Both TEL and AML-1 contribute repression domains to the t(12;21) fusion protein

Molecular and Cellular Biology

Volumn 19, Issue 10, 1999, Pages 6566-6574

  Fenrick, Randy ^a,b   Amann, Joseph M ^a,b   Lutterbach, Bart ^a,b   Wang, Lilin ^a,b   Westendorf, Jennifer J ^a,b   Downing, James R ^c   Hiebert, Scott W ^a,b  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VANDERBILT INGRAM CANCER CENTER   (United States)

^c ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA BINDING PROTEIN; HYBRID PROTEIN; TRANSCRIPTION FACTOR;

ACUTE LYMPHOBLASTIC LEUKEMIA; ANIMAL CELL; ARTICLE; B CELL LEUKEMIA; CHROMOSOME TRANSLOCATION 12; CHROMOSOME TRANSLOCATION 21; GENE DELETION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN STRUCTURE; TRANSCRIPTION REGULATION;

ANIMALIA;

EID: 0032873462     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.10.6566     Document Type: Article

References (73)

1. Agape, P., B. Gerard, H. Cave, I. Devaux, E. Vilmer, M. C. Lecomte, and B. Grandchamp. 1997. Analysis of ETV6 and ETV6-AML1 proteins in acute lymphoblastic leukaemia. Br. J. Haematol. 98:234-239.
2. Alland, L., R. Muhle, H. Hou, Jr., J. Potes, L. Chin, N. Schreiber-Agus, and R. A. DePinho. 1997. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 387:49-55.
3. Andreasson, P., B. Johansson, K. Arheden, R. Billstrom, F. Mitelman, and M. Hoglund. 1997. Deletions of CDKN1B and ETV6 in acute myeloid leukemia and myelodysplastic syndromes without cytogenetic evidence of 12p abnormalities. Genes Chromosomes Cancer 19:77-83.
4. Aronson, B. D., A. L. Fisher, K. Blechman, M. Caudy, and J. P. Gergen. 1997. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol. Cell. Biol. 17:5581-5587.
5. Ayer, D. E., Q. A. Lawrence, and R. N. Eisenman. 1995. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 80:767-776.
6. Baccichet, A., and D. Sinnett. 1997. Frequent deletion of chromosome 12p12.3 in children with acute lymphoblastic leukaemia. Br. J. Haematol. 99:107-114.
7. Bae, S. C., E. Ogawa, M. Maruyama, H. Oka, M. Satake, K. Shigesada, N. A. Jenkins, D. J. Gilbert, N. G. Copeland, and Y. Ito. 1993. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. EMBO J. 13:3324-3339.
8. Berger, J., J. Hauber, R. Hauber, R. Geiger, and B. R. Cullen. 1988. Secreted placental alkaline phosphatase: a powerful new quantitative indicator of gene expression in eukaryotic cells. Gene 66:1-10.
9. Bernard, O. A., S. P. Romana, H. Poirel, and R. Berger. 1996. Molecular cytogenetics of t(12;21) (p13;q22). Leukemia Lymphoma 23:459-465.
10. Borras, F. E., J. Lloberas, R. A. Maki, and A. Celada. 1995. Repression of I-A beta gene expression by the transcription factor PU.1. J. Biol. Chem. 270:24385-24391.
11. Caligiuri, M. A., M. P. Strout, and D. G. Gilliland. 1997. Molecular biology of acute myeloid leukemia. Semin. Oncol. 24:32-44.
12. Carroll, M., M. H. Tomasson, G. F. Barker, T. R. Golub, and D. G. Gilliland. 1996. The TEL/platelet-derived growth factor beta receptor (PDGF beta R) fusion in chronic myelomonocytic leukemia is a transforming protein that self-associates and activates PDGF beta R kinase-dependent signaling pathways. Proc. Natl. Acad. Sci. USA 93:14845-14850.
13. Cave, H., V. Cacheux, S. Raynaud, G. Brunie, M. Bakkus, P. Cochaux, C. Preudhomme, J. L. Lai, E. Vilmer, and B. Grandchamp. 1997. ETV6 is the target of chromosome 12p deletions in t(12;21) childhood acute lymphocytic leukemia. Leukemia 11:1459-1464.
14. Cullen, B. R. 1987. Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol. 152:684-703.
15. Darby, T. G., J. D. Meissner, A. Ruhlmann, W. H. Mueller, and R. J. Scheibe. 1997. Functional interference between retinoic acid or steroid hormone receptors and the oncoprotein Fli-1. Oncogene 15:3067-3082.
16. el Deiry, W. S., T. Tokino, V. E. Velculescu, D. B. Levy, R. Parsons, J. M. Trent, D. Lin, W. E. Mercer, K. W. Kinzler, and B. Vogelstein. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817-825.
17. Fears, S., M. Gavin, D. E. Zhang, C. Hetherington, V. Ben-David, J. D. Rowley, and G. Nucifora. 1997. Functional characterization of ETV6 and ETV6/CBFA2 in the regulation of the MCSFR proximal promoter. Proc. Natl. Acad. Sci. USA 94:1949-1954.
18. Gamou, T., E. Kitamura, F. Hosoda, K. Shimizu, K. Shinohara, Y. Hayashi, T. Nagase, Y. Yokoyama, and M. Ohki. 1998. The partner gene of AML1 in t(16;21) myeloid malignancies is a novel member of the MTG8(ETO) family. Blood 91:4028-4037.
19. Goldberg, Y., M. Treier, J. Ghysdael, and D. Bohmann. 1994. Repression of AP-1-stimulated transcription by c-Ets-1. J. Biol. Chem. 269:16566-16573.
20. Golub, T. R., G. F. Barker, S. K. Bohlander, S. W. Hiebert, D. C. Ward, P. Bray-Ward, E. Morgan, S. C. Raimondi, J. D. Rowley, and D. G. Gilliland. 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.
21. Golub, T. R., G. F. Barker, M. Lovett, and D. G. Gilliland. 1994. Fusion of PDGF receptor beta to a novel ets-like gene, tel, in chronic myelomonocytic leukemia with t(5;12) chromosomal translocation. Cell 77:307-316.
22. Golub, T. R., A. Goga, G. F. Barker, D. E. Afar, J. McLaughlin, S. K. Bohlander, J. D. Rowley, O. N. Witte, and D. G. Gilliland. 1996. Oligomerization of the ABL tyrosine kinase by the Ets protein TEL in human leukemia. Mol. Cell. Biol. 16:4107-4116.
23. Golub, T. R., T. McLean, K. Stegmaier, M. Carroll, M. Tomasson, and D. G. Gilliland. 1996. The TEL gene and human leukemia. Biochim. Biophys. Acta 1288:M7-M10. (Review.)
24. Gorman, C. M., L. F. Moffat, and B. H. Howard. 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044-1051.
25. Hassig, C. A., T. C. Fleischer, A. N. Billin, S. L. Schreiber, and D. E. Ayer. 1997. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 89:341-347.
26. Heinzel, T., R. M. Lavinsky, T. M. Mullen, M. Soderstrom, C. D. Laherty, J. Torchia, W. M. Yang, G. Brard, S. D. Ngo, J. R. Davie, E. Seto, R. N. Eisenman, D. W. Rose, C. K. Glass, and M. G. Rosenfeld. 1997. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387:43-48.
27. Hiebert, S. W., W. Sun, J. N. Davis, T. Golub, S. Shurtleff, A. Buijs, J. R. Downing, G. Grosveld, M. F. Roussell, D. G. Gilliland, N. Lenny, and S. Meyers. 1996. The t(12;21) translocation converts AML-1B from an activator to a repressor of transcription. Mol. Cell. Biol. 16:1349-1355.
28. Horton, R. M., S. N. Ho, J. K. Pullen, H. D. Hunt, Z. Cai, and L. R. Pease. 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270-279.
29. Kadosh, D., and K. Struhl. 1997. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365-371.
30. Kitabayashi, I., A. Yokoyama, K. Shimizu, and M. Ohki. 1998. Interaction and functional cooperation of the leukemia-associated factors AML1 and p300 in myeloid cell differentiation. EMBO J. 17:2994-3004.
31. Knezevich, S. R., M. J. Garnett, T. J. Pysher, J. B. Beckwith, P. E. Grundy, and P. H. Sorensen. 1998. ETV6-NTRK3 gene fusions and trisomy 11 establish a histogenetic link between mesoblastic nephroma and congenital fibrosarcoma. Cancer Res. 58:5046-5048.
32. Kodadek, T. 1993. How does the GAL4 transcription factor recognize the appropriate DNA binding sites in vivo? Cell. Mol. Biol. Res. 39:355-360.
33. Kozu, T., H. Miyoshi, K. Shimizu, N. Maseki, Y. Kaneko, H. Asou, N. Kamada, and M. Ohki. 1995. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85:3662-3670.
34. Kwiatkowski, B. A., L. S. Bastian, T. R. Bauer, Jr., S. Tsai, A. G. Zielinska-Kwiatkowska, and D. D. Hickstein. 1998. The ets family member Tel binds to the Fli-1 oncoprotein and inhibits its transcriptional activity. J. Biol. Chem. 273:17525-17530.
35. Lacronique, V., A. Boureux, V. Della Valle, H. Poirel, C. T. Quang, M. Mauchauffe, C. Berthou, M. Lessard, R. Berger, J. Ghysdael, and O. A. Bernard. 1997. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science 278:1309-1312.
36. Laherty, C. D., W. M. Yang, J. M. Sun, J. R. Davie, E. Seto, and R. N. Eisenman. 1997. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89:349-356.
37. Lenny, N., J. J. Westendorf, and S. W. Hiebert. 1997. Transcriptional regulation during myelopoiesis. Mol. Biol. Rep. 24:157-168. (Review.)
38. Levanon, D., R. E. Goldstein, Y. Bernstein, H. Tang, D. Goldenberg, S. Stifani, Z. Paroush, and Y. Groner. 1998. Transcriptional repression by AML1 and LEF-1 is mediated by the TEL/Groucho corepressors. Proc. Natl. Acad. Sci. USA 95:11590-11595.
39. Liu, P., S. A. Tarle, A. Hajra, D. F. Claxton, P. Marlton, M. Freedman, M. J. Siciliano, and F. S. Collins. 1993. Fusion between transcription factor CBF beta/PEBP2 beta and a myosin heavy chain in acute myeloid leukemia. Science 261:1041-1044.
40. Look, A. T. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278:1059-1064.
41. Lutterbach, B. 1999. Unpublished data.
42. Lutterbach, B., J. J. Westendorf, B. Linggi, A. Patten, M. Moniwa, J. R. Davie, K. D. Huynh, V. J. Bardwell, R. M. Lavinsky, C. K. Glass, M. G. Rosenfeld, E. Seto, and S. W. Hiebert. 1998. ETO, a target of the t(8;21) in acute leukemia, interacts with N-CoR, mSin3, and histone deacetylases. Mol. Cell. Biol. 18:7176-7184.
43. Lutterbach, B., J. J. Westendorf, B. Linggi, E. Seto, and S. W. Hiebert. AML-1, a target of multiple chromosomal translocations in acute leukemia, interacts with mSin3 and represses transcription from the p21Waf1/Cip1 promoter. Submitted for publication.
44. McLean, T. W., S. Ringold, D. Neuberg, K. Stegmaier, R. Tantravahi, J. Ritz, H. P. Koeffler, S. Takeuchi, J. W. Janssen, T. Seriu, C. R. Bartram, S. E. Sallan, D. G. Gilliland, and T. R. Golub. 1996. TEL/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood 88:4252-4258.
45. Meyers, S., N. Lenny, and S. W. Hiebert. 1995. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974-1982.
46. Miyamoto, T., K. Nagafuji, K. Akashi, M. Harada, T. Kyo, T. Akashi, K. Takenaka, S. Mizuno, H. Gondo, T. Okamura, H. Dohy, and Y. Niho. 1996. Persistence of multipotent progenitors expressing AML1/ETO transcripts in long-term remission patients with t(8;21) acute myelogenous leukemia. Blood 87:4789-4796.
47. Miyoshi, H., T. Kozu, K. Shimizu, K. Enomoto, N. Maseki, Y. Kaneko, N. Kamada, and M. Ohki. 1993. The t(8;21) translocation in acute myeloid leukemia results in production of an AML1-MTG8 fusion transcript. EMBO J. 12:2715-2721.
48. Nagy, L., H. Y. Kao, D. Chakravarti, R. J. Lin, C. A. Hassig, D. E. Ayer, S. L. Schreiber, and R. M. Evans. 1997. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89:373-380.
49. Nozaki, M., Y. Onishi, N. Kanno, Y. Ono, and Y. Fujimura. 1996. Molecular cloning of Elk-3, a new member of the Ets family expressed during mouse embryogenesis and analysis of its transcriptional repression activity. DNA Cell Biol. 15:855-862.
50. Nucifora, G., C. R. Begy, P. Erickson, H. A. Drabkin, and J. D. Rowley. 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 90:7784-8.
51. Poirel, H., V. Lacronique, M. Mauchauffe, M. Le Coniat, E. Raffoux, M. T. Daniel, P. Erickson, H. Drabkin, R. A. MacLeod, H. G. Drexler, J. Ghysdael, R. Berger, and O. A. Bernard. 1998. Analysis of TEL proteins in human leukemias. Oncogene 16:2895-2903.
52. Raynaud, S., H. Cave, M. Baens, C. Bastard, V. Cacheux, J. Grosgeorge, C. Guidal-Giroux, C. Guo, E. Vilmer, P. Marynen, and B. Grandchamp. 1996. The 12;21 translocation involving TEL and deletion of the other TEL allele: two frequently associated alterations found in childhood acute lymphoblastic leukemia. Blood 87:2891-2899.
53. Romana, S. P., M. Le Coniat, H. Poirel, P. Marynen, O. Bernard, and R. Berger. 1996. Deletion of the short arm of chromosome 12 is a secondary event in acute lymphoblastic leukemia with t(12;21). Leukemia 10:167-170.
54. Romana, S. P., M. Mauchauffe, M. Le Coniat, I. Chumakov, D. Le Paslier, R. Berger, and O. A. Bernard. 1995. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85:3662-3670.
55. Romana, S. P., H. Poirel, M. Leconiat, M. A. Flexor, M. Mauchauffe, P. Jonveaux, E. A. Macintyre, R. Berger, and O. A. Bernard. 1995. High frequency of t(12;21) in childhood B-lineage acute lymphoblastic leukemia. Blood 86:4263-4269.
56. Rubin, C. M., R. A. Larson, J. Anastasi, J. N. Winter, M. Thangavelu, J. W. Vardiman, J. D. Rowley, and M. M. LeBeau. 1990. t(3;21)(q26;q22) translocation: a recurring chromosomal abnormality in therapy-related myelodysplastic syndrome and acute myeloid leukemia. Blood 76:2594-2598.
57. Rubnitz, J. E., and C. H. Pui. 1997. Recent advances in the biology and treatment of childhood acute lymphoblastic leukemia. Curr. Opin. Hematol. 4:233-241.
58. Seth, A., and T. S. Papas. 1990. The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene 5:1761-1767.
59. Sgouras, D. N., M. A. Athanasiou, G. J. Beal, Jr., R. J. Fisher, D. G. Blair, and G. J. Mavrothalassitis. 1985. ERF: an ETS domain protein with strong transcriptional repressor activity, can suppress ets-associated tumorigenesis and is regulated by phosphorylation during cell cycle and mitogenic stimulation. Dev. Biol. 109:321-335.
60. Shibata, H., Z. Nawaz, S. Y. Tsai, B. W. O'Malley, and M. J. Tsai. 1997. Gene silencing by chicken ovalbumin upstream promoter-transcription factor I (COUP-TF1) is mediated by transcriptional corepressors, nuclear receptor-corepressor (N-CoR) and silencing mediator for retinoic acid recep7 tor and thyroid hormone receptor (SMRT). Mol. Endocrinol. 11:714-724.
61. Shurtleff, S. A., A. Buijs, F. G. Behm, J. E. Rubnitz, S. C. Raimondi, M. L. Hancock, G. C. Chan, C. H. Pui, G. Grosveld, and J. R. Downing. 1995. TEL/AML1 fusion resulting from a cryptic t(12;21) is the most common genetic lesion in pediatric ALL and defines a subgroup of patients with an excellent prognosis. Leukemia 9:1985-1989.
62. Sommer, A., S. Hilfenhaus, A. Menkel, E. Kremmer, C. Seiser, P. Loidl, and B. Luscher. 1997. Cell growth inhibition by the Mad/Max complex through recruitment of histone deacetylase activity. Curr. Biol. 7:357-365.
63. Stegmaier, K., S. Pendse, G. F. Barker, P. Bray-Ward, D. C. Ward, K. T. Montgomery, K. S. Krauter, C. Reynolds, J. Sklar, M. Donnelly, et al. 1995. Frequent loss of heterozygosity at the TEL gene locus in acute lymphoblastic leukemia of childhood. Blood 86:38-44.
64. Strom, O. K., J. L. Cleveland, S. Chellappan, J. Nip, and S. W. Hiebert. 1998. E2F-1 and E2F-3 are functionally distinct in their ability to promote myeloid cell cycle progression and block granulocyte differentiation. Cell Growth Differ. 9:59-69.
65. Takeuchi, S., T. Serra, C. R. Bartram, T. R. Golub, A. Reiter, I. Miyoshi, D. G. Gilliland, and H. P. Koeffler. 1997. TEL is one of the targets for deletion on 12p in many cases of childhood B-lineage acute lymphoblastic leukemia. Leukemia 11:1220-1223.
66. Uchida, H., J. R. Downing, Y. Miyazaki, R. Frank, J. Zhang, and S. D. Nimer. 1999. Three distinct domains in TEL-AML1 are required for transcriptional repression of the IL-3 promoter. Oncogene 18:1015-1022.
67. Wang, S., Q. Wang, B. E. Crute, I. N. Melnikova, S. R. Keller, and N. A. Speck. 1993. Cloning and characterization of subunits of the T-cell receptor and murine leukemia virus enhancer core-binding factor. Mol. Cell. Biol. 13:3324-3339.
68. Wasylyk, B., J. Hagman, and A. Gutierrez-Hartmann. 1998. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 23:213-216.
69. Watson, D. K., R. Ascione, and T. S. Papas. 1990. Molecular analysis of the ets genes and their products. Crit. Rev. Oncog. 1:409-436.
70. Westendorf, J. J., C. M. Yamamoto, N. Lenny, J. R. Downing, M. E. Selsted, and S. W. Hiebert. 1998. The t(8;21) fusion product, AML-1-ETO, associates with C/EBP-α, inhibits C/EBP-α-dependent transcription, and blocks granulocyte differentiation. Mol. Cell. Biol. 18:322-333.
71. Wlodarska, I., M. Baens, P. Peeters, J. Aerssens, C. Mecucci, P. Brock, P. Marynen, and H. Van den Berghe. 1996. Biallelic alterations of both ETV6 and CDKN1B genes in a t(12;21) childhood acute lymphoblastic leukemia case. Cancer Res. 56:2655-2661.
72. Wong, J., D. Patterton, A. Imhof, D. Guschin, Y. B. Shi, and A. P. Wolffe. 1998. Distinct requirements for chromatin assembly in transcriptional repression by thyroid hormone receptor and histone deacetylase. EMBO J. 17:520-534.
73. Zhang, Y., and M. G. Lichtenheld. 1997. Non-killer cell-specific transcription factors silence the perform promoter. J. Immunol. 158:1734-1741.