Microbiotal influence on T cell subset development

Seminars in Immunology

Volumn 23, Issue 2, 2011, Pages 146-153

  Atarashi, Koji ^a   Umesaki, Yoshinori ^b   Honda, Kenya ^a,c  

^a UNIVERSITY OF TOKYO   (Japan)

^b YAKULT CENTRAL INSTITUTE FOR MICROBIOLOGICAL RESEARCH   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

Microbial flora; Segmented filamentous bacteria; Th17; Treg

Indexed keywords

ENTERITIS; HUMAN; INTESTINE FLORA; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE SUBPOPULATION; TH17 CELL;

ANIMALS; CELL DIFFERENTIATION; HUMANS; INTESTINES; RECEPTORS, ANTIGEN, T-CELL, GAMMA-DELTA; T-LYMPHOCYTE SUBSETS; TH17 CELLS;

EID: 79953164640     PISSN: 10445323     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.smim.2011.01.010     Document Type: Review

References (95)

1. Berg R.D. The indigenous gastrointestinal microflora. Trends Microbiol 1996, 4:430-435.
2. Boudeau J., Glasser A.L., Masseret E., Joly B., Darfeuille-Michaud A. Invasive ability of an Escherichia coli strain isolated from the ileal mucosa of a patient with Crohn's disease. Infect Immun 1999, 67:4499-4509.
3. Giaffer M.H., Holdsworth C.D., Duerden B.I. The assessment of faecal flora in patients with inflammatory bowel disease by a simplified bacteriological technique. J Med Microbiol 1991, 35:238-243.
4. Frank D.N., St Amand A.L., Feldman R.A., Boedeker E.C., Harpaz N., Pace N.R. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci USA 2007, 104:13780-13785.
5. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L.G., Gratadoux J.J., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc Natl Acad Sci USA 2008, 105:16731-16736.
6. Garrett W.S., Lord G.M., Punit S., Lugo-Villarino G., Mazmanian S.K., Ito S., et al. Communicable ulcerative colitis induced by T-bet deficiency in the innate immune system. Cell 2007, 131:33-45.
7. Garrett W.S., Gallini C.A., Yatsunenko T., Michaud M., DuBois A., Delaney M.L., et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microb 2010, 8:292-300.
8. Bouskra D., Brezillon C., Berard M., Werts C., Varona R., Boneca I.G., et al. Lymphoid tissue genesis induced by commensals through NOD1 regulates intestinal homeostasis. Nature 2008, 456:507-510.
9. Cash H.L., Whitham C.V., Behrendt C.L., Hooper L.V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 2006, 313:1126-1130.
10. 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.
11. Brandl K., Plitas G., Mihu C.N., Ubeda C., Jia T., Fleisher M., et al. Vancomycin-resistant enterococci exploit antibiotic-induced innate immune deficits. Nature 2008, 455:804-807.
12. Hooper L.V., Stappenbeck T.S., Hong C.V., Gordon J.I. Angiogenins: a new class of microbicidal proteins involved in innate immunity. Nat Immunol 2003, 4:269-273.
13. 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.
14. Lee J., Mo J.H., Katakura K., Alkalay I., Rucker A.N., Liu Y.T., et al. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat Cell Biol 2006, 8:1327-1336.
15. Satoh-Takayama N., Vosshenrich C.A., Lesjean-Pottier S., Sawa S., Lochner M., Rattis F., et al. Microbial flora drives interleukin 22 production in intestinal NKp46+ cells that provide innate mucosal immune defense. Immunity 2008, 29:958-970.
16. Sanos S.L., Bui V.L., Mortha A., Oberle K., Heners C., Johner C., et al. RORgammat and commensal microflora are required for the differentiation of mucosal interleukin 22-producing NKp46+ cells. Nat Immunol 2009, 10:83-91.
17. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., et al. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 2006, 126:1121-1133.
18. Littman D.R., Rudensky A.Y. Th17 and regulatory T cells in mediating and restraining inflammation. Cell 2010, 140:845-858.
19. Korn T., Bettelli E., Oukka M., Kuchroo V.K. IL-17 and Th17 cells. Annu Rev Immunol 2009, 27:485-517.
20. Mitsdoerffer M., Lee Y., Jager A., Kim H.J., Korn T., Kolls J.K., et al. Proinflammatory T helper type 17 cells are effective B-cell helpers. Proc Natl Acad Sci USA 2010, 107:14292-14297.
21. Kolls J.K., McCray P.B., Chan Y.R. Cytokine-mediated regulation of antimicrobial proteins. Nat Rev Immunol 2008, 8:829-835.
22. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., et al. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 2006, 441:231-234.
23. Conti H.R., Shen F., Nayyar N., Stocum E., Sun J.N., Lindemann M.J., et al. Th17 cells and IL-17 receptor signaling are essential for mucosal host defense against oral candidiasis. J Exp Med 2009, 206:299-311.
24. Ishigame H., Kakuta S., Nagai T., Kadoki M., Nambu A., Komiyama Y., et al. Differential roles of interleukin-17A and -17F in host defense against mucoepithelial bacterial infection and allergic responses. Immunity 2009, 30:108-119.
25. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., et al. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat Immunol 2007, 8:967-974.
26. Zhou L., Lopes J.E., Chong M.M., Ivanov I.I., Min R., Victora G.D., et al. TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 2008, 453:236-240.
27. Yang X.O., Pappu B.P., Nurieva R., Akimzhanov A., Kang H.S., Chung Y., et al. T helper 17 lineage differentiation is programmed by orphan nuclear receptors ROR alpha and ROR gamma. Immunity 2008, 28:29-39.
28. Veldhoen M., Hirota K., Westendorf A.M., Buer J., Dumoutier L., Renauld J.C., et al. The aryl hydrocarbon receptor links TH17-cell-mediated autoimmunity to environmental toxins. Nature 2008, 453:106-109.
29. Schraml B.U., Hildner K., Ise W., Lee W.L., Smith W.A., Solomon B., et al. The AP-1 transcription factor Batf controls T(H)17 differentiation. Nature 2009, 460:405-409.
30. Locke N.R., Patterson S.J., Hamilton M.J., Sly L.M., Krystal G., Levings M.K. SHIP regulates the reciprocal development of T regulatory and Th17 cells. J Immunol 2009, 183:975-983.
31. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 2007, 448:484-487.
32. McGeachy M.J., Bak-Jensen K.S., Chen Y., Tato C.M., Blumenschein W., McClanahan T., et al. TGF-beta and IL-6 drive the production of IL-17 and IL-10 by T cells and restrain T(H)-17 cell-mediated pathology. Nat Immunol 2007, 8:1390-1397.
33. Duerr R.H., Taylor K.D., Brant S.R., Rioux J.D., Silverberg M.S., Daly M.J., et al. A genome-wide association study identifies IL23R as an inflammatory bowel disease gene. Science 2006, 314:1461-1463.
34. Chung Y., Chang S.H., Martinez G.J., Yang X.O., Nurieva R., Kang H.S., et al. Critical regulation of early Th17 cell differentiation by interleukin-1 signaling. Immunity 2009, 30:576-587.
35. Meng G., Zhang F., Fuss I., Kitani A., Strober W. A mutation in the Nlrp3 gene causing inflammasome hyperactivation potentiates Th17 cell-dominant immune responses. Immunity 2009, 30:860-874.
36. Manel N., Unutmaz D., Littman D.R. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 2008, 9:641-649.
37. Yang L., Anderson D.E., Baecher-Allan C., Hastings W.D., Bettelli E., Oukka M., et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature 2008, 454:350-352.
38. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., et al. ATP drives lamina propria T(H)17 cell differentiation. Nature 2008, 455:808-812.
39. Ivanov I.I., Frutos Rde L., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microb 2008, 4:337-349.
40. Hall J.A., Bouladoux N., Sun C.M., Wohlfert E.A., Blank R.B., Zhu Q., et al. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 2008, 29:637-649.
41. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishiyama M., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat Immunol 2008, 9:769-776.
42. Torchinsky M.B., Garaude J., Martin A.P., Blander J.M. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 2009, 458:78-82.
43. Wen L., Ley R.E., Volchkov P.Y., Stranges P.B., Avanesyan L., Stonebraker A.C., et al. Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature 2008, 455:1109-1113.
44. Iwase T., Shinji H., Tajima A., Sato F., Tamura T., Iwamoto T., et al. Isolation and identification of ATP-secreting bacteria from mice and humans. J Clin Microbiol 2010, 48:1949-1951.
45. Khakh B.S., North R.A. P2X receptors as cell-surface ATP sensors in health and disease. Nature 2006, 442:527-532.
46. Mariathasan S., Weiss D.S., Newton K., McBride J., O'Rourke K., Roose-Girma M., et al. Cryopyrin activates the inflammasome in response to toxins and ATP. Nature 2006, 440:228-232.
47. Li M.O., Flavell R.A. TGF-beta: a master of all T cell trades. Cell 2008, 134:392-404.
48. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat Immunol 2007, 8:1086-1094.
49. Niess J.H., Brand S., Gu X., Landsman L., Jung S., McCormick B.A., et al. CX3CR1-mediated dendritic cell access to the intestinal lumen and bacterial clearance. Science 2005, 307:254-258.
50. Ivanov I.I., Atarashi K., Manel N., Brodie E.L., Shima T., Karaoz U., et al. Induction of intestinal Th17 cells by segmented filamentous bacteria. Cell 2009, 139:485-498.
51. Davis C.P., Savage D.C. Effect of penicillin on the succession, attachment, and morphology of segmented, filamentous microbes in the murine small bowel. Infect Immun 1976, 13:180-188.
52. Klaasen H.L., Koopman J.P., Van den Brink M.E., Bakker M.H., Poelma F.G., Beynen A.C. Intestinal, segmented, filamentous bacteria in a wide range of vertebrate species. Lab Anim 1993, 27:141-150.
53. Umesaki Y., Setoyama H. Structure of the intestinal flora responsible for development of the gut immune system in a rodent model. Microbes Infect 2000, 2:1343-1351.
54. Heczko U., Abe A., Finlay B.B. Segmented filamentous bacteria prevent colonization of enteropathogenic Escherichia coli O103 in rabbits. J Infect Dis 2000, 181:1027-1033.
55. Talham G.L., Jiang H.Q., Bos N.A., Cebra J.J. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect Immun 1999, 67:1992-2000.
56. Umesaki Y., Setoyama H., Matsumoto S., Imaoka A., Itoh K. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect Immun 1999, 67:3504-3511.
57. Gaboriau-Routhiau V., Rakotobe S., Lecuyer E., Mulder I., Lan A., Bridonneau C., et al. The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity 2009, 31:677-689.
58. Salzman N.H., Hung K., Haribhai D., Chu H., Karlsson-Sjoberg J., Amir E., et al. Enteric defensins are essential regulators of intestinal microbial ecology. Nat Immunol 2010, 11:76-83.
59. Wu S., Rhee K.J., Albesiano E., Rabizadeh S., Wu X., Yen H.R., et al. A human colonic commensal promotes colon tumorigenesis via activation of T helper type 17 T cell responses. Nat Med 2009, 15:1016-1022.
60. Wu H.J., Ivanov I.I., Darce J., Hattori K., Shima T., Umesaki Y., et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 2010, 32:815-827.
61. Lee Y.K., Menezes J.S., Umesaki Y., Mazmanian S.K. Microbes and Health Sackler Colloquium: proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci USA 2010.
62. Sakaguchi S., Yamaguchi T., Nomura T., Ono M. Regulatory T cells and immune tolerance. Cell 2008, 133:775-787.
63. Koch M.A., Tucker-Heard G., Perdue N.R., Killebrew J.R., Urdahl K.B., Campbell D.J. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009, 10:595-602.
64. Zheng Y., Chaudhry A., Kas A., deRoos P., Kim J.M., Chu T.T., et al. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 2009, 458:351-356.
65. Chaudhry A., Rudra D., Treuting P., Samstein R.M., Liang Y., Kas A., et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 2009, 326:986-991.
66. Tsuji M., Komatsu N., Kawamoto S., Suzuki K., Kanagawa O., Honjo T., et al. Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches. Science 2009, 323:1488-1492.
67. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., et al. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 2007, 204:1757-1764.
68. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., et al. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 2007, 317:256-260.
69. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., et al. 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.
70. Maynard C.L., Harrington L.E., Janowski K.M., Oliver J.R., Zindl C.L., Rudensky A.Y., et al. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat Immunol 2007, 8:931-941.
71. Rubtsov Y.P., Rasmussen J.P., Chi E.Y., Fontenot J., Castelli L., Ye X., et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008, 28:546-558.
72. Apetoh L., Quintana F.J., Pot C., Joller N., Xiao S., Kumar D., et al. The aryl hydrocarbon receptor interacts with c-Maf to promote the differentiation of type 1 regulatory T cells induced by IL-27. Nat Immunol 2010, 11:854-861.
73. Manicassamy S., Reizis B., Ravindran R., Nakaya H., Salazar-Gonzalez R.M., Wang Y.C., et al. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 2010, 329:849-853.
74. 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.
75. Karimi K., Inman M.D., Bienenstock J., Forsythe P. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med 2009, 179:186-193.
76. Livingston M., Loach D., Wilson M., Tannock G.W., Baird M. Gut commensal Lactobacillus reuteri 100-23 stimulates an immunoregulatory response. Immunol Cell Biol 2010, 88:99-102.
77. 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.
78. Foligne B., Zoumpopoulou G., Dewulf J., Ben Younes A., Chareyre F., Sirard J.C., et al. A key role of dendritic cells in probiotic functionality. PLoS One 2007, 2:e313.
79. Forsythe P., Inman M.D., 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.
80. O'Mahony C., Scully P., O'Mahony D., Murphy S., O'Brien F., Lyons A., et al. Commensal-induced regulatory T cells mediate protection against pathogen-stimulated NF-kappaB activation. PLoS Pathog 2008, 4:e1000112.
81. Maslowski K.M., Vieira A.T., Ng A., Kranich J., Sierro F., Yu D., et al. Regulation of inflammatory responses by gut microbiota and chemoattractant receptor GPR43. Nature 2009, 461:1282-1286.
82. Round J.L., Mazmanian S.K. Inducible Foxp3+ regulatory T-cell development by a commensal bacterium of the intestinal microbiota. Proc Natl Acad Sci USA 2010, 107:12204-12209.
83. Bauer S., Groh V., Wu J., Steinle A., Phillips J.H., Lanier L.L., et al. Activation of NK cells and T cells by NKG2D, a receptor for stress-inducible MICA. Science 1999, 285:727-729.
84. Das G., Augustine M.M., Das J., Bottomly K., Ray P., Ray A. An important regulatory role for CD4+CD8 alpha alpha T cells in the intestinal epithelial layer in the prevention of inflammatory bowel disease. Proc Natl Acad Sci USA 2003, 100:5324-5329.
85. Ismail A.S., Behrendt C.L., Hooper L.V. Reciprocal interactions between commensal bacteria and gamma delta intraepithelial lymphocytes during mucosal injury. J Immunol 2009, 182:3047-3054.
86. Momose Y., Maruyama A., Iwasaki T., Miyamoto Y., Itoh K. 16S rRNA gene sequence-based analysis of clostridia related to conversion of germfree mice to the normal state. J Appl Microbiol 2009, 107:2088-2097.
87. Lockhart E., Green A.M., Flynn J.L. IL-17 production is dominated by gammadelta T cells rather than CD4 T cells during Mycobacterium tuberculosis infection. J Immunol 2006, 177:4662-4669.
88. Shibata K., Yamada H., Hara H., Kishihara K., Yoshikai Y. Resident Vdelta1+ gammadelta T cells control early infiltration of neutrophils after Escherichia coli infection via IL-17 production. J Immunol 2007, 178:4466-4472.
89. Martin B., Hirota K., Cua D.J., Stockinger B., Veldhoen M. Interleukin-17-producing gammadelta T cells selectively expand in response to pathogen products and environmental signals. Immunity 2009, 31:321-330.
90. Awasthi A., Riol-Blanco L., Jager A., Korn T., Pot C., Galileos G., et al. Cutting edge: IL-23 receptor gfp reporter mice reveal distinct populations of IL-17-producing cells. J Immunol 2009, 182:5904-5908.
91. Sutton C.E., Lalor S.J., Sweeney C.M., Brereton C.F., Lavelle E.C., Mills K.H. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity 2009, 31:331-341.
92. Duan J., Chung H., Troy E., Kasper D.L. Microbial colonization drives expansion of IL-1 receptor 1-expressing and IL-17-producing gamma/delta T cells. Cell Host Microb 2010, 7:140-150.
93. Cua D.J., Tato C.M. Innate IL-17-producing cells: the sentinels of the immune system. Nat Rev Immunol 2010, 10:479-489.
94. Ito Y., Usui T., Kobayashi S., Iguchi-Hashimoto M., Ito H., Yoshitomi H., et al. Gamma/delta T cells are the predominant source of interleukin-17 in affected joints in collagen-induced arthritis, but not in rheumatoid arthritis. Arthritis Rheum 2009, 60:2294-2303.
95. Petermann F., Rothhammer V., Claussen M.C., Haas J.D., Blanco L.R., Heink S., et al. gammadelta T cells enhance autoimmunity by restraining regulatory T cell responses via an interleukin-23-dependent mechanism. Immunity 2010, 33:351-363.