized, double-blind, placebo-controlled trial. J Allergy Clin Immunol 2007;119:192–198.

    Article  PubMed  CAS  Google Scholar 

  125. Kopp MV, Hennemuth I, Heinzmann A, Urbanek R. Randomized, double-blind, placebo-controlled trial of probiotics for primary prevention: no clinical effects of Lactobacillus GG supplementation. Pediatrics 2008;121:e850–e856.

    Article  PubMed  Google Scholar 

  126. Prescott SL, Björkstén B. Probiotics for the prevention or treatment of allergic diseases. J Allergy Clin Immunol 2007;120:255–262.

    Article  PubMed  CAS  Google Scholar 

  127. Rautava S, Kalliomäki M, Isolauri E. Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J Allergy Clin Immunol 2002;109:119–121.

    Article  PubMed  Google Scholar 

  128. Böttcher MF, Abrahamsson TR, Fredriksson M, Jakobsson T, Björkstén B. Low breast milk TGF-β2 is induced by Lactobacillus reuteri supplementation and associates with reduced risk of sensitization during infancy. Pediatr Allergy Immunol 2008;2008 Jan 22 [Epub ahead of print].

  129. Marschan E, Kuitunen M, Kukkonen K, Poussa T, Sarnesto A, Haahtela T, et al. Probiotics in infancy induce protective immune profiles that are characteristic for chronic low-grade inflammation. Clin Exp Allergy 2008;38:611–618.

    Article  PubMed  CAS  Google Scholar 

  130. Viljanen M, Pohjavuori E, Haahtela T, Korpela R, Kuitunen M, Sarnesto A, et al. Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome. J Allergy Clin Immunol 2005;115:1254–1259.

    Article  PubMed  CAS  Google Scholar 

  131. Viljanen M, Savilahti E, Haahtela T, Juntunen-Backman K, Korpela R, Poussa T, et al. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: a double-blind placebo-controlled trial. Allergy 2005;60:494–500.

    Article  PubMed  CAS  Google Scholar 

  132. Betsi GI, Papadavid E, Falagas ME. Probiotics for the treatment or prevention of atopic dermatitis: a review of the evidence from randomized controlled trials. Am J Clin Dermatol 2008;9:93–103.

    Article  PubMed  Google Scholar 

  133. Weston S, Halbert A, Richmond P, Prescott SL. Effects of probiotics on atopic dermatitis: a randomised controlled trial. Arch Dis Child 2005;90:892–897.

    Article  PubMed  CAS  Google Scholar 

  134. Brouwer ML, Wolt-Plompen SA, Dubois AE, van der Heide S, Jansen DF, Hoijer MA, et al. No effects of probiotics on atopic dermatitis in infancy: a randomized placebo-controlled trial. Clin Exp Allergy 2006;36:899–906.

    Article  PubMed  CAS  Google Scholar 

  135. Rosenfeldt V, Benfeldt E, Nielsen SD, Michaelsen KF, Jeppesen DL, Valerius NH, et al. Effect of probiotic Lactobacillus strains in children with atopic dermatitis. J Allergy Clin Immunol 2003;111:389–395.

    Article  PubMed  Google Scholar 

  136. Pohjavuori E, Viljanen M, Korpela R, Kuitunen M, Tiittanen M, Vaarala O, et al. Lactobacillus GG effect in increasing IFN-γ production in infants with cow’s milk allergy. J Allergy Clin Immunol 2004;114:131–136.

    Article  PubMed  CAS  Google Scholar 

  137. Prescott SL, Dunstan JA, Hale J, Breckler L, Lehmann H, Weston S, et al. Clinical effects of probiotics are associated with increased interferon-γ responses in very young children with atopic dermatitis. Clin Exp Allergy 2005;35:1557–1564.

    PubMed  CAS  Google Scholar 

  138. Cross ML, Mortensen RR, Kudsk J, Gill HS. Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med Microbiol Immunol 2002;191:49–53.

    Article  PubMed  CAS  Google Scholar 

  139. Forsythe P, Inman MD, Bienenstock J. Oral treatment with live Lactobacillus reuteri inhibits the allergic airway response in mice. Am J Respir Crit Care Med 2007;175:561–569.

    Article  PubMed  Google Scholar 

  140. Feleszko W, Jaworska J, Rha RD, Steinhausen S, Avagyan A, Jaudszus A, et al. Probiotic-induced suppression of allergic sensitization and airway inflammation is associated with an increase of T regulatory-dependent mechanisms in a murine model of asthma. Clin Exp Allergy 2007;37:498–505.

    Article  PubMed  CAS  Google Scholar 

  141. Veckman V, Miettinen M, Pirhonen J, Sirén J, Matikainen S, Julkunen I. Streptococcus pyogenes and Lactobacillus rhamnosus differentially induce maturation and production of Th1-type cytokines and chemokines in human monocyte-derived dendritic cells. J Leukoc Biol 2004;75:764–771.

    Article  PubMed  CAS  Google Scholar 

  142. Pochard P, Gosset P, Grangette C, Andre C, Tonnel AB, Pestel J, et al. Lactic acid bacteria inhibit TH2 cytokine production by mononuclear cells from allergic patients. J Allergy Clin Immunol 2002;110:617–623.

    Article  PubMed  CAS  Google Scholar 

  143. Kopp MV, Goldstein M, Dietschek A, Sofke J, Heinzmann A, Urbanek R. Lactobacillus GG has in vitro effects on enhanced interleukin-10 and interferon-γ release of mononuclear cells but no in vivo effects in supplemented mothers and their neonates. Clin Exp Allergy 2008;38:602–610.

    Article  PubMed  CAS  Google Scholar 

  144. Miettinen M, Matikainen S, Vuopio-Varkila J, Pirhonen J, Varkila K, Kurimoto M, et al. Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infect Immun 1998;66:6058–6062.

    PubMed  CAS  Google Scholar 

  145. Van Overtvelt L, Lombardi V, Razafindratsita A, Saint-Lu N, Horiot S, Moussu H, et al. IL-10-inducing adjuvants enhance sublingual immunotherapy efficacy in a murine asthma model. Int Arch Allergy Immunol 2008;145:152–162.

    Article  PubMed  CAS  Google Scholar 

  146. Ishida Y, Bandou I, Kanzato H, Yamamoto N. Decrease in ovalbumin specific IgE of mice serum after oral uptake of lactic acid bacteria. Biosci Biotechnol Biochem 2003;67:951–957.

    Article  PubMed  CAS  Google Scholar 

  147. Sunada Y, Nakamura S, Kamei C. Effects of Lactobacillus acidophilus strain L-55 on experimental allergic rhinitis in BALB/c mice. Biol Pharm Bull 2007;30:2163–2166.

    Article  PubMed  CAS  Google Scholar 

  148. Kim H, Kwack K, Kim DY, Ji GE. Oral probiotic bacterial administration suppressed allergic responses in an ovalbumin-induced allergy mouse model. FEMS Immunol Med Microbiol 2005;45:259–267.

    Article  PubMed  CAS  Google Scholar 

  149. Sheth AA, Garcia-Tsao G. Probiotics and liver disease. J Clin Gastroenterol 2008;42Suppl 2:S80–S84.

    Article  PubMed  Google Scholar 

  150. Wiest R, Garcia-Tsao G. Bacterial translocation (BT) in cirrhosis. Hepatology 2005;41:422–433.

    Article  PubMed  CAS  Google Scholar 

  151. Ewaschuk J, Endersby R, Thiel D, Diaz H, Backer J, Ma M, et al. Probiotic bacteria prevent hepatic damage and maintain colonic barrier function in a mouse model of sepsis. Hepatology 2007;46:841–850.

    Article  PubMed  CAS  Google Scholar 

  152. Selmi C, Bowlus CL, Keen CL, Gershwin ME. Non-alcoholic fatty liver disease: the new epidemic and the need for novel nutritional approaches. J Med Food 2007;10:563–565.

    Article  PubMed  Google Scholar 

  153. Vollmers HP, Brandlein S. Natural antibodies and cancer. J Autoimmun 2007;29:295–302.

    Article  PubMed  CAS  Google Scholar 

  154. Lan RY, Selmi C, Gershwin ME. The regulatory, inflammatory, and T cell programming roles of interleukin-2 (IL-2). J Autoimmun 2008;31:7–12.

    Article  PubMed  CAS  Google Scholar 

  155. de Moreno de LeBlanc A, Matar C, Perdigon G. The application of probiotics in cancer. Br J Nutr 2007;98(Suppl 1):S105–S110.

    PubMed  Google Scholar 

  156. Perdigon G, de Moreno de LeBlanc A, Valdez J, Rachid M. Role of yoghurt in the prevention of colon cancer. Eur J Clin Nutr 2002;56(Suppl 3):S65–S68.

    Article  PubMed  CAS  Google Scholar 

  157. de Moreno de LeBlanc A, Matar C, Theriault C, Perdigon G. Effects of milk fermented by Lactobacillus helveticus R389 on immune cells associated to mammary glands in normal and a breast cancer model. Immunobiology 2005;210:349–358.

    Article  PubMed  CAS  Google Scholar 

  158. Besselink MG, van Santvoort HC, Buskens E, Boermeester MA, van Goor H, Timmerman HM, et al. Probiotic prophylaxis in predicted severe acute pancreatitis: a randomised, double-blind, placebo-controlled trial. Lancet 2008;371:651–659.

    Article  PubMed  Google Scholar 

  159. Nagao F, Nakayama M, Muto T, Okumura K. Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the immune system in healthy human subjects. Biosci Biotechnol Biochem 2000;64:2706–2708.

    Article  PubMed  CAS  Google Scholar 

  160. Takeda K, Okumura K. Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity. J Nutr 2007;137:791S–793S.

    PubMed  CAS  Google Scholar 

  161. Morimoto K, Takeshita T, Nanno M, Tokudome S, Nakayama K. Modulation of natural killer cell activity by supplementation of fermented milk containing Lactobacillus casei in habitual smokers. Prev Med 2005;40:589–594.

    Article  PubMed  Google Scholar 

  162. Parra MD, Martínez de Morentin BE, Cobo JM, Mateos A, Martínez JA. Daily ingestion of fermented milk containing Lactobacillus casei DN114001 improves innate-defense capacity in healthy middle-aged people. J Physiol Biochem 2004;60:85–91.

    Article  PubMed  CAS  Google Scholar 

  163. Sheih YH, Chiang BL, Wang LH, Liao CK, Gill HS. Systemic immunity-enhancing effects in healthy subjects following dietary consumption of the lactic acid bacterium Lactobacillus rhamnosus HN001. J Am Coll Nutr 2001;20:149–156.

    PubMed  CAS  Google Scholar 

  164. Gill HS, Rutherfurd KJ, Cross ML. Dietary probiotic supplementation enhances natural killer cell activity in the elderly: an investigation of age-related immunological changes. J Clin Immunol 2001;21:264–271.

    Article  PubMed  CAS  Google Scholar 

  165. Chiang BL, Sheih YH, Wang LH, Liao CK, Gill HS. Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium (Bifidobacterium lactis HN019): optimization and definition of cellular immune responses. Eur J Clin Nutr 2000;54:849–855.

    Article  PubMed  CAS  Google Scholar 

  166. Gill HS, Rutherfurd KJ, Cross ML, Gopal PK. Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 2001;74:833–839.

    PubMed  CAS  Google Scholar 

  167. Klein A, Friedrich U, Vogelsang H, Jahreis G. Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. Eur J Clin Nutr 2008;62:584–593.

    Article  PubMed  CAS  Google Scholar 

  168. Roessler A, Friedrich U, Vogelsang H, Bauer A, Kaatz M, Hipler UC, et al. The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clin Exp Allergy 2008;38:93–102.

    PubMed  CAS  Google Scholar 

  169. Christensen HR, Larsen CN, Kaestel P, Rosholm LB, Sternberg C, Michaelsen KF, et al. Immunomodulating potential of supplementation with probiotics: a dose-response study in healthy young adults. FEMS Immunol Med Microbiol 2006;47:380–390.

    Article  PubMed  CAS  Google Scholar 

  170. Spanhaak S, Havenaar R, Schaafsma G. The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. Eur J Clin Nutr 1998;52:899–907.

    Article  PubMed  CAS  Google Scholar 

  171. Kekkonen RA, Lummela N, Karjalainen H, Latvala S, Tynkkynen S, Järvenpää S, et al. Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World J Gastroenterol 2008;14:2029–2036.

    Article  PubMed  Google Scholar 

  172. Olivares M, Díaz-Ropero MP, Sierra S, Lara-Villoslada F, Fonollá J, Navas M, et al. Oral intake of Lactobacillus fermentum CECT5716 enhances the effects of influenza vaccination. Nutrition 2007;23:254–260.

    Article  PubMed  CAS  Google Scholar 

  173. de Vrese M, Rautenberg P, Laue C, Koopmans M, Herremans T, Schrezenmeir J. Probiotic bacteria stimulate virus-specific neutralizing antibodies following a booster polio vaccination. Eur J Nutr 2005;44:406–413.

    Article  PubMed  CAS  Google Scholar 

  174. Kukkonen K, Nieminen T, Poussa T, Savilahti E, Kuitunen M. Effect of probiotics on vaccine antibody responses in infancy—a randomized placebo-controlled double-blind trial. Pediatr Allergy Immunol 2006;17:416–421.

    Article  PubMed  Google Scholar 

  175. West CE, Gothefors L, Granström M, Käyhty H, Hammarström ML, Hernell O. Effects of feeding probiotics during weaning on infections and antibody responses to diphtheria, tetanus and Hib vaccines. Pediatr Allergy Immunol 2008;19:53–60.

    PubMed  Google Scholar 

  176. Ma D, Forsythe P, Bienenstock J. Live Lactobacillus reuteri is essential for the inhibitory effect on tumor necrosis factor alpha-induced interleukin-8 expression. Infect Immun 2004;72:5308–5314.

    Article  PubMed  CAS  Google Scholar 

  177. Medina M, Izquierdo E, Ennahar S, Sanz Y. Differential immunomodulatory properties of Bifidobacterium logum [sic] strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol 2007;150:531–538.

    Article  PubMed  CAS  Google Scholar 

  178. Sashihara T, Sueki N, Ikegami S. An analysis of the effectiveness of heat-killed lactic acid bacteria in alleviating allergic diseases. J Dairy Sci 2006;89:2846–2855.

    PubMed  CAS  Google Scholar 

  179. Helwig U, Lammers KM, Rizzello F, Brigidi P, Rohleder V, Caramelli E, et al. Lactobacilli, bifidobacteria and E. coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J Gastroenterol 2006;12:5978–5986.

    PubMed  CAS  Google Scholar 

  180. Shida K, Kiyoshima-Shibata J, Nagaoka M, Watanabe K, Nanno M. Induction of interleukin-12 by Lactobacillus strains having a rigid cell wall resistant to intracellular digestion. J Dairy Sci 2005;89:3306–3317.

    Google Scholar 

  181. Matsuguchi T, Takagi A, Matsuzaki T, Nagaoka M, Ishikawa K, Yokokura T, et al. Lipoteichoic acids from Lactobacillus strains elicit strong tumor necrosis factor alpha-inducing activities in macrophages through Toll-like receptor 2. Clin Diagn Lab Immunol 2003;10:259–266.

    Article  PubMed  CAS  Google Scholar 

  182. Iliev ID, Kitazawa H, Shimosato T, Katoh S, Morita H, He F, et al. Strong immunostimulation in murine immune cells by Lactobacillus rhamnosus GG DNA containing novel oligodeoxynucleotide pattern. Cell Microbiol 2005;7:403–414; Erratum, 611.

    Article  PubMed  CAS  Google Scholar 

  183. Kitazawa H, Watanabe H, Shimosato T, Kawai Y, Itoh T, Saito T. Immunostimulatory oligonucleotide, CpG-like motif exists in Lactobacillus delbrueckii ssp. bulgaricus NIAI B6. Int J Food Microbiol 2003;85:11–21.

    Article  PubMed  CAS  Google Scholar 

  184. Kitazawa H, Ueha S, Itoh S, Watanabe H, Konno K, Kawai Y, et al. AT oligonucleotides inducing B lymphocyte activation exist in probiotic Lactobacillus gasseri. Int J Food Microbiol 2001;65:149–162.

    Article  PubMed  CAS  Google Scholar 

  185. Takahashi N, Kitazawa H, Shimosato T, Iwabuchi N, Xiao JZ, Iwatsuki K, et al. An immunostimulatory DNA sequence from a probiotic strain of Bifidobacterium longum inhibits IgE production in vitro. FEMS Immunol Med Microbiol 2006;46:461–469.

    Article  PubMed  CAS  Google Scholar 

  186. Takahashi N, Kitazawa H, Iwabuchi N, Xiao JZ, Miyaji K, Iwatsuki K, et al. Oral administration of an immunostimulatory DNA sequence from Bifidobacterium longum improves Th1/Th2 balance in a murine model. Biosci Biotechnol Biochem 2006;70:2013–2017.

    Article  PubMed  CAS  Google Scholar 

  187. Iliev ID, Tohno M, Kurosaki D, Shimosato T, He F, Hosoda M, et al. Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from Lactobacillus rhamnosus GG DNA potentially suppresses OVA-specific IgE production in mice. Scand J Immunol 2008;67:370–376.

    Article  PubMed  CAS  Google Scholar 

  188. Zeuthen LH, Fink LN, Frøkiær H. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology 2008;124:489–502.

    Article  PubMed  CAS  Google Scholar 

  189. Karlsson H, Hessle C, Rudin A. Innate immune responses of human neonatal cells to bacteria from the normal gastrointestinal flora. Infect Immun 2002;70:6688–6696.

    Article  PubMed  CAS  Google Scholar 

  190. Ichikawa S, Fujii R, Fujiwara D, Komiyama Y, Kaisho T, Sakaguchi M, et al. MyD88 but not TLR2, 4 or 9 is essential for IL-12 induction by lactic acid bacteria. Biosci Biotechnol Biochem 2007;71:3026–3032.

    Article  PubMed  CAS  Google Scholar 

  191. Baken KA, Ezendam J, Gremmer ER, de Klerk A, Pennings JL, Matthee B, et al. Evaluation of immunomodulation by Lactobacillus casei Shirota: immune function, autoimmunity and gene expression. Int J Food Microbiol 2006;112:8–18.

    Article  PubMed  CAS  Google Scholar 

  192. Ezendam J, van Loveren H. Lactobacillus casei Shirota administered during lactation increases the duration of autoimmunity in rats and enhances lung inflammation in mice. Br J Nutr 2008;99:83–90.

    Article  PubMed  CAS  Google Scholar 

  193. Maassen CB, van Holten JC, Balk F, Heijne den Bak-Glashouwer MJ, Leer R, Laman JD, et al. Orally administered Lactobacillus strains differentially affect the direction and efficacy of the immune response. Vet Q 1998;20:S81–S83.

    PubMed  Google Scholar 

  194. Maassen CB, Claassen E. Strain-dependent effects of probiotic lactobacilli on EAE autoimmunity. Vaccine 2008;26:2056–2057.

    Article  PubMed  CAS  Google Scholar 

  195. Baharav E, Mor F, Halpern M, Weinberger A. Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr 2004;123:1964–1969.

    Google Scholar 

  196. So JS, Kwon HK, Lee CG, Yi HJ, Park JA, Lim SY, et al. Lactobacillus casei suppresses experimental arthritis by downregulating T helper 1 effector functions. Mol Immunol 2008;45:2690–2699.

    Article  PubMed  CAS  Google Scholar 

  197. Kato I, Endo-Tanaka K, Yokokura T. Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci 1998;63:635–644.

    Article  PubMed  CAS  Google Scholar 

  198. Calcinaro F, Dionisi S, Marinaro M, Candeloro P, Bonato V, Marzotti S, et al. Oral probiotic administration induces interleukin-10 production and prevents spontaneous autoimmune diabetes in the non-obese diabetic mouse. Diabetologia 2005;48: 1565–1575.

    Article  PubMed  CAS  Google Scholar 

  199. Ratajczak C, Duez C, Grangette C, Pochard P, Tonnel AB, Pestel J. Impact of lactic acid bacteria on dendritic cells from allergic patients in an experimental model of intestinal epithelium. J Biomed Biotechnol 2007;2007:71921. Epub 2007 Feb 28.

    PubMed  Google Scholar 

  200. Pelto L, Isolauri E, Lilius EM, Nuutila J, Salminen S. Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin Exp Allergy 1998;28:1474–1479.

    Article  PubMed  CAS  Google Scholar 

  201. Pochard P, Hammad H, Ratajczak C, Charbonnier-Hatzfeld AS, Just N, Tonnel AB, et al. Direct regulatory immune activity of lactic acid bacteria on Der p 1-pulsed dendritic cells from allergic patients. J Allergy Clin Immunol 2005;116:198–204.

    Article  PubMed  CAS  Google Scholar 

  202. Christensen HR, Frøkiær H, Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 2002;168:171–178.

    PubMed  CAS  Google Scholar 

  203. Kim H, Lee SY, Ji GE. Timing of Bifidobacterium administration influences the development of allergy to ovalbumin in mice. Biotechnol Lett 2005;27:1361–1367.

    Article  PubMed  CAS  Google Scholar 

  204. Peng S, Lin JY, Lin MY. Antiallergic effect of milk fermented with lactic acid bacteria in a murine animal model. J Agric Food Chem 2007;55:5092–5096.

    Article  PubMed  CAS  Google Scholar 

  205. Ohno H, Tsunemine S, Isa Y, Shimakawa M, Yamamura H. Oral administration of Bifidobacterium bifidum G9-1 suppresses total and antigen specific immunoglobulin E production in mice. Biol Pharm Bull 2005;28:1462–1466.

    Article  PubMed  CAS  Google Scholar 

  206. Torii A, Torii S, Fujiwara S, Tanaka H, Inagaki N, Nagai H. Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol Int 2007;56:293–301.

    Article  PubMed  CAS  Google Scholar 

  207. Segawa S, Nakakita Y, Takata Y, Wakita Y, Kaneko T, Kaneda H, et al. Effect of oral administration of heat-killed Lactobacillus brevis SBC8803 on total and ovalbumin-specific immunoglobulin E production through the improvement of Th1/Th2 balance. Int J Food Microbiol 2008;121:1–10.

    Article  PubMed  CAS  Google Scholar 

  208. Matsuzaki T, Yamazaki R, Hashimoto S, Yokokura T. The effect of oral feeding of Lactobacillus casei strain Shirota on immunoglobulin E production in mice. J Dairy Sci 1998;81:48–53.

    Article  PubMed  CAS  Google Scholar 

  209. Fujiwara D, Inoue S, Wakabayashi H, Fujii T. The anti-allergic effects of lactic acid bacteria are strain dependent and mediated by effects on both Th1/Th2 cytokine expression and balance. Int Arch Allergy Immunol 2004;135:205–215.

    Article  PubMed  CAS  Google Scholar 

  210. Nonaka Y, Izumo T, Izumi F, Maekawa T, Shibata H, Nakano A, et al. Antiallergic effects of Lactobacillus pentosus strain S-PT84 mediated by modulation of Th1/Th2 immunobalance and induction of IL-10 production. Int Arch Allergy Immunol 2008;145:249–257.

    Article  PubMed  Google Scholar 

  211. Hisbergues M, Magi M, Rigaux P, Steuve J, Garcia L, Goudercourt D, et al. In vivo and in vitro immunomodulation of Der p 1 allergen-specific response by Lactobacillus plantarum bacteria. Clin Exp Allergy 2007;37:1286–1295.

    Article  PubMed  CAS  Google Scholar 

  212. Ruiz PA, Hoffmann M, Szcesny S, Blaut M, Haller D. Innate mechanisms for Bifidobacterium lactis to activate transient proinflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats. Immunology 2005;115:441–450.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Nutrition, Allergy and Clinical Immunology, University of California at Davis, Davis, CA, USA

    Andrea T. Borchers & Carl L. Keen

  2. Division of Rheumatology, Allergy and Clinical Immunology, University of California at Davis, Genome and Biomedical Sciences Facility, 451 Health Sciences Drive, Suite 6510, Davis, CA, 95616, USA

    Carlo Selmi & M. Eric Gershwin

  3. Department of Internal Medicine, IRCCS Istituto Clinico Humanitas, University of Milan, Milan, Italy

    Carlo Selmi

  4. Department of Internal Medicine, University of California at Davis Medical Center, Sacramento, CA, USA

    Frederick J. Meyers

Authors
  1. Andrea T. Borchers
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlo Selmi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Frederick J. Meyers
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Carl L. Keen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M. Eric Gershwin
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Borchers, A.T., Selmi, C., Meyers, F.J. et al. Probiotics and immunity. J Gastroenterol 44, 26–46 (2009). https://doi.org/10.1007/s00535-008-2296-0

Download citation

  • Received: 03 September 2008

  • Accepted: 03 September 2008

  • Published: 22 January 2009

  • Issue Date: January 2009

  • DOI: https://doi.org/10.1007/s00535-008-2296-0

Share this article

Anyone you share the following link with will be able to read this content:

Sorry, a shareable link is not currently available for this article.

Provided by the Springer Nature SharedIt content-sharing initiative

Key words

  • microflora
  • nutritional immunology
  • dietary supplement
  • innate immunity
  • vaccine
Use our pre-submission checklist

Avoid common mistakes on your manuscript.

Advertisement

Search

Navigation

  • Find a journal
  • Publish with us
  • Track your research

Discover content

  • Journals A-Z
  • Books A-Z

Publish with us

  • Journal finder
  • Publish your research
  • Open access publishing

Products and services

  • Our products
  • Librarians
  • Societies
  • Partners and advertisers

Our imprints

  • Springer
  • Nature Portfolio
  • BMC
  • Palgrave Macmillan
  • Apress
  • Your US state privacy rights
  • Accessibility statement
  • Terms and conditions
  • Privacy policy
  • Help and support
  • Cancel contracts here

44.222.131.239

Not affiliated

Springer Nature

© 2024 Springer Nature