Notch activation is an early and critical event during T-cell leukemogenesis in Ikaros-deficient mice

Molecular and Cellular Biology

Volumn 26, Issue 1, 2006, Pages 209-220

  Dumortier, Alexis ^a,d   Jeannet, Robin ^a   Kirstetter, Peggy ^a,e   Kleinmann, Eva ^a   Sellars, MacLean ^a   Dos Santos, Nuno R ^b   Thibault, Christelle ^a   Barths, Jochen ^a   Ghysdael, Jacques ^b   Punt, Jennifer A ^a   Kastner, Philippe ^a,c   Chan, Susan ^a,c  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSTITUT CURIE   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

^d LUDWIG INSTITUTE FOR CANCER RESEARCH   (Switzerland)

^e EUROPEAN MOLECULAR BIOLOGY LABORATORY EMBL   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

IKAROS TRANSCRIPTION FACTOR; NOTCH RECEPTOR; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; HES1 PROTEIN, MOUSE; HOMEODOMAIN PROTEIN; NOTCH1 RECEPTOR;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CARBOXY TERMINAL SEQUENCE; CARCINOGENESIS; CELL PROLIFERATION; CONTROLLED STUDY; DELTEX 1 GENE; GENE; GENE EXPRESSION; GENE MUTATION; GENE REPRESSION; HES 1 GENE; LEUKEMOGENESIS; LYMPHOCYTE DIFFERENTIATION; MALIGNANT TRANSFORMATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN BINDING; PROTEIN FUNCTION; T LYMPHOCYTE; THYMUS LYMPHOMA; TRANSCRIPTION REGULATION; TRANSCRIPTION REPRESSION; AMINO ACID SEQUENCE; ANIMAL; DNA RESPONSIVE ELEMENT; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION; T CELL LYMPHOMA; THYMUS;

ANIMALIA;

AMINO ACID SEQUENCE; ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; HOMEODOMAIN PROTEINS; IKAROS TRANSCRIPTION FACTOR; LYMPHOMA, T-CELL; MICE; MOLECULAR SEQUENCE DATA; MUTATION; PROMOTER REGIONS (GENETICS); RECEPTOR, NOTCH1; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; THYMUS GLAND;

EID: 33645227683     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.1.209-220.2006     Document Type: Article

References (58)

1. 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.
2. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
3. Avitahl, N., S. Winandy, C. Friedrich, B. Jones, Y. Ge, and K. Georgopoulos. 1999. Ikaros sets thresholds for T cell activation and regulates chromosome propagation. Immunity 10:333-343.
4. Back, J., A. Dierich, C. Bronn, P. Kastner, and S. Chan. 2004. PU.1 determines the self-renewal capacity of erythroid progenitor cells. Blood 103:3615-3623.
5. Bellavia, D., A. F. Campese, E. Alesse, A. Vacca, M. P. Felli, A. Balestri, A. Stoppacciaro, C. Tiveron, L. Tatangelo, M. Giovarelli, C. Gaetano, L. Ruco, E. S. Hoffman, A. C. Hayday, U. Lendahl, L. Frati, A. Gulino, and I. Screpanti. 2000. Constitutive activation of NF-kappaB and T-cell leukemia/lymphoma in Notch3 transgenic mice. EMBO J. 19:3337-3348.
6. Bellavia, D., A. F. Campese, S. Checquolo, A. Balestri, A. Biondi, G. Cazzaniga, U. Lendahl, H. J. Fehling, A. C. Hayday, L. Frati, H. von Boehmer, A. Gulino, and I. Screpanti. 2002. Combined expression of pTalpha and Notch3 in T cell leukemia identifies the requirement of preTCR for leukemogenesis. Proc. Natl. Acad. Sci. USA 99:3788-3793.
7. 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.
8. Brown, K. E., S. S. Guest, S. T. Smale, K. Hahm, M. Merkenschlager, and A. G. Fisher. 1997. Association of transcriptionally silent genes with Ikaros complexes at centromeric heterochromatin. Cell 91:845-854.
9. Capobianco, A. J., P. Zagouras, C. M. Blaumueller, S. Artavanis-Tsakonas, and J. M. Bishop. 1997. Neoplastic transformation by truncated alleles of human NOTCH1/TAN1 and NOTCH2. Mol. Cell. Biol. 17:6265-6273.
10. Carron, C., F. Cormier, A. Janin, V. Lacronique, M. Giovannini, M. T. Daniel, O. Bernard, and J. Ghysdael. 2000. TEL-JAK2 transgenic mice develop T-cell leukemia. Blood 95:3891-3899.
11. Chiaramonte, R., A. Basile, E. Tassi, E. Calzavara, V. Cecchinato, V. Rossi, A. Biondi, and P. Comi. 2005. A wide role for NOTCH1 signaling in acute leukemia. Cancer Lett. 219:113-120.
12. 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.
13. 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.
14. Eisen, M. B., P. T. Spellman, P. O. Brown, and D. Botstein. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA 95:14863-14868.
15. Ellisen, L. W., J. Bird, D. C. West, A. L. Soreng, T. C. Reynolds, S. D. Smith, and J. Sklar. 1991. TAN-1, the human homolog of the Drosophila notch gene, is broken by chromosomal translocations in T lymphoblastic neoplasms. Cell 66:649-661.
16. Feldman, B. J., T. Hampton, and M. L. Cleary. 2000. A carboxy-terminal deletion mutant of Notch1 accelerates lymphoid oncogenesis in E2A-PBX1 transgenic mice. Blood 96:1906-1913.
17. 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.
18. Girard, L., Z. Hanna, N. Beaulieu, C. D. Hoemann, C. Simard, C. A. Kozak, and P. Jolicoeur. 1996. Frequent provirus insertional mutagenesis of Notch1 in thymomas of MMTVD/myc transgenic mice suggests a collaboration of c-myc and Notch1 for oncogenesis. Genes Dev. 10:1930-1944.
19. Harker, N., T. Naito, M. Cortes, A. Hostert, S. Hirschberg, M. Tolaini, K. Roderick, K. Georgopoulos, and D. Kioussis. 2002. The CD8alpha gene locus is regulated by the Ikaros family of proteins. Mol. Cell 10:1403-1415.
20. Hoemann, C. D., N. Beaulieu, L. Girard, N. Rebai, and P. Jolicoeur. 2000. Two distinct Notch1 mutant alleles are involved in the induction of T-cell leukemia in c-myc transgenic mice. Mol. Cell. Biol. 20:3831-3842.
21. 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.
22. Jarriault, S., C. Brou, F. Logeat, E. H. Schroeter, R. Kopan, and A. Israel. 1995. Signalling downstream of activated mammalian Notch. Nature 377:355-358.
23. Jeffries, S., and A. J. Capobianco. 2000. Neoplastic transformation by Notch requires nuclear localization. Mol. Cell. Biol. 20:3928-3941.
24. Kakinuma, S., M. Nishimura, A. Kubo, J. Y. Nagai, Y. Amasaki, H. J. Minima, T. Sado, and Y. Shimada. 2005. Frequent retention of heterozygosity for point mutations in p53 and Ikaros in N-ethyl-N-nitrosourea-induced mouse thymic lymphomas. Mutat. Res. 572:132-141.
25. Kaneta, M., M. Osawa, K. Sudo, H. Nakauchi, A. G. Farr, and Y. Takahama. 2000. A role for pref-1 and HES-1 in thymocyte development. J. Immunol. 164:256-264.
26. Karlsson, A., P. Soderkvist, and S. M. Zhuang. 2002. Point mutations and deletions in the znfn1a1/ikaros gene in chemically induced murine lymphomas. Cancer Res. 62:2650-2653.
27. 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.
28. Kim, J., S. Sif, B. Jones, A. Jackson, J. Koipally, E. Heller, S. Winandy, A. Viel, A. Sawyer, T. Ikeda, R. Kingston, and K. Georgopoulos. 1999. Ikaros DNA-binding proteins direct formation of chromatin remodeling complexes in lymphocytes. Immunity 10:345-355.
29. Kirstetter, P., M. Thomas, A. Dierich, P. Kastner, and S. Chan. 2002. Ikaros is critical for B cell differentiation and function. Eur. J. Immunol. 32:720-730.
30. Klug, C. A., S. J. Morrison, M. Masek, K. Hahm, S. T. Smale, and I. L. Weissman. 1998. Hematopoietic stem cells and lymphoid progenitors express different Ikaros isoforms, and Ikaros is localized to heterochromatin in immature lymphocytes. Proc. Natl. Acad. Sci. USA 95:657-662.
31. Koipally, J., and K. Georgopoulos. 2000. Ikaros interactions with CtBP reveal a repression mechanism that is independent of histone deacetylase activity. J. Biol. Chem. 275:19594-19602.
32. Koipally, J., A. Renold, J. Kim, and K. Georgopoulos. 1999. Repression by Ikaros and Aiolos is mediated through histone deacetylase complexes. EMBO J. 18:3090-3100.
33. Laws, A. M., and B. A. Osborne. 2004. p53 regulates thymic Notch1 activation. Eur. J. Immunol. 34:726-734.
34. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25:402-408.
35. 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 gamma-radiation-induced mouse thymic lymphomas. Carcinogenesis 25:1299-1304.
36. Maillard, I., S. H. Adler, and W. S. Pear. 2003. Notch and the immune system. Immunity 19:781-791.
37. Molnar, A., and K. Georgopoulos. 1994. The Ikaros gene encodes a family of functionally diverse zinc finger DNA-binding proteins. Mol. Cell. Biol. 14:8292-8303.
38. Nakase, K., F. Ishimaru, N. Avitahl, H. Dansako, K. Matsuo, K. Fujii, N. Sezaki, H. Nakayama, T. Yano, S. Fukuda, K. Imajoh, M. Takeuchi, A. Miyata, M. Hara, M. Yasukawa, I. Takahashi, H. Taguchi, K. Matsue, S. Nakao, Y. Niho, K. Takenaka, K. Shinagawa, K. Ikeda, K. Niiya, and M. Harada. 2000. Dominant negative isoform of the Ikaros gene in patients with adult B-cell acute lymphoblastic leukemia. Cancer Res. 60:4062-4065.
39. Nishii, K., N. Katayama, H. Miwa, M. Shikami, E. Usui, M. Masuya, H. Araki, F. Lorenzo, T. Ogawa, T. Kyo, K. Nasu, H. Shiku, and K. Kita. 2002. Non-DNA-binding Ikaros isoform gene expressed in adult B-precursor acute lymphoblastic leukemia. Leukemia 16:1285-1292.
40. Okano, H., Y. Saito, T. Miyazawa, T. Shinbo, D. Chou, S. Kosugi, Y. Takahashi, S. Odani, O. Niwa, and R. Kominami. 1999. Homozygous deletions and point mutations of the Ikaros gene in gamma-ray-induced mouse thymic lymphomas. Oncogene 18:6677-6683.
41. Papathanasiou, P., A. C. Perkins, B. S. Cobb, R. Ferrini, R. Sridharan, G. F. Hoyne, K. A. Nelms, S. T. Smale, and C. C. Goodnow. 2003. Widespread failure of hematolymphoid differentiation caused by a recessive niche-filling allele of the Ikaros transcription factor. Immunity 19:131-144.
42. 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.
43. Pear, W. S., J. P. Miller, L. Xu, J. C. Pui, B. Soffer, R. C. Quackenbush, A. M. Pendergast, R. Bronson, J. C. Aster, M. L. Scott, and D. Baltimore. 1998. Efficient and rapid induction of a chronic myelogenous leukemia-like myeloproliferative disease in mice receiving P210 bcr/abl-transduced bone marrow. Blood 92:3780-3792.
44. Radtke, F., A. Wilson, S. J. Mancini, and H. R. MacDonald. 2004. Notch regulation of lymphocyte development and function. Nat. Immunol. 5:247-253.
45. 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.
46. ic. Mol. Cell. Biol. 21:5925-5934.
47. Schroeter, E. H., J. A. Kisslinger, and R. Kopan. 1998. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393:382-386.
48. Shimada, Y., M. Nishimura, S. Kakinuma, M. Okumoto, T. Shiroishi, K. H. Clifton, and S. Wakana. 2000. Radiation-associated loss of heterozygosity at the Znfn1a1 (Ikaros) locus on chromosome 11 in murine thymic lymphomas. Radiat. Res. 154:293-300.
49. Sun, L., M. L. Crotty, M. Sensel, H. Sather, C. Navara, J. Nachman, P. G. Steinherz, P. S. Gaynon, N. Seibel, C. Mao, A. Vassilev, G. H. Reaman, and F. M. Uckun. 1999. Expression of dominant-negative Ikaros isoforms in T-cell acute lymphoblastic leukemia. Clin. Cancer Res. 5:2112-2120.
50. Sun, L., P. A. Goodman, C. M. Wood, M. L. Crotty, M. Sensel, H. Sather, C. Navara, J. Nachman, P. G. Steinherz, P. S. Gaynon, N. Seibel, A. Vassilev, B. D. Juran, G. H. Reaman, and F. M. Uckun. 1999. Expression of aberrantly spliced oncogenic ikaros isoforms in childhood acute lymphoblastic leukemia. J. Clin. Oncol. 17:3753-3766.
51. Sun, L., N. Heerema, L. Crotty, X. Wu, C. Navara, A. Vassilev, M. Sensel, G. H. Reaman, and F. M. Uckun. 1999. Expression of dominant-negative and mutant isoforms of the antileukemic transcription factor Ikaros in infant acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 96:680-685.
52. 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.
53. Takanashi, M., T. Yagi, T. Imamura, Y. Tabata, A. Morimoto, S. Hibi, E. Ishii, and S. Imashuku. 2002. Expression of the Ikaros gene family in childhood acute lymphoblastic leukaemia. Br. J. Haematol. 117:525-530.
54. Trinh, L. A., R. Ferrini, B. S. Cobb, A. S. Weinmann, K. Hahm, P. Ernst, I. P. Garraway, M. Merkenschlager, and S. T. Smale. 2001. Down-regulation of TDT transcription in CD4(+)CD8(+) thymocytes by Ikaros proteins in direct competition with an Ets activator. Genes Dev. 15:1817-1832.
55. 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.
56. Winandy, S., L. Wu, J. H. Wang, and K. Georgopoulos. 1999. Pre-T cell receptor (TCR) and TCR-controlled checkpoints in T cell differentiation are set by Ikaros. J. Exp. Med. 190:1039-1048.
57. 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.
58. Zweidler-McKay, P. A., and W. S. Pear. 2004. Notch and T cell malignancy. Semin. Cancer Biol. 14:329-340.