A novel transcript encoding an N-terminally truncated AML1/PEBP2αB protein interferes with transactivation and blocks granulocytic differentiation of 32Dc13 myeloid cells

Molecular and Cellular Biology

Volumn 17, Issue 7, 1997, Pages 4133-4145

  Zhang, Yu Wen ^a   Bae, Suk Chul ^a   Huang, Gang ^a   Fu, Yang Xin ^a   Lu, Jie ^a   Ahn, Mee Young ^a   Kanno, Yuka ^a   Kanno, Tomohiko ^a   Ito, Yoshiaki ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

GENE PRODUCT; GRANULOCYTE COLONY STIMULATING FACTOR; MUTANT PROTEIN; RIBONUCLEASE; TRANSCRIPTION FACTOR;

ADULT; ALTERNATIVE RNA SPLICING; AMINO TERMINAL SEQUENCE; ARTICLE; BONE MARROW CELL; CELL DIFFERENTIATION; CONTROLLED STUDY; FETUS LIVER; GENE REARRANGEMENT; GRANULOCYTE; HEMATOPOIESIS; HUMAN; HUMAN CELL; LYMPHOID CELL; PRIORITY JOURNAL; PROTEIN DNA BINDING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; T CELL LEUKEMIA; TRANSACTIVATION;

EID: 0030927824     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/mcb.17.7.4133     Document Type: Article

References (73)

1. Adams, R. A., A. Flowers, and B. J. Davis. 1968. Direct implantation and serial transplantation of human acute lymphoblastic leukemia in hamsters, SB-2. Cancer Res. 28:1121-1125.
2. Asou, H., S. Tashiro, K, Hamamoto, A. Otsuji, K. Kita, and N. Kamada. 1991. Establishment of a human acute myeloid leukemia cell line (Kasumi-1) with 8;21 chromosome translocation. Blood 77:2031-2036.
3. 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.
4. Bae, S. C., E. Takahashi, Y. W. Zhang, E. Ogawa, K. Shigesada, Y. Namba, M. Satake, and Y. Ito. 1995. Cloning, mapping and expression of PEBP2αC, a third gene encoding the mammalian Runt domain. Gene 159:245-248.
5. Bae, S. C., and Y. Ito. Unpublished data.
6. 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.
7. Britos-Bray, M., N. Sacchi, and A. D. Friedman. 1996. DNA-binding domain of AML1, expressed in t(8; 21) and t(3; 21) myeloid leukemias, inhibits PEBP2/CBF DNA-binding but is not sufficient to transform 32Dcl3 myeloid cells. Leukemia 10:984-990.
8. Chen, C., and H. Okayama. 1987. High-efficiency transformation of mammalian cells by plasmid DNA. Mol. Cell. Biol. 7:2745-2752.
9. Chen, L. F., and Y. Ito. Unpublished data.
10. Collins, S. J., R. C. Gallo, and R. E. Gallagher. 1977. Continuous growth and differentiation of human myeloid leukaemic cells in suspension culture. Nature (London) 270:347-349.
11. Daga, A., C. A. Karlovich, K. Dumstrei, and U. Banerjee. 1996. Patterning of cells in the Drosophila eye by lozenge, which shares homologous domains with AML1. Genes Dev. 10:1194-1205.
12. Danos, O., and R. C. Mulligan. 1988. Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges. Proc. Natl. Acad. Sci. USA 85:6460-6464.
13. Foulkes, N. S., and P. Sassone-Corsi. 1992. More is better: activators and repressors from the same gene. Cell 68:411-414.
14. Friedman, A. D., B. L. Krieder, D. Venturelli, and G. Rovera. 1991. Transcriptional regulation of two myeloid-specific genes, myeloperoxidase and lactoferrin, during differentiation of the murine cell line 32D C13. Blood 78:2426-2432.
15. Giese, K., C. Kingsley, J. R. Kirshner, and R. Grosschedl. 1995. Assembly and function of a TCRα enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev. 9:995-1008.
16. Hanada, S., F. Tsubai, and Y. Namba. 1987. The characterization of T-cell lines derived from peripheral blood of patients with adult T-cell leukemia/ lymphoma. Recent Adv. RES Res. 25:124-133.
17. Hansen, J. A., P. J. Martin, and R. C. Nowinski. 1980. Monoclonal antibodies identifying a novel T-cell antigen and Ia antigens of human lymphocytes. Immunogenetics 10:247-260.
18. Hernandez-Munain, C., and M. S. Krangel. 199S. c-Myb and core-binding factor/PEBP2 display functional synergy but bind independently to adjacent sites in the T-cell receptor δ enhancer. Mol. Cell. Biol. 15:3090-3099.
19. Hiebert, S. W., W. Sun, J. N. Davis, T. Golub, S. Shurtleff, A. Buijs, J. R. Downing, G. Grosveld, M. F. Roussel, D. G. Gilliland, N. Lenny, and S. Meyers. 1996. The t(12;21) translocation converts AML-1B from an activator to a represser of transcription. Mol. Cell. Biol. 16:1349-1355.
20. Hinuma, Y., M. Konn, J. Yamaguchi, D. J. Wudarski, J. R. Blakeslee, Jr., and J. T. Grace, Jr. 1967. Immunofluorescence and herpes-type virus particles in the P3HR-1 Burkitt lymphoma cell line. J. Virol. 1:1045-1051.
21. Ito, Y. 1996. Structural alterations in the transcription factor PEBP2/CBF linked to four different types of leukemia. J. Cancer Res. Clin. Oncol. 122:266-274.
22. Ito, Y., and S. C. Bae. The Runt domain transcription factor, PEBP2/CBF, and its involvement in human leukemia. In J. Ghysdael and M. Yaniv (ed.), Oncogenes as transcriptional regulators, in press. Birkhauser Verlag Publisher, Basel, Switzerland.
23. Kagoshima, H., Y. Akamatsu, Y. Ito, and K. Shigesada. 1996. Functional dissection of the α and β subunits of transcription factor PEBP2 and the redox susceptibility of its DNA binding activity. J. Biol. Chem. 271:33074-33082.
24. Kagoshima, H., K. Shigesada, M. Satake, Y. Ito, H. Miyoshi, M. Ohki, M. Pepling, and P. Gergen. 1993. The Runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet. 9:338-341.
25. Kamachi, Y., E. Ogawa, M. Asano, S. Ishida, Y. Murakami, M. Satake, Y. Ito, and K. Shigesada. 1990. Purification of a mouse nuclear factor that binds to both the A and B cores of the polyomavirus enhancer. J. Virol. 64:4808-4819.
26. Kania, M. A., A. S. 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.
27. Kim, Y. H., and Y. Ito. Unpublished data.
28. Kim, K. J., C. Kanellopoulos-Langevin, R. M. Merwin, D. H. Sachs, and R. Asofsky. 1979. Establishment and characterization of BALB/c lymphoma lines with B cell properties. J. Immunol. 122:549-554.
29. Kozak, M. 1987. An analysis of 5'-noncoding sequences from 699 vertebrate messenger RNAs. Nucleic Acids Res. 15:8125-8148.
30. Levanon, D., V. Negreanu, Y. Bernstein, I. Bar-Am, L. Avivi, and Y. Groner. 1994. AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23:425-432.
31. 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.
32. Lozzio, C. B., and B. B. Lozzio. 1975. Human chronic myelogenous leukemia cell-line with positive Philadelphia chromosome. Blood 45:321-330.
33. Lu, J., M. Maruyama, M. Satake, S. C. Bae, E. Ogawa, H. Kagoshima, K. Shigesada, and Y. Ito. 1995. Subcellular localization of the a and β subunits of the acute myeloid leukemia-linked transcription factor PEBP2/CBF. Mol. Cell. Biol. 15:1651-1661.
34. Mann, R-, R. C. Mulligan, and D. Baltimore. 1983. Construction of a retrovirus package mutant and its use to produce helper-free defective retrovirus. Cell 33:153-159.
35. McBurney, M. W., and B. J. Rogers. 1982. Isolation of male embryonal carcinoma cells and their chromosome replication patterns. Dev. Biol. 89: 503-508.
36. Meyer, S., N. Lenny, and S. W. Hiebert. 1995. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974-1982.
37. Migliaccio, G., A. R. Migliaccio, B. L. Kreider, 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.
38. Minowada, J., T. Ohnuma, and G. E. Moore. 1972. Brief communication: rosette-forming human lymphoid cell lines. 1. Establishment and evidence for origin of thymus-derived lymphocytes. J. Natl. Cancer Inst. 49:891-895.
39. Miyoshi, H., K. Shimizu, T. Kozu, N. Maseki, Y. Kaneko, and M. Ohki. 1991. t(8;21) breakpoints on chromosome 21 in acute myeloid leukemia are clustered within a limited region of a single gene, AML1. Proc. Natl. Acad. Sci. USA 88:10431-10434.
40. Miyoshi, H., M. Ohira, K. Shimizu, K. Mitani, H. Hirai, T. Imai, K. Yokoyama, E. Soeda, and M. Ohki. 1995. Alternative splicing and genomic structure of the AML1 gene involved in acute myeloid leukemia. Nucleic Acids Res. 23:2762-2769.
41. Mizushima, S., and S. Nagata. 1990. pEF-BOS, a powerful mammalian expression vector. Nucleic Acids Res. 18:5322.
42. Morgenstern, J. P., and H. Land. 1990. Advanced mammalian gene transfer: high titre retroviral vectors with multiple drug selection markers and a complementary helper-free packaging cell line. Nucleic Acids Res. 18:3587-3596.
43. Morikawa, S., E. Tatsumi, M. Baba, T. Harada, and K. Yasuhira. 1978. Two E-rosette-forming lymphoid cell lines. Int. J. Cancer 21:166-170.
44. Niki, M., H. Okada, H. Takano, J. Kuno, K. Tani, H. Hibino, S. Asano, Y. Ito, M. Satake, and T. Noda. Hematopoiesis in the fetal liver is impaired by the targeted mutagenesis of the gene encoding a non-DNA binding subunit of the transcription factor, PEBP2/CBF. Proc. Natl. Acad. Sci. USA, in press.
45. Nuchprayoon, I, S. Meyers, L. M. Scott, J. Suzow, S. W. Hiebert, and A. D. Friedman. 1994. PEBP2/CBF, the murine homolog of the human myeloid AML1 and PEBP2β/CBFβ proto-oncoproteins, regulates the murine myeloperoxidase and neutrophil elastase genes in immature myeloid cells. Mol. Cell. Biol. 14:5558-5568.
46. Nucifora, G., and J. D. Rowley. 1995. AML1 and the 8;21 and 3:21 translocations in acute and chronic myeloid leukemia. Blood 86:1-14.
47. 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.
48. Ogawa, E., and Y. Ito. Unpublished data.
49. Ogawa, E., M. Maruyama, H. Kagoshima, M. Inuzuka, J. Lu, M. Satake, K. Shigesada, and Y. Ito. 1993. PEBP2/PEA2 represents a new 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.
50. Okada, H., M. Niki, Y. Ito, M. Satake, and T. Noda. Unpublished data.
51. Okuda, T., J. van-Deursen, S. W. Hiebert, G. Grosveld, and J. R. Downing. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell 84:321-330.
52. Pagano, M., M. Durst, S. Joswig, G. Draetta, and P. Jansen-Durr. 1992. Binding of the human E2F transcription factor to the retinoblastoma protein but not to cyclin A is abolished in HPV-16-immortalized cells. Oncogene 7:1681-1686.
53. Sakakura, C., Y. Yamaguchi-Iwai, M. Satake, S. C. Bae, A. Takahashi, E. Ogawa, A. Hagiwara, T. Takahashi, A. Murakami, K. Makino, T. Nakagawa, N. Kamada, and Y. Ito. 1994. Growth inhibition and induction of differentiation of t(8;21) acute myeloid leukemia cells by the DNA-binding domain of PEBP2 and the AML1/MTG8(ETO)-specific antisense oligonucleotide. Proc. Natl. Acad. Sci. USA 91:11723-11727.
54. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
55. Sasaki, K., H. Yagi, R. T. Bronson, K. Tominaga, T. Matsunashi, K. Deguchi, Y. Tani, T. Kishimoto, and T. Komori. Absence of fetal liver hematopoiesis in transcriptional co-activator, core binding factor β (Cbfb) deficient mice. Submitted for publication.
56. Satake, M., T. Ibaraki, and Y. Ito. 1988. Modulation of polyomavirus enhancer binding proteins by Ha-ras oncogene. Oncogene 3:69-78.
57. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67:31-40.
58. Sun, W., B. J. Graves, and N. A. Speck. 1995. Transactivation of the Moloney murine leukemia virus and T-cell receptor β-chain enhancers by cbf and ets requires intact binding sites for both proteins. J. Virol. 69:4941-4949.
59. Takahashi, A., M. Satake, Y. Yamaguchi-Iwai, S. C. Bae, J. Lu, M. Maruyama, Y. W. Zhang, H. Oka, N. Arai, K. Arai, and Y. Ito. 1995. Positive and negative regulation of granulocyte-macrophage colony-stimulating factor promoter activity by AML1-related transcription factor, PEBP2. Blood 86: 607-616.
60. Tanaka, T., K. Mitani, M. Kurokawa, S. Ogawa, K. Tanaka, J. Nishida, Y. Yazaki, Y. Shibata, and H. Hirai. 1995. Dual functions of the AML1/Evi-1 chimeric protein in the mechanism of leukemogenesis in t(3;21) leukemias. Mol. Cell. Biol. 15:2383-2392.
61. 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 transcripional activation antagonistically by two alternative spliced forms. EMBO J. 14: 341-350.
62. Tanaka, T., M. Kurokawa, K. Ueki, K. Tanaka, Y. Imai, K. Mitani, K. Okazaki, N. Sagata, Y. Yazaki, Y. Shibata, T. Kadowaki, and H. Hirai. 1996. The extracellular signal-regulated kinase pathway phosphorylates AML1. an acute myeloid leukemia gene product, and potentially regulates its transactivation ability. Mol. Cell. Biol. 16:3967-3979.
63. Taniguchi, T., H. Matsui, T. Fujita, C. Takaoka, N. Kashima, R. Yoshimoto, and J. Hamuro. 1983. Structure and expression of a cloned cDNA for human interleukin-2. Nature 302:305-310.
64. Valtieri, M., D. J. Tweardy, D. Caracciolo, K. Johnson, F. Mavilio, S. Altmann, D. Santoli, and G. Rovera. 1987. Cytokine-dependent granulocytic differentiation: regulation of proliferative and differentiative responses in a murine progenitor cell line. J. Immunol. 138:3829-3835.
65. Wang, Q., T. Stacy, J. D. Miller, A. F. Lewis, T. L. Gu, X. Huang, J. H. Bushweller, J. C. Bories, F. W. Alt, G. Ryan, P. P. Liu, A. Wynshaw-Boris. M. Binder, M. Marin-Padilla, A. H. Sharpe, and N. A. Speck. 1996. The CBFβ subunit is essential for CBFα2 (AML1) function in vivo. Cell 87:697-708.
66. Wang, Q., T. Stacy, M. Binder, M. Marin-Padilla, A. H. Sharpe, and N.A Speck. 1996. Disruption of the cbfα2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. USA 93:3444-3449.
67. 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. Mo1. Cell. Biol. 13:3324-3339.
68. Warner, N. L., M. A. S. Moore, and D. Metcalf. 1969. A transplantable myelomonocytic leukemia in BALB/c mice: cytology, karyotype, and muramidase content. J. Natl. Cancer lost. 43:963-982.
69. Wijimenga, C., N. A. Speck, N. C. Dracopoli, M. H. Hofker, P. Liu, and F. S. Collins. 1995. Identification of a new murine runt domain-containing gene, cbf3, and localization of the human homolog, CBFA3, to chromosome 1p35-pter. Genomics 26:611-614.
70. Wotton, D., J. Ghysdael, S. Wang, N. A. Speck, and M. J. Owen. 1994. Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 14:840-850.
71. 4Eo. Blood 78:451-457.
72. Zhang, D. E., C. J. Hetherington, S. Meyers, K. L. Rhoades, C. J. Larson, H. M. Chen, S. W. Hietert, and D. G. Tenen. 1996. CCAAT enhancer-binding protein (C/EBP) and AML1 (CBFα2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16:1231-1240.
73. Zhang, Y. W., and Y. Ito. Unpublished data.