Specific Microbiota Direct the Differentiation of IL-17-Producing T-Helper Cells in the Mucosa of the Small Intestine

Cell Host and Microbe

Volumn 4, Issue 4, 2008, Pages 337-349

  Ivanov, Ivaylo I ^a   Frutos, Rosa de Llanos ^b   Manel, Nicolas ^a   Yoshinaga, Keiji ^a   Rifkin, Daniel B ^a   Sartor, R Balfour ^c   Finlay, B Brett ^b   Littman, Dan R ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

CELLIMMUNO; MICROBIO

Indexed keywords

ANTIBIOTIC AGENT; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 23; TOLL LIKE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ARTICLE; BACTERIAL COLONIZATION; BACTEROIDETES; COMMENSAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOPHAGA; ENTERITIS; FLAVOBACTERIA; HELPER CELL; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INTESTINE FLORA; LAMINA PROPRIA; LYMPHOCYTE COUNT; LYMPHOCYTE DIFFERENTIATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION;

ANIMALS; ANTI-BACTERIAL AGENTS; BACTERIA; CELL DIFFERENTIATION; INTERLEUKIN-17; INTESTINAL MUCOSA; INTESTINE, SMALL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MUCOUS MEMBRANE; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY;

ANIMALIA; BACTEROIDETES; CYTOPHAGA; FLAVOBACTER; MUS;

EID: 53349173070     PISSN: 19313128     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.chom.2008.09.009     Document Type: Article

References (48)

1. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., et al. ATP drives lamina propria T(H)17 cell differentiation. Nature (2008) 10.1038/nature07240 Published online August 20, 2008
2. Aujla S.J., Dubin P.J., and Kolls J.K. Th17 cells and mucosal host defense. Semin. Immunol. 19 (2007) 377-382
3. Aujla S.J., Chan Y.R., Zheng M., Fei M., Askew D.J., Pociask D.A., Reinhart T.A., McAllister F., Edeal J., Gaus K., et al. IL-22 mediates mucosal host defense against Gram-negative bacterial pneumonia. Nat. Med. 14 (2008) 275-281
4. Backhed F., Ley R.E., Sonnenburg J.L., Peterson D.A., and Gordon J.I. Host-bacterial mutualism in the human intestine. Science 307 (2005) 1915-1920
5. Bettelli E., Carrier Y., Gao W., Korn T., Strom T.B., Oukka M., Weiner H.L., and Kuchroo V.K. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441 (2006) 235-238
6. Bettelli E., Oukka M., and Kuchroo V.K. T(H)-17 cells in the circle of immunity and autoimmunity. Nat. Immunol. 8 (2007) 345-350
7. Coombes J.L., Robinson N.J., Maloy K.J., Uhlig H.H., and Powrie F. Regulatory T cells and intestinal homeostasis. Immunol. Rev. 204 (2005) 184-194
8. Coquet J.M., Chakravarti S., Smyth M.J., and Godfrey D.I. Cutting edge: IL-21 is not essential for Th17 differentiation or experimental autoimmune encephalomyelitis. J. Immunol. 180 (2008) 7097-7101
9. Denning T.L., Wang Y.C., Patel S.R., Williams I.R., and Pulendran B. Lamina propria macrophages and dendritic cells differentially induce regulatory and interleukin 17-producing T cell responses. Nat. Immunol. 8 (2007) 1086-1094
10. Dewhirst F.E., Chien C.C., Paster B.J., Ericson R.L., Orcutt R.P., Schauer D.B., and Fox J.G. Phylogeny of the defined murine microbiota: altered Schaedler flora. Appl. Environ. Microbiol. 65 (1999) 3287-3292
11. Eberl G., Marmon S., Sunshine M.J., Rennert P.D., Choi Y., and Littman D.R. An essential function for the nuclear receptor RORgamma(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5 (2004) 64-73
12. Elson C.O., Cong Y., McCracken V.J., Dimmitt R.A., Lorenz R.G., and Weaver C.T. Experimental models of inflammatory bowel disease reveal innate, adaptive, and regulatory mechanisms of host dialogue with the microbiota. Immunol. Rev. 206 (2005) 260-276
13. Fujiwara D., Wei B., Presley L.L., Brewer S., McPherson M., Lewinski M.A., Borneman J., and Braun J. Systemic control of plasmacytoid dendritic cells by CD8+ T cells and commensal microbiota. J. Immunol. 180 (2008) 5843-5852
14. He B., Xu W., Santini P.A., Polydorides A.D., Chiu A., Estrella J., Shan M., Chadburn A., Villanacci V., Plebani A., et al. Intestinal bacteria trigger T cell-independent immunoglobulin A(2) class switching by inducing epithelial-cell secretion of the cytokine APRIL. Immunity 26 (2007) 812-826
15. Ivanov I.I., McKenzie B.S., Zhou L., Tadokoro C.E., Lepelley A., Lafaille J.J., Cua D.J., and Littman D.R. The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell 126 (2006) 1121-1133
16. Ivanov I.I., Zhou L., and Littman D.R. Transcriptional regulation of Th17 cell differentiation. Semin. Immunol. 19 (2007) 409-417
17. Jensen K.D., Su X., Shin S., Li L., Youssef S., Yamasaki S., Steinman L., Saito T., Locksley R.M., Davis M.M., et al. Thymic Selection Determines gammadelta T Cell Effector Fate: Antigen-Naive Cells Make Interleukin-17 and Antigen-Experienced Cells Make Interferon gamma. Immunity 29 (2008) 90-100
18. Kelsall B.L., and Leon F. Involvement of intestinal dendritic cells in oral tolerance, immunity to pathogens, and inflammatory bowel disease. Immunol. Rev. 206 (2005) 132-148
19. Khader S.A., Bell G.K., Pearl J.E., Fountain J.J., Rangel-Moreno J., Cilley G.E., Shen F., Eaton S.M., Gaffen S.L., Swain S.L., et al. 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 (2007) 369-377
20. Korn T., Bettelli E., Gao W., Awasthi A., Jager A., Strom T.B., Oukka M., and Kuchroo V.K. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature 448 (2007) 484-487
21. Langrish C.L., Chen Y., Blumenschein W.M., Mattson J., Basham B., Sedgwick J.D., McClanahan T., Kastelein R.A., and Cua D.J. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201 (2005) 233-240
22. Ley R.E., Hamady M., Lozupone C., Turnbaugh P.J., Ramey R.R., Bircher J.S., Schlegel M.L., Tucker T.A., Schrenzel M.D., Knight R., et al. Evolution of Mammals and Their Gut Microbes. Science 320 (2008) 1647-1651
23. Lupp C., Robertson M.L., Wickham M.E., Sekirov I., Champion O.L., Gaynor E.C., and Finlay B.B. Host-mediated inflammation disrupts the intestinal microbiota and promotes the overgrowth of Enterobacteriaceae. Cell Host Microbe 2 (2007) 119-129
24. Macpherson A.J., and Harris N.L. Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4 (2004) 478-485
25. Mangan P.R., Harrington L.E., O'Quinn D.B., Helms W.S., Bullard D.C., Elson C.O., Hatton R.D., Wahl S.M., Schoeb T.R., and Weaver C.T. Transforming growth factor-beta induces development of the T(H)17 lineage. Nature 441 (2006) 231-234
26. Mazmanian S.K., Liu C.H., Tzianabos A.O., and Kasper D.L. An immunomodulatory molecule of symbiotic bacteria directs maturation of the host immune system. Cell 122 (2005) 107-118
27. Mazmanian S.K., Round J.L., and Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453 (2008) 620-625
28. McKenzie B.S., Kastelein R.A., and Cua D.J. Understanding the IL-23-IL-17 immune pathway. Trends Immunol. 27 (2006) 17-23
29. Mebius R.E. Organogenesis of lymphoid tissues. Nat. Rev. Immunol. 3 (2003) 292-303
30. Mucida D., Park Y., Kim G., Turovskaya O., Scott I., Kronenberg M., and Cheroutre H. Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid. Science 317 (2007) 256-260
31. Nurieva R., Yang X.O., Martinez G., Zhang Y., Panopoulos A.D., Ma L., Schluns K., Tian Q., Watowich S.S., Jetten A.M., et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448 (2007) 480-483
32. Ouyang W., Kolls J.K., and Zheng Y. The biological functions of T helper 17 cell effector cytokines in inflammation. Immunity 28 (2008) 454-467
33. Rakoff-Nahoum S., Paglino J., Eslami-Varzaneh F., Edberg S., and Medzhitov R. Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118 (2004) 229-241
34. Sartor R.B. Microbial influences in inflammatory bowel diseases. Gastroenterology 134 (2008) 577-594
35. Sonderegger I., Kisielow J., Meier R., King C., and Kopf M. IL-21 and IL-21R are not required for development of Th17 cells and autoimmunity in vivo. Eur. J. Immunol. 38 (2008) 1833-1838
36. Stockinger B., and Veldhoen M. Differentiation and function of Th17 T cells. Curr. Opin. Immunol. 19 (2007) 281-286
37. Strober W., Fuss I., and Mannon P. The fundamental basis of inflammatory bowel disease. J. Clin. Invest. 117 (2007) 514-521
38. Talham G.L., Jiang H.Q., Bos N.A., and Cebra J.J. Segmented filamentous bacteria are potent stimuli of a physiologically normal state of the murine gut mucosal immune system. Infect. Immun. 67 (1999) 1992-2000
39. Travis M.A., Reizis B., Melton A.C., Masteller E., Tang Q., Proctor J.M., Wang Y., Bernstein X., Huang X., Reichardt L.F., et al. Loss of integrin alpha(v)beta8 on dendritic cells causes autoimmunity and colitis in mice. Nature 449 (2007) 361-365
40. Uematsu S., Fujimoto K., Jang M.H., Yang B.G., Jung Y.J., Nishiyama M., Sato S., Tsujimura T., Yamamoto M., Yokota Y., et al. Regulation of humoral and cellular gut immunity by lamina propria dendritic cells expressing Toll-like receptor 5. Nat. Immunol. 9 (2008) 769-776
41. Umesaki Y., Setoyama H., Matsumoto S., Imaoka A., and Itoh K. Differential roles of segmented filamentous bacteria and clostridia in development of the intestinal immune system. Infect. Immun. 67 (1999) 3504-3511
42. Veldhoen M., Hocking R.J., Atkins C.J., Locksley R.M., and Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity 24 (2006) 179-189
43. Weaver C.T., Harrington L.E., Mangan P.R., Gavrieli M., and Murphy K.M. Th17: an effector CD4 T cell lineage with regulatory T cell ties. Immunity 24 (2006) 677-688
44. Weaver C.T., Hatton R.D., Mangan P.R., and Harrington L.E. IL-17 family cytokines and the expanding diversity of effector T cell lineages. Annu. Rev. Immunol. 25 (2007) 821-852
45. Yang X.O., Panopoulos A.D., Nurieva R., Chang S.H., Wang D., Watowich S.S., and Dong C. STAT3 regulates cytokine-mediated generation of inflammatory helper T cells. J. Biol. Chem. 282 (2007) 9358-9363
46. Zheng Y., Valdez P.A., Danilenko D.M., Hu Y., Sa S.M., Gong Q., Abbas A.R., Modrusan Z., Ghilardi N., de Sauvage F.J., et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008) 282-289
47. Zhou L., Ivanov I.I., Spolski R., Min R., Shenderov K., Egawa T., Levy D.E., Leonard W.J., and Littman D.R. IL-6 programs T(H)-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8 (2007) 967-974
48. Zhou L., Lopes J.E., Chong M.M., Ivanov I.I., Min R., Victora G.D., Shen Y., Du J., Rubtsov Y.P., Rudensky A.Y., et al. TGF-beta-induced Foxp3 inhibits T(H)17 cell differentiation by antagonizing RORgammat function. Nature 453 (2008) 236-240