The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages

Cell

Volumn 86, Issue 1, 1996, Pages 47-57

  Porcher, Catherine ^a   Swat, Wojciech ^a,b   Rockwell, Karen ^a   Fujiwara, Yuko ^a,b   Alt, Frederick W ^a,b   Orkin, Stuart H ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; EMBRYO; ERYTHROPOIESIS; GENETIC REGULATION; HEMATOPOIESIS; LYMPHOPOIESIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; T CELL LEUKEMIA;

ANIMALIA;

EID: 0030581174     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80076-8     Document Type: Article

References (69)

1. Aplan, P.D., Begley, C.G., Bertness, V., Nussmeier, M., Ezquerra, A., Coligan, J., and Kirsch, I.R. (1990). The SCL gene is formed from a transcriptionally complex locus. Mol. Cell. Biol. 10, 6426-6435.
2. Aplan, P.D., Nakahara, K., Orkin, S.H., and Kirsch, I.R. (1992). The SCL gene product: a positive regulator of erythroid differentiation. EMBO J. 11, 4073-4081.
3. Bash, R.O., Hall, S., Timmons, C.F., Crist, W.M., Amylon, M., Smith, R.G., and Baer, R. (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., 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 Kirsch, I.R. (1989a). Chromosomal translocation in a human leukemic 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.
5. Begley, C.G., Apian, P.D., Denning, S.M., Haynes, B.F., Waldmann, T.A., and Kirsch, I.R. (1989b). The gene SCL is expressed during early hematopoiesis and encodes a differentiation-related DNA-binding motif. Proc. Natl. Acad. Sci. USA 86, 10128-10132.
6. Begley, C.G., Visvader, J., Green, A.R., Aplan, P.D., Metcalf, D., Kirsch, I.R., and Gough, N. (1991). Molecular cloning and chromosomal location of the mouse homolog of the human helix-loop-helix gene SCL. Proc. Natl. Acad. Sci. 88, 869-873.
7. Berger, C.N., Tam, P.P.L., and Sturm, K.S. (1995). The development of haematopoietic cells is biased in embryonic stem cell chimeras. Dev. Biol. 170, 651-663.
8. Boehm, T., Baer, R., Lavenir, I., Forster, A., Waters, J.J., Nacheva, E., and Rabbitts, T.H. (1988). The mechanism of chromosomal translocation t(11;14) involving the T cell receptor Cd locus on human chromosome 14q11 and a transcribed region of chromosome 11p15. EMBO J. 7, 385-394.
9. Chen, J., Lansford, R., Stewart, V., Young, F., and Alt, F.W. (1993). RAG-2-deficient blastocyst complementation: an assay of gene function in lymphocyte development. Proc. Natl. Acad. Sci. USA 90, 4528-4532.
10. Chen, Q., Cheng, J.-T., Tsai, L.-H., Schneider, N., Buchanan, G., Carroll, A., Grist, W., Ozanne, B., Siciliano, M.J., and Baer, R. (1990). The tal gene undergoes chromosome translocation in T cell leukemia and potentially encodes a helix-loop-helix protein. EMBO J. 9, 415-424.
11. Chomczynski, P., and Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162, 156-159.
12. Erickson, P., Gao, J., Chang, K.S., Look, A.T., Whisenant, E., Raimondi, S., Lasher, R., Trujillo, J., Rowley, J., and Drabkin, H. (1992). Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript, AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood 80, 1825-1831.
13. Finger, L.R., Kagan, J., Christopher, G., Kurtzberg, J., Hershfield, M.S., Nowell, P.C., and Croce, C.M. (1989). Involvement of theTCL5 gene on human chromosome 1 in T cell leukemia and melanoma. Proc. Natl. Acad. Sci. USA 86, 5039-5043.
14. Georgopoulos, K., Bigby, M., Wang, J.-H., Molnar, A., Wu, P., Winandy, S., and Sharpe, A. (1994). The Ikaros gene is required for the development of all lymphoid lineages. Cell 79, 143-156.
15. Golub, T.R., Barker, G.F., Bohlander, S.F., Hiebert, S.W., Ward, D.C., Bray-Ward, P., Morgan, E., Raimondi, S.C., Rowley, J.D., and Gilliland, D.G. (1995). Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 92, 4917-4921.
16. Green, A.R., Salvaris, E., and Begley, C.G. (1991). Erythroid expression of the helix-loop-helix gene, SCL. Oncogene 6, 475-479.
17. Green, A.R., Lints, T., Visvader, J., Harvey, R., and Begley, C.G. (1992). SCL is coexpressed with GATA-1 in hemopoietic cells but is also expressed in developing brain. Oncogene 7, 653-660.
18. Gu, Y., Nakamura, T., Alder, H., Prasad, R., Canaani, O., Cimino, G., Croce, C.M., and Canaani, E. (1992). The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene. Cell 71, 701-708.
19. Guillemot, F., Lo, L.-C., Johnson, J.E., Auerbach, A., Anderson, D.J., and Joyner, A.L. (1993). Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75, 463-476.
20. Hawley, R.G., Lieu, F.H.L., Fong, A.Z.C., and Hawley, T.S. (1994). Versatile retroviral vectors for potential use in gene therapy. Gene Therapy 1, 136-138.
21. Higuchi, R. (1989). Simple and rapid preparation of samples for PCR. In PCR Technology: Principles and Applications for DNA Amplification, H.A. Erlich, ed. (New York: Stockton Press), pp. 31-38.
22. Hoang, T., Paradis, E., Brady, G., Billia, F., Nakahara, K., Iscove, N.N., and Kirsch, I.R. (1996). Opposing effects of the basic-helix-loop-helix transcription factor SCL on erythroid and monocytic differentiation. Blood 87, 102-111.
23. Hsu, H.-L., Cheng, J.-T., Chen, Q., and Baer, R. (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.
24. Hsu, H.-L., Huang, L., Tsan, J.T., Funk, W., Wright, W.E., Hu, J.-S., Kingston, R.E., and Baer, R. (1994). Preferred sequences for DNA recognition by the TAL1 helix-loop-helix proteins. Mol. Cell. Biol. 14, 1256-1265.
25. Hwang, L.-Y., Siegelman, M., Davis, L., Oppenheimer-Marks, N., and Baer, R. (1993). Expression of the TAL1 proto-oncogene in cultured endothelial cells and blood vessels of the spleen. Oncogene 8, 3043-3046.
26. Kallianpur, A.R., Jordan, J.E., and Brandt, S.J. (1994). The SCL/ TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83, 1200-1208.
27. Keller, G., Kennedy, M., Papayannopoulou, T., and Wiles, M.V. (1993). Hematopoietic differentiation during embryonic stem cell differentiation in culture. Mol. Cell Biol. 13, 472-486.
28. Larson, R.C., Lavenir, I., Larson, T.A., Baer, R., Warren, A.J., Wadman, I., Nottage, K., and Rabbits, T.H. (1996). Protein dimerization between Lmo2 (Rbtn2) and Tal1 alters thymocyte development and potentiates T cell tumorigenesis in transgenic mice. EMBO J. 15, 1021-1027.
29. Lecointe, N., Bernard, O., Naert, K., Joulin, V., Larsen, C.J., Romeo, P.H., and Mathieu-Mahul, D. (1994). GATA-and SP1-binding sites are required for the full activity of the tissue-specific promoter of the tal-1 gene. Oncogene 9, 2623-2632.
30. Lee, J.E., Hollenberg, S.M., Snider, L., Turner, D.L., Lipnick, N., and Weintraub, H. (1995). Conversion of Xenopus ectoderm into neurons by NeuroD, a basic-helix-loop-helix protein. Science 268, 836-844.
31. Mellentin, J.D., Smith, S.D., and Cleary, M.L. (1989). lyl-1, a novel gene altered by chromosomal translocation in T cell leukemia, codes for a protein with a helix-loop-helix DMA-binding motif. Cell 58, 77-83.
32. Miyoshi, H., Shimizu, K., Kozu, T., Maseki, N., Kaneko, Y., and Ohki, M. (1991). t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. USA 88, 10431-10434.
33. Mombaerts, P., Iacomini, J., Johnson, R.S., Herrup, K., Tonegawa, S., and Papaloannou, V.E. (1992). RAG-1-deficient mice have no mature B and T lymphocytes. Cell 68, 869-877.
34. Mortensen, R.M., Conner, D.A., Chao, S., Geisterfer-Lowrance, A.A.T., and Seidman, J.G. (1992). Production of homozygous mutant ES cells with a single targeting construct. Mol. Cell. Biol. 12, 2391-2395.
35. Mouthon, M.-A., Bernard, O., Mitjavila, M.-T., Romeo, P.-H., Vainchenker, W., and Mathieu-Mahul, D. (1993). Expression of tal-1 and GATA-binding proteins during human hematopoiesis. Blood 81, 647-655.
36. Mucenski, M.L., McLain, K., Kier, A.B., Swerdlow, S.H., Schreiner, C.M., Miller, T.A., Pietryga, D.W., Scott, W.J., Jr., and Potter, S.S. (1991 ). A functional c-myb gene is required for normal fetal hepatic hematopoiesis. Cell 65, 677-689.
37. Murre, C., McCaw, P.S., and Baltimore, D. (1989). A new DNA binding and dimerization motif in immunoglobin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56, 777-783.
38. Nucifora, G., Begy, C.R., Erickson, P., Drabkin, H.A., and Rowley, J.D. (1993). The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER 1. Proc. Natl. Acad. Sci. USA 90, 7784-7788.
39. Okuda, T., van Deursen, J., Hiebert, S.W., Grosveld, G., and Downing, J.R. (1996). AML1 ,the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84, 321-330.
40. Olson, E.N., and Klein, W.H. (1994). bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev. 8, 1-8.
41. Olson, E.N., Arnold, H.-H., Rigby, P.W.J., and Wold, B.J. (1996). Know your neighbors: three phenotypes in null mutants of the myogenic bHLH gene MRF4. Cell 85, 1-4.
42. Olson, M.C., Scott, E.W., Hack, A.A., Su, G.H., Tenen, D.G., Singh, H., and Simon, M.C. (1995). PU.1 is not essential for early myeloid gene expression but is required for terminal myeloid differentiation. Immunity 3, 703-714.
43. Orkin, S.H. (1995). Hematopoiesis: how does it happen? Curr. Opin. Cell Biol. 7, 870-877.
44. Osada, H., Grutz, G., Axelson, H., Forster, A., and Rabbitts, T.H. (1995). Association of erythroid transcription factors: complexes involving the LIM protein RBTN2 and the zinc-finger protein GATA1. Proc. Natl. Acad. Sci. USA 92, 9585-9589.
45. Pear, W.S., Scott, M.L., and Nolan, G.P. (1996). Generation of helper-free retroviruses by transient transfection. In Methods in Molecular Biology: Methods in Gene Therapy, P. Robbins, ed. (Tonawa, New Jersey: Humana Press), in press.
46. Pevny, L., Simon, M.C., Robertson, E., Klein, W.H., Tsai, S.-F., D'Agati, V., Orkin, S.H., and Costantini, F. (1991). Erythroid differentiation in chimeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349, 257-260.
47. Rabbits, T.H. (1994). Chromosomal translocations in human cancer. Nature 372, 143-149.
48. Robb, L., Lyons, I., Li, R., Hartley, L., Kontgen, F., Harvey, R.P., Metcalf, D., and Begley, G.G. (1995a). Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc. Natl. Acad. Sci. USA 92, 7075-7079.
49. Robb, L., Rasko, J.E.J., Bath, M.L., Strasser, A., and Begley, G.G. (1995b). sel, a gene frequently activated in human T cell leukemia, does not induce lymphomas in transgenic mice. Oncogene 10, 205-209.
50. Robertson, E.E. (1987). Teratocarcinomas and Embryonic Stem Cells: A Practical Approach (Washington, D.C.: IRL Press).
51. Romans, S.P., Mauchauffe, M., Leconiat, M., Chumakov, I., Le Pastier, D., Berger, R., and Bernard, O.A. (1995). The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85, 3662-3670.
52. Rowley, J.D. (1993). Rearrangements involving chromosome band 11Q23 in acute leukaemia. Semin. Cancer Biol. 4, 377-385.
53. Rudnicki, M.A., Schnegelsberg, P.N.J., Stead, R.H., Braun, T., Arnold, H.-H., and Jaenisch, R. (1993). MyoD or Myf-5 is required for the formation of skeletal muscle. Cell 75, 1351-1359.
54. Scott, E.W., Simon, M.C., Anastasi, J., and Singh, H. (1994). Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265, 1573-1577.
55. Shinkai, Y., Rathbun, G., Lam, K.P., Oltz, E.M., Stewart, V., Mendelsohn, M., Charron, J., Datta, M., Young, F., Stall, A.M., and Alt, F.W. (1992). RAG-2-deficient mice lack mature lymphocytes owing to inability to initiate V(D)J rearrangement. Cell 68, 855-867.
56. Shivdasani, R., Mayer, E., and Orkin, S.H. (1995). Absence of blood formation in mice lacking the T cell leukemia oncoprotein tal-1/SCL. Nature 373, 432-434.
57. Tanigawa, T., Elwood, N., Metcalf, D., Gary, D., DeLuca, E., Nicola, N.A., and Begley, G.G. (1993). The SCL gene product is regulated by and differentially regulates cytokines during myeloid leukemic cell differentiation. Proc. Natl. Acad. Sci. USA 90, 7864-7868.
58. Tkachuk, D.C., Kohler, S., and Clearly, M.L. (1992). Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell 71, 691-700.
59. Tsai, F.-Y., Keller, G., Kuo, F.C., Weiss, M.J., Chen, J.-Z., Rosenblatt, M., Alt, F., and Orkin, S.H. (1994). An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 377, 221-226.
60. Valge-Archer, V.E., Osada, H., Warren, A.J., Forster, A., Li, J., Baer, R., and Rabbitts, T.H. (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 97, 8617-8621.
61. Villares, R., and Cabrera, C.V. (1987). The achaete-scute gene complex of D. melanogaster: conserved domains in a subset of genes required for neurogenesis and their homology to myc. Cell 50, 415-424.
62. Visvader, J., Begley, C.G., and Adams, J.M. (1991). Differential expression of the LyI, SCL, and E2a helix-loop-helix genes within the hemopoietic system. Oncogene 6, 187-194.
63. Wadman, I., Li, J., Bash, R.O., Forster, A., Osada, H., Rabbitts, T.H., and Baer, R. (1994). Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO J. 73, 4831-4839.
64. Warren, A.J., Colledge, W.H., Carlton, M.B.L., Evans, M.J., Smith, A.J.H., and Rabbitts, T.H. (1994). The oncogenic cysteine-rich LIM domain protein Rbtn2 is essential for erythroid development. Cell 78, 45-57.
65. Weiss, M.J., Keller, G., and Orkin, S.H. (1994). Novel insights into erythroid development revealed through in vitro differentiation of GATA-1 embryonic stem cells. Genes Dev. 8, 1184-1197.
66. Whitney, J.B. (1978). Simplified typing of mouse hemoglobin (Hbb) phenotypes using cystamine. Biochem. Genet. 76, 667-672.
67. Wiles, M.V., and Keller, G. (1991). Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 777, 259-267.
68. Wong, P.M.C., Chung, S.W., Chui, D.H.K., and Eaves, C.J. (1986). Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murineyolk sac. Proc. Natl. Acad. Sci. USA 83, 3851-3854.
69. Yu, B.D., Hess, J.L., Horning, S.E., Brown, G.A.J., and Korsmeyer, S.J. (1995). Altered Hox expression and segmental identity in MII-mutant mice. Nature 378, 505-508.