T cell polarizing properties of probiotic bacteria

Immunology Letters

Volumn 168, Issue 2, 2015, Pages 337-342

  Barberi, Chiara ^a   Campana, Stefania ^a   De Pasquale, Claudia ^a   Rabbani Khorasgani, Mohammad ^b   Ferlazzo, Guido ^a,c   Bonaccorsi, Irene ^a,c  

^a UNIVERSITY OF MESSINA   (Italy)

^b UNIVERSITY OF ISFAHAN   (Iran)

^c UNIVERSITY OF MESSINA   (Italy)

Author keywords

Dendritic cells; Inflammatory bowel diseases; Probiotic bacteria; T cell polarization

Indexed keywords

CD103 ANTIGEN; CD11B ANTIGEN; CHEMOKINE RECEPTOR CX3CR1; GAMMA INTERFERON; GLYCOPROTEIN P 15095; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 12P70; PROBIOTIC AGENT; CYTOKINE;

ALLERGY; ANTIGEN PRESENTING CELL; BACTERIAL STRAIN; BACTERIUM; BIFIDOBACTERIUM; CELLULAR IMMUNITY; DENDRITIC CELL; GUT MICROENVIRONMENT; HOMEOSTASIS; IMMUNE RESPONSE; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE FLORA; LACTOBACILLUS JOHNSONII; LACTOBACILLUS RHAMNOSUS; LYMPHOCYTE ACTIVATION; LYMPHOID CELL; MICROENVIRONMENT; MONOCYTE; NATURAL KILLER CELL; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; REVIEW; T LYMPHOCYTE; TH1 CELL; TH2 CELL; BIOLOGICAL MODEL; CLASSIFICATION; HUMAN; IMMUNOLOGY; LACTOBACILLUS; METABOLISM;

BACTERIA; CYTOKINES; DENDRITIC CELLS; GASTROINTESTINAL MICROBIOME; HUMANS; LACTOBACILLUS; LYMPHOCYTE ACTIVATION; MODELS, IMMUNOLOGICAL; PROBIOTICS; T-LYMPHOCYTES;

EID: 84949553233     PISSN: 01652478     EISSN: 18790542     Source Type: Journal    
DOI: 10.1016/j.imlet.2015.11.005     Document Type: Review

References (77)

1. Macpherson A.J., Harris N.L. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 2004, 4:478-485.
2. Mowat A.M. Anatomical basis of tolerance and immunity to intestinal antigens. Nat. Rev. Immunol. 2003, 3:331-341.
3. Xavier R.J., Podolsky D.K. Unravelling the pathogenesis of inflammatory bowel disease. Nature 2007, 448:427-434.
4. Meresse B., Ripoche J., Heyman M., Cerf-Bensussan N. Celiac disease: from oral tolerance to intestinal inflammation, autoimmunity and lymphomagenesis. Mucosal Immunol. 2009, 2:8-23.
5. Rescigno M. Intestinal microbiota and its effects on the immune system. Cell Microbiol. 2014, 16:1004-1013.
6. Rimoldi M., Chieppa M., Salucci V., Avogadri F., Sonzogni A., Sampietro G.M., Nespoli A., Viale G., Allavena P., Rescigno M. Intestinal immune homeostasis is regulated by the crosstalk between epithelial cells and dendritic cells. Nat. Immunol. 2005, 6:507-514.
7. Schulz O., Jaensson E., Persson E.K., Liu X., Worbs T., Agace W.W., Pabst O. Intestinal CD103+, but not CX3CR1+, antigen sampling cells migrate in lymph and serve classical dendritic cell functions. J. Exp. Med. 2009, 206:3101-3114.
8. Mazzini E., Massimiliano L., Penna G., Rescigno M. Oral tolerance can be established via gap junction transfer of fed antigens from CX3CR1(+) macrophages to CD103(+) dendritic cells. Immunity 2014, 40:248-261.
9. Reis e Sousa C. Activation of dendritic cells: translating innate into adaptive immunity. Curr. Opin. Immunol. 2004, 16:21-25.
10. Report of a Joint FAO/WHOWorking group, Guidelines for evaluation of probiotics in food, London, Ontario, Canada: FAO/ WHO, (2002).
11. Fuller R. Probiotics in man and animals. J. Appl. Bacteriol. 1989, 66:365-378.
12. Walter J. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research. Appl. Environ. Microbiol. 2008, 74:4985-4996.
13. Guarner F., Malagelada J.R. Gut flora in health and disease. Lancet 2003, 361:512-519.
14. Vanderpool C., Yan F., Polk D.B. Mechanisms of probiotic action: implications for therapeutic applications in inflammatory bowel diseases. Inflamm. Bowel Dis. 2008, 14:1585-1596.
15. Corthesy B., Gaskins H.R., Mercenier A. Cross-talk between probiotic bacteria and the host immune system. J. Nutr. 2007, 137:781S-790S.
16. Christensen H.R., Frokiaer H., Pestka J.J. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 2002, 168:171-178.
17. Zeuthen L.H., Christensen H.R., Frokiaer 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.
18. Fink L.N., Zeuthen L.H., Ferlazzo G., Frokiaer 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.
19. Latvala S., Pietila T.E., Veckman V., Kekkonen R.A., Tynkkynen S., Korpela R., Julkunen I. Potentially probiotic bacteria induce efficient maturation but differential cytokine production in human monocyte-derived dendritic cells. World J. Gastroenterol. 2008, 14:5570-5583. discussion 5581-5572.
20. Mohamadzadeh M., Olson S., Kalina W.V., Ruthel G., Demmin G.L., Warfield K.L., Bavari S., Klaenhammer T.R. Lactobacilli activate human dendritic cells that skew T cells toward T helper 1 polarization. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:2880-2885.
21. Rizzello V., Bonaccorsi I., Dongarra M.L., Fink L.N., Ferlazzo G. Role of natural killer and dendritic cell crosstalk in immunomodulation by commensal bacteria probiotics. J. Biomed. Biotechnol. 2011, 2011. 473097.
22. Rivollier A., He J., Kole A., Valatas V., Kelsall B.L. Inflammation switches the differentiation program of Ly6Chi monocytes from antiinflammatory macrophages to inflammatory dendritic cells in the colon. J. Exp. Med. 2012, 209:139-155.
23. Zigmond E., Varol C., Farache J., Elmaliah E., Satpathy A.T., Friedlander G., Mack M., Shpigel N., Boneca I.G., Murphy K.M., Shakhar G., Halpern Z., Jung S. Ly6C hi monocytes in the inflamed colon give rise to proinflammatory effector cells and migratory antigen-presenting cells. Immunity 2012, 37:1076-1090.
24. Hadis U., Wahl B., Schulz O., Hardtke-Wolenski M., Schippers A., Wagner N., Muller W., Sparwasser T., Forster R., Pabst O. Intestinal tolerance requires gut homing and expansion of FoxP3+ regulatory T cells in the lamina propria. Immunity 2011, 34:237-246.
25. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., Liu K., Jakubzick C., Ingersoll M.A., Leboeuf M., Stanley E.R., Nussenzweig M., Lira S.A., Randolph G.J., Merad M. Origin of the lamina propria dendritic cell network. Immunity 2009, 31:513-525.
26. Dongarra M.L., Rizzello V., Muccio L., Fries W., Cascio A., Bonaccorsi I., Ferlazzo G. Mucosal immunology and probiotics. Curr. Allergy Asthma Rep. 2013, 13:19-26.
27. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., Vyas J.M., Boes M., Ploegh H.L., Fox J.G., Littman D.R., Reinecker H.C. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005, 307:254-258.
28. Farache J., Koren I., Milo I., Gurevich I., Kim K.W., Zigmond E., Furtado G.C., Lira S.A., Shakhar G. Luminal bacteria recruit CD103+ dendritic cells into the intestinal epithelium to sample bacterial antigens for presentation. Immunity 2013, 38:581-595.
29. Di Sabatino A., Pickard K.M., Gordon J.N., Salvati V., Mazzarella G., Beattie R.M., Vossenkaemper A., Rovedatti L., Leakey N.A., Croft N.M., Troncone R., Corazza G.R., Stagg A.J., Monteleone G., MacDonald T.T. Evidence for the role of interferon-alfa production by dendritic cells in the Th1 response in celiac disease. Gastroenterology 2007, 133:1175-1187.
30. Wendland M., Czeloth N., Mach N., Malissen B., Kremmer E., Pabst O., Forster R. CCR9 is a homing receptor for plasmacytoid dendritic cells to the small intestine. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:6347-6352.
31. Raki M., Beitnes A.C., Lundin K.E., Jahnsen J., Jahnsen F.L., Sollid L.M. Plasmacytoid dendritic cells are scarcely represented in the human gut mucosa and are not recruited to the celiac lesion. Mucosal Immunol. 2013, 6:985-992.
32. Bonaccorsi I., Morandi B., Antsiferova O., Costa G., Oliveri D., Conte R., Pezzino G., Vermiglio G., Anastasi G.P., Navarra G., Munz C., Di Carlo E., Mingari M.C., Ferlazzo G. Membrane transfer from tumor cells overcomes deficient phagocytic ability of plasmacytoid dendritic cells for the acquisition and presentation of tumor antigens. J. Immunol. 2014, 192:824-832.
33. Bonaccorsi I., Pezzino G., Morandi B., Ferlazzo G. Drag cells in immunity: plasmacytoid DCs dress up as cancer cells. Oncoimmunology 2014, 3:e28184.
34. Fuchs A., Cella M., Kondo T., Colonna M. Paradoxic inhibition of human natural interferon-producing cells by the activating receptor NKp44. Blood 2005, 106:2076-2082.
35. Bonaccorsi I., Cantoni C., Carrega P., Oliveri D., Lui G., Conte R., Navarra M., Cavaliere R., Traggiai E., Gattorno M., Martini A., Mingari M.C., Moretta A., Ferlazzo G. The immune inhibitory receptor LAIR-1 is highly expressed by plasmacytoid dendritic cells and acts complementary with NKp44 to control IFNalpha production. PLoS One 2010, 5:e15080.
36. Martin-Fontecha A., Thomsen L.L., Brett S., Gerard C., Lipp M., Lanzavecchia A., Sallusto F. Induced recruitment of NK cells to lymph nodes provides IFN-gamma for T(H) 1 priming. Nat. Immunol. 2004, 5:1260-1265.
37. Ferlazzo G., Pack M., Thomas D., Paludan C., Schmid D., Strowig T., Bougras G., Muller W.A., Moretta L., Munz C. Distinct roles of IL-12 and IL-15 in human natural killer cell activation by dendritic cells from secondary lymphoid organs. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:16606-16611.
38. Spits H., Cupedo T. Innate lymphoid cells: emerging insights in development, lineage relationships, and function. Annu. Rev. Immunol. 2012, 30:647-675.
39. Sonnenberg G.F., Artis D. Innate lymphoid cell interactions with microbiota: implications for intestinal health and disease. Immunity 2012, 37:601-610.
40. Carrega P., Loiacono F., Carlo E.D., Scaramuccia A., Mora M., Conte R., Benelli R., Spaggiari G.M., Cantoni C., Campana S., Bonaccorsi I., Morandi B., Truini M., Mingari M.C., Moretta L., Ferlazzo G. NCR+ILC3 concentrate in human lung cancer and associate with intratumoral lymphoid structures. Nat. Commun. 2015, 6:8280.
41. Buonocore S., Ahern P.P., Uhlig H.H., Ivanov I.I., Littman D.R., Maloy K.J., Powrie F. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology. Nature 2010, 464:1371-1375.
42. Hepworth M.R., Monticelli L.A., Fung T.C., Ziegler C.G., Grunberg S., Sinha R., Mantegazza A.R., Ma H.L., Crawford A., Angelosanto J.M., Wherry E.J., Koni P.A., Bushman F.D., Elson C.O., Eberl G., Artis D., Sonnenberg G.F. Innate lymphoid cells regulate CD4+ T-cell responses to intestinal commensal bacteria. Nature 2013, 498:113-117.
43. Rescigno M., Di Sabatino A. Dendritic cells in intestinal homeostasis and disease. J. Clin. Invest. 2009, 119:2441-2450.
44. Iwasaki A., Kelsall B.L. Freshly isolated Peyer's patch, but not spleen, dendritic cells produce interleukin 10 and induce the differentiation of T helper type 2 cells. J. Exp. Med. 1999, 190:229-240.
45. Everson M.P., Lemak D.G., McDuffie D.S., Koopman W.J., McGhee J.R., Beagley K.W. Dendritic cells from Peyer's patch and spleen induce different T helper cell responses. J. Interferon Cytokine Res. 1998, 18:103-115.
46. Lipscomb M.F., Masten B.J. Dendritic cells: immune regulators in health and disease. Physiol. Rev. 2002, 82:97-130.
47. Semper A.E., Hartley J.A. Dendritic cells in the lung: what is their relevance to asthma?. Clin. Exp. Allergy 1996, 26:485-490.
48. Novak N., Haberstok J., Geiger E., Bieber T. Dendritic cells in allergy. Allergy 1999, 54:792-803.
49. Bonaccorsi I., De Pasquale C., Campana S., Barberi C., Cavaliere R., Benedetto F., Ferlazzo G. Natural killer cells in the innate immunity network of atherosclerosis. Immunol. Lett. 2015, 168:51-57.
50. Brand S. Crohn's disease: Th1, Th17 or both? The change of a paradigm: new immunological and genetic insights implicate Th17 cells in the pathogenesis of Crohn's disease. Gut 2009, 58:1152-1167.
51. Kobayashi T., Okamoto S., Hisamatsu T., Kamada N., Chinen H., Saito R., Kitazume M.T., Nakazawa A., Sugita A., Koganei K., Isobe K., Hibi T. IL23 differentially regulates the Th1/Th17 balance in ulcerative colitis and Crohn's disease. Gut 2008, 57:1682-1689.
52. Galvez J. Role of Th17Cells in the pathogenesis of human IBD. ISRN Inflamm. 2014, 2014. 928461.
53. Robinson D.S., Kay A.B. Role of Th1 and Th2 cells in human allergic disorders. Chem. Immunol. 1996, 63:187-203.
54. Weiss G., Christensen H.R., Zeuthen L.H., Vogensen F.K., Jakobsen M., Frokiaer H. Lactobacilli and bifidobacteria induce differential interferon-beta profiles in dendritic cells. Cytokine 2011, 56:520-530.
55. Baba N., Samson S., Bourdet-Sicard R., Rubio M., Sarfati M. Commensal bacteria trigger a full dendritic cell maturation program that promotes the expansion of non-Tr1 suppressor T cells. J. Leukoc. Biol. 2008, 84:468-476.
56. Hessle C., Hanson L.A., Wold A.E. Lactobacilli from human gastrointestinal mucosa are strong stimulators of IL-12 production. Clin. Exp. Immunol. 1999, 116:276-282.
57. Kato I., Tanaka K., Yokokura T. Lactic acid bacterium potently induces the production of interleukin-12 and interferon-gamma by mouse splenocytes. Int. J. Immunopharmacol. 1999, 21:121-131.
58. Shida K., Makino K., Morishita A., Takamizawa K., Hachimura S., Ametani A., Sato T., Kumagai Y., Habu S., Kaminogawa S. Lactobacillus casei inhibits antigen-induced IgE secretion through regulation of cytokine production in murine splenocyte cultures. Int. Arch. Allergy Immunol. 1998, 115:278-287.
59. Morita H., He F., Fuse T., Ouwehand A.C., Hashimoto H., Hosoda M., Mizumachi K., Kurisaki J. Cytokine production by the murine macrophage cell line J774.1 after exposure to lactobacilli. Biosci. Biotechnol. Biochem. 2002, 66:1963-1966.
60. Chuang L., Wu K.G., Pai C., Hsieh P.S., Tsai J.J., Yen J.H., Lin M.Y. Heat-killed cells of lactobacilli skew the immune response toward T helper 1 polarization in mouse splenocytes and dendritic cell-treated T cells. J. Agric. Food. Chem. 2007, 55:11080-11086.
61. Braat H., de J., ong E.C., van, den B., rande J.M., Kapsenberg M.L., Peppelenbosch M.P., van T., ol E.A., van D., eventer S.J. Dichotomy between Lactobacillus rhamnosus and Klebsiella pneumoniae on dendritic cell phenotype and function. J. Mol. Med. (Berl.) 2004, 82:197-205.
62. Veckman V., Miettinen M., Pirhonen J., Siren 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.
63. Veckman V., Miettinen M., Matikainen S., Lande R., Giacomini E., Coccia E.M., Julkunen I. Lactobacilli and streptococci induce inflammatory chemokine production in human macrophages that stimulates Th1 cell chemotaxis. J. Leukoc. Biol. 2003, 74:395-402.
64. Marcinkiewicz J., Ciszek M., Bobek M., Strus M., Heczko P.B., Kurnyta M., Biedron R., Chmielarczyk A. Differential inflammatory mediator response in vitro from murine macrophages to lactobacilli and pathogenic intestinal bacteria. Int. J. Exp. Pathol. 2007, 88:155-164.
65. Amar Y., Rizzello V., Cavaliere R., Campana S., De Pasquale C., Barberi C., Oliveri D., Pezzino G., Costa G., Meddah A.T., Ferlazzo G., Bonaccorsi I. Divergent signaling pathways regulate IL-12 production induced by different species of Lactobacilli in human dendritic cells. Immunol. Lett. 2015, 166:6-12.
66. 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.
67. Grangette C., Nutten S., Palumbo E., Morath S., Hermann C., Dewulf J., Pot B., Hartung T., Hols P., Mercenier A. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:10321-10326.
68. 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-beta-bearing regulatory cells. J. Immunol. 2005, 174:3237-3246.
69. Kalliomaki 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.
70. Pessi T., Sutas Y., Hurme M., Isolauri E. Interleukin-10 generation in atopic children following oral Lactobacillus rhamnosus GG. Clin Exp Allergy 2000, 30:1804-1808.
71. Rembacken B.J., Snelling A.M., Hawkey P.M., Chalmers D.M., Axon A.T. Non-pathogenic E. coli versus mesalazine for the treatment of ulcerative colitis: a randomised trial. Lancet 1999, 354:635-639.
72. Kruis W., Fric P., Pokrotnieks J., Lukas M., Fixa B., Kascak M., Kamm M.A., Weismueller J., Beglinger C., Stolte M., Wolff C., Schulze J. Maintaining remission of ulcerative colitis with the probiotic E. coli Nissle 1917 is as effective as with standard mesalazine. Gut 2004, 53:1617-1623.
73. Bousvaros A., Guandalini S., Baldassano R.N., Botelho C., Evans J., Ferry G.D., Goldin B., Hartigan L., Kugathasan S., Levy J., Murray K.F., Oliva-Hemker M., Rosh J.R., Tolia V., Zholudev A., Vanderhoof J.A., Hibberd P.L. A randomized, double-blind trial of Lactobacillus GG versus placebo in addition to standard maintenance therapy for children with Crohn's disease. Inflamm. Bowel Dis. 2005, 11:833-839.
74. Marteau P., Lemann M., Seksik P., Laharie D., Colombel J.F., Bouhnik Y., Cadiot G., Soule J.C., Bourreille A., Metman E., Lerebours E., Carbonnel F., Dupas J.L., Veyrac M., Coffin B., Moreau J., Abitbol V., Blum-Sperisen S., Mary J.Y. Ineffectiveness of Lactobacillus johnsonii LA1 for prophylaxis of postoperative recurrence in Crohn's disease: a randomised, double blind, placebo controlled GETAID trial. Gut 2006, 55:842-847.
75. Prantera C., Scribano M.L., Falasco G., Andreoli A., Luzi C. Ineffectiveness of probiotics in preventing recurrence after curative resection for Crohn's disease: a randomised controlled trial with Lactobacillus GG. Gut 2002, 51:405-409.
76. Bonaccorsi I., Pezzino G., Morandi B., Ferlazzo G. Novel perspectives on dendritic cell-based immunotherapy of cancer. Immunol. Lett. 2013, 155:6-10.
77. Morandi B., Bonaccorsi I., Mesiti M., Conte R., Carrega P., Costa G., Iemmo R., Martini S., Ferrone S., Cantoni C., Mingari M.C., Moretta L., Ferlazzo G. Characterization of human afferent lymph dendritic cells from seroma fluids. J Immunol. 2013, 191:4858-4866.