Ectopic TAL-1/SCL expression in phenotypically normal or leukemic myeloid precursors: Proliferative and antiapoptotic effects coupled with a differentiation blockade

Molecular and Cellular Biology

Volumn 17, Issue 5, 1997, Pages 2954-2969

  Condorelli, G L ^a   Tocci, A ^b   Botta, R ^b   Facchiano, F ^b   Testa, U ^b   Vitelli, L ^b   Valtieri, M ^b   Croce, C M ^b   Peschle, C ^a  

^a THOMAS JEFFERSON UNIVERSITY   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

COLECALCIFEROL; COMPLEMENTARY DNA; DNA; GRANULOCYTE COLONY STIMULATING FACTOR; INTERLEUKIN 3; RETINOIC ACID; TRANSCRIPTION FACTOR;

APOPTOSIS; ARTICLE; CELL CYCLE; CELL STRAIN HL 60; DNA BINDING; DNA SYNTHESIS; GENE EXPRESSION; GENE TRANSFER; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; LEUKEMIA; LYMPHOCYTE DIFFERENTIATION; ONCOGENE C MYC; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; T LYMPHOCYTE ACTIVATION;

MURINAE;

EID: 0030907392     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.17.5.2954     Document Type: Article

References (61)

1. Aplan, P. D., K. Nakahara, S. H. Orkin, and I. R. Kirsch. 1992. The SCL gene product: a positive regulator of erythroid differentiation. EMBO J. 11:4073-4081.
2. Arcari, P., R. Martinelli, and F. Salvatore. 1984. The complete sequence of a full length cDNA for human liver glyceraldehyde-3-phosphate dehydrogenase: evidence for multiple mRNA species. Nucleic Acids Res. 12:9179-9189.
3. Baer, R. 1993. TAL1, TAL2 and LYL1: a family of basic helix-loop-helix proteins implicated in T cell acute leukaemia. Semin. Cancer Biol. 4:341-347.
4. Bash, R. O., S. Hall, C. F. Timmons, W. M. Crist, M. Amylon, R. G. Smith, and R. Baer. 1995. Does activation of the TALI gene occur in a majority of patients with T-cell acute lymphoblastic leukemia? A pediatric oncology group study. Blood 86:666-676.
5. Begley, C. G., P. D. Aplan, M. P. Davey, K. Nakahara, K. Tchorz, J. Kurtzberg, M. S. Hershfield, B. F. Haynes, D. I. Cohen, T. A. Waldmann, and I. R. Kirsh. 1989. Chromosomal translocation in a human leukemia stem-cell line disrupts the T-cell antigen receptor delta-chain diversity region and results in a previously unreported fusion transcript. Proc. Natl. Acad. Sci. USA 86:2031-2035.
6. Bernard, O., O. Azogui, N. Lecointe, F. Mugneret, R. Berger, C. J. Larsen, and D. Mathieu-Mahul. 1992. A third tal-1 promoter is specifically used in human T cell leukemia. J. Exp. Med. 176:919-925.
7. Blandino, G., R. Scardigli, M. G. Rizzo, M. Crescenzi, S. Soddu, and A. Sacchi. 1995. Wild-type p53 modulates apoptosis of normal, IL-3 deprived, hematopoietic cells. Oncogene 10:731-737.
8. Brown, L., J. T. Cheng, Q. Chen, M. J. Siciliano, W. Crist, G. Buchanan, and R. Baer. 1990. Site-specific recombination of the tal-1 gene is a common occurrence in human T cell leukemia. EMBO J. 9:3343-3351.
9. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
10. Chen, Q., J. T. Cheng, L. H. Tsai, N. Schneider, G. Buchanan, A. Carroll, W. Crist, B. Ozanne, M. J. Siciliano, and R. Baer. 1990. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes helix-loop-helix protein. EMBO J. 9:415-424.
11. Chirgwin, J. M., A. E. Przybyla, R. J. MacDonald, and W. J. Rutter. 1979 Isolation of a biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18:5294-5299.
12. Collins, S. J. 1988. Retinoic acid-induced differentiation of retrovirus-infected HL-60 cells is associated with enhanced transcription from the viral long terminal repeat. J. Virol. 62:4349-4352.
13. Condorelli, G. L., L. Vitelli, M. Valtieri, I. Maria, 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.
14. 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.
15. Cone, R. D., and R. C. Mulligan. 1984. High-efficiency gene transfer into mammalian cells: generation of helper-free recombinant retrovirus with broad mammalian host range. Proc. Natl. Acad. Sci. USA 81:6349-6353.
16. Correll, P. H., S. Colilla, and S. Karlsson. 1994. Retroviral vector design for long-term expression in murine hematopoietic cells in vivo. Blood 84:1812-1822.
17. Elwood, N. J., and C. G. Begley. 1995. Reconstitution of mice with bone marrow cells expressing the SCL gene is insufficient to cause leukemia. Cell Growth Differ. 6:19-25.
18. Finger, L. R., G. Kagan, C. Christopher, J. Kurtzberg, M. Hershfield, P. C. Nowell, and C. M. Croce. 1989. Involvement of TCL-5 gene on human chromosome 1 in T-cell leukemia and melanoma. Proc. Natl. Acad. Sci. USA 86:5039-5043.
19. Goldfarb, A. N., and K. Lewandowska. 1995. Inhibition of cellular differentiation by the SCL/tal oncoprotein: transcriptional repression by an Id-like mechanism. Blood 85:465-471.
20. Green, A. R., E. DeLuca, and C. G. Begley. 1991. Antisense SCL suppresses self-renewal and enhances spontaneous erythroid differentiation of the human leukaemic cell line K562. EMBO J. 10:4153-4158.
21. Green, A. R., T. Lints, J. Visvader, R. Harvey, and C. G. Begley. 1992. SCL is coexpressed with GATA-1 in hemopoietic cells but is also expressed in developing brain. Oncogene 7:653-660.
22. Grignani, F., Jr., P. F. Ferrucci. U. Testa, G. P. Talamo, M. Fagioli, M. Alcalay, A. Mencarelli, F. Grignani, C. Peschle, I. Nicoletti, and P. G. Pelicci. 1993. The acute promyelocytic leukemia-specific PML/RARa fusion protein inhibits differentiation and promotes survival of U937 myeloid precursor cells. Cell 74:423-431.
23. Hermeking, H., and D. Eick. 1994. Mediation of c-myc-induced apoptosis by p53. Science 265:2091-2093.
24. Hoang, T., E. Paradis, G. Brady, F. Billia, K. Nakabara, N. N. Iscove, and I. R. Kirsch. 1996. Opposing effects of the basic helix-loop-helix transcription factor SCL on erythroid and monocytic differentiation. Blood 87:102-111.
25. Homburg, C. H. E., M. De Haas, A. Von Dem Borne, A. J. Verhoeven, C. P. M. Reutelingsperger, and D. Roos. 1995. Human neutrophils lose their surface FcγRIII and acquire annexin V binding sites during apoptosis in vitro. Blood 85:532-540.
26. 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.
27. 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.
28. Hsu, H. L., I. Waldman, and R. Baer. 1994. Formation of in vivo complexes between the TAL1 and E2A polypeptides in leukemic T cells. Proc. Natl. Acad. Sci. USA 91:3181-3185.
29. Kallianpur, A. R., J. E. Jordan, and S. J. Brandt. 1994. The SCL/Tal-1 gene is expressed in progenitors of both the hematopoietic and vascular system during embryogenesis. Blood 83:1200-1208.
30. Khanna-Gupta, A., M. C. Lopingeo, T. Savinelli, T. Zibello, N. Berliner, and A. S. Perkins. 1996. Retroviral insertional activation of the EV11 oncogene does not prevent G-CSF-induced maturation of the murine pluripotent myeloid cell line 32Dcl3. Oncogene 12:563-569.
31. Kotani, H., P. B. Newton, S. Zhang, Y. L. Chiang, E. Otto, L. Weaver, R. M. Blaese, W. F. Anderson, and G. J. McGarrity. 1994. Improved methods of retroviral vector transduction and production for gene therapy. Hum. Gene Ther. 5:19-28.
32. Leroy-Viard, K., M. A. Vinit, N. Lecointe, H. Jouault, U. Hibner, P. H. Romeo, and D. Mathieu-Mahul. 1995. Loss of TAL-1 protein activity induces premature apoptosis of Jurkat leukemic T cells upon medium depletion EMBO J. 14:2341-2349.
33. Martinez, J., I. Georgoff, and A. J. Levine. 1991. Cellular localization and cell cycle regulation by a temperature-sensitive p53 protein. Genes Dev. 5:151-159.
34. Metz, T., A. W. Harris, and J. M. Adams. 1995. Absence of p53 allows direct immortalization of hematopoietic cells by the myc and raf oncogenes. Cell 82:29-36.
35. Miller, A. D., and C. Buttimore. 1986. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell. Biol. 6:2895-2902.
36. 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.
37. Nicoletti, I., G. Migliorati, M. C. Pagliacci, F. Grignani, and C. Riccardi. 1991. A rapid and simple method for measuring thymocyte apoptosis by propidium iodide staining and flow cytometry. J. Immunol. Methods 139: 271-279.
38. Park, J. R., K. Robertson, D. D. Hickstein, S. Tsai, D. M. Hockenbery, and S. J. Collins. 1994. Dysregulated bcl-2 expression inhibits apoptosis but not differentiation of retinoic acid-induced HL-60 granulocytes. Blood 84:440-445.
39. Peverali, F. A., T. Ramqvist, R. Saffrich, R. Pepperkok, M. V. Barone, and L. Philipson. 1994. Regulation of G1 progression by E2A and Id helix-loop-helix proteins. EMBO J. 13:4291-4301.
40. Porcher, C., W. Swat, K. Rockwell, Y. Fujiwara, F. W. Alt, and S. H. Orkin. 1996. The T cell leukemia oncoprotein SCL/tal1 is essential for development of all hematopoietic lineages. Cell 86:47-57.
41. 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.
42. Qín, X. Q., D. M. Livingston, W. G. Kaelin, and P. D. Adams. 1994. Deregulated transcription factor E2F-1 expression leads to S-phase entry and p53-mediated apoptosis. Proc. Natl. Acad. Sci. USA 91:10918-10922.
43. Robb, L., N. J. Elwood, A. G. Alfanty, F. Kontgen, R. Li, D. Bonnett, and C. G. Begley. 1996. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J. 15:4123-4129.
44. 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.
45. Sachs, L., and J. Lotem. 1993. Control of programmed cell death in normal and leukemic cells: new implications for therapy. Blood 82:15-21.
46. 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.
47. Shimamoto, T., K. Ohyashiki, J. H. Ohyashiki, K. Kawakubo, T. Fujimura, H. Iwama, S. Nakazawa, and K. Toyama. 1995. The expression pattern of erythrocyte/megakaryocyte-related transcription factors GATA-1 and the stem cell leukemia gene correlates with hematopoietic differentiation and is associated with outcome of acute myeloid leukemia. Blood 86:3173-3180.
48. 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.
49. Soddu, S., G. Blandino, R. Scardigli, R. Martinelli, M. G. Rizzo, M. Crescenzi, and A. Sacchi. 1996. Wild-type p53 induces diverse effects in 32D cells expressing different oncogenes. Mol. Cell. Biol. 16:487-495.
50. Tanigawa, T., N. Elwood, D. Metcalf, D. Cary, E. DeLuca, N. A. Nicola, and C. G. Begley. 1993. The SCL gene product is regulated by and differentially regulates cytokine responses during myeloid leukemic ceil differentiation. Proc. Natl. Acad. Sci. USA 90:7864-7868.
51. Tanigawa, T., N. Nicola, G. A. McArthur, A. Strasser, and C. G. Begley. 1995. Differential regulation of macrophage differentiation in response to leukemic inhibitory factor/oncostatin-M/interleukin-6: the effect of enforced expression of the SCL transcription factor. Blood 85:379-390.
52. Testa, U., R. Masciulli, E. Tritarelli, R. Pustorino, G. Mariani, R. Martucci, T. Barberi, A. Camagna, M. Valtieri, and C. Peschle. 1993. Transforming growth factor-β potentiates vitamin D3-induced terminal monocytic differentiation of human leukemic cell lines. J. Immunol. 150:2418-2430.
53. Testa, U., G. L. Condorelli, M. Valtieri, L. Vitelli, B. Ziegler, and C. Peschle. Unilineage hematopoietic differentiation cultures: insight into blood cell production mechanisms. Submitted for publication.
54. 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.
55. Vallieri, M., et al. Unpublished data.
56. Valtieri, M., D. J. Tweardy, D. Caracciolo, K. Johnson, F. Mavilio, S. Altmann, D. Santoli, and G. Rovera. 1987. Cytokine-dependent granulocytic differentiation. Regulation of proliferative and differentiative responses in a murine progenitor cell line. J. Immunol. 138:3829-3835.
57. Visvader, J., C. G. Begley, and J. M. Adams. 1991. Differential expression of the LYL, SCL, and E2A helix-loop-helix genes within the hematopoietic system. Oncogene 6:187-194.
58. waf1/cip1. Genes Dev. 8:2817-2830.
59. Waldman, 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. Wolf, D., and V. Rotter. 1985. Major deletions in the gene encoding the p53 tumor antigen cause lack of p53 expression in HL-60 cells. Proc. Natl. Acad. Sci. USA 82:790-794.
61. Yonish-Rouach, E., D. Resnitzky, J. Lotem, L. Sachs, A. Kimchi, and M. Oren. 1991. Wild-type p53 induces apoptosis of myeloid leukemic cells that is inhibited by interleukin-6. Nature 352:345-347.