AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis

Cell

Volumn 84, Issue 2, 1996, Pages 321-330

  Okuda, Tsukasa ^a   Van Deursen, Jan ^a   Hiebert, Scott W ^a   Grosveld, Gerard ^a   Downing, James R ^a  

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

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR RUNX1; UNCLASSIFIED DRUG;

ARTICLE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ERYTHROID CELL; FETUS; GENE EXPRESSION REGULATION; GENE MUTATION; GENE REARRANGEMENT; GENE TARGETING; HEMATOPOIESIS; HOMOZYGOSITY; HUMAN; HUMAN CELL; LEUKEMOGENESIS; LIVER DEVELOPMENT; PRIORITY JOURNAL;

ANIMALIA;

EID: 0030061554     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)80986-1     Document Type: Article

References (78)

1. Bae, S.C., Yamaguchi-Iwai, Y., Ogawa, E., Maruyama, M., Inuzuka, M., Kagoshima, H., Shigesada, K., Satake, M., and Ito, Y. (1993). Isolation of PEBP2βB cDNA representing the mouse homolog of human acute myeloid leukemia gene, AML1. Oncogene 8, 809-814.
2. Boral, A.L., Okenquist, S.A., and Lenz, J. (1989). Identification of the SL3-3 virus enhancer core as a T-lymphoma cell-specific element. J. Virol. 63, 76-84.
3. Daga, A., Tighe, J.E., and Calabi, F. (1992). Leukemia/Drosophila homology. Nature 356, 484.
4. Downing, J.R., Head, D.R., Curcio-Brint, A.M., Hulshof, M.G., Motroni, T.A., Raimondi, S.C., Corroll, A.J., Drabkin, H.A., Willman, C., Theil, K.S., Civin, C.I., and Erickson, P. (1993). An AML1/ETO fusion transcript is consistently detected by RNA-based polymerase chain reaction in acute myelogenous leukemia containing the (8;21)(q22;q22) translocation. Blood 81, 2860-2865.
5. Dranoff, G., Crawford, A.D., Sadelain, M., Ream, B., Rashid, A., Bronson, R.T., Dickersin, G.R., Bachurski, C.J., Mark, E.L., Whitsett, J.A., and Mulligan, R.C. (1994). Involvement of granulocyte-macrophage colony-stimulating factor in pulmonary homeostasis. Science 264, 713-715.
6. Duffy, J.B., and Gergen, J.P. (1991). The Drosophila segmentation gene runt acts as a position-specific numerator element necessary for the uniform expression of the sex-determining gene Sex-lethal. Genes Dev. 5, 2176-2187.
7. Erickson, P., Gao, J., Chang, K.S., Look, AT., Whisenant, E., Raimondi, S., Lasher, R., Trujillo, J., Rowley, J., and Drabkin, H. (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.
8. Gergen, J.P., and Wieschaus, E. (1985). The localized requirements for a gene affecting segmentation in Drosophila: analysis of larvae mosaic for runt. Dev. Biol. 109, 321-335.
9. Gergen, J.P., and Wieschaus, E. (1986). Dosage requirements for runt in the segmentation of Drosophila embryos. Cell 45, 289-299.
10. Golub, T.R., Barker, G.F., Bohlander, S.K., Hiebert, S.W., Ward, D.C., Bray-Ward, P., Morgan, E., Raimondi, S.C., Rowley, J.D., and Gilliland, D.G. (1995). Fusion of the TEL gene on 12p13 to the AML1 gene on 21q22 in acute lymphoblastic leukemia. Proc. Natl. Acad. Sci. USA 92, 4917-921.
11. Hajra, A., Liu, P.P., Speck, N.A., and Collins, F.S. (1995a). Overexpression of core-binding factor (CBF) reverses cellular transformation by the CBFβ-smooth muscle myosin heavy chain chimeric oncoprotein. Mol. Cell. Biol. 15, 4980-4989.
12. Hajra, A., Liu, P.P., Wang, Q., Kelley, C.A., Stacy, T., Adelstein, R.S., Speck, N.A., and Collins, F.S. (1995b). The leukemic core binding factor β-smooth muscle myosin heavy chain (CBFβ-SMMHC) chimeric protein requires both CBFβ and myosin heavy chain domains for transformation of NIH 3T3 cells. Proc. Natl. Acad. Sci. USA 92, 1926-1930.
13. Hernandez-Munain, C., and Krangel, M.S. (1995). c-Myb and core-binding factor/PEBP2 display functional synergy but bind independently to adjacent sites in the T-cell receptor enhancer. Mol. Cell. Biol. 15, 3090-3099.
14. Hsiang, Y.H., Spencer, D., Wang, S., Speck, N.A., and Raulet, D.H. (1993). The role of viral enhancer "core" motif-related sequences in regulating T cell receptor-γ and -δ gene expression. J. Immunol. 150, 3905-3916.
15. Ihle, J.N. (1992). Interleukin-3 and hematopoiesis. Chem. Immunol. 51, 65-106.
16. Kagoshima, H., Shigesada, K., Satake, M., Ito, Y., Miyoshi, H., Ohki, M., Pepling, M., and Gergen, P. (1993). The runt domain identifies a new family of heteromeric transcriptional regulators. Trends Genet. 9, 338-341.
17. Kamachi, T., Ogawa, E., Asano, M., Ishida, S., Murakami, Y., Satake, M., Ito, Y., and Shigesada, K. (1990). Purification of a mouse nuclear factor that binds both the A and B cores of the polyomavirus enhancer. J. Virol. 64, 4808-4819.
18. Kania, M.A., Bonner, A.S., Duffy, J.B., and Gergen, J.P. (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.
19. Keller, G., Kennedy, M., Papayannopoulou, T., and Wiles, M.V. (1993). Hematopoietic differentiation during embryonic stem cell differentiation in culture. Mol. Cell. Biol. 13, 472-486.
20. Levanon, D., Negreanu, V., Bernstein, Y., Bar-Am, I., Avivi, L., and Groner, Y. (1994). AML1, AML2, and AML3, the human members of the runt domain gene-family: cDNA structure, expression, and chromosomal localization. Genomics 23, 425-432.
21. Lieschke, G.J., Stanley, E., Grail, D., Hodgson, G., Sinickas, V., Gail, J.A.M., Sinclair, R.A., and Dunn, A.R. (1994). Mice lacking both macrophage- and granulocyte-macrophage colony-stimulating factor have macrophages and coexistent osteopetrosis and severe lung disease. Blood 84, 27-35.
22. Liu, P., Tarle, S.A., Hajra, A., Claxton, D.F., Marlton, P., Freedman, M., Siciliano, M.J., and Collins, F.S. (1993). Fusion between transcription factor CBFβ/PEBP2β and a myosin heavy chain in acute myeloid leukemia. Science 261, 1041-1044.
23. Liu, P.P., Hajra, A., Wijmenga, C., and Collins, F.S. (1995). Molecular pathogenesis of chromosome 16 inversion in the M4Eo subtype of acute myeloid leukemia. Blood 85, 2289-2302.
24. LoSardo, J.E., Boral, A.L., and Lenz, J. (1990). Relative importance of elements within the SL3-3 virus enhancer for T-cell specificity. J. Virol. 64, 1756-1763.
25. Manley, N.R., O'Connell, M., Sun, W., and Speck, N.A. (1993). Two factors that bind to highly conserved sequences in mammalian type C retroviral enhancers. J. Virol. 67, 1967-1975.
26. Meyers, S., and Hiebert, S.W. (1996). Indirect and direct disruption of transcriptional regulation in cancer, E2F and AML-1. Crit. Rev. Euk. Gene Expr., in press.
27. Meyers, S., Downing, J.R., and Hiebert, S.W. (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, 6336-6345.
28. Meyers, S., Lenny, N., and Hiebert, S.W. (1995). The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15, 1974-1982.
29. Mitani, K., Ogawa, S., Tanaka, T., Miyoshi, H., Kurokawa, M., Mano, H., Yazaki, Y., Ohki, M., and Hirai, H. (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.
30. Miyoshi, H., Shimizu, K., Kozu, T., Maseki, N., Kaneko, Y., and Ohki, M. (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.
31. Miyoshi, H., Kozu, T., Shimizu, K., Enomoto, K., Maseki, N., Kaneko, Y., Kamada, N., and Ohki, M. (1993). The t(8;21) translocation in acute myeloid leukemia results in production of an AML1-MTG8 fusion transcript. EMBO J. 12, 2715-2721.
32. Miyoshi, H., Ohira, M., Shimizu, K., Mitani, K., Hirai, H., Imai, T., Yokoyama, K., Soeda, E., and Ohki, M. (1995). Alternative splicing and genomic structure of the AML1 gene involved in acute myeloid leukemia. Nucl. Acids Res. 23, 2762-2769.
33. Mucenski, M.L., McLain, K., Kier, A.B., Swerdlow, S.H., Schreiner, C.M., Miller, T.A., Pietryga, D.W., Scott, W.J., and Potter, S. (1991). A functional c-myb gene is required for normal murine fetal hepatic hematopoiesis. Cell 65, 677-689.
34. Nisson, P.E., Watkins, P.C., and Sacchi, N. (1992). Transcriptionally active chimeric gene derived from the fusion of the AML1 gene and a novel gene on chromosome 8 in t(8;21) leukemic cells. Cancer Genet. Cytogenet. 63, 81-88.
35. Nuchprayoon, I., Meyers, S., Scott, L.M., Suzow, J., Hiebert, S., and Friedman, A.D. (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.
36. Nucifora, G., and Rowley, J.D. (1995). AML1 and the 8;21 and 3;21 translocations in acute and chronic myeloid leukemia. Blood 86, 1-14.
37. Nucifora, G., Begy, C.R., Erickson, P., Drabkin, H.A., and Rowley, J.D. (1993). The 3;21 translocation in myelodysplasia results in a fusion transcript between the AML1 gene and the gene for EAP, a highly conserved protein associated with the Epstein-Barr virus small RNA EBER 1. Proc. Natl. Acad. Sci. USA 90, 7784-7788.
38. Nucifora, G., Begy, C.R., Kobayashi, H., Roulston, D., Claxton, D., Pedersen-Bjergaard, J., Parganas, E., Ihle, J.N., and Rowley, J.D. (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.
39. Ogawa, E., Inuzuka, M., Maruyama, M., Satake, M., Naito-Fujimoto, M., Ito, Y., and Shigesada, K. (1993a). Molecular cloning and characterization of PEBP2β, the heterodimeric partner of a novel Drosophila runt-related DNA binding protein PEBP2 . Virology 194, 314-331.
40. Ogawa, E., Maruyama, M., Kagoshima, H., Inuzuka, M., Lu, J., Satake, M., Shigesada, K., and Ito, Y. (1993b). 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.
41. INK4b/MTS2 in pediatric acute lymphoblastic leukemia. Blood 85, 2321-2330.
42. Orkin, S.H. (1995). Transcription factors and hematopoietic development. J. Biol. Chem. 270, 4955-4958.
43. Pandolfi, P.P., Roth, M.E., Karis, A., Leonard, M.W., Dzierzak, E., Grosveld, F.G., Douglas, E., and Lindenbaum, M.H. (1995). Targeted disruption of the GATA-3 gene causes severe abnormalities in the nervous system and in fetal liver haematopoiesis. Nature Genet. 11, 40-44.
44. Pevny, L., Simon, M.C., Robertson, E., Klein, W.H., Tsai, S.-F., D'Agati, V., Orkin, S.H., and Costantini, F. (1991). Erythroid differentiation in chimaeric mice blocked by a targeted mutation in the gene for transcription factor GATA-1. Nature 349, 257-260.
45. Prasser, H.M., Wotton, D., Gegonne, A., Ghysdael, J., Wang, S., Speck, N.A., and Owen, M.J. (1992). A phorbol ester response element within the human T-cell receptor β-chain enhancer. Proc. Natl. Acad. Sci. USA 89, 9934-9938.
46. Pui, C.-H. (1995). Childhood leukemias. N. Engl. J. Med. 332, 1618-1630.
47. Rabbitts, T.H. (1994). Chromosomal translocations in human cancer. Nature 372, 143-149.
48. Redondo, J.M., Pfohl, J.L., Hernandez-Munain, C., Wang, S., Speck, N.A., and Krangel, M.S. (1992). Indistinguishable nuclear factor binding to functional core sites of the T-cell receptor δ and murine leukemia virus enhancers. Mol. Cell. Biol. 12, 4817-4823.
49. Romana, S.P., Mauchauffe, M., Le Coniat, M., Chumakov, I., Le Paslier, D., Berger, R., and Bernard, O.A. (1995a). The t(12;21) of acute lymphoblastic leukemia results in a tel-AML1 gene fusion. Blood 85, 3662-3670.
50. Romana, S.P., Poirel, H., Le Coniat, M., Flexor, M.-A., Mauchauffe, M., Jonveaux, P., Macintyre, E.A., Berger, R., and Bernard, O.A. (1995b). High frequency of t(12;21) in childhood B lineage acute lymphoblastic leukemia. Blood, 86, 4263-4269.
51. Satake, M., Nomura, S., Yamaguchi-Iwai, Y., Takahama, Y., Hashimoto, Y., Niki, M., Kitamura, Y., and Ito, Y. (1995). Expression of the runt domain-encoding PEBP2 genes in T-cells during thymic development. Mol. Cell. Biol. 15, 1662-1670.
52. Scott, E.W., Simon, M.C., Anastasi, J., and Singh, H. (1994). Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science 265, 1573-1577.
53. Shivdasani, R.A., Mayer, E.L., and Orkin, S.H. (1995). Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373, 432-434.
54. Shoemaker, S.G., Hromas, R., and Kaushansky, K. (1990). Transcriptional regulation of interleukin 3 gene expression in T lymphocytes. Proc. Natl. Acad. Sci. USA 87, 9650-9654.
55. Shurtleff, S.A., Meyers, S., Hiebert, S.W., Raimondi, S.C., Head, D.R., Willman, C.L., Wolman, S., Slovak, M.L., Carroll, A.J., Behm, F., Hulshof, M.G., Motroni, T.A., Okuda, T., Liu, P., Collins, F.S., and Downing, J.R. (1995a). Heterogeneity in CBFB/MYH11 fusion messages encoded by the inv(16)(p13q22) and the t(16;16)(p13;q22) in acute myelogenous leukemia. Blood 85, 3695-3703.
56. Shurtleff, S.A., Buijs, A., Behm, F.G., Rubnitz, J.E., Raimondi, S.C., Hancock, M.L., Chan, G.C.-H., Pui, C.-H., Grosveld, G., and Downing, J.R. (1995b). TEL/AML1 fusion resulting from a cryptic t(12;21) is the most common genetic lesion in pediatric ALL and defines a subgroup of patients with an excellent prognosis. Leukemia, in press.
57. Simon, M.C., Pevny, L., Wiles, M.V., Keller, G., Costantini, F., and Orkin, S.H. (1992). Rescue of erythroid development in gene targeted GATA-1-mouse embryonic stem cells. Nature Genet. 1, 92-98.
58. Smith, A.G., and Hooper, M.L. (1987). Buffalo rat liver cells produce a diffusible activity which inhibits the differentiation of murine embryonal carcinoma and embryonic stem cells. Dev. Biol. 121, 1-9.
59. Sonoda, Y., Okuda, T., Yokota, S., Maekawa, T., Shizumi, Y., Nishigaki, H., Misawa, S., Fujii, H., and Abe, T. (1990). Actions of human interleukin-4/B-cell stimulatory factor-1 on proliferation and differentiation of enriched hematopoietic progenitor cells in culture. Blood 75, 1615-1621.
60. Speck, N.A., Renjifo, B., Golemis, E., Fredrickson, T.N., Hartley, J.W., and Hopkins, N. (1990). Mutation of the core or adjacent LVb elements of the Moloney murine leukemia virus enhancer alters disease specificity. Genes Dev. 4, 233-242.
61. Stanley, E., Lieschke, G.J., Grail, D., Metcalf, D., Hodgson, G., Gall, J.A., Maher, D.W., Cebon, J., Sinickas, V., and Dunn, A.R. (1994). Granulocyte/macrophage colony-stimulating factor-deficient mice show no major perturbation of hematopoiesis but develop a characteristic pulmonary pathology. Proc. Natl. Acad. Sci. USA 91, 5592-5596.
62. Sun, W., O'Connell, M., and Speck, N.A. (1993). Characterization of a protein that binds multiple sequences in mammalian type C retrovirus enhancers. J. Virol. 67, 1976-1986.
63. Takahashi, A., Satake, M., Yamaguchi-Iwai, Y., Bae, S.C., Lu, J., Maruyama, M., Zhang, Y.W., Oka, H., Arai, N., Arai, K., and Ito, Y. (1995). Positive and negative regulation of granulocyte-macrophage colony-stimulating factor promoter activity by AML1-related transcription factor, PEBP2. Blood 86, 607-616.
64. Tsai, F.-Y., Keller, G., Kuo, F.C., Weiss, M., Chen, J., Rosenblatt, M., Alt, F.W., and Orkin, S.H. (1994). An early haematopoietic defect in mice lacking the transcription factor GATA-2. Nature 371, 221-226.
65. van Deursen, J., and Weiringa, B. (1992). Targeting of the creatine kinase M gene in embryonic stem cells using isogenic and nonisogenic vectors. Nucl. Acids Res. 20, 3815-3820.
66. van Deursen, J., Lovell-Badge, R., Oerlemans, F., Schepens, J., and Weiringa, B. (1991). Modulation of gene activity by consecutive gene targeting of one creatine kinase M allele in mouse embryonic stem cells. Nucl. Acids Res. 19, 2637-2643.
67. van Deursen, J., Schepens, J., Peters, W., Meijer, D., Grosveld, G., Hendriks, W., and Weiringa, B. (1992). Genetic variability of the murine creatine kinase B gene locus and related pseudogenes in different inbred strains of mice. Genomics 12, 340-349.
68. Wang, S., Wang, Q., Crute, B.E., Melnikova, I.N., Keller, S.R., and Speck, N.A. (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.
69. Warren, A.J., Colledge, W.H., Carlton, M.B.L., Evans, M.J., Smith, A.J.H., and Rabbitts, T.H. (1994). The oncogenic cysteine-rich LIM domain protein Rbtn2 is essential for erythroid development. Cell 78, 45-57.
70. Weiher, H., Konig, M., and Gruss, P. (1983). Multiple point mutations affecting the simian virus 40 enhancer. Science 219, 626-631.
71. Weiss, M.J., Keller, G., and Orkin, S.H. (1994). Novel insights into erythroid development revealed through in vitro differentiation of GATA-1-embryonic stem cells. Genes Dev. 8, 1184-1197.
72. Wiles, M.V., and Keller, G. (1991). Multiple hematopoietic lineages develop from embryonic stem (ES) cells in culture. Development 111, 259-267.
73. Williams, B.O., Schmitt, E.M., Remington, L., Bronson, R.T., Albert, D.M., Weinberg, R.A., and Jacks, T. (1994). Extensive contribution of Rb-deficient cells to adult chimeric mice with limited histopathological consequences. EMBO J. 13, 4251-4259.
74. Wong, P.M.C., Chung, S.W., Chui, D.H.K., and Eaves, C.J. (1986). Properties of the earliest clonogenic hemopoietic precursors to appear in the developing murine yolk sac. Proc. Natl. Acad. Sci. USA 83, 3851-3854.
75. Wotton, D., Ghysdael, J., Wang, S., Speck, N.A., and Owen, M.J. (1994). Cooperative binding of Ets-1 and core binding factor to DNA. Mol. Cell. Biol. 14, 840-850.
76. Yoshida, H., Hayashi, S.-I., Kunisada, T., Ogawa, M., Nishikawa, S., Okamura, H., Sudo, T., Shultz, L.D., and Nishikawa, S.-I. (1990). The murine mutation osteopetrosis is in the coding region of the macrophage colony-stimulating factor gene. Nature 345, 442-443.
77. Zhang, D.E., Fujioka, K., Hetherington, C.J., Shapiro, L.H., Chen, H.M., Look, A.T., and Tenen, D.G. (1994). Identification of a region which directs the monocytic activity of the colony-stimulating factor 1 (macrophage colony-stimulating factor) receptor promoter and binds PEBP2/CBF (AML1). Mol. Cell. Biol. 14, 8085-8095.
78. Zhu, X., Yeadon, J.E., and Burden, S.J. (1994). AML1 is expressed in skeletal muscle and is regulated by innervation. Mol. Cell. Biol. 14, 8051-8057. Erratum: Mol. Cell. Biol. 15, 1136.