Controlling the fire-tissue-specific mechanisms of effector regulatory T-cell homing

Immunology and Cell Biology

Volumn 93, Issue 4, 2015, Pages 355-363

  Chow, Zachary ^a   Banerjee, Ashish ^b   Hickey, Michael J ^a  

^a MONASH UNIVERSITY   (Australia)

^b HUDSON INSTITUTE OF MEDICAL RESEARCH   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA E INTEGRIN; ALPHA INTEGRIN; CD103 ANTIGEN; CD18 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CXCR3; FUCOSYLTRANSFERASE; FUCOSYLTRANSFERASE VII; SELECTIN; UNCLASSIFIED DRUG; CHEMOKINE RECEPTOR; HOMING RECEPTOR;

ANTIGEN RECOGNITION; CELL HOMING; HUMAN; IN VIVO STUDY; INTERSTITIUM; LEUKOCYTE MIGRATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE MIGRATION; LYMPHOCYTE SUBPOPULATION; MICROVASCULATURE; NONHUMAN; PHENOTYPE; REGULATORY T LYMPHOCYTE; REVIEW; ANIMAL; ANTIBODY SPECIFICITY; CELL MOTION; HOMEOSTASIS; IMMUNOLOGY; IMMUNOMODULATION; INFLAMMATION; LYMPHOCYTE ACTIVATION; METABOLISM;

ANIMALS; CELL ADHESION MOLECULES; CELL MOVEMENT; HOMEOSTASIS; HUMANS; IMMUNOMODULATION; INFLAMMATION; LYMPHOCYTE ACTIVATION; ORGAN SPECIFICITY; RECEPTORS, CHEMOKINE; RECEPTORS, LYMPHOCYTE HOMING; T-LYMPHOCYTES, REGULATORY;

EID: 84928214068     PISSN: 08189641     EISSN: 14401711     Source Type: Journal    
DOI: 10.1038/icb.2014.117     Document Type: Review

References (89)

1. Vignali DA, Collison LW, Workman CJ. How regulatory T cells work. Nat Rev Immunol 2008; 8: 523-532.
2. Tang Q, Bluestone JA. The Foxp3+ regulatory T cell: a jack of all trades, master of regulation. Nat Immunol 2008; 9: 239-244.
3. Bennett CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27: 20-21.
4. Williams LM, Rudensky AY. Maintenance of the Foxp3-dependent developmental program in mature regulatory T cells requires continued expression of Foxp3. Nat Immunol 2007; 8: 277-284.
5. Brunkow ME, Jeffery EW, Hjerrild KA, Paeper B, Clark LB, Yasayko SA et al. Disruption of a new forkhead/winged-helix protein, scurfin, results in the fatal lymphoproliferative disorder of the scurfy mouse. Nat Genet 2001; 27: 68-73.
6. Fontenot JD, Gavin M. A, Rudensky AY. Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4: 330-336.
7. Huehn J, Hamann A. Homing to suppress: address codes for Treg migration. Trends Immunol 2005; 26: 632-636.
8. Rudensky AY, Campbell DJ. In vivo sites and cellular mechanisms of T reg cellmediated suppression. J Exp Med 2006; 203: 489-492.
9. Ding Y, Xu J, Bromberg JS. Regulatory T cell migration during an immune response. Trends Immunol 2012; 33: 174-180.
10. Iellem A, Mariani M, Lang R, Recalde H, Panina-Bordignon P, Sinigaglia F et al. Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J Exp Med 2001; 194: 847-853.
11. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol 2007; 7: 678-689.
12. 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.
13. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299: 1057-1061.
14. 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.
15. Liston A, Gray DH. Homeostatic control of regulatory T cell diversity. Nat Rev Immunol 2014; 14: 154-165.
16. Baecher-Allan C, Brown JA, Freeman GJ, Hafler DA. CD4+CD25high regulatory cells in human peripheral blood. J Immunol 2001; 167: 1245-1253.
17. Hoffmann P, Eder R, Kunz-Schughart LA, Andreesen R, Edinger M. Large-scale in vitro expansion of polyclonal human CD4(+)CD25high regulatory T cells. Blood 2004; 104: 895-903.
18. Lehmann J, Huehn J, de la Rosa M, Maszyna F, Kretschmer U, Krenn V et al. Expression of the integrin alpha Ebeta 7 identifies unique subsets of CD25+ as well as CD25-regulatory T cells. Proc Natl Acad Sci USA 2002; 99: 13031-13036.
19. Huehn J, Siegmund K, Lehmann JC, Siewert C, Haubold U, Feuerer M et al. Developmental stage, phenotype, and migration distinguish naive-and effector/memory-like CD4+ regulatory T cells. J Exp Med 2004; 199: 303-313.
20. Duhen T, Duhen R, Lanzavecchia A, Sallusto F, Campbell DJ. Functionally distinct subsets of human FOXP3+ Treg cells that phenotypically mirror effector Th cells. Blood 2012; 119: 4430-4440.
21. Ito T, Hanabuchi S, Wang YH, Park WR, Arima K, Bover L et al. Two functional subsets of FOXP3+ regulatory T cells in human thymus and periphery. Immunity 2008; 28: 870-880.
22. Sugiyama D, Nishikawa H, Maeda Y, Nishioka M, Tanemura A, Katayama I et al. Anti-CCR4 mAb selectively depletes effector-type FoxP3+CD4+ regulatory T cells, evoking antitumor immune responses in humans. Proc Natl Acad Sci USA 2013; 110: 17945-17950.
23. Kleinewietfeld M, Puentes F, Borsellino G, Battistini L, Rotzschke O, Falk K. CCR6 expression defines regulatory effector/memory-like cells within the CD25(+)CD4+ T-cell subset. Blood 2005; 105: 2877-2886.
24. Siegmund K, Feuerer M, Siewert C, Ghani S, Haubold U, Dankof A et al. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 2005; 106: 3097-3104.
25. Cretney E, Kallies A, Nutt SL. Differentiation and function of Foxp3(+) effector regulatory T cells. Trends Immunol 2013; 34: 74-80.
26. Koch M. A, Tucker-Heard G, Perdue NR, Killebrew JR, Urdahl KB, Campbell DJ. The transcription factor T-bet controls regulatory T cell homeostasis and function during type 1 inflammation. Nat Immunol 2009; 10: 595-602.
27. Chaudhry A, Rudra D, Treuting P, Samstein RM, Liang Y, Kas A et al. CD4+ regulatory T cells control TH17 responses in a Stat3-dependent manner. Science 2009; 326: 986-991.
28. Linterman M. A, Pierson W, Lee SK, Kallies A, Kawamoto S, Rayner TF et al. Foxp3+ follicular regulatory T cells control the germinal center response. Nat Med 2011; 17: 975-982.
29. Chung Y, Tanaka S, Chu F, Nurieva RI, Martinez GJ, Rawal S et al. Follicular regulatory T cells expressing Foxp3 and Bcl-6 suppress germinal center reactions. Nat Med 2011; 17: 983-988.
30. Cretney E, Xin A, Shi W, Minnich M, Masson F, Miasari M et al. The transcription factors Blimp-1 and IRF4 jointly control the differentiation and function of effector regulatory T cells. Nat Immunol 2011; 12: 304-311.
31. Zheng Y, Chaudhry A, Kas A, deRoos P, Kim JM, Chu TT et al. Regulatory T-cell suppressor program co-opts transcription factor IRF4 to control T(H)2 responses. Nature 2009; 458: 351-356.
32. Burzyn D, Benoist C, Mathis D. Regulatory T cells in nonlymphoid tissues. Nat Immunol 2013; 14: 1007-1013.
33. Rosenblum MD, Gratz IK, Paw JS, Lee K, Marshak-Rothstein A, Abbas AK. Response to self antigen imprints regulatory memory in tissues. Nature 2011; 480: 538-542.
34. Gratz IK, Truong HA, Yang SH, Maurano MM, Lee K, Abbas AK et al. Cutting edge: memory regulatory t cells require IL-7 and not IL-2 for their maintenance in peripheral tissues. J Immunol 2013; 190: 4483-4487.
35. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y et al. 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.
36. Schiering C, Krausgruber T, Chomka A, Frohlich A, Adelmann K, Wohlfert EA et al. The alarmin IL-33 promotes regulatory T-cell function in the intestine. Nature 2014; 513: 564-568.
37. Sanchez Rodriguez R, Pauli ML, Neuhaus IM, Yu SS, Arron ST, Harris HW et al. Memory regulatory T cells reside in human skin. J Clin Invest 2014; 124: 1027-1036.
38. Cipolletta D, Feuerer M, Li A, Kamei N, Lee J, Shoelson SE et al. PPAR-gamma is a major driver of the accumulation and phenotype of adipose tissue Treg cells. Nature 2012; 486: 549-553.
39. Feuerer M, Herrero L, Cipolletta D, Naaz A, Wong J, Nayer A et al. Lean, but not obese, fat is enriched for a unique population of regulatory T cells that affect metabolic parameters. Nat Med 2009; 15: 930-939.
40. Burzyn D, Kuswanto W, Kolodin D, Shadrach JL, Cerletti M, Jang Y et al. A special population of regulatory T cells potentiates muscle repair. Cell 2013; 155: 1282-1295.
41. 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.
42. Schneider M. A, 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.
43. Hirahara K, Liu L, Clark RA, Yamanaka K, Fuhlbrigge RC, Kupper TS. The majority of human peripheral blood CD4+CD25highFoxp3+ regulatory T cells bear functional skinhoming receptors. J Immunol 2006; 177: 4488-4494.
44. Siewert C, Menning A, Dudda J, Siegmund K, Lauer U, Floess S et al. Induction of organ-selective CD4+ regulatory T cell homing. Eur J Immunol 2007; 37: 978-989.
45. Yuan Q, Bromley SK, Means TK, Jones KJ, Hayashi F, Bhan AK et al. CCR4-dependent regulatory T cell function in inflammatory bowel disease. J Exp Med 2007; 204: 1327-1334.
46. Taylor PA, Panoskaltsis-Mortari A, Swedin JM, Lucas PJ, Gress RE, Levine BL et al. L-Selectin(hi) but not the L-selectin(lo) CD4+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood 2004; 104: 3804-3812.
47. Tang Q, Adams JY, Tooley AJ, Bi M, Fife BT, Serra P et al. Visualizing regulatory T cell control of autoimmune responses in nonobese diabetic mice. Nat Immunol 2006; 7: 83-92.
48. Mempel TR, Pittet MJ, Khazaie K, Weninger W, Weissleder R, von Boehmer H et al. Regulatory T cells reversibly suppress cytotoxic T cell function independent of effector differentiation. Immunity 2006; 25: 129-141.
49. Bai Y, Liu J, Wang Y, Honig S, Qin L, Boros P et al. L-selectin-dependent lymphoid occupancy is required to induce alloantigen-specific tolerance. J Immunol 2002; 168: 1579-1589.
50. Ochando JC, Yopp AC, Yang Y, Garin A, Li Y, Boros P et al. Lymph node occupancy is required for the peripheral development of alloantigen-specific Foxp3+ regulatory T cells. J Immunol 2005; 174: 6993-7005.
51. 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.
52. Wagner N, Lohler J, Kunkel EJ, Ley K, Leung E, Krissansen G et al. Critical role for beta7 integrins in formation of the gut-associated lymphoid tissue. Nature 1996; 382: 366-370.
53. Penna G, Vulcano M, Roncari A, Facchetti F, Sozzani S, Adorini L. Cutting edge: differential chemokine production by myeloid and plasmacytoid dendritic cells. J Immunol 2002; 169: 6673-6676.
54. Chen Z, Herman AE, Matos M, Mathis D, Benoist C. Where CD4+CD25+ T reg cells impinge on autoimmune diabetes. J Exp Med 2005; 202: 1387-1397.
55. Schon MP, Schon M, Warren HB, Donohue JP, Parker CM. Cutaneous inflammatory disorder in integrin alphaE (CD103)-deficient mice. J Immunol 2000; 165: 6583-6589.
56. Banz A, Peixoto A, Pontoux C, Cordier C, Rocha B, Papiernik M. A unique subpopulation of CD4+ regulatory T cells controls wasting disease, IL-10 secretion and T cell homeostasis. Eur J Immunol 2003; 33: 2419-2428.
57. 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.
58. Maly P, Thall A, Petryniak B, Rogers CE, Smith PL, Marks RM et al. The alpha(1, 3) fucosyltransferase Fuc-TVII controls leukocyte trafficking through an essential role in L-, E-, and P-selectin ligand biosynthesis. Cell 1996; 86: 643-653.
59. Erdmann I, Scheidegger EP, Koch FK, Heinzerling L, Odermatt B, Burg G et al. Fucosyltransferase VII-deficient mice with defective E-, P-, and L-selectin ligands show impaired CD4+ and CD8+ T cell migration into the skin, but normal extravasation into visceral organs. J Immunol 2002; 168: 2139-2146.
60. 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.
61. Angiari S, Rossi B, Piccio L, Zinselmeyer BH, Budui S, Zenaro E et al. Regulatory T cells suppress the late phase of the immune response in lymph nodes through P-selectin glycoprotein ligand-1. J Immunol 2013; 191: 5489-5500.
62. Sather BD, Treuting P, Perdue N, Miazgowicz M, Fontenot JD, Rudensky AY et al. Altering the distribution of Foxp3(+) regulatory T cells results in tissue-specific inflammatory disease. J Exp Med 2007; 204: 1335-1347.
63. Lehtimaki S, Tillander S, Puustinen A, Matikainen S, Nyman T, Fyhrquist N et al. Absence of CCR4 exacerbates skin inflammation in an oxazolone-induced contact hypersensitivity model. J Invest Dermatol 2010; 130: 2743-2751.
64. Tang HL, Cyster JG. Chemokine Up-regulation and activated T cell attraction by maturing dendritic cells. Science 1999; 284: 819-822.
65. Suga H, Sugaya M, Miyagaki T, Ohmatsu H, Okochi H, Sato S. CXCR3 deficiency prolongs Th1-type contact hypersensitivity. J Immunol 2013; 190: 6059-6070.
66. Haasken S, Auger JL, Binstadt BA. Absence of beta2 integrins impairs regulatory T cells and exacerbates CD4+ T cell-dependent autoimmune carditis. J Immunol 2011; 187: 2702-2710.
67. Marski M, Kandula S, Turner JR, Abraham C. CD18 is required for optimal development and function of CD4+CD25+ T regulatory cells. J Immunol 2005; 175: 7889-7897.
68. Gratz IK, Campbell DJ. Organ-specific and memory Treg cells: specificity, development, function, and maintenance. Front Immunol 2014; 5: 333.
69. Levine AG, Arvey A, Jin W, Rudensky AY. Continuous requirement for the TCR in regulatory T cell function. Nat Immunol 2014; 15: 1070-1078.
70. Killebrew JR, Perdue N, Kwan A, Thornton AM, Shevach EM, Campbell DJ. A selfreactive TCR drives the development of Foxp3+ regulatory T cells that prevent autoimmune disease. J Immunol 2011; 187: 861-869.
71. Reinhardt RL, Bullard DC, Weaver CT, Jenkins MK. Preferential accumulation of antigen-specific effector CD4 T cells at an antigen injection site involves CD62Edependent migration but not local proliferation. J Exp Med 2003; 197: 751-762.
72. Maganto-Garcia E, Bu DX, Tarrio ML, Alcaide P, Newton G, Griffin GK et al. Foxp3 +-inducible regulatory T cells suppress endothelial activation and leukocyte recruitment. J Immunol 2011; 187: 3521-3529.
73. Deane JA, Abeynaike LD, Norman MU, Wee JL, Kitching AR, Kubes P et al. Endogenous regulatory T cells adhere in inflamed dermal vessels via ICAM-1: association with regulation of effector leukocyte adhesion. J Immunol 2012; 188: 2179-2188.
74. Abeynaike LD, Deane JA, Westhorpe CL, Chow Z, Alikhan M. A, Kitching AR et al. Regulatory T cells dynamically regulate selectin ligand function during multiple challenge contact hypersensitivity. J Immunol 2014; 193: 4934-4944.
75. Chow Z, Mueller SN, Deane JA, Hickey MJ. Dermal regulatory T cells display distinct migratory behavior that is modulated during adaptive and innate inflammation. J Immunol 2013; 191: 3049-3056.
76. Xu C, Shen Y, Littman DR, Dustin ML, Velazquez P. Visualization of mucosal homeostasis via single-and multiphoton intravital fluorescence microscopy. J Leukoc Biol 2012; 92: 413-419.
77. Bauer CA, Kim EY, Marangoni F, Carrizosa E, Claudio NM, Mempel TR. Dynamic Treg interactions with intratumoral APCs promote local CTL dysfunction. J Clin Invest 2014; 124: 2425-2440.
78. Fujisaki J, Wu J, Carlson AL, Silberstein L, Putheti P, Larocca R et al. In vivo imaging of Treg cells providing immune privilege to the haematopoietic stem-cell niche. Nature 2011; 474: 216-219.
79. Seneschal J, Clark RA, Gehad A, Baecher-Allan CM, Kupper TS. Human epidermal Langerhans cells maintain immune homeostasis in skin by activating skin resident regulatory T cells. Immunity 2012; 36: 873-884.
80. Strauss L, Bergmann C, Szczepanski M, Gooding W, Johnson JT, Whiteside TL. A unique subset of CD4+CD25highFoxp3+ T cells secreting interleukin-10 and transforming growth factor-beta1 mediates suppression in the tumor microenvironment. Clin Cancer Res 2007; 13: 4345-4354.
81. Fahlen L, Read S, Gorelik L, Hurst SD, Coffman RL, Flavell RA et al. T cells that cannot respond to TGF-beta escape control by CD4(+)CD25(+) regulatory T cells. J Exp Med 2005; 201: 737-746.
82. Rubtsov YP, Rasmussen JP, Chi EY, Fontenot J, Castelli L, Ye X et al. Regulatory T cellderived interleukin-10 limits inflammation at environmental interfaces. Immunity 2008; 28: 546-558.
83. Onishi Y, Fehervari Z, Yamaguchi T, Sakaguchi S. Foxp3+ natural regulatory T cells preferentially form aggregates on dendritic cells in vitro and actively inhibit their maturation. Proc Natl Acad Sci USA 2008; 105: 10113-10118.
84. Ring S, Schafer SC, Mahnke K, Lehr HA, Enk AH. CD4+ CD25+ regulatory T cells suppress contact hypersensitivity reactions by blocking influx of effector T cells into inflamed tissue. Eur J Immunol 2006; 36: 2981-2992.
85. Fu H, Kishore M, Gittens B, Wang G, Coe D, Komarowska I et al. Self-recognition of the endothelium enables regulatory T-cell trafficking and defines the kinetics of immune regulation. Nat Commun 2014; 5: 3436.
86. Fulton RB, Meyerholz DK, Varga SM. Foxp3+ CD4 regulatory T cells limit pulmonary immunopathology by modulating the CD8 T cell response during respiratory syncytial virus infection. J Immunol 2010; 185: 2382-2392.
87. Iellem A, Colantonio L, D'Ambrosio D. Skin-versus gut-skewed homing receptor expression and intrinsic CCR4 expression on human peripheral blood CD4+CD25+ suppressor T cells. Eur J Immunol 2003; 33: 1488-1496.
88. Faustino L, da Fonseca DM, Takenaka MC, Mirotti L, Florsheim EB, Guereschi MG et al. Regulatory T cells migrate to airways via CCR4 and attenuate the severity of airway allergic inflammation. J Immunol 2013; 190: 2614-2621.
89. Yamazaki T, Yang XO, Chung Y, Fukunaga A, Nurieva R, Pappu B et al. CCR6 regulates the migration of inflammatory and regulatory T cells. J Immunol 2008; 181: 8391-8401.