Advertisement

Applied Microbiology and Biotechnology

, Volume 96, Issue 4, pp 853–862 | Cite as

The immunomodulatory effects of lactic acid bacteria for improving immune functions and benefits

Mini-Review

Abstract

Probiotics have a number of beneficial health effects in humans and animals, such as reducing lactose intolerance symptoms and enhancing the bioavailability of nutrients. Probiotics help regulate intestinal microflora and immunomodulatory properties. Probiotics also decrease the prevalence of allergies in susceptible individuals, inhibit the inflammatory responses in the gut, and have antagonistic effects against intestinal and food-borne pathogens. Bacteria typically colonize the intestinal tract first and then reinforce the host defense systems by inducing generalized mucosal immune responses, including modulation of DC/NK interaction, a balanced T-helper cell response, self-limited inflammatory response, and the secretion of polymeric IgA. A lot of reports showed that lactic acid bacteria (LAB) as Lactobacillus and Bifidobacterium and their fermented products are effective at enhancing innate and adaptive immunity, prevent gastric mucosal lesion development, alleviate allergies, and put up defense against intestinal pathogen infection. In this review paper, we compared the influence of immunomodulatory effects on the function and efficacy of lactobacillus products with different strains. We also discuss the beneficial effects of several LAB strain and its derivative products for human immunity and related diseases.

Keywords

Lactobacillus paracasei subsp. paracasei NTU 101 Innate immune response Mucosal immunity Allergy Escherichia coli O157:H7 

References

  1. Aderem A, Underhill DM (1999) Mechanisms of phagocytosis in macrophages. Annu Rev Immunol 17:593–623CrossRefGoogle Scholar
  2. Ahrne S, Nobaek S, Jeppsson B, Adlerberth I, Wold AE, Molin G (1998) The normal Lactobacillus flora of healthy human rectal and oral mucosa. J Appl Microbiol 85:88–94CrossRefGoogle Scholar
  3. Andreoli SP, Trachtman H, Acheson DW, Siegler RL, Obrig TG (2002) Hemolytic uremic syndrome: epidemiology, pathophysiology, and therapy. Pediatr Nephrol 17:293–298CrossRefGoogle Scholar
  4. Bae EA, Min SW, Lee B, Kim NJ, Baek NI, Han EJ, Chung HG, Kim DH (2007) Antiasthmic effect of fermented Artemisia princeps in asthmic mice induced by ovalbumin. J Microbiol Biotechnol 17:1554–1557Google Scholar
  5. Biller JA, Katz AJ, Flores AF, Buie TM, Gorbach SL (1995) Treatment of recurrent Clostridium difficile colitis with Lactobacillus GG. J Pediatr Gastroenterol Nutr 21:224–226CrossRefGoogle Scholar
  6. Boirivant M, Strober W (2007) The mechanism of action of probiotics. Curr Opin Gastroenterol 23:679–692CrossRefGoogle Scholar
  7. Candela M, Perna F, Carnevali P, Vitali B, Ciati R, Gionchetti P, Rizzello F, Campieri M, Brigidi P (2008) Interaction of probiotic Lactobacillus and Bifidobacterium strains with human intestinal epithelial cells: adhesion properties, competition against enteropathogens and modulation of IL-8 production. Int J Food Microbiol 125:286–292CrossRefGoogle Scholar
  8. Cerwenka A, Lanier LL (2001) Natural killer cells, viruses and cancer. Nat Rev Immunol 1:41–49CrossRefGoogle Scholar
  9. Chiang SS, Pan TM (2011) Antiosteoporotic effects of Lactobacillus-fermented soy skim milk on bone mineral density and the microstructure of femoral bone in ovariectomized mice. J Agric Food Chem 59:7734–7742CrossRefGoogle Scholar
  10. Chiang SS, Liu CF, Tseng KC, Mau JL, Pan TM (2012) Immunomodulatory effects of dead Lactobacillus on murine splenocytes and macrophages. Food Agric Immunol 23:183–202CrossRefGoogle Scholar
  11. Chiu CH, Lu TY, Tseng YY, Pan TM (2006) The effects of Lactobacillus-fermented milk on lipid metabolism in hamsters fed on high-cholesterol diet. Appl Microbiol Biotechnol 71:238–245CrossRefGoogle Scholar
  12. Christensen HR, Frokiaer H, Pestka JJ (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168:171–178Google Scholar
  13. Cross ML (2002) Microbes versus microbes: immune signals generated by probiotic lactobacilli and their role in protection against microbial pathogens. FEMS Immunol Med Microbiol 34:245–253CrossRefGoogle Scholar
  14. Cross ML, Mortensen RR, Kudsk J, Gill HS (2002) Dietary intake of Lactobacillus rhamnosus HNOO1 enhances production of both Th1 and Th2 cytokines in antigen-primed mice. Med Microbiol Immunol 191:49–53CrossRefGoogle Scholar
  15. De Moreno de LeBlanc A, Chaves S, Carmuega E, Weill R, Antoine J, Perdigon G (2008) Effect of long-term continuous consumption of fermented milk containing probiotic bacteria on mucosal immunity and the activity of peritoneal macrophages. Immunobiology 213:97–108CrossRefGoogle Scholar
  16. de Vrese M, Schrezenmeir J (2008) Probiotics, prebiotics, and synbiotics. Adv Biochem Eng Biotechnol 111:1–66Google Scholar
  17. de Waard R, Garssen J, Bokken GC, Vos JG (2002) Antagonistic activity of Lactobacillus casei strain Shirota against gastrointestinal Listeria monocytogenes infection in rats. Int J Food Microbiol 73:93–100CrossRefGoogle Scholar
  18. Drakes M, Blanchard T, Czinn S (2004) Bacterial probiotic modulation of dendritic cellfs. Infect Immun 72:3299–3309CrossRefGoogle Scholar
  19. Enomoto M, Noguchi S, Hattori M, Sugiyama H, Suzuki Y, Hanaoka A, Okada S, Yoshida T (2009) Oral administration of Lactobacillus plantarum NRIC0380 suppresses IgE production and induces CD4(+)CD25(+)Foxp3(+) cells in vivo. Biosci Biotechnol Biochem 73:457–460CrossRefGoogle Scholar
  20. Fayette J, Dubois B, Vandenabeele S, Bridon JM, Vanbervliet B, Durand I, Banchereau J, Caux C, Briere F (1997) Human dendritic cells skew isotype switching of CD40-activated naive B cells towards IgA1 and IgA2. J Exp Med 185:1909–1918CrossRefGoogle Scholar
  21. Fernandez NC, Lozier A, Flament C, Ricciardi-Castagnoli P, Bellet D, Suter M, Perricaudet M, Tursz T, Maraskovsky E, Zitvogel L (1999) Dendritic cells directly trigger NK cell functions: cross-talk relevant in innate anti-tumor immune responses in vivo. Nat Med 5:405–411CrossRefGoogle Scholar
  22. Fink LN, Frokiaer H (2008) Dendritic cells from Peyer’s patches and mesenteric lymph nodes differ from spleen dendritic cells in their response to commensal gut bacteria. Scand J Immunol 68:270–279CrossRefGoogle Scholar
  23. Fink LN, Zeuthen LH, Christensen HR, Morandi B, Frokiaer H, Ferlazzo G (2007) Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. Int Immunol 19:1319–1327CrossRefGoogle Scholar
  24. Fooks LJ, Fuller R, Gibson GR (1999) Prebiotics, probiotics and human gut microbiology. Int Dairy J 9:53–61CrossRefGoogle Scholar
  25. Fujiwara D, Inoue S, Wakabayashi H, Fujii T (2004) 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 135:205–215CrossRefGoogle Scholar
  26. Fukuda S, Toh H, Hase K, Oshima K, Nakanishi Y, Yoshimura K, Tobe T, Clarke JM, Topping DL, Suzuki T, Taylor TD, Itoh K, Kikuchi J, Morita H, Hattori M, Ohno H (2011) Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469:543–547CrossRefGoogle Scholar
  27. Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66:365–378CrossRefGoogle Scholar
  28. Galdeano CM, Perdigon G (2004) Role of viability of probiotic strains in their persistence in the gut and in mucosal immune stimulation. J Appl Microbiol 97:673–681CrossRefGoogle Scholar
  29. Gill HS, Rutherfurd KJ, Prasad J, Gopal PK (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83:167–176CrossRefGoogle Scholar
  30. Gill HS, Rutherfurd KJ, Cross ML, Gopal PK (2001) Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. Am J Clin Nutr 74:833–839Google Scholar
  31. Goktepe I, Juneja VK, Ahmedna M (2006) Probiotics in food safety and human health. CRC PressGoogle Scholar
  32. Goldin BR (1998) Health benefits of probiotics. Br J Nutr 80:S203–S207Google Scholar
  33. Grewal IS, Flavell RA (1998) CD40 and CD154 in cell-mediated immunity. Annu Rev Immunol 16:111–135CrossRefGoogle Scholar
  34. Hiramatsu Y, Hosono A, Konno T, Nakanishi Y, Muto M, Suyama A, Hachimura S, Sato R, Takahashi K, Kaminogawa S (2011) Orally administered Bifidobacterium triggers immune responses following capture by CD11c(+) cells in Peyer’s patches and cecal patches. Cytotechnology 63:307–317CrossRefGoogle Scholar
  35. Hori T, Kiyoshima J, Yasui H (2003) Effect of an oral administration of Lactobacillus casei strain Shirota on the natural killer activity of blood mononuclear cells in aged mice. Biosci Biotechnol Biochem 67:420–422CrossRefGoogle Scholar
  36. Inamine A, Sakurai D, Horiguchi S, Yonekura S, Hanazawa T, Hosokawa H, Matuura-Suzuki A, Nakayama T, Okamoto Y (2012) Sublingual administration of Lactobacillus paracasei KW3110 inhibits Th2-dependent allergic responses via upregulation of PD-L2 on dendritic cells. Clin Immunol 143:170–179CrossRefGoogle Scholar
  37. Ivory K, Chambers SJ, Pin C, Prieto E, Arques JL, Nicoletti C (2008) Oral delivery of Lactobacillus casei Shirota modifies allergen-induced immune responses in allergic rhinitis. Clin Exp Allergy 38:1282–1289CrossRefGoogle Scholar
  38. Iwasaki A, Kelsall BL (2001) Unique functions of CD11b+, CD8 alpha+, and double-negative Peyer’s patch dendritic cells. J Immunol 166:4884–4890Google Scholar
  39. Jeal H, Harris J, Draper A, Taylor AN, Jones M (2004) Specific IgG and IgG4 antibodies to rat urinary allergen in sensitized and non-sensitized individuals. J Allergy Clin Immunol 113:S336CrossRefGoogle Scholar
  40. Jeannin P, Renno T, Goetsch L, Miconnet I, Aubry JP, Delneste Y, Herbault N, Baussant T, Magistrelli G, Soulas C, Romero P, Cerottini JC, Bonnefoy JY (2000) OmpA targets dendritic cells, induces their maturation and delivers antigen into the MHC class I presentation pathway. Nat Immunol 1:502–509CrossRefGoogle Scholar
  41. Johnson-Henry KC, Donato KA, Shen-Tu G, Gordanpour M, Sherman PM (2008) Lactobacillus rhamnosus strain GG prevents enterohemorrhagic Escherichia coli O157:H7-induced changes in epithelial barrier function. Infect Immun 76:1340–1348CrossRefGoogle Scholar
  42. Kim JY, Choi YO, Ji GE (2008) Effect of oral probiotics (Bifidobacterium lactis AD011 and Lactobacillus acidophilus AD031) administration on ovalbumin-induced food allergy mouse model. J Microbiol Biotechnol 18:1393–1400Google Scholar
  43. Kirjavainen PV, El-Nezami HS, Salminen SJ, Ahokas JT, Wright PF (1999) The effect of orally administered viable probiotic and dairy lactobacilli on mouse lymphocyte proliferation. FEMS Immunol Med Microbiol 26:131–135CrossRefGoogle Scholar
  44. Korcheva V, Wong J, Corless C, Iordanov M, Magun B (2005) Administration of ricin induces a severe inflammatory response via nonredundant stimulation of ERK, JNK, and P38 MAPK and provides a mouse model of hemolytic uremic syndrome. Am J Pathol 166:323–339CrossRefGoogle Scholar
  45. Lee JW, Shin JG, Kim EH, Kang HE, Yim IB, Kim JY, Joo HG, Woo HJ (2004) Immunomodulatory and antitumor effects in vivo by the cytoplasmic fraction of Lactobacillus casei and Bifidobacterium longum. J Vet Sci 5:41–48Google Scholar
  46. 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 18:2613–2623CrossRefGoogle Scholar
  47. MacDonald TT (2003) The mucosal immune system. Parasite Immunol 25:235–246CrossRefGoogle Scholar
  48. McNeilly TN, Mitchell MC, Nisbet AJ, McAteer S, Erridge C, Inglis NF, Smith DG, Low JC, Gally DL, Huntley JF, Mahajan A (2010) IgA and IgG antibody responses following systemic immunization of cattle with native H7 flagellin differ in epitope recognition and capacity to neutralise TLR5 signalling. Vaccine 28:1412–1421CrossRefGoogle Scholar
  49. Mead PS, Griffin PM (1998) Escherichia coli O157:H7. Lancet 352:1207–1212CrossRefGoogle Scholar
  50. Medeiros KC, Figueiredo CA, Figueredo TB, Freire KR, Santos FA, Alcantara-Neves NM, Silva TM, Piuvezam MR (2008) Anti-allergic effect of bee pollen phenolic extract and myricetin in ovalbumin-sensitized mice. J Ethnopharmacol 119:41–46CrossRefGoogle Scholar
  51. Medellin-Pena MJ, Griffiths MW (2009) Effect of molecules secreted by Lactobacillus acidophilus strain La-5 on Escherichia coli O157:H7 colonization. Appl Environ Microbiol 75:1165–1172CrossRefGoogle Scholar
  52. 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 84:1092–1100CrossRefGoogle Scholar
  53. 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 102:2880–2885CrossRefGoogle Scholar
  54. Mora JR, Iwata M, Eksteen B, Song SY, Junt T, Senman B, Otipoby KL, Yokota A, Takeuchi H, Ricciardi-Castagnoli P, Rajewsky K, Adams DH, von Andrian UH (2006) Generation of gut-homing IgA-secreting B cells by intestinal dendritic cells. Science 314:1157–1160CrossRefGoogle Scholar
  55. Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86:309–317Google Scholar
  56. Nagafuchi S, Takahashi T, Yajima T, Kuwata T, Hirayama K, Itoh K (1999) Strain dependency of the immunopotentiating activity of Lactobacillus delbrueckii subsp. bulgaricus. Biosci Biotechnol Biochem 63:474–479CrossRefGoogle Scholar
  57. Nagano K, Sugisaki T, Taguchi K, Hara T, Naiki M, Mori H (2003) A murine model of enterohemorrhagic Escherichia coli O157:H7 infection to assess immunopotentiating activity of drugs on mucosal immunity: effect of drugs. J Pharmacol Sci 91:219–228CrossRefGoogle Scholar
  58. Nonaka Y, Izumo T, Izumi F, Maekawa T, Shibata H, Nakano A, Kishi A, Akatani K, Kiso Y (2008) 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 145:249–257CrossRefGoogle Scholar
  59. Norderhaug IN, Johansen FE, Schjerven H, Brandtzaeg P (1999) Regulation of the formation and external transport of secretory immunoglobulins. Crit Rev Immunol 19:481–508Google Scholar
  60. Ogawa M, Shimizu K, Nomoto K, Takahashi M, Watanuki M, Tanaka R, Tanaka T, Hamabata T, Yamasaki S, Takeda Y (2001) Protective effect of Lactobacillus casei strain Shirota on Shiga toxin-producing Escherichia coli O157:H7 infection in infant rabbits. Infect Immun 69:1101–1108CrossRefGoogle Scholar
  61. Oliveira M, Bosco N, Perruisseau G, Nicolas J, Segura-Roggero I, Duboux S, Briand M, Blum S, Benyacoub J (2011) Lactobacillus paracasei reduces intestinal inflammation in adoptive transfer mouse model of experimental colitis. Clin Dev Immunol 2011:1–13CrossRefGoogle Scholar
  62. O’Mahony C, Scully P, O’Mahony D, Murphy S, O’Brien F, Lyons A, Sherlock G, MacSharry J, Kiely B, Shanahan F, O’Mahony L (2008) Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 4:e1000112CrossRefGoogle Scholar
  63. Ostberg JR, Dayanc BE, Yuan M, Oflazoglu E, Repasky EA (2007) Enhancement of natural killer (NK) cell cytotoxicity by fever-range thermal stress is dependent on NKG2D function and is associated with plasma membrane NKG2D clustering and increased expression of MICA on target cells. J Leukoc Biol 82:1322–1331CrossRefGoogle Scholar
  64. Pan TM, Chiu CH, Guu YK (2002) Characterization of Lactobacillus isolates from pickled vegetables for use as dietary or pickle adjuncts. Foods Food Ingred J Jpn 206:45–51Google Scholar
  65. Paturi G, Phillips M, Jones M, Kailasapathy K (2007) Immune enhancing effects of Lactobacillus acidophilus LAFTI L10 and Lactobacillus paracasei LAFTI L26 in mice. Int J Food Microbiol 115:115–118CrossRefGoogle Scholar
  66. Peng GC, Hsu CH (2005) The efficacy and safety of heat-killed Lactobacillus paracasei for treatment of perennial allergic rhinitis induced by house-dust mite. Pediatr Allergy Immunol 16:433–438CrossRefGoogle Scholar
  67. Perdigon G, Vintini E, Alvarez S, Medina M, Medici M (1999) Study of the possible mechanisms involved in the mucosal immune system activation by lactic acid bacteria. J Dairy Sci 82:1108–1114CrossRefGoogle Scholar
  68. Perdigon G, Maldonado-Galdeano C, Valdez JC, Medici M (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56(Suppl 4):S21–S26CrossRefGoogle Scholar
  69. Philippe D, Favre L, Foata F, Adolfsson O, Perruisseau-Carrier G, Vidal K, Reuteler G, Dayer-Schneider J, Mueller C, Blum S (2011) Bifidobacterium lactis attenuates onset of inflammation in a murine model of colitis. World J Gastroenterol 17:459–469CrossRefGoogle Scholar
  70. Prioult G, Pecquet S, Fliss I (2004) Stimulation of interleukin-10 production by acidic beta-lactoglobulin-derived peptides hydrolyzed with Lactobacillus paracasei NCC2461 peptidases. Clin Diagn Lab Immunol 11:266–271Google Scholar
  71. Rada V, Rychly I (1995) The effect of Lactobacillus salivarius administration on coliform bacteria and enterococci in the crop and cecum of broiler chickens. Vet Med (Praha) 40:311–315Google Scholar
  72. Re F, Strominger JL (2001) Toll-like receptor 2 (TLR2) and TLR4 differentially activate human dendritic cells. J Biol Chem 276:37692–37699CrossRefGoogle Scholar
  73. Rizzello V, Bonaccorsi I, Dongarra ML, Fink LN, Ferlazzo G (2011) Role of natural killer and dendritic cell crosstalk in immunomodulation by commensal bacteria probiotics. J Biomed Biotechnol 2011:473097CrossRefGoogle Scholar
  74. Segarra-Newnham M (2007) Probiotics for Clostridium difficile-associated diarrhea: focus on Lactobacillus rhamnosus GG and Saccharomyces boulardii. Ann Pharmacother 41:1212–1221CrossRefGoogle Scholar
  75. Shimizu K, Asahara T, Nomoto K, Tanaka R, Hamabata T, Ozawa A, Takeda Y (2003) Development of a lethal Shiga toxin-producing Escherichia coli-infection mouse model using multiple mitomycin C treatment. Microb Pathog 35:1–9CrossRefGoogle Scholar
  76. Sudo N, Sawamura S, Tanaka K, Aiba Y, Kubo C, Koga Y (1997) The requirement of intestinal bacterial flora for the development of an IgE production system fully susceptible to oral tolerance induction. J Immunol 159:1739–1745Google Scholar
  77. Takeda K, Okumura K (2007) Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity. J Nutr 137:791S–793SGoogle Scholar
  78. Takeda K, Suzuki T, Shimada SI, Shida K, Nanno M, Okumura K (2006) Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin Exp Immunol 146:109–115CrossRefGoogle Scholar
  79. Tapping RI, Akashi S, Miyake K, Godowski PJ, Tobias PS (2000) Toll-like receptor 4, but not toll-like receptor 2, is a signaling receptor for Escherichia and Salmonella lipopolysaccharides. J Immunol 165:5780–5787Google Scholar
  80. Tobita K, Yanaka H, Otani H (2010a) Anti-allergic effects of Lactobacillus crispatus KT-11 strain on ovalbumin-sensitized BALB/c mice. Anim Sci J 81:699–705CrossRefGoogle Scholar
  81. Tobita K, Yanaka H, Otani H (2010b) The antiallergic effects and acute toxicity of Lactobacillus crispatus KT-11 cultured in food grade medium. J Agric Food Chem 58:6498–6502CrossRefGoogle Scholar
  82. Tsai YT, Cheng PC, Fan CK, Pan TM (2008) Time-dependent persistence of enhanced immune response by a potential probiotic strain Lactobacillus paracasei subsp. paracasei NTU 101. Int J Food Microbiol 128:219–225CrossRefGoogle Scholar
  83. Tsai YT, Cheng PC, Liao JW, Pan TM (2010a) Effect of the administration of Lactobacillus paracasei subsp. paracasei NTU 101 on Peyer’s patch-mediated mucosal immunity. Int Immunopharmacol 10:791–798CrossRefGoogle Scholar
  84. Tsai YT, Cheng PC, Pan TM (2010b) Immunomodulating activity of Lactobacillus paracasei subsp. paracasei NTU 101 in enterohemorrhagic Escherichia coli O157:H7-infected mice. J Agric Food Chem 58:11265–11272CrossRefGoogle Scholar
  85. Urbanek R, Forster J, Karitzky D, Ziupa J (1981) The prognostic significance of specific IgG antibodies in insect sting allergy. Eur J Pediatr 136:31–34CrossRefGoogle Scholar
  86. Vinderola G, Perdigon G, Duarte J, Farnworth E, Matar C (2006) Effects of the oral administration of the exopolysaccharide produced by Lactobacillus kefiranofaciens on the gut mucosal immunity. Cytokine 36:254–260CrossRefGoogle Scholar
  87. Vizoso Pinto MG, Rodriguez Gomez 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 133:86–93CrossRefGoogle Scholar
  88. Vremec D, Shortman K (1997) Dendritic cell subtypes in mouse lymphoid organs: cross-correlation of surface markers, changes with incubation, and differences among thymus, spleen, and lymph nodes. J Immunol 159:565–573Google Scholar
  89. Yan F, Cao H, Cover TL, Washington MK, Shi Y, Liu L, Chaturvedi R, Peek RM, Wilson KT, Polk DB (2011) Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J Clin Invest 121:2242–2253CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2012

Authors and Affiliations

  1. 1.Department of Biochemical Science and Technology, College of Life ScienceNational Taiwan UniversityTaipeiTaiwan
  2. 2.Department of Parasitology, College of MedicineTaipei Medical UniversityTaipeiTaiwan

Personalised recommendations