Immortalization and leukemic transformation of a myelomonocytic precursor by retrovirally transduced HRX-ENL

EMBO Journal

Volumn 16, Issue 14, 1997, Pages 4226-4237

  Lavau, Catherine ^a   Szilvassy, Stephen J ^b   Slany, Robert ^c   Cleary, Michael L ^c  

^a NOVARTIS PHARMA AG   (Switzerland)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF KENTUCKY   (United States)

Author keywords

HRX ENL; Immortalization; MLL; Myeloid leukemia; Retroviral vector

Indexed keywords

COMPLEMENTARY DNA; HYBRID PROTEIN; INTERLEUKIN 3; MESSENGER RNA; STEM CELL FACTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL TRANSFORMATION; CHROMOSOME TRANSLOCATION 11; CHROMOSOME TRANSLOCATION 19; COLONY FORMING UNIT; CONTROLLED STUDY; DELETION MUTANT; GENE FUSION; GENE TRANSFER; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL; LEUKEMOGENESIS; MOUSE; MYELOID LEUKEMIA; NONHUMAN; PRIORITY JOURNAL; PROVIRUS; RETROVIRUS; SCID MOUSE;

ACUTE DISEASE; ANIMALS; CELL DIVISION; CELL LINE, TRANSFORMED; CELL TRANSFORMATION, NEOPLASTIC; DNA, VIRAL; DNA-BINDING PROTEINS; FLOW CYTOMETRY; GENETIC VECTORS; HEMATOPOIETIC STEM CELLS; LEUKEMIA, MYELOID; MICE; MICE, INBRED C57BL; MICE, SCID; MONOCYTES; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NEOPLASM PROTEINS; NUCLEAR PROTEINS; PROTO-ONCOGENES; RECOMBINANT FUSION PROTEINS; RETROVIRIDAE; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSFECTION; TRANSLOCATION, GENETIC;

ANIMALIA; UNIDENTIFIED RETROVIRUS;

EID: 0030791974     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.14.4226     Document Type: Article

References (51)

1. Bahnson, A.B., Dunigan, J.T., Baysal, B.E., Mohney, T., Atchison, R.W., Nimgaonkar, M.T., Ball, E.D. and Barranger, J.A. (1995) Centrifugal enhancement of retroviral mediated gene transfer. J. Virol. Methods, 54, 131-143.
2. Blatt, C., Aberdam, D., Schwartz, R. and Sachs, L. (1988) DNA rearrangement of a homeobox gene in myeloid leukaemic cells. EMBO J., 7, 4283-4290.
3. Borrow, J. et al. (1996) The t(7:11)(p15:p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nature Genet., 12, 159-167.
4. Breen, T.R. and Harte, P.J. (1993) trithorax regulates multiple homeotic genes in the bithorax and Antennapedia complexes and exerts different tissue-specific, parasegment-specific and promoter-specific effects on each. Development, 117, 119-134.
5. Butler, L.H., Slany, R., Cui, X., Cleary, M.L. and Mason, D.Y. (1997) The HRX proto-oncogene product is widely expressed in human tissues and localizes to nuclear structures. Blood, 89, 3361-3370.
6. Cairns, B.R., Henry, N.L. and Kornberg, R.D. (1996) TFG3/TAF30/ANC1, a component of the yeast SWI/SNF complex that is similar to the leukemogenic proteins ENL and AF-9. Mol. Cell Biol., 16, 3308-3316.
7. Caslini, C., Murti, K.G., Ashmun, R.A., Domer, P.H., Korsmeyer, S.J., Boer, J.M., Grosveld, G.C. and Look, A.T. (1996) Subcellular localization and cell cycle effects of the MLL-AF4 fusion oncoprotein. Blood, 88, 557a.
8. Cleary, M.L. (1991) Oncogenic conversion of transcription factors by chromosomal translocations. Cell, 66, 619-622.
9. Corral, J. et al. (1996) An Mll-AF9 fusion gene made by homologous recombination causes acute leukemia in chimeric mice: a method to create fusion oncogenes. Cell, 85, 853-861.
10. Djabali, M. Selleri, L., Parry, P., Bower, M., Young, B.D. and Evans, G.A. (1992) A trithorax-like gene is interrupted by chromosome 11q23 translocations in acute leukemia. Nature Genet., 2, 113-118.
11. Gu, Y., Nakamura, T., Alder, H., Prasad, R., Cananni, O., Cimino, G., Croce, C.M. and Canaani, E. (1992) The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene. Cell, 71, 701-708.
12. Hawley, R.G., Lieu, F.H.L., Fong, A.Z.C. and Hawley, T.S. (1994) Versatile retroviral vectors for potential use in gene therapy. Gene Ther., 1, 136-138.
13. Hawley, R.G., Fong, A.Z.C., Ngan, B.-Y. and Hawley, T.S. (1995) Hematopoietic transforming potential of activated ras in chimeric mice. Oncogene, 11, 1113-1123.
14. Henry, N.L., Campbell, A.M., Feaver, W.J., Poon, D., Weil, P.A. and Kornberg, R.D. (1994) TFIIF-TAF-RNA polymerase II connection. Genes Dev., 8, 2868-2878.
15. Hirschhorn, J.N., Brown, S.A., Clark, C.D. and Winston, F. (1992) Evidence that SNF2/SWI2 and SNF5 activate transcription in yeast by altering chromatin structure. Genes Dev., 6, 2288-2298.
16. Iida, S., Seto, M., Yamamoto, K., Komatsu, H., Tojo, A., Asano, S., Kamada, N., Ariyoshi, Y., Takahashi, T. and Ueda, R. (1993) MLLT3 gene on 9p22 involved in t(9;11) leukemia encodes a serine/proline rich protein homologous to MLLT1 on 19p13. Oncogene, 8, 3085-3092.
17. Jang, S.K., Davies, M.V., Kaufman, R.J. and Wimmer, E. (1989) Initiation of protein synthesis by internal entry of ribosomes into 5′ nontranslated region of encephalomyocarditis virus RNA in vivo. J. Virol., 63, 1651-1660.
18. Johnson, D., Lanahan, A., Buck, C.R., Sehgal, A., Morgan, C., Mercer, E., Bothwell, M. and Chao, M. (1986) Expression and structure of the NGF receptor. Cell. 47, 545-554.
19. Kennison, J.A. (1993) Transcriptional activation of Drosophila homeotic genes from distant regulatory elements. Trends Genet., 9, 75-79.
20. Kongsuwan, K., Webb, E., Honsiaux, P. and Adams, J.M. (1989) Expression of Hox-2.4 homeobox gene directed by proviral insertion in a myeloid leukemia. Nucleic Acids Res., 17, 1881-1892.
21. Lavau, C., Heard, J.M., Danos, O. and Dejean, A. (1996) Retroviral vectors for the transduction of the PML-RARα fusion product of acute promyelocytic leukemia. Exp. Hematol., 24, 544-551.
22. Lawrence, H.J. and Largman, C. (1992) Homeobox genes in normal hematopoiesis and leukemia. Blood, 80, 2445-2453.
23. Lowney, P. et al. (1991) A human Hox1 homeobox gene exhibits myeloid-specific expression of alternative transcripts in human hematopoietic cells. Nucleic Acids Res., 19, 3443-3449.
24. Mitani, K., Kanda, Y., Ogawa, S., Tanaka, T., Inazawa, J., Yazaki, Y. and Hirai, H. (1995) Cloning of several species of MLL/MEN chimeric cDNAs in myeloid leukemia with t(11;19)(q23;p13.1) translocation. Blood, 85, 2017-2024.
25. Moore, T., Huang, S., Terstappen, L.W.M.M., Bennett, M. and Kumar, V. (1994) Expression of CD43 on murine and human pluripotent hematopoietic stem cells. J. Immunol., 153, 4978-4987.
26. Nakamura, T. et al. (1993) Genes on chromosomes 4, 9, and 19 involved in 11q23 abnormalities in acute leukemia share sequence homology and/or common motifs. Proc. Natl Acad. Sci. USA, 90, 4631-4635.
27. Nakamura, T. et al. (1996a) Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7:11)(p15;p15) in human myeloid leukemias. Nature Genet., 12, 154-158.
28. Nakamura, T., Largaespada, D.A., Shaughnessy, J.D., Jr, Jenkins, N.A. and Copeland, N.G. (1996b) Cooperative activation of Hoxa and Pbx1-related genes in murine myeloid leukaemias. Nature Genet., 12, 149-153.
29. Pagé, B., Pagé, M. and No'l, C. (1993) A new fluorometric assay for cytotoxicity measurements in vitro. Int. J. Oncol., 3, 473-476.
30. Pear, W., Nolan, G., Scott, M. and Baltimore, D. (1993) Production of high-titer helper-free retroviruses by transient transfection. Proc. Natl Acad. Sci. USA, 90, 8392-8396.
31. Perkins, A.C. and Cory, S. (1993) Conditional immortalization of mouse myelomonocytic, megakaryocytic and mast cell progenitors by the Hox-2.4 homeobox gene. EMBO J., 12, 3835-3846.
32. Perkins, A., Kongsuwan, K., Visvader, J., Adams, J.M. and Cory, S. (1990) Homeobox gene expression plus autocrine growth factor production elicits myeloid leukemia. Proc. Natl Acad. Sci. USA, 87, 8398-8402.
33. Rabbitts, T.H. (1991) Translocations, master genes, and differences between the origins of acute and chronic leukemias. Cell. 67, 641-644.
34. Rubnitz, J.E., Morrissey, J., Savage, P.A. and Cleary, M.L. (1994) ENL, the gene fused with HRX in t(11;19) leukemias, encodes a nuclear protein with transcriptional activation potential in lymphoid and myeloid cells. Blood, 84, 1747-1752.
35. Ruhnitz, J.E., Behm, F.G., Curcio-Brint, A.M., Pinheiro, V.R.P., Carroll, A.J., Raimondi, S.C., Shurtleff, S.A. and Downing, J.R. (1996) Molecular analysis of t(11;19) breakpoints in childhood acute leukemias. Blood, 87, 4804-4808.
36. + subpopulations of human bone marrow cells. Proc. Natl Acad. Sci. USA, 91, 12223-12227.
37. Sauvageau, G., Thorsteinsdottir, U., Eaves, C.J., Lawrence, H.J., Largman, C., Lansdorp, P.M. and Humphries, R.K. (1995) Overexpression of HoxB4 in hematopoietic cells causes the selective expansion of more primitive populations in vitro and in vivo. Genes Dev., 9, 1753-1765.
38. Schichman, S.A., Caligiuri, M.A., Gu, Y., Strout, M.P., Canaani, E., Bloomfield, C.D. and Croce, C.M. (1994) ALL-1 partial duplication in acute leukemia. Proc. Natl Acad. Sci. USA, 91, 6236-6239.
39. Shilatifard, A., Lane, W.S., Jackson, K.W., Conaway, R.C. and Conaway, J.W. (1996) An RNA polymerase II elongation factor encoded by the human ELL gene. Science, 271, 1873-1876.
40. Szilvassy, S.J. and Cory, S. (1993) Phenotypic and functional characterization of competitive long-term repopulating hematopoietic stem cells enriched from 5-fluorouracil-treated murine marrow. Blood, 81, 2310-2320.
41. Szilvassy, S.J., Humphries, R.K., Lansdorp, P.M., Eaves, A.C. and Eaves, C.J. (1990) Quantitative assay for totipotent reconstituting hematopoietic stem cells by a competitive repopulating strategy. Proc. Natl Acad. Sci. USA, 87, 8736-8740.
42. Szilvassy, S.J., Weller, K.P., Lin, W., Sharma, A.K., Ho, A.S.Y., Tsukamoto, A., Hoffman, R., Leiby, K.R. and Gearing, D.P. (1996a) Leukemia inhibitory factor upregulates cytokine expression by a murine stromal cell line enabling the maintenance of highly enriched competitive repopulating stem cells. Blood, 87, 4618-4628.
43. Szilvassy, S.J., Weller, K.P., Chen, B., Juttner, C.A., Tsukamoto, A. and Hoffman, R. (1996b) Partially differentiated ex vivo expanded cells accelerate hematologic recovery in myeloablated mice transplanted with highly enriched long-term repopulating stem cells. Blood, 88, 3642-3653.
44. Thirman, M.J., Levitan, D.A., Kobayashi, H., Simon, M.C. and Rowley, J.D. (1994) Cloning of ELL, a gene that fuses to MLL in a t(11:19)(q23; p13.1) in acute myeloid leukemia. Proc. Natl Acad. Sci. USA, 91, 12110-12114.
45. Thorsteinsdottir, U., Sauvageau, G., Hough, M.R., Dragowska, W., Lansdorp, P.M., Lawrence, H.J., Largman, C. and Humphries, R.K. (1997) Overexpression of HoxA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemias. Mol. Cell. Biol., 17, 495-505.
46. Tkachuk, D.C., Kohler, S. and Cleary, M.L. (1992) Involvement of a homolog of Drosophila trithorax by 11q23 chromosomal translocations in acute leukemias. Cell, 71, 691-700.
47. Waring, P.M. and Cleary, M.L. (1997) Disruption of a homolog of trithorax by 11q23 translocations: leukemogenic and transcriptional implications. Curr. Top. Microbiol. Immunol., 220, 1-23.
48. Welch, M.D. and Drubin, D.G. (1994) A nuclear protein with sequence similarity to proteins implicated in human leukemias is important for cellular morphogenesis and actin cytoskeletal function in Saccharomyces cerevisiae. Mol. Biol. Cell., 5, 617-632.
49. Whitlock, C.A., Tidmarsh, G.K. Muller-Seiburg, C. and Weissman, I.L. (1987) Bone marrow stromal cell lines with lymphopoietic activity express high levels of a pre-B neoplasia-associated molecule. Cell, 48, 1009-1021.
50. Ymer, S., Tucker, W., Sanderson, C.J., Hapel, A.J., Campbell, H.D. and Young, I.G. (1985) Constitutive synthesis of interleukin-3 by leukaemia cell line WEHI-3B is due to retroviral insertion near the gene. Nature, 317, 255-258.
51. Yu, B.D., Hess, J.L., Horning, S.E., Brown, G.A. and Korsmeyer, S.J. (1995) Altered Hox expression and segmental identity in Mil-mutant mice. Nature, 378, 505-508.