SLUG, a ces-1-related zinc finger transcription factor gene with antiapoptotic activity, is a downstream target of the E2A-HLF oncoprotein

Molecular Cell

Volumn 4, Issue 3, 1999, Pages 343-352

  Inukai, Takeshi ^a,e   Inoue, Akira ^a   Kurosawa, Hidemitsu ^a   Goi, Kumiko ^a   Shinjyo, Tetsuharu ^c   Ozawa, Keiya ^c   Mao, Mao ^d   Inaba, Toshiya ^c   Look, A Thomas ^a,b  

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

^b HARVARD MEDICAL SCHOOL   (United States)

^c JICHI MEDICAL UNIVERSITY   (Japan)

^d SHANGHAI SECOND MEDICAL UNIVERSITY   (China)

^e UNIVERSITY OF YAMANASHI   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ONCOPROTEIN; TRANSCRIPTION FACTOR; ZINC FINGER PROTEIN;

APOPTOSIS; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; HUMAN; LEUKEMIA CELL LINE; MOUSE; NONHUMAN; PROTEIN DNA BINDING; PROTEIN TARGETING; TRANSCRIPTION REGULATION;

GASTROPODA; MAMMALIA; MURINAE;

EID: 0033197879     PISSN: 10972765     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1097-2765(00)80336-6     Document Type: Article

References (63)

1. Alnemri, E.S., Livingston, D.J., Nicholson, D.W., Salvesen, G., Thornberry, N.A., Wong, W.W., and Yuan, J. (1996). Human ICE/ CED-3 protease nomenclature. Cell 87, 171-171.
2. Altura, R.A., Inukai, T., Ashmun, R.A., Zambetti, G.P., Roussel, M.F., and Look, A.T. (1998). The chimeric E2A-HLF transcription factor abrogates p53-induced apoptosis in myeloid leukemia cells. Blood 92, 1397-1405.
3. Aronheim, A., Shiran, R., Rosen, A., and Walker, M.D. (1993). The E2A gene product contains two separable and functionally distinct transcription activation domains. Proc. Natl. Acad. Sci. USA 90, 8063-8067.
4. Boulay, J.L., Dennefeld, C., and Alberga, A. (1987). The Drosophila developmental gene snail encodes a protein with nucleic acid binding fingers. Nature 330, 395-398.
5. Boyd, J.M., Gallo, G.J., Elangovan, B., Houghton, A.B., Malstrom, S., Avery, B.J., Ebb, R.G., Subramanian, T., Chittenden, T., and Lutz, R.J., et al. (1995). Bik, a novel death-inducing protein shares a distinct sequence motif with Bcl-2 family proteins and interacts with viral and cellular survival-promoting proteins. Oncogene 11, 1921-1928.
6. Buxton, P., Hunt, P., Ferreti, P., and Thorogood, P. (1997). A role for midline closure in the reestablishment of dorsoventral pattern following dorsal hindbrain ablation. Dev. Biol. 183, 150-165.
7. Cecconi, F., Alvarez-Bolado, G., Meyer, B.I., Roth, K.A., and Gruss, P. (1998). Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727-737.
8. Conradt, B., and Horvitz, H.R. (1998). The C. elegans protein EGL-1 is required for programmed cell death and interacts with the Bcl-2-like protein CED-9. Cell 93, 519-529.
9. Elangovan, B., and Chinnadurai, G. (1997). Functional dissection of the pro-apoptotic protein Bik. Heterodimerization with anti-apoptosis proteins is insufficient for induction of cell death. J. Biol. Chem. 272, 24494-24498.
10. Ellis, R.E., and Horvitz, H.R. (1991). Two C. elegans genes control the programmed deaths of specific cells in the pharynx. Development 112, 591-603.
11. Green, D.R. (1998). Apoptotic pathways: The roads to ruin. Cell 94, 695-698.
12. 1 arrest induced by interleukin-2 withdrawal. Mol. Cell. Biol. 16, 6263-6272.
13. Han, J., Sabbatini, P., and White, E. (1996). Induction of apoptosis by human Nbk/Bik, a BH3-containing protein that interacts with E1B 19K. Mol. Cell. Biol. 16, 5857-5864.
14. Hayashi, S., Hirose, S., Metcalfe, T., and Shirras, A.D. (1993). Control of imaginal cell development by the escargot gene of Drosophila. Development 118, 105-115.
15. L, is a potent death agonist. J. Biol. Chem. 273, 7783-7786.
16. Hengartner, M.O., and Horvitz, H.R. (1994). C. elegans cell survival gene ced-9 encodes a functional homolog of the mammalian protooncogene Bcl-2. Cell 76, 665-676.
17. Henthorn, P., Kiledjian, M., and Kadesch, T. (1990). Two distinct transcription factors that bind the immunoglobulin enhancer E5/E2 motif. Science 247, 467-470.
18. Horvitz, H.R., Shaham, S., and Hengartner, M.O. (1994). The genetics of programmed cell death in the nematode Caenorhabditis elegans. Cold Spring Harb. Symp. Quant. Biol. 59, 377-385.
19. Hubank, M., and Schatz, D.G. (1994). Identifying differences in mRNA expression by representational difference analysis of cDNA. Nucleic Acids Res. 22, 5640-5648.
20. Hunger, S.P., Brown, R., and Cleary, M.L. (1994). DNA-binding and transcriptional regulatory properties of hepatic leukemia factor (HLF) and the t(17;19) acute lymphoblastic leukemia chimera E2A-HLF. Mol. Cell. Biol. 14, 5986-5996.
21. Ikushima, S., Inukai, T., Inaba, T., Nimer, S.D., Cleveland, J.L., and Look, A.T. (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.
22. Imaizumi, K., Tsuda, M., Imai, Y., Wanaka, A., Takagi, T., and TohYama, M. (1997). Molecular cloning of a novel polypeptide, DP5, induced during programmed neuronal death. J. Biol. Chem. 272, 18842-18848.
23. Inaba, T., Roberts, W.M., Shapiro, L.H., Jolly, K.W., Raimondi, S.C., Smith, S.D., and Look, A.T. (1992). Fusion of the leucine zipper gene HLF to the E2A gene in human acute B-lineage leukemia. Science 257, 531-534.
24. Inaba, T., Shapiro, L.H., Funabiki, T., Sinclair, A.E., Jones, B.G., Ashmun, R.A., and Look, A.T. (1994). DNA-binding specificity and trans-activating potential of the leukemia-associated E2A-hepatic leukemia factor fusion protein. Mol. Cell. Biol. 14, 3403-3413.
25. Inaba, T., Inukai, T., Yoshihara, T., Seyschab, H., Ashmun, R.A., Canman, C.E., Laken, S.J., Kastan, M.B., and Look, A.T. (1996). Reversal of apoptosis by the leukaemia-associated E2A-HLF chimaeric transcription factor. Nature 382, 541-544.
26. L. EMBO J. 16, 1686-1694.
27. Inukai, T., Inaba, T., Yoshihara, T., and Look, A.T. (1997). Cell transformation mediated by homodimeric E2A-HLF transcription factors. Mol. Cell. Biol. 17, 1417-1424.
28. Inukai, T., Inaba, T., Ikushima, S., and Look, A.T. (1998). The AD1 and AD2 transactivation domains of E2A are essential for the antiapoptotic activity of the chimeric oncoprotein E2A-HLF. Mol. Cell. Biol. 18, 6035-6043.
29. Ip, Y.T., Park, R.E., Kosman, D., Bier, E., and Levine, M. (1992). The dorsal gradient morphogen regulates stripes of rhomboid expression in the presumptive neuroectoderm of the Drosophila embryo. Genes Dev. 6, 1728-1739.
30. Jiang, R., Lan, Y., Norton, C.R., Sundberg, J.P., and Gridley, T. (1998). The slug gene is not essential for mesoderm or neural crest development in mice. Dev. Biol. 198, 277-285.
31. Kasai, Y., Nambu, J.R., Lieberman, P.M., and Crews, ST. (1992). Dorsal-ventral patterning in Drosophila: DNA binding of snail protein to the single-minded gene. Proc. Natl. Acad. Sci. USA 89, 3414-3418.
32. L regulate the survival of murine pro-B lymphocytes. Mol. Cell. Biol, 19, 2754-2762.
33. Kurosawa, H., Goi, K., Inukai, T., Inaba, T., Chang, K.S., Shinjyo, T., Rakestraw, K., Naeve, C.W., and Look, A.T. (1999). Two candidate downstream target genes for E2A-HLF. Blood 93, 321-332.
34. Li, H., Zhu, H., Xu, C.-J., and Yuan, J. (1998). Cleavage of BID by caspase 8 mediates the mitochondrial damage in the Fas pathway of apoptosis. Cell 94, 491-501.
35. Look, A.T. (1997). Oncogenic transcription factors in the human acute leukemias. Science 278, 1059-1064.
36. Luo, X., Budihardjo, I., Zou, H., Slaughter, C., and Wang, X. (1998). Bid, a Bcl2 interacting protein, mediates cytochrome c release from mitochondria in response to activation of cell surface death receptors. Cell 94, 481-490.
37. Massari, M.E., Jennings, P.A., and Murre, C. (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.
38. Mauhin, V., Lutz, Y., Dennefeld, C., and Alberga, A. (1993). Definition of the DNA-binding site repertoire for the Drosophila transcription factor SNAIL. Nucleic Acids Res. 21, 3951-3957.
39. Metzstein, M.M., and Horvitz, H.R. (1999). The C. elegans cell death specification gene ces-1 encodes a snail family zinc finger protein. Mol. Cell 4, this issue, 309-319.
40. Metzstein, M.M., Hengartner, M.O., Tsung, N., Ellis, R.E., and Horvitz, H.R. (1996). Transcriptional regulator of programmed cell death encoded by Caenorhabditis elegans gene ces-2. Nature 382, 545-547.
41. Metzstein, M.M., Stanfield, G.M., and Horvitz, H.R. (1998). Genetics of programmed cell death in C. elegans: Past, present and future. Trends Genet. 14, 410-416.
42. Nieto, M.A., Sargent, M.G., Wilkinson, D.G., and Cooke, J. (1994). Control of cell behavior during vertebrate development by slug, a zinc finger gene. Science 264, 835-839.
43. O'Connor, L., Strasser, A., O'Reilly, L.A., Hausmann, G., Adams, J.M., Cory, S., and Huang, D.C. (1998). Bim: A novel member of the Bcl-2 family that promotes apoptosis. EMBO J. 17, 384-395.
44. Onishi, M., Nosaka, T., Misawa, K., Mui, A.L.-F., Gorman, D., McMaHon, M., Miyajima, A., and Kitamura, T. (1998). Identification and characterization of a constitutively active STAT5 mutant that promotes cell proliferation. Mol. Cell. Biol. 18, 3871-3879.
45. Osborne, B.A. (1996). Cell death in vertebrates: Lessons from the worm. Trends Genet. 12, 489-491.
46. Ottilie, S., Diaz, J.L., Horne, W., Chang, J., Wang, Y., Wilson, G., Chang, S., Weeks, S., Fritz, L.C., and Oltersdorf, T. (1997). Dimerization properties of human BAD. J. Biol. Chem. 272, 30866-30872.
47. Packham, G., and Cleveland, J.L. (1995). c-Myc and apoptosis. BioChim. Biophys. Acta 1242, 11-28.
48. Palacios, R., Henson, G., Steinmetz, M., and McKearn, J.P. (1984). Interleukin-3 supports growth of mouse pre-B-cell clones in vitro. Nature 309, 126-131.
49. Quong, M.W., Massari, M.E., Zwart, R., and Murre, C. (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. Raff, M.C. (1992). Social controls on cell survival and cell death. Nature 356, 397-400.
51. Roark, M., Sturtevant, M.A., Emery, J., Vaessin, H., Grell, E., and Bier, E. (1995). Scratch, a pan-neural gene encoding a zinc finger protein related to snail, promotes neuronal development. Genes Dev. 9, 2384-2398.
52. Roberts, T., and Cowell, J.K. (1997). Cloning of the human Gfi-1 gene and its mapping to chromosome region 1p22. Oncogene 14, 1003-1005.
53. Sargent, M.G., and Bennett, M.F. (1990). Identification in Xenopus of a structural homologue of the Drosophila gene snail. Development 109, 967-973.
54. Savagner, P., Yamada, K.M., and Thiery, J.P. (1997). The zinc-finger protein slug causes desmosome dissociation, an initial and necessary step for growth factor-induced epithelial-mesenchymal transition. J. Cell. Biol. 137, 1403-1419.
55. Steller, H. (1995). Mechanisms and genes of cellular suicide. Science 267, 1445-1449.
56. Thompson, C.B. (1995). Apoptosis in the pathogenesis and treatment of disease. Science 267, 1456-1462.
57. Vaux, D.L., and Strasser, A. (1996). The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA 93, 2239-2244.
58. Wang, K., Yin, X.-M., Chao, D.T., Milliman, C.L., and Korsmeyer, S.J. (1996). BID: A novel BH3 domain-only death agonist. Genes Dev. 10, 2859-2869.
59. Yang, E., and Korsmeyer, S.J. (1996). Molecular thanatopsis: A discourse on the BCL2 family and cell death. Blood 88, 386-401.
60. L and Bcl-2, displaces bax and promotes cell death. Cell 80, 285-291.
61. Yoshida, H., Kong, Y.Y., Yoshida, R., Elia, A.J., Hakem, A., Hakem, R., Penninger, J.M., and Mak, T.W. (1998). Apafl is required for mitochondrial pathways of apoptosis and brain development. Cell 94, 739-750.
62. Yoshihara, T., Inaba, T., Shapiro, L.H., Kato, J., and Look, A.T. (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.
63. Zou, H., Henzel, W.J., Liu, X., Lutschg, A., and Wang, X. (1997). Apaf-1, a human protein homologous to C. elegans CED-4, participates in cytochrome c-dependent activation of caspase-3. Cell 90, 405-413.