A pentamer transcriptional complex including tal-1 and retinoblastoma protein downmodulates c-kit expression in normal erythroblasts

Molecular and Cellular Biology

Volumn 20, Issue 14, 2000, Pages 5330-5342

  Vitelli, Luigi ^a   Condorelli, Gianluigi ^a,b   Lulli, Valentina ^a   Hoang, Trang ^c   Luchetti, Luisella ^b   Croce, Carlo M ^b   Peschle, Cesare ^a,b  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^c CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

RETINOBLASTOMA PROTEIN; STEM CELL FACTOR; TRANSCRIPTION FACTOR;

ADULT; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; ERYTHROBLAST; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE TARGETING; GENETIC TRANSCRIPTION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; MALE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RETINOBLASTOMA;

ADULT; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELLS, CULTURED; DNA-BINDING PROTEINS; DOWN-REGULATION; ERYTHROCYTES; GENE EXPRESSION REGULATION; HUMANS; MALE; METALLOPROTEINS; PROMOTER REGIONS (GENETICS); PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-KIT; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 0033944604     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.20.14.5330-5342.2000     Document Type: Article

References (68)

1. Agulnick, A. D., M. Taira, J. J. Breen, T. Tanaka, I. B. Dawid, and H. Westphal. 1996. Interactions of the LIM-domain-binding factor Ldb1 with LIM homeodomain proteins. Nature 384:270-272.
2. Baker, S. J., S. Markowitz, E. R. Fearon, J. K. Willson, and B. Vogelstein. 1990. Suppression of human colorectal carcinoma cell growth by wild-type p53. Science 249:912-915.
3. Bash, R. O., S. Hall, C. F. Timmons, W. M. Crist, M. Amylon, R. G. Smith, and R. Baer. 1995. Does activation of the TAL1 gene occur in a majority of patients with T-cell acute lymphoblastic leukemia? A pediatric oncology group study. Blood 86:666-676.
4. Begley, C. G., and A. R. Green. 1999. The SCL gene: from case report to critical hematopoietic regulator. Blood 93:2760-2770.
5. Bernard, O., N. Lecointe, P. Jonveaux, M. Souyri, M. Mauchauffé, R. Berger, C. J. Larsen, and D. Mathieu-Mahul. 1991. Two site-specific deletions and t(1;14) translocation restricted to human T-cell acute leukemias disrupt the 5′ part of the tal-1 gene. Oncogene 6:1477-1488.
6. Boehm, T., L. Foroni, M. Kennedy, and T. H. Rabbitts. 1990. The rhombotin gene belongs to a class of transcriptional regulators with a potential novel protein dimerization motif. Oncogene 5:1103-1105.
7. Chen, P.-L., D. J. Riley, S. Chen-Kiang, and W.-H. Lee. 1996. Retinoblastoma protein directly interacts with and activates the transcription factor NF-IL6. Proc. Natl. Acad. Sci. USA 93:465-469.
8. Chen, P.-L., D. J. Riley, Y. Chen, and W.-H. Lee. 1996. Retinoblastoma protein positively regulates terminal adipocyte differentiation through direct interaction with C/EBPs. Genes Dev. 10:2794-2804.
9. Clarke, A. R., E. R. Maandag, M. van Roon, N. M. T. van de Lugt, M. van der Valk, M. L. Hooper, A. Berns, and H. te Riele. 1992. Requirement for a functional Rb-1 gene in murine development. Nature 359:328-330.
10. Cohen-Kaminski, S. L., L. Maouche-Chretien, L. Vitelli, M. A. Vinit, I. Blanchard, M. Yamamoto, C. Peschle, and P. H. Romeo. 1998. Chromatin immunoselection defines a TAL-1 target gene. EMBO J. 17:5151-5160.
11. Condorelli, G. L., U. Testa, M. Valtieri, L. Vitelli, A. De Luca, T. Barberi, E. Montesoro, S. Campisi, A. Giordano, and C. Peschle. 1995. Modulation of retinoblastoma gene in normal adult hematopoiesis: peak expression and functional role in advanced erythroid differentiation. Proc. Natl. Acad. Sci. USA 92:4808-4812.
12. Condorelli, G. L., L. Vitelli, M. Valtieri, I. Marta, E. Montesoro, V. Lulli, R. Baer, and C. Peschle. 1995. Coordinate expression and developmental role of Id2 protein and TAL1/E2A heterodimer in erythroid progenitor differentiation. Blood 86:164-175.
13. Condorelli, G. L., F. Facchiano, M. Valtieri, E. Proietti, L. Vitelli, V. Lulli, K. Huebner, C. Peschle, and C. M. Croce. 1996. T-cell-directed TAL-1 expression induces T-cell malignancies in transgenic mice. Cancer Res. 56: 5113-5119.
14. Condorelli, G. L., A. Tocci, R. Botta, R. Facchiano, U. Testa, L. Vitelli, M. Valtieri, C. M. Croce, and C. Peschle. 1997. Ectopic TAL-1/SCL expression in phenotypically normal or leukemic myeloid precursors: proliferative and antiapoptotic effects coupled with a differentiation blockade. Mol. Cell. Biol. 17:2954-2969.
15. Field, S. J., F.-Y. Tsai, F. Kuo, A. M. Zubiaga, W. G. Kaelin, Jr., D. M. Livingston, S. H. Orkin, and M. E. Greenberg. 1996. E2F-1 functions in mice to promote apoptosis and suppress proliferation. Cell 85:549-561.
16. Gabbianelli, M., E. Pelosi, E. Montesoro, M. Valtieri, L. Luchetti, P. Samoggia, L. Vitelli, T. Barberi, U. Testa, S. Lyman, et al. 1995. Multi-level effects of flt3 ligand on human hematopoiesis: expansion of putative stem cells and proliferation of granulomonocytic progenitors/monocytic precursors. Blood 86:1661-1670.
17. Gabbianelli, M., M. Sargiacomo, E. Pelosi, U. Testa, G. Isacchi, and C. Peschle. 1990. "Pure" human hematopoietic progenitors: permissive action of basic fibroblast growth factor. Science 249:1561-1564.
18. Gattei, V., D. Aldinucci, J. M. Quinn, M. Degan, M. Cozzi, V. Perin, A. D. Iuliis, S. Juzbasic, S. Improta, N. A. Athanasou, L. K. Ashman, and A. Pinto. 1996. Human osteoclasts and preosteoclast cells (FLG 29.1) express functional c-kit receptors and interact with osteoblast and stromal cells via membrane-bond stem cell factor. Cell Growth Differ. 7:753-763.
19. Gu, W., J. W. Schneider, G. Condorelli, S. Kaushal, V. Mahdavi, and B. Nadal-Ginard. 1993. Interaction of myogenic factors and the retinoblastoma protein mediates muscle cell commitment and differentiation. Cell 72:309-324.
20. Hsu, H.-L., J.-T. Cheng, Q. Chen, and R. Baer. 1991. Enhancer-binding activity of the tal-1 oncoprotein in association with the E47/E12 helix-loop-helix proteins. Mol. Cell. Biol. 11:3037-3042.
21. Hsu, H. L., L. Huang, J. T. Tsan, W. Funk, W. E. Wright, J. S. Hu, R. E. Kingston, and R. Baer. 1994. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol. Cell. Biol. 14:1256-1265.
22. Hsu, H. L., I. Wadman, and R. Baer. 1994. Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells. Proc. Natl. Acad. Sci. USA 91:3181-3185.
23. Hu, N., M. L. Gulley, J. T. Kung, and E. Y.-H. P. Lee. 1997. Retinoblastoma gene deficiency has mitogenic but not tumorigenic effects on erythropoiesis. Cancer Res. 57:4123-4129.
24. Jacks, T., A. Fazeli, E. M. Schmitt, R. T. Bronson, M. A. Goodell, and R. A. Weinberg. 1992. Effects of an Rb mutation in the mouse. Nature 359:295-300.
25. Jurata, L. W., D. A. Kenny, and G. N. Gill. 1996. Nuclear LIM interactor, a rhombotin and LIM homeodomain interacting protein, is expressed early in neuronal development. Proc. Natl. Acad. Sci. USA 93:11693-11698.
26. Katayama, N., J. P. Shih, S. Nishikawa, T. Kina, S. C. Clark, and M. Ogawa. 1993. Stage-specific expression of c-kit protein by murine hematopoietic progenitors. Blood 82:2353-2360.
27. Kelliher, M. A., D. C. Seldin, and P. Leder. 1996. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase IIalpha. EMBO J. 15: 5160-5166.
28. Kouzarides, T. 1995. Transcriptional control by the retinoblastoma protein. Semin. Cancer Biol. 6:91-98.
29. Krosl, G., G. He, M. Lefrancois, F. Charron, P. H. Romeo, P. Jolicoeur, I. R. Kirsch, M. Nemer, and T. Hoang. 1998. Transcription factor SCL is required for c-kit expression and c-kit function in hematopoietic cells. J. Exp. Med. 188:439-450.
30. Labbaye, C., M. Valtieri, T. Barberi, E. Meccia, B. Masella, E. Pelosi, G. Condorelli, U. Testa, and C. Peschle. 1995. Differential expression and functional role of GATA-2, NF-E2 and GATA-1 in normal adult hematopoiesis. J. Clin. Investig. 95:2346-2358.
31. Larson, R. C., I. Lavenir, T. A. Larson, R. Baer, A. J. Warren, I. Waldman, K. Nottage, and T. H. Rabbitts. 1996. Protein dimerization between Lmo2 (Rbtn2) and Tall alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J. 15:1021-1027.
32. Lee, E. Y., N. Hu, S. S. Yuan, L. A. Cox, A. Bradley, W.-H. Lee, and K. Herrup. 1994. Dual roles of the retinoblastoma protein in cell cycle regulation and neuron differentiation. Genes Dev. 8:2008-2021.
33. Lee, E. Y.-H. P., C. Y. Chang, N. Hu, Y. C. J. Wang, C. C. Lai, K. Herrup, W. H. Lee, and A. Bradley. 1992. Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis. Nature 359:288-294.
34. Lyman, S. D., and S. E. Jacobsen. 1998. c-kit ligand and Flt3 ligand: stem/progenitor cell factors with overlapping yet distinct activities. Blood 91:1101-1134.
35. Maandag, E. C., M. van der Valk, M. Vlaar, C. Feltkamp, J. O'Brien, M. van Roon, N. van der Lugt, A. Berns, and H. te Riele. 1994. Developmental rescue of an embryonic-lethal mutation in the retinoblastoma gene in chimeric mice. EMBO J. 13:4260-4268.
36. Mao, S., G. A. M. Neale, and R. M. Goorha. 1997. T-cell oncogene rhombotin-2 interacts with retinoblastoma-binding protein 2. Oncogene 14:1531-1539.
37. Maouche, L., J. P. Cartron, and S. Chretien. 1994. Different domains regulate the human erythropoietin receptor gene transcription. Nucleic Acids Res. 22:338-346.
38. Mouthon, M. A., O. Bernard, M. T. Mitjavila, P. H. Romeo, W. Vainchenker, and D. Mathieu-Mahul. 1993. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 81:647-655.
39. Nordeen, S. K. 1988. Luciferase reporter gene vectors for analysis of promoters and enhancers. BioTechniques 6:454-458.
40. Osada, H., G. Grutz, H. Axelson, A. Forster, and T. H. Rabbitts. 1995. Association of erythroid transcription factors: complexes involving the LIM protein RBTN2 and the zinc-finger protein GATA-1. Proc. Natl. Acad. Sci. USA 92:9585-9589.
41. Park, G. H., H. K. Plummer III, and G. W. Krystal. 1998. Selective Sp1 binding is critical for maximal activity of the human c-kit promoter. Blood 92:4138-4149.
42. Porcher, C., W. Swat, K. Rockwell, Y. Fujiwara, F. W. Alt, and S. H. Orkin. 1996. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86:47-57.
43. Pulford, K., N. Lecointe, K. Leroy-Viard, M. Jones, D. Mathieu-Mahul, and D. Y. Mason. 1995. Expression of TAL-1 proteins in human tissues. Blood 85:675-684.
44. Ratajczak, M. Z., D. Perrotti, P. Melotti, M. Powzaniuk, B. Calabretta, K. Onodera, D. A. Kregenow, B. Machalinski, and A. M. Gerwitz. 1998. Myb and ets proteins are candidate regulators of c-kit expression in human hematopoietic cells. Blood 91:1934-1946.
45. Richon, V. M., and G. Venta-Perez. 1996. Changes in E2F DNA-binding activity during induced erythroid differentiation. Cell Growth Differ. 7:31-42.
46. Robb, L., I. Lyons, R. Li, L. Hartley, F. Kontgen, R. P. Harvey, D. Metcalf, and C. G. Begley. 1995. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. USA 92:7075-7079.
47. Sellers, W. R., B. G. Novitch, S. Miyake, A. Heith, G. A. Otterson, F. J. Kaye, A. B. Lassar, and W. G. Kaelin, Jr. 1998. Stable binding to E2F is not required for the retinoblastoma protein to activate transcription, promote differentiation, and suppress tumor cell growth. Genes Dev. 12:95-106.
48. Shan, B., and W. H. Lee. 1994. Deregulated expression of E2F-1 induces S-phase entry and leads to apoptosis. Mol. Cell. Biol. 14:8166-8173.
49. Shivdasani, R. A., E. L. Mayer, and S. H. Orkin. 1995 Absence of blood formation in mice lacking the T-cell leukemia oncoprotein tal-1/SCL. Nature 373:432-434.
50. Sieweke, M. H., and T. Graf. 1998. A transcription factor party during blood cell differentiation. Curr. Opin. Genet. Dev. 8:545-551.
51. Taya, Y. 1997. RB kinases and RB-binding proteins: new points of view. Trends Biochem. Sci. 22:14-17.
52. Tsujimura, T., E. Morii, M. Nozaki, K. Hashimoto, Y. Moriyama, K. Takebayashi, T. Kondo, Y. Kanakura, and Y. Kitamura. 1996. Involvement of transcription factor encoded by the mi locus in the expression of c-kit receptor tyrosine kinase in cultured mast cells of mice. Blood 88:1225-1233.
53. Valge-Archer, V. E., H. Osada, A. J. Warren, A. Forster, J. Li, R. Baer, and T. H. Rabbitts. 1994. The LIM protein RBTN2 and the basic helix-loop-helix protein TAL1 are present in a complex in erythroid cells. Proc. Natl. Acad. Sci. USA 91:8617-8621.
54. Valtieri, M., M. Gabbianelli, E. Pelosi, E. Bassano, S. Petti, G. Russo, U. Testa, and C. Peschle. 1989. Erythropoietin alone induces erythroid burst formation by human embryonic but not adult BFU-E in unicellular serum-free culture. Blood 74:460-470.
55. Valtieri, M., A. Tocci, M. Gabbianelli, L. Luchetti, B. Masella, L. Vitelli, R. Botta, U. Testa, G. L. Condorelli, and C. Peschle. 1998. Enforced TAL-1 expression stimulates primitive, erythroid, and megakaryocytic progenitors but blocks the granulopoietic differentiation program. Cancer Res. 58:562-569.
56. Vandenbark, G. R., Y. Chen, E. Friday, K. Pavlik, B. Anthony, C. deCastro, and R. E. Kaufman. 1996. Complex regulation of human c-kit transcription by promoters, repressors, activators, and specific myb elements. Cell Growth Differ. 7:1383-1392.
57. Visvader, J., C. G. Begley, and J. M. Adams. 1991. Differential expression of the LYL, SCL, and E2A helix-loop-helix gene within the hematopoietic system. Oncogene 6:187-194.
58. Visvader, J. E., X. Mao, Y. Fujiwara, K. Hahm, and S. H. Orkin. 1997. The LIM-domain binding protein Ldb1 and its partner LMO2 act as negative regulators of erythroid differentiation. Proc. Natl. Acad. Sci. USA 94:13707-13712.
59. Wadman, I., J. Li, R. O. Bash, A. Forster, H. Osada, T. H. Rabbitts, and R. Baer. 1994. Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO J. 13:4831-4839.
60. Wadman, I. A., H. Osada, G. G. Grütz, A. D. Agulnik, H. Westphal, A. Forster, and T. H. Rabbitts. 1997. The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL-1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J. 16:3145-3157.
61. Wang, J. Y. 1997. Retinoblastoma protein in growth suppression and death protection. Curr. Opin. Genet. Dev. 7:39-45.
62. Weinberg, R. A. 1995. The retinoblastoma protein and cell cycle control. Cell 81:323-330.
63. Williams, B. O., E. M. Schmitt, L. Remington, R. T. Bronson, D. M. Albert, R. A. Weinberg, and T. Jacks. 1994. Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO J. 13:4251-4259.
64. Yamamoto, K., A. Tojo, N. Aoki, and M. Shibuya. 1993. Characterization of the promoter region of the human c-kit proto-oncogene. Jpn. J. Cancer Res. 84:1136-1144.
65. Zacksenhaus, E., Z. Jiang, D. Chung, J. D. Marth, R. A. Phillips, and B. L. Gallie. 1996. pRb controls proliferation, differentiation, and death of skeletal muscle cells and other lineages during embryogenesis. Genes Dev. 10:3051-3064.
66. Ziegler, B. L., U. Testa, G. Condorelli, L. Vitelli, M. Valtieri, and C. Peschle. 1998. Unilineage hematopoietic differentiation in bulk and single cell culture. Stem Cells 16:51-73.
67. Ziegler, B. L., M. Valtieri, G. Almeida Porada, R. De Maria, R. Müller, B. Masella, M. Gabbianelli, I. Casella, E. Pelosi, T. Bock, E. Zanjani, and C. Peschle. 1999. KDR receptor: a key marker defining hematopoietic stem cells. Science 285:1553-1558.
68. Zon, L. I., and S. H. Orkin. 1992. Sequence of the human GATA-1 promoter. Nucleic Acids Res. 20:1812.