Regulatory T Cells Reinforce Intestinal Homeostasis

Immunity

Volumn 31, Issue 3, 2009, Pages 401-411

  Barnes, Michael J ^a   Powrie, Fiona ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIUM LIPOPOLYSACCHARIDE; CD4 ANTIGEN; COLECALCIFEROL; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; DEXAMETHASONE; FLAGELLIN; GAMMA INTERFERON; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 2; INTERLEUKIN 23; INTERLEUKIN 27; INTERLEUKIN 4; TOLL LIKE RECEPTOR 5; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; CANCER IMMUNOTHERAPY; CD4+ T LYMPHOCYTE; CELL FUNCTION; CELL TYPE; CYTOKINE PRODUCTION; DENDRITIC CELL; DRUG RESEARCH; EFFECTOR CELL; ENTERITIS; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGICAL TOLERANCE; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; INTESTINE FLORA; INTESTINE FUNCTION; INTESTINE LYMPHATIC TISSUE; INTESTINE MUCOSA; LYMPHATIC DRAINAGE; LYMPHOCYTE FUNCTION; MACROPHAGE; MESENTERY LYMPH NODE; MUCOSAL IMMUNITY; NONHUMAN; PANETH CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTAKE; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; HOMEOSTASIS; HUMANS; INFLAMMATORY BOWEL DISEASES; INTESTINES; LYMPHOID TISSUE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY;

EID: 70049098536     PISSN: 10747613     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.immuni.2009.08.011     Document Type: Review

References (133)

1. Andersson J., Tran D.Q., Pesu M., Davidson T.S., Ramsey H., O'Shea J.J., and Shevach E.M. CD4+ FoxP3+ regulatory T cells confer infectious tolerance in a TGF-beta-dependent manner. J. Exp. Med. 205 (2008) 1975-1981
2. Annacker O., Burlen-Defranoux O., Pimenta-Araujo R., Cumano A., and Bandeira A. Regulatory CD4 T cells control the size of the peripheral activated/memory CD4 T cell compartment. J. Immunol. 164 (2000) 3573-3580
3. Annacker O., Coombes J.L., Malmstrom V., Uhlig H.H., Bourne T., Johansson-Lindbom B., Agace W.W., Parker C.M., and Powrie F. Essential role for CD103 in the T cell-mediated regulation of experimental colitis. J. Exp. Med. 202 (2005) 1051-1061
4. Aranda R., Sydora B.C., McAllister P.L., Binder S.W., Yang H.Y., Targan S.R., and Kronenberg M. Analysis of intestinal lymphocytes in mouse colitis mediated by transfer of CD4+, CD45RBhigh T cells to SCID recipients. J. Immunol. 158 (1997) 3464-3473
5. Artis D. Epithelial-cell recognition of commensal bacteria and maintenance of immune homeostasis in the gut. Nat. Rev. Immunol. 8 (2008) 411-420
6. Asseman C., Mauze S., Leach M.W., Coffman R.L., and Powrie F. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J. Exp. Med. 190 (1999) 995-1004
7. Asseman C., Read S., and Powrie F. Colitogenic Th1 cells are present in the antigen-experienced T cell pool in normal mice: Control by CD4+ regulatory T cells and IL-10. J. Immunol. 171 (2003) 971-978
8. Atarashi K., Nishimura J., Shima T., Umesaki Y., Yamamoto M., Onoue M., Yagita H., Ishii N., Evans R., Honda K., and Takeda K. ATP drives lamina propria T(H)17 cell differentiation. Nature 455 (2008) 808-812
9. Barnes M.J., Krebs P., Harris N., Eidenschenk C., Gonzalez-Quintial R., Arnold C.N., Crozat K., Sovath S., Moresco E.M., Theofilopoulos A.N., et al. Commitment to the regulatory T cell lineage requires CARMA1 in the thymus but not in the periphery. PLoS Biol. 7 (2009) e51
10. Barrett J.C., Hansoul S., Nicolae D.L., Cho J.H., Duerr R.H., Rioux J.D., Brant S.R., Silverberg M.S., Taylor K.D., Barmada M.M., et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40 (2008) 955-962
11. Bauquet A.T., Jin H., Paterson A.M., Mitsdoerffer M., Ho I.C., Sharpe A.H., and Kuchroo V.K. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat. Immunol. 10 (2009) 167-175
12. Bautista J.L., Lio C.W., Lathrop S.K., Forbush K., Liang Y., Luo J., Rudensky A.Y., and Hsieh C.S. Intraclonal competition limits the fate determination of regulatory T cells in the thymus. Nat. Immunol. 10 (2009) 610-617
13. Bour-Jordan H., and Bluestone J.A. Regulating the regulators: Costimulatory signals control the homeostasis and function of regulatory T cells. Immunol. Rev. 229 (2009) 41-66
14. Braat H., Rottiers P., Hommes D.W., Huyghebaert N., Remaut E., Remon J.P., van Deventer S.J., Neirynck S., Peppelenbosch M.P., and Steidler L. A phase I trial with transgenic bacteria expressing interleukin-10 in Crohn's disease. Clin. Gastroenterol. Hepatol. 4 (2006) 754-759
15. Brenchley J.M., and Douek D.C. HIV infection and the gastrointestinal immune system. Mucosal Immunol. 1 (2008) 23-30
16. Burchill M.A., Yang J., Vang K.B., Moon J.J., Chu H.H., Lio C.W., Vegoe A.L., Hsieh C.S., Jenkins M.K., and Farrar M.A. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 28 (2008) 112-121
17. Cerovic V., Jenkins C.D., Barnes A.G., Milling S.W., MacPherson G.G., and Klavinskis L.S. Hyporesponsiveness of intestinal dendritic cells to TLR stimulation is limited to TLR4. J. Immunol. 182 (2009) 2405-2415
18. Chan V., Crocetti G., Grehan M., Zhang L., Danon S., Lee A., and Mitchell H. Visualization of Helicobacter species within the murine cecal mucosa using specific fluorescence in situ hybridization. Helicobacter 10 (2005) 114-124
19. Chase A.J., Sedaghat A.R., German J.R., Gama L., Zink M.C., Clements J.E., and Siliciano R.F. Severe depletion of CD4+ CD25+ regulatory T cells from the intestinal lamina propria but not peripheral blood or lymph nodes during acute simian immunodeficiency virus infection. J. Virol. 81 (2007) 12748-12757
20. Chaudhry A., Rudra D., Treuting P., Samstein R.M., Liang Y., Kas A., and Rudensky A. CD4+ regulatory T cells control Th17 responses in a Stat3-dependent manner. Science (2009) in press
21. Chen Y., Kuchroo V.K., Inobe J., Hafler D.A., and Weiner H.L. Regulatory T cell clones induced by oral tolerance: Suppression of autoimmune encephalomyelitis. Science 265 (1994) 1237-1240
22. Chen W., Frank M.E., Jin W., and Wahl S.M. TGF-beta released by apoptotic T cells contributes to an immunosuppressive milieu. Immunity 14 (2001) 715-725
23. Chen Y., Chou K., Fuchs E., Havran W.L., and Boismenu R. Protection of the intestinal mucosa by intraepithelial gamma delta T cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14338-14343
24. Chen W., Jin W., Hardegen N., Lei K.J., Li L., Marinos N., McGrady G., and Wahl S.M. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J. Exp. Med. 198 (2003) 1875-1886
25. Cobbold S.P., Adams E., Farquhar C.A., Nolan K.F., Howie D., Lui K.O., Fairchild P.J., Mellor A.L., Ron D., and Waldmann H. Infectious tolerance via the consumption of essential amino acids and mTOR signaling. Proc. Natl. Acad. Sci. USA 106 (2009) 12055-12060
26. Collison L.W., Workman C.J., Kuo T.T., Boyd K., Wang Y., Vignali K.M., Cross R., Sehy D., Blumberg R.S., and Vignali D.A. The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 450 (2007) 566-569
27. Collison L.W., Pillai M.R., Chaturvedi V., and Vignali D.A. Regulatory T cell suppression is potentiated by target T cells in a cell contact, IL-35- and IL-10-dependent manner. J. Immunol. 182 (2009) 6121-6128
28. Coombes J.L., and Powrie F. Dendritic cells in intestinal immune regulation. Nat. Rev. Immunol. 8 (2008) 435-446
29. 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
30. Coombes J.L., Siddiqui K.R., Arancibia-Carcamo C.V., Hall J., Sun C.M., Belkaid Y., and Powrie F. 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. 204 (2007) 1757-1764
31. Crawford S.E., Stellmach V., Murphy-Ullrich J.E., Ribeiro S.M., Lawler J., Hynes R.O., Boivin G.P., and Bouck N. Thrombospondin-1 is a major activator of TGF-beta1 in vivo. Cell 93 (1998) 1159-1170
32. Crispe I.N. The liver as a lymphoid organ. Annu. Rev. Immunol. 27 (2009) 147-163
33. Curotto de Lafaille M.A., and Lafaille J.J. Natural and adaptive foxp3+ regulatory T cells: More of the same or a division of labor?. Immunity 30 (2009) 626-635
34. Curotto de Lafaille M.A., Kutchukhidze N., Shen S., Ding Y., Yee H., and Lafaille J.J. Adaptive Foxp3+ regulatory T cell-dependent and -independent control of allergic inflammation. Immunity 29 (2008) 114-126
35. Dale C., and Moran N.A. Molecular interactions between bacterial symbionts and their hosts. Cell 126 (2006) 453-465
36. Denning T.L., Kim G., and Kronenberg M. Cutting edge: CD4+CD25+ regulatory T cells impaired for intestinal homing can prevent colitis. J. Immunol. 174 (2005) 7487-7491
37. 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
38. Diebold R.J., Eis M.J., Yin M., Ormsby I., Boivin G.P., Darrow B.J., Saffitz J.E., and Doetschman T. Early-onset multifocal inflammation in the transforming growth factor beta 1-null mouse is lymphocyte mediated. Proc. Natl. Acad. Sci. USA 92 (1995) 12215-12219
39. Duerkop B.A., Vaishnava S., and Hooper L.V. Immune responses to the microbiota at the intestinal mucosal surface. Immunity 31 (2009) 368-376 this issue
40. Fahlén L., Read S., Gorelik L., Hurst S.D., Coffman R.L., Flavell R.A., and Powrie F. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J. Exp. Med. 201 (2005) 737-746
41. Fantini M.C., Rizzo A., Fina D., Caruso R., Sarra M., Stolfi C., Becker C., Macdonald T.T., Pallone F., Neurath M.F., and Monteleone G. Smad7 controls resistance of colitogenic T cells to regulatory T cell-mediated suppression. Gastroenterology 136 (2009) 1308-1316
42. Feuerer M., Hill J.A., Mathis D., and Benoist C. Foxp3+ regulatory T cells: Differentiation, specification, subphenotypes. Nat. Immunol. 10 (2009) 689-695
43. Fontenot J.D., Gavin M.A., and Rudensky A.Y. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4 (2003) 330-336
44. Fowler S., and Powrie F. CTLA-4 expression on antigen-specific cells but not IL-10 secretion is required for oral tolerance. Eur. J. Immunol. 32 (2002) 2997-3006
45. Franke A., Balschun T., Karlsen T.H., Sventoraityte J., Nikolaus S., Mayr G., Domingues F.S., Albrecht M., Nothnagel M., Ellinghaus D., et al. Sequence variants in IL10, ARPC2 and multiple other loci contribute to ulcerative colitis susceptibility. Nat. Genet. 40 (2008) 1319-1323
46. Gewirtz A.T., Navas T.A., Lyons S., Godowski P.J., and Madara J.L. Cutting edge: Bacterial flagellin activates basolaterally expressed TLR5 to induce epithelial proinflammatory gene expression. J. Immunol. 167 (2001) 1882-1885
47. Gorelik L., and Flavell R.A. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 12 (2000) 171-181
48. Hall J.A., Bouladoux N., Sun C.M., Wohlfert E.A., Blank R.B., Zhu Q., Grigg M.E., Berzofsky J.A., and Belkaid Y. Commensal DNA limits regulatory T cell conversion and is a natural adjuvant of intestinal immune responses. Immunity 29 (2008) 637-649
49. Hill J.A., Feuerer M., Tash K., Haxhinasto S., Perez J., Melamed R., Mathis D., and Benoist C. Foxp3 transcription-factor-dependent and -independent regulation of the regulatory T cell transcriptional signature. Immunity 27 (2007) 786-800
50. Hill J.A., Hall J.A., Sun C.M., Cai Q., Ghyselinck N., Chambon P., Belkaid Y., Mathis D., and Benoist C. Retinoic acid enhances Foxp3 induction indirectly by relieving inhibition from CD4+CD44hi Cells. Immunity 29 (2008) 758-770
51. Huehn J., Siegmund K., Lehmann J.C., Siewert C., Haubold U., Feuerer M., Debes G.F., Lauber J., Frey O., Przybylski G.K., et al. Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J. Exp. Med. 199 (2004) 303-313
52. Ito T., Hanabuchi S., Wang Y.H., Park W.R., Arima K., Bover L., Qin F.X., Gilliet M., and Liu Y.J. Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 28 (2008) 870-880
53. Ivanov I.I., Frutos Rde L., Manel N., Yoshinaga K., Rifkin D.B., Sartor R.B., Finlay B.B., and Littman D.R. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4 (2008) 337-349
54. Izcue A., Hue S., Buonocore S., Arancibia-Carcamo C.V., Ahern P.P., Iwakura Y., Maloy K.J., and Powrie F. Interleukin-23 restrains regulatory T cell activity to drive T cell-dependent colitis. Immunity 28 (2008) 559-570
55. Josefowicz S.Z., and Rudensky A. Control of regulatory T cell lineage commitment and maintenance. Immunity 30 (2009) 616-625
56. Kallies A., Hawkins E.D., Belz G.T., Metcalf D., Hommel M., Corcoran L.M., Hodgkin P.D., and Nutt S.L. Transcriptional repressor Blimp-1 is essential for T cell homeostasis and self-tolerance. Nat. Immunol. 7 (2006) 466-474
57. Kamanaka M., Kim S.T., Wan Y.Y., Sutterwala F.S., Lara-Tejero M., Galan J.E., Harhaj E., and Flavell R.A. Expression of interleukin-10 in intestinal lymphocytes detected by an interleukin-10 reporter knockin tiger mouse. Immunity 25 (2006) 941-952
58. Kitani A., Fuss I., Nakamura K., Kumaki F., Usui T., and Strober W. Transforming growth factor (TGF)-beta1-producing regulatory T cells induce Smad-mediated interleukin 10 secretion that facilitates coordinated immunoregulatory activity and amelioration of TGF-beta1-mediated fibrosis. J. Exp. Med. 198 (2003) 1179-1188
59. Koch M.A., Tucker-Heard G., Perdue N.R., Killebrew J.R., Urdahl K.B., and Campbell D.J. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat. Immunol. 10 (2009) 595-602
60. Kraus T.A., Toy L., Chan L., Childs J., and Mayer L. Failure to induce oral tolerance to a soluble protein in patients with inflammatory bowel disease. Gastroenterology 126 (2004) 1771-1778
61. Kraus T.A., Cheifetz A., Toy L., Meddings J.B., and Mayer L. Evidence for a genetic defect in oral tolerance induction in inflammatory bowel disease. Inflamm. Bowel Dis. 12 (2006) 82-88
62. Kullberg M.C., Ward J.M., Gorelick P.L., Caspar P., Hieny S., Cheever A., Jankovic D., and Sher A. Helicobacter hepaticus triggers colitis in specific-pathogen-free interleukin-10 (IL-10)-deficient mice through an IL-12- and gamma interferon-dependent mechanism. Infect. Immun. 66 (1998) 5157-5166
63. Kullberg M.C., Jankovic D., Gorelick P.L., Caspar P., Letterio J.J., Cheever A.W., and Sher A. Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J. Exp. Med. 196 (2002) 505-515
64. Kullberg M.C., Hay V., Cheever A.W., Mamura M., Sher A., Letterio J.J., Shevach E.M., and Piccirillo C.A. TGF-beta1 production by CD4+ CD25+ regulatory T cells is not essential for suppression of intestinal inflammation. Eur. J. Immunol. 35 (2005) 2886-2895
65. Lacy-Hulbert A., Smith A.M., Tissire H., Barry M., Crowley D., Bronson R.T., Roes J.T., Savill J.S., and Hynes R.O. Ulcerative colitis and autoimmunity induced by loss of myeloid alphav integrins. Proc. Natl. Acad. Sci. USA 104 (2007) 15823-15828
66. Lathrop S.K., Santacruz N.A., Pham D., Luo J., and Hsieh C.S. Antigen-specific peripheral shaping of the natural regulatory T cell population. J. Exp. Med. 205 (2008) 3105-3117
67. Leppkes M., Becker C., Ivanov I.I., Hirth S., Wirtz S., Neufert C., Pouly S., Murphy A.J., Valenzuela D.M., Yancopoulos G.D., et al. RORgamma-expressing Th17 cells induce murine chronic intestinal inflammation via redundant effects of IL-17A and IL-17F. Gastroenterology 136 (2009) 257-267
68. Li M.O., Sanjabi S., and Flavell R.A. Transforming growth factor-beta controls development, homeostasis, and tolerance of T cells by regulatory T cell-dependent and -independent mechanisms. Immunity 25 (2006) 455-471
69. Li M.O., Wan Y.Y., and Flavell R.A. T cell-produced transforming growth factor-beta1 controls T cell tolerance and regulates Th1- and Th17-cell differentiation. Immunity 26 (2007) 579-591
70. Lio C.W., and Hsieh C.S. A two-step process for thymic regulatory T cell development. Immunity 28 (2008) 100-111
71. Lotz M., Gutle D., Walther S., Menard S., Bogdan C., and Hornef M.W. Postnatal acquisition of endotoxin tolerance in intestinal epithelial cells. J. Exp. Med. 203 (2006) 973-984
72. Lumeng C.N., Maillard I., and Saltiel A.R. T-ing up inflammation in fat. Nat. Med. 15 (2009) 846-847
73. Maloy K.J., Salaun L., Cahill R., Dougan G., Saunders N.J., and Powrie F. CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J. Exp. Med. 197 (2003) 111-119
74. Marie J.C., Letterio J.J., Gavin M., and Rudensky A.Y. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J. Exp. Med. 201 (2005) 1061-1067
75. Marie J.C., Liggitt D., and Rudensky A.Y. Cellular mechanisms of fatal early-onset autoimmunity in mice with the T cell-specific targeting of transforming growth factor-beta receptor. Immunity 25 (2006) 441-454
76. Martins G.A., Cimmino L., Shapiro-Shelef M., Szabolcs M., Herron A., Magnusdottir E., and Calame K. Transcriptional repressor Blimp-1 regulates T cell homeostasis and function. Nat. Immunol. 7 (2006) 457-465
77. Maynard C.L., and Weaver C.T. Intestinal effector T cells in health and disease. Immunity 31 (2009) 389-400 this issue
78. Maynard C.L., Harrington L.E., Janowski K.M., Oliver J.R., Zindl C.L., Rudensky A.Y., and Weaver C.T. Regulatory T cells expressing interleukin 10 develop from Foxp3+ and Foxp3- precursor cells in the absence of interleukin 10. Nat. Immunol. 8 (2007) 931-941
79. Maynard C.L., Hatton R.D., Helms W.S., Oliver J.R., Stephensen C.B., and Weaver C.T. Contrasting roles for all-trans retinoic acid in TGF-beta-mediated induction of Foxp3 and Il10 genes in developing regulatory T cells. J. Exp. Med. 206 (2009) 343-357
80. 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
81. Mazmanian S.K., Round J.L., and Kasper D.L. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 453 (2008) 620-625
82. Medoff B.D., Sandall B.P., Landry A., Nagahama K., Mizoguchi A., Luster A.D., and Xavier R.J. Differential requirement for CARMA1 in agonist-selected T-cell development. Eur. J. Immunol. 39 (2009) 78-84
83. Min B., McHugh R., Sempowski G.D., Mackall C., Foucras G., and Paul W.E. Neonates support lymphopenia-induced proliferation. Immunity 18 (2003) 131-140
84. Molinero L.L., Yang J., Gajewski T., Abraham C., Farrar M.A., and Alegre M.L. CARMA1 controls an early checkpoint in the thymic development of FoxP3+ regulatory T cells. J. Immunol. 182 (2009) 6736-6743
85. Monteleone G., Kumberova A., Croft N.M., McKenzie C., Steer H.W., and MacDonald T.T. Blocking Smad7 restores TGF-beta1 signaling in chronic inflammatory bowel disease. J. Clin. Invest. 108 (2001) 601-609
86. Mottet C., Uhlig H.H., and Powrie F. Cutting edge: Cure of colitis by CD4+CD25+ regulatory T cells. J. Immunol. 170 (2003) 3939-3943
87. 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
88. Munger J.S., Huang X., Kawakatsu H., Griffiths M.J., Dalton S.L., Wu J., Pittet J.F., Kaminski N., Garat C., Matthay M.A., et al. The integrin alpha v beta 6 binds and activates latent TGF beta 1: A mechanism for regulating pulmonary inflammation and fibrosis. Cell 96 (1999) 319-328
89. Nedjic J., Aichinger M., Emmerich J., Mizushima N., and Klein L. Autophagy in thymic epithelium shapes the T-cell repertoire and is essential for tolerance. Nature 455 (2008) 396-400
90. O'Garra A., and Vieira P. T(H)1 cells control themselves by producing interleukin-10. Nat. Rev. Immunol. 7 (2007) 425-428
91. Oida T., Zhang X., Goto M., Hachimura S., Totsuka M., Kaminogawa S., and Weiner H.L. CD4+CD25- T cells that express latency-associated peptide on the surface suppress CD4+CD45RBhigh-induced colitis by a TGF-beta-dependent mechanism. J. Immunol. 170 (2003) 2516-2522
92. Onishi Y., Fehervari Z., Yamaguchi T., and Sakaguchi S. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc. Natl. Acad. Sci. USA 105 (2008) 10113-10118
93. Peggs K.S., Quezada S.A., Korman A.J., and Allison J.P. Principles and use of anti-CTLA4 antibody in human cancer immunotherapy. Curr. Opin. Immunol. 18 (2006) 206-213
94. Perruche S., Zhang P., Liu Y., Saas P., Bluestone J.A., and Chen W. CD3-specific antibody-induced immune tolerance involves transforming growth factor-beta from phagocytes digesting apoptotic T cells. Nat. Med. 14 (2008) 528-535
95. Pesu M., Watford W.T., Wei L., Xu L., Fuss I., Strober W., Andersson J., Shevach E.M., Quezado M., Bouladoux N., et al. T-cell-expressed proprotein convertase furin is essential for maintenance of peripheral immune tolerance. Nature 455 (2008) 246-250
96. Pot C., Jin H., Awasthi A., Liu S.M., Lai C.Y., Madan R., Sharpe A.H., Karp C.L., Miaw S.C., Ho I.C., and Kuchroo V.K. Cutting edge: IL-27 induces the transcription factor c-Maf, cytokine IL-21, and the costimulatory receptor ICOS that coordinately act together to promote differentiation of IL-10-producing Tr1 cells. J. Immunol. 183 (2009) 797-801
97. Powell B.R., Buist N.R., and Stenzel P. An X-linked syndrome of diarrhea, polyendocrinopathy, and fatal infection in infancy. J. Pediatr. 100 (1982) 731-737
98. Powrie F., Leach M.W., Mauze S., Caddle L.B., and Coffman R.L. Phenotypically distinct subsets of CD4+ T cells induce or protect from chronic intestinal inflammation in C. B-17 scid mice. Int. Immunol. 5 (1993) 1461-1471
99. Powrie F., Leach M.W., Mauze S., Menon S., Caddle L.B., and Coffman R.L. Inhibition of Th1 responses prevents inflammatory bowel disease in scid mice reconstituted with CD45RBhi CD4+ T cells. Immunity 1 (1994) 553-562
100. Powrie F., Carlino J., Leach M.W., Mauze S., and Coffman R.L. A critical role for transforming growth factor-beta but not interleukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J. Exp. Med. 183 (1996) 2669-2674
101. Read S., Malmstrom V., and Powrie F. Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192 (2000) 295-302
102. Rieger K., Loddenkemper C., Maul J., Fietz T., Wolff D., Terpe H., Steiner B., Berg E., Miehlke S., Bornhauser M., et al. Mucosal FOXP3+ regulatory T cells are numerically deficient in acute and chronic GvHD. Blood 107 (2006) 1717-1723
103. Roers A., Siewe L., Strittmatter E., Deckert M., Schluter D., Stenzel W., Gruber A.D., Krieg T., Rajewsky K., and Muller W. T cell-specific inactivation of the interleukin 10 gene in mice results in enhanced T cell responses but normal innate responses to lipopolysaccharide or skin irritation. J. Exp. Med. 200 (2004) 1289-1297
104. Rubtsov Y.P., Rasmussen J.P., Chi E.Y., Fontenot J., Castelli L., Ye X., Treuting P., Siewe L., Roers A., Henderson Jr. W.R., et al. Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces. Immunity 28 (2008) 546-558
105. Saraiva M., Christensen J.R., Veldhoen M., Murphy T.L., Murphy K.M., and O'Garra A. Interleukin-10 production by Th1 cells requires interleukin-12-induced STAT4 transcription factor and ERK MAP kinase activation by high antigen dose. Immunity 31 (2009) 209-219
106. Sauer S., Bruno L., Hertweck A., Finlay D., Leleu M., Spivakov M., Knight Z.A., Cobb B.S., Cantrell D., O'Connor E., et al. T cell receptor signaling controls Foxp3 expression via PI3K, Akt, and mTOR. Proc. Natl. Acad. Sci. USA 105 (2008) 7797-7802
107. Schneider M.A., Meingassner J.G., Lipp M., Moore H.D., and Rot A. CCR7 is required for the in vivo function of CD4+ CD25+ regulatory T cells. J. Exp. Med. 204 (2007) 735-745
108. Shevach E.M. Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity 30 (2009) 636-645
109. Shkoda A., Ruiz P.A., Daniel H., Kim S.C., Rogler G., Sartor R.B., and Haller D. Interleukin-10 blocked endoplasmic reticulum stress in intestinal epithelial cells: impact on chronic inflammation. Gastroenterology 132 (2007) 190-207
110. Singh B., Read S., Asseman C., Malmstrom V., Mottet C., Stephens L.A., Stepankova R., Tlaskalova H., and Powrie F. Control of intestinal inflammation by regulatory T cells. Immunol. Rev. 182 (2001) 190-200
111. Sokol H., Pigneur B., Watterlot L., Lakhdari O., Bermudez-Humaran L.G., Gratadoux J.J., Blugeon S., Bridonneau C., Furet J.P., Corthier G., et al. Faecalibacterium prausnitzii is an anti-inflammatory commensal bacterium identified by gut microbiota analysis of Crohn disease patients. Proc. Natl. Acad. Sci. USA 105 (2008) 16731-16736
112. Spolski R., Kim H.P., Zhu W., Levy D.E., and Leonard W.J. IL-21 mediates suppressive effects via its induction of IL-10. J. Immunol. 182 (2009) 2859-2867
113. Stepankova R., Powrie F., Kofronova O., Kozakova H., Hudcovic T., Hrncir T., Uhlig H., Read S., Rehakova Z., Benada O., et al. Segmented filamentous bacteria in a defined bacterial cocktail induce intestinal inflammation in SCID mice reconstituted with CD45RBhigh CD4+ T cells. Inflamm. Bowel Dis. 13 (2007) 1202-1211
114. Strauch U.G., Obermeier F., Grunwald N., Gurster S., Dunger N., Schultz M., Griese D.P., Mahler M., Scholmerich J., and Rath H.C. Influence of intestinal bacteria on induction of regulatory T cells: Lessons from a transfer model of colitis. Gut 54 (2005) 1546-1552
115. Strober W., Fuss I.J., and Blumberg R.S. The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20 (2002) 495-549
116. Stumhofer J.S., Silver J.S., Laurence A., Porrett P.M., Harris T.H., Turka L.A., Ernst M., Saris C.J., O'Shea J.J., and Hunter C.A. Interleukins 27 and 6 induce STAT3-mediated T cell production of interleukin 10. Nat. Immunol. 8 (2007) 1363-1371
117. Sun C.M., Hall J.A., Blank R.B., Bouladoux N., Oukka M., Mora J.R., and Belkaid Y. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204 (2007) 1775-1785
118. Tadokoro C.E., Shakhar G., Shen S., Ding Y., Lino A.C., Maraver A., Lafaille J.J., and Dustin M.L. Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo. J. Exp. Med. 203 (2006) 505-511
119. Takeda K., Clausen B.E., Kaisho T., Tsujimura T., Terada N., Forster I., and Akira S. Enhanced Th1 activity and development of chronic enterocolitis in mice devoid of Stat3 in macrophages and neutrophils. Immunity 10 (1999) 39-49
120. Torchinsky M.B., Garaude J., Martin A.P., and Blander J.M. Innate immune recognition of infected apoptotic cells directs T(H)17 cell differentiation. Nature 458 (2009) 78-82
121. 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
122. Uhlig H.H., Coombes J., Mottet C., Izcue A., Thompson C., Fanger A., Tannapfel A., Fontenot J.D., Ramsdell F., and Powrie F. Characterization of Foxp3+CD4+CD25+ and IL-10-secreting CD4+CD25+ T cells during cure of colitis. J. Immunol. 177 (2006) 5852-5860
123. Valencia X., Stephens G., Goldbach-Mansky R., Wilson M., Shevach E.M., and Lipsky P.E. TNF downmodulates the function of human CD4+CD25hi T-regulatory cells. Blood 108 (2006) 253-261
124. Veldhoen M., Hirota K., Christensen J., O'Garra A., and Stockinger B. Natural agonists for aryl hydrocarbon receptor in culture medium are essential for optimal differentiation of Th17 T cells. J. Exp. Med. 206 (2009) 43-49
125. Vieira P.L., Christensen J.R., Minaee S., O'Neill E.J., Barrat F.J., Boonstra A., Barthlott T., Stockinger B., Wraith D.C., and O'Garra A. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J. Immunol. 172 (2004) 5986-5993
126. Villarino A.V., Artis D., Bezbradica J.S., Miller O., Saris C.J., Joyce S., and Hunter C.A. IL-27R deficiency delays the onset of colitis and protects from helminth-induced pathology in a model of chronic IBD. Int. Immunol. 20 (2008) 739-752
127. Wei G., Wei L., Zhu J., Zang C., Hu-Li J., Yao Z., Cui K., Kanno Y., Roh T.Y., Watford W.T., et al. Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells. Immunity 30 (2009) 155-167
128. Wikoff W.R., Anfora A.T., Liu J., Schultz P.G., Lesley S.A., Peters E.C., and Siuzdak G. Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc. Natl. Acad. Sci. USA 106 (2009) 3698-3703
129. Wirnsberger G., Mair F., and Klein L. Regulatory T cell differentiation of thymocytes does not require a dedicated antigen-presenting cell but is under T cell-intrinsic developmental control. Proc. Natl. Acad. Sci. USA 106 (2009) 10278-10283
130. Yuan Q., Bromley S.K., Means T.K., Jones K.J., Hayashi F., Bhan A.K., and Luster A.D. CCR4-dependent regulatory T cell function in inflammatory bowel disease. J. Exp. Med. 204 (2007) 1327-1334
131. Zheng Y., Chaudhry A., Kas A., deRoos P., Kim J.M., Chu T.T., Corcoran L., Treuting P., Klein U., and Rudensky A.Y. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 458 (2009) 351-356
132. Zheng Y., Josefowicz S.Z., Kas A., Chu T.T., Gavin M.A., and Rudensky A.Y. Genome-wide analysis of Foxp3 target genes in developing and mature regulatory T cells. Nature 445 (2007) 936-940
133. Ziegler S.F. FOXP3: Of mice and men. Annu. Rev. Immunol. 24 (2006) 209-226