Cytokines of the γc family control CD4+ T cell differentiation and function

Nature Immunology

Volumn 13, Issue 11, 2012, Pages 1037-1044

  Yamane, Hidehiro ^a   Paul, William E ^a  

^a NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIGEN; BETA CATENIN; CYTOKINE; GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 12 RECEPTOR; INTERLEUKIN 15; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 21; INTERLEUKIN 4; INTERLEUKIN 4 RECEPTOR ALPHA; INTERLEUKIN 6; INTERLEUKIN 7; MAJOR HISTOCOMPATIBILITY ANTIGEN; MESSENGER RNA; NOTCH RECEPTOR; PROTEIN BCL 3; RETINOIC ACID; STAT5 PROTEIN; STAT6 PROTEIN; T LYMPHOCYTE RECEPTOR; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSCRIPTION FACTOR FOXP3; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR T BET; TRANSFORMING GROWTH FACTOR BETA; UNINDEXED DRUG; WNT PROTEIN;

ADOPTIVE TRANSFER; AUTOIMMUNITY; BASOPHIL; CD25+ T LYMPHOCYTE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CELL FUNCTION; CYTOKINE PRODUCTION; DELAYED HYPERSENSITIVITY; EFFECTOR CELL; GENE EXPRESSION; HELPER CELL; IMMUNE RESPONSE; IMMUNIZATION; IN VITRO STUDY; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; RECEPTOR UPREGULATION; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL; TRICHURIS MURIS; WILD TYPE;

ANIMALS; ANTIGENS; CELL DIFFERENTIATION; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION; HUMANS; LYMPHOCYTE ACTIVATION; MICE; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, HELPER-INDUCER; TRANSCRIPTION FACTORS;

EID: 84867714627     PISSN: 15292908     EISSN: 15292916     Source Type: Journal    
DOI: 10.1038/ni.2431     Document Type: Review

References (100)

1. Bazan, J.F. Structural design and molecular evolution of a cytokine receptor superfamily. Proc. Natl. Acad. Sci. USA 87, 6934-6938 (1990).
2. Rochman, Y., Spolski, R. & Leonard, W.J. New insights into the regulation of T cells by γc family cytokines. Nat. Rev. Immunol. 9, 480-490 (2009).
3. Wang, X., Lupardus, P., Laporte, S.L. & Garcia, K.C. Structural biology of shared cytokine receptors. Annu. Rev. Immunol. 27, 29-60 (2009).
4. Dubois, S., Mariner, J., Waldmann, T.A. & Tagaya, Y. IL-15Rα recycles and presents IL-15 in trans to neighboring cells. Immunity 17, 537-547 (2002).
5. Rautajoki, K.J., Kylaniemi, M.K., Raghav, S.K., Rao, K. & Lahesmaa, R. An insight into molecular mechanisms of human T helper cell differentiation. Ann. Med. 40, 322-335 (2008).
6. Fry, T.J. & Mackall, C.L. The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J. Immunol. 174, 6571-6576 (2005).
7. Singer, A., Adoro, S. & Park, J.H. Lineage fate and intense debate: myths, models and mechanisms of CD4-versus CD8-lineage choice. Nat. Rev. Immunol. 8, 788-801 (2008).
8. Vicente, R. et al. Molecular and cellular basis of T cell lineage commitment. Semin. Immunol. 22, 270-275 (2010).
9. Zhu, J., Yamane, H. & Paul, W.E. Differentiation of effector CD4 T cell populations. Annu. Rev. Immunol. 28, 445-489 (2010).
10. Shi, M., Lin, T.H., Appell, K.C. & Berg, L.J. Janus-kinase-3- dependent signals induce chromatin remodeling at the Ifng locus during T helper 1 cell differentiation. Immunity 28, 763-773 (2008).
11. Chang, J.T., Segal, B.M. & Shevach, E.M. Role of costimulation in the induction of the IL-12/IL-12 receptor pathway and the development of autoimmunity. J. Immunol. 164, 100-106 (2000).
12. Liao, W., Lin, J.X., Wang, L., Li, P. & Leonard, W.J. Modulation of cytokine receptors by IL-2 broadly regulates differentiation into helper T cell lineages. Nat. Immunol. 12, 551-559 (2011).
13. Zheng, W. & Flavell, R.A. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89, 587-596 (1997).
14. Le Gros, G., Ben-Sasson, S.Z., Seder, R., Finkelman, F.D. & Paul, W.E. Generation of interleukin 4 (IL-4)-producing cells in vivo and in vitro: IL-2 and IL-4 are required for in vitro generation of IL-4-producing cells. J. Exp. Med. 172, 921-929 (1990).
15. Cote-Sierra, J. et al. Interleukin 2 plays a central role in Th2 differentiation. Proc. Natl. Acad. Sci. USA 101, 3880-3885 (2004).
16. Zhu, J., Cote-Sierra, J., Guo, L. & Paul, W.E. Stat5 activation plays a critical role in Th2 differentiation. Immunity 19, 739-748 (2003).
17. Liao, W. et al. Priming for T helper type 2 differentiation by interleukin 2-mediated induction of interleukin 4 receptor α-chain expression. Nat. Immunol. 11, 1288-1296 (2008).
18. + T cells: fate determination, positive feedback and plasticity. Cell Mol. Life Sci. 69, 1577-1583 (2012).
19. + T cell interactions promote TH2 cytokine-dependent immunity. Nat. Immunol. 10, 697-705 (2009).
20. + T cells. Nat. Immunol. 10, 706-712 (2009).
21. Sokol, C.L. et al. Basophils function as antigen-presenting cells for an allergen-induced T helper type 2 response. Nat. Immunol. 10, 713-720 (2009).
22. Hammad, H. et al. Inflammatory dendritic cells-not basophils-are necessary and sufficient for induction of Th2 immunity to inhaled house dust mite allergen. J. Exp. Med. 207, 2097-2111 (2010).
23. Sullivan, B.M.et al. Genetic analysis of basophil function in vivo. Nat. Immunol. 12, 527-535 (2011).
24. Parish, C.R. & Liew, F.Y. Immune response to chemically modified flagellin. 3. Enhanced cell-mediated immunity during high and low zone antibody tolerance to flagellin. J. Exp. Med. 135, 298-311 (1972).
25. + T cell responses: the alternative approaches. Annu. Rev. Immunol. 15, 297-322 (1997).
26. Aguado, E. et al. Induction of T helper type 2 immunity by a point mutation in the LAT adaptor. Science 296, 2036-2040 (2002).
27. Sommers, C.L. et al. A LAT mutation that inhibits T cell development yet induces lymphoproliferation. Science 296, 2040-2043 (2002).
28. Altin, J.A. et al. Decreased T-cell receptor signaling through CARD11 differentially compromises forkhead box protein 3-positive regulatory versus TH2 effector cells to cause allergy. J. Allergy Clin. Immunol. 127, 1277-1285 (2011).
29. + T cells to generate a Th2-inducing cytokine environment. J. Exp. Med. 202, 793-804 (2005).
30. Das, J. et al. A critical role for NF-κB in Gata3 expression and TH2 differentiation in allergic airway inflammation. Nat. Immunol. 2, 45-50 (2001).
31. Corn, R.A., Hunter, C., Liou, H.C., Siebenlist, U. & Boothby, M.R. Opposing roles for RelB and Bcl-3 in regulation of T-box expressed in T cells, GATA-3, and Th effector differentiation. J. Immunol. 175, 2102-2010 (2005).
32. Amsen, D. et al. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 27, 89-99 (2007).
33. Fang, T.C. et al. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27, 100-110 (2007).
34. Yu, Q. et al. T cell factor 1 initiates the T helper type 2 fate by inducing the transcription factor GATA-3 and repressing interferon-γ. Nat. Immunol. 10, 992-999 (2009).
35. Schulze-Luehrmann, J. & Ghosh, S. Antigen-receptor signaling to nuclear factor κB. Immunity 25, 701-715 (2006).
36. + thymocyte survival. Nat. Immunol. 2, 691-697 (2001).
37. Ong, C.T., Sedy, J.R., Murphy, K.M. & Kopan, R. Notch and presenilin regulate cellular expansion and cytokine secretion but cannot instruct Th1/Th2 fate acquisition. PLoS ONE 3, e2823 (2008).
38. Everts, B. et al. Omega-1, a glycoprotein secreted by Schistosoma mansoni eggs, drives Th2 responses. J. Exp. Med. 206, 1673-1680 (2009).
39. Steinfelder, S. et al. The major component in schistosome eggs responsible for conditioning dendritic cells for Th2 polarization is a T2 ribonuclease (omega-1). J. Exp. Med. 206, 1681-1690 (2009).
40. Swain, S.L., Weinberg, A.D., English, M. & Huston, G. IL-4 directs the development of Th2-like helper effectors. J. Immunol. 145, 3796-3806 (1990).
41. van Panhuys, N. et al. In vivo studies fail to reveal a role for IL-4 or STAT6 signaling in Th2 lymphocyte differentiation. Proc. Natl. Acad. Sci. USA 105, 12423-12428 (2008).
42. Paul, W.E. & Zhu, J. How are TH2-type immune responses initiated and amplified? Nat. Rev. Immunol. 10, 225-235 (2010).
43. Zhu, J. et al. Conditional deletion of Gata3 shows its essential function in TH1-TH2 responses. Nat. Immunol. 5, 1157-1165 (2004).
44. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M. & Toda, M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor α-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155, 1151-1164 (1995).
45. + T cell tolerance. Nat. Immunol. 6, 512-519 (2010).
46. Lio, C.W. & Hsieh, C.S. A two-step process for thymic regulatory T cell development. Immunity 28, 100-111 (2008).
47. Burchill, M.A. et al. Linked T cell receptor and cytokine signaling govern the development of the regulatory T cell repertoire. Immunity 28, 112-121 (2008).
48. Fontenot, J.D., Rasmussen, J.P., Gavin, M.A. & Rudensky, A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nat. Immunol. 6, 1142-1151 (2005).
49. Yu, A., Zhu, L., Altman, N.H. & Malek, T.R. A low interleukin-2 receptor signaling threshold supports the development and homeostasis of T regulatory cells. Immunity 30, 204-217 (2009).
50. + regulatory T cells. J. Immunol. 178, 280-290 (2007).
51. + regulatory T cell development. J. Immunol. 181, 3285-3290 (2007).
52. + regulatory T cells. Nat. Immunol. 9, 632-640 (2008).
53. Ouyang, W., Beckett, O., Ma, Q. & Li, M.O. Transforming growth factor-β signaling curbs thymic negative selection promoting regulatory T cell development. Immunity 32, 642-653 (2010).
54. + regulatory T cells by TGF-β induction of transcription factor Foxp3. J. Exp. Med. 198, 1875-1886 (2003).
55. + T regulatory cells. J. Immunol. 178, 4022-4026 (2007).
56. Elias, K.M. et al. Retinoic acid inhibits Th17 polarization and enhances FoxP3 expression through a Stat-3/Stat-5 independent signaling pathway. Blood 111, 1013-1020 (2008).
57. + regulatory T cells via a TGF-β and retinoic acid-dependent mechanism. J. Exp. Med. 204, 1757-1764 (2007).
58. Benson, M.J., Pino-Lagos, K., Rosemblatt, M. & Noelle, R.J. All-trans retinoic acid mediates enhanced Treg cell growth, differentiation, and gut homing in the face of high levels of co-stimulation. J. Exp. Med. 204, 1765-1774 (2007).
59. Sun, C.M. et al. Small intestine lamina propria dendritic cells promote de novo generation of Foxp3 T reg cells via retinoic acid. J. Exp. Med. 204, 1775-1785 (2007).
60. + T cell effector responses via retinoic acid receptor α. Immunity 34, 435-447 (2011).
61. + T cell suppressor function. J. Immunol. 172, 6519-6523 (2004).
62. + regulatory T cell activity. J. Immunol. 175, 7274-7280 (2005).
63. + T cells. Nat. Immunol. 8, 1353-1362 (2007).
64. Bettelli, E., Korn, T., Oukka, M. & Kuchroo, V.K. Induction and effector functions of TH17 cells. Nature 453, 1051-1057 (2008).
65. Dong, C. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8, 337-348 (2008).
66. Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. & Stockinger, B. TGFβ in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing cells. Immunity 24, 179-189 (2006).
67. Mangan, P.R. et al. Transforming growth factor-β induces development of the TH17 lineage. Nature 441, 231-234 (2006).
68. Bettelli, E. et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 441, 235-238 (2006).
69. + T helper cells. Cell 126, 1121-1133 (2006).
70. Nurieva, R. et al. Essential autocrine regulation by IL-21 in the generation of inflammatory T cells. Nature 448, 480-483 (2007).
71. Bauquet, A.T. et al. The costimulatory molecule ICOS regulates the expression of c-Maf and IL-21 in the development of follicular T helper cells and TH-17 cells. Nat. Immunol. 10, 167-175 (2009).
72. Korn, T. et al. IL-21 initiates an alternative pathway to induce proinflammatory TH17 cells. Nature 448, 484-487 (2007).
73. Zhou, L. et al. IL-6 programs TH-17 cell differentiation by promoting sequential engagement of the IL-21 and IL-23 pathways. Nat. Immunol. 8, 967-974 (2008).
74. Sonderegger, I., Kisielow, J., Meier, R., King, C. & Kopf, M. IL-21 and IL-21R are not required for development of Th17 cells and autoimmunity in vivo. Eur. J. Immunol. 38, 1833-1838 (2008).
75. Crotty, S. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29, 621-663 (2011).
76. Nurieva, R.I. et al. Bcl6 mediates the development of T follicular helper cells. Science 325, 1001-1005 (2009).
77. Johnston, R.J. et al. Bcl6 and Blimp-1 are reciprocal and antagonistic regulators of T follicular helper cells. Science 325, 1006-1010 (2009).
78. Yu, D. et al. The transcriptional repressor Bcl-6 directs T follicular helper cell lineage commitment. Immunity 31, 457-468 (2009).
79. Breitfeld, D. et al. Follicular B helper T cells express CXC chemokine receptor 5, localize to B cell follicles, and support immunoglobulin production. J. Exp. Med. 192, 1545-1552 (2000).
80. Schaerli, P. et al. CXC chemokine receptor 5 expression defines follicular homing T cells with B cell helper function. J. Exp. Med. 192, 1553-1562 (2000).
81. Haynes, N.M. et al. Role of CXCR5 and CCR7 in follicular Th cell positioning and appearance of a programmed cell death gene-1high germinal center-associated subpopulation. J. Immunol. 179, 5099-5108 (2007).
82. M'Hidi, H. et al. High expression of the inhibitory receptor BTLA in T-follicular helper cells and in B-cell small lymphocytic lymphoma/chronic lymphocytic leukemia. Am. J. Clin. Pathol. 132, 589-596 (2009).
83. Yusuf, I. et al. Germinal center T follicular helper cell IL-4 production is dependent on signaling lymphocytic activation molecule receptor (CD150). J. Immunol. 185, 190-202 (2010).
84. Nurieva, R.I. et al. Generation of T follicular helper cells is mediated by interleukin-21 but independent of T helper 1, 2, or 17 cell lineages. Immunity 29, 138-149 (2008).
85. Poholek, A.C. et al. In vivo regulation of Bcl6 and T follicular helper cell development. J. Immunol. 185, 313-326 (2010).
86. Eto, D. et al. IL-21 and IL-6 are critical for different aspects of B cell immunity and redundantly induce optimal follicular helper CD4 T cell (Tfh) differentiation. PLoS ONE 6, e17739 (2011).
87. Laurence, A. et al. Interleukin-2 signaling via STAT5 constrains T helper 17 cell generation. Immunity 26, 371-381 (2007).
88. Yang, X.P. et al. Opposing regulation of the locus encoding IL-17 through direct, reciprocal actions of STAT3 and STAT5. Nat. Immunol. 12, 247-254 (2011).
89. Choi, Y.S. et al. ICOS receptor instructs T follicular helper cell versus effector cell differentiation via induction of the transcriptional repressor Bcl6. Immunity 34, 932-946 (2011).
90. Oestreich, K.J., Mohn, S.E. & Weinmann, A.S. Molecular mechanisms that control the expression and activity of Bcl-6 in TH1 cells to regulate flexibility with a TFH-like gene profile. Nat. Immunol. 13, 405-411 (2012).
91. Ballesteros-Tato, A. et al. Interleukin-2 inhibits germinal center formation by limiting T follicular helper cell differentiation. Immunity 36, 847-856 (2012).
92. Johnston, R.J., Choi, Y.S., Diamond, J.A., Yang, J.A. & Crotty, S. STAT5 is a potent negative regulator of TFH cell differentiation. J. Exp. Med. 209, 243-250 (2012).
93. Nurieva, R.I. et al. STAT5 protein negatively regulates T follicular hlper (Tfh) cell generation and function. J. Biol. Chem. 287, 11234-11239 (2012).
94. + regulatory T cell induction and expansion. J. Immunol. 183, 4895-4903 (2009).
95. + T cells. Proc. Natl. Acad. Sci. USA 106, 876-881 (2009).
96. Molinero, L.L., Miller, M.L., Evaristo, C. & Alegre, M.L. High TCR stimuli prevent induced regulatory T cell differentiation in a NF-κB-dependent manner. J. Immunol. 186, 4609-4617 (2011).
97. Fazilleau, N., McHeyzer-Williams, L.J., Rosen, H. & McHeyzer-Williams, M.G. The function of follicular helper T cells is regulated by the strength of T cell antigen receptor binding. Nat. Immunol. 10, 375-384 (2009).
98. Lee, I.H., Li, W.P., Hisert, K.B. & Ivashkiv, L.B. Inhibition of interleukin 2 signaling and signal transducer and activator of transcription (STAT)5 activation during T cell receptor-mediated feedback inhibition of T cell expansion. J. Exp. Med. 190, 1263-1274 (1999).
99. Powell, J.D., Pollizzi, K.N., Heikamp, E.B. & Horton, M.R. Regulation of immune responses by mTOR. Annu. Rev. Immunol. 30, 39-68 (2012).
100. Chi, H. Regulation and function of mTOR signalling in T cell fate decisions. Nat. Rev. Immunol. 12, 325-338 (2012).