Enforced TAL-1 expression stimulates primitive, erythroid, and megakaryocytic progenitors but blocks the granulopoietic differentiation program

Cancer Research

Volumn 58, Issue 3, 1998, Pages 562-569

  Valtieri, M ^a   Tocci, A ^a   Gabbianelli, M ^a   Luchetti, L ^a   Masella, B ^a   Vitelli, L ^a   Botta, R ^a   Testa, U ^a   Condorelli, G L ^b   Peschle, C ^a,b  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HELIX LOOP HELIX PROTEIN; RECOMBINANT GROWTH FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; BURST FORMING UNIT E; CELL DIFFERENTIATION; COLONY FORMING UNIT GM; CONTROLLED STUDY; GENE TRANSFER; GRANULOPOIESIS; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MEGAKARYOPOIESIS; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RETROVIRUS;

ADULT; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL DIFFERENTIATION; CELL LINEAGE; CELLS, CULTURED; COLONY-FORMING UNITS ASSAY; CULTURE MEDIA; CULTURE TECHNIQUES; DNA-BINDING PROTEINS; ERYTHROID PROGENITOR CELLS; ERYTHROPOIESIS; FIBROBLAST GROWTH FACTOR 2; GENETIC VECTORS; GRANULOCYTES; HEMATOPOIESIS; HEMATOPOIETIC CELL GROWTH FACTORS; HEMATOPOIETIC STEM CELLS; HUMANS; INTERLEUKINS; MEGAKARYOCYTES; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; RECOMBINANT PROTEINS; RETROVIRIDAE; TRANSCRIPTION FACTORS; TRANSFECTION;

EID: 0032005207     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (45)

1. Brown, L., Cheng, J. T., Chen, Q., Siciliano, M. J., Crist, W., Buchanan, G., and Baer, R. Site-specific recombination of the tal-1 gehe is a common occurrence in human T cell leukemia. EMBO J., 9: 3343-3351, 1990.
2. Begley, C. G., Aplan, P. D., Davey, M. P., Nakahara, K., Tchorz, K., Kurtzberg, J., Hershfield, M. S., Haynes, B. F., Cohen, D. I., Waldmann, T. A., and Kirsh, I. R. Chromosomal translocation in a human leukemia stem-cell line disrupts the T-cell antigen receptor δ-chain diversity region and results in a previously unreported fusion transcript. Proc. Natl. Acad. Sci. USA, 86: 2031-2035, 1989.
3. Hsu, H. L., Huang, L., Tsan, J. T., Funk, W., Wright, W. E., Hu, J. S., Kingston, R. E., and Baer, R. Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol. Cell. Biol., 14: 1256-1265, 1994.
4. Hsu, H. L., Wadman, I., and Baer, R. Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells. Proc. Natl. Acad. Sci. USA, 91: 3181-3185, 1994.
5. Bernard, O., Azogui, O., Lecointe, N., Mugneret, F., Berger, R., Larsen, C. J., and Mathieu-Mahul, D. A third tal-1 promoter is specifically used in human T cell leukemia. J. Exp. Med., 176: 919-925, 1992.
6. Bash, R. O., Hall, S., Timmons, C. F., Crist, W. M., Amylon, M., Smith, R. G., and Baer, R. 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, 1995.
7. Kelliher, M. A., Seldin, D. C., and Leder, P. Tal-1 induces T cell acute lymphoblastic leukemia accelerated by casein kinase IIα. EMBO J., 15: 5160-5166, 1996.
8. Condorelli, G. L., Facchiano, F., Valtieri, M., Proietti, E., Vitelli, L., Lulli, V., Huebner, K., Peschle, C., and Croce, C. M. T-cell directed TAL-1 expression induces T cell malignancies in transgenic mice. Cancer Res., 56: 5113-5119, 1996.
9. Shivdasani, R. A., Mayer, E. L., and Orkin, S. H. Absence of blood formation in mice lacking the T-cell leukemia oncoprotein tal-1/SCL. Nature (Lond.), 373: 432-434, 1995.
10. Robb, L., Lyons, I., Li, R., Hartley, L., Kontgen, F., Harvey, R. P., Metcalf, D., and Begley, C. G. Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. USA, 92: 7075-7079, 1995.
11. Porcher, C., Swat, W., Rockwell, K., Fujiwara, Y., Alt, F. W., and Orkin, S. H. The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell, 86: 47-57, 1996.
12. Robb, L., Elwood, N. J., Elefanty, A. G., Kontgen, F., Li, R., Barnett, L. D., and Begley, C. G. The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J., 15: 4123-4129, 1996.
13. Green, A. R., Lints, T., Visvader, J., Harvey, R., and Begley, C. G. SCL is coexpressed with GATA-1 in hemopoietic cells but is also expressed in developing brain. Oncogene, 7: 653-660, 1992.
14. Kallianpur, A. R., Jordan, J. E., and Brandt, S. J. The SCL/Tal-1 gene is expressed in progenitors of both the hematopoietic and vascular system during embryogenesis. Blood, 83: 1200-1208, 1994.
15. Condorelli, G. L., Vitelli, L., Valtieri, M., Marta, I., Montesoro, E., Lulli, V., Baer, R., and Peschle, C. Coordinate expression and developmental role of Id2 protein and TAL1/E2A heterodimer in erythroid progenitor differentiation. Blood, 86: 164-175, 1995.
16. Mouthon, M. A., Bernard, O., Mitjavila, M. T., Romeo, P. H., Vainchenker, W., and Mathieu-Mahul, D. Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood, 81: 647-655, 1993.
17. Pulford, K., Lecointe, N., Leroy-Viard, K., Jones, M., Mathieu-Mahul, D., and Mason, D. Y. Expression of TAL-1 proteins in human tissues. Blood, 85: 675-684, 1995.
18. Visvader, J., Begley, C. G., and Adams, J. M. Differential expression of the LYL, SCL, and E2A helix-loop-helix genes within the hematopoietic system. Oncogene, 6: 187-194, 1991.
19. Valge-Archer, V. E., Osada, H., Warren, A. J., Forster, A., Li, J., Baer, R., and Rabbitts, T. H. 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, 1994.
20. Waldman, I., Li, J., Bash, R. O., Forster, A., Osada, H., Rabbitts, T. H., and Baer, R. Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO J., 13: 4831-4839, 1994.
21. Condorelli, G. L., Tocci, A., Botta, R., Facchiano, R., Testa, U., Vitelli, L., Valtieri, M., Croce, C. M., and Peschle, C. Ectopic TAL-1 expression in normal or leukemic myeloid precursors and non-hematopoietic cells lines: proliferative/anti-apoptotic effects coupled with differentiation blockade. Mol. Cell. Biol., 17: 2954-2969, 1997.
22. Miller, A. D., and Buttimore, C. Redesign of retrovirus packaging cell lines to avoid recombination leading to helper virus production. Mol. Cell. Biol., 6: 2895-2902, 1986.
23. Chen, Q., Cheng, J. T., Tsai, L. H., Schneider, N., Buchanan, G., Carroll, A., Crist, W., Ozanne, B., Siciliano, M. J., and Baer, R. The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes helix-loop-helix protein. EMBO J., 9: 415-424, 1990.
24. Chen, C., and Okayama, H. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol., 7: 2745-2752, 1987.
25. Cone, R. D., and Mulligan, R. C. 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, 1984.
26. Gabbianelli, M., Sargiacomo, M., Pelosi, E., Testa, U., Isacchi, G., and Peschle, C. "Pure" human hematopoietic progenitors: permissive action of basic fibroblast growth factor. Science (Washington DC), 249: 1561-1564, 1990.
27. Labbaye, C., Valtieri, M., Barberi, T., Meccia, E., Masella, B., Pelosi, E., Condorelli, G., Testa, U., and Peschle, C. Differential expression and functional role of GATA-2, NF-E2, and GATA-1 in normal adult hematopoiesis. J. Clin. Invest, 95: 2346-2358, 1995.
28. Gabbianelli, M., Pelosi, E., Montesoro, E., Valtieri, M., Luchetti, L., Samoggia, P., Vitelli, L., Barberi, T., Testa, U., Lyman, S., and Peschle, C. 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, 1995.
29. Valtieri, M., Schirò, R., Chelucci, C., Masella, B., Testa, U., Casella, I., Montesoro, E., Mariani, G., Hassan, H. J., and Peschle, C. Efficient transfer of selectable and membrane reporter genes in hematopoietic progenitor and stem cells purified from human peripheral blood. Cancer Res., 54: 4398-4404, 1994.
30. Valtieri, M., Gabbianelli, M., Pelosi, E., Bassano, E., Petti, S., Russo, G., Testa, U., and Peschle, C. Erythropoietin alone induces erythroid burst formation by human embryonic but not adult BFU-E in unicellular serum-free culture. Blood, 74: 460-470, 1989.
31. Guerriero, R., Testa, U., Gabbianelli, M., Mattia, G., Montesoro, E., Macioce, G., Pace, A., Ziegler, B., Hassan, H. J., and Peschle, C. Unilineage megakaryocytic proliferation and differentiation of purified hematopoietic progenitors in serum-free liquid culture. Blood, 86: 3725-3736, 1995.
32. Cross, M. A., Heyworth, C. M., Murrell, A. M., Bockamp, E. O., Dexter, T. M., and Green, A. R. Expression of lineage restricted transcription factors precedes lineage specific differentiation in a multipotent haemopoietic progenitor cell line. Oncogene, 9: 3013-3016, 1994.
33. Labbaye, C., Valtieri, M., Testa, U., Giampaolo, A., Meccia, E., Sterpetti, P., Parolini, I., Pelosi, E., Bulgarini, D., Cayre, Y. E., and Peschle, C. Retinoic acid downmodulates erythroid differentiation and GATA-1 expression in purified adult progenitor culture. Blood, 83: 651-656, 1994.
34. Tocci, A., Parolini, I., Gabbianelli, M., Testa, U., Luchetti, L., Samoggia, P., Masella, B., Russo, G., Valtieri, M., and Peschle, C. Dual action of retinoic acid on human embryonic-fetal hematopoiesis: blockade of primitive progenitor proliferation and shift from multipotent/erythroid/monocytic to granulocytic differentiation program Blood, 88: 2878-2888, 1996.
35. Testa, U., Fossati, C., Samoggia, P., Masciulli, R., Mariani, G., Hassan, H. J., Sposi, N. M., Guerriero, R., Rosato, V., Gabbianelli, M., Pelosi, E., Valtieri, M., and Peschle, C. Expression of growth factor receptors in unilineage differentiation culture of purified hematopoietic progenitors. Blood, 88: 3391-3406, 1996.
36. Sposi, N. M., Zon, L. I., Carè, A., Valtieri, M., Testa, U., Gabbianelli, M., Mariani, G., Bottero, L., Mather, C., Orkin, S. H., and Peschle, C. Cell cycle-dependent initiation and lineage-dependent abrogation of GATA-1 expression in pure differentiating hematopoietic progenitors. Proc. Natl. Acad. Sci. USA, 89: 6353-6357, 1992.
37. Giampaolo, A., Sterpetti, P., Bulgarini, D., Samoggia, P., Pelosi, E., Valtieri, M., and Peschle, C. Key functional role and lineage-specific expression of selected HOXB genes in purified hematopoietic progenitor differentiation. Blood, 84: 3637-3647, 1994.
38. Condorelli, G. L., Testa, U., Valtieri, M., Vitelli, L., De Luca, A., Barberi, T., Montesoro, E., Campisi, S., Giordano, A., and Peschle, C. 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, 1995.
39. Apian, P. D., Nakahara, K., Orkin, S. H., and Kirsch, I. R. The SCL gene product: a positive regulator of erythroid differentiation. EMBO J., 11: 4073-4081, 1992.
40. Green, A. R., DeLuca, E., and Begley, C. G. Antisense SCL suppresses self-renewal and enhances spontaneous erythroid differentiation of the human leukaemic cell line K562. EMBO J., 10: 4153-4158, 1991.
41. Hoang, T., Paradis, E., Brady, G., Billia, F., Nakahara, K., Iscove, N. N., and Kirsch, I. R. Opposing effects of the basic helix-loop-helix transcription factor SCL on erythroid and monocytic differentiation. Blood, 87: 102-111, 1996.
42. Tanigawa, T., Nicola, N., McArthur, G. A., Strasser, A., and Begley, C. G. 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, 1995.
43. Tanigawa, T., Elwood, N., Metcalf, D., Cary, D., DeLuca, E., Nicola, N. A., and Begley, C. G. The SCL gene product is regulated by and differentially regulates cytokine responses during myeloid leukemic cell differentiation. Proc. Natl. Acad. Sci. USA, 90: 7864-7868, 1993.
44. Elwood, N. J., and Begley, C. G. Reconstitution of mice with bone marrow cells expressing the SCL gene is insufficient to cause leukemia. Cell Growth Differ., 6: 19-25, 1995.
45. Udomsakdi, C., Lansdorp, P. M., Hogge, D. E., Reid, D. S., Eaves, A. C., and Eaves, C. J. Characterization of primitive hematopoietic cells in normal human peripheral blood. Blood, 80: 2513-2521, 1992.