Multivalent binding of the ETO corepressor to E proteins facilitates dual repression controls targeting chromatin and the basal transcription machinery

Molecular and Cellular Biology

Volumn 29, Issue 10, 2009, Pages 2644-2657

  Guo, Chun ^a   Hu, Qiande ^a   Yan, Chunxia ^a,b   Zhang, Jinsong ^a  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b MEDICAL SCHOOL OF XI AN JIAOTONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

E PROTEIN; HISTONE DEACETYLASE; HYBRID PROTEIN; PROTEIN; PROTEIN ETO; PROTEIN P300; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG; BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; ONCOPROTEIN; REPRESSOR PROTEIN; RUNX1 PROTEIN, HUMAN; RUNX1T1 PROTEIN, HUMAN; TRANSCRIPTION FACTOR;

ARTICLE; CHROMATIN; GENE REPRESSION; GENE SILENCING; GENETIC TRANSCRIPTION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; SIGNAL TRANSDUCTION; ANIMAL; CELL LINE; CHEMICAL STRUCTURE; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN BINDING;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL LINE; CHROMATIN; CORE BINDING FACTOR ALPHA 2 SUBUNIT; GENE EXPRESSION REGULATION; HUMANS; MODELS, MOLECULAR; PROTEIN BINDING; PROTO-ONCOGENE PROTEINS; RECOMBINANT FUSION PROTEINS; REPRESSOR PROTEINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 66349117082     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00073-09     Document Type: Article

References (67)

1. Amann, J. M., B. J. Chyla, T. C. Ellis, A. Martinez, A. C. Moore, J. L. Franklin, L. McGhee, S. Meyers, J. E. Ohm, K. S. Luce, A. J. Ouelette, M. K. Washington, M. A. Thompson, D. King, S. Gautam, R. J. Coffey, R. H. Whitehead, and S. W. Hiebert. 2005. Mtgr1 is a transcriptional corepressor that is required for maintenance of the secretory cell lineage in the small intestine. Mol. Cell. Biol. 25:9576-9585.
2. Amann, J. M., J. Nip, D. K. Strom, B. Lutterbach, H. Harada, N. Lenny, J. R. Downing, S. Meyers, and S. W. Hiebert. 2001. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol. Cell. Biol. 21:6470-6483.
3. An, W., J. Kim, and R. G. Roeder. 2004. Ordered cooperative functions of PRMT1, p300, and CARM1 in transcriptional activation by p53. Cell 117: 735-748.
4. An, W., and R. G. Roeder. 2004. Reconstitution and transcriptional analysis of chromatin in vitro. Methods Enzymol. 377:460-474.
5. Aspland, S. E., H. H. Bendall, and C. Murre. 2001. The role of E2A-PBX1 in leukemogenesis. Oncogene 20:5708-5717.
6. Barndt, R. J., M. Dai, and Y. Zhuang. 2000. Functions of E2A-HEB heterodimers in T-cell development revealed by a dominant-negative mutation of HEB. Mol. Cell. Biol. 20:6677-6685.
7. Bayly, R., L. Chuen, R. A. Currie, B. D. Hyndman, R. Casselman, G. A. Blobel, and D. P. LeBrun. 2004. E2A-PBX1 interacts directly with the KIX domain of CBP/p300 in the induction of proliferation in primary hematopoietic cells. J. Biol. Chem. 279:55362-55371.
8. Bhalla, S., C. Spaulding, R. L. Brumbaugh, D. E. Zagort, M. E. Massari, C. Murre, and B. L. Kee. 2008. differential roles for the E2A activation domains in B lymphocytes and macrophages. J. Immunol. 180:1694-1703.
9. Black, J. C., J. E. Choi, S. R. Lombardo, and M. Carey. 2006. A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol. Cell 23:809-818.
10. Bradney, C., M. Hjelmeland, Y. Komatsu, M. Yoshida, T. P. Yao, and Y. Zhuang. 2003. Regulation of E2A activities by histone acetyltransferases in B lymphocyte development. J. Biol. Chem. 278:2370-2376.
11. Calabi, F., R. Pannell, and G. Pavloska. 2001. Gene targeting reveals a crucial role for MTG8 in the gut. Mol. Cell. Biol. 21:5658-5666.
12. Chyla, B. J., I. Moreno-Miralles, M. A. Steapleton, M. A. Thompson, S. Bhaskara, M. Engel, and S. W. Hiebert. 2008. Deletion of Mtg16, a target of t(16;21), alters hematopoietic progenitor cell proliferation and lineage allocation. Mol. Cell. Biol. 28:6234-6247.
13. Cisse, B., M. L. Caton, M. Lehner, T. Maeda, S. Scheu, R. Locksley, D. Holmberg, C. Zweier, N. S. den Hollander, S. G. Kant, W. Holter, A. Rauch, Y. Zhuang, and B. Reizis. 2008. Transcription factor E2-2 is an essential and specific regulator of plasmacytoid dendritic cell development. Cell 135: 37-48.
14. Cochrane, S. W., Y. Zhao, R. S. Welner, and X. H. Sun. 2009. Balance between Id and E proteins regulates myeloid-versus-lymphoid lineage decisions. Blood 113:1016-1026.
15. Courey, A. J., and S. Jia. 2001. Transcriptional repression: the long and the short of it. Genes Dev. 15:2786-2796.
16. Dias, S., R. Mansson, S. Gurbuxani, M. Sigvardsson, and B. L. Kee. 2008. E2A proteins promote development of lymphoid-primed multipotent progenitors. Immunity 29:217-227.
17. Fyodorov, D. V., and J. T. Kadonaga. 2003. Chromatin assembly in vitro with purified recombinant ACF and NAP-1. Methods Enzymol. 371:499-515.
18. Gardini, A., M. Cesaroni, L. Luzi, A. J. Okumura, J. R. Biggs, S. P. Minardi, E. Venturini, D. E. Zhang, P. G. Pelicci, and M. Alcalay. 2008. AML1/ETO oncoprotein is directed to AML1 binding regions and co-localizes with AML1 and HEB on its targets. PLoS Genet. 4:e1000275.
19. Ge, H., E. Martinez, C. M. Chiang, and R. G. Roeder. 1996. Activator-dependent transcription by mammalian RNA polymerase II: in vitro reconstitution with general transcription factors and cofactors. Methods Enzymol. 274:57-71.
20. Gelmetti, V., J. Zhang, M. Fanelli, S. Minucci, P. G. Pelicci, and M. A. Lazar. 1998. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol. Cell. Biol. 18:7185-7191.
21. Glass, C. K., and M. G. Rosenfeld. 2000. The coregulator exchange in transcriptional functions of nuclear receptors. Genes Dev. 14:121-141.
22. Goardon, N., J. A. Lambert, P. Rodriguez, P. Nissaire, S. Herblot, P. Thibault, D. Dumenil, J. Strouboulis, P. H. Romeo, and T. Hoang. 2006. ETO2 coordinates cellular proliferation and differentiation during erythropoiesis. EMBO J. 25:357-366.
23. Guermah, M., V. B. Palhan, A. J. Tackett, B. T. Chait, and R. G. Roeder. 2006. Synergistic functions of SII and p300 in productive activator-dependent transcription of chromatin templates. Cell 125:275-286.
24. Hamlett, I., J. Draper, J. Strouboulis, F. Iborra, C. Porcher, and P. Vyas. 2008. Characterisation of megakaryocyte GATA1-interacting proteins: the corepressor ETO2 and GATA1 interact to regulate terminal megakaryocyte maturation. Blood 112:2738-2749.
25. 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.
26. Henthorn, P., M. Kiledijian, and T. Kadesch. 1990. Two distinct transcription factors that bind the immunoglobulin enhancer μE5/κE2 motif. Science 247:467-470.
27. Hiebert, S. W., J. R. Downing, N. Lenny, and S. Meyers. 1996. Transcriptional regulation by the t(8;21) fusion protein, AML-1/ETO. Curr. Top. Microbiol. Immunol. 211:253-258.
28. Hildebrand, D., J. Tiefenbach, T. Heinzel, M. Grez, and A. B. Maurer. 2001. Multiple regions of ETO cooperate in transcriptional repression. J. Biol. Chem. 276:9889-9895.
29. Hug, B. A., and M. A. Lazar. 2004. ETO interacting proteins. Oncogene 23:4270-4274.
30. Jankovic, V., A. Ciarrocchi, P. Boccuni, T. DeBlasio, R. Benezra, and S. D. Nimer. 2007. Id1 restrains myeloid commitment, maintaining the self-renewal capacity of hematopoietic stem cells. Proc. Natl. Acad. Sci. USA 104:1260-1265.
31. Koch, F., F. Jourquin, P. Ferrier, and J. C. Andrau. 2008. Genome-wide RNA polymerase II: not genes only! Trends Biochem. Sci. 33:265-273.
32. Kondo, M. 2008. Multitalented E2A: a new role in lymphoid-lineage priming. Immunity 29:169-170.
33. Lee, Y. H., S. S. Koh, X. Zhang, X. Cheng, and M. R. Stallcup. 2002. Synergy among nuclear receptor coactivators: selective requirement for protein methyltransferase and acetyltransferase activities. Mol. Cell. Biol. 22:3621-3632.
34. Licht, J. D. 2001. AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML. Oncogene 20:5660-5679.
35. Lin, R. J., L. Nagy, S. Inoue, W. Shao, W. H. Miller, Jr., and R. M. Evans. 1998. Role of the histone deacetylase complex in acute promyelocytic leukaemia. Nature 391:811-814.
36. Lindberg, S. R., A. Olsson, A. M. Persson, and I. Olsson. 2005. The leukemia-associated ETO homologues are differently expressed during hematopoietic differentiation. Exp. Hematol. 33:189-198.
37. Liu, Y., M. D. Cheney, J. J. Gaudet, M. Chruszcz, S. M. Lukasik, D. Sugiyama, J. Lary, J. Cole, Z. Dauter, W. Minor, N. A. Speck, and J. H. Bushweller. 2006. The tetramer structure of the Nervy homology two domain, NHR2, is critical for AML1/ETO's activity. Cancer Cell 9:249-260.
38. Look, A. T. 1997. E2A-HLF chimeric transcription factors in pro-B cell acute lymphoblastic leukemia. Curr. Top. Microbiol. Immunol. 220:45-53.
39. Lutterbach, B., D. Sun, J. Schuetz, and S. W. Hiebert. 1998. The MYND motif is required for repression of basal transcription from the multidrug resistance 1 promoter by the t(8;21) fusion protein. Mol. Cell. Biol. 18:3604-3611.
40. Lutterbach, B., J. J. Westendorf, B. Linggi, A. Patten, M. Moniwa, J. R. Davie, K. D. Huynh, V. J. Bardwell, R. M. Lavinsky, M. G. Rosenfeld, C. Glass, E. Seto, and S. W. Hiebert. 1998. ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol. Cell. Biol. 18:7176-7184.
41. Markus, M., Z. Du, and R. Benezra. 2002. Enhancer-specific modulation of E protein activity. J. Biol. Chem. 277:6469-6477.
42. Massari, M. E., P. A. Grant, M. G. Pray-Grant, S. L. Berger, J. L. Workman, and C. Murre. 1999. A conserved motif present in a class of helix-loop-helix proteins activates transcription by direct recruitment of the SAGA complex. Mol. Cell 4:63-73.
43. Massari, M. E., and C. Murre. 2000. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell. Biol. 20:429-440.
44. Meier, N., S. Krpic, P. Rodriguez, J. Strouboulis, M. Monti, J. Krijgsveld, M. Gering, R. Patient, A. Hostert, and F. Grosveld. 2006. Novel binding partners of Ldb1 are required for haematopoietic development. Development 133: 4913-4923.
45. Minucci, S., M. Maccarana, M. Cioce, P. De Luca, V. Gelmetti, S. Segalla, L. Di Croce, S. Giavara, C. Matteucci, A. Gobbi, A. Bianchini, E. Colombo, I. Schiavoni, G. Badaracco, X. Hu, M. A. Lazar, N. Landsberger, C. Nervi, and P. G. Pelicci. 2000. Oligomerization of RAR and AML1 transcription factors as a novel mechanism of oncogenic activation. Mol. Cell 5:811-820.
46. Nimer, S. D., and M. A. Moore. 2004. Effects of the leukemia-associated AML1-ETO protein on hematopoietic stem and progenitor cells. Oncogene 23:4249-4254.
47. O'Neil, J., J. Shank, N. Cusson, C. Murre, and M. Kelliher. 2004. TAL1/SCL induces leukemia by inhibiting the transcriptional activity of E47/HEB. Cancer Cell 5:587-596.
48. Perissi, V., A. Aggarwal, C. K. Glass, D. W. Rose, and M. G. Rosenfeld. 2004. A corepressor/coactivator exchange complex required for transcriptional activation by nuclear receptors and other regulated transcription factors. Cell 116:511-526.
49. Peterson, L. F., A. Boyapati, E. Y. Ahn, J. R. Biggs, A. J. Okumura, M. C. Lo, M. Yan, and D. E. Zhang. 2007. Acute myeloid leukemia with the 8q22; 21q22 translocation: secondary mutational events and alternative t(8;21) transcripts. Blood 110:799-805.
50. Plevin, M. J., J. Zhang, C. Guo, R. G. Roeder, and M. Ikura. 2006. The acute myeloid leukemia fusion protein AML1-ETO targets E proteins via a paired amphipathic helix-like TBP-associated factor homology domain. Proc. Natl. Acad. Sci. USA 103:10242-10247.
51. Quong, M. W., W. J. Romanow, and C. Murre. 2002. E protein function in lymphocyte development. Annu. Rev. Immunol. 20:301-322.
52. Rochford, J. J., R. K. Semple, M. Laudes, K. B. Boyle, C. Christodoulides, C. Mulligan, C. J. Lelliott, S. Schinner, D. Hadaschik, M. Mahadevan, J. K. Sethi, A. Vidal-Puig, and S. O'Rahilly. 2004. ETO/MTG8 is an inhibitor of C/EBPβ activity and a regulator of early adipogenesis. Mol. Cell. Biol. 24:9863-9872.
53. Rosenfeld, M. G., V. V. Lunyak, and C. K. Glass. 2006. Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev. 20:1405-1428.
54. Ruzinova, M. B., and R. Benezra. 2003. Id proteins in development, cell cycle and cancer. Trends Cell Biol. 13:410-418.
55. Santoso, B., and J. T. Kadonaga. 2006. Reconstitution of chromatin transcription with purified components reveals a chromatin-specific repressive activity of p300. Nat. Struct. Mol. Biol. 13:131-139.
56. Schuh, A. H., A. J. Tipping, A. J. Clark, I. Hamlett, B. Guyot, F. J. Iborra, P. Rodriguez, J. Strouboulis, T. Enver, P. Vyas, and C. Porcher. 2005. ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol. Cell. Biol. 25:10235-10250.
57. Sjogren, H., B. Wedell, J. M. Meis-Kindblom, L. G. Kindblom, G. Stenman, and J. M. Kindblom. 2000. Fusion of the NH2-terminal domain of the basic helix-loop-helix protein TCF12 to TEC in extraskeletal myxoid chondrosarcoma with translocation t(9;15)(q22;q21). Cancer Res. 60:6832-6835.
58. Wallberg, A. E., K. Pedersen, U. Lendahl, and R. G. Roeder. 2002. p300 and PCAF act cooperatively to mediate transcriptional activation from chromatin templates by notch intracellular domains in vitro. Mol. Cell. Biol. 22: 7812-7819.
59. Wang, D., C. L. Claus, G. Vaccarelli, M. Braunstein, T. M. Schmitt, J. C. Zuniga-Pflucker, E. V. Rothenberg, and M. K. Anderson. 2006. The basic helix-loop-helix transcription factor HEBAlt is expressed in pro-T cells and enhances the generation of T cell precursors. J. Immunol. 177:109-119.
60. Wang, J., T. Hoshino, R. L. Redner, S. Kajigaya, and J. M. Liu. 1998. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3/HDAC1 complex. Proc. Natl. Acad. Sci. USA 95:10860-10865.
61. Wang, X., D. M. Truckses, S. Takada, T. Matsumura, N. Tanese, and R. H. Jacobson. 2007. Conserved region I of human coactivator TAF4 binds to a short hydrophobic motif present in transcriptional regulators. Proc. Natl. Acad. Sci. USA 104:7839-7844.
62. Wei, Y., S. Liu, J. Lausen, C. Woodrell, S. Cho, N. Biris, N. Kobayashi, Y. Wei, S. Yokoyama, and M. H. Werner. 2007. A TAF4-homology domain from the corepressor ETO is a docking platform for positive and negative regulators of transcription. Nat. Struct. Mol. Biol. 14:653-661.
63. Wichmann, C., L. Chen, M. Heinrich, D. Baus, E. Pfitzner, M. Zornig, O. G. Ottmann, and M. Grez. 2007. Targeting the oligomerization domain of ETO interferes with RUNX1/ETO oncogenic activity in t(8;21)-positive leukemic cells. Cancer Res. 67:2280-2289.
64. Yan, M., S. A. Burel, L. F. Peterson, E. Kanbe, H. Iwasaki, A. Boyapati, R. Hines, K. Akashi, and D. E. Zhang. 2004. Deletion of an AML1-ETO C-terminal NcoR/SMRT-interacting region strongly induces leukemia development. Proc. Natl. Acad. Sci. USA 101:17186-17191.
65. Yan, M., E. Kanbe, L. F. Peterson, A. Boyapati, Y. Miao, Y. Wang, I. M. Chen, Z. Chen, J. D. Rowley, C. L. Willman, and D. E. Zhang. 2006. A previously unidentified alternatively spliced isoform of t(8;21) transcript promotes leukemogenesis. Nat. Med. 12:945-949.
66. Zhang, J., B. A. Hug, E. Y. Huang, C. W. Chen, V. Gelmetti, M. Maccarana, S. Minucci, P. G. Pelicci, and M. A. Lazar. 2001. Oligomerization of ETO is obligatory for corepressor interaction. Mol. Cell. Biol. 21:156-163.
67. Zhang, J., M. Kalkum, S. Yamamura, B. T. Chait, and R. G. Roeder. 2004. E protein silencing by the leukemogenic AML1-ETO fusion protein. Science 305:1286-1289.