Sustained expression of pre-TCR induced β-catenin in post-β-selection thymocytes blocks T cell development

Journal of Immunology

Volumn 182, Issue 2, 2009, Pages 759-765

  Xu, Mai ^a   Sharma, Archna ^a   Hossain, M Zulfiquer ^a   Wiest, David L ^b   Sen, Jyoti Misra ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b FOX CHASE CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; EARLY GROWTH RESPONSE FACTOR; INTERLEUKIN 7 RECEPTOR; RAR RELATED ORPHAN RECEPTOR GAMMA; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; CATNB PROTEIN, MOUSE; GROWTH INHIBITOR; LYMPHOCYTE ANTIGEN RECEPTOR; PROTEIN PRECURSOR;

ANIMAL EXPERIMENT; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; DOWN REGULATION; EGR GENE; GENE; GENE EXPRESSION; MOLECULAR BIOLOGY; MOLECULAR RECOGNITION; MOUSE; NONHUMAN; PRE T LYMPHOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE; THYMOCYTE; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CELL CYCLE; CELL DIFFERENTIATION; CYTOLOGY; DRUG ANTAGONISM; GENE REARRANGEMENT; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; THYMUS; TIME; TRANSGENIC MOUSE;

ANIMALS; BETA CATENIN; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CELL CYCLE; CELL DIFFERENTIATION; DOWN-REGULATION; GENE REARRANGEMENT, BETA-CHAIN T-CELL ANTIGEN RECEPTOR; GROWTH INHIBITORS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PROTEIN PRECURSORS; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; T-LYMPHOCYTE SUBSETS; THYMUS GLAND; TIME FACTORS;

EID: 60549088959     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.182.2.759     Document Type: Article

References (49)

1. Sen, J., Y. Shinkai, F. W. Alt, R. Sen, and S. J. Burakoff. 1994. Nuclear factors that mediate intrathymic signals are developmentally regulated. J. Exp. Med. 180: 2321-2327.
2. Sen, J., L. Venkataraman, Y. Shinkai, J. W. Pierce, F. W. Alt, S. J. Burakoff, and R. Sen. 1995. Expression and induction of nuclear factor-κ B-related proteins in thymocytes. J. Immunol. 154: 3213-3221.
3. Aifantis, I., M. Mandal, K. Sawai, A. Ferrando, and T. Vilimas. 2006. Regulation of T-cell progenitor survival and cell-cycle entry by the pre-T-cell receptor. Immunol. Rev. 209: 159-169.
4. Ciofani, M., and J. C. Zuniga-Pflucker. 2006. A survival guide to early T cell development. Immunol. Res. 34: 117-132.
5. von Boehmer, H. 2005. Unique features of the pre-T-cell receptor α-chain: not just a surrogate. Nat. Rev. Immunol. 5: 571-577.
6. Hoffman, E. S., L. Passoni, T. Crompton, T. M. Leu, D. G. Schatz, A. Koff, M. J. Owen, and A. C. Hayday. 1996. Productive T-cell receptor β-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10: 948-962.
7. Jiang, H., F. C. Chang, A. E. Ross, J. Lee, K. Nakayama, K. Nakayama, and S. Desiderio. 2005. Ubiquitylation of RAG-2 by Skp2-SCF links destruction of the V(D)J recombinase to the cell cycle. Mol. Cell. 18: 699-709.
8. Jiang, H., A. E. Ross, and S. Desiderio. 2004. Cell cycle-dependent accumulation in vivo of transposition-competent complexes between recombination signal ends and full-length RAG proteins. J. Biol. Chem. 279: 8478-8486.
9. Janeway, C. A., Jr. 1999. T-cell development: a role for self-peptides in positive selection. Curr. Biol. 9: R342-R345.
10. Saito, T., and N. Watanabe. 1998. Positive and negative thymocyte selection. Crit. Rev. Immunol. 18: 359-370.
11. Fowlkes, B. J., and E. Schweighoffer. 1995. Positive selection of T cells. Curr. Opin. Immunol. 7: 188-195.
12. Jameson, S. C., K. A. Hogquist, and M. J. Bevan. 1995. Positive selection of thymocytes. Annu. Rev. Immunol. 13: 93-126.
13. + stage. J. Immunol. 168: 1649-1658.
14. +. J. Immunol. 172: 964-971.
15. Carter, J. H., J. M. Lefebvre, D. L. Wiest, and W. G. Tourtellotte. 2007. Redundant role for early growth response transcriptional regulators in thymocyte differentiation and survival. J. Immunol. 178: 6796-6805.
16. Eberl, G., S. Marmon, M. J. Sunshine, P. D. Rennert, Y. Choi, and D. R. Littman. 2004. An essential function for the nuclear receptor RORγ(t) in the generation of fetal lymphoid tissue inducer cells. Nat. Immunol. 5: 64-73.
17. He, Y. W., C. Beers, M. L. Deftos, E. W. Ojala, K. A. Forbush, and M. J. Bevan. 2000. Down-regulation of the orphan nuclear receptor ROR γ t is essential for T lymphocyte maturation. J. Immunol. 164: 5668-5674.
18. He, Y. W., M. L. Deftos, E. W. Ojala, and M. J. Bevan. 1998. RORγ t, a novel isoform of an orphan receptor, negatively regulates Fas ligand expression and IL-2 production in T cells. Immunity 9: 797-806.
19. Xi, H., R. Schwartz, I. Engel, C. Murre, and G. J. Kersh. 2006. Interplay between RORγt, Egr3, and E proteins controls proliferation in response to pre-TCR signals. Immunity 24: 813-826.
20. Di Santo, J. P., I. Aifantis, E. Rosmaraki, C. Garcia, J. Feinberg, H. J. Fehling, A. Fischer, H. von Boehmer, and B. Rocha. 1999. The common cytokine receptor γ chain and the pre-T cell receptor provide independent but critically overlapping signals in early α/β T cell development. J. Exp. Med. 189: 563-574.
21. Trop, S., P. De Sepulveda, J. C. Zuniga-Pflucker, and R. Rottapel. 2001. Over-expression of suppressor of cytokine signaling-1 impairs pre-T-cell receptor-induced proliferation but not differentiation of immature thymocytes. Blood 97: 2269-2277.
22. Yasuda, Y., A. Kaneko, I. Nishijima, S. Miyatake, and K. Arai. 2002. Interleukin-7 inhibits pre-T-cell differentiation induced by the pre-T-cell receptor signal and the effect is mimicked by hGM-CSF in hGM-CSF receptor transgenic mice. Immunology 106: 212-221.
23. Yu, Q., B. Erman, J. H. Park, L. Feigenbaum, and A. Singer. 2004. IL-7 receptor signals inhibit expression of transcription factors TCF-1, LEF-1, and RORγt: impact on thymocyte development. J. Exp. Med. 200: 797-803.
24. Mulroy, T., J. A. McMahon, S. J. Burakoff, A. P. McMahon, and J. Sen. 2002. Wnt-1 and Wnt-4 regulate thymic cellularity. Eur. J. Immunol. 32: 967-971.
25. Xu, Y., D. Banerjee, J. Huelsken, W. Birchmeier, and J. M. Sen. 2003. Deletion of β-catenin impairs T cell development. Nat. Immunol. 4: 1177-1182.
26. Verbeek, S., D. Izon, F. Hofhuis, E. Robanus-Maandag, H. te Riele, M. van de Wetering, M. Oosterwegel, A. Wilson, H. R. MacDonald, and H. Clevers. 1995. An HMG-box-containing T-cell factor required for thymocyte differentiation. Nature 374: 70-74.
27. Okamura, R. M., M. Sigvardsson, J. Galceran, S. Verbeek, H. Clevers, and R. Grosschedl. 1998. Redundant regulation of T cell differentiation and TCRα gene expression by the transcription factors LEF-1 and TCF-1. Immunity 8: 11-20.
28. Schilham, M. W., A. Wilson, P. Moerer, B. J. Benaissa-Trouw, A. Cumano, and H. C. Clevers. 1998. Critical involvement of Tcf-1 in expansion of thymocytes. J. Immunol. 161: 3984-3991.
29. Gounari, F., I. Aifantis, K. Khazaie, S. Hoeflinger, N. Harada, M. M. Taketo, and H. von Boehmer. 2001. Somatic activation of β-catenin bypasses pre-TCR signaling and TCR selection in thymocyte development. Nat. Immunol. 2: 863-869.
30. Staal, F. J., J. Meeldijk, P. Moerer, P. Jay, B. C. van de Weerdt, S. Vainio, G. P. Nolan, and H. Clevers. 2001. Wnt signaling is required for thymocyte development and activates Tcf-1 mediated transcription. Eur. J. Immunol. 31: 285-293.
31. Pongracz, J. E., S. M. Parnell, T. Jones, G. Anderson, and E. J. Jenkinson. 2006. Overexpression of ICAT highlights a role for catenin-mediated canonical Wnt signaling in early T cell development. Eur. J. Immunol. 36: 2376-2383.
32. Hossain, M. Z., Q. Yu, M. Xu, and J. M. Sen. 2008. ICAT expression disrupts β-catenin-TCF interactions and impairs survival of thymocytes and activated mature T cells. Int. Immunol.
33. Cobas, M., A. Wilson, B. Ernst, S. J. Mancini, H. R. MacDonald, R. Kemler, and F. Radtke. 2004. β-catenin is dispensable for hematopoiesis and lymphopoiesis. J. Exp. Med. 199: 221-229.
34. Koch, U., A. Wilson, M. Cobas, R. Kemler, H. R. Macdonald, and F. Radtke. 2007. Simultaneous loss of β- and γ-catenin does not perturb hematopoiesis or lymphopoiesis. Blood 111: 160-164.
35. Jeannet, G., M. Scheller, L. Scarpellino, S. Duboux, N. Gardiol, J. Back, F. Kuttler, I. Malanchi, W. Birchmeier, A. Leutz, et al. 2007. Long-term, multilineage hematopoiesis occurs in the combined absence of β-catenin and γ-catenin. Blood 111: 142-149.
36. Goux, D., J. D. Coudert, D. Maurice, L. Scarpellino, G. Jeannet, S. Piccolo, K. Weston, J. Huelsken, and W. Held. 2005. Cooperating pre-T-cell receptor and TCF-1-dependent signals ensure thymocyte survival. Blood 106: 1726-1733.
37. Fukushima, T., J. M. Zapata, N. C. Singha, M. Thomas, C. L. Kress, M. Krajewska, S. Krajewski, Z. Ronai, J. C. Reed, and S. Matsuzawa. 2006. Critical function for SIP, a ubiquitin E3 ligase component of the β-catenin degradation pathway, for thymocyte development and G1 checkpoint. Immunity 24: 29-39.
38. Mulroy, T., Y. Xu, and J. M. Sen. 2003. β-Catenin expression enhances generation of mature thymocytes. Int. Immunol. 15: 1485-1494.
39. Xu, Y., and J. Sen. 2003. β-catenin expression in thymocytes accelerates thymic involution. Eur. J. Immunol. 33: 12-18.
40. Zhumabekov, T., P. Corbella, M. Tolaini, and D. Kioussis. 1995. Improved version of a human CD2 minigene based vector for T cell-specific expression in transgenic mice. J. Immunol. Methods 185: 133-140.
41. Cleverley, S., S. Henning, and D. Cantrell. 1999. Inhibition of Rho at different stages of thymocyte development gives different perspectives on Rho function. Curr. Biol. 9: 657-660.
42. Yu, Q., and J. M. Sen. 2007. β-catenin regulates positive selection of thymocytes but not lineage commitment. J. Immunol. 178: 5028-5034.
43. -/- mice in the absence of TCR β chain expression. Int. Immunol. 6: 995-1001.
44. Xu, M., Q. Yu, R. Subrahmanyam, M. J. Difilippantonio, T. Ried, and J. M. Sen. 2008. β-catenin expression results in p53-independent DNA damage and oncogene-induced senescence in prelymphomagenic thymocytes in vivo. Mol. Cell. Biol. 28: 1713-1723.
45. Gounari, F., R. Chang, J. Cowan, Z. Guo, M. Dose, E. Gounaris, and K. Khazaie. 2005. Loss of adenomatous polyposis coli gene function disrupts thymic development. Nat. Immunol. 6: 800-809.
46. Trigueros, C., K. Hozumi, B. Silva-Santos, L. Bruno, A. C. Hayday, M. J. Owen, and D. J. Pennington. 2003. Pre-TCR signaling regulates IL-7 receptor α expression promoting thymocyte survival at the transition from the double-negative to double-positive stage. Eur. J. Immunol. 33: 1968-1977.
47. Takahama, Y., J. J. Letterio, H. Suzuki, A. G. Farr, and A. Singer. 1994. Early progression of thymocytes along the CD4/CD8 developmental pathway is regulated by a subset of thymic epithelial cells expressing transforming growth factor β. J. Exp. Med. 179: 1495-1506.
48. Weerkamp, F., M. R. Baert, B. A. Naber, E. E. Koster, E. F. de Haas, K. R. Atkuri, J. J. van Dongen, L. A. Herzenberg, and F. J. Staal. 2006. Wnt signaling in the thymus is regulated by differential expression of intracellular signaling molecules. Proc. Natl. Acad. Sci. USA 103: 3322-3326
49. Xu, M., A. Sharma, D. L. Wiest, and J. M. Sen. 2008. Pre-TCR-induced β-catenin facilitates traversal through β-selectin. J. Immunol. 182: 751-758.