Dual functions of the AML1/Evi-1 chimeric protein in the mechanism of leukemogenesis in t(3;21) leukemias

Molecular and Cellular Biology

Volumn 15, Issue 5, 1995, Pages 2383-2392

  Tanaka, Tomoyuki ^a   Mitani, Kinuko ^a   Kurokawa, Mineo ^a   Ogawa, Seishi ^a   Tanaka, Kozo ^a   Nishida, Junji ^b   Yazaki, Yoshio ^a   Shibata, Yoichi ^a   Hirai, Hisamaru ^a,b  

^a UNIVERSITY OF TOKYO   (Japan)

^b JICHI MEDICAL UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHIMERIC PROTEIN; GRANULOCYTE COLONY STIMULATING FACTOR; TRANSCRIPTION FACTOR;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL DIFFERENTIATION; CELL TRANSFORMATION; CHROMOSOME TRANSLOCATION; CHRONIC MYELOID LEUKEMIA; DELETION MUTANT; DNA BINDING; ENHANCER REGION; HUMAN; HUMAN CELL; LEUKEMOGENESIS; MYELODYSPLASTIC SYNDROME; ONCOGENE C FOS; PRIORITY JOURNAL; PROMOTER REGION; TRANSACTIVATION;

MURINE POLYOMAVIRUS;

EID: 0028943758     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.15.5.2383     Document Type: Article

References (70)

1. Andrews, N. C., and D. V. Faller. 1991. A rapid micropreparation technique for extraction of DNA-binding proteins from limiting numbers of mammalian cells. Nucleic Acids Res. 19:2499.
2. Angel, P., and M. Karin. 1991. The role of Jun, Fos and the AP-1 complex in cell-proliferation and transformation. Biochim. Biophys. Acta 1072:129-157.
3. Askew, D. S., R. S. 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. 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. 1994. PEBP2αB/mouse AML1 consists of multiple isoforms that possess differential transactivation potentials. Mol. Cell. Biol. 14:3242-3252.
5. Bae, S. C., Y. Yamaguchi-Iwai, E. Ogawa, M. Maruyama, M. Inuzuka, H. Kagoshima, K. Shigesada, M. Satake, and Y. Ito. 1993. Isolation of PEBP2αB cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene 8:809-814.
6. Bartholomew, C., and J. N. Ihle. 1991. Retroviral insertions 90 kilobases proximal to the Evi-1 myeloid transforming gene activate transcription from the normal promoter. Mol. Cell. Biol. 11:1820-1828.
7. Bartholomew, C., K. Morishita, D. Askew, A. Buchberg, N. A. Jenkins, N. G. Copeland, and J. N. Ihle. 1989. Retroviral insertions in the CB-1/Fim-3 common site of integration activate expression of the Evi-1 gene. Oncogene 4:529-534.
8. Brown, A. M. C., and M. R. D. Scott. 1987. Retroviral vectors, p. 189-212. In D. M. Glover (ed.), DNA cloning, vol. III. IRL Press, Oxford.
9. Cleary, M. L. 1991. Oncogenic conversion of transcription factors by chromosomal translocations. Cell 66:619-612.
10. Colotta, F., N. Polentarutti, M. Sironi, and A. Mantovani. 1992. Expression and involvement of c-fos and c-jun protooncogenes in programmed cell death induced by growth factor deprivation in lymphoid cell lines. J. Biol. Chem. 267:18278-18283.
11. Daniel, M. T., M. Koken, O. Romagne, S. Barbey, A. Bazarbachi, M. Stadler, M. C. Guillemin, L. Degos, C. Chomienne, and H. deThe. 1993. PML protein expression in hematopoictic and acute promyelocytic leukemia cells. Blood 82:1858-1867.
12. deThe H., C. Lavau, A. Marchio, C. Chomienne, L. Degos, and A. Dejean. 1991. The PML-RARα fusion mRNA generated by the t(15;17) translocation in acute promyelocytic leukemia encodes a functionally altered RAR. Cell 66:675-684.
13. Dong, F., C. van Buitenen, K. Pouwels, L. H. Hoefsloot, B. Lowenberg, and I. P. Touw. 1993. Distinct cytoplasmic regions of the human granulocyte colony-stimulating factor receptor involved in induction of proliferation and maturation. Mol. Cell. Biol. 13:7774-7781.
14. Dyck, J. A., G. G. Maul, H. M. Wilson, Jr., J. D. Chen, A. Kakizuka, and R. M. Evans. 1993. A novel macromolecular structure is a target of the promyelocyte-retinoic acid receptor oncoprotein. Cell 76:333-343.
15. Erickson, P., J. Gao, K. S. Chang, T. Look, E. Whisenant, S. Raimondi, R. Lasher, J. Trujillo, J. Rowley, and H. Drabkin. 1992. Identification of breakpoints in t(8;21) acute myelogenous leukemia and isolation of a fusion transcript. AML1/ETO, with similarity to Drosophila segmentation gene, runt. Blood 80:1825-1831.
16. Fearon, E. R., and B. Vogelstein. 1990. A genetic model for colorectal tumorigenesis. Cell 61:759-767.
17. Fichelson, S., F. Dreyfus, R. Berger, J. Melle, C. Bastard, J. M. Miclea, and S. Gisselbrecht. 1992. Evi-1 expression in leukemic patients with rearrangements of the 3q25-q28 chromosomal region. Leukemia 6:93-99.
18. Fort, P., L. Marty, M. Piechaczyk, S. Sabrouty, C. Dani, P. Jeanteur, and J. M. Blanchard. 1985. Various rat adult tissues express only one major mRNA species from the glyceraldehyde-3-phosphate-dehydrogenase multigenic family. Nucleic Acids Res. 13:1431-1442.
19. Fukunaga, R., E. Ishizaka-Ikeda, and S. Nagata. 1993. Growth and differentiation signals mediated by different regions in the cytoplasmic domain of granulocyte colony-stimulating factor receptor. Cell 74:1079-1087.
20. Funabiki, T., B. L. Kreider, and J. N. Ihle. 1994. The carboxyl domain of zinc fingers of the Evi-1 myeloid transforming gene binds a consensus sequence of GAAGATGAG. Oncogene 9:1575-1581.
21. Furukawa, K., Y. Yamaguchi, E. Ogawa, K. Shigesada, M. Satake. and Y. Ito. 1990. A ubiquitous repressor interacting with an F9 cell-specific silencer and its functional suppression by differentiated cell-specific positive factors. Cell Growth Differ. 1:135-147.
22. Garriga, G., C. Guenther, and H. R. Horvitz. 1993. Migration of the Caenorhabditis elegans HSNs are regulated by egl-43, a gene encoding two zinc finger proteins. Genes Dev. 7:2097-2109.
23. Goldstone, S. D., and M. F. Lavin. 1994. Prolonged expression of c-jun and associated activity of the transcription factor AP-1, during apoptosis in a human leukaemic cell line. Oncogene 9:2305-2311.
24. Grigoriadis, A. E., K. Schellander, Z. Q. Wang, and E. F. Wagner. 1993. Osteoblasts are target cells for transformation in c-fos transgenic mice. J. Cell Biol. 122:685-701.
25. 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.
26. Kakizuka, A., W. Miller, Jr., K. Umesono, R. Warrell, Jr., S. R. Frankel, V. V. Murty, E. Dmitrovsky, and R. M. Evans. 1991. Chromosomal translocation t(15;17) in human acute promyelocytic leukemia fuses RARα with a novel putative transcription factor, PML. Cell 66:663-674.
27. Kamps, M. P., C. Murre, X. H. Sun, and D. Baltimore. 1990. A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL. Cell 60:547-555.
28. Kania, M. A., K. B. Bonner, J. B. Duffy, and J. P. Gergen. 1990. The Drosophila segmentation gene runt encodes a novel nuclear regulatory protein that is also expressed in the developing nervous system. Genes Dev. 4:1701-1713.
29. Kingston, R. E., C. A. Chen, and H. Okayama. 1990, Calcium phosphate transfection, p. 9.1.1.-9.1.7. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 1. Greene Publishing Associates and Wiley-Interscience, New York.
30. Koken, M. H. M., F. Puvion-Dutilleul, M. C. Guillemin, A. Viron, G. Linares-Cruz, N. Stuurman, L. deJong, C. Szostecki, F. Calvo, C. Chomienne, L. Degos, E. Puvion, and H. deThe. 1994. The t(15;17) translocation alters a nuclear body in a retinoic acid-reversible fashion. EMBO J. 13:1073-1083.
31. Kunkel, T. A., J. D. Roberts, and R. A. Zakour. 1987. Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol. 154:367-382.
32. Kurokawa, M., S. Ogawa, T. Tanaka, K. Mitani, Y. Yazaki, O. N. Witte, and H. Hirai. Submitted for publication.
33. 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 CBFβ/ PEBP2β and a myosin heavy chain in acute myeloid leukemia. Science 261:1041-1044.
34. Marti, A., B. Jehn, E. Costello, N. Keon, G. Ke, F. Martin, and R. Jaggi. 1994. Protein kinase A and AP-1 (c-Fos/JunD) are induced during apoptosis of mouse mammary epithelial cells. Oncogene 9:1213-1223.
35. Meyers, S., J. R. Downing, and S. W. Hiebert. 1993. Identification of AML-1 and the (8;21) translocation protein (AML-1/ETO) as sequence-specific DNA-binding proteins: the runt homology domain is required for DNA binding and protein-protein interactions. Mol. Cell. Biol. 13:6336-6445.
36. Migliaccio, G., A. R. Migliaccio, B. L. Kreide, G. Rovera, and J. W. Adamson. 1989. Selection of lineage-restricted cell lines immortalized at different stages of hematopoietic differentiation from the murine cell line 32D. J. Cell Biol. 109:833-841.
37. Miller, A. D., T. Curran, and I. M. Verma. 1984. c-fos protein can induce cellular transformation: a novel mechanism of activation of a cellular oncogene. Cell 36:259-268.
38. Mitani, K., S. Ogawa, T. Tanaka, H. Miyoshi, M. Kurokawa, H. Mano, Y. Yazaki, M. Ohki, and H. Hirai. 1994. Generation of the AML1-Evi-1 fusion gene in the t(3;21)(q26;q22) causes blastic crisis in chronic myelocytic leukemia. EMBO J. 13:504-510.
39. 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.
40. Miyoshi, H., M. Ohira, K. Shimizu, K. Mitani, H. Hirai, T. Imai, K. Yokoyama, E. Soeda, and M. Ohki. Submitted for publication.
41. Miyoshi, H., K. Shimizu, T. Kozu, N. Maskeki, Y. Kaneko, and M. Ohki. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia arc clustered within a limited region of a single gene. AML1. Proc. Natl. Acad. Sci. USA 88:10431-10434.
42. Morishita, K., E. Parganas, E. C. Douglass, and J. N. Ihle. 1990. Unique expression of the human Evi-1 gene in an endometrial carcinoma cell line: sequence of cDNAs and structure of alternatively spliced transcripts. Oncogene 5:963-971.
43. Morishita, K., E. Parganas, T. Matsugi, and J. N. Ihle. 1992. Expression of the Evi-1 zinc finger gene in 32Dcl3 myeloid cells blocks granulocytic differentiation in response to granulocyte colony-stimulating factor. Mol. Cell. Biol. 12:183-189.
44. Morishita, K., E. Parganas, D. M. Parham, T. Matsugi, and J. N. Ihle. 1990. The Evi-1 zinc finger myeloid transforming gene is normally expressed in the kidney and in developing oocytes. Oncogene 5:1419-1923.
45. Morishita, K., E. Parganas, C. L. William, M. H. Whittaker, H. Drabkin, J. Oval, R. Taetle, M. B. Valentine, and J. N. Ihle. 1992. Activation of EVI1 gene expression in human acute myelogenous leukemias by translocations spanning 300-400 kilobases on chromosome band 3q26. Proc. Natl. Acad. Sci. USA 89:3937-3941.
46. Morishita, K., D. S. Parker, M. L. Mucenski, N. A. Jenkins, N. G. Copeland, and J. N. Ihle. 1988. Retroviral activation of a novel gene encoding a zinc finger protein in IL-3-dependent myeloid leukemia cell lines. Cell 54:831-840.
47. Mucenski, M. L., B. A. Taylor, J. N. Ihle, J. W. Hartley, H. Morse, III, N. A. Jenkins, and N. G. Copeland. 1988. Identification of a common ecotropic viral integration site, Evi-1, in the DNA of AKXD murine myeloid tumors. Mol. Cell. Biol. 8:301-308.
48. Nichols. J., and S. D. Nimer. 1992. Transcription factors, translocations, and leukemia. Blood 80:2953-2963.
49. Nourse, J., J. D. Mellentin, N. Galili, J. Wilkinson, E. Stanbridge, S. D. Smith, and M. L. Cleary. 1990. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor. Cell 60:535-545.
50. Nucifora, G., C. R. Begy, H. Kobayashi, D. Roulston, D. Claxton, J. Pedersen-Bjergaard, E. Parganas, J. N. Ihle, and J. D. Rowley. 1994. Consistent intergenic splicing and production of multiple transcripts between AML1 at 21q22 and unrelated genes at 3q26 in (3;21 )(q26;q22) translocations. Proc. Natl. Acad. Sci. USA 91:4004-4008.
51. Ogawa, E., M. Inuzuka, M. Maruyama, M. Satake, M. Naito-Fujimoto, Y. Ito, and K. Shigesada. 1993. Molecular cloning and characterization of PEBP2β, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2α. Virology 194:314-331.
52. Ogawa, E., M. Maruyama, H. Kagoshima, M. Inuzuka, J. Lu, M. Satake, K. Shigesada, and Y. Ito. 1993. PEBP2/PEA2 represents a family of transcription factors homologous to the products of the Drosophila runt gene and the human AML1 gene. Proc. Natl. Acad. Sci. USA 90:6859-6863.
53. Oval, J., M. Smedsrud, and R. Taetle. 1992. Expression and regulation of the evi-1 gene in the human factor-dependent leukemia cell line, UCSD/AML1. Leukemia 6:446-451.
54. Piette, J., and M. Yaniv. 1987. Two different factors bind to the α-domain of the polyoma virus enhancer, one of which also interacts with the SV40 and c-fos enhancers. EMBO J. 6:1331-1337.
55. Potter, H. 1990. Transfection by electroporation, p. 9.3.1.-9.3.4. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 1. Greene Publishing Associates and Wiley-Interscience, New York.
56. Rubin, C. M., R. A. J. Larson, J. N. Anastasi-Winter, M. Thangavelu, J. W. Vardiman, J. D. Rowley, and M. M. Le Beau. 1990. t(3;21)(q26;q22): a recurring chromosomal abnormality in therapy-related myelodysplastic syndrome and acute myeloid leukemia. Blood 76:2594-2598.
57. Rudnicki, M. A., and M. W. McBurney. 1987. Cell culture methods and induction of differentiation of embryonal carcinoma cell lines, p. 19-49. In E. J. Robertson (ed.), Teratocarcinomas and embryonic stem cells. IRL Press. Oxford.
58. Sadowski, I., J. Ma, S. Triezenberg, and M. Ptashne. 1988. GAL4-VP16 is an unusually potent transcriptional activator. Nature (London) 335:563-564.
59. Satake, M., T. Ibaraki, and Y. Ito. 1988. Modulation of polyomavirus enhancer binding proteins by Ha-ras oncogene. Oneogene 3:69-78.
60. Satake, M., M. Inuzuka, K. Shigesada, T. Oikawa, and Y. Ito. 1992. Differential expression of subspecies of polyomavirus and murine leukemia virus enhancer core binding protein, PEBP2, in various hematopoietic cells. Jpn. J. Cancer Res. 83:714-722.
61. Schneider, N. R., W. P. Bowman, and E. P. Frenkel. 1991. Translocation (3;21)(q26;q22) in secondary leukemia. Ann. Genet. 34:256-263.
62. Selden, R. F. 1990. Transfection using DEAE-dextran, p. 9.2.1.-9.2.6. In F. M. Ausubel, R. Brent, R. E. Kingston, D. D. Moore, J. G. Seidman, J. A. Smith, and K. Struhl (ed.), Current protocols in molecular biology, vol. 1. Greene Publishing Associates and Wiley-Interscience, New York.
63. Takebe, Y., M. Seiki, J. Fujisawa, P. Hoy, K. Yokota, K. Arai, M. Yoshida, and N. Arai. 1988. SRα promoter: an efficient and versatile mammalian cDNA expression system composed of the simian virus 40 early promoter and the R-U5 segment of human T-cell leukemia virus type 1 long terminal repeat. Mol. Cell. Biol. 8:466-472.
64. Tanaka, T., et al. Unpublished data.
65. Tanaka, T., J. Nishida, K. Mitani, S. Ogawa, Y. Yazaki, and H. Hirai. 1994. Evi-1 raises AP-1 activity and stimulates c-fos promoter transactivation with dependence on the second zinc finger domain. J. Biol. Chem. 269:24020-24026.
66. Tanaka, T., F. Shibasaki, M. Ishikawa, N. Hirano, R. Sakai, J. Nishida, T. Takenawa, and H. Hirai. 1992. Molecular cloning of bovine actin-like protein, actin2. Biochem. Biophys. Res. Commun. 187:1022-1028.
67. Tanaka, T., K. Tanaka, S. Ogawa, M. Kurokawa, K. Mitani, J. Nishida, Y. Shibata, Y. Yazaki, and H. Hirai. 1995. An acute myeloid leukemia gene, AML1, regulates hemopoietic myeloid cell differentiation and transcriptional activation antagonistically by two alternative spliced forms. EMBO J. 14: 341-350.
68. von Lindern, M., M. Fornerod, N. Soekarman, S. van Baal, M. Jaegle, A. Hagemeijer, D. Bootsma, and G. Grosveld. 1992. Translocation t(6;9) in acute non-lymphocytic leukaemia results in the formation of a DEK-CAN fusion gene. Baillieres Clin. Haematol. 5:857-879.
69. 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.
70. Weis, K., S. Rambaud, C. Lavau, J. Jansen, T. Carvalho, M. Carmo-Fonseca, A. Lamond, and A. Dejean. 1994. Retinoic acid regulates aberrant nuclear localization of PML-RARα in acute promyelocytic leukemic cells. Cell 76: 345-356.