Intrathymic IL-7: The where, when, and why of IL-7 signaling during T cell development

Seminars in Immunology

Volumn 24, Issue 3, 2012, Pages 151-158

  Hong, Changwan ^a   Luckey, Megan A ^a   Park, Jung Hyun ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

IL 7 receptor; Positive selection; SOCS; Thymocytes; Thymus

Indexed keywords

INTERLEUKIN 7; INTERLEUKIN 7 RECEPTOR;

CELL SURVIVAL; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; LYMPHOPOIESIS; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; THYMOCYTE; THYMOPOIESIS; THYMUS;

ANIMALS; CELL DIFFERENTIATION; HUMANS; INTERLEUKIN-7; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; THYMUS GLAND;

EID: 84862821294     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2012.02.002     Document Type: Review

References (106)

1. Corcoran A.E., Riddell A., Krooshoop D., Venkitaraman A.R. Impaired immunoglobulin gene rearrangement in mice lacking the IL-7 receptor. Nature 1998, 391:904-907.
2. Durum S.K., Candeias S., Nakajima H., Leonard W.J., Baird A.M., Berg L.J., et al. Interleukin 7 receptor control of T cell receptor gamma gene rearrangement: role of receptor-associated chains and locus accessibility. J Exp Med 1998, 188:2233-2241.
3. Maki K., Sunaga S., Ikuta K. The V-J recombination of T cell receptor-gamma genes is blocked in interleukin-7 receptor-deficient mice. J Exp Med 1996, 184:2423-2427.
4. Muegge K., Vila M.P., Durum S.K. Interleukin-7: a cofactor for V(D)J rearrangement of the T cell receptor beta gene. Science 1993, 261:93-95.
5. 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. J Exp Med 1994, 180:1955-1960.
6. 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. J Exp Med 1995, 181:1519-1526.
7. Fry T.J., Mackall C.L. The many faces of IL-7: from lymphopoiesis to peripheral T cell maintenance. J Immunol 2005, 174:6571-6576.
8. Radtke F., Wilson A., Stark G., Bauer M., van Meerwijk J., MacDonald H.R., et al. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 1999, 10:547-558.
9. Robey E. Regulation of T cell fate by Notch. Annu Rev Immunol 1999, 17:283-295.
10. Vicente R., Swainson L., Marty-Gres S., De Barros S.C., Kinet S., Zimmermann V.S., et al. Molecular and cellular basis of T cell lineage commitment. Semin Immunol 2010, 22:270-275.
11. Schlenner S.M., Madan V., Busch K., Tietz A., Laufle C., Costa C., et al. Fate mapping reveals separate origins of T cells and myeloid lineages in the thymus. Immunity 2010, 32:426-436.
12. - triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J Immunol 1993, 150:4244-4252.
13. Yu Q., Erman B., Park J.H., Feigenbaum L., Singer A. IL-7 receptor signals inhibit expression of transcription factors TCF-1, LEF-1, and RORgammat: impact on thymocyte development. J Exp Med 2004, 200:797-803.
14. von Freeden-Jeffry U., Solvason N., Howard M., Murray R. The earliest T lineage-committed cells depend on IL-7 for Bcl-2 expression and normal cell cycle progression. Immunity 1997, 7:147-154.
15. Akashi K., Kondo M., von Freeden-Jeffry U., Murray R., Weissman I.L. Bcl-2 rescues T lymphopoiesis in interleukin-7 receptor-deficient mice. Cell 1997, 89:1033-1041.
16. Khaled A.R., Li W.Q., Huang J., Fry T.J., Khaled A.S., Mackall C.L., et al. Bax deficiency partially corrects interleukin-7 receptor alpha deficiency. Immunity 2002, 17:561-573.
17. Maraskovsky E., O'Reilly L.A., Teepe M., Corcoran L.M., Peschon J.J., Strasser A. Bcl-2 can rescue T lymphocyte development in interleukin-7 receptor-deficient mice but not in mutant rag-1-/- mice. Cell 1997, 89:1011-1019.
18. Pellegrini M., Bouillet P., Robati M., Belz G.T., Davey G.M., Strasser A. Loss of Bim increases T cell production and function in interleukin 7 receptor-deficient mice. J Exp Med 2004, 200:1189-1195.
19. + T cells. J Exp Med 2003, 197:475-487.
20. Yu Q., Park J.H., Doan L.L., Erman B., Feigenbaum L., Singer A. Cytokine signal transduction is suppressed in preselection double-positive thymocytes and restored by positive selection. J Exp Med 2006, 203:165-175.
21. + T cells. Immunity 2000, 13:59-71.
22. Park J.H., Adoro S., Guinter T., Erman B., Alag A.S., Catalfamo M., et al. Signaling by intrathymic cytokines, not T cell antigen receptors, specifies CD8 lineage choice and promotes the differentiation of cytotoxic-lineage T cells. Nat Immunol 2010, 11:257-264.
23. 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 2008, 8:788-801.
24. + cells driven by IL-2. J Exp Med 2007, 204:1787-1801.
25. Ma A., Koka R., Burkett P. Diverse functions of IL-2, IL-15, and IL-7 in lymphoid homeostasis. Annu Rev Immunol 2006, 24:657-679.
26. Rathmell J.C., Farkash E.A., Gao W., Thompson C.B. IL-7 enhances the survival and maintains the size of naive T cells. J Immunol 2001, 167:6869-6876.
27. Vivien L., Benoist C., Mathis D. T lymphocytes need IL-7 but not IL-4 or IL-6 to survive in vivo. Int Immunol 2001, 13:763-768.
28. Anderson G., Lane P.J., Jenkinson E.J. Generating intrathymic microenvironments to establish T-cell tolerance. Nat Rev Immunol 2007, 7:954-963.
29. Kim G.Y., Hong C., Park J.H. Seeing is believing: illuminating the source of in vivo interleukin-7. Immune Netw 2011, 11:1-10.
30. Grabstein K.H., Waldschmidt T.J., Finkelman F.D., Hess B.W., Alpert A.R., Boiani N.E., et al. Inhibition of murine B and T lymphopoiesis in vivo by an anti-interleukin 7 monoclonal antibody. J Exp Med 1993, 178:257-264.
31. Bhatia S.K., Tygrett L.T., Grabstein K.H., Waldschmidt T.J. The effect of in vivo IL-7 deprivation on T cell maturation. J Exp Med 1995, 181:1399-1409.
32. Sudo T., Nishikawa S., Ohno N., Akiyama N., Tamakoshi M., Yoshida H., et al. Expression and function of the interleukin 7 receptor in murine lymphocytes. Proc Natl Acad Sci U S A 1993, 90:9125-9129.
33. Mazzucchelli R., Durum S.K. Interleukin-7 receptor expression: intelligent design. Nat Rev Immunol 2007, 7:144-154.
34. Rochman Y., Spolski R., Leonard W.J. New insights into the regulation of T cells by gamma(c) family cytokines. Nat Rev Immunol 2009, 9:480-490.
35. 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 Rev 2005, 16:513-533.
36. 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. J Exp Med 2007, 204:619-631.
37. Jiang Q., Huang J., Li W.Q., Cavinato T., Keller J.R., Durum S.K. Role of the intracellular domain of IL-7 receptor in T cell development. J Immunol 2007, 178:228-234.
38. Van De Wiele C.J., Marino J.H., Murray B.W., Vo S.S., Whetsell M.E., Teague T.K. Thymocytes between the beta-selection and positive selection checkpoints are nonresponsive to IL-7 as assessed by STAT-5 phosphorylation. J Immunol 2004, 172:4235-4244.
39. Akashi K., Kondo M., Weissman I.L. Two distinct pathways of positive selection for thymocytes. Proc Natl Acad Sci U S A 1998, 95:2486-2491.
40. 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. Nat Immunol 2004, 5:1036-1044.
41. 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.
42. Yucel R., Karsunky H., Klein-Hitpass L., Moroy T. The transcriptional repressor Gfi1 affects development of early, uncommitted c-Kit+ T cell progenitors and CD4/CD8 lineage decision in the thymus. J Exp Med 2003, 197:831-844.
43. Egawa T., Tillman R.E., Naoe Y., Taniuchi I., Littman D.R. The role of the Runx transcription factors in thymocyte differentiation and in homeostasis of naive T cells. J Exp Med 2007, 204:1945-1957.
44. 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. Nat Immunol 2009, 10:176-184.
45. 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.
46. 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. Nat Immunol 2011, 12:544-550.
47. + T cells. Nat Immunol 2009, 10:149-157.
48. 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.
49. 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. Proc Natl Acad Sci U S A 2009, 106:1512-1517.
50. 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.
51. 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. Eur J Immunol 2010, 40:2391-2400.
52. Klug D.B., Carter C., Crouch E., Roop D., Conti C.J., Richie E.R. Interdependence of cortical thymic epithelial cell differentiation and T-lineage commitment. Proc Natl Acad Sci U S A 1998, 95:11822-11827.
53. Zamisch M., Moore-Scott B., Su D.M., Lucas P.J., Manley N., Richie E.R. Ontogeny and regulation of IL-7-expressing thymic epithelial cells. J Immunol 2005, 174:60-67.
54. Takahama Y. Journey through the thymus: stromal guides for T-cell development and selection. Nat Rev Immunol 2006, 6:127-135.
55. Love P.E., Bhandoola A. Signal integration and crosstalk during thymocyte migration and emigration. Nat Rev Immunol 2011, 11:469-477.
56. Saba I., Kosan C., Vassen L., Moroy T. IL-7R-dependent survival and differentiation of early T-lineage progenitors is regulated by the BTB/POZ domain transcription factor Miz-1. Blood 2011, 117:3370-3381.
57. Laouar Y., Crispe I.N., Flavell R.A. Overexpression of IL-7R alpha provides a competitive advantage during early T-cell development. Blood 2004, 103:1985-1994.
58. Munitic I., Williams J.A., Yang Y., Dong B., Lucas P.J., El Kassar N., et al. Dynamic regulation of IL-7 receptor expression is required for normal thymopoiesis. Blood 2004, 104:4165-4172.
59. + T cell differentiation. Immunity 2003, 18:475-487.
60. Weinreich M.A., Jameson S.C., Hogquist K.A. Postselection thymocyte maturation and emigration are independent of IL-7 and ERK5. J Immunol 2010, 186:1343-1347.
61. Sarafova S.D., Van Laethem F., Adoro S., Guinter T., Sharrow S.O., Feigenbaum L., et al. Upregulation of CD4 expression during MHC class II-specific positive selection is essential for error-free lineage choice. Immunity 2009, 31:480-490.
62. Schluns K.S., Kieper W.C., Jameson S.C., Lefrancois L. Interleukin-7 mediates the homeostasis of naive and memory CD8T cells in vivo. Nat Immunol 2000, 1:426-432.
63. 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. Proc Natl Acad Sci U S A 2001, 98:8732-8737.
64. Sprent J., Surh C.D. Normal T cell homeostasis: the conversion of naive cells into memory-phenotype cells. Nat Immunol 2011, 12:478-484.
65. 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. Nat Immunol 2007, 8:1049-1059.
66. Pellegrini M., Calzascia T., Toe J.G., Preston S.P., Lin A.E., Elford A.R., et al. IL-7 engages multiple mechanisms to overcome chronic viral infection and limit organ pathology. Cell 2011, 144:601-613.
67. Cao X., Shores E.W., Hu-Li J., Anver M.R., Kelsall B.L., Russell S.M., et al. Defective lymphoid development in mice lacking expression of the common cytokine receptor gamma chain. Immunity 1995, 2:223-238.
68. Park S.Y., Saijo K., Takahashi T., Osawa M., Arase H., Hirayama N., et al. Developmental defects of lymphoid cells in Jak3 kinase-deficient mice. Immunity 1995, 3:771-782.
69. Meier D., Bornmann C., Chappaz S., Schmutz S., Otten L.A., Ceredig R., et al. Ectopic lymphoid-organ development occurs through interleukin 7-mediated enhanced survival of lymphoid-tissue-inducer cells. Immunity 2007, 26:643-654.
70. Kim K., Lee C.K., Sayers T.J., Muegge K., Durum S.K. The trophic action of IL-7 on pro-T cells: inhibition of apoptosis of pro-T1, -T2, and -T3 cells correlates with Bcl-2 and Bax levels and is independent of Fas and p53 pathways. J Immunol 1998, 160:5735-5741.
71. 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.
72. Sportes C., Hakim F.T., Memon S.A., Zhang H., Chua K.S., Brown M.R., et al. Administration of rhIL-7 in humans increases in vivo TCR repertoire diversity by preferential expansion of naive T cell subsets. J Exp Med 2008, 205:1701-1714.
73. 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. Proc Natl Acad Sci U S A 1999, 96:14476-14481.
74. Li W.Q., Guszczynski T., Hixon J.A., Durum S.K. Interleukin-7 regulates Bim proapoptotic activity in peripheral T-cell survival. Mol Cell Biol 2010, 30:590-600.
75. 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. J Biol Chem 2004, 279:29160-29166.
76. 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.
77. Masse G.X., Corcuff E., Decaluwe H., Bommhardt U., Lantz O., Buer J., et al. gamma(c) cytokines provide multiple homeostatic signals to naive CD4(+) T cells. Eur J Immunol 2007, 37:2606-2616.
78. Fisher A.G., Burdet C., Bunce C., Merkenschlager M., Ceredig R. Lymphoproliferative disorders in IL-7 transgenic mice: expansion of immature B cells which retain macrophage potential. Int Immunol 1995, 7:415-423.
79. El Kassar N., Lucas P.J., Klug D.B., Zamisch M., Merchant M., Bare C.V., et al. A dose effect of IL-7 on thymocyte development. Blood 2004, 104:1419-1427.
80. + T regulatory cells. J Immunol 2007, 178:4062-4071.
81. 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 2005, 6:1142-1151.
82. Mosmann T.R., Cherwinski H., Bond M.W., Giedlin M.A., Coffman R.L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol 1986, 136:2348-2357.
83. Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med 2007, 13:139-145.
84. Setoguchi R., Tachibana M., Naoe Y., Muroi S., Akiyama K., Tezuka C., et al. Repression of the transcription factor Th-POK by Runx complexes in cytotoxic T cell development. Science 2008, 319:822-825.
85. Crotty S. Follicular helper CD4 T cells (TFH). Annu Rev Immunol 2011, 29:621-663.
86. Malek T.R., Yu A., Zhu L., Matsutani T., Adeegbe D., Bayer A.L. IL-2 family of cytokines in T regulatory cell development and homeostasis. J Clin Immunol 2008, 28:635-639.
87. Suzuki H., Zhou Y.W., Kato M., Mak T.W., Nakashima I. Normal regulatory alpha/beta T cells effectively eliminate abnormally activated T cells lacking the interleukin 2 receptor beta in vivo. J Exp Med 1999, 190:1561-1572.
88. Schorle H., Holtschke T., Hunig T., Schimpl A., Horak I. Development and function of T cells in mice rendered interleukin-2 deficient by gene targeting. Nature 1991, 352:621-624.
89. Kuhn R., Rajewsky K., Muller W. Generation and analysis of interleukin-4 deficient mice. Science 1991, 254:707-710.
90. + B-1 cells and lack eosinophilia but have normal antibody and cytotoxic T cell responses. Immunity 1996, 4:15-24.
91. Kopf M., Baumann H., Freer G., Freudenberg M., Lamers M., Kishimoto T., et al. Impaired immune and acute-phase responses in interleukin-6-deficient mice. Nature 1994, 368:339-342.
92. Townsend J.M., Fallon G.P., Matthews J.D., Smith P., Jolin E.H., McKenzie N.A. IL-9-deficient mice establish fundamental roles for IL-9 in pulmonary mastocytosis and goblet cell hyperplasia but not T cell development. Immunity 2000, 13:573-583.
93. Kuhn R., Lohler J., Rennick D., Rajewsky K., Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993, 75:263-274.
94. Kennedy M.K., Glaccum M., Brown S.N., Butz E.A., Viney J.L., Embers M., et al. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin 15-deficient mice. J Exp Med 2000, 191:771-780.
95. Dalton D.K., Pitts-Meek S., Keshav S., Figari I.S., Bradley A., Stewart T.A. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 1993, 259:1739-1742.
96. Willerford D.M., Chen J., Ferry J.A., Davidson L., Ma A., Alt F.W. Interleukin-2 receptor alpha chain regulates the size and content of the peripheral lymphoid compartment. Immunity 1995, 3:521-530.
97. Suzuki H., Kundig T.M., Furlonger C., Wakeham A., Timms E., Matsuyama T., et al. Deregulated T-cell activation and autoimmunity in mice lacking interleukin-2 receptor-beta. Science 1995, 268:1472-1476.
98. Di Santo J.P., Muller W., Guy-Grand D., Fischer A., Rajewsky K. Lymphoid development in mice with a targeted deletion of the interleukin 2 receptor gamma chain. Proc Natl Acad Sci U S A 1995, 92:377-381.
99. Mohrs M., Ledermann B., Kohler G., Dorfmuller A., Gessner A., Brombacher F. Differences between IL-4- and IL-4 receptor alpha-deficient mice in chronic leishmaniasis reveal a protective role for IL-13 receptor signaling. J Immunol 1999, 162:7302-7308.
100. Lodolce J.P., Boone D.L., Chai S., Swain R.E., Dassopoulos T., Trettin S., et al. IL-15 receptor maintains lymphoid homeostasis by supporting lymphocyte homing and proliferation. Immunity 1998, 9:669-676.
101. Ozaki K., Spolski R., Feng C.G., Qi C.F., Cheng J., Sher A., et al. A critical role for IL-21 in regulating immunoglobulin production. Science 2002, 298:1630-1634.
102. Carpino N., Thierfelder W.E., Chang M.S., Saris C., Turner S.J., Ziegler S.F., et al. Absence of an essential role for thymic stromal lymphopoietin receptor in murine B-cell development. Mol Cell Biol 2004, 24:2584-2592.
103. Rodig S.J., Meraz M.A., White J.M., Lampe P.A., Riley J.K., Arthur C.D., et al. Disruption of the Jak1 gene demonstrates obligatory and nonredundant roles of the Jaks in cytokine-induced biologic responses. Cell 1998, 93:373-383.
104. Thomis D.C., Gurniak C.B., Tivol E., Sharpe A.H., Berg L.J. Defects in B lymphocyte maturation and T lymphocyte activation in mice lacking Jak3. Science 1995, 270:794-797.
105. Nosaka T., van Deursen J.M., Tripp R.A., Thierfelder W.E., Witthuhn B.A., McMickle A.P., et al. Defective lymphoid development in mice lacking Jak3. Science 1995, 270:800-802.
106. 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. Proc Natl Acad Sci U S A 2006, 103:1000-1005.