Regulatory T-cells in systemic lupus erythematosus and rheumatoid arthritis

FEBS Letters

Volumn 585, Issue 23, 2011, Pages 3603-3610

  Chavele, Konstantia Maria ^a   Ehrenstein, Michael R ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Autoimmunity; RA; Regulatory T cells (Tregs); SLE

Indexed keywords

CD3 ANTIBODY; CD4 ANTIGEN; CD69 ANTIGEN; CORTICOSTEROID; DICER; INFLIXIMAB; INTERLEUKIN 1; INTERLEUKIN 15; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 7 RECEPTOR; L SELECTIN; MICRORNA; RITUXIMAB; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA INHIBITOR;

ADOPTIVE TRANSFER; AUTOIMMUNITY; B LYMPHOCYTE ACTIVATION; CD4+ CD25+ T LYMPHOCYTE; CELL ACTIVATION; CYTOKINE PRODUCTION; DISEASE MODEL; EFFECTOR CELL; HUMAN; IMMUNOLOGICAL TOLERANCE; INFLAMMATION; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PATHOGENESIS; PHENOTYPE; PLASMAPHERESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; TREATMENT OUTCOME;

ANIMALS; ARTHRITIS, RHEUMATOID; DISEASE MODELS, ANIMAL; HUMANS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MODELS, IMMUNOLOGICAL; T-LYMPHOCYTES, REGULATORY;

MURINAE;

EID: 81755184312     PISSN: 00145793     EISSN: 18733468     Source Type: Journal    
DOI: 10.1016/j.febslet.2011.07.043     Document Type: Review

References (116)

1. M.R. Walker Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+CD25- T cells J. Clin. Invest. 112 9 2003 1437 1443 (Pubitemid 38057697)
2. S. Sakaguchi Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease Immunol. Rev. 212 2006 8 27 (Pubitemid 44116697)
3. C. Baecher-Allan CD4+CD25high regulatory cells in human peripheral blood J. Immunol. 167 3 2001 1245 1253 (Pubitemid 32703119)
4. S. Sakaguchi 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 3 1995 1151 1164
5. W. Liu CD127 expression inversely correlates with FoxP3 and suppressive function of human CD4+ T reg cells J. Exp. Med. 203 7 2006 1701 1711 (Pubitemid 44036276)
6. N. Seddiki Expression of interleukin (IL)-2 and IL-7 receptors discriminates between human regulatory and activated T cells J. Exp. Med. 203 7 2006 1693 1700 (Pubitemid 44036275)
7. J.D. Fontenot, M.A. Gavin, and A.Y. Rudensky Foxp3 programs the development and function of CD4+CD25+ regulatory T cells Nat. Immunol. 4 4 2003 330 336 (Pubitemid 36432314)
8. S. Hori, T. Nomura, and S. Sakaguchi Control of regulatory T cell development by the transcription factor Foxp3 Science 299 5609 2003 1057 1061 (Pubitemid 36222930)
9. R. Khattri An essential role for Scurfin in CD4+CD25+ T regulatory cells Nat. Immunol. 4 4 2003 337 342 (Pubitemid 36432315)
10. M.E. Brunkow Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorDer of the scurfy mouse Nat. Genet. 27 1 2001 68 73 (Pubitemid 32044521)
11. J.M. Kim, J.P. Rasmussen, and A.Y. Rudensky Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice Nat. Immunol. 8 2 2007 191 197 (Pubitemid 46152650)
12. C.L. Bennett The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3 Nat. Genet. 27 1 2001 20 21 (Pubitemid 32044513)
13. R.S. Wildin X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy Nat. Genet. 27 1 2001 18 20 (Pubitemid 32044512)
14. M.A. Gavin Single-cell analysis of normal and FOXP3-mutant human T cells: FOXP3 expression without regulatory T cell development Proc. Natl. Acad. Sci. U.S.A. 103 17 2006 6659 6664
15. D.Q. Tran, H. Ramsey, and E.M. Shevach Induction of FOXP3 expression in naive human CD4+FOXP3 T cells by T-cell receptor stimulation is transforming growth factor-beta dependent but does not confer a regulatory phenotype Blood 110 8 2007 2983 2990 (Pubitemid 350006952)
16. D. Getnet A role for the transcription factor Helios in human CD4(+)CD25(+) regulatory T cells Mol. Immunol. 47 7-8 2010 1595 1600
17. A.M. Thornton Expression of Helios, an Ikaros transcription factor family member, differentiates thymic-derived from peripherally induced Foxp3+ T regulatory cells J. Immunol. 184 7 2010 3433 3441
18. P.C. Janson FOXP3 promoter demethylation reveals the committed Treg population in humans PLoS One 3 2 2008 e1612
19. M. Miyara Functional delineation and differentiation dynamics of human CD4+ T cells expressing the FoxP3 transcription factor Immunity 30 6 2009 899 911
20. M. Vukmanovic-Stejic Human CD4+ CD25hi Foxp3+ regulatory T cells are derived by rapid turnover of memory populations in vivo J. Clin. Invest. 116 9 2006 2423 2433 (Pubitemid 44330141)
21. A.M. Thornton, and E.M. Shevach CD4+CD25+ immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production J. Exp. Med. 188 2 1998 287 296 (Pubitemid 28357757)
22. T. Takahashi 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 12 1998 1969 1980 (Pubitemid 28566059)
23. L.S. Taams Modulation of monocyte/macrophage function by human CD4+CD25+ regulatory T cells Hum. Immunol. 66 3 2005 222 230 (Pubitemid 40395242)
24. D.M. Zhao Activated CD4+CD25+ T cells selectively kill B lymphocytes Blood 107 10 2006 3925 3932
25. N. Misra Cutting edge: human CD4+CD25+ T cells restrain the maturation and antigen-presenting function of dendritic cells J. Immunol. 172 8 2004 4676 4680 (Pubitemid 38456386)
26. K. Nakamura, A. Kitani, and W. Strober Cell contact-dependent immunosuppression by CD4(+)CD25(+) regulatory T cells is mediated by cell surface-bound transforming growth factor beta J. Exp. Med. 194 5 2001 629 644 (Pubitemid 32844773)
27. L.W. Collison The inhibitory cytokine IL-35 contributes to regulatory T-cell function Nature 450 7169 2007 566 569 (Pubitemid 350190247)
28. Y.P. Rubtsov Regulatory T cell-derived interleukin-10 limits inflammation at environmental interfaces Immunity 28 4 2008 546 558
29. T. De Smedt Effect of interleukin-10 on dendritic cell maturation and function Eur. J. Immunol. 27 5 1997 1229 1235 (Pubitemid 27197228)
30. M.A. Gavin Foxp3-dependent programme of regulatory T-cell differentiation Nature 445 7129 2007 771 775 (Pubitemid 46279714)
31. W.J. Grossman Human T regulatory cells can use the perforin pathway to cause autologous target cell death Immunity 21 4 2004 589 601 (Pubitemid 39370513)
32. P. Pandiyan CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells Nat. Immunol. 8 12 2007 1353 1362 (Pubitemid 350131172)
33. N. Oberle Rapid suppression of cytokine transcription in human CD4+CD25 T cells by CD4+Foxp3+ regulatory T cells: independence of IL-2 consumption, TGF-beta, and various inhibitors of TCR signaling J. Immunol. 179 6 2007 3578 3587
34. T. Bopp Cyclic adenosine monophosphate is a key component of regulatory T cell-mediated suppression J. Exp. Med. 204 6 2007 1303 1310 (Pubitemid 46919868)
35. S. Deaglio Adenosine generation catalyzed by CD39 and CD73 expressed on regulatory T cells mediates immune suppression J. Exp. Med. 204 6 2007 1257 1265 (Pubitemid 46919862)
36. G. Borsellino Expression of ectonucleotidase CD39 by Foxp3+ Treg cells: hydrolysis of extracellular ATP and immune suppression Blood 110 4 2007 1225 1232 (Pubitemid 47281420)
37. J.J. Kobie T regulatory and primed uncommitted CD4 T cells express CD73, which suppresses effector CD4 T cells by converting 5'-adenosine monophosphate to adenosine J. Immunol. 177 10 2006 6780 6786 (Pubitemid 44715042)
38. P.E. Zarek A2A receptor signaling promotes peripheral tolerance by inducing T-cell anergy and the generation of adaptive regulatory T cells Blood 111 1 2008 251 259
39. C. Oderup Cytotoxic T lymphocyte antigen-4-dependent down-modulation of costimulatory molecules on dendritic cells in CD4+ CD25+ regulatory T-cell-mediated suppression Immunology 118 2 2006 240 249 (Pubitemid 43727429)
40. O.S. Qureshi Trans-endocytosis of CD80 and CD86: A molecular basis for the cell-extrinsic function of CTLA-4 Science 332 6029 2011 600 603
41. D.H. Munn, M.D. Sharma, and A.L. Mellor Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2, 3-dioxygenase activity in dendritic cells J. Immunol. 172 7 2004 4100 4110 (Pubitemid 38375222)
42. O. Manches HIV-activated human plasmacytoid DCs induce Tregs through an indoleamine 2, 3-dioxygenase-dependent mechanism J. Clin. Invest. 118 10 2008 3431 3439
43. M. Brenk Tryptophan deprivation induces inhibitory receptors ILT3 and ILT4 on dendritic cells favoring the induction of human CD4+CD25+ Foxp3+ T regulatory cells J. Immunol. 183 1 2009 145 154
44. T. Hayashi, K. Hasegawa, and C. Adachi Elimination of CD4(+)CD25(+) T cell accelerates the development of glomerulonephritis during the preactive phase in autoimmune-prone female NZB x NZW F mice Int. J. Exp. Pathol. 86 5 2005 289 296 (Pubitemid 41413624)
45. H. Bagavant, and K.S. Tung Failure of CD25+ T cells from lupus-prone mice to suppress lupus glomerulonephritis and sialoadenitis J. Immunol. 175 2 2005 944 950 (Pubitemid 41094978)
46. K.J. Scalapino Suppression of disease in New Zealand Black/New Zealand White lupus-prone mice by adoptive transfer of ex vivo expanded regulatory T cells J. Immunol. 177 3 2006 1451 1459 (Pubitemid 44092478)
47. Y. Chen, C. Cuda, and L. Morel Genetic determination of T cell help in loss of tolerance to nuclear antigens J. Immunol. 174 12 2005 7692 7702 (Pubitemid 40806274)
48. W.T. Hsu, J.L. Suen, and B.L. Chiang The role of CD4CD25 T cells in autoantibody production in murine lupus Clin. Exp. Immunol. 145 3 2006 513 519
49. C.M. Cuda Murine lupus susceptibility locus Sle1a controls regulatory T cell number and function through multiple mechanisms J. Immunol. 179 11 2007 7439 7447
50. A.N. Theofilopoulos Splenic immunoglobulin-secreting cells and their regulation in autoimmune mice J. Exp. Med. 151 2 1980 446 466 (Pubitemid 10139753)
51. C.E. Zielinski Naive CD4+ T cells from lupus-prone Fas-intact MRL mice display TCR-mediated hyperproliferation due to intrinsic threshold defects in activation J. Immunol. 174 8 2005 5100 5109
52. C.R. Monk MRL/Mp CD4+, CD25- T cells show reduced sensitivity to suppression by CD4+, CD25+ regulatory T cells in vitro: A novel defect of T cell regulation in systemic lupus erythematosus Arthritis Rheum. 52 4 2005 1180 1184 (Pubitemid 40530125)
53. A.A. Divekar Dicer insufficiency and microRNA-155 overexpression in lupus regulatory T cells: an apparent paradox in the setting of an inflammatory milieu J. Immunol. 186 2 2011 924 930
54. J.L. Zhang CD3 mAb treatment ameliorated the severity of the cGVHD-induced lupus nephritis in mice by up-regulation of Foxp3+ regulatory T cells in the target tissue: kidney Transpl. Immunol. 24 1 2010 17 25
55. J.C. Crispin, A. Martinez, and J. Alcocer-Varela Quantification of regulatory T cells in patients with systemic lupus erythematosus J. Autoimmun. 21 3 2003 273 276 (Pubitemid 37410115)
56. A. Fathy Diminished CD4+CD25+ T-lymphocytes in peripheral blood of patients with systemic lupus erythematosus Egypt J. Immunol. 12 1 2005 25 31
57. J.H. Lee Inverse correlation between CD4+ regulatory T-cell population and autoantibody levels in paediatric patients with systemic lupus erythematosus Immunology 117 2 2006 280 286
58. X.Y. Yang Clinical significance of CD4+CD25+ T cells in peripheral blood of patients in systemic lupus erythematosus Zhonghua Nei Ke Za Zhi 44 8 2005 570 572
59. M. Bonelli Foxp3 expression in CD4+ T cells of patients with systemic lupus erythematosus: A comparative phenotypic analysis Ann. Rheum. Dis. 67 5 2008 664 671 (Pubitemid 351571931)
60. M. Miyara Global natural regulatory T cell depletion in active systemic lupus erythematosus J. Immunol. 175 12 2005 8392 8400 (Pubitemid 41798406)
61. X. Valencia Deficient CD4+CD25high T regulatory cell function in patients with active systemic lupus erythematosus J. Immunol. 178 4 2007 2579 2588 (Pubitemid 46233461)
62. H.Y. Lee Altered frequency and migration capacity of CD4+CD25+ regulatory T cells in systemic lupus erythematosus Rheumatology (Oxford) 47 6 2008 789 794
63. A. Suarez Enrichment of CD4+ CD25high T cell population in patients with systemic lupus erythematosus treated with glucocorticoids Ann. Rheum. Dis. 65 11 2006 1512 1517 (Pubitemid 44629132)
64. S. Barath The severity of systemic lupus erythematosus negatively correlates with the increasing number of CD4+CD25(high)FoxP3+ regulatory T cells during repeated plasmapheresis treatments of patients Autoimmunity 40 7 2007 521 528 (Pubitemid 351233173)
65. P.P. Sfikakis Increased expression of the FoxP3 functional marker of regulatory T cells following B cell depletion with rituximab in patients with lupus nephritis Clin. Immunol. 123 1 2007 66 73 (Pubitemid 46401511)
66. T. Vallerskog Treatment with rituximab affects both the cellular and the humoral arm of the immune system in patients with SLE Clin. Immunol. 122 1 2007 62 74 (Pubitemid 46026695)
67. R.K. Venigalla Reduced CD4+, CD25- T cell sensitivity to the suppressive function of CD4+, CD25high, CD127 -/low regulatory T cells in patients with active systemic lupus erythematosus Arthritis Rheum. 58 7 2008 2120 2130 (Pubitemid 351988104)
68. J. Yates Natural regulatory T cells: number and function are normal in the majority of patients with lupus nephritis Clin. Exp. Immunol. 153 1 2008 44 55 (Pubitemid 351809334)
69. B. Franz Low number of regulatory T cells in skin lesions of patients with cutaneous lupus erythematosus Arthritis Rheum. 56 6 2007 1910 1920 (Pubitemid 47110390)
70. E.Y. Lyssuk Reduced number and function of CD4+CD25highFoxP3+ regulatory T cells in patients with systemic lupus erythematosus Adv. Exp. Med. Biol. 601 2007 113 119
71. S. Barath Measurement of natural (CD4+CD25high) and inducible (CD4+IL-10+) regulatory T cells in patients with systemic lupus erythematosus Lupus 16 7 2007 489 496 (Pubitemid 47242522)
72. S.S. Zhao Expression of CD4+ CD25+ CD127(low/-) T cells in patients with systemic lupus erythematosus Zhonghua Yi Xue Za Zhi 88 7 2008 453 456
73. S.C. Lin The quantitative analysis of peripheral blood FOXP3-expressing T cells in systemic lupus erythematosus and rheumatoid arthritis patients Eur. J. Clin. Invest. 37 12 2007 987 996
74. B. Yan Dysfunctional CD4+, CD25+ regulatory T cells in untreated active systemic lupus erythematosus secondary to interferon-alpha-producing antigen-presenting cells Arthritis Rheum. 58 3 2008 801 812 (Pubitemid 351364878)
75. B. Zhang Clinical significance of increased CD4+CD25-Foxp3+ T cells in patients with new-onset systemic lupus erythematosus Ann. Rheum. Dis. 67 7 2008 1037 1040 (Pubitemid 351956671)
76. E.C. Jury Abnormal CTLA-4 function in T cells from patients with systemic lupus erythematosus Eur. J. Immunol. 40 2 2010 569 578
77. M. Bonelli Phenotypic and functional analysis of CD4+ CD25- Foxp3+ T cells in patients with systemic lupus erythematosus J. Immunol. 182 3 2009 1689 1695
78. S. Mellor-Pita Decrease of regulatory T cells in patients with systemic lupus erythematosus Ann. Rheum. Dis. 65 4 2006 553 554
79. M. Bonelli Quantitative and qualitative deficiencies of regulatory T cells in patients with systemic lupus erythematosus (SLE) Int. Immunol. 20 7 2008 861 868 (Pubitemid 351876312)
80. M.I. Vargas-Rojas Quantitative and qualitative normal regulatory T cells are not capable of inducing suppression in SLE patients due to T-cell resistance Lupus 17 4 2008 289 294 (Pubitemid 351655795)
81. B. Zhang Reduction of forkhead box P3 levels in CD4+CD25high T cells in patients with new-onset systemic lupus erythematosus Clin. Exp. Immunol. 153 2 2008 182 187 (Pubitemid 351989160)
82. V. Pillai Transient regulatory T-cells: A state attained by all activated human T-cells Clin. Immunol. 123 1 2007 18 29 (Pubitemid 46401504)
83. J. Wang Transient expression of FOXP3 in human activated nonregulatory CD4+ T cells Eur. J. Immunol. 37 1 2007 129 138 (Pubitemid 46128793)
84. M.C. Boissier Shifting the imbalance from Th1/Th2 to Th17/treg: the changing rheumatoid arthritis paradigm Joint Bone Spine 75 4 2008 373 375
85. J.S. Courtenay Immunisation against heterologous type II collagen induces arthritis in mice Nature 283 5748 1980 666 668 (Pubitemid 10099994)
86. P.H. Wooley Type II collagen-induced arthritis in mice. I. Major histocompatibility complex (I region) linkage and antibody correlates J. Exp. Med. 154 3 1981 688 700 (Pubitemid 11060781)
87. M.E. Morgan CD25+ cell depletion hastens the onset of severe disease in collagen-induced arthritis Arthritis Rheum. 48 5 2003 1452 1460 (Pubitemid 36554546)
88. M.E. Morgan Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells Arthritis Rheum. 52 7 2005 2212 2221 (Pubitemid 40994344)
89. J. Ohata Enhanced efficacy of regulatory T cell transfer against increasing resistance, by elevated Foxp3 expression induced in arthritic murine hosts Arthritis Rheum. 56 9 2007 2947 2956 (Pubitemid 47502741)
90. D. Brackertz, G.F. Mitchell, and I.R. Mackay Antigen-induced arthritis in mice I. Induction of arthritis in various strains of mice Arthritis Rheum. 20 3 1977 841 850
91. O. Frey The role of regulatory T cells in antigen-induced arthritis: aggravation of arthritis after depletion and amelioration after transfer of CD4+CD25+ T cells Arthritis Res. Ther. 7 2 2005 R291 R301
92. G.P. Wright Adoptive therapy with redirected primary regulatory T cells results in antigen-specific suppression of arthritis Proc. Natl. Acad. Sci. U.S.A. 106 45 2009 19078 19083
93. F. Arce Selective ERK activation differentiates mouse and human tolerogenic dendritic cells, expands antigen-specific regulatory T cells, and suppresses experimental inflammatory arthritis Arthritis Rheum. 63 1 2011 84 95
94. C.A. Notley ANTI-CD3 therapy expands the numbers of CD4+ and CD8+ Treg cells and induces sustained amelioration of collagen-induced arthritis Arthritis Rheum. 62 1 2010 171 178
95. M. Mottonen CD4+ CD25+ T cells with the phenotypic and functional characteristics of regulatory T cells are enriched in the synovial fluid of patients with rheumatoid arthritis Clin. Exp. Immunol. 140 2 2005 360 367 (Pubitemid 40559165)
96. D. Cao CD25brightCD4+ regulatory T cells are enriched in inflamed joints of patients with chronic rheumatic disease Arthritis Res. Ther. 6 4 2004 R335 R346
97. C.A. Lawson Early rheumatoid arthritis is associated with a deficit in the CD4+CD25high regulatory T cell population in peripheral blood Rheumatology (Oxford) 45 10 2006 1210 1217 (Pubitemid 44548851)
98. E. Toubi Increased spontaneous apoptosis of CD4+CD25+ T cells in patients with active rheumatoid arthritis is reduced by infliximab Ann. N Y Acad. Sci. 1051 2005 506 514 (Pubitemid 41362778)
99. D. Cao Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis Eur. J. Immunol. 33 1 2003 215 223 (Pubitemid 36157659)
100. M.F. Liu The presence of cytokine-suppressive CD4+CD25+ T cells in the peripheral blood and synovial fluid of patients with rheumatoid arthritis Scand. J. Immunol. 62 3 2005 312 317
101. M.R. Ehrenstein Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy J. Exp. Med. 200 3 2004 277 285 (Pubitemid 39031247)
102. J.M. Van Amelsfort CD4(+)CD25(+) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid Arthritis Rheum. 50 9 2004 2775 2785 (Pubitemid 39209514)
103. G.M. Han CD4+CD25high T cell numbers are enriched in the peripheral blood of patients with rheumatoid arthritis Cell Immunol. 253 1-2 2008 92 101
104. C. Baecher-Allan, V. Viglietta, and D.A. Hafler Inhibition of human CD4(+)CD25(+high) regulatory T cell function J. Immunol. 169 11 2002 6210 6217 (Pubitemid 36903467)
105. F. Flores-Borja Defects in CTLA-4 are associated with abnormal regulatory T cell function in rheumatoid arthritis Proc. Natl. Acad. Sci. U.S.A. 105 49 2008 19396 19401
106. S. Han Meta-analysis of the association of CTLA-4 exon-1 +49A/G polymorphism with rheumatoid arthritis Hum. Genet. 118 1 2005 123 132
107. M. Barreto Evidence for CTLA4 as a susceptibility gene for systemic lupus erythematosus Eur. J. Hum. Genet. 12 8 2004 620 626 (Pubitemid 39172422)
108. C. Pasare, and R. Medzhitov Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells Science 299 5609 2003 1033 1036 (Pubitemid 36222922)
109. J.M. Van Amelsfort Proinflammatory mediator-induced reversal of CD4+, CD25+ regulatory T cell-mediated suppression in rheumatoid arthritis Arthritis Rheum. 56 3 2007 732 742 (Pubitemid 46399420)
110. X. Valencia TNF downmodulates the function of human CD4+CD25hi T-regulatory cells Blood 108 1 2006 253 261 (Pubitemid 43990636)
111. S. Nadkarni, C. Mauri, and M.R. Ehrenstein Anti-TNF-alpha therapy induces a distinct regulatory T cell population in patients with rheumatoid arthritis via TGF-beta J. Exp. Med. 204 1 2007 33 39 (Pubitemid 46148753)
112. J. Biton Interplay between TNF and regulatory T cells in a TNF-driven murine model of arthritis J. Immunol. 186 7 2011 3899 3910
113. M. Ayyoub Human memory FOXP3+ Tregs secrete IL-17 ex vivo and constitutively express the T(H)17 lineage-specific transcription factor RORgamma t Proc. Natl. Acad. Sci. U.S.A. 106 21 2009 8635 8640
114. G. Beriou IL-17-producing human peripheral regulatory T cells retain suppressive function Blood 113 18 2009 4240 4249
115. X.O. Yang Molecular antagonism and plasticity of regulatory and inflammatory T cell programs Immunity 29 1 2008 44 56
116. G. Lal, and J.S. Bromberg Epigenetic mechanisms of regulation of Foxp3 expression Blood 114 18 2009 3727 3735