Ikaros regulates Notch target gene expression in developing thymocytes

Journal of Immunology

Volumn 181, Issue 9, 2008, Pages 6265-6274

  Chari, Sheila ^a   Winandy, Susan ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

IKAROS TRANSCRIPTION FACTOR; NOTCH RECEPTOR; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR DELTEX1; TRANSCRIPTION FACTOR GATA 3; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR PTA; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; DNA BINDING PROTEIN; DTX1 PROTEIN, MOUSE; GATA3 PROTEIN, MOUSE; HES1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; LIGAND; LYMPHOCYTE ANTIGEN RECEPTOR; MEMBRANE PROTEIN; PRE T CELL RECEPTOR ALPHA; PRE-T CELL RECEPTOR ALPHA; RUNX1 PROTEIN, MOUSE; ZFPN1A1 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW; CELL DIFFERENTIATION; CELL MATURATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEREGULATION; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN FUNCTION; RECEPTOR DOWN REGULATION; REGULATORY MECHANISM; T CELL LEUKEMIA; T LYMPHOCYTE; THYMOCYTE; ANIMAL; BIOSYNTHESIS; COCULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; PATHOLOGY; PHYSIOLOGY; T LYMPHOCYTE SUBPOPULATION; TUMOR CELL LINE;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINE, TUMOR; COCULTURE TECHNIQUES; CORE BINDING FACTOR ALPHA 2 SUBUNIT; DNA-BINDING PROTEINS; GATA3 TRANSCRIPTION FACTOR; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; IKAROS TRANSCRIPTION FACTOR; LEUKEMIA, T-CELL; LIGANDS; MEMBRANE GLYCOPROTEINS; MICE; RECEPTORS, ANTIGEN, T-CELL, ALPHA-BETA; RECEPTORS, NOTCH; T-LYMPHOCYTE SUBSETS;

EID: 58749096380     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.181.9.6265     Document Type: Article

References (62)

1. Georgopoulos, K., S. Winandy, and N. Avitahl. 1997. The role of the Ikaros gene in lymphocyte development and homeostasis. Annu. Rev. Immunol. 15: 155-176. (Pubitemid 27169278)
2. Winandy, S., P. Wu, and K. Georgopoulos. 1995. A dominant mutation in the Ikaros gene leads to rapid development of leukemia and lymphoma. Cell 83: 289-299.
3. Wang, J. H., A. Nichogiannopoulou, L. Wu, L. Sun, A. H. Sharpe, M. Bigby, and K. Georgopoulos. 1996. Selective defects in the development of the fetal and adult lymphoid system in mice with an Ikaros null mutation. Immunity 5: 537-549.
4. Kathrein, K. L., R. Lorenz, A. M. Innes, E. Griffiths, and S. Winandy. 2005. Ikaros induces quiescence and T-cell differentiation in a leukemia cell line. Mol. Cell. Biol. 25: 1645-1654. (Pubitemid 40280134)
5. Dumortier, A., R. Jeannet, P. Kirstetter, E. Kleinmann, M. Sellars, N. R. dos Santos, C. Thibault, J. Barths, J. Ghysdael, et al. 2006. Notch activation is an early and critical event during T-Cell leukemogenesis in Ikaros-deficient mice. Mol. Cell. Biol. 26: 209-220.
6. Beverly, L. J., and A. J. Capobianco. 2003. Perturbation of Ikaros isoform selection by MLV integration is a cooperative event in Notch(IC)-induced T cell leukemogenesis. Cancer Cell 3: 551-564.
7. Beverly, L. J., and A. J. Capobianco. 2004. Targeting promiscuous signaling pathways in cancer: another Notch in the bedpost. Trends Mol. Med. 10: 591-598.
8. Lopez-Nieva, P., J. Santos, and J. Fernandez-Piqueras. 2004. Defective expression of Notch1 and Notch2 in connection to alterations of c-Myc and Ikaros in γ-radiation-induced mouse thymic lymphomas. Carcinogenesis 25: 1299-1304. (Pubitemid 38968058)
9. Pui, J. C., D. Allman, L. Xu, S. DeRocco, F. G. Karnell, S. Bakkour, J. Y. Lee, T. Kadesch, R. R. Hardy, J. C. Aster, and W. S. Pear. 1999. Notch1 expression in early lymphopoiesis influences B versus T lineage determination. Immunity 11: 299-308.
10. 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. (Pubitemid 29262657)
11. Wu, L., J. C. Aster, S. C. Blacklow, R. Lake, S. Artavanis-Tsakonas, and J. D. Griffin. 2000. MAML1, a human homologue of Drosophila mastermind, is a transcriptional co-activator for NOTCH receptors. Nat. Genet. 26: 484-489.
12. Kathrein, K. L., S. Chari, and S. Winandy. 2008. Ikaros directly represses the Notch target gene Hes1 in a leukemia T cell line: implications for CD4 regulation. J. Biol. Chem. 283: 10476-10484.
13. Baron, M. 2003. An overview of the Notch signalling pathway. Semin. Cell Dev. Biol. 14: 113-119.
14. Felli, M. P., M. Maroder, T. A. Mitsiadis, A. F. Campese, D. Bellavia, A. Vacca, R. S. Mann, L. Frati, U. Lendahl, A. Gulino, and I. Screpanti. 1999. Expression pattern of notch1, 2 and 3 and Jagged1 and 2 in lymphoid and stromal thymus components: distinct ligand-receptor interactions in intrathymic T cell development. Int. Immunol. 11: 1017-1025.
15. Kitamoto, T., K. Takahashi, H. Takimoto, K. Tomizuka, M. Hayasaka, T. Tabira, and K. Hanaoka. 2005. Functional redundancy of the Notch gene family during mouse embryogenesis: analysis of Notch gene expression in Notch3-deficient mice. Biochem. Biophys. Res. Commun. 331: 1154-1162. (Pubitemid 40692479)
16. Saito, T., S. Chiba, M. Ichikawa, A. Kunisato, T. Asai, K. Shimizu, T. Yamaguchi, G. Yamamoto, S. Seo, K. Kumano, et al. 2003. Notch2 is preferentially expressed in mature B cells and indispensable for marginal zone B lineage development. Immunity 18: 675-685. (Pubitemid 36588584)
17. Bellavia, D., M. Mecarozzi, A. F. Campese, P. Grazioli, C. Talora, L. Frati, A. Gulino, and I. Screpanti. 2007. Notch3 and the Notch3-upregulated RNA-binding protein HuD regulate Ikaros alternative splicing. EMBO J. 26: 1670-1680. (Pubitemid 46480945)
18. Deftos, M. L., Y. W. He, E. W. Ojala, and M. J. Bevan. 1998. Correlating notch signaling with thymocyte maturation. Immunity 9: 777-786.
19. Molnar, A., P. Wu, D. A. Largespada, A. Vortkamp, S. Scherer, N. G. Copeland, N. A. Jenkins, G. Bruns, and K. Georgopoulos. 1996. The Ikaros gene encodes a family of lymphocyte-restricted zinc finger DNA binding proteins, highly conserved in human and mouse. J. Immunol. 156: 585-592. (Pubitemid 26028917)
20. 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.
21. Hasserjian, R. P., J. C. Aster, F. Davi, D. S. Weinberg, and J. Sklar. 1996. Modulated expression of notch1 during thymocyte development. Blood 88: 970-976.
22. Aster, J. C., and W. S. Pear. 2001. Notch signaling in leukemia. Curr. Opin. Hematol. 8: 237-244.
23. Fryer, C. J., E. Lamar, I. Turbachova, C. Kintner, and K. A. Jones. 2002. Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev. 16: 1397-1411.
24. Oswald, F., U. Kostezka, K. Astrahantseff, S. Bourteele, K. Dillinger, U. Zechner, L. Ludwig, M. Wilda, H. Hameister, W. Knochel, et al. 2002. SHARP is a novel component of the Notch/RBP-Jκ signalling pathway. EMBO J. 21: 5417-5426. (Pubitemid 35231021)
25. Kao, H. Y., P. Ordentlich, N. Koyano-Nakagawa, Z. Tang, M. Downes, C. R. Kintner, R. M. Evans, and T. Kadesch. 1998. A histone deacetylase corepressor complex regulates the Notch signal transduction pathway. Genes Dev. 12: 2269-2277.
26. Hsieh, J. J., S. Zhou, L. Chen, D. B. Young, and S. D. Hayward. 1999. CIR, a corepressor linking the DNA binding factor CBF1 to the histone deacetylase complex. Proc. Natl. Acad. Sci. USA 96: 23-28.
27. Oswald, F., M. Winkler, Y. Cao, K. Astrahantseff, S. Bourteele, W. Knochel, and T. Borggrefe. 2005. RBP-Jκ/SHARP recruits CtIP/CtBP corepressors to silence Notch target genes. Mol. Cell. Biol. 25: 10379-10390. (Pubitemid 41681962)
28. Tsuji, M., R. Shinkura, K. Kuroda, D. Yabe, and T. Honjo. 2007. Msx2-interacting nuclear target protein (Mint) deficiency reveals negative regulation of early thymocyte differentiation by Notch/RBP-J signaling. Proc. Natl. Acad. Sci. USA 104: 1610-1615. (Pubitemid 46214638)
29. Yamamoto, N., S. Yamamoto, F. Inagaki, M. Kawaichi, A. Fukamizu, N. Kishi, K. Matsuno, K. Nakamura, G. Weinmaster, H. Okano, and M. Nakafuku. 2001. Role of Deltex-1 as a transcriptional regulator downstream of the Notch receptor. J. Biol. Chem. 276: 45031-45040. (Pubitemid 37391294)
30. Reizis, B., and P. Leder. 2002. Direct induction of T lymphocyte-specific gene expression by the mammalian Notch signaling pathway. Genes Dev. 16: 295-300. (Pubitemid 34111409)
31. Jarriault, S., O. Le Bail, E. Hirsinger, O. Pourquie, F. Logeat, C. F. Strong, C. Brou, N. G. Seidah, and A. Israel. 1998. [Delta]-1 activation of Notch-1 signaling results in HES-1 transactivation. Mol. Cell. Biol. 18: 7423-7431. (Pubitemid 28533061)
32. Huang, Y. H., D. Li, A. Winoto, and E. A. Robey. 2004. Distinct transcriptional programs in thymocytes responding to T cell receptor, Notch, and positive selection signals. Proc. Natl. Acad. Sci. USA 101: 4936-4941.
33. Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, et al. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10: 345-355. (Pubitemid 29165289)
34. Lin, Y. W., R. A. Nichols, J. J. Letterio, and P. D. Aplan. 2006. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 107: 2540-2543.
35. Georgopoulos, K., M. Bigby, J. H. Wang, A. Molnar, P. Wu, S. Winandy, and A. Sharpe. 1994. The Ikaros gene is required for the development of all lymphoid lineages. Cell 79: 143-156. (Pubitemid 24309520)
36. Sun, L., A. Liu, and K. Georgopoulos. 1996. Zinc finger-mediated protein interactions modulate Ikaros activity, a molecular control of lymphocyte development. EMBO J. 15: 5358-5369. (Pubitemid 26336218)
37. Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, et al. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10: 345-355. (Pubitemid 29165289)
38. O'Neil, J., J. Grim, P. Strack, S. Rao, D. Tibbitts, C. Winter, J. Hardwick, M. Welcker, J. P. Meijerink, R. Pieters, et al. 2007. FBW7 mutations in leukemic cells mediate NOTCH pathway activation and resistance to γ-secretase inhibitors. J. Exp. Med. 204: 1813-1824. (Pubitemid 47236319)
39. Weng, A. P., A. A. Ferrando, W. Lee, J. P. t. Morris, L. B. Silverman, C. Sanchez-Irizarry, S. C. Blacklow, A. T. Look, and J. C. Aster. 2004. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 306: 269-271.
40. Wu, L., T. Sun, K. Kobayashi, P. Gao, and J. D. Griffin. 2002. Identification of a family of mastermind-like transcriptional coactivators for mammalian notch receptors. Mol. Cell. Biol. 22: 7688-7700.
41. Lin, S. E., T. Oyama, T. Nagase, K. Harigaya, and M. Kitagawa. 2002. Identification of new human mastermind proteins defines a family that consists of positive regulators for notch signaling. J. Biol. Chem. 277: 50612-50620.
42. Maillard, I., A. P. Weng, A. C. Carpenter, C. G. Rodriguez, H. Sai, L. Xu, D. Allman, J. C. Aster, and W. S. Pear. 2004. Mastermind critically regulates Notch-mediated lymphoid cell fate decisions. Blood 104: 1696-1702. (Pubitemid 39202276)
43. Adler, S. H., E. Chiffoleau, L. Xu, N. M. Dalton, J. M. Burg, A. D. Wells, M. S. Wolfe, L. A. Turka, and W. S. Pear. 2003. Notch signaling augments T cell responsiveness by enhancing CD25 expression. J. Immunol. 171: 2896-2903.
44. Amsen, D., A. Antov, D. Jankovic, A. Sher, F. Radtke, A. Souabni, M. Busslinger, B. McCright, T. Gridley, and R. A. Flavell. 2007. Direct regulation of Gata3 expression determines the T helper differentiation potential of Notch. Immunity 27: 89-99. (Pubitemid 47096801)
45. Fang, T. C., Y. Yashiro-Ohtani, C. Del Bianco, D. M. Knoblock, S. C. Blacklow, and W. S. Pear. 2007. Notch directly regulates Gata3 expression during T helper 2 cell differentiation. Immunity 27: 100-110. (Pubitemid 47096803)
46. Burns, C. E., D. Traver, E. Mayhall, J. L. Shepard, and L. I. Zon. 2005. Hematopoietic stem cell fate is established by the Notch-Runx pathway. Genes Dev. 19: 2331-2342. (Pubitemid 41396910)
47. Krebs, L. T., M. L. Deftos, M. J. Bevan, and T. Gridley. 2001. The Nrarp gene encodes an ankyrin-repeat protein that is transcriptionally regulated by the notch signaling pathway. Dev. Biol. 238: 110-119.
48. Huang, E. Y., A. M. Gallegos, S. M. Richards, S. M. Lehar, and M. J. Bevan. 2003. Surface expression of Notch1 on thymocytes: correlation with the double-negative to double-positive transition. J. Immunol. 171: 2296-2304.
49. Harker, N., T. Naito, M. Cortes, A. Hostert, S. Hirschberg, M. Tolaini, K. Roderick, K. Georgopoulos, and D. Kioussis. 2002. The CD8α gene locus is regulated by the Ikaros family of proteins. Mol. Cell 10: 1403-1415. (Pubitemid 36050881)
50. Naito, T., P. Gomez-Del Arco, C. J. Williams, and K. Georgopoulos. 2007. Antagonistic interactions between Ikaros and the chromatin remodeler Mi-2β determine silencer activity and Cd4 gene expression. Immunity 27: 723-734. (Pubitemid 350102255)
51. Urban, J. A., and S. Winandy. 2004. Ikaros null mice display defects in T cell selection and CD4 versus CD8 lineage decisions. J. Immunol. 173: 4470-4478.
52. Schmitt, T. M., and J. C. Zuniga-Pflucker. 2002. Induction of T cell development from hematopoietic progenitor cells by δ-like-1 in vitro. Immunity 17: 749-756. (Pubitemid 35477794)
53. Ciofani, M., T. M. Schmitt, A. Ciofani, A. M. Michie, N. Cuburu, A. Aublin, J. L. Maryanski, and J. C. Zuniga-Pflucker. 2004. Obligatory role for cooperative signaling by pre-TCR and Notch during thymocyte differentiation. J. Immunol. 172: 5230-5239. (Pubitemid 38542020)
54. 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.
55. Hernandez-Hoyos, G., M. K. Anderson, C. Wang, E. V. Rothenberg, and J. Alberola-Ila. 2003. GATA-3 expression is controlled by TCR signals and regulates CD4/CD8 differentiation. Immunity 19: 83-94. (Pubitemid 36859903)
56. 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. (Pubitemid 36193019)
57. Nichogiannopoulou, A., M. Trevisan, S. Neben, C. Friedrich, and K. Georgopoulos. 1999. Defects in hemopoietic stem cell activity in Ikaros mutant mice. J. Exp. Med. 190: 1201-1214. (Pubitemid 29522205)
58. Maeda, T., T. Merghoub, R. M. Hobbs, L. Dong, M. Maeda, J. Zakrzewski, M. R. van den Brink, A. Zelent, H. Shigematsu, K. Akashi, et al. 2007. Regulation of B versus T lymphoid lineage fate decision by the proto-oncogene LRF. Science 316: 860-866. (Pubitemid 46764272)
59. Pear, W. S., and J. C. Aster. 2004. T cell acute lymphoblastic leukemia/lymphoma: a human cancer commonly associated with aberrant NOTCH1 signaling. Curr. Opin. Hematol 11: 426-433.
60. Wolfer, A., A. Wilson, M. Nemir, H. R. MacDonald, and F. Radtke. 2002. Inactivation of Notch1 impairs VDJβ rearrangement and allows pre-TCR-independent survival of early α β lineage thymocytes. Immunity 16: 869-879. (Pubitemid 34786485)
61. Tanigaki, K., M. Tsuji, N. Yamamoto, H. Han, J. Tsukada, H. Inoue, M. Kubo, and T. Honjo. 2004. Regulation of αβ/γδ T cell lineage commitment and peripheral T cell responses by Notch/RBP-J signaling. Immunity 20: 611-622. (Pubitemid 38638130)
62. Bellavia, D., A. F. Campese, E. Alesse, A. Vacca, M. P. Felli, A. Balestri, A. Stoppacciaro, C. Tiveron, L. Tatangelo, M. Giovarelli, et al. 2000. Constitutive activation of NF-κB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J. 19: 3337-3348. (Pubitemid 30428211)