Cellular and molecular pathways through which commensal bacteria modulate sensitization to dietary antigens

Current Opinion in Immunology

Volumn 31, Issue , 2014, Pages 79-86

  Feehley, Taylor ^a   Nagler, Cathryn R ^a  

^a UNIVERSITY OF CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; FOOD ANTIGEN; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3;

ANTIGEN PRESENTING CELL; BACTERIAL COLONIZATION; BASOPHIL; CELL INTERACTION; COMMENSAL; COMMENSAL BACTERIA; DENDRITIC CELL; DISEASE ASSOCIATION; FOOD ALLERGY; HUMAN; IMMUNE RESPONSE; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; LYMPHOID CELL; MOLECULAR MECHANICS; NATURAL KILLER CELL; NONHUMAN; ORGANISMAL INTERACTION; PROTEIN EXPRESSION; REGULATORY MECHANISM; REVIEW; SENSITIZATION; SIGNAL TRANSDUCTION; ANIMAL; BACTERIUM; DIET; GENETICS; GENOTYPE ENVIRONMENT INTERACTION; HOMEOSTASIS; IMMUNOLOGY; MICROBIOLOGY; MICROFLORA; PATHOGENICITY;

ANIMALS; BACTERIA; DIET; FOOD HYPERSENSITIVITY; GENE-ENVIRONMENT INTERACTION; HOMEOSTASIS; HUMANS; MICROBIOTA;

EID: 84908311837     PISSN: 09527915     EISSN: 18790372     Source Type: Journal    
DOI: 10.1016/j.coi.2014.10.001     Document Type: Review

References (81)

1. Strachan D.P. Hay fever, hygiene, and household size. BMJ 1989, 299:1259-1260.
2. The Human Microbiome Project Consortium: structure, function and diversity of the healthy human microbiome. Nature 2012, 486:207-214.
3. Feehley T., Stefka A.T., Cao S., Nagler C.R. Microbial regulation of allergic responses to food. Semin Immunopathol 2012, 34:671-688.
4. Bashir M.E., Louie S., Shi H.N., Nagler-Anderson C. Toll-like receptor 4 signaling by intestinal microbes influences susceptibility to food allergy. J Immunol 2004, 172:6978-6987.
5. Cahenzli J., Köller Y., Wyss M., Geuking Markus B., McCoy Kathy D. Intestinal microbial diversity during early-life colonization shapes long-term IgE levels. Cell Host Microbe 2013, 14:559-570.
6. Stefka A.T., Feehley T., Tripathi P., Qiu J., McCoy K., Mazmanian S.K., Tjota M.Y., Seo G.-Y., Cao S., Theriault B.R., et al. Commensal bacteria protect against food allergen sensitization. Proc Natl Acad Sci USA 2014, 111:13145-13150.
7. Noval Rivas M., Burton O.T., Wise P., Zhang Y.Q., Hobson S.A., Garcia Lloret M., Chehoud C., Kuczynski J., DeSantis T., Warrington J., et al. A microbiota signature associated with experimental food allergy promotes allergic sensitization and anaphylaxis. J Allergy Clin Immunol 2013, 131:201-212.
8. Turner J.R. Intestinal mucosal barrier function in health and disease. Nat Rev Immunol 2009, 9:799-809.
9. Otte J.M., Cario E., Podolsky D.K. Mechanisms of cross hyporesponsiveness to Toll-like receptor bacterial ligands in intestinal epithelial cells. Gastroenterology 2004, 126:1054-1070.
10. Abreu M.T., Arnold E.T., Thomas L.S., Gonsky R., Zhou Y., Hu B., Arditi M. TLR-4 and MD-2 expression is regulated by immune-mediated signals in human intestinal epithelial cells. J Biol Chem 2002, 277:20431-20437.
11. Bambou J.C., Giraud A., Menard S., Begue B., Rakotobe S., Heyman M., Taddei F., Cerf-Bensussan N., Gaboriau-Routhiau V. In vitro and ex vivo activation of the TLR5 signaling pathway in intestinal epithelial cells by a commensal Escherichia coli strain. J Biol Chem 2004, 279:42984-42992.
12. Gribar S.C., Richardson W.M., Sodhi C.P., Hackam D.J. No longer an innocent bystander: epithelial toll-like receptor signaling in the development of mucosal inflammation. Mol Med 2008, 14:645-659.
13. Neal M.D., Leaphart C., Levy R., Prince J., Billiar T.R., Watkins S., Li J., Cetin S., Ford H., Schreiber A., et al. Enterocyte TLR4 mediates phagocytosis and translocation of bacteria across the intestinal barrier. J Immunol 2006, 176:3070-3079.
14. Shang L., Fukata M., Thirunarayanan N., Martin A.P., Arnaboldi P., Maussang D., Berin C., Unkeless J.C., Mayer L., Abreu M.T., et al. Toll-like receptor signaling in small intestinal epithelium promotes B-cell recruitment and IgA production in lamina propria. Gastroenterology 2008, 135:529-538.
15. Vora P., Youdim A., Thomas L.S., Fukata M., Tesfay S.Y., Lukasek K., Michelsen K.S., Wada A., Hirayama T., Arditi M., et al. Beta-defensin-2 expression is regulated by TLR signaling in intestinal epithelial cells. J Immunol 2004, 173:5398-5405.
16. Prescott D., Lee J., Philpott D.J. An epithelial armamentarium to sense the microbiota. Semin Immunol 2013, 25:323-333.
17. Neutra M.R., Mantis N.J., Frey A., Giannasca P.J. The composition and function of M cell apical membranes: implications for microbial pathogenesis. Semin Immunol 1999, 11:171-181.
18. Neutra M.R., Mantis N.J., Kraehenbuhl J.P. Collaboration of epithelial cells with organized mucosal lymphoid tissues. Nat Immunol 2001, 2:1004-1009.
19. + dendritic cells in the small intestine. Nature 2012, 483:345-349.
20. Knoop K.A., Miller M.J., Newberry R.D. Transepithelial antigen delivery in the small intestine: different paths, different outcomes. Curr Opin Gastroenterol 2013, 29:112-118.
21. Vaishnava S., Behrendt C.L., Ismail A.S., Eckmann L., Hooper L.V. Paneth cells directly sense gut commensals and maintain homeostasis at the intestinal host-microbial interface. Proc Natl Acad Sci USA 2008, 105:20858-20863.
22. Vaishnava S., Yamamoto M., Severson K.M., Ruhn K.A., Yu X., Koren O., Ley R., Wakeland E.K., Hooper L.V. The antibacterial lectin RegIIIgamma promotes the spatial segregation of microbiota and host in the intestine. Science 2011, 334:255-258.
23. Brandl K., Plitas G., Schnabl B., DeMatteo R.P., Pamer E.G. MyD88-mediated signals induce the bactericidal lectin RegIII gamma and protect mice against intestinal Listeria monocytogenes infection. J Exp Med 2007, 204:1891-1900.
24. Nava G.M., Stappenbeck T.S. Diversity of the autochthonous colonic microbiota. Gut Microbes 2011, 2:99-104.
25. Nava G.M., Friedrichsen H.J., Stappenbeck T.S. Spatial organization of intestinal microbiota in the mouse ascending colon. ISME J 2011, 5:627-638.
26. Sabat R., Ouyang W., Wolk K. Therapeutic opportunities of the IL-22-IL-22R1 system. Nat Rev Drug Discov 2014, 13:21-38.
27. + innate lymphoid cells. Immunology 2011, 132:453-465.
28. Sonnenberg G.F., Fouser L.A., Artis D. Border patrol: regulation of immunity, inflammation and tissue homeostasis at barrier surfaces by IL-22. Nat Immunol 2011, 12:383-390.
29. Bogunovic M., Ginhoux F., Helft J., Shang L., Hashimoto D., Greter M., Liu K., Jakubzick C., Ingersoll M.A., Leboeuf M., et al. Origin of the lamina propria dendritic cell network. Immunity 2009, 31:513-525.
30. + dendritic cells display unique functional properties that are conserved between mice and humans. J Exp Med 2008, 205:2139-2149.
31. + dendritic cells in the regulation of tissue-selective T cell homing. J Exp Med 2005, 202:1063-1073.
32. + regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007, 204:1757-1764.
33. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., Belkaid Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J Exp Med 2007, 204:1775-1785.
34. +) T cell effector responses via retinoic acid receptor alpha. Immunity 2011, 34:435-447.
35. Chu D.K., Jimenez-Saiz R., Verschoor C.P., Walker T.D., Goncharova S., Llop-Guevara A., Shen P., Gordon M.E., Barra N.G., Bassett J.D., et al. Indigenous enteric eosinophils control DCs to initiate a primary Th2 immune response in vivo. J Exp Med 2014, 211:1657-1672.
36. +) dendritic cells in response to bacterial flagellin enhances mucosal innate immune defense. Immunity 2012, 36:276-287.
37. Chieppa M., Rescigno M., Huang A.Y., Germain R.N. 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.
38. Niess J.H., Adler G. Enteric flora expands gut lamina propria CX3CR1+ dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J Immunol 2010, 184:2026-2037.
39. + macrophages to CD103+ dendritic cells. Immunity 2014, 40:248-261.
40. + regulatory T cells in the lamina propria. Immunity 2011, 34:237-246.
41. 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.
42. hi cells. Nature 2013, 494:116-120.
43. Monticelli L.A., Sonnenberg G.F., Artis D. Innate lymphoid cells: critical regulators of allergic inflammation and tissue repair in the lung. Curr Opin Immunol 2012, 24:284-289.
44. Sanos S.L., Diefenbach A. Innate lymphoid cells: from border protection to the initiation of inflammatory diseases. Immunol Cell Biol 2013, 91:215-224.
45. + T-cell responses to intestinal commensal bacteria. Nature 2013, 498:113-117.
46. Rutz S., Eidenschenk C., Ouyang W. IL-22, not simply a Th17 cytokine. Immunol Rev 2013, 252:116-132.
47. Mielke L.A., Jones S.A., Raverdeau M., Higgs R., Stefanska A., Groom J.R., Misiak A., Dungan L.S., Sutton C.E., Streubel G., et al. Retinoic acid expression associates with enhanced IL-22 production by gammadelta T cells and innate lymphoid cells and attenuation of intestinal inflammation. J Exp Med 2013, 210:1117-1124.
48. Mortha A., Chudnovskiy A., Hashimoto D., Bogunovic M., Spencer S.P., Belkaid Y., Merad M. Microbiota-dependent crosstalk between macrophages and ILC3 promotes intestinal homeostasis. Science 2014, 343:1477-1487.
49. Rakoff-Nahoum S., Medzhitov R. Innate immune recognition of the indigenous microbial flora. Mucosal Immunol 2008, 1:S10-S14.
50. Kamdar K., Nguyen V., DePaolo R.W. Toll-like receptor signaling and regulation of intestinal immunity. Virulence 2013, 4:207-212.
51. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 2004, 118:229-241.
52. Crellin N.K., Trifari S., Kaplan C.D., Satoh-Takayama N., Di Santo J.P., Spits H. Regulation of cytokine secretion in human CD127+ LTi-like innate lymphoid cells by Toll-like receptor 2. Immunity 2010, 33:752-764.
53. Round J.L., Lee S.M., Li J., Tran G., Jabri B., Chatila T.A., Mazmanian S.K. The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science 2011, 332:974-977.
54. Han D., Walsh Matthew C., Cejas Pedro J., Dang Nicholas N., Kim Youngmi F., Kim J., Charrier-Hisamuddin L., Chau L., Zhang Q., Bittinger K., et al. Dendritic cell expression of the signaling molecule TRAF6 is critical for gut microbiota-dependent immune tolerance. Immunity 2013, 38:1211-1222.
55. Varol C., Vallon-Eberhard A., Elinav E., Aychek T., Shapira Y., Luche H., Fehling H.J., Hardt W.D., Shakhar G., Jung S. Intestinal lamina propria dendritic cell subsets have different origin and functions. Immunity 2009, 31:502-512.
56. Mandal P. Dioxin: a review of its environmental effects and its aryl hydrocarbon receptor biology. J Comp Physiol B 2005, 175:221-230.
57. Frericks M., Meissner M., Esser C. Microarray analysis of the AHR system: tissue-specific flexibility in signal and target genes. Toxicol Appl Pharmacol 2007, 220:320-332.
58. Qiu J., Heller J.J., Guo X., Chen Z.M., Fish K., Fu Y.X., Zhou L. The aryl hydrocarbon receptor regulates gut immunity through modulation of innate lymphoid cells. Immunity 2012, 36:92-104.
59. Veldhoen M., Hirota K., Westendorf A.M., Buer J., Dumoutier L., Renauld J.C., Stockinger B. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008, 453:106-109.
60. Stockinger B., Meglio P.D., Gialitakis M., Duarte J.H. The aryl hydrocarbon receptor: multitasking in the immune system. Ann Rev Immunol 2014, 32:403-432.
61. Bjeldanes L.F., Kim J.Y., Grose K.R., Bartholomew J.C., Bradfield C.A. Aromatic hydrocarbon responsiveness-receptor agonists generated from indole-3-carbinol in vitro and in vivo: comparisons with 2,3,7,8-tetrachlorodibenzo-p-dioxin. Proc Natl Acad Sci USA 1991, 88:9543-9547.
62. Qiu J., Guo X., Chen Z.M., He L., Sonnenberg G.F., Artis D., Fu Y.X., Zhou L. Group 3 innate lymphoid cells inhibit T-cell-mediated intestinal inflammation through aryl hydrocarbon receptor signaling and regulation of microflora. Immunity 2013, 39:386-399.
63. Schulz V.J., Smit J.J., Willemsen K.J., Fiechter D., Hassing I., Bleumink R., Boon L., van den Berg M., van Duursen M.B., Pieters R.H. Activation of the aryl hydrocarbon receptor suppresses sensitization in a mouse peanut allergy model. Toxicol Sci 2011, 123:491-500.
64. + regulatory T cells. Toxicol Lett 2012, 215:100-109.
65. Schulz V.J., van Roest M., Bol-Schoenmakers M., van Duursen M.B.M., van den Berg M., Pieters R.H.H., Smit J.J. Aryl hydrocarbon receptor activation affects the dendritic cell phenotype and function during allergic sensitization. Immunobiology 2013, 218:1055-1062.
66. De Filippo C., Cavalieri D., Di Paola M., Ramazzotti M., Poullet J.B., Massart S., Collini S., Pieraccini G., Lionetti P. Impact of diet in shaping gut microbiota revealed by a comparative study in children from Europe and rural Africa. Proc Natl Acad Sci USA 2010, 107:14691-14696.
67. Tan J., McKenzie C., Potamitis M., Thorburn A.N., Mackay C.R., Macia L. The role of short-chain fatty acids in health and disease. Adv Immunol 2014, 121:91-119.
68. Brestoff J.R., Artis D. Commensal bacteria at the interface of host metabolism and the immune system. Nat Immunol 2013, 14:676-684.
69. Ganapathy V., Thangaraju M., Gopal E., Martin P., Itagaki S., Miyauchi S., Prasad P. Sodium-coupled monocarboxylate transporters in normal tissues and in cancer. AAPS J 2008, 10:193-199.
70. Waldecker M., Kautenburger T., Daumann H., Busch C., Schrenk D. Inhibition of histone-deacetylase activity by short-chain fatty acids and some polyphenol metabolites formed in the colon. J Nutr Biochem 2008, 19:587-593.
71. Brown A.J., Goldsworthy S.M., Barnes A.A., Eilert M.M., Tcheang L., Daniels D., Muir A.I., Wigglesworth M.J., Kinghorn I., Fraser N.J., et al. The orphan G protein-coupled receptors GPR41 and GPR43 are activated by propionate and other short chain carboxylic acids. J Biol Chem 2003, 278:11312-11319.
72. Thangaraju M., Cresci G.A., Liu K., Ananth S., Gnanaprakasam J.P., Browning D.D., Mellinger J.D., Smith S.B., Digby G.J., Lambert N.A., et al. GPR109A Is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res 2009, 69:2826-2832.
73. Singh N., Gurav A., Sivaprakasam S., Brady E., Padia R., Shi H., Thangaraju M., Prasad P.D., Manicassamy S., Munn D.H., et al. Activation of gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 2014, 40:128-139.
74. Furusawa Y., Obata Y., Fukuda S., Endo T.A., Nakato G., Takahashi D., Nakanishi Y., Uetake C., Kato K., Kato T., et al. Commensal microbe-derived butyrate induces differentiation of colonic regulatory T cells. Nature 2013, 504:446-450.
75. Arpaia N., Campbell C., Fan X., Dikiy S., van der Veeken J., deRoos P., Liu H., Cross J.R., Pfeffer K., Coffer P.J., et al. Metabolites produced by commensal bacteria promote peripheral regulatory T cell generation. Nature 2013, 504:451-455.
76. Smith P.M., Howitt M.R., Panikov N., Michaud M., Gallini C.A., Bohlooly Y.M., Glickman J.N., Garrett W.S. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science 2013, 341:569-573.
77. Trompette A., Gollwitzer E.S., Yadava K., Sichelstiel A.K., Sprenger N., Ngom-Bru C., Blanchard C., Junt T., Nicod L.P., Harris N.L., et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat Med 2014, 20:159-166.
78. Berni Canani R., Nocerino R., Terrin G., Coruzzo A., Cosenza L., Leone L., Troncone R. Effect of Lactobacillus GG on tolerance acquisition in infants with cow's milk allergy: a randomized trial. J Allergy Clin Immunol 2012, 129:580-582.
79. Berni Canani R, Stefka AT, Khan AA, Nocerino R. Aitoro R, Patton TJ, Calignano A, Meli R, Mattace Raso G, Simeoli R, et al.: Lactobacillus rhamnosus GG supplemented formula expands butyrate producing bacteria in cow's milk allergic infants, submitted for publication.
80. Hill D.A., Siracusa M.C., Abt M.C., Kim B.S., Kobuley D., Kubo M., Kambayashi T., Larosa D.F., Renner E.D., Orange J.S., et al. Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat Med 2012, 18:538-546.
81. Olszak T., An D., Zeissig S., Vera M.P., Richter J., Franke A., Glickman J.N., Siebert R., Baron R.M., Kasper D.L., et al. Microbial exposure during early life has persistent effects on natural killer T cell function. Science 2012, 336:489-493.