Migration rules: Functional properties of naive and effector/memory-like regulatory T cell subsets

Current Topics in Microbiology and Immunology

Volumn 293, Issue , 2005, Pages 89-114

  Huehn, J ^a   Siegmund, K ^a   Hamann, A ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHAEBETA7 INTEGRIN; B7 ANTIGEN; BETA1 INTEGRIN; CD4 ANTIGEN; CD45 ANTIGEN; CD45RO ANTIGEN; CD69 ANTIGEN; CD86 ANTIGEN; CELL MARKER; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR6; CHEMOKINE RECEPTOR CCR7; CHEMOKINE RECEPTOR CXCR3; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; HERMES ANTIGEN; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 2 RECEPTOR ALPHA; KI 67 ANTIGEN; LYMPHOCYTE FUNCTION ASSOCIATED ANTIGEN 1; NEUROPILIN 1; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR RECEPTOR; UNCLASSIFIED DRUG;

ADOPTIVE TRANSFER; ANTIGEN PRESENTING CELL; ANTIGEN SPECIFICITY; AUTOIMMUNE DISEASE; B LYMPHOCYTE; COLITIS; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; INFLAMMATION; LEISHMANIA MAJOR; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE MIGRATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SKIN INFLAMMATION; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; THYMUS;

EID: 20344392877     PISSN: 0070217X     EISSN: None     Source Type: Book Series    
DOI: 10.1007/3-540-27702-1_5     Document Type: Review

References (111)

1. Annacker O, Pimenta-Araujo R, Burlen-Defranoux O, Barbosa TC, Cumano A, Bandeira A (2001) CD25+ CD4+ T cells regulate the expansion of peripheral CD4 T cells through the production of IL-10. J Immunol 166:3008-3018
2. Annacker O, Malmstroem V, Bournbe T, Parker CM, Powrie F (2003) Essential role for CD103 in the T cell-mediated regulation of experimental colitis (abstract). Immunology 110:117
3. Apostolou I, Sarukhan A, Klein L, von Boehmer H (2002) Origin of regulatory T cells with known specificity for antigen. Nat Immunol 3:756-763
4. Apostolou I, von Boehmer H (2004) In vivo induction of suppressor commitment in naive T cells. J Exp Med 199:1401-1408
5. Asano M, Toda M, Sakaguchi N, Sakaguchi S (1996) Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 184:387-396
6. Asseman C, Mauze S, Leach MW, Coffman RL, Powrie F (1999) An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 190:995-1004
7. Austrup F, Rebstock S, Kilshaw PJ, Hamann A (1995) TGF beta1-induced expression of the mucosa-related integrin alpha E on lymphocytes is not associated with mucosa-specific homing. Eur J Immunol 25:1487-1491
8. Austrup F, Vestweber D, Borges E, Löhning M, Bräuer R, Herz U, Renz H, Hallmann R, Scheffold A, Radbruch A, Hamann A (1997) P-and E-selectin mediate recruitment of T helper 1 but not T helper 2 cells into inflamed tissues. Nature 385:81-83
9. Banz A, Peixoto A, Pontoux C, Cordier C, Rocha B, Papiernik M (2003) A unique subpopulation of CD4+ cells regulatory T cells controls wasting disease IL-10 secretion and T cell homeostasis. Eur J Imm 33:2419-2428
10. Belkaid Y, Piccirillo CA, Mendez S, Shevach EM, Sacks DL (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420:502-507
11. Bluestone JA, Abbas AK (2003) Natural versus adaptive regulatory T cells. Nat Rev Immunol 3:253-257
12. Brown DC, Gatter KC (2002) Ki67 protein: the immaculate deception? Histopathology 40:2-11
13. Bruder D, Probst-Kepper M, Westendorf AM, Geffers R, Beissert S, Loser K, von Boehmer H, Buer J, Hansen W (2004) Neuropilin-1: a surface marker of regulatory T cells. Eur J Immunol 34:623-630
14. Bruhl H, Cihak J, Schneider MA, Plachy J, Rupp T, Wenzel I, Shakarami M, Milz S, Ellwart JW, Stangassinger M et al (2004) Dual role of CCR2 during initiation and progression of collagen-induced arthritis: evidence for regulatory activity of CCR2+ T cells. J Immunol 172:890-898
15. Bystry RS, Aluvihare V, Welch KA, Kallikourdis M, Betz AG (2001) B cells and professional APCs recruit regulatory T cells via CCL4. Nat Immunol 2:1126-1132
16. Campbell DJ, Butcher EC (2002) Rapid acquisition of tissue-specific homing phenotypes by CD4+ T cells activated in cutaneous or mucosal lymphoid tissues. J Exp Med 195:135-141
17. Cao D, Malmstrom V, Baecher-Allan C, Hafler D, Klareskog L, Trollmo C (2003) Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur J Immunol 33:215-223
18. Cederbom L, Hall H, Ivars F (2000) CD4+CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 30:1538-1543
19. Cepek KL, Shaw SK, Parker CM, Russell GJ, Morrow JS, Rimm DL, Brenner MB (1994) Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the alpha E beta 7 integrin. Nature 372:190-193
20. Cerf-Bensussan N, Jarry A, Brousse N, Lisowska-Grospierre B, Guy-Grand D, Griscelli C (1987) A monoclonal antibody (HML-1) defining a novel membrane molecule present on human intestinal lymphocytes. Eur J Immunol 17:1279-1285
21. Chen Y, Kuchroo VK, Inobe J, Hafler DA, Weiner HL (1994) Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265:1237-1240
22. Colantonio L, Iellem A, Sinigaglia F, D'Ambrosio D (2002) Skin-homing CLA+ T cells and regulatory CD25+ T cells represent major subsets of human peripheral blood memory T cells migrating in response to CCL1/I-309. Eur J Immunol 32:3506-3514
23. Cozzo C, Larkin J 3rd, Caton AJ (2003) Cutting edge: self-peptides drive the peripheral expansion of CD4+CD25+ regulatory T cells. J Immunol 171:5678-5682
24. Dittmer U, He H, Messer RJ, Schimmer S, Olbrich AR, Ohlen C, Greenberg PD, Stromnes IM, Iwashiro M, Sakaguchi S et al (2004) Functional impairment of CD8(+) T cells by regulatory T cells during persistent retroviral infection. Immunity 20:293-303
25. Fisson S, Darrasse-Jeze G, Litvinova E, Septier F, Klatzmann D, Liblau R, Salomon BL (2003) Continuous activation of autoreactive CD4+ CD25+ regulatory T cells in the steady state. J Exp Med 198:737-746
26. Fontenot JD, Gavin MA, Rudensky AY (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 4:330-336
27. Forster R, Schubel A, Breitfeld D, Kremmer E, Renner Muller I, Wolf E, Lipp M (1999) CCR7 coordinates the primary immune response by establishing functional microenvironments in secondary lymphoid organs. Cell 99:23-33
28. Fu S, Yopp AC, Mao X, Chen D, Zhang N, Mao M, Ding Y, Bromberg JS (2004) CD4+ CD25+ CD62+ T-regulatory cell subset has optimal suppressive and proliferative potential. Am J Transplant 4:65-78
29. Gallatin WM, Weissman IL, Butcher EC (1983) A cell-surface molecule involved in organ-specific homing of lymphocytes. Nature 304:30-34
30. Gambineri E, Torgerson TR, Ochs HD (2003) Immune dysregulation, polyendocrinopathy, enteropathy X-linked inheritance (IPEX), a syndrome of systemic autoimmunity caused by mutations of FOXP3, a critical regulator of T-cell homeostasis. Curr Opin Rheumatol 15:430-435
31. Gavin M, Rudensky A (2003) Control of immune homeostasis by naturally arising regulatory CD4+ T cells. Curr Opin Immunol 15:690-696
32. Gavin MA, Clarke SR, Negrou E, Gallegos A, Rudensky A (2002) Homeostasis and anergy of CD4+CD25+ suppressor T cells in vivo. Nat Immunol 3:33-41
33. Gershon RK (1975) A disquisition on suppressor T cells. Transplant Rev 26:170-185
34. Gershon RK, Kondo K (1970) Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology 18:723-737
35. Goulvestre C, Batteux F, Charreire J (2002) Chemokines modulate experimental autoimmune thyroiditis through attraction of autoreactive or regulatory T cells. Eur J Immunol 32:3435-3442
36. Graca L, Cobbold SP, Waldmann H (2002) Identification of regulatory T cells in tolerated allografts. J Exp Med 195:1641-1646
37. Green EA, Choi Y, Flavell RA (2002) Pancreatic lymph node-derived CD4(+)CD25(+) Treg cells: highly potent regulators of diabetes that require TRANCE-RANK signals. Immunity 16:183-191
38. Groux H, O'Garra A, Bigler M, Rouleau M, Antonenko S, de Vries JE, Roncarolo MG (1997) A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389:737-742
39. Hamann Andrew DP, Jablonski-Westrich D, Holzmann B, Butcher EC (1994) Role of a4-integrins in lymphocyte homing to mucosal tissues in vivo. J Immunol 152:3282-3293
40. Herbelin A, Gombert JM, Lepault F, Bach JF, Chatenoud L (1998) Mature mainstream TCR alpha beta+CD4+ thymocytes expressing L-selectin mediate "active tolerance" in the nonobese diabetic mouse. J Immunol 161:2620-2628
41. Hori S, Carvalho TL, Demengeot J (2002a) CD25+CD4+ regulatory T cells suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur J Immunol 32:1282-1291
42. Hori S, Haury M, Coutinho A, Demengeot J (2002b) Specificity requirements for selection and effector functions of CD25+4+ regulatory T cells in anti-myelin basic protein T cell receptor transgenic mice. Proc Natl Acad Sci U S A 99:8213-8218
43. Hori S, Haury M, Lafaille JJ, Demengeot J, Coutinho A (2002c) Peripheral expansion of thymus-derived regulatory cells in anti-myelin basic protein T cell receptor transgenic mice. Eur J Immunol 32:3729-3735
44. Hori S, Nomura T, Sakaguchi S (2003a) Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-1061
45. Hori S, Takahashi T, Sakaguchi S (2003b) Control of autoimmunity by naturally arising regulatory CD4+ T cells. Adv Immunol 81:331-371
46. Huehn J, Siegmund K, Lehmann J, Siewert C, Haubold U, Feuerer M, Debes GF, Lauber J, Frey O, Przybylski GK et al (2004) Developmental stage, phenotype and migration distinguish naive- and effector/memory-like CD4+ regulatory T cells. J Exp Med 199:303-313
47. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, Sinigaglia F, D'Ambrosio D (2001) Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 194:847-853
48. Iellem A, Colantonio L, D'Ambrosio D (2003) Skin-versus gut-skewed homing receptor expression and intrinsic CCR4 expression on human peripheral blood CD4+CD25+ suppressor T cells. Eur J Immunol 33:1488-1496
49. Itoh M, Takahashi T, Sakaguchi N, Kuniyasu Y, Shimizu J, Otsuka F, Sakaguchi S (1999) Thymus and autoimmunity: production of CD25+CD4+ naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 162:5317-5326
50. Jacob J, Baltimore D (1999) Modelling T-cell memory by genetic marking of memory T cells in vivo [see comments]. Nature 399:593-597
51. Janssens W, Carlier V, Wu B, VanderElst L, Jacquemin MG, Saint-Remy JM (2003) CD4+CD25+ T cells lyse antigen-presenting B cells by Fas-Fas ligand interaction in an epitope-specific manner. J Immunol 171:4604-4612
52. Jonuleit H, Schmitt E (2003) The regulatory T cell family: distinct subsets and their interrelations. J Immunol 171:6323-6327
53. Jordan MS, Boesteanu A, Reed AJ, Petrone AL, Holenbeck AE, Lerman MA, Naji A, Caton AJ (2001) Thymic selection of CD4+CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2:301-306
54. Karim M, Kingsley CI, Bushell AR, Sawitzki BS, Wood KJ (2004) Alloantigen-induced CD25+CD4+ regulatory T cells can develop in vivo from CD25-CD4+ precursors in a thymus-independent process. J Immunol 172:923-928
55. Kawahata K, Misaki Y, Yamauchi M, Tsunekawa S, Setoguchi K, Miyazaki J, Yamamoto K (2002) Generation of CD4(+)CD25(+) regulatory T cells from autoreactive T cells simultaneously with their negative selection in the thymus and from nonautoreactive T cells by endogenous TCR expression. J Immunol 168:4399-4405
56. Khattri R, Cox T, Yasayko SA, Ramsdell F (2003) An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 4:337-342
57. Kilshaw PJ, Murant SJ (1991) Expression and regulation of beta 7(beta p) integrins on mouse lymphocytes: relevance to the mucosal immune system. Eur J Immunol 21:2591-2597
58. Klein L, Khazaie K, von Boehmer H (2003) In vivo dynamics of antigen-specific regulatory T cells not predicted from behavior in vitro. Proc Natl Acad Sci U S A 100:8886-8891
59. Kullberg MC, Jankovic D, Gorelick PL, Caspar P, Letterio JJ, Cheever AW, Sher A (2002) Bacteria-triggered CD4(+) T regulatory cells suppress Helicobacter hepaticus-induced colitis. J Exp Med 196:505-515
60. Kuniyasu Y, Takahashi T, Itoh M, Shimizu J, Toda G, Sakaguchi S (2000) Naturally anergic and suppressive CD25(+)CD4(+) T cells as a functionally and phenotypically distinct immunoregulatory T cell subpopulation. Int Immunol 12:1145-1155
61. Lefrancois L, Parker CM, Olson S, Muller W, Wagner N, Puddington L (1999) The role of beta7 integrins in CD8 T cell trafficking during an antiviral immune response. J Exp Med 189:1631-1638
62. Lehmann J, Huehn J, Rosa MDI, Maszyna F, Kretschmer U, Brunner M, Scheffold A, Krenn V, Hamann A (2002) Expression of the integrin alphaEbeta7 identifies unique subsets of CD25+ as well as CD25-regulatory T cells. Proceed Natl Acad Sci U S A 99:13031-13036
63. Lepault F, Gagnerault MC (2000) Characterization of peripheral regulatory CD4+ T cells that prevent diabetes onset in nonobese diabetic mice. J Immunol 164:240-247
64. Luther SA, Tang HL, Hyman PL, Farr AG, Cyster JG (2000) Coexpression of the chemokines ELC and SLC by T zone stromal cells and deletion of the ELC gene in the plt/plt mouse. Proc Natl Acad Sci U S A 97:12694-12699
65. Mackay CR, Marston WL, Dudler L (1990) Naive and memory T cells show distinct pathways of lymphocyte recirculation. J Exp Med 171:801-817
66. Maloy KJ, Powrie F (2001) Regulatory T cells in the control of immune pathology. Nat Immunol 2:816-822
67. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F (2003) CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 197:111-119
68. Masopust D, Vezys V, Marzo AL, Lefrancois L (2001) Preferential localization of effector memory cells in nonlymphoid tissue. Science 291:2413-2417
69. McHugh R, Whitters MJ, Piccorillo CA, Young DA, Shevach EM, Collins M, Byrne MC (2002) CD4+CD25+ immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 16:311-323
70. Moser B, Loetscher P (2001) Lymphocyte traffic control by chemokines. Nat Immunol 2:123-128
71. Mottet C, Uhlig HH, Powrie F (2003) Cutting edge: cure of colitis by CD4(+)CD25(+) regulatory T cells. J Immunol 170:3939-3943
72. Murakami M, Sakamoto A, Bender J, Kappler J, Marrack P (2002) CD25+CD4+ T cells contribute to the control of memory CD8+ T cells. Proc Natl Acad Sci U S A 99:8832-8837
73. Nakamura K, Kitani A, Strober W (2001) Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta. J Exp Med 194:629-644
74. Nascimbeni M, Shin EC, Chiriboga L, Kleiner DE, Rehermann B (2004) Peripheral CD4/CD8 double-positive T cells are differentiated effector memory cells with antiviral functions. Blood 104:478-486
75. Oldenhove G, de Heusch M, Urbain-Vansanten G, Urbain J, Maliszewski C, Leo O, Moser M (2003) CD4+ CD25+ regulatory T cells control T helper cell type 1 responses to foreign antigens induced by mature dendritic cells in vivo. J Exp Med 198:259-266
76. Pacholczyk R, Kraj P, Ignatowicz L (2002) Peptide specificity of thymic selection of CD4+CD25+ T cells. J Immunol 168:613-620
77. Papiernik M, de Moraes ML, Pontoux C, Vasseur F, Penit C (1998) Regulatory CD4 T cells: expression of IL-2R alpha chain, resistance to clonal deletion and IL-2 dependency. Int Immunol 10:371-378
78. Piccirillo CA, Shevach EM (2001) Cutting edge: control of cd8(+) t cell activation by cd4(+)cd25(+) immunoregulatory cells. J Immunol 167:1137-1140
79. Piccirillo CA, Letterio JJ, Thornton AM, McHugh RS, Mamura M, Mizuhara H, Shevach EM (2002) CD4(+)CD25(+) regulatory T cells can mediate suppressor function in the absence of transforming growth factor beta1 production and responsiveness. J Exp Med 196:237-246
80. Powrie F, Carlino J, Leach MW, Mauze S, Coffman RL (1996) 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 183:2669-2674
81. Prud'homme GJ, Piccirillo CA (2000) The inhibitory effects of transforming growth factor-beta-1 (TGF-beta1) in autoimmune diseases. J Autoimmun 14:23-42
82. Read S, Malmstrom V, Powrie F (2000) 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 192:295-302
83. Romagnoli P, Hudrisier D, van Meerwijk JP (2002) Preferential recognition of self antigens despite normal thymic deletion of CD4(+)CD25(+) regulatory T cells. J Immunol 168:1644-1648
84. Roncarolo MG, Bacchetta R, Bordignon C, Narula S, Levings MK (2001) Type 1 T regulatory cells. Immunol Rev 182:68-79
85. Sakaguchi S (2004) Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 22:531-562
86. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M (1995) 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 155:1151-1164
87. Sakaguchi S, Hori S, Fukui Y, Sasazuki T, Sakaguchi N, Takahashi T (2003) Thymic generation and selection of CD25+CD4+ regulatory T cells: implications of their broad repertoire and high self-reactivity for the maintenance of immunological self-tolerance. Novartis Found Symp 252:6-16; discussion 16-23, 106-114
88. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A, Bluestone JA (2000) B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431-440
89. Schon MP, Arya A, Murphy EA, Adams CM, Strauch UG, Agace WW, Marsal J, Donohue JP, Her H, Beier DR et al (1999) Mucosal T lymphocyte numbers are selectively reduced in integrin alpha E (CD103)-deficient mice. J Immunol 162:6641-6649
90. Schon MP, Schon M, Warren HB, Donohue JP, Parker CM (2000) Cutaneous inflammatory disorder in integrin alphaE (CD103)-deficient mice. J Immunol 165:6583-6589
91. Schwarz A, Maeda A, Wild MK, Kernebeck K, Gross N, Aragane Y, Beissert S, Vestweber D, Schwarz T (2004) Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J Immunol 172:1036-1043
92. Sebastiani S, Allavena P, Albanesi C, Nasorri F, Biancchi G, Traidl C, Sozzani S, Girolomoni G, Cavani A (2001) Chemokine receptor expression and function in CD4+ T Lymphocytes with regulatory activity 1. J Immunol 166:996-1002
93. Shevach EM (2002) CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2:389-400
94. Shimizu J, Yamazaki S, Takahashi T, Ishida Y, Sakaguchi S (2002) Stimulation of CD25(+)CD4(+) regulatory T cells through GITR breaks immunological self-tolerance. Nat Immunol 3:135-142
95. Stassen M, Fondel S, Bopp T, Richter C, Müller C, Kubach J, Becker C, Knop J, Enk AH, Schmitt S, Schmitt E, Jonuleit H (2004) Human CD25+ regulatory T cells: two subsets defined by the integrins a4b7 or a4b1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 34:1303-1311
96. Stephens LA, Mason D (2000) CD25 is a marker for CD4+ thymocytes that prevent autoimmune diabetes in rats, but peripheral T cells with this function are found in both CD25+ and CD25- subpopulations. J Immunol 165:3105-3110
97. Suri-Payer E, Cantor H (2001) Differential cytokine requirements for regulation of autoimmune gastritis and colitis by CD4(+)CD25(+) T cells. J Autoimmun 16:115-123
98. Suvas S, Kumaraguru U, Pack CD, Lee S, Rouse BT (2003) CD4+CD25+ T cells regulate virus-specific primary and memory CD8+ T cell responses. J Exp Med 198:889-901
99. Szanya V, Ermann J, Taylor C, Holness C, Fathman CG (2002) The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7. J Immunol 169:2461-2465
100. Takahashi T, Kuniyasu Y, Toda M, Sakaguchi N, Itoh M, Iwata M, Shimizu J, Sakaguchi S (1998) 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 10:1969-1980
101. Takahashi T, Tagami T, Yamazaki S, Uede T, Shimizu J, Sakaguchi N, Mak TW, Sakaguchi S (2000) Immunologic self-tolerance maintained by CD25(+)CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 192:303-310
102. Thornton AM, Shevach EM (1998) CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188:287-296
103. Thornton AM, Shevach EM (2000) Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J Immunol 164:183-190
104. Thorstenson KM, Khoruts A (2001) Generation of anergic and potentially immunoregulatory CD25+CD4 T cells in vivo after induction of peripheral tolerance with intravenous or oral antigen. J Immunol 167:188-195
105. Tietz W, Allemand Y, Borges E, Laer DV, Hallmann R, Vestweber D, Hamann A (1998) CD4+ T-cells only migrate into inflamed skin if they express ligands for E- and P-selectin. J Immunol 161:963-970
106. Von Boehmer H (2003) Dynamics of suppressor T cells: in vivo veritas. J Exp Med 198:845-849
107. Walker LS, Chodos A, Eggena M, Dooms H, Abbas AK (2003) Antigen-dependent proliferation of CD4+ CD25+ regulatory T cells in vivo. J Exp Med 198:249-258
108. Weiner HL (2001) Oral tolerance: immune mechanisms and the generation of Th3-type TGF-beta-secreting regulatory cells. Microbes Infect 3:947-954
109. Woo EY, Yeh H, Chu CS, Schlienger K, Carroll RG, Riley JL, Kaiser LR, June CH (2002) Cutting edge: regulatory T cells from lung cancer patients directly inhibit autologous T cell proliferation. J Immunol 168:4272-4276
110. Yamazaki S, Iyoda T, Tarbell K, Olson K, Velinzon K, Inaba K, Steinman rm (2003) Direct expansion of functional CD25+ CD4+ regulatory T cells by antigen-processing dendritic cells. J Exp Med 198:235-247
111. Zelenika D, Adams E, Humm S, Graca L, Thompson S, Cobbold SP, Waldmann H (2002) Regulatory T cells overexpress a subset of th2 gene transcripts. J Immunol 168:1069-1079