AML1-ETO inhibits maturation of multiple lymphohematopoietic lineages and induces myeloblast transformation in synergy with ICSBP deficiency

Journal of Experimental Medicine

Volumn 196, Issue 9, 2002, Pages 1227-1240

  Schwieger, Maike ^a   Löhler, Jürgen ^a   Friel, Jutta ^a   Scheller, Marina ^b   Horak, Ivan ^b   Stocking, Carol ^a  

^a LEIBNIZ INSTITUTE FOR EXPERIMENTAL VIROLOGY   (Germany)

^b FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

B cell differentiation; IFN regulatory factor; Leukemia; Myeloid differentiation; Translocation (genetics)

Indexed keywords

COMPLEMENTARY DNA; HYBRID PROTEIN; INTERFERON CONSENSUS SEQUENCE BINDING PROTEIN; RETROVIRUS VECTOR; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BONE MARROW CELL; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; GENE TRANSLOCATION; INTERNAL RIBOSOME ENTRY SITE; LEUKEMIA; MOUSE; MYELOBLAST; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSGENIC MOUSE;

ANIMALS; B-LYMPHOCYTES; BONE MARROW TRANSPLANTATION; CELL DIFFERENTIATION; CELL LINEAGE; CORE BINDING FACTOR ALPHA 2 SUBUNIT; ERYTHROPOIESIS; GENE EXPRESSION; GENETIC VECTORS; HEMATOPOIESIS; INTERFERON REGULATORY FACTORS; LYMPHOPOIESIS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; ONCOGENE PROTEINS, FUSION; REPRESSOR PROTEINS; RETROVIRIDAE; TRANSCRIPTION FACTORS; TRANSDUCTION, GENETIC;

EID: 0037020837     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20020824     Document Type: Article

References (75)

1. Brunning, R., E. Matutes, N. Harris, G. Flandrin, J. Vardiman, J. Bennett, and D. Head. 2001. Acute myeloid leukemias. In Pathology and Genetics of Tumours of Haematopoietic and Lymphoid Tissues. E. Jaffe, N. Harris, H. Stein, and J. Vardiman, editors. IARC Press, Lyon. 77-80.
2. Erikson, 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, AML-ETO, with similarity to Drosophila segmentation gene, runt. Blood. 80:1825-1831.
3. 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.
4. 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.
5. Leiden, J. 1993. Transcriptional regulation of T cell receptor genes. Annu. Rev. Immunol. 11:539-570.
6. Tenen, D., T. Hromas, J. Licht, and D.-E. Zhang. 1997. Transcription factors, normal myeloid development, and leukemia. Blood. 90:489-519.
7. Licht, J. 2001. AML1 and the AML1-ETO fusion protein in the pathogenesis of t(8;21) AML. Oncogene. 20:5660-5679.
8. 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 factor homologous to the products of the Drosophila runt and the human AML1 gene. Proc. Natl. Acad. Sci. USA. 90:6859-6863.
9. Meyers, S., J. Downing, and S. 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. 13:6336-6345.
10. Kitabayashi, I., A. Tokoyama, K. Shimazu, and M. Ohki. 1998. Interaction and functional cooperation of the leukemia-associated factors AML1 and p300 in myeloid cell differention. EMBO J. 17:2994-3004.
11. Amann, J., J. Nip, D. Strom, B. Lutterbach, H. Harada, N. Lenny, J. Downing, S. Meyers, and S. Hiebert. 2001. ETO, a target of t(8;21) in acute leukemia, makes distinct contacts with multiple histone deacetylases and binds mSin3A through its oligomerization domain. Mol. Cell. Biol. 21: 6470-6483.
12. Lutterbach, B., J. Westendorf, B. Linggi, A. Patten, M. Moniwa, J. Davie, K. Huynh, V. Bardwell, R. Lavinsky, M. Rosenfeld, et al. 1998. ETO, a target of t(8;21) in acute leukemia, interacts with the N-CoR and mSin3 corepressors. Mol. Cell. Biol. 18:7176-7184.
13. Wang, J., T. Hoshino, R. Redner, S. Kajigaya, and J. Liu. 1998. ETO, fusion partner in t(8;21) acute myeloid leukemia, represses transcription by interaction with the human N-CoR/mSin3A/HDAC1 complex. Proc. Natl. Acad. Sci. USA. 95:10860-10865.
14. Gelmetti, V., J. Zhang, M. Fanelli, S. Minucci, P. Pelicci, and M. Lazar. 1998. Aberrant recruitment of the nuclear receptor corepressor-histone deacetylase complex by the acute myeloid leukemia fusion partner ETO. Mol. Cell. Biol. 18: 7185-7191.
15. Frank, R., J. Zhang, S. Meyers, S. Hiebert, and S. Nimer. 1995. The AML1/ETO fusion protein blocks transactivation of the GM-CSF promoter by AML 1B. Oncogene. 11:2667-2674.
16. Meyers, S., N. Lenny, and S. Hiebert. 1995. The t(8;21) fusion protein interferes with AML-1B-dependent transcriptional activation. Mol. Cell. Biol. 15:1974-1982.
17. Zhang, D., C. Hetherington, S. Meyers, K. Rhoades, C. Larson, H.-M. Chen, S. Hiebert, and D. Tenen. 1996. CAAT enhancer-binding protein (C/EBP) and AML1(CBFα2) synergistically activate the macrophage colony-stimulating factor receptor promoter. Mol. Cell. Biol. 16:1231-1240.
18. Westendorf, J., C. Yamamoto, N. Lenny, J. Downing, M. Selsted, and S. Hiebert. 1998. The t(8;21) fusion product, AML-1-ETO, associates with C/EBP-α, inhibits C/EBP-α-dependent transcription, and blocks granulocytic differentiation. Mol. Cell. Biol. 18:323-333.
19. Petrovick, M., S. Hiebert, A. Friedman, C. Hetherington, D. Tenen, and D.-E. Zhang. 1998. Multiple functional domains of AML1: PU.1 and C/EBPα synergize with different regions of AML1. Mol. Cell. Biol. 18:3915-3925.
20. Mao, S., R. Frank, J. Zhang, Y. Miyazaki, and S. Nimer. 1999. Functional and physical interactions between AML1 proteins and an ETS protein, MEF: Implications for the pathogenesis of t(8;21)-positive leukemias. Mol. Cell. Biol. 19:3635-3644.
21. Pabst, T., B. Mueller, N. Harakawa, C. Schoch, T. Haferlach, G. Behre, W. Hiddemann, D.-E. Zhang, and D. Tenen. 2001. AML1-ETO downregulates the granulocytic differentiation factor C/EBP-α in t(8;21) myeloid leukemia. Nat. Med. 7:1-8.
22. Giese, K., C. Kingsley, J. Kirschner, and R. Grosschedl. 1995. Assembly and function of a TCR alpha enhancer complex is dependent on LEF-1-induced DNA bending and multiple protein-protein interactions. Genes Dev. 9:995-1008.
23. Okuda, T., Z. Cai, S. Yang, N. Lenny, C.-J. Lyu, J. van Duersen, H. Harada, and J. Downing. 1998. Expression of a knocked-in AML1-ETO leukemia gene inhibits the establishment of normal definitive hematopoiesis and directly generates dysplastic hematopoietic progenitors. Blood. 91:3134-3143.
24. Yergeau, D., C. Hetherington, Q. Wang, P. Zhang, A. Sharpe, M. Binder, M. Marin-Padilla, D. Tenen, N. Speck, and D.-E. Zhang. 1997. Embryonic lethality and impairment of haematopoiesis in mice heterozygous for an AML1-ETO fusion gene. Nat. Genet. 15:303-306.
25. Wang, Q., T. Stacy, M. Binder, M. Marín-Padilla, A. Sharpe, and N. Speck. 1996. Disruption of the Cbfa2 gene causes necrosis and hemorrhaging in the central nervous system and blocks definitive hematopoiesis. Proc. Natl. Acad. Sci. USA. 93:3444-3449.
26. Wang, Q., T. Stacy, J. Miller, A. Lewis, T.-L. Gu, X. Huang, J. Bushweller, J.-C. Bories, F. Alt, G. Ryan, et al. 1996. The CBFβ subunit is essential for CBFα2 (AML1) function in vivo. Cell. 87:697-708.
27. Okuda, T., J. van Deursen, S. Hiebert, G. Grosveld, and J. Downing. 1996. AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hematopoiesis. Cell. 84:321-330.
28. Buchholz, F., Y. Refaeli, A. Trump, and J. Bishop. 2000. Inducible chromosomal translocation of AML1 and ETO genes through Cre/loxP-mediated recombination in the mouse. EMBO Rep. 1:133-139.
29. Rhoades, K., C. Hetherington, N. Harakawa, D. Yergeau, L. Zhou, L.-Q. Liu, M.-T. Little, D. Tenen, and D.-E. Zhang. 2000. Analysis of the role of AML1-ETO in leukemogenesis, using an inducible transgenic mouse model. Blood. 96:2108-2115.
30. Yuan, Y., L. Zhou, T. Miyamato, H. Iwasaki, N. Harakawa, C. Hetherington, S. Burel, E. Lagasse, I. Weissman, K. Akashi, and D.-E. Zhang. 2001. AML1-ETO expression is directly involved in the development of acute myeloid leukemia in the presence of additional mutations. Proc. Natl. Acad. Sci. USA. 98:10398-10403.
31. Higuichi, M., D.O. Brien, P. Kumaravelu, N. Lenny, E.-J. Yeah, and J. Downing. 2002. Expression of a conditional AML1-ETO oncogene bypasses embryonic lethality and establishes a murine model of human t(8;21) acute myeloid leukemia. Cancer Cell. 1:63-74.
32. Bonnet, D., and J. Dick. 1997. Human acute myeloid leukemia is organized as a hierarchy that originates from a primitive hematopoietic cell. Nat. Med. 3:730-737.
33. Miyamoto, T., I. Weissman, and K. Akashi. 2000. AML1/ETO-expressing nonleukemic stein cells in acute myelogenous leukemia with 8;21 chromosomal translocation. Proc. Natl. Acad. Sci. USA. 97:7521-7526.
34. Raskind, W., and P.J. Fialkow. 1987. The use of cell markers in the study of human hematopoietic neoplasia. Adv. Cancer Res. 49:127-167.
35. Baum, C., W. Ostertag, C. Stocking, and D. von Laer. 2001. Retroviral vector design for cancer gene therapy. 2nd ed. In Gene Therapy of Cancer. E. Lattime and S. Gerson, editors. Academic Press, San Diego. 3-29.
36. Stocking, C., and C. Baum. 1997. Gene transfer in hematopoietic cells. In Bailliére's Clinical Hematology. A. Whetton, editor. Baillière Tindall, London. 445-466.
37. Holtschke, T., J. Löhler, Y. Kanno, T. Fehr, N. Giese, F. Rosenbauer, J. Lou, K.-P. Knobeloch, L. Gabriele, J. Waring, et al. 1996. Immunodeficiency and chronic myelogenous leukemia-like syndrome in mice with a targeted mutation of the ICSBP gene. Cell. 87:307-317.
38. Scheller, M., J. Foerster, C. Heyworth, J. Waring, J. Lohler, G. Gilmore, R. Shadduck, T. Dexter, and I. Horak. 1999. Altered development and cytokine responses of myeloid progenitors in the absence of transcription factor, interferon consensus sequence binding protein. Blood. 94:3764-3771.
39. Gabriele, L., J. Phung, J. Fukumoto, D. Segal, I.-M. Wang, P. Giannakakou, N. Giese, K. Ozato, and H. Morse, III. 1999. Regulation of apoptosis in myeloid cells by interferon consensus sequence-binding protein. J. Exp. Med. 190:411-421.
40. Schmidt, M., A. Hochhaus, A. Nitsche, R. Hehlmann, and A. Neubauer. 2001. Expression of nuclear transcription factor interferon consensus sequence binding protein in chronic myeloid leukemia correlates with pretreatment risk features and cytogenetic response to interferon-α. Blood. 97:3648-3650.
41. Schmidt, M., S. Nagel, J. Proba, C. Thiede, M. Ritter, J. Waring, F. Rosenbauer, D. Huhn, B. Wittig, I. Horak, and A. Neubauer. 1998. Lack of interferon consensus binding protein (ICSBP) transcripts in human myeloid leukemia. Blood. 91:22-29.
42. Hao, S., and R. Ren. 2000. Expression of interferon consensus sequence binding protein (ICSBP) is downregulated in bcr-abl-induced murine chronic myelogenous leukemia-like disease, and forced coexpression of ICSBP inhibits bcr-abl-induced myeloproliferative disorder. Mol. Cell. Biol. 20: 1149-1161.
43. Baum, C., S. Hegewisch-Becker, H.-G. Eckert, C. Stocking, and W. Ostertag. 1995. Novel retroviral vectors for efficient expression of the multidrug resistance (mdr-1) gene in early hematopoietic cells. J. Virol. 69:7541-7547.
44. Hildinger, M., K. Abel, W. Ostertag, and C. Baum. 1999. Design of 5′ untranslated sequences in retroviral vectors developed for medical use. J. Virol. 73:4083-4089.
45. Schambach, A., H. Wodrich, M. Hildinger, J. Bohne, H. Krausslich, and C. Baum. 2000. Context dependence of different modules for posttranscriptional enhancement of gene expression from retroviral vectors. Mol. Ther. 2:435-445.
46. Morita, S., T. Kojima, and T. Kitamura. 2000. Plat-E: An efficient and stable system for transient packaging of retroviruses. Gene Ther. 7:1063-1066.
47. Beyer, W., M. Westphal, W. Ostertag, and D. von Laer. 2002. Oncoretrovirus and lentivirus vectors pseudotyped with lymphocytic choriomeningitis virus glycoprotein: Generation, concentration, and broad host range. J. Virol. 76: 1488-1495.
48. Wahlers, A., M. Schwieger, Z. Li, D. Meier-Tackmann, C. Lindemann, H.-G. Eckert, D. von Laer, and C. Baum. 2001. Influence of multiplicity of infection and protein stability on retroviral vector-mediated gene expression in hematopoietic cells. Gene Ther. 8:477-486.
49. Asou, H., S. Tahiro, 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.
50. Meyer, J., M. Jücker, W. Ostertag, and C. Stocking. 1998. Carboxyl-truncated STAT5β is generated by a nucleus-associated serine protease in early hematopoietic progenitors. Blood. 91:1901-1908.
51. Baum, C., K. Itoh, J. Meyer, C. Laker, Y. Ito, and W. Ostertag. 1997. The potent enhancer activity of the polycythemic strain of spleen focus-forming virus in hematopoietic cells is governed by a binding site for Sp1 in the upstream control region and by a unique enhancer core motif, creating an exclusive target for PEBP/CBF. J. Virol. 71:6323-6331.
52. Hardy, R., C. Carmack, S. Shinton, J. Kemp, and K. Hayakawa. 1991. Resolution and characterization of pro-B and pre-B-cell stages in normal mouse bone marrow. J. Exp. Med. 173:1213-1225.
53. Hestdal, K., F. Ruscetti, J. Ihle, S. Jacobsen, C. Dubois, W. Kopp, D. Longo, and J. Keller. 1991. Characterization and regulation of RB6-8C5 antigen expression on murine bone marrow cells. J. Immunol. 147:22-28.
54. Tallman, M., D. Hakimian, J. Shaw, G. Lissner, E. Russell, and D. Variakojis. 1993. Granulocytic sarcoma is associated with the 8;21 translocation in acute myeloid leukemia. J. Clin. Oncol. 11:690-697.
55. Abe, R., H. Umezu, T. Uchida, S. Kariyone, N. Maseki, Y. Kaneko, and M. Sakurai. 1986. Myeloblastoma with an 8;21 chromosome translocation in acute myeloblastic leukemia. Cancer. 58:1260-1264.
56. Meis, J., J. Butler, B. Osborne, and J. Manning. 1986. Granulocytic sarcoma in non-leukemic patients. Cancer. 58:2697.
57. Neiman, R., M. Barcos, C. Berard, H. Bonner, R. Mann, R. Rydell, and J. Bennett. 1981. Granulocytic sarcoma: A chnicopathologic study of 61 biopsied cases. Cancer. 48:1426-1437.
58. de Guzman, C., A. Warren, Z. Zhang, L. Gartland, P. Erikson, H. Drabkin, S. Hiebert, and C. Klug. 2002. Hematopoietic stem cell expansion and distinct myeloid developmental abnormalities in a murine model of the AML1-ETO translocation. Mol. Cell. Biol. 22:5506-5517.
59. Hayashi, K., W. Natsume, T. Watanabe, N. Abe, N. Iwai, H. Okada, Y. Ito, M. Asano, Y. Iwakura, S. Habu, et al. 2000. Diminution of the AML1 transcription factor function causes differential effects on the-fates of CD4 and CD8 single-positive T cells. J. Immunol. 165:6816-6824.
60. Hayashi, K., N. Abe, T. Watanabe, M. Obinata, M. Ito, T. Sato, S. Habu, and M. Satake. 2001. Overexpression of AML1 transcription factor drives thymocytes into the CD8 single-positive lineage. J. Immunol. 167:4957-4965.
61. Sakakura, C., Y. Yamaguchi-Iwai, M. Satake, S.-C. Bae, A. Takahashi, E. Ogawa, A. Hagiwara, T. Takahashi, A. Murakami, K. Makino, et al. 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.
62. Ahn, M., G. Huang, S. Bae, J. Wee, W. Kim, and Y. Ito. 1998. Negative regulation of granulocyte differentiation in the myeloid precursor cell line 32Dc13 by ear-2, a mammalian homolog of Drosophila seven-up, and a chimeric leukemogenic gene, AML1/ETO. Proc. Natl. Acad. Sci. USA. 95: 1812-1817.
63. Kitabayashi, I., K. Ida, F. Morohoshi, A. Yokoyama, N. Mitsuhashi, K. Shimizu, N. Nomura, Y. Hayashi, and M. Ohki. 1998. The AML1-MTG8 leukemic fusion protein forms a complex with a novel member of the MTG8(ETO/CDR) family, MTGN1. Mol. Cell. Biol. 18:846-858.
64. Burel, S., N. Harakawa, L. Zhou, T. Pabst, D. Tenen, and D. Zhang. 2001. Dichotomy of AML1-ETO functions: Apoptosis versus block of differentiation. Mol. Cell. Biol. 21: 5577-5590.
65. Mulloy, J., J. Cammenga, K. MacKenzie, F. Berguido, A. Moore, and S. Nimer. 2002. The AML1-ETO fusion protein promotes the expansion of human hematopoietic stem cells. Blood. 99:15-23.
66. McKercher, S., B. Torbett, K. Anderson, G. Henkel, D. Vestal, H. Baribault, M. Klemsz, A. Freeney, G. Wu, C. Paige, and R. Maki. 1996. Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J. 15:5647-5658.
67. Scott, E., M. Simon, J. Anastasi, and H. Singh. 1994. Requirement of transcription factor PU.1 in the development of multiple hematopoietic lineages. Science. 265:1573-1577.
68. Zhang, D., P. Zhang, N. Wang, C. Hetherington, G. Darlington, and D. Tenen. 1997. Absence of G-CSF signaling and neutrophil development in C/EBP α deficient mice. Proc. Natl. Acad. Sci. USA. 94:569-574.
69. Erman, B., M. Cortes, B. Nikolajczyk, N. Speck, and R. Sen. 1998. ETS-core binding factor: A common composite motif in antigen receptor gene enhancers. Mol. Cell. Biol. 18: 1322-1330.
70. Libermann, T., Z. Pan, Y. Akbarali, C. Hetherington, J. Boltax, D. Yergeau, and D.-E. Zhang. 1999. AML1 (CBFa2) cooperates with B cell-specific activating protein (BSAP/Pax5) in activation of the B cell-specific BLK gene promoter. J. Biol. Chem. 274:24671-24676.
71. Harada, H., Y. Harada, D. O'Brien, D. Rice, C. Naeve, and J. Downing. 1999. HERF1, a novel hematopoiesis-specific RING finger protein, is required for terminal differentiation of erythroid cells. Mol. Cell. Biol. 19:3808-3815.
72. Harada, Y., H. Harada, J. Downing, and A. Kimura. 2001. A hematopoietic-specific transmembrane protein, Art-1, is possibly regulated by AML1. Biochem. Biophys. Res. Commun. 284:714-722.
73. Rosenbauer, F., A. Kallies, M. Scheller, K.-P. Knobeloch, C. Rock, M. Schwieger, C. Stocking, and I. Horak. 2002. Disabled-2 is transcriptionally regulated by interferon consensus sequence binding protein and augments macrophage spreading and adhesion. EMBO J. 21:211-220.
74. Beghini, A., P. Peterlongo, C. Ripamonti, L. Larizza, R. Cairoli, E. Morra, and C. Mecucci. 2000. C-kit mutations in core binding factor leukemias. Blood. 95:726-727.
75. Yokota, S., H. Kiyoi, M. Nakao, T. Iwai, T. Misawa, T. Okujda, Y. Sonodo, T. Abe, K. Kahsima, Y. Matsuo, and T. Naoe. 1997. Internal tandem duplication of the FLT3 gene is preferentially seen in acute myeloid leukemia and myelodyspastic syndrome among various hematological malignancies. A study on a large series of patients and cell lines. Leukemia. 11:1605-1609.