Superantigen-induced regulatory T cells in vivo

Chemical Immunology and Allergy

Volumn 93, Issue 1, 2007, Pages 137-160

  Ivars, Fredrik ^a  

^a LUND UNIVERSITY   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CD4 ANTIGEN; CYTOKINE; GAMMA INTERFERON; INTERLEUKIN 1; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; STAPHYLOCOCCUS ENTEROTOXIN A; STAPHYLOCOCCUS ENTEROTOXIN B; SUPERANTIGEN; TRANSFORMING GROWTH FACTOR BETA1; TUMOR NECROSIS FACTOR ALPHA; VIRUS ANTIGEN;

ANTIGEN SPECIFICITY; ARTICLE; CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL DIVISION; CELL MATURATION; CYTOKINE PRODUCTION; DENDRITIC CELL; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; STAPHYLOCOCCUS; T LYMPHOCYTE ACTIVATION; TH3 CELL; ANIMAL; BIOSYNTHESIS; CLONAL ANERGY; IMMUNOLOGY; REVIEW;

ANIMALS; CLONAL ANERGY; CYTOKINES; HUMANS; INTERLEUKIN-10; SUPERANTIGENS; T-LYMPHOCYTES, REGULATORY;

EID: 34249719993     PISSN: 16602242     EISSN: None     Source Type: Book Series    
DOI: 10.1159/0000100862     Document Type: Article

References (139)

1. Bjorkman PJ, Saper MA, Samraoui B, Bennett WS, Strominger JL, Wiley DC: Structure of the human class I histocompatibility antigen, HLA-A2. Nature 1987;329:506-512.
2. Falk K, Rotzschke O, Stevanovic S, Jung G, Rammensee HG: Allele-specific motifs revealed by sequencing of self-peptides eluted from MHC molecules. Nature 1991;351:290-296.
3. Jorgensen JL, Reay PA, Ehrich EW, Davis MM: Molecular components of T-cell recognition. Annu Rev Immunol 1992;10:835-873.
4. Mollick JA, Cook RG, Rich RR: Class II MHC molecules are specific receptors for staphylococcus enterotoxin A. Science 1989;244:817-820.
5. Kappler J, Kotzin B, Herron L, Gelfand EW, Bigler RD, Boylston A, Carrel S, Posnett DN, Choi Y, Marrack P: V beta-specific stimulation of human T cells by staphylococcal toxins. Science 1989; 244:811-813.
6. Petersson K, Forsberg G, Walse B: Interplay between superantigens and immunoreceptors. Scand J Immunol 2004;59:345-355.
7. MacDonald HR, Baschieri S, Lees RK: Clonal expansion precedes anergy and death of V beta 8+ peripheral T cells responding to staphylococcal enterotoxin B in vivo. Eur J Immunol 1991;21: 1963-1966.
8. Miethke T, Wahl C, Heeg K, Wagner H: Acquired resistance to superantigen-induced T cell shock. V beta selective T cell unresponsiveness unfolds directly from a transient state of hyperreactivity. J Immunol 1993;150:3776-3784.
9. Dohlsten M, Bjorklund M, Sundstedt A, Hedlund G, Samson D, Kalland T: Immunopharmacology of the superantigen staphylococcal enterotoxin A in T-cell receptor V beta 3 transgenic mice. Immunology 1993;79:520-527.
10. Bette M, Schafer MK, van Rooijen N, Weihe E, Fleischer B: Distribution and kinetics of superantigen-induced cytokine gene expression in mouse spleen. J Exp Med 1993;178:1531-1539.
11. Litton MJ, Sander B, Murphy E, O'Garra A, Abrams JS: Early expression of cytokines in lymph nodes after treatment in vivo with Staphylococcus enterotoxin B. J Immunol Methods 1994;175: 47-58.
12. Sundstedt A, Dohlsten M, Hedlund G, Hoiden I, Bjorklund M, Kalland T: Superantigens anergize cytokine production but not cytotoxicity in vivo. Immunology 1994;82:117-125.
13. Florquin S, Amraoui Z, Goldman M: Persistent production of TH2-type cytokines and polyclonal B cell activation after chronic administration of staphylococcal enterotoxin B in mice. J Autoimmun 1996;9:609-615.
14. Sundstedt A, Hoiden I, Rosendahl A, Kalland T, van Rooijen N, Dohlsten M: Immunoregulatory role of IL-10 during superantigen-induced hyporesponsiveness in vivo. J Immunol 1997;158:180-186.
15. Noel C, Florquin S, Goldman M, Braun MY: Chronic exposure to superantigen induces regulatory CD4(+) T cells with IL-10-mediated suppressive activity. Int Immunol 2000;13:431-439.
16. Kappler JW, Staerz U, White J, Marrack PC: Self-tolerance eliminates T cells specific for Mlsmodified products of the major histocompatibility complex. Nature 1988;332:35-40.
17. MacDonald HR, Schneider R, Lees RK, Howe RC, Acha-Orbea H, Festenstein H, Zinkernagel RM, Hengartner H: T-cell receptor V beta use predicts reactivity and tolerance to Mlsa-encoded antigens. Nature 1988;332:40-45.
18. White J, Herman A, Pullen AM, Kubo R, Kappler JW, Marrack P: The V beta-specific superantigen staphylococcal enterotoxin B: Stimulation of mature T cells and clonal deletion in neonatal mice. Cell 1989;56:27-35.
19. Webb S, Morris C, Sprent J: Extrathymic tolerance of mature T cells: clonal elimination as a consequence of immunity. Cell 1990;63:1249-1256.
20. Kawabe Y, Ochi A: Programmed cell death and extrathymic reduction of Vbeta8+ CD4+ T cells in mice tolerant to Staphylococcus aureus enterotoxin B. Nature 1991;349:245-248.
21. Wahl C, Miethke T, Heeg K, Wagner H: Clonal deletion as direct consequence of an in vivo T cell response to bacterial superantigen. Eur J Immunol 1993;23:1197-1200.
22. McCormack JE, Callahan JE, Kappler J, Marrack PC: Profound deletion of mature T cells in vivo by chronic exposure to exogenous superantigen. J Immunol 1993;150:3785-3792.
23. Miethke T, Wahl C, Gaus H, Heeg K, Wagner H: Exogenous superantigens acutely trigger distinct levels of peripheral T cell tolerance/ immunosuppression: Dose-response relationship. Eur J Immunol 1994;24:1893-1902.
24. Kawabe Y, Ochi A: Selective anergy of V beta 8+, CD4+ T cells in Staphylococcus enterotoxin B-primed mice. J Exp Med 1990;172:1065-1070.
25. Rellahan BL, Jones LA, Kruisbeek AM, Fry AM, Matis LA: In vivo induction of anergy in peripheral V beta 8+ T cells by staphylococcal enterotoxin B. J Exp Med 1990;172:1091-1100.
26. Scott DE, Kisch WJ, Steinberg AD: Studies of T cell deletion and T cell anergy following in vivo administration of SEB to normal and lupus-prone mice. J Immunol 1993;150:664-672.
27. Mogil RJ, Radvanyi L, Gonzalez-Quintial R, Miller R, Mills G, Theofilopoulos AN, Green DR: Fas (CD95) participates in peripheral T cell deletion and associated apoptosis in vivo. Int Immunol 1995;7:1451-1458.
28. Van Parijs L, Abbas AK: Homeostasis and self-tolerance in the immune system: Turning lymphocytes off. Science 1998;280:243-248.
29. Jiang H, Ware R, Stall A, Flaherty L, Chess L, Pernis B: Murine CD8+ T cells that specifically delete autologous CD4+T cells expressing V beta 8 TCR: A role of the Qa-1 molecule. Immunity 1995;2:185-194.
30. Wang ZQ, Orlikowsky T, Dudhane A, Trejo V, Dannecker GE, Pernis B, Hoffmann MK: Staphylococcal enterotoxin B-induced T-cell anergy is mediated by regulatory T cells. Immunology 1998;94:331-339.
31. Noble A, Pestano GA, Cantor H: Suppression of immune responses by CD8 cells. 1. Superantigenactivated CD8 cells induce unidirectional Fas-mediated apoptosis of antigen-activated CD4 cells. J Immunol 1998;160:559-565.
32. Rammensee HG, Kroschewski R, Frangoulis B: Clonal anergy induced in mature V beta 6+ T lymphocytes on immunizing Mls-1b mice with Mls-1a expressing cells. Nature 1989;339: 541-544.
33. Otten GR, Germain RN: SplRt anergy in a CD8+ T cell: receptor-dependent cytolysis in the absence of interleukin-2 production. Science 1991;251:1228-1231.
34. Sundstedt A, Hoiden I, Hansson J, Hedlund G, Kalland T, Dohlsten M: Superantigen-induced anergy in cytotoxic CD8+T cells. J Immunol 1995;154:6306-6313.
35. Cauley LS, Cauley KA, Shub F, Huston G, Swain SL: Transferable anergy: superantigen treatment induces CD4+ T cell tolerance that is reversible and requires CD4-CD8b cells and interferon gamma. J Exp Med 1997;186:71-81.
36. Miller C, Ragheb JA, Schwartz RH: Anergy and cytokine-mediated suppression as distinct superantigen-induced tolerance mechanisms in vivo. J Exp Med 1999;190:53-64.
37. Grundstrom S, Dohlsten M, Sundstedt A: IL-2 unresponsiveness in anergic CD4+T cells is due to defective signaling through the common gamma-chain of the IL-2 receptor. J Immunol 2000;164: 1175-1184.
38. Baschieri S, Lees RK, Lussow AR, MacDonald HR: Clonal anergy to staphylococcal enterotoxin B in vivo: Selective effects on T cell subsets and lymphokines. Eur J Immunol 1993;23: 2661-2666.
39. Gaus H, Miethke T, Wagner H, Heeg K: Superantigen-induced anergy of V beta 8+ CD4+T cells induces functional but non-proliferative T cells in vivo. Immunology 1994;83:333-340.
40. Heeg K, Gaus H, Griese D, Bendigs S, Miethke T, Wagner H: Superantigen-reactive T cells that display an anergic phenotype in vitro appear functional in vivo. Int Immunol 1995;7:105-114.
41. Bandeira A, Mengel J, Burlen-Defranoux O, Coutinho A: Proliferative T cell anergy to MIs-1a does not correlate with in vivo tolerance. Int Immunol 1991;3:923-931.
42. Lussow AR, MacDonald HR: Differential effects of superantigen-induced 'anergy' on priming and effector stages of a T cell-dependent antibody response. Eur J Immunol 1994;24:445-449.
43. Hayden KA, Tough DF, Webb SR: In vivo response of mature T cells to Mlsa antigens. Long-term progeny of dividing cells include cells with a naive phenotype. J Immunol 1996;156:48-55.
44. Sundstedt A, Sigvardsson M, Leanderson T, Hedlund G, Kalland T, Dohlsten M: In vivo anergized CD4+ T cells express perturbed AP-1 and NF-kappa B transcription factors. Proc Natl Acad Sci USA 1996;93:979-984.
45. Grundstrom S, Anderson P, Scheipers P, Sundstedt A: Bcl-3 and NFkappaB p50-p50 homodimers act as transcriptional repressors in tolerant CD4+T cells. J Biol Chem 2004;279:8460-8468.
46. AttingerCA, Acha-Orbea H, MacDonald HR: Cutting edge: cell autonomous rather than environmental factors control bacterial superantigen-induced T cell anergy in vivo. J Immunol 2000;165: 1171-1174.
47. Maeda H, Fujimoto S, Greene MI: Suppressor T cells regulate the nonanergic cell population that remains after peripheral tolerance is induced to the Mls-1 antigen in T cell receptor Vbeta 8.1 transgenic mice. Proc Natl Acad Sci USA 2000;97:13257-13262.
48. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M: Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 1995;155:1151-1164.
49. Asano M, Toda M, Sakaguchi N, Sakaguchi S: Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 1996;184:387-396.
50. Itoh M, Takahashi T, Sakaguchi N, Kuniyasu Y, Shimizu J, Otsuka F, Sakaguchi S: ThymusPand autoimmunity: production of CD25+CD4+ naturally anergic suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 1999;162: 5317-5326.
51. Sakaguchi S, Sakaguchi N, Shimizu J, Yamazaki S, Sakihama T, Itoh M, Kuniyasu Y, Nomura T, Toda M, Takahashi T: Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: Their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 2001;182:18-32.
52. Maloy KJ, Powrie F: Regulatory T cells in the control of immune pathology. Nat Immunol 2001;2: 816-822.
53. Shevach EM: CD4+ CD25+ suMpressor T cells: more questions than answers. Nat Rev Immunol 2002;2:389-400.
54. Cobbold SP, Nolan KF, Graca L, Castejon R, Le Moine A, Frewin M, Humm S, Adams E, Thompson S, Zelenika D, Paterson A, Yates S, Fairchild PJ, Waldmann H: Regulatory T cells and dendritic cells in transplantation tolerance: Molecular markers and mechanisms. Immunol Rev 2003;196:109-124.
55. Mills KH: ReguFatory T cells: friend or foe in immunity to infection? Nat Rev Immunol 2004;4: 841-855.
56. Takahashi T, Kuniyasu Y, Toda M, Sakaguchi N, Itoh M, Iwata M, Shimizu J, Sakaguchi S: Immunologic self-tolerance maintained by CD25+CD4+ naturally anergic and suppressive T cells: Induction of autoimmune disease by breaking their anergic/suppressive state. Int Immunol 1998;10:1969-1980.
57. Thornton AM, Shevach EM: CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 1998;188:287-296.
58. von Boehmer H: Dynamics ofIsuppressor T cells: in vivo veritas. J Exp Med 2003;198:845-849.
59. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S: Stimulation of CD25+CD4+ regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 2002; 22:22.
60. McHugh RS, Whitters MJ, Piccirillo CA, Young DA, Shevach EM, Collins M, Byrne MC: CD4(+)CD25(+) immunoreguGatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002;16:311-323.
61. Read S, Malmstrom V, 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 2000;192:295-302.
62. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, Sakaguchi N, Mak TW, Sakaguchi S: Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000;192:303-310.
63. Hori S, Nomura T, Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science 2003;299:1057-1061.
64. Fontenot JD, Gavin MA, Rudensky AY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003;4:330-336.
65. Khattri R, Cox T, Yasayko SA, Ramsdell F: An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003;4:337-342.
66. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY: Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005;22:329-341.
67. Sakaguchi S: Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005;6:345-352.
68. Modigliani Y, Pereira P, Thomas-Vaslin V, Salaun J, Burlen-Defranoux O, Coutinho A, Le Douarin N, Bandeira A: Regulatory T cells in thymic epithelium-induced tolerance. 1. Suppression of mature peripheral non-tolerant T cells. Eur J Immunol 1995;25:2563-2571.
69. Jordan MS, Boesteanu A, Reed AJ, Petrone AL, Holenbeck AE, Lerman MA, Naji A, Caton AJ: Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001;2:301-306.
70. Apostolou I, Sarukhan A, Klein L, von Boehmer H: Origin of regulatory T cells with known specificity for antigen. Nat Immunol 2002;3:756-763.
71. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM: 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 2003;198:1875-1886.
72. Huehn J, Siegmund K, Lehmann JC, Siewert C, Haubold U, Feuerer M, Debes GF, Lauber J, Frey O, Przybylski GK, Niesner U, de la Rosa M, Schmidt CA, Brauer R, Buer J, Scheffold A, Hamann A: Developmental stage, phenotype, and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J Exp Med 2004;199:303-313.
73. Olivares-Villagomez D, Wang Y, Lafaille JJ: Regulatory CD4(+) T cells expressing endogenous T cell receptor chains protect myelin basic protein-specific transgenic mice from spontaneous autoimmune encephalomyelitis. J Exp Med 1998;188:1883-1894.
74. Apostolou I, von Boehmer H: In vivo instruction of suppressor commitment in naive T cells. J Exp Med 2004;199:1401-1408.
75. Cobbold SP, Castejon R, Adams E, Zelenika D, Graca L, Humm S, Waldmann H: Induction of foxP3+ regulatory T cells in the periphery of T cell receptor transgenic mice tolerized to transplants. J Immunol 2004;172:6003-6010.
76. Fazekas de St Groth B: DCs and peripheral T cell tolerance. Semin Immunol 2001;13:311-322.
77. Roncarolo MG, Levings MK, Traversari C: Differentiation of T regulatory cells by immature dendritic cells. J Exp Med 2001;193:F5-F9.
78. Steinman RM, NussenzweiT MC: Avoiding horror autotoxicus: the importance of dendritic cells in peripheral T cell tolerance. Proc Natl Acad Sci USA 2002;99:351-358.
79. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F: An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999;190: 995-1004.
80. Suri-Payer E, Cantor H: Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4(+)CD25(+) T cells. J Autoimmun 2001;16:115-123.
81. Gorelik L, Flavell RA: Transforming growth factor-beta in T-cell biology. Nat Rev Immunol 2002;2:46-53.
82. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A: Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001;19:683-765.
83. Fahlen L, Read S, Gorelik L, Hurst SD, Coffman RL, Flavell RA, Powrie F: T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J Exp Med 2005;201:737-746.
84. Dieckmann D, Bruett CH, Ploettner H, Lutz MB, Schuler G: Human CD4(+)CD25(+) regulatory, contact-dependent T cells induce interleukin 10-producing, contact-independent type 1-like regulatory T cells. J Exp Med 2002;196:247-253.
85. Jonuleit H, Schmitt E, Kakirman H, Stassen M, Knop J, Enk AH: Infectious tolerance: Human CD25(+) regulatory T cells convey suppressor activity to conventional CD4(a) T helper cells. J Exp Med 2002;196:255-260.
86. Foussat A, Cottrez F, Brun V, Fournier N, Breittmayer JP, Groux H: A comparative study between T regulatory type 1 and CD4aCD25a T cells in the control of inflammation. J Immunol 2003;171:5018-5026.
87. Annacker O, Pimenta-Araujo R, Burlen-Defranoux O, Barbosa TC, Cumano A, Bandeira A: CD25+ CD4+T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J Immunol 2001;166:3008-3018.
88. Martin B, Banz A, Bienvenu B, Cordier C, Dautigny N, Becourt C, Lucas B: Suppression of CD4+ T lymphocyte effector functions by CD4+CD25+ cells in vivo. J Immunol 2004;172: 3391-3398.
89. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F: CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 2003;197: 111-119.
90. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG: A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997;389: 737-742.
91. Sundstedt A, O'Neill EJ, Nicolson KS, Wraith DC: Role for IL-10 in suppression mediated by peptide-induced regulatory T cells in vivo. J Immunol 2003;170:1240-1248.
92. Chen TC, Cobbold SP, Fairchild PJ, Waldmann H: Generation of anergic and regulatory T cells following prolonged exposure to a harmless antigen. J Immunol 2004;172:5900-5907.
93. Grundstrom S, Cederbom L, Sundstedt A, Scheipers P, Ivars F: Superantigen-induced regulatory T cells display different suppressive functions in the presence or absence of natural CD4+CD25+ regulatory T cells in vivo. J Immunol 2003;170:5008-5017.
94. Jonuleit H, Schmitt E, Schuler G, Knop J, Enk AH: Induction of interleukin 10-producing, nonproliferating CD4(+) T cells with regulatory properties by repetitive stimulation with allogeneic immature human dendritic cells. J Exp Med 2000;192:1213-1222.
95. Vieira PL, Christensen JR, Minaee S, O'Neill EJ, Barrat FJ, Boonstra A, Barthlott T, Stockinger B, Wraith DC, 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 2004;172:5986-5993.
96. Barrat FJ, Cua DJ, Boonstra A, Richards DF, Crain C, Savelkoul HF, de Waal-Malefyt R, Coffman RL, Hawrylowicz CM, O'Garra A: In vitro generation of interleukin 10-producing regulatory CD4(+) T cells is induced by immunosuppressive drugs and inhibited by T helper type 1 (Th1)- and Th2- inducing cytokines. J Exp Med 2002;195:603-616.
97. Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, Sharpe AH, Berry G, DeKruyff RH, Umetsu DT: Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med 2002;8:1024-1032.
98. Boussiotis VA, Tsai EY, Yunis EJ, Thim S, Delgado JC, Dascher CC, Berezovskaya A, Rousset D, Reynes JM, Goldfeld AE: IL-10-producing T cells suppress immune responses in anergic tuberculosis patients. J Clin Invest 2000;105:1317-1325.
99. McGuirk P, McCann C, Mills KH: Pathogen-specific T regulatory 1 cells induced in the respiratory tract by a bacterial molecule that stimulates interleukin 10 production by dendritic cells: A novel strategy for evasion of protective T helper type 1 responses by Bordetella pertussis. J Exp Med 2002;195:221-231.
100. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL: Regulatory T cell clones induced by oral tolerance: Suppression of autoimmune encephalomyelitis. Science 1994;265:1237-1240.
101. Weiner HL: Induction and mechanism of action of transforming growth factor-beta-secreting Th3 regulatory cells. Immunol Rev 2001;182:207-214.
102. Zhang X, Izikson L, Liu L, Weiner HL: Activation of CD25+CD4+ regulatory T cells by oral antigen administration. J Immunol 2001;167:4245-4253.
103. Feunou P, Poulin L, Habran C, Le Moine A, Goldman M, Braun MY: CD4+CD25+ and CD4+CD25- T cells act respectively as inducer and effector T suppressor cells in superantigeninduced tolerance. J Immunol 2003;171:3475-3484.
104. Malek TR: The main function of IL-2 is to promote the development of T regulatory cells. J Leukoc Biol 2003;74:961-965.
105. Pontoux C, Banz A, Papiernik M: Natural CD4 CD25(+) regulatory T cells control the burst of superantigen-induced cytokine production: The role of IL-10. Int Immunol 2002;14:233-239.
106. Gutgemann I, Fahrer AM, Altman JD, Davis MM, Chien YH: Induction of rapid T cell activation and tolerance by systemic presentation of an orally administered antigen. Immunity 1998;8:667-673.
107. Thorstenson KM, Khoruts A: Generation of anergic and potentially immunoregulatory CD25+ CD4 T cells in vivo after induction of peripheral tolerance with intravenous or oral antigen. J Immunol 2001;167:188-195.
108. Papiernik M, do Carmo Leite-de-Moraes M, Pontoux C, Joret AM, Rocha B, Penit C, Dy M: T cell deletion induced by chronic infection with mouse mammary tumor virus spares a CD25-positive, IL-10-producing T cell population with infectious capacity. J Immunol 1997;158:4642-4653.
109. Cederbom L, Hall H, Ivars F: CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 2000;30:1538-1543.
110. Thornton AM, Piccirillo CA, Shevach EM: Activation requirements for the induction of CD4+CD25+T cell suppressor function. Eur J Immunol 2004;34:366-376.
111. Fu S, Zhang N, Yopp AC, Chen D, Mao M, Zhang H, Ding Y, Bromberg JS: TGF-beta induces Foxp3+T-regulatory cells from CD4+ CD25- precursors. Am J Transplant 2004;4:1614-1627.
112. Setoguchi R, Hori S, Takahashi T, Sakaguchi S: Homeostatic maintenance of natural Foxp3(+) CD25(+) CD4(+) regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 2005;201:723-735.
113. Acha-Orbea H, Held W, Waanders GA, Shakhov AN, Scarpellino L, Lees RK, MacDonald HR: Exogenous and endogenous mouse mammary tumor virus superantigens. Immunol Rev 1993;131: 5-25.
114. Pape KA, Merica R, Mondino A, Khoruts A, Jenkins MK: Direct evidence that functionally impaired CD4+ T cells persist in vivo following induction of peripheral tolerance. J Immunol 1998;160:4719-4729.
115. Cauley LS, Miller EE, Yen M, Swain SL: Superantigen-induced CD4 T cell tolerance mediated by myeloid cells and IFN-gamma. J Immunol 2000;165:6056-6066.
116. Webb SR, Okamoto A, Ron Y, Sprent J: Restricted tissue distribution of Mlsa determinants. Stimulation of Mlsa-reactive T cells by B cells but not by dendritic cells or macrophages. J Exp Med 1989;169:1-12.
117. Izcue A, Morales G, Minguet S, Sanchez-Movilla A, Morales P, Martinez MJ, Gaspar ML, Marcos MA: Both B and gammadelta TCR(+) lymphocytes regulate alphabeta TCR(+) lymphocytes involved in superantigen specific responses. Eur J Immunol 2001;31:2811-2817.
118. Vacheron S, Luther SA, Acha-Orbea H: Preferential infection of immature dendritic cells and B cells by mouse mammary tumor virus. J Immunol 2002;168:3470-3476.
119. Beutner U, Kraus E, Kitamura D, Rajewsky K, Huber BT: B cells are essential for murine mammary tumor virus transmission, but not for presentation of endogenous superantigens. J Exp Med 1994;179:1457-1466.
120. Bhardwaj N, Young JW, Nisanian AJ, Baggers J, Steinman RM: Small amounts of superantigen, when presented on dendritic cells, are sufficient to initiate T cell responses. J Exp Med 1993;178: 633-642.
121. Muraille EM, De Becker G, Bakkus M, Thielemans K, Urbain J, Moser M, Leo O: Co-stimulation lowers the threshold for activation of naive T cells by bacterial superantigens. Int Immunol 1995;7:295-304.
122. Miethke T, Wahl C, Heeg K, Wagner H: Bacterial superantigens induce T cell unresponsiveness in B cell-deficient mice. Eur J Immunol 1995;25:3187-3190.
123. Fuchs EJ, Matzinger P: B cells turn off virgin but not memory T cells. Science 1992;258: 1156-1159.
124. Eynon EE, Parker DC: Small B cells as antigen-presenting cells in the induction of tolerance to soluble protein antigens. J Exp Med 1992;175:131-138.
125. Kearney ER, Pape KA, Loh DY, Jenkins MK: Visualization of peptide-specific T cell immunity and peripheral tolerance induction in vivo. Immunity 1994;1:327-339.
126. Itano AA, McSorley SJ, Reinhardt RL, Ehst BD, Ingulli E, Rudensky AY, Jenkins MK: Distinct dendritic cell populations sequentially present antigen to CD4 T cells and stimulate different aspects of cell-mediated immunity. Immunity 2003;19:47-57.
127. Yoon S, Bae KL, Shin JY, Yoo HJ, Lee HW, Baek SY, Kim BS, Kim JB, Lee HD: Analysis of the in vivo dendritic cell response to the bacterial superantigen staphylococcal enterotoxin B in the mouse spleen. Histol Histopathol 2001;16:1149-1159.
128. Muraille E, De Trez C, Pajak B, Brait M, Urbain J, Leo O: T cell-dependent maturation of dendritic cells in response to bacterial superantigens. J Immunol 2002;168:4352-4360.
129. Chen Y, Inobe J, Marks R, Gonnella P, Kuchroo VK, Weiner HL: Peripheral deletion of antigenreactive T cells in oral tolerance. Nature 1995;376:177-180.
130. Hammerling GJ, Schonrich G, Momburg F, Auphan N, Malissen M, Malissen B, Schmitt-Verhulst AM, Arnold B: Non-deletional mechanisms of peripheral and central tolerance: Studies with transgenic mice with tissue-specific expression of a foreign MHC class I antigen. Immunol Rev 1991;122: 47-67.
131. Girgis L, Davis MM, Fazekas de St Groth B: The avidity spectrum of T cell receptor interactions accounts for T cell anergy in a double transgenic model. J Exp Med 1999;189:265-278.
132. Jordan MS, Riley MP, von Boehmer H, Caton AJ: Anergy and suppression regulate CD4(+) T cell responses to a self peptide. Eur J Immunol 2000;30:136-144.
133. McCormack JE, Kappler J, Marrack P: Stimulation with specific antigen can block superantigenmediated deletion of T cells in vivo. Proc Natl Acad Sci USA 1994;91:2086-2090.
134. Akira S, TakedaCK, Kaisho T: Toll-like receptors: critical proteins linking innate and acquired immunity. Nat Immunol 2001;2:675-680.
135. Vella AT, McCormack JE, Linsley PS, Kappler JW, Marrack P: Lipopolysaccharide interferes with the induction of peripheral T cell death. Immunity 1995;2:261-270.
136. Nakata Y, Matsuda K, Uzawa A, Nomura M, Akashi M, Suzuki G: Administration of recombinant human IL-1 by Staphylococcus enterotoxin B prevents tolerance induction in vivo. J Immunol 1995;155:4231-4235.
137. Hasko G, Virag L, Egnaczyk G, Salzman AL, Szabo C: The crucial role of IL-10 in the suppression of the immunological response in mice exposed to staphylococcal enterotoxin B. Eur J Immunol 1998;28:1417-1425.
138. Wakkach A, Fournier N, Brun V, Breittmayer JP, Cottrez F, Groux H: Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003;18: 605-617.
139. Svensson M, Maroof A, Ato M, Kaye PM: Stromal cells direct local differentiation of regulatory dendritic cells. Immunity 2004;21:805-816.