IL-7 signaling and CD127 receptor regulation in the control of T cell homeostasis

Seminars in Immunology

Volumn 24, Issue 3, 2012, Pages 209-217

  Carrette, Florent ^a   Surh, Charles D ^a,b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b Pohang University of Science and Technology (POSTECH)   (South Korea)

Author keywords

CD127; Homeostasis; IL 7; Signaling pathways; T cells

Indexed keywords

INTERLEUKIN 15; INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR; JANUS KINASE; PHOSPHATIDYLINOSITOL 3 KINASE; STAT PROTEIN; T LYMPHOCYTE RECEPTOR;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL SURVIVAL; ENZYME ACTIVITY; LIPID RAFT; MEMORY T LYMPHOCYTE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PROCESSING; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE;

ANIMALS; HOMEOSTASIS; HUMANS; INTERLEUKIN-7; INTERLEUKIN-7 RECEPTOR ALPHA SUBUNIT; RECEPTORS, ANTIGEN, T-CELL; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 84861193543     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2012.04.010     Document Type: Review

References (106)

1. Sprent J., Surh C.D. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nature Immunology 2011, 12:478-484.
2. Surh C.D., Sprent J. Homeostasis of naive and memory T cells. Immunity 2008, 29:848-862.
3. Tough D.F., Sprent J. Turnover of naive- and memory-phenotype T cells. The Journal of Experimental Medicine 1994, 179:1127-1135.
4. Parretta E., Cassese G., Santoni A., Guardiola J., Vecchio A., Di Rosa F. Kinetics of in vivo proliferation and death of memory and naive CD8 T cells: parameter estimation based on 5-bromo-2'-deoxyuridine incorporation in spleen, lymph nodes, and bone marrow. Journal of Immunology 2008, 180:7230-7239.
5. Rochman Y., Spolski R., Leonard W.J. New insights into the regulation of T cells by gamma(c) family cytokines. Nature Reviews Immunology 2009, 9:480-490.
6. Peschon J.J., Morrissey P.J., Grabstein K.H., Ramsdell F.J., Maraskovsky E., Gliniak B.C., et al. Early lymphocyte expansion is severely impaired in interleukin 7 receptor-deficient mice. The Journal of Experimental Medicine 1994, 180:1955-1960.
7. von Freeden-Jeffry U., Vieira P., Lucian L.A., McNeil T., Burdach S.E., Murray R. Lymphopenia in interleukin (IL)-7 gene-deleted mice identifies IL-7 as a nonredundant cytokine. The Journal of Experimental Medicine 1995, 181:1519-1526.
8. Surh C.D., Sprent J. Regulation of mature T cell homeostasis. Seminars in Immunology 2005, 17:183-191.
9. Jacobs S.R., Michalek R.D., Rathmell J.C. IL-7 is essential for homeostatic control of T cell metabolism in vivo. Journal of Immunology 2010, 184:3461-3469.
10. Fontenot J.D., Rasmussen J.P., Gavin M.A., Rudensky A.Y. A function for interleukin 2 in Foxp3-expressing regulatory T cells. Nature Immunology 2005, 6:1142-1151.
11. Bayer A.L., Yu A., Malek T.R. Function of the IL-2R for thymic and peripheral CD4+CD25+ Foxp3+ T regulatory cells. Journal of Immunology 2007, 178:4062-4071.
12. Burchill M.A., Yang J., Vogtenhuber C., Blazar B.R., Farrar M.A. IL-2 receptor beta-dependent STAT5 activation is required for the development of Foxp3+ regulatory T cells. Journal of Immunology 2007, 178:280-290.
13. Bayer A.L., Lee J.Y., de la Barrera A., Surh C.D., Malek T.R. A function for IL-7R for CD4+CD25+Foxp3+ T regulatory cells. Journal of Immunology 2008, 181:225-234.
14. Mazzucchelli R., Hixon J.A., Spolski R., Chen X., Li W.Q., Hall V.L., et al. Development of regulatory T cells requires IL-7Ralpha stimulation by IL-7 or TSLP. Blood 2008, 112:3283-3292.
15. Peffault de Latour R., Dujardin H.C., Mishellany F., Burlen-Defranoux O., Zuber J., Marques R., et al. Ontogeny, function, and peripheral homeostasis of regulatory T cells in the absence of interleukin-7. Blood 2006, 108:2300-2306.
16. Feuerer M., Hill J.A., Mathis D., Benoist C. Foxp3+ regulatory T cells: differentiation, specification, subphenotypes. Nature Immunology 2009, 10:689-695.
17. Li C.R., Deiro M.F., Godebu E., Bradley L.M. IL-7 uniquely maintains FoxP3(+) adaptive Treg cells that reverse diabetes in NOD mice via integrin-beta7-dependent localization. Journal of Autoimmunity 2011, 37:217-227.
18. Ernst B., Lee D.S., Chang J.M., Sprent J., Surh C.D. The peptide ligands mediating positive selection in the thymus control T cell survival and homeostatic proliferation in the periphery. Immunity 1999, 11:173-181.
19. Tan J.T., Ernst B., Kieper W.C., LeRoy E., Sprent J., Surh C.D. Interleukin (IL)-15 and IL-7 jointly regulate homeostatic proliferation of memory phenotype CD8+ cells but are not required for memory phenotype CD4+ cells. The Journal of Experimental Medicine 2002, 195:1523-1532.
20. Schluns K.S., Kieper W.C., Jameson S.C., Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8 T cells in vivo. Nature Immunology 2000, 1:426-432.
21. Alves N.L., Richard-Le Goff O., Huntington N.D., Sousa A.P., Ribeiro V.S., Bordack A., et al. Characterization of the thymic IL-7 niche in vivo. Proceedings of the National Academy of Sciences of the United States of America 2009, 106:1512-1517.
22. Kim G.Y., Hong C., Park J.-H. Seeing is believing: illuminating the source of in vivo interleukin-7. Immune Network 2011, 11:1.
23. Link A., Vogt T.K., Favre S., Britschgi M.R., Acha-Orbea H., Hinz B., et al. Fibroblastic reticular cells in lymph nodes regulate the homeostasis of naive T cells. Nature Immunology 2007, 8:1255-1265.
24. Mazzucchelli R.I., Warming S., Lawrence S.M., Ishii M., Abshari M., Washington A.V., et al. Visualization and identification of IL-7 producing cells in reporter mice. PLoS ONE 2009, 4:e7637.
25. Repass J.F., Laurent M.N., Carter C., Reizis B., Bedford M.T., Cardenas K., et al. IL7-hCD25 and IL7-Cre BAC transgenic mouse lines: new tools for analysis of IL-7 expressing cells. Genesis 2009, 47:281-287.
26. Shalapour S., Deiser K., Sercan O., Tuckermann J., Minnich K., Willimsky G., et al. Commensal microflora and interferon-gamma promote steady-state interleukin-7 production in vivo. European Journal of Immunology 2010, 40:2391-2400.
27. Dai Z., Lakkis F.G. Cutting edge: secondary lymphoid organs are essential for maintaining the CD4, but not CD8, naive T cell pool. Journal of Immunology 2001, 167:6711-6715.
28. Dummer W., Ernst B., LeRoy E., Lee D., Surh C. Autologous regulation of naive T cell homeostasis within the T cell compartment. Journal of Immunology 2001, 166:2460-2468.
29. Guimond M., Veenstra R.G., Grindler D.J., Zhang H., Cui Y., Murphy R.D., et al. Interleukin 7 signaling in dendritic cells regulates the homeostatic proliferation and niche size of CD4+ T cells. Nature Immunology 2009, 10:149-157.
30. Martin C.E., Kim D.M., Sprent J., Surh C.D. Is IL-7 from dendritic cells essential for the homeostasis of CD4+ T cells?. Nature Immunology 2010, 11:548. [547-8; author reply].
31. Tan J.T., Dudl E., LeRoy E., Murray R., Sprent J., Weinberg K.I., et al. IL-7 is critical for homeostatic proliferation and survival of naive T cells. Proceedings of the National Academy of Sciences of the United States of America 2001, 98:8732-8737.
32. Cho J.H., Kim H.O., Surh C.D., Sprent J. T cell receptor-dependent regulation of lipid rafts controls naive CD8+ T cell homeostasis. Immunity 2010, 32:214-226.
33. Barata J.T., Silva A., Brandao J.G., Nadler L.M., Cardoso A.A., Boussiotis V.A. Activation of PI3K is indispensable for interleukin 7-mediated viability, proliferation, glucose use, and growth of T cell acute lymphoblastic leukemia cells. The Journal of Experimental Medicine 2004, 200:659-669.
34. Johnson S.E., Shah N., Bajer A.A., LeBien T.W. IL-7 activates the phosphatidylinositol 3-kinase/AKT pathway in normal human thymocytes but not normal human B cell precursors. Journal of Immunology 2008, 180:8109-8117.
35. Mazzucchelli R., Durum S.K. Interleukin-7 receptor expression: intelligent design. Nature Reviews Immunology 2007, 7:144-154.
36. Le Campion A., Bourgeois C., Lambolez F., Martin B., Leaument S., Dautigny N., et al. Naive T cells proliferate strongly in neonatal mice in response to self-peptide/self-MHC complexes. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:4538-4543.
37. Min B., McHugh R., Sempowski G.D., Mackall C., Foucras G., Paul W.E. Neonates support lymphopenia-induced proliferation. Immunity 2003, 18:131-140.
38. Swainson L., Kinet S., Mongellaz C., Sourisseau M., Henriques T., Taylor N. IL-7-induced proliferation of recent thymic emigrants requires activation of the PI3K pathway. Blood 2007, 109:1034-1042.
39. Lali F.V., Crawley J., McCulloch D.A., Foxwell B.M. A late, prolonged activation of the phosphatidylinositol 3-kinase pathway is required for T cell proliferation. Journal of Immunology 2004, 172:3527-3534.
40. Osborne L.C, Dhanji S., Snow J.W., Priatel J.J., Ma M.C., Miners M.J., et al. Impaired CD8 T cell memory and CD4 T cell primary responses in IL-7R alpha mutant mice. The Journal of Experimental Medicine 2007, 204:619-631.
41. Chetoui N., Boisvert M., Gendron S., Aoudjit F. Interleukin-7 promotes the survival of human CD4+ effector/memory T cells by up-regulating Bcl-2 proteins and activating the JAK/STAT signalling pathway. Immunology 2010, 130:418-426.
42. Park J.H., Yu Q., Erman B., Appelbaum J.S., Montoya-Durango D., Grimes H.L., et al. Suppression of IL7Ralpha transcription by IL-7 and other prosurvival cytokines: a novel mechanism for maximizing IL-7-dependent T cell survival. Immunity 2004, 21:289-302.
43. Palmer M.J., Mahajan V.S., Chen J., Irvine D.J., Lauffenburger D.A. Signaling thresholds govern heterogeneity in IL-7-receptor-mediated responses of naive CD8(+) T cells. Immunology and Cell Biology 2011, 89:581-594.
44. Fruman D.A, Bismuth G. Fine tuning the immune response with PI3K. Immunological Reviews 2009, 228:253-272.
45. Deane J.A., Kharas M.G., Oak J.S., Stiles L.N., Luo J., Moore T.I., et al. T-cell function is partially maintained in the absence of class IA phosphoinositide 3-kinase signaling. Blood 2007, 109:2894-2902.
46. Okkenhaug K., Bilancio A., Farjot G., Priddle H., Sancho S., Peskett E., et al. Impaired B and T cell antigen receptor signaling in p110delta PI 3-kinase mutant mice. Science 2002, 297:1031-1034.
47. Suzuki K., Nakajima H., Saito Y., Saito T., Leonard W.J., Iwamoto I. Janus kinase 3 (Jak3) is essential for common cytokine receptor gamma chain (gamma(c))-dependent signaling: comparative analysis of gamma(c) Jak3, and gamma(c) and Jak3 double-deficient mice. International Immunology 2000, 12:123-132.
48. Foxwell B.M., Beadling C., Guschin D., Kerr I., Cantrell D. Interleukin-7 can induce the activation of Jak 1 Jak 3 and STAT 5 proteins in murine T cells. European Journal of Immunology 1995, 25:3041-3046.
49. Jiang Q., Li W.Q., Aiello F.B., Mazzucchelli R., Asefa B., Khaled A.R., et al. Cell biology of IL-7, a key lymphotrophin. Cytokine & Growth Factor Reviews 2005, 16:513-533.
50. Rochman Y., Kashyap M., Robinson G.W., Sakamoto K., Gomez-Rodriguez J., Wagner K.U., et al. Thymic stromal lymphopoietin-mediated STAT5 phosphorylation via kinases JAK1 and JAK2 reveals a key difference from IL-7-induced signaling. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:19455-19460.
51. Yao Z., Cui Y., Watford W.T., Bream J.H., Yamaoka K., Hissong B.D., et al. Stat5a/b are essential for normal lymphoid development and differentiation. Proceedings of the National Academy of Sciences of the United States of America 2006, 103:1000-1005.
52. Seki Y., Yang J., Okamoto M., Tanaka S., Goitsuka R., Farrar M.A., et al. IL-7/STAT5 cytokine signaling pathway is essential but insufficient for maintenance of naive CD4 T cell survival in peripheral lymphoid organs. Journal of Immunology 2007, 178:262-270.
53. Hand T.W., Cui W., Jung Y.W., Sefik E., Joshi N.S., Chandele A., et al. Differential effects of STAT5 and PI3K/AKT signaling on effector and memory CD8 T-cell survival. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:16601-16606.
54. Tripathi P., Kurtulus S., Wojciechowski S., Sholl A., Hoebe K., Morris S.C., et al. STAT5 is critical to maintain effector CD8+ T cell responses. Journal of Immunology 2010, 185:2116-2124.
55. Venkitaraman A.R., Cowling R.J. Interleukin-7 induces the association of phosphatidylinositol 3-kinase with the alpha chain of the interleukin-7 receptor. European Journal of Immunology 1994, 24:2168-2174.
56. Dzhagalov I., Dunkle A., He Y.W. The anti-apoptotic Bcl-2 family member Mcl-1 promotes T lymphocyte survival at multiple stages. Journal of Immunology 2008, 181:521-528.
57. Opferman J.T., Letai A., Beard C., Sorcinelli M.D., Ong C.C., Korsmeyer S.J. Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 2003, 426:671-676.
58. Dunkle A., Dzhagalov I., He Y.W. Mcl-1 promotes survival of thymocytes by inhibition of Bak in a pathway separate from Bcl-2. Cell Death and Differentiation 2010, 17:994-1002.
59. Khaled A.R., Kim K., Hofmeister R., Muegge K., Durum S.K. Withdrawal of IL-7 induces Bax translocation from cytosol to mitochondria through a rise in intracellular pH. Proceedings of the National Academy of Sciences of the United States of America 1999, 96:14476-14481.
60. Li W.Q., Jiang Q., Khaled A.R., Keller J.R., Durum S.K. Interleukin-7 inactivates the pro-apoptotic protein Bad promoting T cell survival. The Journal of Biological Chemistry 2004, 279:29160-29166.
61. Li W.Q., Guszczynski T., Hixon J.A., Durum S.K. Interleukin-7 regulates Bim proapoptotic activity in peripheral T-cell survival. Molecular and Cellular Biology 2010, 30:590-600.
62. Buentke E., Mathiot A., Tolaini M., Di Santo J., Zamoyska R., Seddon B. Do CD8 effector cells need IL-7R expression to become resting memory cells?. Blood 2006, 108:1949-1956.
63. Pearson C., Silva A., Saini M., Seddon B. IL-7 determines homeostatic fitness of T cells by distinct mechanisms at different signalling thresholds in vivo. European Journal of Immunology 2011, 41:3656-3666.
64. Michalek R.D., Rathmell J.C. The metabolic life and times of a T-cell. Immunological Reviews 2010, 236:190-202.
65. Rathmell J.C., Farkash E.A., Gao W., Thompson C.B. IL-7 enhances the survival and maintains the size of naive T cells. Journal of Immunology 2001, 167:6869-6876.
66. Wofford J.A., Wieman H.L., Jacobs S.R., Zhao Y., Rathmell J.C. IL-7 promotes Glut1 trafficking and glucose uptake via STAT5-mediated activation of Akt to support T-cell survival. Blood 2008, 111:2101-2111.
67. Loisel-Meyer S., Swainson L., Craveiro M., Oburoglu L., Mongellaz C., Costa C., et al. Glut1-mediated glucose transport regulates HIV infection. Proceedings of the National Academy of Sciences of the United States of America 2012, 109:2549-2554.
68. Luo H., Charpentier T., Wang X., Qi S., Han B., Wu T., et al. Efnb1 and Efnb2 proteins regulate thymocyte development, peripheral T cell differentiation, and antiviral immune responses and are essential for interleukin-6 (IL-6) signaling. The Journal of Biological Chemistry 2011, 286:41135-41152.
69. Luo H., Wu Z., Qi S., Jin W., Han B., Wu J. Ephrinb1 and Ephrinb2 are associated with interleukin-7 receptor alpha and retard its internalization from the cell surface. The Journal of Biological Chemistry 2011, 286:44976-44987.
70. Henriques C.M., Rino J., Nibbs R.J., Graham G.J., Barata J.T. IL-7 induces rapid clathrin-mediated internalization and JAK3-dependent degradation of IL-7Ralpha in T cells. Blood 2010, 115:3269-3277.
71. Hemar A., Subtil A., Lieb M., Morelon E., Hellio R., Dautry-Varsat A. Endocytosis of interleukin 2 receptors in human T lymphocytes: distinct intracellular localization and fate of the receptor alpha, beta, and gamma chains. The Journal of Cell Biology 1995, 129:55-64.
72. Pua H.H., Dzhagalov I., Chuck M., Mizushima N., He Y.W. A critical role for the autophagy gene Atg5 in T cell survival and proliferation. The Journal of Experimental Medicine 2007, 204:25-31.
73. Williams R.L., Urbe S. The emerging shape of the ESCRT machinery. Nature Reviews Molecular Cell Biology 2007, 8:355-368.
74. McLeod I.X., Zhou X., Li Q.J., Wang F., He Y.W. The class III kinase Vps34 promotes T lymphocyte survival through regulating IL-7Ralpha surface expression. Journal of Immunology 2011, 187:5051-5061.
75. Kaech S.M., Tan J.T., Wherry E.J., Konieczny B.T., Surh C.D., Ahmed R. Selective expression of the interleukin 7 receptor identifies effector CD8 T cells that give rise to long-lived memory cells. Nature Immunology 2003, 4:1191-1198.
76. Klonowski K.D., Williams K.J., Marzo A.L., Lefrancois L. Cutting edge: IL-7-independent regulation of IL-7 receptor alpha expression and memory CD8 T cell development. Journal of Immunology 2006, 177:4247-4251.
77. Chandele A., Joshi N.S., Zhu J., Paul W.E., Leonard W.J., Kaech S.M. Formation of IL-7Ralphahigh and IL-7Ralphalow CD8 T cells during infection is regulated by the opposing functions of GABPalpha and Gfi-1. Journal of Immunology 2008, 180:5309-5319.
78. Xue H.H., Bollenbacher J., Rovella V., Tripuraneni R., Du Y.B., Liu C.Y., et al. GA binding protein regulates interleukin 7 receptor alpha-chain gene expression in T cells. Nature Immunology 2004, 5:1036-1044.
79. Doan L.L., Kitay M.K., Yu Q., Singer A., Herblot S., Hoang T., et al. Growth factor independence-1B expression leads to defects in T cell activation, IL-7 receptor alpha expression, and T cell lineage commitment. Journal of Immunology 2003, 170:2356-2366.
80. Guo F., Hildeman D., Tripathi P., Velu C.S., Grimes H.L., Zheng Y. Coordination of IL-7 receptor and T-cell receptor signaling by cell-division cycle 42 in T-cell homeostasis. Proceedings of the National Academy of Sciences of the United States of America 2010, 107:18505-18510.
81. Clements J.L., John S.A., Garrett-Sinha L.A. Impaired generation of CD8+ thymocytes in Ets-1-deficient mice. Journal of Immunology 2006, 177:905-912.
82. Grenningloh R., Tai T.S., Frahm N., Hongo T.C., Chicoine A.T., Brander C., et al. Ets-1 maintains IL-7 receptor expression in peripheral T cells. Journal of Immunology 2011, 186:969-976.
83. Kieper W.C., Troy A., Burghardt J.T., Ramsey C., Lee J.Y., Jiang H.Q., et al. Recent immune status determines the source of antigens that drive homeostatic T cell expansion. Journal of Immunology 2005, 174:3158-3163.
84. Kerdiles Y.M., Beisner D.R., Tinoco R., Dejean A.S., Castrillon D.H., DePinho R.A., et al. Foxo1 links homing and survival of naive T cells by regulating L-selectin CCR7 and interleukin 7 receptor. Nature Immunology 2009, 10:176-184.
85. Ouyang W., Beckett O., Flavell R.A., Li M.O. An essential role of the Forkhead-box transcription factor Foxo1 in control of T cell homeostasis and tolerance. Immunity 2009, 30:358-371.
86. Gubbels Bupp M.R., Edwards B., Guo C., Wei D., Chen G., Wong B., et al. T cells require Foxo1 to populate the peripheral lymphoid organs. European Journal of Immunology 2009, 39:2991-2999.
87. Fabre S., Carrette F., Chen J., Lang V., Semichon M., Denoyelle C., et al. FOXO1 regulates L-selectin and a network of human T cell homing molecules downstream of phosphatidylinositol 3-kinase. Journal of Immunology 2008, 181:2980-2989.
88. Hedrick S.M. The cunning little vixen: foxo and the cycle of life and death. Nature Immunology 2009, 10:1057-1063.
89. Smith K., Seddon B., Purbhoo M.A., Zamoyska R., Fisher A.G., Merkenschlager M. Sensory adaptation in naive peripheral CD4 T cells. The Journal of Experimental Medicine 2001, 194:1253-1261.
90. Kassiotis G., Zamoyska R., Stockinger B. Involvement of avidity for major histocompatibility complex in homeostasis of naive and memory T cells. The Journal of Experimental Medicine 2003, 197:1007-1016.
91. Kieper W.C., Burghardt J.T., Surh C.D. A role for TCR affinity in regulating naive T cell homeostasis. Journal of Immunology 2004, 172:40-44.
92. Park J.H., Adoro S., Lucas P.J., Sarafova S.D., Alag A.S., Doan L.L., et al. 'Coreceptor tuning': cytokine signals transcriptionally tailor CD8 coreceptor expression to the self-specificity of the TCR. Nature Immunology 2007, 8:1049-1059.
93. D'Souza W.N., Chang C.F., Fischer A.M., Li M., Hedrick S.M. The Erk2 MAPK regulates CD8 T cell proliferation and survival. Journal of Immunology 2008, 181:7617-7629.
94. Nekrasova T., Shive C., Gao Y., Kawamura K., Guardia R., Landreth G., et al. ERK1-deficient mice show normal T cell effector function and are highly susceptible to experimental autoimmune encephalomyelitis. Journal of Immunology 2005, 175:2374-2380.
95. Pages G., Guerin S., Grall D., Bonino F., Smith A., Anjuere F., et al. Defective thymocyte maturation in p44 MAP kinase (Erk 1) knockout mice. Science 1999, 286:1374-1377.
96. Lapinski P.E., Qiao Y., Chang C.H., King P.D. A role for p120 RasGAP in thymocyte positive selection and survival of naive T cells. Journal of Immunology 2011, 187:151-163.
97. Katzman S.D., Hoyer K.K., Dooms H., Gratz I.K., Rosenblum M.D., Paw J.S., et al. Opposing functions of IL-2 and IL-7 in the regulation of immune responses. Cytokine 2011, 56:116-121.
98. Xue H.H., Kovanen P.E., Pise-Masison C.A., Berg M., Radovich M.F., Brady J.N., et al. IL-2 negatively regulates IL-7 receptor alpha chain expression in activated T lymphocytes. Proceedings of the National Academy of Sciences of the United States of America 2002, 99:13759-13764.
99. Feng X., Wang H., Takata H., Day T.J., Willen J., Hu H. Transcription factor Foxp1 exerts essential cell-intrinsic regulation of the quiescence of naive T cells. Nature Immunology 2011, 12:544-550.
100. Ouyang W., Beckett O., Ma Q., Paik J.H., DePinho R.A., Li M.O. Foxo proteins cooperatively control the differentiation of Foxp3+ regulatory T cells. Nature Immunology 2010, 11:618-627.
101. Kerdiles Y.M., Stone E.L., Beisner D.R., McGargill M.A., Ch'en I.L., Stockmann C., et al. Foxo transcription factors control regulatory T cell development and function. Immunity 2010, 33:890-904.
102. Simeoni L., Posevitz V., Kolsch U., Meinert I., Bruyns E., Pfeffer K., et al. The transmembrane adapter protein SIT regulates thymic development and peripheral T-cell functions. Molecular and Cellular Biology 2005, 25:7557-7568.
103. Posevitz V., Arndt B., Krieger T., Warnecke N., Schraven B., Simeoni L. Regulation of T cell homeostasis by the transmembrane adaptor protein SIT. Journal of Immunology 2008, 180:1634-1642.
104. Alves N.L., van Leeuwen E.M., Derks I.A., van Lier R.A. Differential regulation of human IL-7 receptor alpha expression by IL-7 and TCR signaling. Journal of Immunology 2008, 180:5201-5210.
105. Zenatti P.P., Ribeiro D., Li W., Zuurbier L., Silva M.C., Paganin M., et al. Oncogenic IL7R gain-of-function mutations in childhood T-cell acute lymphoblastic leukemia. Nature Genetics 2011, 43:932-939.
106. Shinnakasu R., Yamashita M., Kuwahara M., Hosokawa H., Hasegawa A., Motohashi S., et al. Gfi1-mediated stabilization of GATA3 protein is required for Th2 cell differentiation. The Journal of Biological Chemistry 2008, 283:28216-28225.