Both TEL and AML-1 Contribute Repression Domains to the t(12;21) Fusion Protein

REFERENCES

• Agape, P., B. Gerard, H. Cave, I. Devaux, E. Vilmer, M. C. Lecomte, and J. Grandchamp 1997. Analysis of ETV6 and ETV6-AML1 proteins in acute lymphoblastic leukaemia. Br. J. Haematol. 98:234–239.
   PubMed Web of Science ®Google Scholar
• Alland, L., R. Muhle, H. Hou Jr., J. Potes, L. Chin, N. Schreiber-Agus, and J. DePinho 1997. Role for N-CoR and histone deacetylase in Sin3-mediated transcriptional repression. Nature 387:49–55.
   PubMed Web of Science ®Google Scholar
• Andreasson, P., B. Johansson, K. Arheden, R. Billstrom, F. Mitelman, and J. 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.
   PubMed Web of Science ®Google Scholar
• Aronson, B. D., A. L. Fisher, K. Blechman, M. Caudy, and J. Gergen 1997. Groucho-dependent and -independent repression activities of Runt domain proteins. Mol. Cell. Biol. 17:5581–5587.
   PubMed Web of Science ®Google Scholar
• Ayer, D. E., Q. A. Lawrence, and J. Eisenman 1995. Mad-Max transcriptional repression is mediated by ternary complex formation with mammalian homologs of yeast repressor Sin3. Cell 80:767–776.
   PubMed Web of Science ®Google Scholar
• Baccichet, A., and J. Sinnett 1997. Frequent deletion of chromosome 12p12.3 in children with acute lymphoblastic leukaemia. Br. J. Haematol. 99:107–114.
   PubMed Web of Science ®Google Scholar
• Bae, S. C., E. Ogawa, M. Maruyama, H. Oka, M. Satake, K. Shigesada, N. A. Jenkins, D. J. Gilbert, N. G. Copeland, and J. 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.
   Google Scholar
• Berger, J., J. Hauber, R. Hauber, R. Geiger, and J. Cullen 1988. Secreted placental alkaline phosphatase: a powerful new quantitative indicator of gene expression in eukaryotic cells. Gene 66:1–10.
   PubMed Web of Science ®Google Scholar
• Bernard, O. A., S. P. Romana, H. Poirel, and J. Berger 1996. Molecular cytogenetics of t(12;21) (p13;q22). Leukemia Lymphoma 23:459–465.
   PubMed Web of Science ®Google Scholar
• Borras, F. E., J. Lloberas, R. A. Maki, and J. Celada 1995. Repression of I-A beta gene expression by the transcription factor PU.1. J. Biol. Chem. 270:24385–24391.
   PubMedGoogle Scholar
• Caligiuri, M. A., M. P. Strout, and J. Gilliland 1997. Molecular biology of acute myeloid leukemia. Semin. Oncol. 24:32–44.
   PubMed Web of Science ®Google Scholar
• Carroll, M., M. H. Tomasson, G. F. Barker, T. R. Golub, and J. 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.
   PubMed Web of Science ®Google Scholar
• Cave, H., V. Cacheux, S. Raynaud, G. Brunie, M. Bakkus, P. Cochaux, C. Preudhomme, J. L. Lai, E. Vilmer, and J. Grandchamp 1997. ETV6 is the target of chromosome 12p deletions in t(12;21) childhood acute lymphocytic leukemia. Leukemia 11:1459–1464.
   PubMed Web of Science ®Google Scholar
• Cullen, B. R. 1987. Use of eukaryotic expression technology in the functional analysis of cloned genes. Methods Enzymol. 152:684–703.
   PubMed Web of Science ®Google Scholar
• Darby, T. G., J. D. Meissner, A. Ruhlmann, W. H. Mueller, and J. Scheibe 1997. Functional interference between retinoic acid or steroid hormone receptors and the oncoprotein Fli-1. Oncogene 15:3067–3082.
   PubMedGoogle Scholar
• 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 J. Vogelstein 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75:817–825.
   PubMed Web of Science ®Google Scholar
• Fears, S., M. Gavin, D. E. Zhang, C. Hetherington, Y. Ben-David, J. D. Rowley, and J. 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.
   PubMed Web of Science ®Google Scholar
• Gamou, T., E. Kitamura, F. Hosoda, K. Shimizu, K. Shinohara, Y. Hayashi, T. Nagase, Y. Yokoyama, and J. 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.
   PubMed Web of Science ®Google Scholar
• Goldberg, Y., M. Treier, J. Ghysdael, and J. Bohmann 1994. Repression of AP-1-stimulated transcription by c-Ets-1. J. Biol. Chem. 269:16566–16573.
   PubMedGoogle Scholar
• 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 J. 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.
   PubMed Web of Science ®Google Scholar
• Golub, T. R., G. F. Barker, M. Lovett, and J. 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.
   PubMed Web of Science ®Google Scholar
• Golub, T. R., A. Goga, G. F. Barker, D. E. Afar, J. McLaughlin, S. K. Bohlander, J. D. Rowley, O. N. Witte, and J. Gilliland 1996. Oligomerization of the ABL tyrosine kinase by the Ets protein TEL in human leukemia. Mol. Cell. Biol. 16:4107–4116.
   PubMed Web of Science ®Google Scholar
• Golub, T. R., T. McLean, K. Stegmaier, M. Carroll, M. Tomasson, and J. Gilliland 1996. The TEL gene and human leukemia. Biochim. Biophys. Acta 1288:M7–M10 (Review.)
   PubMed Web of Science ®Google Scholar
• Gorman, C. M., L. F. Moffat, and J. Howard 1982. Recombinant genomes which express chloramphenicol acetyltransferase in mammalian cells. Mol. Cell. Biol. 2:1044–1051.
   PubMed Web of Science ®Google Scholar
• Hassig, C. A., T. C. Fleischer, A. N. Billin, S. L. Schreiber, and J. Ayer 1997. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 89:341–347.
   PubMed Web of Science ®Google Scholar
• 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 J. Rosenfeld 1997. A complex containing N-CoR, mSin3 and histone deacetylase mediates transcriptional repression. Nature 387:43–48.
   PubMed Web of Science ®Google Scholar
• 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 J. Meyers 1996. The t(12;21) translocation converts AML-1B from an activator to a repressor of transcription. Mol. Cell. Biol. 16:1349–1355.
   PubMed Web of Science ®Google Scholar
• Horton, R. M., S. N. Ho, J. K. Pullen, H. D. Hunt, Z. Cai, and J. Pease 1993. Gene splicing by overlap extension. Methods Enzymol. 217:270–279.
   PubMed Web of Science ®Google Scholar
• Kadosh, D., and J. Struhl 1997. Repression by Ume6 involves recruitment of a complex containing Sin3 corepressor and Rpd3 histone deacetylase to target promoters. Cell 89:365–371.
   PubMed Web of Science ®Google Scholar
• Kitabayashi, I., A. Yokoyama, K. Shimizu, and J. Ohki 1998. Interaction and functional cooperation of the leukemia-associated factors AML1 and p300 in myeloid cell differentiation. EMBO J. 17:2994–3004.
   PubMedGoogle Scholar
• Knezevich, S. R., M. J. Garnett, T. J. Pysher, J. B. Beckwith, P. E. Grundy, and J. Sorensen 1998. ETV6-NTRK3 gene fusions and trisomy 11 establish a histogenetic link between mesoblastic nephroma and congenital fibrosarcoma. Cancer Res. 58:5046–5048.
   PubMed Web of Science ®Google Scholar
• Kodadek, T. 1993. How does the GAL4 transcription factor recognize the appropriate DNA binding sites in vivo? Cell. Mol. Biol. Res. 39:355–360.
   PubMedGoogle Scholar
• Kozu, T., H. Miyoshi, K. Shimizu, N. Maseki, Y. Kaneko, H. Asou, N. Kamada, and J. Ohki 1995. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85:3662–3670.
   PubMedGoogle Scholar
• Kwiatkowski, B. A., L. S. Bastian, T. R. Bauer Jr., S. Tsai, A. G. Zielinska-Kwiatkowska, and J. Hickstein 1998. The ets family member Tel binds to the Fli-1 oncoprotein and inhibits its transcriptional activity. J. Biol. Chem. 273:17525–17530.
   PubMed Web of Science ®Google Scholar
• Lacronique, V., A. Boureux, V. Della Valle, H. Poirel, C. T. Quang, M. Mauchauffe, C. Berthou, M. Lessard, R. Berger, J. Ghysdael, and J. Bernard 1997. A TEL-JAK2 fusion protein with constitutive kinase activity in human leukemia. Science 278:1309–1312.
   PubMed Web of Science ®Google Scholar
• Laherty, C. D., W. M. Yang, J. M. Sun, J. R. Davie, E. Seto, and J. Eisenman 1997. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 89:349–356.
   PubMed Web of Science ®Google Scholar
• Lenny, N., J. J. Westendorf, and J. Hiebert 1997. Transcriptional regulation during myelopoiesis. Mol. Biol. Rep. 24:157–168 (Review.)
   PubMed Web of Science ®Google Scholar
• Levanon, D., R. E. Goldstein, Y. Bernstein, H. Tang, D. Goldenberg, S. Stifani, Z. Paroush, and J. Groner 1998. Transcriptional repression by AML1 and LEF-1 is mediated by the TEL/Groucho corepressors. Proc. Natl. Acad. Sci. USA 95:11590–11595.
   PubMed Web of Science ®Google Scholar
• Liu, P., S. A. Tarle, A. Hajra, D. F. Claxton, P. Marlton, M. Freedman, M. J. Siciliano, and J. Collins 1993. Fusion between transcription factor CBF beta/PEBP2 beta and a myosin heavy chain in acute myeloid leukemia. Science 261:1041–1044.
   PubMed Web of Science ®Google Scholar
• Look, A. T. 1997. Oncogenic transcription factors in the human acute leukemias. Science 278:1059–1064.
   PubMed Web of Science ®Google Scholar
• Lutterbach, B. 1999. Unpublished data.
   Google Scholar
• 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 J. 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.
   PubMed Web of Science ®Google Scholar
• 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.
   Google Scholar
• 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 J. Golub 1996. TEL/AML-1 dimerizes and is associated with a favorable outcome in childhood acute lymphoblastic leukemia. Blood 88:4252–4258.
   PubMed Web of Science ®Google Scholar
• Meyers, S., N. Lenny, and J. Hiebert 1995. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974–1982.
   PubMed Web of Science ®Google Scholar
• Miyamoto, T., K. Nagafuji, K. Akashi, M. Harada, T. Kyo, T. Akashi, K. Takenaka, S. Mizuno, H. Gondo, T. Okamura, H. Dohy, and J. 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.
   PubMed Web of Science ®Google Scholar
• Miyoshi, H., T. Kozu, K. Shimizu, K. Enomoto, N. Maseki, Y. Kaneko, N. Kamada, and J. 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.
   PubMed Web of Science ®Google Scholar
• Nagy, L., H. Y. Kao, D. Chakravarti, R. J. Lin, C. A. Hassig, D. E. Ayer, S. L. Schreiber, and J. Evans 1997. Nuclear receptor repression mediated by a complex containing SMRT, mSin3A, and histone deacetylase. Cell 89:373–380.
   PubMed Web of Science ®Google Scholar
• Nozaki, M., Y. Onishi, N. Kanno, Y. Ono, and J. 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.
   PubMedGoogle Scholar
• Nucifora, G., C. R. Begy, P. Erickson, H. A. Drabkin, and J. 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.
   PubMed Web of Science ®Google Scholar
• 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 J. Bernard 1998. Analysis of TEL proteins in human leukemias. Oncogene 16:2895–2903.
   PubMed Web of Science ®Google Scholar
• Raynaud, S., H. Cave, M. Baens, C. Bastard, V. Cacheux, J. Grosgeorge, C. Guidal-Giroux, C. Guo, E. Vilmer, P. Marynen, and J. 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.
   PubMed Web of Science ®Google Scholar
• Romana, S. P., M. Le Coniat, H. Poirel, P. Marynen, O. Bernard, and J. 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.
   PubMed Web of Science ®Google Scholar
• Romana, S. P., M. Mauchauffe, M. Le Coniat, I. Chumakov, D. Le Paslier, R. Berger, and J. Bernard 1995. The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85:3662–3670.
   PubMed Web of Science ®Google Scholar
• Romana, S. P., H. Poirel, M. Leconiat, M. A. Flexor, M. Mauchauffe, P. Jonveaux, E. A. Macintyre, R. Berger, and J. Bernard 1995. High frequency of t(12;21) in childhood B-lineage acute lymphoblastic leukemia. Blood 86:4263–4269.
   PubMed Web of Science ®Google Scholar
• Rubin, C. M., R. A. Larson, J. Anastasi, J. N. Winter, M. Thangavelu, J. W. Vardiman, J. D. Rowley, and J. 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.
   PubMed Web of Science ®Google Scholar
• Rubnitz, J. E., and J. Pui 1997. Recent advances in the biology and treatment of childhood acute lymphoblastic leukemia. Curr. Opin. Hematol. 4:233–241.
   PubMedGoogle Scholar
• Seth, A., and J. Papas 1990. The c-ets-1 proto-oncogene has oncogenic activity and is positively autoregulated. Oncogene 5:1761–1767.
   PubMed Web of Science ®Google Scholar
• Sgouras, D. N., M. A. Athanasiou, G. J. Beal Jr., R. J. Fisher, D. G. Blair, and 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.
   PubMedGoogle Scholar
• Shibata, H., Z. Nawaz, S. Y. Tsai, B. W. O’Malley, and J. Tsai 1997. Gene silencing by chicken ovalbumin upstream promoter-transcription factor I (COUP-TFI) is mediated by transcriptional corepressors, nuclear receptor-corepressor (N-CoR) and silencing mediator for retinoic acid receptor and thyroid hormone receptor (SMRT). Mol. Endocrinol. 11:714–724.
   PubMedGoogle Scholar
• 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. 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.
   PubMed Web of Science ®Google Scholar
• Sommer, A., S. Hilfenhaus, A. Menkel, E. Kremmer, C. Seiser, P. Loidl, and J. Luscher 1997. Cell growth inhibition by the Mad/Max complex through recruitment of histone deacetylase activity. Curr. Biol. 7:357–365.
   PubMed Web of Science ®Google Scholar
• 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.
   PubMed Web of Science ®Google Scholar
• Strom, D. K., J. L. Cleveland, S. Chellappan, J. Nip, and J. 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.
   PubMedGoogle Scholar
• Takeuchi, S., T. Seriu, C. R. Bartram, T. R. Golub, A. Reiter, I. Miyoshi, D. G. Gilliland, and J. 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.
   PubMed Web of Science ®Google Scholar
• Uchida, H., J. R. Downing, Y. Miyazaki, R. Frank, J. Zhang, and J. Nimer 1999. Three distinct domains in TEL-AML1 are required for transcriptional repression of the IL-3 promoter. Oncogene 18:1015–1022.
   PubMed Web of Science ®Google Scholar
• Wang, S., Q. Wang, B. E. Crute, I. N. Melnikova, S. R. Keller, and J. 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.
   PubMed Web of Science ®Google Scholar
• Wasylyk, B., J. Hagman, and J. Gutierrez-Hartmann 1998. Ets transcription factors: nuclear effectors of the Ras-MAP-kinase signaling pathway. Trends Biochem. Sci. 23:213–216.
   PubMed Web of Science ®Google Scholar
• Watson, D. K., R. Ascione, and J. Papas 1990. Molecular analysis of the ets genes and their products. Crit. Rev. Oncog. 1:409–436.
   PubMedGoogle Scholar
• Westendorf, J. J., C. M. Yamamoto, N. Lenny, J. R. Downing, M. E. Selsted, and J. 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.
   PubMed Web of Science ®Google Scholar
• Wlodarska, I., M. Baens, P. Peeters, J. Aerssens, C. Mecucci, P. Brock, P. Marynen, and J. 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.
   PubMedGoogle Scholar
• Wong, J., D. Patterton, A. Imhof, D. Guschin, Y. B. Shi, and J. Wolffe 1998. Distinct requirements for chromatin assembly in transcriptional repression by thyroid hormone receptor and histone deacetylase. EMBO J. 17:520–534.
   PubMedGoogle Scholar
• Zhang, Y., and J. Lichtenheld 1997. Non-killer cell-specific transcription factors silence the perforin promoter. J. Immunol. 158:1734–1741.
   PubMedGoogle Scholar