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Cited by 773T-cell and B-cell ImmunologyPsoriasis: Treatment and PathogenesisIL-33, ST2, and ILC Pathways

Phenotypical and functional specialization of FOXP3+ regulatory T cells

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Campbell, Daniel J., Koch, Meghan A.·2011·Nature Reviews Immunology
DOI 10.1038/nri2916PMC PMC3289970
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Abstract

Forkhead box P3 (FOXP3)(+) regulatory T (T(Reg)) cells prevent autoimmune disease, maintain immune homeostasis and modulate immune responses during infection. To accomplish these tasks, T(Reg) cell activity is precisely controlled, and this requires T(Reg) cells to alter their migratory, functional and homeostatic properties in response to specific cues in the immune environment. We review progress in understanding the diversity of T(Reg) cells, T(Reg) cell function in different anatomical and inflammatory settings, and the influence of the immune environment on T(Reg) cell activity. We also consider how these factors affect immune-mediated disease in the contexts of infection, autoimmunity, cancer and transplantation.

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  • The inflammatory milieu in chronic inflammation destabilizes Foxp3 expression in Tregs and impairs their suppressive functions.

    “This inflammatory milieu destabilizes Foxp3 expression in Tregs and impairs their suppressive functions (Campbell and Koch 2011; Komatsu et al. 2014).”

    From The double-edged sword of regulatory T cells in MASLD: from inflammation control to fibrosis promotion (2026) · cites this paper as Campbell and Koch 2011

    The “Stability of Treg cells” section reports that some inflammatory cytokines can downregulate FOXP3 and that highly polarized inflammatory environments may subvert Treg function. But it also reports FOXP3 stability in highly inflammatory settings, while the “Inflammatory cytokines and Treg cells” section says cytokines can enhance or inhibit Treg activity. The claim overstates these conditional findings as a general effect of chronic inflammation; no page numbers are available in our copy. (LLM, conf=0.87)

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  1. [1]Sakaguchi S Yamaguchi T Nomura T Ono M Regulatory T cells and immune tolerance Cell 2008 133 775 787 18510923
  2. [2]Horwitz DA Regulatory T cells in systemic lupus erythematosus: past, present and future Arthritis Res. Ther 2008 10 227 19040771 PMC2656253
  3. [3]Viglietta V Baecher-Allan C Weiner HL Hafler DA Loss of functional suppression by CD4+CD25+ regulatory T cells in patients with multiple sclerosis J. Exp. Med 2004 199 971 979 15067033 PMC2211881
  4. [4]Ehrenstein MR Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy J. Exp. Med 2004 200 277 285 15280421 PMC2211983
  5. [5]Lindley S Defective suppressor function in CD4(+)CD25(+) T-cells from patients with type 1 diabetes Diabetes 2005 54 92 99 15616015
  6. [6]Belkaid Y Regulatory T cells and infection: a dangerous necessity Nat. Rev. Immunol 2007 7 875 888 17948021
  7. [7]Nishikawa H Sakaguchi S Regulatory T cells in tumor immunity Int. J. Cancer 2010 127 759 767 20518016
  8. [8]Feuerer M Hill JA Mathis D Benoist C Foxp3+ regulatory T cells: differentiation, specification, subphenotypes Nat. Immunol 2009 10 689 695 19536194
  9. [9]Campbell DJ Kim CH Butcher EC Chemokines in the systemic organization of immunity Immunol. Rev 2003 195 58 71 12969310
  10. [10]Sather BD Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease J. Exp. Med 2007 204 1335 1347 17548521 PMC2118615
  11. [11]Dudda JC Perdue N Bachtanian E Campbell DJ Foxp3+ regulatory T cells maintain immune homeostasis in the skin J. Exp. Med 2008 205 1559 1565 18573908 PMC2442633
  12. [12]Suffia I Reckling SK Salay G Belkaid Y A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection J. Immunol 2005 174 5444 5455 15845457
  13. [13]Freyschmidt EJ Skin inflammation arising from cutaneous regulatory T cell deficiency leads to impaired viral immune responses J. Immunol 2010 185 1295 1302 20548030 PMC3873154
  14. [14]Schneider MA Meingassner JG Lipp M Moore HD Rot A CCR7 is required for the in vivo function of CD4+ CD25+ regulatory T cells J. Exp. Med 2007 204 735 745 17371928 PMC2118557
  15. [15]Yamazaki T CCR6 regulates the migration of inflammatory and regulatory T cells J. Immunol 2008 181 8391 8401 19050256 PMC2752441
  16. [16]Santodomingo-Garzon T Han J Le T Yang Y Swain MG Natural killer T cells regulate the homing of chemokine CXC receptor 3-positive regulatory T cells to the liver in mice Hepatology 2008 19140218
  17. [17]Muller M CXCR3 signaling reduces the severity of experimental autoimmune encephalomyelitis by controlling the parenchymal distribution of effector and regulatory T cells in the central nervous system J. Immunol 2007 179 2774 2786 17709491
  18. [18]Zhang N Regulatory T cells sequentially migrate from inflamed tissues to draining lymph nodes to suppress the alloimmune response Immunity 2009 30 458 469 19303390 PMC2737741
  19. [19]Lee JH Kang SG Kim CH FoxP3+ T cells undergo conventional first switch to lymphoid tissue homing receptors in thymus but accelerated second switch to nonlymphoid tissue homing receptors in secondary lymphoid tissues J. Immunol 2007 178 301 311 17182567
  20. [20]Huehn J Developmental Stage, Phenotype, and Migration Distinguish Naive- and Effector/Memory-like CD4+ Regulatory T Cells J. Exp. Med 2004 199 303 313 14757740 PMC2211798
  21. [21]Min B Gut flora antigens are not important in the maintenance of regulatory T cell heterogeneity and homeostasis Eur. J. Immunol 2007 37 1916 1923 17549737
  22. [22]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 10510089 PMC2195650
  23. [23]Belkaid Y Piccirillo CA Mendez S Shevach EM Sacks DL CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity Nature 2002 420 502 507 12466842
  24. [24]Loser K IL-10 controls ultraviolet-induced carcinogenesis in mice J. Immunol 2007 179 365 371 17579057
  25. [26]Wing K CTLA-4 control over Foxp3+ regulatory T cell function Science 2008 322 271 275 18845758
  26. [27]Fallarino F Modulation of tryptophan catabolism by regulatory T cells Nat. Immunol 2003 4 1206 1212 14578884
  27. [28]Onodera T Constitutive expression of IDO by dendritic cells of mesenteric lymph nodes: functional involvement of the CTLA-4/B7 and CCL22/CCR4 interactions J. Immunol 2009 183 5608 5614 19843945
  28. [29]Tadokoro CE Regulatory T cells inhibit stable contacts between CD4+ T cells and dendritic cells in vivo J. Exp. Med 2006 203 505 511 16533880 PMC2118249
  29. [30]Tang Q Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice Nat. Immunol 2006 7 83 92 16311599 PMC3057888
  30. [31]Boissonnas A Foxp3+ T cells induce perforin-dependent dendritic cell death in tumor-draining lymph nodes Immunity 2010 32 266 278 20137985
  31. [32]Kim JM Rasmussen JP Rudensky AY Regulatory T cells prevent catastrophic autoimmunity throughout the lifespan of mice Nat. Immunol 2007 8 191 197 17136045
  32. [33]Lund JM Hsing L Pham TT Rudensky AY Coordination of early protective immunity to viral infection by regulatory T cells Science 2008 320 1220 1224 18436744 PMC2519146
  33. [34]Vignali DA Collison LW Workman CJ How regulatory T cells work Nat. Rev. Immunol 2008 8 523 532 18566595 PMC2665249
  34. [35]Zhu J Yamane H Paul WE Differentiation of effector CD4 T cell populations (*) Annu. Rev. Immunol 2010 28 445 489 20192806 PMC3502616
  35. [36]Chen Z Laurence A O'Shea JJ Signal transduction pathways and transcriptional regulation in the control of Th17 differentiation Semin. Immunol 2007 19 400 408 18166487 PMC2323678
  36. [37]Szabo SJ Sullivan BM Peng SL Glimcher LH Molecular mechanisms regulating Th1 immune responses Annu. Rev. Immunol 2003 21 713 758 12500979
  37. [38]Ansel KM Djuretic I Tanasa B Rao A Regulation of Th2 differentiation and Il4 locus accessibility Annu. Rev. Immunol 2006 24 607 656 16551261
  38. [40]Szabo SJ A novel transcription factor, T-bet, directs Th1 lineage commitment Cell 2000 100 655 669 10761931
  39. [42]Dardalhon V Korn T Kuchroo VK Anderson AC Role of Th1 and Th17 cells in organ-specific autoimmunity J. Autoimmun 2008 31 252 256 18502610 PMC3178062
  40. [43]Kim HY DeKruyff RH Umetsu DT The many paths to asthma: phenotype shaped by innate and adaptive immunity Nat. Immunol 2010 11 577 584 20562844 PMC3114595
  41. [44]Townsend MJ T-bet regulates the terminal maturation and homeostasis of NK and Valpha14i NKT cells Immunity 2004 20 477 494 15084276
  42. [45]Szabo SJ Distinct effects of T-bet in TH1 lineage commitment and IFN-gamma production in CD4 and CD8 T cells Science 2002 295 338 342 11786644
  43. [46]Sullivan BM Juedes A Szabo SJ von HM Glimcher LH Antigen-driven effector CD8 T cell function regulated by T-bet Proc. Natl. Acad. Sci. U. S. A 2003 100 15818 15823 14673093 PMC307651
  44. [47]Koch MA The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation Nat. Immunol 2009 10 595 602 19412181 PMC2712126
  45. [48]Zheng Y Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses Nature 2009 PMC2864791 19182775
  46. [49]Kwon H Analysis of interleukin-21-induced Prdm1 gene regulation reveals functional cooperation of STAT3 and IRF4 transcription factors Immunity 2009 31 941 952 20064451 PMC3272079
  47. [50]Chaudhry A CD4+ Regulatory T Cells Control TH17 Responses in a Stat3-Dependent Manner Science 2009 PMC4408196 19797626
  48. [52]Strober W Vitamin A rewrites the ABCs of oral tolerance Mucosal. Immunol 2008 1 92 95 19079166
  49. [53]Ghoreishi M Expansion of antigen-specific regulatory T cells with the topical vitamin d analog calcipotriol J. Immunol 2009 182 6071 6078 19414758 PMC4572475
  50. [54]Jeffery LE 1, 25-Dihydroxyvitamin D3 and IL-2 combine to inhibit T cell production of inflammatory cytokines and promote development of regulatory T cells expressing CTLA-4 and FoxP3 J. Immunol 2009 183 5458 5467 19843932 PMC2810518
  51. [55]Malek TR The biology of interleukin-2 Annu. Rev. Immunol 2008 26 453 479 18062768
  52. [56]Fontenot JD Gavin MA Rudensky AY Foxp3 programs the development and function of CD4+CD25+ regulatory T cells Nat. Immunol 2003 4 330 336 12612578
  53. [57]Fontenot JD Rasmussen JP Gavin MA Rudensky AY A function for interleukin 2 in Foxp3-expressing regulatory T cells Nat. Immunol 2005 6 1142 1151 16227984
  54. [58]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 15753206 PMC2212841
  55. [59]Burchill MA Yang J Vogtenhuber C Blazar BR Farrar MA IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells J. Immunol 2007 178 280 290 17182565
  56. [60]Soper DM Kasprowicz DJ Ziegler SF IL-2Rbeta links IL-2R signaling with Foxp3 expression Eur. J. Immunol 2007 37 1817 1826 17559173
  57. [61]Burkett PR Coordinate expression and trans presentation of interleukin (IL)-15Ralpha and IL-15 supports natural killer cell and memory CD8+ T cell homeostasis J. Exp. Med 2004 200 825 834 15452177 PMC2213280
  58. [62]Siewert C Induction of organ-selective CD4+ regulatory T cell homing Eur. J. Immunol 2007 37 978 989 17345581
  59. [63]Mucida D Reciprocal TH17 and regulatory T cell differentiation mediated by retinoic acid Science 2007 317 256 260 17569825
  60. [64]Coombes JL 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 2007 204 1757 1764 17620361 PMC2118683
  61. [65]Sun CM Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid J. Exp. Med 2007 204 1775 1785 17620362 PMC2118682
  62. [66]Zhou X Cutting edge: all-trans retinoic acid sustains the stability and function of natural regulatory T cells in an inflammatory milieu J. Immunol 2010 185 2675 2679 20679534 PMC3098624
  63. [67]Gorman S Topically applied 1, 25-dihydroxyvitamin D3 enhances the suppressive activity of CD4+CD25+ cells in the draining lymph nodes J. Immunol 2007 179 6273 6283 17947703
  64. [68]Sigmundsdottir H DCs metabolize sunlight-induced vitamin D3 to 'program' T cell attraction to the epidermal chemokine CCL27 Nat. Immunol 2007 8 285 293 17259988
  65. [69]Murphy KM T helper differentiation proceeds through Stat1-dependent, Stat4-dependent and Stat4-independent phases Curr. Top. Microbiol. Immunol 1999 238 13 26 10087648
  66. [70]Cooper AM Disseminated tuberculosis in interferon gamma gene-disrupted mice J. Exp. Med 1993 178 2243 2247 8245795 PMC2191280
  67. [71]Harty JT Bevan MJ Specific immunity to Listeria monocytogenes in the absence of IFN gamma Immunity 1995 3 109 117 7621071
  68. [72]Wang ZE Reiner SL Zheng S Dalton DK Locksley RM CD4+ effector cells default to the Th2 pathway in interferon gamma-deficient mice infected with Leishmania major J. Exp. Med 1994 179 1367 1371 7908325 PMC2191434
  69. [73]Caretto D Katzman SD Villarino AV Gallo E Abbas AK Cutting edge: the Th1 response inhibits the generation of peripheral regulatory T cells J. Immunol 2010 184 30 34 19949064 PMC2908389
  70. [74]Lu LF Function of miR-146a in controlling Treg cell-mediated regulation of Th1 responses Cell 2010 142 914 929 20850013 PMC3049116
  71. [75]Oldenhove G Decrease of Foxp3+ Treg cell number and acquisition of effector cell phenotype during lethal infection Immunity 2009 31 772 786 19896394 PMC2814877
  72. [76]Kishimoto T IL-6: from its discovery to clinical applications Int. Immunol 2010 22 347 352 20410258
  73. [77]Bettelli E Oukka M Kuchroo VK T(H)-17 cells in the circle of immunity and autoimmunity Nat. Immunol 2007 8 345 350 17375096
  74. [79]Zheng SG Wang J Horwitz DA Cutting edge: Foxp3+CD4+CD25+ regulatory T cells induced by IL-2 and TGF-beta are resistant to Th17 conversion by IL-6 J. Immunol 2008 180 7112 7116 18490709
  75. [80]Xu L Kitani A Fuss I Strober W Cutting edge: regulatory T cells induce CD4+CD25-Foxp3- T cells or are self-induced to become Th17 cells in the absence of exogenous TGF-beta J. Immunol 2007 178 6725 6729 17513718
  76. [81]Pasare C Medzhitov R Toll pathway-dependent blockade of CD4+CD25+ T cell-mediated suppression by dendritic cells Science 2003 299 1033 1036 12532024
  77. [82]Mima T Nishimoto N Clinical value of blocking IL-6 receptor Curr. Opin. Rheumatol 2009 21 224 230 19365268
  78. [84]Veldhoen M Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset Nat. Immunol 2008 9 1341 1346 18931678
  79. [85]Pillemer BB STAT6 activation confers upon T helper cells resistance to suppression by regulatory T cells J. Immunol 2009 183 155 163 19535633 PMC2754746
  80. [86]Maerten P Effects of interleukin 4 on CD25+CD4+ regulatory T cell function J. Autoimmun 2005 25 112 120 16051465
  81. [87]Trinchieri G Type I interferon: friend or foe? J. Exp. Med 2010 207 2053 2063 20837696 PMC2947062
  82. [88]Namdar A Nikbin B Ghabaee M Bayati A Izad M Effect of IFN-beta therapy on the frequency and function of CD4(+)CD25(+) regulatory T cells and Foxp3 gene expression in relapsing-remitting multiple sclerosis (RRMS): a preliminary study J. Neuroimmunol 2010 218 120 124 19932513
  83. [89]Vandenbark AA Interferon-beta-1a treatment increases CD56bright natural killer cells and CD4+CD25+ Foxp3 expression in subjects with multiple sclerosis J. Neuroimmunol 2009 215 125 128 19758707
  84. [90]Golding A Rosen A Petri M Akhter E Andrade F Interferon-alpha regulates the dynamic balance between human activated regulatory and effector T cells: implications for antiviral and autoimmune responses Immunology 2010 131 107 117 20465564 PMC2966763
  85. [91]Hoffman HM Therapy of autoinflammatory syndromes J. Allergy Clin. Immunol 2009 124 1129 1138 20004774 PMC4508191
  86. [92]Chen X Oppenheim JJ TNF-alpha: an activator of CD4+FoxP3+TNFR2+ regulatory T cells Curr. Dir. Autoimmun 2010 11 119 134 20173391 PMC6314650
  87. [93]Chen X Baumel M Mannel DN Howard OM Oppenheim JJ Interaction of TNF with TNF receptor type 2 promotes expansion and function of mouse CD4+CD25+ T regulatory cells J. Immunol 2007 179 154 161 17579033
  88. [94]Ma HL Tumor necrosis factor alpha blockade exacerbates murine psoriasis-like disease by enhancing Th17 function and decreasing expansion of Treg cells Arthritis Rheum 2010 62 430 440 20112373
  89. [95]Brinster C Shevach EM Costimulatory effects of IL-1 on the expansion/differentiation of CD4+CD25+Foxp3+ and CD4+CD25+Foxp3- T cells J. Leukoc. Biol 2008 84 480 487 18477692 PMC2493074
  90. [96]Deknuydt F Bioley G Valmori D Ayyoub M IL-1beta and IL-2 convert human Treg into T(H)17 cells Clin. Immunol 2009 131 298 307 19211307
  91. [97]Floess S Epigenetic control of the foxp3 locus in regulatory T cells PLoS. Biol 2007 5 e38 17298177 PMC1783672
  92. [98]Tsuji M Preferential generation of follicular B helper T cells from Foxp3+ T cells in gut Peyer's patches Science 2009 323 1488 1492 19286559
  93. [99]Komatsu N Heterogeneity of natural Foxp3+ T cells: a committed regulatory T-cell lineage and an uncommitted minor population retaining plasticity Proc. Natl. Acad. Sci. U. S. A 2009 106 1903 1908 19174509 PMC2644136
  94. [100]Gavin MA Foxp3-dependent programme of regulatory T-cell differentiation Nature 2007 445 771 775 17220874
  95. [101]Zhou X Instability of the transcription factor Foxp3 leads to the generation of pathogenic memory T cells in vivo Nat. Immunol 2009 10 1000 1007 19633673 PMC2729804
  96. [102]Wei G Global mapping of H3K4me3 and H3K27me3 reveals specificity and plasticity in lineage fate determination of differentiating CD4+ T cells Immunity 2009 30 155 167 19144320 PMC2722509
  97. [103]Rubtsov YP Stability of the regulatory T cell lineage in vivo Science 2010 329 1667 1671 20929851 PMC4262151
  98. [104]Akbar AN Vukmanovic-Stejic M Taams LS Macallan DC The dynamic co-evolution of memory and regulatory CD4+ T cells in the periphery Nat. Rev. Immunol 2007 7 231 237 17318234
  99. [105]Allan SE CD4+ T-regulatory cells: toward therapy for human diseases Immunol. Rev 2008 223 391 421 18613849
  100. [106]Picca CC Role of TCR specificity in CD4+ CD25+ regulatory T-cell selection Immunol. Rev 2006 212 74 85 16903907
  101. [107]Lathrop SK Santacruz NA Pham D Luo J Hsieh CS Antigen-specific peripheral shaping of the natural regulatory T cell population J. Exp. Med 2008 205 3105 3117 19064700 PMC2605228
  102. [108]Tang Q Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells J. Immunol 2003 171 3348 3352 14500627
  103. [109]Salomon B B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes Immunity 2000 12 431 440 10795741
  104. [110]Darrasse-Jeze G Feedback control of regulatory T cell homeostasis by dendritic cells in vivo J. Exp. Med 2009 206 1853 1862 19667061 PMC2737156
  105. [111]Bollyky PL Intact extracellular matrix and the maintenance of immune tolerance: high molecular weight hyaluronan promotes persistence of induced CD4+CD25+ regulatory T cells J. Leukoc. Biol 2009 86 567 572 19401397 PMC2735281
  106. [112]Venturi GM Conway RM Steeber DA Tedder TF CD25+CD4+ regulatory T cell migration requires L-selectin expression: L-selectin transcriptional regulation balances constitutive receptor turnover J. Immunol 2007 178 291 300 17182566
  107. [113]Szanya V Ermann J Taylor C Holness C Fathman CG The subpopulation of CD4+CD25+ splenocytes that delays adoptive transfer of diabetes expresses L-selectin and high levels of CCR7 J. Immunol 2002 169 2461 2465 12193715
  108. [114]Hirahara K The majority of human peripheral blood CD4+CD25highFoxp3+ regulatory T cells bear functional skin-homing receptors J. Immunol 2006 177 4488 4494 16982885
  109. [115]Siegmund K Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo Blood 2005 106 3097 3104 16014565 PMC1895340
  110. [116]Denning TL Kim G Kronenberg M Cutting edge: CD4+CD25+ regulatory T cells impaired for intestinal homing can prevent colitis J. Immunol 2005 174 7487 7491 15944246
  111. [117]Lim HW Lee J Hillsamer P Kim CH Human Th17 cells share major trafficking receptors with both polarized effector T cells and FOXP3+ regulatory T cells J. Immunol 2008 180 122 129 18097011
  112. [118]Yuan Q CCR4-dependent regulatory T cell function in inflammatory bowel disease J. Exp. Med 2007 204 1327 1334 17548518 PMC2118617
  113. [119]Kang SG Identification of a chemokine network that recruits FoxP3(+) regulatory T cells into chronically inflamed intestine Gastroenterology 2007 132 966 981 17324406
  114. [120]Yurchenko E CCR5-dependent homing of naturally occurring CD4+ regulatory T cells to sites of Leishmania major infection favors pathogen persistence J. Exp. Med 2006 203 2451 2460 17015634 PMC2118140
  115. [121]Kleinewietfeld M CCR6 expression defines regulatory effector/memory-like cells within the CD25+CD4+ T cell subset Blood 2004 15613550
  116. [122]Hirota K Preferential recruitment of CCR6-expressing Th17 cells to inflamed joints via CCL20 in rheumatoid arthritis and its animal model J. Exp. Med 2007 204 2803 2812 18025126 PMC2118525
  117. [123]Soler D CCR8 expression identifies CD4 memory T cells enriched for FOXP3+ regulatory and Th2 effector lymphocytes J. Immunol 2006 177 6940 6951 17082609
  118. [124]Guo Z CD4+CD25+ regulatory T cells in the small intestinal lamina propria show an effector/memory phenotype Int. Immunol 2008 20 307 315 18184698
  119. [125]Eksteen B Epithelial inflammation is associated with CCL28 production and the recruitment of regulatory T cells expressing CCR10 J. Immunol 2006 177 593 603 16785557
  120. [126]Oo YH Distinct roles for CCR4 and CXCR3 in the recruitment and positioning of regulatory T cells in the inflamed human liver J. Immunol 2010 184 2886 2898 20164417
  121. [127]Lim HW Broxmeyer HE Kim CH Regulation of trafficking receptor expression in human forkhead box P3+ regulatory T cells J. Immunol 2006 177 840 851 16818738
  122. [128]Lim HW Hillsamer P Kim CH Regulatory T cells can migrate to follicles upon T cell activation and suppress GC-Th cells and GC-Th cell-driven B cell responses J. Clin. Invest 2004 114 1640 1649 15578096 PMC529283
  123. [129]Grauer OM CD4+FoxP3+ regulatory T cells gradually accumulate in gliomas during tumor growth and efficiently suppress antiglioma immune responses in vivo Int. J. Cancer 2007 121 95 105 17315190
  124. [130]Wald O CD4+CXCR4highCD69+ T cells accumulate in lung adenocarcinoma J. Immunol 2006 177 6983 6990 17082613

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Authors
Campbell, D. J., & Koch, M. A.
Affiliations
  • Benaroya Research Institute (US)
  • University of Washington (US)
Corresponding author
Campbell, Daniel J.
ORCID
Venue
Nature Reviews Immunology
Publisher
Springer Science and Business Media LLC
Published
2011-01-25
Volume
11
Issue
2
Pages
119-130
ISSN
  • 1474-1733 (ISSN-L)
  • 1474-1741
DOI
10.1038/nri2916
PMC
PMC3289970
OpenAlex
W2012628829
Cited by
773
References
6
Citations by year
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FWCI
8.09
Type
journal article
Language
en
Open access
Licence
www.springer.com/tdm (tdm)
Locations
  • Nature reviews. Immunology (publishedVersion)
  • PubMed (publishedVersion)
  • PubMed Central (acceptedVersion)
Funders
  • National Institute of Allergy and Infectious Diseases (R01AI067750, R01AI085130, R21AI069889)
  • National Institute of Diabetes and Digestive and Kidney Diseases (R01DK072295)
Topics
  • Life Sciences › Immunology and Microbiology › Immunology › T-cell and B-cell Immunology
  • Life Sciences › Immunology and Microbiology › Immunology › Psoriasis: Treatment and Pathogenesis
  • Life Sciences › Immunology and Microbiology › Immunology › IL-33, ST2, and ILC Pathways
Keywords
Foxp3+ regulatory T cells, Treg cell migration, Treg cell homeostasis, autoimmune disease, immune homeostasis, infection, tumor immunology, transplantation, immune-mediated diseases, Treg therapy
MeSH terms
Cell Movement, Homeostasis, Humans, Immunity, Active, Lymphoid Tissue, Cytokines, T-Lymphocytes, Regulatory, Forkhead Transcription Factors

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