Id1 Attenuates Notch Signaling and Impairs T-Cell Commitment by Elevating Deltex1 Expression

REFERENCES

• Agata, Y., N. Tamaki, S. Sakamoto, T. Ikawa, K. Masuda, H. Kawamoto, and C. Murre. 2007. Regulation of T cell receptor beta gene rearrangements and allelic exclusion by the helix-loop-helix protein, E47. Immunity 27:871–884.
   PubMedGoogle Scholar
• Allman, D., J. A. Punt, D. J. Izon, J. C. Aster, and W. S. Pear. 2002. An invitation to T and more: notch signaling in lymphopoiesis. Cell 109 Suppl.:S1–S11.
   PubMedGoogle Scholar
• Allman, D., A. Sambandam, S. Kim, J. P. Miller, A. Pagan, D. Well, A. Meraz, and A. Bhandoola. 2003. Thymopoiesis independent of common lymphoid progenitors. Nat. Immunol. 4:168–174.
   PubMedGoogle Scholar
• Anderson, M. K., G. Hernandez-Hoyos, C. J. Dionne, A. M. Arias, D. Chen, and E. V. Rothenberg. 2002. Definition of regulatory network elements for T cell development by perturbation analysis with PU.1 and GATA-3. Dev. Biol. 246:103–121.
   PubMed Web of Science ®Google Scholar
• Artavanis-Tsakonas, S., K. Matsuno, and M. E. Fortini. 1995. Notch signaling. Science 268:225–232.
   PubMed Web of Science ®Google Scholar
• Bain, G., I. Engel, E. C. Robanus Maandag, H. P. te Riele, J. R. Voland, L. L. Sharp, J. Chun, B. Huey, D. Pinkel, and C. Murre. 1997. E2A deficiency leads to abnormalities in alphabeta T-cell development and to rapid development of T-cell lymphomas. Mol. Cell. Biol. 17:4782–4791.
   PubMed Web of Science ®Google Scholar
• Bain, G., M. W. Quong, R. S. Soloff, S. M. Hedrick, and C. Murre. 1999. Thymocyte maturation is regulated by the activity of the helix-loop-helix protein, E47. J. Exp. Med. 190:1605–1616.
   PubMedGoogle Scholar
• Barndt, R., M. F. Dai, and Y. Zhuang. 1999. A novel role for HEB downstream or parallel to the pre-TCR signaling pathway during alpha beta thymopoiesis. J. Immunol. 163:3331–3343.
   PubMedGoogle Scholar
• Barndt, R. J., M. Dai, and Y. Zhuang. 2000. Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant negative mutation of HEB. Mol. Cell. Biol. 20:6677–6685.
   PubMedGoogle Scholar
• Bookout, A. L., and D. J. Mangelsdorf. 2003. Quantitative real-time PCR protocol for analysis of nuclear receptor signaling pathways. Nucl. Recept. Signal. 1:e012.
   PubMedGoogle Scholar
• Choi, J. W., C. Pampeno, S. Vukmanovic, and D. Meruelo. 2002. Characterization of the transcriptional expression of Notch-1 signaling pathway members, Deltex and HES-1, in developing mouse thymocytes. Dev. Comp. Immunol. 26:575–588.
   PubMedGoogle Scholar
• Deftos, M. L., E. Huang, E. W. Ojala, K. A. Forbush, and M. J. Bevan. 2000. Notch1 signaling promotes the maturation of CD4 and CD8 SP thymocytes. Immunity 13:73–84.
   PubMed Web of Science ®Google Scholar
• Dudley, E. C., H. T. Petrie, L. M. Shah, M. J. Owen, and A. C. Hayday. 1994. T cell receptor beta chain gene rearrangement and selection during thymocyte development in adult mice. Immunity 1:83–93.
   PubMed Web of Science ®Google Scholar
• Godfrey, D. I., J. Kennedy, T. Suda, and A. Zlotnik. 1993. A developmental pathway involving four phenotypically and functionally distinct subsets of CD3-CD4-CD8- triple-negative adult mouse thymocytes defined by CD44 and CD25 expression. J. Immunol. 150:4244–4252.
   PubMed Web of Science ®Google Scholar
• Han, H., K. Tanigaki, N. Yamamoto, K. Kuroda, M. Yoshimoto, T. Nakahata, K. Ikuta, and T. Honjo. 2002. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14:637–645.
   PubMed Web of Science ®Google Scholar
• Ho, I. C., and S. Y. Pai. 2007. GATA-3—not just for Th2 cells anymore. Cell. Mol. Immunol. 4:15–29.
   PubMedGoogle Scholar
• 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 beta-chain gene rearrangement: coincident regulation of cell cycle and clonality during development in vivo. Genes Dev. 10:948–962.
   PubMedGoogle Scholar
• Hori, K., M. Fostier, M. Ito, T. J. Fuwa, M. J. Go, H. Okano, M. Baron, and K. Matsuno. 2004. Drosophila deltex mediates suppressor of Hairless-independent and late-endosomal activation of Notch signaling. Development 131:5527–5537.
   PubMed Web of Science ®Google Scholar
• Hu, X., A. Y. Chung, I. Wu, J. Foldi, J. Chen, J. D. Ji, T. Tateya, Y. J. Kang, J. Han, M. Gessler, R. Kageyama, and L. B. Ivashkiv. 2008. Integrated regulation of Toll-like receptor responses by Notch and interferon-gamma pathways. Immunity 29:691–703.
   PubMedGoogle Scholar
• Ikawa, T., H. Kawamoto, A. W. Goldrath, and C. Murre. 2006. E proteins and Notch signaling cooperate to promote T cell lineage specification and commitment. J. Exp. Med. 203:1329–1342.
   PubMedGoogle Scholar
• Izon, D. J., J. C. Aster, Y. He, A. Weng, F. G. Karnell, V. Patriub, L. Xu, S. Bakkour, C. Rodriguez, D. Allman, and W. S. Pear. 2002. Deltex1 redirects lymphoid progenitors to the B cell lineage by antagonizing Notch1. Immunity 16:231–243.
   PubMedGoogle Scholar
• Kageyama, R., and T. Ohtsuka. 1999. The Notch-Hes pathway in mammalian neural development. Cell Res. 9:179–188.
   PubMedGoogle Scholar
• Kageyama, R., T. Ohtsuka, and K. Tomita. 2000. The bHLH gene Hes1 regulates differentiation of multiple cell types. Mol. Cells 10:1–7.
   PubMed Web of Science ®Google Scholar
• Kim, D., X. C. Peng, and X. H. Sun. 1999. Massive apoptosis of thymocytes in T-cell-deficient Id1 transgenic mice. Mol. Cell. Biol. 19:8240–8253.
   PubMedGoogle Scholar
• Kim, D., M. Xu, L. Nie, X. C. Peng, E. Jimi, R. E. Voll, T. Nguyen, S. Ghosh, and X. H. Sun. 2002. Helix-loop-helix proteins regulate pre-TCR and TCR signaling through modulation of Rel/NF-kappaB activities. Immunity 16:9–21.
   PubMedGoogle Scholar
• Kisielow, P., and H. von Boehmer. 1995. Development and selection of T cells: facts and puzzles. Adv. Immunol. 58:87–209.
   PubMedGoogle Scholar
• Lazorchak, A., M. E. Jones, and Y. Zhuang. 2005. New insights into E-protein function in lymphocyte development. Trends Immunol. 26:334–338.
   PubMedGoogle Scholar
• Lehar, S. M., and M. J. Bevan. 2006. T cells develop normally in the absence of both Deltex1 and Deltex2. Mol. Cell. Biol. 26:7358–7371.
   PubMedGoogle Scholar
• Liu, W. H., and M. Z. Lai. 2005. Deltex regulates T-cell activation by targeted degradation of active MEKK1. Mol. Cell. Biol. 25:1367–1378.
   PubMedGoogle Scholar
• McDonald, H. R., A. Wilson, and F. Radtke. 2001. Notch1 and T-cell development: insights from conditional knockout mice. Trends Immunol. 22:155–160.
   PubMedGoogle Scholar
• Maillard, I., T. Fang, and W. S. Pear. 2005. Regulation of lymphoid development, differentiation, and function by the Notch pathway. Annu. Rev. Immunol. 23:945–974.
   PubMed Web of Science ®Google Scholar
• Matsuno, K., R. J. Diederich, M. J. Go, C. M. Blaumueller, and S. Artavanis-Tsakonas. 1995. Deltex acts as a positive regulator of Notch signaling through interactions with the Notch ankyrin repeats. Development 121:2633–2644.
   PubMed Web of Science ®Google Scholar
• Michie, A. M., and J. C. Zuniga-Pflucker. 2002. Regulation of thymocyte differentiation: pre-TCR signals and beta-selection. Semin. Immunol. 14:311–323.
   PubMed Web of Science ®Google Scholar
• Murre, C. 2005. Helix-loop-helix proteins and lymphocyte development. Nat. Immunol. 6:1079–1086.
   PubMed Web of Science ®Google Scholar
• Pear, W. S., J. C. Aster, M. L. Scott, R. P. Hasserjian, B. Soffer, J. Sklar, and D. Baltimore. 1996. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J. Exp. Med. 183:2283–2291.
   PubMed Web of Science ®Google Scholar
• Perry, S. S., R. S. Welner, T. Kouro, P. W. Kincade, and X. H. Sun. 2006. Primitive lymphoid progenitors in bone marrow with T lineage reconstituting potential. J. Immunol. 177:2880–2887.
   PubMedGoogle Scholar
• Porritt, H. E., L. L. Rumfelt, S. Tabrizifard, T. M. Schmitt, J. C. Zuniga-Pflucker, and H. T. Petrie. 2004. Heterogeneity among DN1 prothymocytes reveals multiple progenitors with different capacities to generate T cell and non-T cell lineages. Immunity 20:735–745.
   PubMed Web of Science ®Google Scholar
• Qi, Z., and X. H. Sun. 2004. Hyperresponse to T-cell receptor signaling and apoptosis of Id1 transgenic thymocytes. Mol. Cell. Biol. 24:7313–7323.
   PubMedGoogle Scholar
• Radtke, F., A. Wilson, G. Stark, M. Bauer, J. van Meerwijk, H. R. MacDonald, and M. Aguet. 1999. Deficient T cell fate specification in mice with an induced inactivation of Notch1. Immunity 10:547–558.
   PubMed Web of Science ®Google Scholar
• Rolink, A. G., S. Massa, G. Balciunaite, and R. Ceredig. 2007. Early lymphocyte development in bone marrow and thymus. Swiss Med. Wkly. 137(Suppl. 155):20S–24S.
   PubMedGoogle Scholar
• Rothenberg, E. V., J. E. Moore, and M. A. Yui. 2008. Launching the T-cell-lineage developmental programme. Nat. Rev. Immunol. 8:9–21.
   PubMed Web of Science ®Google Scholar
• Sambandam, A., I. Maillard, V. P. Zediak, L. Xu, R. M. Gerstein, J. C. Aster, W. S. Pear, and A. Bhandoola. 2005. Notch signaling controls the generation and differentiation of early T lineage progenitors. Nat. Immunol. 6:663–670.
   PubMed Web of Science ®Google Scholar
• Schmitt, T. M., and J. C. Zuniga-Pflucker. 2002. Induction of T cell development from hematopoietic progenitor cells by delta-like-1 in vitro. Immunity 17:749–756.
   PubMed Web of Science ®Google Scholar
• Storck, S., F. Delbos, N. Stadler, C. Thirion-Delalande, F. Bernex, C. Verthuy, P. Ferrier, J. C. Weill, and C. A. Reynaud. 2005. Normal immune system development in mice lacking the Deltex-1 RING finger domain. Mol. Cell. Biol. 25:1437–1445.
   PubMedGoogle Scholar
• Sun, X. H. 2004. Multitasking of helix-loop-helix proteins in lymphopoiesis. Adv. Immunol. 84:43–77.
   PubMedGoogle Scholar
• Taghon, T., M. A. Yui, and E. V. Rothenberg. 2007. Mast cell lineage diversion of T lineage precursors by the essential T cell transcription factor GATA-3. Nat. Immunol. 8:845–855.
   PubMed Web of Science ®Google Scholar
• Tanigaki, K., and T. Honjo. 2007. Regulation of lymphocyte development by Notch signaling. Nat. Immunol. 8:451–456.
   PubMed Web of Science ®Google Scholar
• Tomita, K., M. Hattori, E. Nakamura, S. Nakanishi, N. Minato, and R. Kageyama. 1999. The bHLH gene Hes1 is essential for expansion of early T cell precursors. Genes Dev. 13:1203–1210.
   PubMedGoogle Scholar
• Visan, I., J. B. Tan, J. S. Yuan, J. A. Harper, U. Koch, and C. J. Guidos. 2006. Regulation of T lymphopoiesis by Notch1 and Lunatic fringe-mediated competition for intrathymic niches. Nat. Immunol. 7:634–643.
   PubMedGoogle Scholar
• Weng, A. P., J. M. Millholland, Y. Yashiro-Ohtani, M. L. Arcangeli, A. Lau, C. Wai, C. Del Bianco, C. G. Rodriguez, H. Sai, J. Tobias, Y. Li, M. S. Wolfe, C. Shachaf, D. Felsher, S. C. Blacklow, W. S. Pear, and J. C. Aster. 2006. c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev. 20:2096–2109.
   PubMed Web of Science ®Google Scholar
• Wilson, A., H. R. MacDonald, and F. Radtke. 2001. Notch 1-deficient common lymphoid precursors adopt a B cell fate in the thymus. J. Exp. Med. 194:1003–1012.
   PubMed Web of Science ®Google Scholar
• Wu, L. 2006. T lineage progenitors: the earliest steps en route to T lymphocytes. Curr. Opin. Immunol. 18:121–126.
   PubMedGoogle Scholar
• Xu, W., and B. L. Kee. 2007. Growth factor independent 1B (Gfi1b) is an E2A target gene that modulates Gata3 in T-cell lymphomas. Blood 109:4406–4414.
   PubMedGoogle Scholar
• Yan, W., A. Z. Young, V. C. Soares, R. Kelley, R. Benezra, and Y. Zhuang. 1997. High incidence of T-cell tumors in E2A-null mice and E2A/Id1 double-knockout mice. Mol. Cell. Biol. 17:7317–7327.
   PubMed Web of Science ®Google Scholar
• Yang, Y., H. C. Liou, and X. H. Sun. 2006. Id1 potentiates NF-kappaB activation upon T cell receptor signaling. J. Biol. Chem. 281:34989–34996.
   PubMedGoogle Scholar
• Yun, T. J., and M. J. Bevan. 2003. Notch-regulated ankyrin-repeat protein inhibits Notch1 signaling: multiple Notch1 signaling pathways involved in T cell development. J. Immunol. 170:5834–5841.
   PubMedGoogle Scholar