The AD1 and AD2 transactivation domains of E2A are essential for the antiapoptotic activity of the chimeric oncoprotein E2A-HLF

Molecular and Cellular Biology

Volumn 18, Issue 10, 1998, Pages 6035-6043

  Inukai, Takeshi ^a,d   Inaba, Toshiya ^b   Ikushima, Satoshi ^a,e   Look, A Thomas ^a,c  

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

^b JICHI MEDICAL UNIVERSITY   (Japan)

^c UNIVERSITY OF TENNESSEE COLLEGE OF MEDICINE   (United States)

^d UNIVERSITY OF YAMANASHI   (Japan)

^e KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

LEUCINE ZIPPER PROTEIN; ONCOPROTEIN;

APOPTOSIS; ARTICLE; CARCINOGENESIS; CELL COMMUNICATION; CELL PROLIFERATION; CYTOKINE PRODUCTION; DIMERIZATION; DNA BINDING; GENE EXPRESSION REGULATION; GENE STRUCTURE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION;

MURINAE;

EID: 0031656237     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.18.10.6035     Document Type: Article

References (62)

1. Adler, S. M. L., M. L. Waterman, X. He, and M. G. Rosenfeld. 1988. Steroid receptor-mediated inhibition of rat prolactin gene expression does not require the receptor DNA-binding domain. Cell 52:685-695.
2. Ananthan, J., R. Baler, D. Morrissey, J. Zuo, Y. Lan, M. Weir, and R. Voellmy. 1993. Synergistic activation of transcription is mediated by the N-terminal domain of Drosophila fushi tarazu homeoprotein and can occur without DNA binding by the protein. Mol. Cell. Biol. 13:1599-1609.
3. Askew, D. S., R. A. Ashmun, B. C. Simmons, and J. L. Cleveland. 1991. Constitutive c-myc expression in an IL-3-dependent myeloid cell line suppresses cell cycle arrest and accelerates apoptosis. Oncogene 6:1915-1922.
4. Bain, G., E. C. Robanus-Maandag, D. J. Izon, D. Amsen, A. M. Kruisbeek, B. C. Weintraub, I. Krop, M. S. Schlissel, A. J. Feeney, M. van Roon, M. van der Valk, H. P. J. te Riele, A. Berns, and C. Murre. 1994. E2A proteins are required for proper B-cell development and initiation of immunoglobulin gene rearrangements. Cell 79:885-892.
5. Bain, G., E. C. Robanus Maandag, H. P. te Riele, A. J. Feeney, A. Sheeny, M. Schlisset, S. A. Shinton, R. R. Hardy, and C. Murre. 1997. Both E12 and E47 allow commitment to the B cell lineage. Immunity 6:145-154.
6. Bakhshi, A., J. P. Jensen, P. Goldman, J. J. Wright, O. W. McBride, A. L. Epstein, and S. J. Korsmeyer. 1985. Cloning the chromosomal breakpoint of t(14;18) human lymphomas: clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41:899-906.
7. Benezra, R., R. L. Davis, D. Lockshon, D. L. Turner, and H. Weintraub. 1990. The protein Id: a negative regulator of helix-loop-helix DNA binding proteins. Cell 61:49-59.
8. Chakraborty, T., T. J. Brennan, L. Li, D. Edmondson, and E. N. Olson. 1991. Inefficient homooligomerization contributes to the dependence of myogenin on E2A products for efficient DNA binding. Mol. Cell. Biol. 11:3633-3641.
9. Chang, C. P., I. de Vivo, and M. L. Cleary. 1997. The Hox cooperativity motif of the chimeric oncoprotein E2a-Pbx1 is necessary and sufficient for oncogenesis. Mol. Cell. Biol. 17:81-88.
10. Chang, C. P., W. F. Shen, S. Rozenfeld, H. J. Lawrence, C. Largman, and M. L. Cleary. 1995. Pbx proteins display hexapeptide-dependent cooperative DNA binding with a subset of Hox proteins. Genes Dev. 9:663-674.
11. Cleary, M. L., and J. Sklar. 1985. Nucleotide sequence of a t(14;18) chromosomal breakpoint in follicular lymphoma and demonstration of a break- point-cluster region near a transcriptionally active locus on chromosome 18, Proc. Natl Acad. Sci. USA 82:7439-7443.
12. Cserjesi, P., D. Brown, K. L. Ligon, G. E. Lyons, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, and E. N. Olson. 1995. Scleraxis: a basic helix-loophelix protein that prefigures skeletal formation during mouse embryogenesis. Development 121:1099-1110.
13. Darnell, J. E., Jr. 1997. STATs and gene regulation. Science 277:1630-1635.
14. Dedera, D. A., E. K. Waller, D. P. LeBrun. A. Sen-Majumdar, M. E. Stevens, G. S. Barsh, and M. L. Cleary. 1993. Chimeric homeohox gene E2A-PBX1 induces proliferation, apoptosis, and malignant lymphomas in transgenic mice. Cell 74:833-843.
15. Drolet, D. W., K. M. Scully, D. M. Simmons, M. Wegner, K. T. Chu, L. W. Swanson, and M. G. Rosenfeld. 1991. TEF, a transcription factor expressed specifically in the anterior pituitary during embryogenesis, defines a new class of leucine zipper proteins. Genes Dev. 5:1739-1753.
16. Evan, G. I., A. H. Wyllie, C. S. Gilbert, T. D. Littlewood, H. Land, M. Brooks, C. M. Waters, L. Z. Penn, and D. C. Hancock. 1992. Induction of apoptosis in fibroblasts by c-myc protein. Cell 69:119-128.
17. Fitzpatrick, V. D., A. Percival-Smith, C. J. Ingles, and H. M. Krause. 1992. Homeodomain-independent activity of the fushi tarazu polypeptide in Drosophila embryos. Nature 356:610-612.
18. Guillemot, F., L. C. Lo, J. E. Johnson, A. Auerbach, D. J. Anderson, and A. L. Joyner. 1993. Mammalian achaete-scute homolog 1 is required for the early development of olfactory and autonomic neurons. Cell 75:463-476.
19. Hsu, H.-L., J.-T. Cheng, Q. Chen, and R. Baer. 1991. Enhancer-binding activity of the Tal-1 oncoprotein in association with the E47/E12 helix-loophelix proteins. Mol. Cell. Biol. 11:3037-3042.
20. Hsu, H. L., I. Wadman, J. T. Tsan, and R. Baer. 1994. Positive and negative transcriptional control by the TAL1 helix-loop-helix protein. Proc. Natl. Acad. Sci. USA 91:5947-5951.
21. Hunger, S. P. 1996. Chromosomal translocations involving the E2A gene in | acute lymphoblastic leukemia: clinical features and molecular pathogenesis. Blood 87:1211-1224.
22. Hunger, S. P., P. E. Devaraj, L. Foroni, L. M. Seeker-Walker, and M. L. Cleary. 1994. Two types of genomic rearrangements create alternative E2A-HLF fusion proteins in t(17;19)-ALL. Blood 83:2261-2267.
23. Hunger, S. P., S. Li, M. Z. Fall, L. Naumovski, and M. L. Cleary. 1996. The proto-oncogene HLF and the related basic leucine zipper protein TEF display highly similar DNA-binding and transcriptional regulatory properties. Blood 87:4607-4617.
24. Hunger, S. P., K. Ohyashiki, K. Toyama, and M. L. Cleary. 1992. Hlf, a novel hepatic bZIP protein, shows altered DNA-binding properties following fusion to E2A in t(17;19) acute lymphoblastic leukemia. Genes Dev. 6:1608-1620.
25. Ikushima, S., T. Inukai, T. Inaba, S. D. Nimer, J. L. Cleveland, and A. T. Look. 1997. Pivotal role for the NFIL3/E4BP4 transcription factor in interleukin 3-mediated survival of pro-B lymphocytes. Proc. Natl. Acad. Sci. USA 94:2609-2614.
26. Inaba, T., T. Inukai, T. Yoshihara, H. Seyschab, R. A. Ashmun, C. E. Canman, S. J. Laken, M. B. Kastan, and A. T. Look. 1996. Reversal of apoptosis by the leukaemia-associated E2A-HLF chimaeric transcription factor. Nature 382:541-544.
27. Inaba, T., W. M. Roberts, L. H. Shapiro, K. W. Jolly, S. C. Raimondi, S. D. Smith, and A. T. Look. 1992. Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science 257:531-534.
28. Inaba, T., L. H. Shapiro, T. Funabiki, A. E. Sinclair, B. G. Jones, R. A. Ashmun, and A. T. Look. 1994. DNA-binding specificity and trans-activating potential of the leukemia-associated E2A-hepatic leukemia factor fusion protein. Mol. Cell. Biol. 14:3403-3413.
29. Inukai, T., T. Inaba, T. Yoshihara, and A. T. Look. 1997. Cell transformation mediated by homodimeric E2A-HLF transcription factors. Mol. Cell. Biol. 17:1417-1424.
30. 29a.Inukai, T., and A. T. Look. Unpublished observations.
31. Kamps, M. P., D. D. Wright, and Q. Lu. 1996. DNA-binding by oncoprotein E2a-Pbx1 is important for blocking differentiation but dispensable for fibroblast transformation. Oncogene 12:19-30.
32. Korsmeyer, S. J. 1992. Bcl-2 initiates a new category of oncogenes: regulators of cell death. Blood 80:879-886.
33. Langdon, W. Y., A. W. Harris, S. Cory, and J. M. Adams. 1986. The C-myc oncogene perturbs B lymphocyte development in Emu-myc transgenic mice. Cell 47:11-18.
34. Lassar, A. B., J. N. Buskin, D. Lockshon, R. L. Davis, S. Apone, S. D. Hauschka, and H. Weintraub. 1989. MyoD is a sequence-specific DNA binding protein requiring a region of myc homology to bind to the muscle creatine kinase enhancer. Cell 58:823-831.
35. Look, A. T. 1997. Oncogenic transcription factors in the human acute leu-kemias. Science 278:1059-1064.
36. Look, A. T. 1998. Genes altered by chromosomal translocations in leukemias and lymphomas, p. 109-141. In B. Vogelstein and K. W. Kinzler (ed.), The genetic basis of human disease. McGraw-Hill, New York, N.Y.
37. Lu, Q., and M. P. Kamps. 1996. Structural determinants within Pbx1 that mediate cooperative DNA binding with pentapeptide-containing Hox pro teins: proposal for a model of a Pbx1-Hox-DNA complex. Mol. Cell. Biol. 16:1632-1640.
38. Massari, M. E., P. A. Jennings, and C. Murre. 1996. The AD1 transactivation domain of E2A contains a highly conserved helix which is required for its activity in both Saccharomyces cerevisiae and mammalian cells. Mol. Cell. Biol. 16:121-129.
39. McKearn, J. P., J. McCubrey, and B. Fagg. 1985. Enrichment of hematopoietic precursor cells and cloning of multipotential B-lymphocyte precursors. Proc. Natl. Acad. Sci. USA 82:7414-7418.
40. Metzstein, M. M., M. O. Hengartner, N. Tsung, R. E. Ellis, and H. R. Horvitz. 1996. Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382:545-547.
41. Monica, K., D. P. LeBrun, D. A. Dedera, R. Brown, and M. L. Cleary. 1994. Transformation properties of the E2A-PBX1 chimeric oncoprotein: fusion with E2A is essential, but the PBX1 homeodomain is dispensable. Mol. Cell. Biol. 14:8304-8314.
42. Murre, C., G. Bain, M. A. Van Dijk, I. Engel, B. A. Furnari, M. E. Massari, J. R. Matthews, M. W. Quong, R. R. Rivera, and M. H. Stuiver. 1994. Structure and function of helix-loop-helix proteins. Biochim. Biophys. Acta 1218:129-135.
43. Murre, C., P. S. McCaw, and D. Baltimore. 1989. A new DNA binding and dimerization motif in immunoglobulin enhancer binding, daughterless, MyoD, and myc proteins. Cell 56:777-783.
44. Murre, C., P. S. McCaw, H. Vaessin, M. Caudy, L. Y. Jan, C. V. Cabrera, J. N. Buskin, S. D. Hauschka, A. B. Lassar, H. Weintraub, and D. Baltimore. 1989. Interactions between heterologous helix-loop-helix proteins generate complexes that bind specifically to a common DNA sequence. Cell 58:537-544.
45. Neuteboom, S. T., L. T. Peltenburg, M. A. Van Dijk, and C. Murre. 1995. The hexapeptide LFPWMR in Hoxb-8 is required for cooperative DNA binding with Pbxl and Pbx2 proteins. Proc. Natl. Acad. Sci. USA 92:9166-9170.
46. Nunez, G., L. London, D. Hockenbery, M. Alexander, J. P. McKearn, and S. J. Korsmeyer. 1990. Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. J. Immunol. 144:3602-3610.
47. Packham, G., and J. L. Cleveland. 1995. c-Myc and apoptosis. Biochim. Biophys. Acta 1242:11-28.
48. Peverali, F. A., T. Ramqvist, R. Saffrich, R. Pepperkok, M. V. Barone, and L. Philipson. 1994. Regulation of G1 progression by E2A and Id helix-loophelix proteins. EMBO J. 13:4291-4301.
49. Quong, M. W., M. E. Massari, R. Zwart, and C. Murre. 1993. A new transcriptional-activation motif restricted to a class of helix-loop-helix proteins is functionally conserved in both yeast and mammalian cells. Mol. Cell. Biol. 13:792-800.
50. Rabbitts, T. H. 1994. Chromosomal translocations in human cancer. Nature 372:143-149.
51. Shen, C. P., and T. Kadesch. 1995. B-cell-specific DNA binding by an E47 homodimer. Mol. Cell. Biol. 15:4518-4524.
52. Shivdasani, R. A., E. L. Mayer, and S. H. Orkin. 1995. Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373:432-434.
53. Smith, K. S., Y. Jacobs, C. P. Chang, and M. L. Cleary. 1997. Chimeric oncoprotein E2a-Pbx1 induces apoptosis of hematopoietic cells by a p53-independent mechanism that is suppressed by Bcl-2. Oncogene 14:2917-2926.
54. Thompson, C. B. 1995. Apoptosis in the pathogenesis and treatment of disease. Science 267:1456-1462.
55. Tontonoz, P., J. B. Kim R. A. Graves, and B. M. Spiegelman. 1993. ADD1: a novel helix-loop-helix transcription factor associated with adipocyte determination and differentiation. Mol. Cell. Biol. 13:4753-4759.
56. Tsujimoto, Y., J. Gorham, J. Cossman, E. Jaffe, and C. M. Croce. 1985. The t(14;18) chromosome translocations involved in B-cell neoplasms result from mistakes in VDJ joining. Science 229:1390-1393.
57. Van Dijk, M. A., L. T. Peltenburg, and C. Murre. 1995. Hox gene products modulate the DNA binding activity of Pbx1 and Pbx2. Mech. Dev. 52:99-108.
58. Vaux, D. L., S. Cory, and J. M. Adams. 1988. Bcl-2 gene promotes haemopoietic cell survival and cooperates with c-myc to immortalize pre-B cells. Nature 335:440-442.
59. Voronova, A. F., and F. Lee. 1994. The E2A and tal-1 helix-loop-helix proteins associate in vivo and are modulated by Id proteins during interleukin 6-induced myeloid differentiation. Proc. Natl. Acad. Sci. USA 91:5952-5956.
60. Yang, E., and S. J. Kursmeyer. 1996. Molecular thanatopsis: a discourse on the BCL2 family and cell death. Blood 88:386-401.
61. Yoshihara, T., T. Inaba, L. H. Shapiro, J. Kato, and A. T. Look. 1995. E2A-HLF-mediated cell transformation requires both the trans-activation domain of E2A and the leucine zipper dimerization domain of HLF. Mol. Cell. Biol. 15:3247-3255.
62. Zhuang, Y., P. Soriano, and H. Weintraub. 1994. The helix-loop-helix gene E2A is required for B-cell formation. Cell 79:875-884.