Involvement of IL-2 in homeostasis of regulatory T cells: The IL-2 cycle

BioEssays

Volumn 30, Issue 9, 2008, Pages 875-888

  Yarkoni, Shai ^a,c   Kaminitz, Ayelet ^b   Sagiv, Yuval ^a   Yaniv, Isaac ^b   Askenasy, Nadir ^b  

^a Target In Ltd   (Israel)

^b SCHNEIDER CHILDREN S MEDICAL CENTER OF ISRAEL   (Israel)

^c NONE   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; INTERLEUKIN 10; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR; TRANSFORMING GROWTH FACTOR BETA;

ARTICLE; CD25+ T LYMPHOCYTE; CELL MATURATION; CELLULAR IMMUNITY; CYTOTOXIC T LYMPHOCYTE; DOWN REGULATION; HOMEOSTASIS; HUMAN; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE FUNCTION; LYMPHOCYTE PROLIFERATION; MOLECULAR EVOLUTION; NEGATIVE FEEDBACK; NONHUMAN; POSITIVE FEEDBACK; PROTEIN EXPRESSION; PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; HOMEOSTASIS; HUMANS; INTERLEUKIN-10; INTERLEUKIN-2; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LYMPHOCYTE ACTIVATION; MICE; MICE, TRANSGENIC; MODELS, IMMUNOLOGICAL; RECEPTORS, INTERLEUKIN-2; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

ERAGROSTIS TEF;

EID: 50249091720     PISSN: 02659247     EISSN: None     Source Type: Journal    
DOI: 10.1002/bies.20812     Document Type: Article

References (110)

1. Shevach EM. 2000. Regulatory T cells in autoimmmunity. Annu Rev Immunol 18:423-449.
2. Shevach EM. 2002. CD4+CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2:389-400.
3. Sakaguchi S. 2005. Naturally arising Foxp3-expressing CD25 CD4 regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 6:345-352.
4. Sakaguchi S, Ono M, Setoguchi R, et al. 2006. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 212:8-27.
5. Maloy KJ, Powrie F. 2001. Regulatory T cells in the control of immune pathology. Nat Immunol 2:816-822.
6. Bluestone JA ,Abbas AK. 2003. Natural versus adaptive regulatory T cells. Nat Rev Immunol 3:253-257.
7. Fehervari Z, Sakaguchi S. 2004. CD4+ Tregs and immune control. J Clin Invest 114:1209-1217.
8. Schwartz RH. 2005. Natural regulatory T cells and self-tolerance. Nat Immunol 6:327-330.
9. Paust S, Cantor H. 2005. Regulatory T cells and autoimmune disease. Immunol Rev 204:195-207.
10. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. 1995. Immunologic self-tolerance maintained by activated T cells expressing L-2 Receptor a-Chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J Immunol 155: 1151-1164.
11. Shevach EM. 2006. From vanilla to 28 flavors: multiple varieties of T regulatory cells. Immunity 25:195-201.
12. Jonuleit H, Schmitt E. 2003. The regulatory T cell family: distinct subsets and their interrelations. J Immunol 171:6323-6327.
13. Cottrez F, Groux H. 2004. Specialization in tolerance: innate CD4+CD25+ versus acquired Tr1 and Th3 regulatory T cells. Transplantation 77:S12-S15.
14. + T cells inhibit both the induction and effector function of autoreactive T cells and represent a unique lineage of immunoregulatory cells. J Immunol 160:1212-1218.
15. Smith KA. 1988. lnterleukin-2: inception, impact, and implications. Science 240:1169-1176.
16. Willerford DM, Chen J, Ferry JA, Davidson L, Ma A, Alt FW. 1995. Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity 3:521-530.
17. Hori S, Nomura T, Sakaguchi S. 2003. Control of regulatory T cell development by the transcription factor Foxp3. Science 299:1057-1061.
18. Gavin MA, Rasmussen JP, Fontenot JD, et al. 2007. Foxp3-dependent programme of regulatory T-cell differentiation. Nature 445:771-775.
19. Fontenot JD, Rasmussen JP, Williams LM, Dooley JL, Farr AG, Rudensky AY. 2005. Regulatory T cell lineage specification by the forkhead transcription factor Foxp3. Immunity 22:329-341.
20. + naturally anergic and suppressive T cells as a key function of the thymus in maintaining immunologic self-tolerance. J Immunol 162:5317-5326.
21. + T cells as a functionally and phenotypically distinct immunoregulatory T cell subpopulation. Int Immunol 12:1145-1155.
22. 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.
23. + regulatory cells mediate dominant transplantation tolerance. J Immunol 168:5558-5565.
24. + T cell subsets. J Leukoc Biol 82:335-346.
25. Park HB, Paik DJ, Jang E, Hong S, Youn J. 2004. Acquisition of anergic and suppressive activities in transforming growth factor-beta-costimulated CD4+CD25- T cells. Int Immunol 16:1203-1213.
26. Li R, Perez N, Karumuthil-Melethil S, Prablhakar BS, Holterman MJ, Vasu C. 2007. Enhanced engagement of CTLA-4 induces antigen-specific CD4+CD25+Foxp3+ and CD4+CD25- TGF-beta 1+ adaptive regulatory T cells. J Immunol 179:5191-5203.
27. Qiao M, Thornton AM, Shevach EM. 2007. CD4+ CD25+ regulatory T cells render naive CD4+ CD25- T cells anergic and suppressive. Immunology 120:447-455.
28. Vieira PL, Christensen JR, Minaee S, et al. 2004. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol 172:5986-5993.
29. Kim CH. 2005. The greater chemotactic network for lymphocyte trafficking: chemokines and beyond. Curr Opin Hematol 12:298-304.
30. Wei S, Kryczek I, Zou W. 2006. Regulatory T cell compartmentalization and trafficking. Blood 108:426-431.
31. Chen Z, Herman AE, Matos M, Mathis D, Benoist C. 2005. Where CD4+CD25+ T reg cells impinge on autoimmune diabetes. J Exp Med 202:1387-1397.
32. Siegmund K, Feuerer M, Siewert C, et al. 2005. Migration matters: regulatory T-cell compartmentalization determines suppressive activity in vivo. Blood 106:3097-3104.
33. Raimondi G, Turner MS, Thomson AW, Morel PA. 2007. Naturally occurring regulatory T cells: recent insights in health and disease. Crit Rev Immunol 27:61-95.
34. 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.
35. Green EA, Gorelik L, McGregor CM, Tran EH, Flavell RA. 2003. CD4+CD25+ T regulatory cells control anti-islet CD8+ T cells through TGF-beta-TGF-beta receptor interactions in type 1 diabetes. Proc Natl Acad Sci USA 100:10878-10883.
36. Weber SE, Harbertson J, Godebu E, Mros GA, Padrick RC, et al. 2006. Adaptive islet-specific regulatory CD4 T cells control autoimmune diabetes and mediate the disappearance of pathogenic Th1 cells in vivo. J Immunol 176:4730-4739.
37. Fisson S, Darrasse-Jeze G, Litvinova E, Septier F, Klatzmann D, et al. 2003. Continuous activation of autoreactive CD4+ CD25+ regulatory T cells in the steady state. J Exp Med 198:737-746.
38. Mohamood AS, Trujillo CJ, Zheng D, Jie C, Murillo FM, et al. 2006. Gld mutation of Fas ligand increases the frequency and up-regulates cell survival genes in CD25+CD4+ TR cells. Int Immunol 18:126512-126577.
39. Askenasy N, Kaminitz A, Yarkoni S. 2008, Mechanisms of T regulatory cell function. Autoimmun Rev 7:370-375.
40. Bienvenu B, Martin B, Auffray C, Cordier C, Becourt C, Lucas B. 2005. Peripheral CD8+CD25+ T lymphocytes from MHC class II-deficient mice exhibit regulatory activity. J Immunol 175:246-253.
41. Thornton AM, Shevach EM. 2000. Suppressor effector function of CD4+CD25+ immunoregulatory T cells is antigen nonspecific. J Immunol 164:183-190.
42. Barthlott T, Kassiotis G, Stockinger B. 2003. T cell regulation as a side effect of homeostasis and competition. J Exp Med 197:451-460.
43. Tang Q, Henriksen KJ, Bi M, Finger EB, Szot G, et al. 2004. In vitro-expanded antigen-specific regulatory T cells suppress autoimmune diabetes. J Exp Med 199:1455-1465.
44. Kumar V. 2004. Homeostatic control of immunity by TCR peptide-specific Tregs. J Clin Invest 114:1222-1226.
45. Steiner D, Brunicki N, Blazar BR, Bachar-Lustig E, Reisner Y. 2006. Tolerance induction by third-party "off-the-shelf" CD4+CD25+ Treg cells. Exp Hematol 34:66-71.
46. Banz A, Pontoux C, Papiernik. M. 2002. Modulation of Fas-dependent apoptosis: a dynamic process controlling both the persistence and death of CD4 regulatory T cells and effector T cells. J Immunol 169: 750-757.
47. Pandyan P, Lenardo MJ. 2008. The control of CD4+CD25+Foxp3+ regulatory T cell survival. Biol Direct 3:6.
48. Yolcu ES, Kaminitz A, Ash S, Sagiv Y, Askenasy N, Yarkoni S. 2008. Apoptosis as a mechanism of T regulatory cell homeostasis and suppression. Immunol Cell Biol in press.
49. Malek TR, Bayer AL. 2004. Tolerance, not immunity, crucially depends on IL-2. Nat Rev Immunol 4:665-674.
50. Nelson BH. 2004. IL-2, regulatory T cells, and tolerance. J Immunol 172:3983-3988.
51. Kim HP, Kelly J, Leonard WJ. 2001. The basis for IL-2-induced IL-2 receptor alpha chain gene regulation: importance of two widely separated IL-2 response elements. Immunity 15:159-172.
52. D'Cruz LM, Klein L. 2005. Development and function of agonist-induced CD25+Foxp3+ regulatory T cells in the absence of interleulkin 2 signaling. Nat Immunol 6:1151-1158.
53. Fontenot JD, Rasmussen JP, Gavin MA, Rudensky AY. 2005. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat Immunol 6:1142-1151.
54. Maloy KJ, Powrie F. 2005. Fueling regulation: IL-2 keeps CD4+ Treg cells fit. Nat Immunol 6:1071-1072.
55. Bayer AL, Yu A, Malek TR. 2007. Function of the IL-2R for thymic and peripheral CD4+CD25+ Foxp3+ T regulatory cells. J Immunol 178: 4062-4071.
56. Malek TR, Yu A, Vincek V, Scibelli P, Kong L. 2002. CD4 regulatory T cells prevent lethal autoimmunity in IL-2R-deficient mice. Implications for the nonredundant function of IL-2. Immunity 17:167-178.
57. + T regulatory cell development during the neonatal period. J Exp Med 201:769-777.
58. + T cell numbers. J Immunol 169:4850-4860.
59. + regulatory T cell function. J Exp Med 196:851-857.
60. + regulatory T cells by peripheral expansion. J Immunol 173:7259-7268.
61. Setoguchi R, Hori S, Takahashi T, Sakaguchi S. 2005. Homeostatic maintenance of natural Foxp3+CD25+CD4V regulatory T cells by interleukin (IL)-2 and induction of autoimmune disease by IL-2 neutralization. J Exp Med 201:723-735.
62. + regulatory T cell function. Eur J Immunol 34:2480-2488.
63. + T cell suppressor function. J Immunol 172:6519-6523.
64. Suzuki H, Kündig TM, Furlonger C, Wakeham A, Timms E, et al. 1995. Deregulated T cell activation and autoimmunity in mice lacking interleukin-2 receptor beta. Science 268:1472-1476.
65. Kung JT, Beller D, Ju ST. 1998. Lymphokine regulation of activation-induced apoptosis in T cells of IL-2 and IL-2R beta knockout mice. Cell Immunol 185:158-163.
66. Laurence A, Tato CM, Davidson TS, et al. 2007. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26:371-381.
67. Kramer S, Schimpl A, Hunig T. 1995. Immunopathology of interleukin (IL) 2-deficient mice: thymus dependence and suppression by thymus-dependent cells with an intact IL-2 gene. J Exp Med 182:1769-1776.
68. Martin B, Banz A, Bienvenu B, Cordier C, Dautigny N, Becourt C, Lucas B. 2004. Suppression of CD4+ T lymphocyte effector functions by CD4+CD25+ cells in vivo. J Immunol 172:3391-3398.
69. Steiger J, Nickerson PW, Steurer W, Moscovitch-Lopatin M, Strom TB. 1995. IL-2 knockout recipient mice reject islet cell allografts. J Immunol 155:489-498.
70. Van Parijs L, Biuckians A, Ibragimov A, Alt FW, Willerford DM, Abbas AK. 1997. Functional responses and apoptosis of CD25 (IL-2R)-deficient T cells expressing a transgenic antigen receptor. J Immunol 158:3738-3745.
71. Leung DT, Morefield S, Willerford DM. 2000. Regulation of lymphoid homeostasis by IL-2 receptor signals in vivo. J Immunol 164:3527-3534.
72. D'Souza WN, Schluns KS, Masopust D, Lefrancois L. 2002. Essential role for IL-2 in the regulation of antiviral extralymphoid CD8 T cell responses. J Immunol 168:5566-5572.
73. - T cells: evidence for two distinct regulatory mechanisms. Eur J Immunol 31:1637-1645.
74. Malek TR, Porter BO, Codias EK, Scibelli P, Yu A. 2000. Normal lymphoid homeostasis and lack of lethal autoimmunity in mice containing mature T cells with severely impaired IL-2 receptors. J Immunol 164:2905-2914.
75. Marie JC, Letterio JJ, Gavin M, Rudensky AY, 2005. TGF-beta1 maintains suppressor function and Foxp3 expression in CD4+CD25+ regulatory T cells. J Exp Med 201:1061-1067.
76. Zhang H, Chua KS, Guimond M, Kapoor V, Brown MV, et al. 2005. Lymphopenia and interleukin-2 therapy alter homeostasis of CD4+CD25+ regulatory T cells. Nat Med 11:1238-1243.
77. Fehervari Z, Yamaguchi T, Sakaguchi S. 2006. The dichotomous role of IL-2: tolerance versus immunity. Trends Immunol 27:109-111.
78. Knoechel B, Lohr J, Kahn E, Bluestone JA, Abbas AK. 2005. Sequential development of interleukin 2-dependent effector and regulatory T cells in response to endogenous systemic antigen. J Exp Med 202:1375-1386.
79. Lenardo MJ. 1991. Interleukin-2 programs mouse T lymphocytes for apoptosis. Nature 353:858-861.
80. Refaeli Y, Van Parijs L, London CA, Tschopp J, Abbas AK. 1998. Biochemical mechanisms of IL-2-regulated Fas-mediated T cell apoptosis. Immunity 8:615-623.
81. - cells to develop suppressive activity: the role of IL-2, TGF-β and IL-10. J Immunol 172:5213-5221.
82. Piccirillo CA, Letteno JJ, Thornton AM, et al. 2002. CD4+ CD25+ regulatory T cells can mediate suppressor function in the absence of transforming growth factor β1 production and responsiveness. J Exp Med 196:237-246.
83. Gondek DC, Lu L-F, Quezada SA, Sakaguchi S, Noelle RJ. 2005. Cutting edge: contact-mediated suppression by CD4+CD25+ regulatory cells involves a granzyme B-dependent, perforin-independent mechanism. J Immunol 174:1783-1786.
84. 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.
85. Graca L, Cobbold SP, Waldmann H. 2002. Identification of regulatory T cells in tolerated allografts. J Exp Med 195:1641-1646.
86. 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.
87. Miyara M, Salkaguchi S. 2007. Natural regulatory T cells: mechanisms of suppression. Trends Mol Med 13:108-116.
88. + naturally anergic and suppressive T cells. Int Immunol 10:1969-1980.
89. + immunoregulatory T cells suppress polyclonal T cell activation in vitro by inhibiting interleukin 2 production. J Exp Med 188:287-296.
90. Piccirillo CA, Shevach EM. 2001. Cuttingedge: control of CD8+ T cell activation byCD4+CD25+ immunoregulatory cells. J Immunol 167: 1137-1140.
91. Pandiyan P, Zheng L, Ishihara S, Reed J, Lenardo MJ. 2007. CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells. Nat Immunol 8:1353-1362.
92. Scheffold A, Huhn J, Hofer T. 2005. Regulation of CD4+CD25+ regulatory T cell activity: it takes (IL-)two to tango. Eur J Immunol 35:133613-133641.
93. Granucci F, Andrews DM, Degli-Esposti MA, Ricciardi-Castagnoli P. 2002. IL-2 mediates adjuvant effect of dendritic cells. Trends Immunol 23:169-171.
94. Groux H, Fournier N, Cottrez F. 2004. Role of dendritic cells in the generation of regulatory T cells. Semin Immunol 16:99-106.
95. Yamazaki S, Inaba K, Tarbell KV, Steinman RM. 2006. Dendritic cells expand antigen-specific Foxp3+ CD25+ CD4v regulatory T cells including suppressors of alloreactivity. Immunol Rev 212:314-329.
96. Davidson TS, DiPaolo RJ, Andersson J, Shevach EM. 2007. Cutting Edge: IL-2 is essential for TGF-beta-mediated induction of Foxp3+ T regulatory cells. J Immunol 178:4022-4026.
97. 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.
98. Tang Q, Boden EK, Henriksen KJ, Bour-Jordan H, Bi M, Bluestone JA. 2004. Distinct roles of CTLA-4 and TGF-beta in CD4+CD25+ regulatory T cell function. Eur J Immunol 34:2996-3005.
99. King C, Davies J, Mueller R, Lee MS, Krahl T, et al. 1998. TGF-beta1 alters APC preference, polarizing islet antigen responses toward a Th2 phenotype. Immunity 8:601-613.
100. 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.
101. Ludviksson BR, Seegers D, Resnick AS, Strober W. 2000. The effect of TGF-beta1 on immune responses of naive versus memory CD4+ Th1/Th2 cells. Eur J Immunol 30:2101-2111.
102. Cottrez F, Groux H. 2001. Regulation of TGF-beta response during T cell activation is modulated by IL-10. J Immunol 167:773-778.
103. Kullberg MC, Hay V, Cheever AW, Mamura M, Sher A, et al. 2005. TGF-beta1 production by CD4+ CID25+ regulatory T cells is not essential for suppression of intestinal inflammation. Eur J Immunol 35:2886-2895.
104. Gorelik L, Constant S, Flavell RA. 2002. Mechanism of transforming growth factor beta-induced inhibition of T helper type 1 differentiation. J Exp Med 195:1499-1505.
105. Fantini MC, Becker C, Monteleone G, Pallone F, Galle PR, Neurath MF. 2004. Cutting edge: TGF-beta induces a regulatory phenotype in CD4+CD25- T cells through Foxp3 induction and down-regulation of Smad7. J Immunol 172:5149-5153.
106. + regulatory T cells. J Exp Med 201:737-746.
107. Chen W, Jin W. Hardegen N, Lei KJ, Li L, et al. 2003. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med 198: 1875-1886.
108. Moore KW, de Waal-Malefyt R, Coffman RL, O'Garra A. 2001. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 19:683-765.
109. Berenson LS, Ota N, Murphy KM. 2004. Issues in T-helper 1 development-resolved and unresolved. Immunol Rev 202:157-174.
110. + lymphocytes convert to anergic or memory-like cells in T cell-deprived recipients. Eur J Immunol 31:2256-2265.