Regulation of mature T cell responses by the Wnt signaling pathway

Annals of the New York Academy of Sciences

Volumn 1247, Issue 1, 2012, Pages 16-33

  Xue, Hai Hui ^a   Zhao, Dong Mei ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

LEF 1; TCF 1; Wnt signaling pathway; catenin

Indexed keywords

B LYMPHOCYTE INDUCED MATURATION PROTEIN 1; BETA CATENIN; CELL PROTEIN; DOUBLE NEGATIVE 1 PROTEIN; GAMMA INTERFERON; GLYCOGEN SYNTHASE KINASE 3BETA; GRANZYME B; IMMATURE SINGLE POSITIVE PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR BETA; INTERLEUKIN 22; INTERLEUKIN 4; INTERLEUKIN 7 RECEPTOR ALPHA; INTERLEUKIN 9; KILLER CELL LECTIN LIKE RECEPTOR G1; LYMPHOID ENHANCER FACTOR 1; MELANOCYTE PROTEIN PMEL 17; NATURAL KILLER CELL LECTIN LIKE RECEPTOR; PLAKOGLOBIN; STAT6 PROTEIN; TRANSCRIPTION FACTOR 7; TRANSCRIPTION FACTOR GATA 3; TRANSFORMING GROWTH FACTOR BETA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; WNT PROTEIN; WNT3A PROTEIN; WNT4 PROTEIN; WNT5A PROTEIN;

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; AMINO ACID SUBSTITUTION; APOPTOSIS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL EXPANSION; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELLULAR IMMUNITY; CHROMATIN STRUCTURE; CONCENTRATION (PARAMETERS); CYTOKINE PRODUCTION; CYTOKINE RESPONSE; DNA POLYMORPHISM; DOWN REGULATION; EFFECTOR CELL; EXON; HELPER CELL; HEMATOPOIETIC STEM CELL; HIGH MOBILITY GROUP BOX DOMAIN; HUMAN; IMMUNOLOGICAL MEMORY; INNATE IMMUNITY; INTRACELLULAR SIGNALING; LYMPHOCYTE DIFFERENTIATION; MACROPHAGE; MEMORY CELL; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REGULATORY T LYMPHOCYTE; REVIEW; T LYMPHOCYTE; TH17 CELL; TH9 CELL; THYMOCYTE; UPREGULATION; VACCINATION;

MAMMALIA;

EID: 84856460891     PISSN: 00778923     EISSN: 17496632     Source Type: Book Series    
DOI: 10.1111/j.1749-6632.2011.06302.x     Document Type: Review

References (127)

1. Logan, C.Y. & R. Nusse 2004. The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20: 781-810.
2. Clevers, H. 2006. Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480.
3. Khan, N.I. & L.J. Bendall 2006. Role of WNT signaling in normal and malignant hematopoiesis. Histol. Histopathol. 21: 761-774.
4. van Amerongen, R., A. Mikels & R. Nusse 2008. Alternative wnt signaling is initiated by distinct receptors. Sci. Signal. 1: re9.
5. Staal, F.J., T.C. Luis & M.M. Tiemessen 2008. WNT signalling in the immune system: WNT is spreading its wings. Nat. Rev. Immunol. 8: 581-593.
6. Arce, L., N.N. Yokoyama & M.L. Waterman 2006. Diversity of LEF/TCF action in development and disease. Oncogene 25: 7492-7504.
7. Mosimann, C, G. Hausmann & K. Basler 2009. Beta-catenin hits chromatin: regulation of Wnt target gene activation. Nat. Rev. Mol. Cell Biol. 10: 276-286.
8. Staal, F.J., M. Noort Mv, G.J. Strous & H.C. Clevers 2002. Wnt signals are transmitted through N-terminally dephosphorylated beta-catenin. EMBO Rep. 3: 63-68.
9. Van de Wetering, M., J. Castrop, V. Korinek & H. Clevers 1996. Extensive alternative splicing and dual promoter usage generate Tcf-1 protein isoforms with differential transcription control properties. Mol. Cell Biol. 16: 745-752.
10. Daniels, D.L. & W.I. Weis 2005. Beta-catenin directly displaces Groucho/TLE repressors from Tcf/Lef in Wnt-mediated transcription activation. Nat. Struct. Mol. Biol. 12: 364-371.
11. Weerkamp, F., M.R. Baert, B.A. Naber, et al 2006. Wnt signaling in the thymus is regulated by differential expression of intracellular signaling molecules. Proc. Natl. Acad. Sci. USA 103: 3322-3326.
12. Jeannet, G., M. Scheller, L. Scarpellino, et al 2008. Long-term, multilineage hematopoiesis occurs in the combined absence of beta-catenin and gamma-catenin. Blood 111: 142-149.
13. Goux, D., J.D. Coudert, D. Maurice, et al 2005. Cooperating pre-T-cell receptor and TCF-1-dependent signals ensure thymocyte survival. Blood 106: 1726-1733.
14. Ioannidis, V., F. Beermann, H. Clevers & W. Held 2001. The beta-catenin-TCF-1 pathway ensures CD4(+)CD8(+) thymocyte survival. Nat. Immunol. 2: 691-697.
15. Maier, E., D. Hebenstreit, G. Posselt, et al. 2001. Inhibition of suppressive T cell factor 1 (TCF-1) isoforms in naive CD4+ T cells is mediated by IL-4/STAT6 signaling. J. Biol. Chem. 286: 919-928.
16. Hoffmann, J.A. & J.M. Reichhart 2002. Drosophila innate immunity: an evolutionary perspective. Nat. Immunol. 3: 121-126.
17. Zettervall, C.J., I. Anderl, M.J. Williams, et al 2004. A directed screen for genes involved in Drosophila blood cell activation. Proc. Natl. Acad. Sci. USA 101: 14, 192-14, 197.
18. Yu, Q., A. Sharma & J.M. Sen 2010. TCF1 and beta-catenin regulate T cell development and function. Immunol. Res. 47: 45-55.
19. Staal, F.J. & J.M. Sen 2008. The canonical Wnt signaling pathway plays an important role in lymphopoiesis and hematopoiesis. Eur. J. Immunol. 38: 1788-1794.
20. Louis, I., K.M. Heinonen, J. Chagraoui, et al. 2008. The signaling protein Wnt4 enhances thymopoiesis and expands multipotent hematopoietic progenitors through beta-catenin-independent signaling. Immunity 29: 57-67.
21. Liang, H., A.H. Coles, Z. Zhu, et al 2007. Noncanonical Wnt signaling promotes apoptosis in thymocyte development. J. Exp. Med. 204: 3077-3084.
22. Luis, T.C., F. Weerkamp, B.A. Naber, et al 2009. Wnt3a deficiency irreversibly impairs hematopoietic stem cell self-renewal and leads to defects in progenitor cell differentiation. Blood 113: 546-554.
23. Schilham, M.W., A. Wilson, P. Moerer, et al. 1998. Critical involvement of Tcf-1 in expansion of thymocytes. J. Immunol. 161: 3984-3991.
24. Okamura, R.M., M. Sigvardsson, J. Galceran, et al. 1998. Redundant regulation of T cell differentiation and TCRalpha gene expression by the transcription factors LEF-1 and TCF-1. Immunity 8: 11-20.
25. Weber, B.N., A.W. Chi, A. Chavez, et al 2011. A critical role for TCF-1 in T-lineage specification and differentiation. Nature 476: 63-68.
26. Huelsken, J., R. Vogel, B. Erdmann, et al. 2001. beta-Catenin controls hair follicle morphogenesis and stem cell differentiation in the skin. Cell 105: 533-545.
27. Kratochwil, K., M. Dull, I. Farinas, et al. 1996. Lef1 expression is activated by BMP-4 and regulates inductive tissue interactions in tooth and hair development. Genes Dev. 10: 1382-1394.
28. Xu, Y., D. Banerjee, J. Huelsken, et al 2003. Deletion of beta-catenin impairs T cell development. Nat. Immunol. 4: 1177-1182.
29. Cobas, M., A. Wilson, B. Ernst, et al 2004. Beta-catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199: 221-229.
30. Koch, U., A. Wilson, M. Cobas, et al. 2008. Simultaneous loss of beta- and gamma-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111: 160-164.
31. Huelsken, J. & W. Held 2009. Canonical Wnt signalling plays essential roles. Eur. J. Immunol. 39: 3582-3583; author reply 3583-3584.
32. Brault, V., R. Moore, S. Kutsch, et al 2001. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128: 1253-1264.
33. Malhotra, S. & P.W. Kincade 2009. Wnt-related molecules and signaling pathway equilibrium in hematopoiesis. Cell Stem Cell. 4: 27-36.
34. Zhao, C., J. Blum, A. Chen, et al 2007. Loss of beta-catenin impairs the renewal of normal and CML stem cells in vivo. Cancer Cell. 12: 528-541.
35. Gounari, F., I. Aifantis, K. Khazaie, et al 2001. Somatic activation of beta-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat. Immunol. 2: 863-869.
36. Xie, H., Z. Huang, M.S. Sadim & Z. Sun 2005. Stabilized beta-catenin extends thymocyte survival by up-regulating Bcl-xL. J. Immunol. 175: 7981-7988.
37. Yu, Q. & J.M. Sen 2007. Beta-catenin regulates positive selection of thymocytes but not lineage commitment. J. Immunol. 178: 5028-5034.
38. Kaech, S.M. & E.J. Wherry 2007. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity 27: 393-405.
39. Harty, J.T. & V.P. Badovinac 2008. Shaping and reshaping CD8+ T-cell memory. Nat. Rev. Immunol. 8: 107-119.
40. Williams, M.A. & M.J. Bevan 2007. Effector and memory CTL differentiation. Annu. Rev. Immunol. 25: 171-192.
41. Lefrancois, L. & A.L. Marzo 2006. The descent of memory T-cell subsets. Nat. Rev. Immunol. 6: 618-623.
42. Pulendran, B. & R. Ahmed 2006. Translating innate immunity into immunological memory: implications for vaccine development. Cell 124: 849-863.
43. Bannard, O., M. Kraman & D.T. Fearon 2009. Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science 323: 505-509.
44. Ahmed, R., M.J. Bevan, S.L. Reiner & D.T. Fearon 2009. The precursors of memory: models and controversies. Nat. Rev. Immunol. 9: 662-668.
45. Sarkar, S., V. Kalia, W.N. Haining, et al. 2008. Functional and genomic profiling of effector CD8 T cell subsets with distinct memory fates. J. Exp. Med. 205: 625-640.
46. Joshi, N.S., W. Cui, A. Chandele, et al 2007. Inflammation directs memory precursor and short-lived effector CD8(+) T cell fates via the graded expression of T-bet transcription factor. Immunity 27: 281-295.
47. Haring, J.S., X. Jing, J. Bollenbacher-Reilley, et al. 2008. Constitutive expression of IL-7 receptor alpha does not support increased expansion or prevent contraction of antigen-specific CD4 or CD8 T cells following Listeria monocytogenes infection. J. Immunol. 180: 2855-2862.
48. Hand, T.W., M. Morre & S.M. Kaech 2007. Expression of IL-7 receptor alpha is necessary but not sufficient for the formation of memory CD8 T cells during viral infection. Proc. Natl. Acad. Sci. USA 104: 11730-11735.
49. Grundemann, C., S. Schwartzkopff, M. Koschella, et al 2010. The NK receptor KLRG1 is dispensable for virus-induced NK and CD8+ T-cell differentiation and function in vivo. Eur. J. Immunol. 40: 1303-1314.
50. Zhao, D.M., S. Yu, X. Zhou, et al 2010. Constitutive activation of Wnt signaling favors generation of memory CD8 T cells. J. Immunol. 184: 1191-1199.
51. Willinger, T., T. Freeman, M. Herbert, et al. 2006. Human naive CD8 T cells down-regulate expression of the WNT pathway transcription factors lymphoid enhancer binding factor 1 and transcription factor 7 (T cell factor-1) following antigen encounter in vitro and in vivo. J. Immunol. 176: 1439-1446.
52. Rutishauser, R.L., G.A. Martins, S. Kalachikov, et al 2009. Transcriptional repressor Blimp-1 promotes CD8(+) T cell terminal differentiation and represses the acquisition of central memory T cell properties. Immunity 31: 296-308.
53. Gattinoni, L., X.S. Zhong, D.C. Palmer, et al 2009. Wnt signaling arrests effector T cell differentiation and generates CD8+ memory stem cells. Nat. Med. 15: 808-813.
54. Driessens, G., Y. Zheng & T.F. Gajewski 2010. Beta-catenin does not regulate memory T cell phenotype. Nat. Med. 16: 513-514; author reply 514-515.
55. Prlic, M. & M.J. Bevan 2011. Cutting Edge: {beta}-Catenin is dispensable for T cell effector differentiation, memory formation, and recall responses. J. Immunol. 187: 1542-1546.
56. Driessens, G., Y. Zheng, F. Locke, et al. 2011. Beta-catenin inhibits T cell activation by selective interference with linker for activation of T cells-phospholipase C-gamma1 phosphorylation. J. Immunol. 186: 784-790.
57. Pashine, A., N.M. Valiante & J.B. Ulmer 2005. Targeting the innate immune response with improved vaccine adjuvants. Nat. Med. 11: S63-S68.
58. Klebanoff, C.A., N. Acquavella, Z. Yu & N.P. Restifo 2011. Therapeutic cancer vaccines: are we there yet? Immunol. Rev. 239: 27-44.
59. Banerjee, A., S.M. Gordon, A.M. Intlekofer, et al 2010. Cutting edge: the transcription factor eomesodermin enables CD8+ T cells to compete for the memory cell niche. J. Immunol. 185: 4988-4992.
60. Jeannet, G., C. Boudousquie, N. Gardiol, et al. 2010. Essential role of the Wnt pathway effector Tcf-1 for the establishment of functional CD8 T cell memory. Proc. Natl. Acad. Sci. USA 107: 9777-9782.
61. Zhou, X., S. Yu, D.M. Zhao, et al. 2010. Differentiation and persistence of memory CD8(+) T cells depend on T cell factor 1. Immunity 33: 229-240.
62. Bianchi, T., S. Gasser, A. Trumpp & H.R. MacDonald 2006. c-Myc acts downstream of IL-15 in the regulation of memory CD8 T-cell homeostasis. Blood 107: 3992-3999.
63. Nishita, M., M.K. Hashimoto, S. Ogata, et al 2000. Interaction between Wnt and TGF-beta signalling pathways during formation of Spemann's organizer. Nature 403: 781-785.
64. Labbe, E., A. Letamendia & L. Attisano 2000. Association of Smads with lymphoid enhancer binding factor 1/T cell-specific factor mediates cooperative signaling by the transforming growth factor-beta and wnt pathways. Proc. Natl. Acad. Sci. USA 97: 8358-8363.
65. Zhu, J., H. Yamane & W.E. Paul 2010. Differentiation of effector CD4 T cell populations (*). Annu. Rev. Immunol. 28: 445-489.
66. Dong C. 2008. TH17 cells in development: an updated view of their molecular identity and genetic programming. Nat. Rev. Immunol. 8: 337-348.
67. Josefowicz, S.Z. & A. Rudensky 2009. Control of regulatory T cell lineage commitment and maintenance. Immunity 30: 616-625.
68. Veldhoen, M., C. Uyttenhove, J. van Snick, et al 2008. Transforming growth factor-beta 'reprograms' the differentiation of T helper 2 cells and promotes an interleukin 9-producing subset. Nat. Immunol. 9: 1341-1346.
69. King, C., S.G. Tangye & C.R. Mackay 2008. T follicular helper (TFH) cells in normal and dysregulated immune responses. Annu. Rev. Immunol. 26: 741-766.
70. Zheng, W. & R.A. Flavell 1997. The transcription factor GATA-3 is necessary and sufficient for Th2 cytokine gene expression in CD4 T cells. Cell 89: 587-596.
71. Zhu, J., B. Min, J. Hu-Li, et al 2004. Conditional deletion of Gata3 shows its essential function in T(H)1-T(H)2 responses. Nat. Immunol. 5: 1157-1165.
72. Yamane, H., J. Zhu & W.E. Paul 2005. Independent roles for IL-2 and GATA-3 in stimulating naive CD4+ T cells to generate a Th2-inducing cytokine environment. J. Exp. Med. 202: 793-804.
73. Amsen, D., A. Antov, D. Jankovic, et al 2007. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 27: 89-99.
74. Fang, T.C., Y. Yashiro-Ohtani, C. Del Bianco, et al 2007. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27: 100-110.
75. Yu, Q., A. Sharma, S.Y. Oh, et al 2009. T cell factor 1 initiates the T helper type 2 fate by inducing the transcription factor GATA-3 and repressing interferon-gamma. Nat. Immunol. 10: 992-999.
76. Notani, D., K.P. Gottimukkala, R.S. Jayani, et al 2008. Global regulator SATB1 recruits beta-catenin and regulates T(H)2 differentiation in Wnt-dependent manner. PLoS Biol. 8: e1000296.
77. Galande, S., P.K. Purbey, D. Notani & P.P. Kumar 2007. The third dimension of gene regulation: organization of dynamic chromatin loopscape by SATB1. Curr. Opin. Genet. Dev. 17: 408-414.
78. Cai, S., C.C. Lee & T. Kohwi-Shigematsu 2006. SATB1 packages densely looped, transcriptionally active chromatin for coordinated expression of cytokine genes. Nat. Genet. 38: 1278-1288.
79. Hebenstreit, D., M. Giaisi, M.K. Treiber, et al 2008. LEF-1 negatively controls interleukin-4 expression through a proximal promoter regulatory element. J. Biol. Chem. 283: 22, 490-22, 497.
80. Hossain, M.B., H. Hosokawa, A. Hasegawa, et al 2008. Lymphoid enhancer factor interacts with GATA-3 and controls its function in T helper type 2 cells. Immunology 125: 377-386.
81. Yu, Q., A. Sharma, A. Ghosh & J.M. Sen 2011. T cell factor-1 negatively regulates expression of IL-17 family of cytokines and protects mice from experimental autoimmune encephalomyelitis. J. Immunol. 186: 3946-3952.
82. Oestreich, K.J., A.C. Huang & A.S. Weinmann 2011. The lineage-defining factors T-bet and Bcl-6 collaborate to regulate Th1 gene expression patterns. J. Exp. Med. 208: 1001-1013.
83. Erlich, H.A., A.M. Valdes, C. Julier, et al. 2009. Evidence for association of the TCF7 locus with type I diabetes. Genes Immun. 10(Suppl 1): S54-S59.
84. Barth, A.I., D.B. Stewart & W.J. Nelson 1999. T cell factor-activated transcription is not sufficient to induce anchorage-independent growth of epithelial cells expressing mutant beta-catenin. Proc. Natl. Acad. Sci. USA 96: 4947-4952.
85. Ding, Y., S. Shen, A.C. Lino, et al. 2008. Beta-catenin stabilization extends regulatory T cell survival and induces anergy in nonregulatory T cells. Nat. Med. 14: 162-169.
86. Graham, J.A., M. Fray, S. de Haseth, et al 2010. Suppressive regulatory T cell activity is potentiated by glycogen synthase kinase 3{beta} inhibition. J. Biol. Chem. 285: 32852-32859.
87. Gordon, M.D., M.S. Dionne, D.S. Schneider & R. Nusse 2005. WntD is a feedback inhibitor of Dorsal/NF-kappaB in Drosophila development and immunity. Nature 437: 746-749.
88. Chaussabel, D., R.T. Semnani, M.A. McDowell, et al 2003. Unique gene expression profiles of human macrophages and dendritic cells to phylogenetically distinct parasites. Blood 102: 672-681.
89. Lehtonen, A., H. Ahlfors, V. Veckman, et al. 2007. Gene expression profiling during differentiation of human monocytes to macrophages or dendritic cells. J. Leukoc. Biol. 82: 710-720.
90. Blumenthal, A., S. Ehlers, J. Lauber, et al 2006. The Wingless homolog WNT5A and its receptor Frizzled-5 regulate inflammatory responses of human mononuclear cells induced by microbial stimulation. Blood 108: 965-973.
91. He, X., J.P. Saint-Jeannet, Y. Wang, et al. 1997. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275: 1652-1654.
92. Lobov, I.B., S. Rao, T.J. Carroll, et al 2005. WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437: 417-421.
93. Manicassamy, S., B. Reizis, R. Ravindran, et al 2010. Activation of beta-catenin in dendritic cells regulates immunity versus tolerance in the intestine. Science 329: 849-853.
94. Wu, B., S.P. Crampton & C.C. Hughes 2007. Wnt signaling induces matrix metalloproteinase expression and regulates T cell transmigration. Immunity 26: 227-239.
95. Tamura, M., M.M. Sato & M. Nashimoto 2011. Regulation of CXCL12 expression by canonical Wnt signaling in bone marrow stromal cells. Int. J. Biochem. Cell Biol. 43: 760-767.
96. Ghosh, M.C., G.D. Collins, B. Vandanmagsar, et al 2009. Activation of Wnt5A signaling is required for CXC chemokine ligand 12-mediated T-cell migration. Blood 114: 1366-1373.
97. Jiang, A., O. Bloom, S. Ono, et al 2007. Disruption of E-cadherin-mediated adhesion induces a functionally distinct pathway of dendritic cell maturation. Immunity 27: 610-624.
98. Zhou, J., P. Cheng, J.I. Youn, et al. 2009. Notch and wingless signaling cooperate in regulation of dendritic cell differentiation. Immunity 30: 845-859.
99. Otero, K., I.R. Turnbull, P.L. Poliani, et al 2009. Macrophage colony-stimulating factor induces the proliferation and survival of macrophages via a pathway involving DAP12 and beta-catenin. Nat. Immunol. 10: 734-743.
100. Yang, P., H. An, X. Liu, et al 2010. The cytosolic nucleic acid sensor LRRFIP1 mediates the production of type I interferon via a beta-catenin-dependent pathway. Nat. Immunol. 11: 487-494.
101. Neumann, J., K. Schaale, K. Farhat, et al 2010. Frizzled1 is a marker of inflammatory macrophages, and its ligand Wnt3a is involved in reprogramming Mycobacterium tuberculosis-infected macrophages. FASEB J. 24: 4599-4612.
102. Pereira, C., D.J. Schaer, E.B. Bachli, et al 2008. Wnt5A/CaMKII signaling contributes to the inflammatory response of macrophages and is a target for the antiinflammatory action of activated protein C and interleukin-10. Arterioscler. Thromb. Vasc. Biol. 28: 504-510.
103. Schaale, K., J. Neumann, D. Schneider, et al 2011. Wnt signaling in macrophages: augmenting and inhibiting mycobacteria-induced inflammatory responses. Eur. J. Cell Biol. 90: 553-559.
104. Sen, M. & G. Ghosh 2008. Transcriptional outcome of Wnt-Frizzled signal transduction in inflammation: evolving concepts. J. Immunol. 181: 4441-4445.
105. Pereira, C.P., E.B. Bachli G. Schoedon 2009. The wnt pathway: a macrophage effector molecule that triggers inflammation. Curr. Atheroscler. Rep. 11: 236-242.
106. Xu, M., A. Sharma, D.L. Wiest & J.M. Sen 2009. Pre-TCR-induced beta-catenin facilitates traversal through beta-selection. J. Immunol. 182: 751-758.
107. Kovalovsky, D., Y. Yu, M. Dose, et al 2009. Beta-catenin/Tcf determines the outcome of thymic selection in response to alphabetaTCR signaling. J. Immunol. 183: 3873-3884.
108. Lovatt, M. & M.J. Bijlmakers 2010. Stabilisation of beta-catenin downstream of T cell receptor signalling. PLoS One. 5.
109. Diehn, M., A.A. Alizadeh, O.J. Rando, et al 2002. Genomic expression programs and the integration of the CD28 costimulatory signal in T cell activation. Proc. Natl. Acad. Sci. USA 99: 11796-11801.
110. Cross, D.A., D.R. Alessi, P. Cohen, et al 1995. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378: 785-789.
111. He, X.C., T. Yin, J.C. Grindley, et al 2007. PTEN-deficient intestinal stem cells initiate intestinal polyposis. Nat. Genet. 39: 189-198.
112. Thornton, T.M., G. Pedraza-Alva, B. Deng, et al 2008. Phosphorylation by p38 MAPK as an alternative pathway for GSK3beta inactivation. Science 320: 667-670.
113. Wu, X., X. Tu, K.S. Joeng, et al 2008. Rac1 activation controls nuclear localization of beta-catenin during canonical Wnt signaling. Cell 133: 340-353.
114. Gwak, J., M. Cho, S.J. Gong, et al 2006. Protein-kinase-C-mediated beta-catenin phosphorylation negatively regulates the Wnt/beta-catenin pathway. J. Cell Sci. 119: 4702-4709.
115. van Buul, J.D., E.C. Anthony, M. Fernandez-Borja, et al 2005. Proline-rich tyrosine kinase 2 (Pyk2) mediates vascular endothelial-cadherin-based cell-cell adhesion by regulating beta-catenin tyrosine phosphorylation. J. Biol. Chem. 280: 21129-21136.
116. Voskas, D., L.S. Ling & J.R. Woodgett 2010. Does GSK-3 provide a shortcut for PI3K activation of Wnt signalling? F1000 Biol Rep. 2: 82.
117. Li, M.O. & R.A. Flavell 2008. TGF-beta: a master of all T cell trades. Cell 134: 392-404.
118. Guo, X. & X.F. Wang 2009. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res. 19: 71-88.
119. Hinrichs, C.S., R. Spolski, C.M. Paulos, et al 2008. IL-2 and IL-21 confer opposing differentiation programs to CD8+ T cells for adoptive immunotherapy. Blood 111: 5326-5333.
120. Paley, M.A. & E.J. Wherry 2010. TCF-1 flips the switch on Eomes. Immunity 33: 145-147.
121. Koehn, B.H. & S.P. Schoenberger 2009. Tumor immunotherapy: making an immortal army. Nat. Med. 15: 731-732.
122. Gattinoni, L., Y. Ji, N.P. Restifo 2010. Wnt/beta-catenin signaling in T-cell immunity and cancer immunotherapy. Clin. Cancer Res. 16: 4695-4701.
123. Bluestone, J.A. & M. Hebrok 2008. Safer, longer-lasting regulatory T cells with beta-catenin. Nat. Med. 14: 118-119.
124. Martinez A. 2008. Preclinical efficacy on GSK-3 inhibitors: towards a future generation of powerful drugs. Med. Res. Rev. 28: 773-796.
125. De Sarno, P, R.C. Axtell, C. Raman, et al 2008. Lithium prevents and ameliorates experimental autoimmune encephalomyelitis. J. Immunol. 181: 338-345.
126. Bottomly, D., S.L. Kyler, S.K. McWeeney & G.S. Yochum 2010. Identification of {beta}-catenin binding regions in colon cancer cells using ChIP-Seq. Nucl. Acids Res. 38: 5735-5745.
127. Hatzis, P., L.G. van der Flier, M.A. van Driel, et al 2008. Genome-wide pattern of TCF7L2/TCF4 chromatin occupancy in colorectal cancer cells. Mol. Cell Biol. 28: 2732-2744.