Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  López, Patricia ^a,b   González Rodríguez, Irene ^b   Gueimonde, Miguel ^b   Margolles, Abelardo ^b   Suárez, Ana ^a  

^a UNIVERSITY OF OVIEDO   (Spain)

^b DEPARTMENT OF MICROBIOLOGY AND BIOCHEMISTRY OF DAIRY PRODUCTS   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; CYTOKINE; INTERLEUKIN 10; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; BACTERIAL STRAIN; BIFIDOBACTERIUM BIFIDUM; CD4+ T LYMPHOCYTE; CELL DIFFERENTIATION; CELL MATURATION; CELL STIMULATION; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DENDRITIC CELL; IMMUNE RESPONSE; IMMUNOASSAY; MEMORY CELL; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHENOTYPE; PLASTICITY; PROTEIN PROTEIN INTERACTION; PROTEIN SECRETION; REGULATORY T LYMPHOCYTE; TH17 CELL; BIFIDOBACTERIUM; CELL CULTURE; CLASSIFICATION; FLOW CYTOMETRY; HOST PATHOGEN INTERACTION; HUMAN; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; MONOCYTE; MONONUCLEAR CELL; PHYSIOLOGY; SPECIES DIFFERENCE; TH1 CELL; TH2 CELL;

BIFIDOBACTERIUM; BIFIDOBACTERIUM BIFIDUM; BIFIDOBACTERIUM BREVE;

BIFIDOBACTERIUM; CD4-POSITIVE T-LYMPHOCYTES; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; FLOW CYTOMETRY; HOST-PATHOGEN INTERACTIONS; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-10; INTERLEUKIN-17; LEUKOCYTES, MONONUCLEAR; MONOCYTES; SPECIES SPECIFICITY; T-LYMPHOCYTES, REGULATORY; TH1 CELLS; TH17 CELLS; TH2 CELLS; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84857681357     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024776     Document Type: Article

References (72)

1. Reid G, Sanders ME, Gaskins HR, Gibson GR, Mercenier A, et al. (2003) New scientific paradigms for probiotics and prebiotics. J Clin Gastroenterol 37: 105-118.
2. FAO/WHO (2006) Probiotics in food. Health and nutritional properties and guidelines for evaluation. paper 85.
3. Frick JS, Schenk K, Quitadamo M, Kahl F, Koberle M, et al. (2007) Lactobacillus fermentum attenuates the proinflammatory effect of Yersinia enterocolitica on human epithelial cells. Inflamm Bowel Dis 13: 83-90.
4. Guarner F, Malagelada JR, (2003) Bacterial flora of the digestive tract. Gastroenterol Hepatol 26 (Suppl 1): 1-5.
5. Macpherson AJ, Harris NL, (2004) Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4: 478-485.
6. Arboleya S, Ruas-Madiedo P, Margolles A, Solis G, Salminen S, et al. (2010) Characterization and in vitro properties of potentially probiotic Bifidobacterium strains isolated from breast-milk. Int J Food Microbiol 149: 28-36.
7. Gionchetti P, Rizzello F, Venturi A, Brigidi P, Matteuzzi D, et al. (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo-controlled trial. Gastroenterology 119: 305-309.
8. Gionchetti P, Rizzello F, Campieri M, (2001) Probiotics and antibiotics in inflammatory bowel disease. Curr Opin Gastroenterol 17: 331-335.
9. Isolauri E, Juntunen M, Rautanen T, Sillanaukee P, Koivula T, (1991) A human Lactobacillus strain (Lactobacillus casei sp strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88: 90-97.
10. Schultz M, Strauch UG, Linde HJ, Watzl S, Obermeier F, et al. (2004) 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 11: 372-378.
11. Turroni F, van Sinderen D, Ventura M, (2009) Bifidobacteria: from ecology to genomics. Front Biosci 14: 4673-4684.
12. Boirivant M, Strober W, (2007) The mechanism of action of probiotics. Curr Opin Gastroenterol 23: 679-692.
13. Erickson KL, Hubbard NE, (2000) Probiotic immunomodulation in health and disease. J Nutr 130: 403S-409S.
14. Vissers YM, Snel J, Zuurendonk PF, Smit BA, Wichers HJ, et al. (2010) Differential effects of Lactobacillus acidophilus and Lactobacillus plantarum strains on cytokine induction in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 59: 60-70.
15. Rescigno M, Urbano M, Valzasina B, Francolini M, Rotta G, et al. (2001) Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nat Immunol 2: 361-367.
16. Rescigno M, (2008) Intestinal epithelial cells control dendritic cell function. J Pediatr Gastroenterol Nutr 46 (Suppl 1): E17-E19.
17. Westendorf AM, Fleissner D, Hansen W, Buer J, (2010) T cells, dendritic cells and epithelial cells in intestinal homeostasis. Int J Med Microbiol 300: 11-18.
18. Joffre O, Nolte MA, Sporri R, Sousa ReisE, (2009) Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunol Rev 227: 234-247.
19. Lopez P, Gueimonde M, Margolles A, Suarez A, (2010) Distinct Bifidobacterium strains drive different immune responses in vitro. Int J Food Microbiol 138: 157-165.
20. Niers LE, Timmerman HM, Rijkers GT, van Bleek GM, van Uden NO, et al. (2005) Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy 35: 1481-1489.
21. Sousa ReisE, (2006) Dendritic cells in a mature age. Nat Rev Immunol 6: 476-483.
22. Banchereau J, Briere F, Caux C, Davoust J, Lebecque S, et al. (2000) Immunobiology of dendritic cells. Annu Rev Immunol 18: 767-811.
23. Zhu J, Paul WE, (2008) CD4 T cells: fates, functions, and faults. Blood 112: 1557-1569.
24. Christensen HR, Frokiaer H, Pestka JJ, (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168: 171-178.
25. Hart AL, Lammers K, Brigidi P, Vitali B, Rizzello F, et al. (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53: 1602-1609.
26. Mohamadzadeh M, Olson S, Kalina WV, Ruthel G, Demmin GL, et al. (2005) Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc Natl Acad Sci U S A 102: 2880-2885.
27. Smits HH, Engering A, van der Kleij D, de Jong EC, Schipper K, et al. (2005) 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 115: 1260-1267.
28. Dalod M, Salazar-Mather TP, Malmgaard L, Lewis C, Asselin-Paturel C, et al. (2002) Interferon alpha/beta and interleukin 12 responses to viral infections: pathways regulating dendritic cell cytokine expression in vivo. J Exp Med 195: 517-528.
29. Aujla SJ, Dubin PJ, Kolls JK, (2007) Th17 cells and mucosal host defense. Semin Immunol 19: 377-382.
30. Bettelli E, Korn T, Oukka M, Kuchroo VK, (2008) Induction and effector functions of T(H)17 cells. Nature 453: 1051-1057.
31. Dubin PJ, Kolls JK, (2008) Th17 cytokines and mucosal immunity. Immunol Rev 226: 160-171.
32. Ivanov II, Frutos RL, Manel N, Yoshinaga K, Rifkin DB, et al. (2008) Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4: 337-349.
33. Khader SA, Bell GK, Pearl JE, Fountain JJ, Rangel-Moreno J, et al. (2007) IL-23 and IL-17 in the establishment of protective pulmonary CD4+ T cell responses after vaccination and during Mycobacterium tuberculosis challenge. Nat Immunol 8: 369-377.
34. McKenzie BS, Kastelein RA, Cua DJ, (2006) Understanding the IL-23-IL-17 immune pathway. Trends Immunol 27: 17-23.
35. Ouyang W, Kolls JK, Zheng Y, (2008) The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28: 454-467.
36. Zhou L, Lopes JE, Chong MM, Ivanov II, Min R, et al. (2008) TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453: 236-240.
37. Belkaid Y, Rouse BT, (2005) Natural regulatory T cells in infectious disease. Nat Immunol 6: 353-360.
38. Karim M, Kingsley CI, Bushell AR, Sawitzki BS, Wood KJ, (2004) Alloantigen-induced CD25+CD4+ regulatory T cells can develop in vivo from CD25-CD4+ precursors in a thymus-independent process. J Immunol 172: 923-928.
39. Di GC, Marinaro M, Sanchez M, Strober W, Boirivant M, (2005) Probiotics ameliorate recurrent Th1-mediated murine colitis by inducing IL-10 and IL-10-dependent TGF-beta-bearing regulatory cells. J Immunol 174: 3237-3246.
40. Foligne B, Zoumpopoulou G, Dewulf J, Ben YA, Chareyre F, et al. (2007) A key role of dendritic cells in probiotic functionality. PLoS ONE 2: e313.
41. de Roock S, van Elk M, van Dijk ME, Timmerman HM, Rijkers GT, et al. (2010) Lactic acid bacteria differ in their ability to induce functional regulatory T cells in humans. Clin Exp Allergy 40: 103-110.
42. O'Mahony D, Murphy S, Boileau T, Park J, O'Brien F, et al. (2010) Bifidobacterium animalis AHC7 protects against pathogen-induced NF-κB activation in vivo. BMC Immunol 11: 63.
43. Taams LS, Smith J, Rustin MH, Salmon M, Poulter LW, et al. (2001) Human anergic/suppressive CD4(+)CD25(+) T cells: a highly differentiated and apoptosis-prone population. Eur J Immunol 31: 1122-1131.
44. Mazmanian SK, Liu CH, Tzianabos AO, Kasper DL, (2005) An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122: 107-118.
45. Baba N, Samson S, Bourdet-Sicard R, Rubio M, Sarfati M, (2008) Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J Leukoc Biol 84: 468-476.
46. Young SL, Simon MA, Baird MA, Tannock GW, Bibiloni R, et al. (2004) Bifidobacterial species differentially affect expression of cell surface markers and cytokines of dendritic cells harvested from cord blood. Clin Diagn Lab Immunol 11: 686-690.
47. Zeuthen LH, Christensen HR, Frokiaer H, (2006) 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 13: 365-375.
48. De Smedt T, Van Mechelen M, De Becker G, Urbain J, Leo O, et al. (1997) Effect of interleukin-10 on dendritic cell maturation and function. Eur J Immunol 27: 1229-1235.
49. Annunziato F, Cosmi L, Liotta F, Maggi E, Romagnani S, (2008) The phenotype of human Th17 cells and their precursors, the cytokines that mediate their differentiation and the role of Th17 cells in inflammation. Int Immunol 20: 1361-1368.
50. Mills KH, (2008) Induction, function and regulation of IL-17-producing T cells. Eur J Immunol 38: 2636-2649.
51. Wilson NJ, Boniface K, Chan JR, McKenzie BS, Blumenschein WM, et al. (2007) Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol 8: 950-957.
52. Medina M, Izquierdo E, Ennahar S, Sanz Y, (2007) Differential immunomodulatory properties of Bifidobacterium logum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol 150: 531-538.
53. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, et al. (2006) The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126: 1121-1133.
54. Yang XO, Nurieva R, Martinez GJ, Kang HS, Chung Y, et al. (2008) Molecular antagonism and plasticity of regulatory and inflammatory T cell programs. Immunity 29: 44-56.
55. Lochner M, Peduto L, Cherrier M, Sawa S, Langa F, et al. (2008) In vivo equilibrium of proinflammatory IL-17+ and regulatory IL-10+ Foxp3+ RORgamma t+ T cells. J Exp Med 205: 1381-1393.
56. Ayyoub M, Deknuydt F, Raimbaud I, Dousset C, Leveque L, et al. (2009) Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t. Proc Natl Acad Sci U S A 106: 8635-8640.
57. Valmori D, Raffin C, Raimbaud I, Ayyoub M, (2010) Human RORgammat+ TH17 cells preferentially differentiate from naive FOXP3+Treg in the presence of lineage-specific polarizing factors. Proc Natl Acad Sci U S A 107: 19402-19407.
58. Esposito M, Ruffini F, Bergami A, Garzetti L, Borsellino G, et al. (2010) IL-17- and IFN-gamma-secreting Foxp3+ T cells infiltrate the target tissue in experimental autoimmunity. J Immunol 185: 7467-7473.
59. Fontenot JD, Gavin MA, Rudensky AY, (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4: 330-336.
60. Pillai V, Ortega SB, Wang CK, Karandikar NJ, (2007) Transient regulatory T-cells: a state attained by all activated human T-cells. Clin Immunol 123: 18-29.
61. Tran DQ, Ramsey H, Shevach EM, (2007) Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype. Blood 110: 2983-2990.
62. Kwon HK, Lee CG, So JS, Chae CS, Hwang JS, et al. (2010) Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc Natl Acad Sci U S A 107: 2159-2164.
63. Lavasani S, Dzhambazov B, Nouri M, Fak F, Buske S, et al. (2010) A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS ONE 5: e9009.
64. Beriou G, Costantino CM, Ashley CW, Yang L, Kuchroo VK, et al. (2009) IL-17-producing human peripheral regulatory T cells retain suppressive function. Blood 113: 4240-4249.
65. Zhu J, Paul WE, (2010) Heterogeneity and plasticity of T helper cells. Cell Res 20: 4-12.
66. Strauch UG, Obermeier F, Grunwald N, Gurster S, Dunger N, et al. (2005) Influence of intestinal bacteria on induction of regulatory T cells: lessons from a transfer model of colitis. Gut 54: 1546-1552.
67. Round JL, Mazmanian SK, (2010) Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci U S A 107: 12204-12209.
68. Garrigues C, Stuer-Lauridsen B, Johansen E, (2005) Characterisation of Bifidobacterium animalis subsp. lactis BB-12 and other probiotic bacteria using genomics, transcriptomics and proteomics. Aust J Dairy Technol 60: 84-92.
69. Turroni F, Bottacini F, Foroni E, Mulder I, Kim JH, et al. (2010) Genome analysis of Bifidobacterium bifidum PRL2010 reveals metabolic pathways for host-derived glycan foraging. Proc Natl Acad Sci U S A 107: 19514-19519.
70. Ruas-Madiedo P, Gueimonde M, Fernández-García M, de los Reyes-Gavilán CG, Margolles A, (2008) Mucin degradation by Bifidobacterium strains isolated from the human intestinal microbiota. Appl Environ Microbiol 74: 1936-1940.
71. Sakata S, Ryu CS, Kitahara M, Sakamoto M, Hayashi H, et al. (2006) Characterization of the genus Bifidobacterium by automated ribotyping and 16S rRNA gene sequences. Microbiol Immunol 50: 1-10.
72. Chalova VI, Lingbeck JM, Kwon YM, Ricke SC, (2008) Extracellular antimutagenic activities of selected probiotic Bifidobacterium and Lactobacillus spp. as a function of growth phase. J Environ Sci Health B 43: 193-198.