The immunomodulatory effects of regulatory T cells: Implications for immune regulation in the skin

British Journal of Dermatology

Volumn 152, Issue 3, 2005, Pages 409-417

  Birch, Katie E ^a,b   Vukmanovic Stejic, M ^b   Reed, J R ^b   Akbar, A N ^b   Rustin, M H A ^a  

^a ROYAL FREE HOSPITAL   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

CD4+ CD25+; Immunoregulution; Regulatory T cell; Skin

Indexed keywords

ALLERGEN;

AUTOIMMUNITY; CELL MIGRATION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOMODULATION; IMMUNOREGULATION; INFECTION; PRIORITY JOURNAL; REVIEW; SKIN; SKIN ALLERGY; SKIN DISEASE; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TUMOR IMMUNITY;

DRUG ERUPTIONS; GRAFT VS HOST DISEASE; HUMANS; HYPERSENSITIVITY, IMMEDIATE; IMMUNOPHENOTYPING; NEOPLASMS; SKIN; SKIN DISEASES; T-LYMPHOCYTE SUBSETS;

EID: 17444422840     PISSN: 00070963     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1365-2133.2005.06476.x     Document Type: Review

References (77)

1. Shevach EM. CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2:389-400.
2. Sakaguchi S, Sakaguchi N, Asano M et al. 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; 155:1151-64.
3. Asano M, Toda M, Sakaguchi N et al. Autoimmune disease as a consequence of developmental abnormality of a T cell subpopulation. J Exp Med 1996; 184:387-96.
4. Jonuleit H, Schmitt E, Stassen M et al. Identification and functional characterization of human CD4(+) CD25(+) T cells with regulatory properties isolated from peripheral blood. J Exp Med 2001; 193:1285-94.
5. Bluestone JA, Abbas AK. Natural versus adaptive regulatory T cells. Nat Rev Immunol 2003; 3:253-7.
6. Umetsu DT, Akbari O, Dekruyff RH. Regulatory T cells control the development of allergic disease and asthma. J Allergy Clin Immunol 2003; 112:480-7.
7. Taams LS, Smith J, Rustin MH et al. Human anergic/suppressive CD4(+) CD25(+) T cells: a highly differentiated and apoptosis-prone population. Eur J Immunol 2001; 31:1122-31.
8. McHugh RS, Whitters MJ, Piccirillo CA et al. CD4(+) CD25(+) immunoregulatory T cells: gene expression analysis reveals a functional role for the glucocorticoid-induced TNF receptor. Immunity 2002; 16:311-23.
9. Walker MR, Kasprowicz DJ, Gersuk VH et al. Induction of FoxP3 and acquisition of T regulatory activity by stimulated human CD4+. J Clin Invest 2003; 112:1437-43.
10. Hori S, Nomura T, Sakaguchi S. Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-61.
11. Baecher-Allan C, Viglietta V, Hafler DA. Human CD4+ CD25+ regulatory T cells. Semin Immunol 2004; 16:89-98.
12. high regulatory cells in human peripheral blood. J Immunol 2001; 167:1245-53.
13. Lehmann J, Huehn J, de la Rosa M 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; 99:13031-6.
14. Stassen M, Fondel S, Bopp T et al. Human CD25+ regulatory T cells: two subsets defined by the integrins alpha4beta7 or alpha4beta1 confer distinct suppressive properties upon CD4+ T helper cells. Eur J Immunol 2004; 34:1303-11.
15. Colantonio L, Iellem A, Sinigaglia F et al. 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 2002; 32:3506-14.
16. 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; 188:287-96.
17. Thornton AM, Shevach EM. Suppressor effector function of CD4+ CD25+ immunoregulatory T cells is antigen nonspecific. J Immunol 2000; 164:183-90.
18. Zheng Y, Manzotti CN, Liu M et al. CD86 and CD80 differentially modulate the suppressive function of human regulatory T cells. J Immunol 2004; 172:2778-84.
19. Takahashi T, Tagami T, Yamazaki S et al. Immunologic self-tolerance maintained by CD25(+) CD4(+) regulatory T cells constitutively expressing cytotoxic T lymphocyte-associated antigen 4. J Exp Med 2000; 192:303-10.
20. Chen W, Jin W, Wahl SM. Engagement of cytotoxic T lymphocyte-associated antigen 4 (CTLA-4) induces transforming growth factor beta (TGF-beta) production by murine CD4(+) T cells. J Exp Med 1998; 188:1849-57.
21. Levings MK, Sangregorio R, Roncarolo MG. Human CD25(+) CD4(+) T regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J Exp Med 2001; 193:1295-302.
22. Piccirillo CA, Shevach EM. Culling edge: control of CD8+ T cell aclivation by CD4+ CD25+ immunoregulatory cells. J Immunol 2001; 167:1137-40.
23. Cederbom L, Hall H, Ivars F. CD4+ CD25+ regulatory T cells down-regulate co-stimulatory molecules on antigen-presenting cells. Eur J Immunol 2000; 30:1538-43.
24. Nakamura K, Kitani A, Strober W. Cell contact-dependent immunosuppression by CD4(+) CD25(+) regulatory T cells is mediated by cell surface-bound lransforming growth factor beta. J Exp Med 2001; 194:629-44.
25. Nakamura K, Kitani A, Fuss I et al. TGF-beta 1 plays an important role in the mechanism of CD4+ CD25+ regulatory T cell activity in both humans and mice. J Immunol 2004; 172:834-42.
26. Asseman C, Mauze S, Leach MW et al. An essential role for interleukin 10 in the function of regulatory T cells that inhibit intestinal inflammation. J Exp Med 1999; 190:995-1004.
27. Singh B, Read S, Asseman C et al. Control of intestinal inflammation by regulatory T cells. Immunol Rev 2001; 182:190-200.
28. Stassen M, Schmitt E, Jonuleit H. Human CD4(+) CD25(+) regulatory T cells and infectious tolerance. Transplantation 2004; 77:S23-5.
29. Stephens LA, Mottet C, Mason D et al. Human CD4(+) CD25(+) thymocytes and peripheral T cells have immune suppressive activity in vitro. Eur J Immunol 2001; 31:1247-54.
30. Itoh M, Takahashi T, Sakaguchi N et al. 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 1999; 162:5317-26.
31. Jordan MS, Boesteanu A, Reed AJ et al. Thymic selection of CD4+ CD25+ regulatory T cells induced by an agonist self-peptide. Nat Immunol 2001; 2:301-6.
32. Romagnoli P, Hudrisier D, van Meerwijk JP. Preferential recognition of self antigens despite normal thymic deletion of CD4(+) CD25(+) regulatory T cells. J Immunol 2002; 168:1644-8.
33. Pacholczyk R, Kraj P, Ignatowicz L. Peptide specificity of thymic selection of CD4+ CD25+ T cells. J Immunol 2002; 168:613-20.
34. Akbar AN, Taams LS, Salmon M et al. The peripheral generation of CD4+ CD25+ regulatory T cells. Immunology 2003; 109:319-25.
35. Tiemessen MM, Hoffen E, Knulst AC et al. CD4 CD25 regulatory T cells are not functionally impaired in adult patients with IgE-mediated cow's milk allergy. J Allergy Clin Immunol 2002; 110:934-6.
36. Papiernik M, de Moraes ML, Pontoux C et al. Regulatory CD4 T cells: expression of IL-2R alpha chain, resistance to clonal deletion and IL-2 dependency. Int Immunol 1998; 10:371-8.
37. Salomon B, Lenschow DJ, Rhee L et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+ CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000; 12:431-40.
38. Kumanogoh A, Wang X, Lee I et al. Increased T cell autoreactivity in the absence of CD40-CD40 ligand interactions: a role of CD40 in regulatory T cell development. J Immunol 2001; 166:353-60.
39. Patel DD. Escape from tolerance in the human X-linked autoimmunity-allergic disregulation syndrome and the Scurfy mouse. J Clin Invest 2001; 107:155-7.
40. Bellinghausen I, Klostermann B, Knop J et al. Human CD4+ CD25+ T cells derived from the majority of atopic donors are able to suppress TH1 and TH2 cytokine production. J Allergy Clin Immunol 2003; 111:862-8.
41. Cosmi L, Liotta F, Angeli R et al. Th2 cells are less susceptible than Th1 cells to the suppressive activity of CD25+ regulatory thymocytes because of their responsiveness to different cytokines. Blood 2004; 103:3117-21.
42. Ling EM, Smith T, Nguyen XD et al. Relation of CD4+ CD25+ regulatory T-cell suppression of allergen-driven T-cell activation to atopic status and expression of allergic disease. Lancet 2004; 363:608-15.
43. Ou LS, Goleva E, Hall C et al. T regulatory cells in atopic dermatitis and subversion of their activity by superantigens. J Allergy Clin Immunol 2004; 113:756-63.
44. Suto A, Nakajima H, Kagami SI et al. Role of CD4(+) CD25(+) regulatory T cells in T helper 2 cell-mediated allergic inflammation in the airways. Am J Respir Crit Care Med 2001; 164:680-7.
45. Cottrez F, Hurst SD, Coffman RL, Groux H. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000; 165:4848-53.
46. Curottodel Lafaille MA, Muriglan S, Sunshine MJ et al. Hyper immunoglobulin E response in mice with monoclonal populations of B and T lymphocytes. J Exp Med 2001; 194:1349-59.
47. Baecher-Allan C. Viglietta V, Hafler DA. Inhibition of human CD4(+) CD25 (+high) regulatory T cell function. J Immunol 2002; 169:6210-17.
48. Roelofs-Haarhuis K, Wu X, Nowak M et al. Infectious nickel tolerance: a reciprocal interplay of tolerogenic APCs and T suppressor cells that is driven by immunization. J Immunol 2003; 171:2863-72.
49. Lecart S, Boulay V, Raison-Peyron N et al. Phenotypic characterization of human CD4+ regulatory T cells obtained from cutaneous dinitrochlorobenzene- induced delayed type hypersensitivity reactions. J Invest Dermatol 2001; 117:318-25.
50. Cavani A, Nasorri F, Ottaviani C et al. Human CD25+ regulatory T cells maintain immune tolerance to nickel in healthy, nonallergic individuals. J Immunol 2003; 171:5760-8.
51. Teraki Y, Shiohara T. IFN-gamma-producing effector CD8+ T cells and IL-10-producing regulatory CD4+ T cells in fixed drug eruption. J Allergy Clin Immunol 2003; 112:609-15.
52. Hori S, Carvalho TL, Demengeot J. CD25+ CD4+ regulatory T cells suppress CD4+ T cell-mediated pulmonary hyperinflammation driven by Pneumocystis carinii in immunodeficient mice. Eur J Immunol 2002; 32:1282-91.
53. MacDonald AJ, Duffy M, Brady MT et al. CD4 T helper type 1 and regulatory T cells induced against the same epitopes on the core protein in hepatitis C virus-infected persons. J Infect Dis 2002; 185:720-7.
54. Belkaid Y, Piccirillo CA, Mendez S et al. CD4+ CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 2002; 420:502-7.
55. Xu D, Liu H, Komai-Koma M et al. CD4+ CD25+ regulatory T cells suppress differentiation and functions of Th1 and Th2 cells, Leishmania major infection, and colitis in mice. J Immunol 2003; 170:394-9.
56. Trenado A, Fisson S, Braunberger E et al. Ex vivo selection of recipient-type alloantigen-specific CD4(+) CD25(+) immunoregulatory T cells for the control of graft-versus-host disease after allogeneic hematopoietic stem-cell transplantation. Transplantation 2004; 77:S32-4.
57. Trenado A, Charlotte F, Fisson S et al. Recipient-type specific CD4+ CD25+ regulatory T cells favor immune reconstitution and control graft-versus-host disease while maintaining graft-versus-leukemia. J Clin Invest 2003; 112:1688-96.
58. Morris ES, MacDonald KP, Rowe V et al. Donor treatment with pegylated G-CSF augments the generation of IL-10-producing regulatory T cells and promotes transplantation tolerance. Blood 2004; 103:3573-81.
59. Waldmann H, Graca L, Cobbold S et al. Regulatory T cells and organ transplantation. Semin Immunol 2004; 16:119-26.
60. Taams LS, Vukmanovic-Stejic M, Smith J et al. Antigen-specific T cell suppression by human CD4+ CD25+ regulatory T cells. Eur J Immunol 2002; 32:1621-30.
61. Kingsley CI, Karim M, Bushell AR et al. CD25+ CD4+ regulatory T cells prevent graft rejection: CTLA-4- and IL-10-dependent immunoregulation of alloresponses. J Immunol 2002; 168:1080-6.
62. Graca L, Cobbold SP, Waldmann H. Identification of regulatory T cells in tolerated allografts. J Exp Med 2002; 195:1641-6.
63. Wolf AM, Wolf D, Steurer M et al. Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res 2003; 9:606-12.
64. Onizuka S, Tawara I, Shimizu J et al. Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor alpha) monoclonal antibody. Cancer Res 1999; 59:3128-33.
65. Steitz J, Bruck J, Lenz J et al. Depletion of CD25(+) CD4(+) T cells and treatment with tyrosinase-related protein 2-transduced dendritic cells enhance the interferon alpha-induced, CD8(+) T-cell-dependent immune defense of B16 melanoma. Cancer Res 2001; 61:8643-6.
66. Sutmuller RP, van Duivenvoorde LM, van Elsas A et al. Synergism of cytotoxic T lymphocyte-associated antigen 4 blockade and depletion of CD25(+) regulatory T cells in antitumor therapy reveals alternative pathways for suppression of autoreactive cytotoxic T lymphocyte responses. J Exp Med 2001; 194:823-32.
67. Awwad M, North RJ. Cyclophosphamide-induced immunologically mediated regression of a cyclophosphamide-resistant murine tumor: a consequence of eliminating precursor L3T4+ suppressor T-cells. Cancer Res 1989; 49:1649-54.
68. Awwad M, North RJ. Sublethal, whole-body ionizing irradiation can be tumor promotive or tumor destructive depending on the stage of development of underlying antitumor immunity. Cancer Immunol Immunother 1988; 26:55-60.
69. Wang HY, Lee DA, Peng G et al. Tumor-specific human CD4+ regulatory T cells and their ligands: implications for immunotherapy. Immunity 2004; 20:107-18.
70. Elmets CA, Bergstresser PR, Tigelaar RE et al. Analysis of the mechanism of unresponsiveness produced by haptens painted on skin exposed to low dose ultraviolet radiation. J Exp Med 1983; 158:781-94.
71. Toews GB, Bergstresser PR, Streilein JW. Epidermal Langerhans cell density determines whether contact hypersensitivily or unresponsiveness follows skin painting with DNFB. J Immunol 1980; 124:445-53.
72. Schwarz A, Maeda A, Wild MK et al. Ultraviolet radiation-induced regulatory T cells not only inhibit the induction but can suppress the effector phase of contact hypersensitivity. J Immunol 2004; 172:1036-43.
73. Shreedhar VK, Pride MW, Sun Y et al. Origin and characteristics of ultraviolet-B radiation-induced suppressor T lymphocytes. J Immunol 1998; 161:1327-35.
74. Aubin F, Mousson C. Ultraviolet light-induced regulatory (suppressor) T cells: an approach for promoting induction of operational allograft tolerance? Transplantation 2004; 77:S29-31.
75. Chen X, Murakami T, Oppenheim JJ et al. Differential response of murine CD4+ CD25+ and CD4+. Eur J Immunol 2004; 34:859-69.
76. Adorini L. Immunomodulatory effects of vitamin D receptor ligands in autoimmune diseases. Int Immunopharmacol 2002; 2:1017-28.
77. Gregori S, Casorati M, Amuchastegui S et al. Regulatory T cells induced by 1 alpha,25-dihydroxyvitamin D3 and mycophenolate mofetil treatment mediate transplantation tolerance. J Immunol 2001; 167:1945-53.