Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b

EMBO Journal

Volumn 17, Issue 13, 1998, Pages 3714-3725

  Kroon, Evert ^a   Krosl, Jana ^a   Thorsteinsdottir, Unnur ^a   Baban, Soheyl ^a   Buchberg, Arthur M ^b   Sauvageau, Guy ^a,c  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b THOMAS JEFFERSON UNIVERSITY   (United States)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Hox; Leukemia; Meis; Oncogenes; Pbx

Indexed keywords

GROWTH FACTOR; HOMEODOMAIN PROTEIN;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; CANCER INCIDENCE; CARCINOGENESIS; CELL STRUCTURE; CELL TRANSFORMATION; CELL TRANSPLANTATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; GENE OVEREXPRESSION; GENE TRANSFER; GENETIC ENGINEERING; HEMATOPOIETIC CELL; LEUKEMIA CELL; MOUSE; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN PROTEIN INTERACTION; SOUTHERN BLOTTING; SURVIVAL TIME;

ANIMALS; BONE MARROW CELLS; CELL LINE; CELL TRANSFORMATION, NEOPLASTIC; CELL TRANSPLANTATION; CELLS, CULTURED; DNA-BINDING PROTEINS; FEMALE; GENETIC VECTORS; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA, MYELOID; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; NEOPLASM PROTEINS; PROTO-ONCOGENE PROTEINS; RESEARCH DESIGN; RETROVIRIDAE;

EID: 0032126633     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.13.3714     Document Type: Article

References (57)

1. Afonja, O., Smith, J., Ohyashiki, K., Ohyashiki, J., Toyama, K., Inghirami, G. and Takeshita, K. (1977) MEIS gene family in human acute myeloid leukemia. Blood, 90 (S1), 67a.
2. Berthelsen, J., Zappavigna, V., Mavilio, F. and Blasi, F. (1998) Prep1, a novel functional partner of Pbx proteins. EMBO J., 17, 1423-1433.
3. 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.
4. Borrow, J. et al. (1996) The t(7;11) (p15;p15) translocation in acute myeloid leukemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nature Genet., 12, 159-167.
5. Burglin, T.R. and Ruvkun, G. (1992) New motif in PBX genes. Nature Genet., 1, 319-320.
6. Caré, A., Testa, U., Bassani, A., Tritarelli, E., Montesoro, E., Samoggia, P., Cianetti, L. and Peschle, C. (1994) Coordinate expression and proliferative role of HOXB genes in activated adult T lymphocytes. Mol. Cell. Biol., 14, 4872-4877.
7. Chan, S.K., Jaffe, L., Capovilla, M., Botas, J. and Mann, R.S. (1994) The DNA binding specificity of Ultrabithorax is modulated by cooperative interactions with extradenticle, another homeoprotein. Cell. 78, 603-615.
8. Chang, C.P., Brocchieri, L., Shen, W.R. Largman, C. and Cleary, M.L. (1996) Pbx modulation of hox homeodomain amino-terminal arms establishes different DNA-binding specificities across the hox locus. Mol. Cell. Biol., 16, 1734-1745.
9. Chang, C.P., Jacobs, Y., Nakamura, T., Jenkins, N.A., Copeland, N.G. and Cleary, M.L. (1997) Meis proteins are major in vivo DNA binding partners for wild-type but not chimeric Pbx proteins. Mol. Cell. Biol., 17, 5679-5687.
10. Cillo, C., Barba, P. Freschi, G., Bucciarelli, G., Magli, M.C. and Boncinelli, E. (1992) HOX gene expression in normal and neoplastic human kidney. Int. J. Cancer, 51, 38-49.
11. Cone, R.B. and Mulligan, R.C. (1984) High-efficiency gene transfer into mammalian cells: generation of helper-free recombinant retrovirus with broad mammalian host range. Proc. Natl Acad. Sci. USA, 81, 6349-6353.
12. Davis, L., Kuehl, M. and Battey, J. (1994a) Preparation and Analysis of RNA from Eukaryotic Cells. Appleton and Lange, Norwalk, CT.
13. Davis, L., Kuehl, M. and Battey, J. (1994b) Sobcloning Fragments into Plasmid Vectors. Appleton and Lange, Norwalk, CT.
14. De Vita, G., Barba, P., Odartchenko, N., Givel, J.C., Freschi, G., Bucciarelli, G., Magli, M.C., Boncinelli, E. and Cillo, C. (1993) Expression of homeobox-containing genes in primary and metastatic colorectal cancer. Eur. J. Cancer, 29A, 887-893.
15. Dexter, T.M., Garland, J., Scott, D., Scolnick, E. and Metcalf, D. (1980) Growth of factor-dependent hemopoietic precursor cell lines. J. Exp. Med., 152, 1036-1047.
16. Friedmann, Y., Daniel, C.A., Strickland, P. and Daniel, C.W. (1994) Hox genes in normal and neoplastic mouse mammary gland. Cancer Res., 54, 5981-5985.
17. Gonzalez-Crespo, S. and Morata, G. (1995) Control of Drosophila adult pattern by extradenticle. Development, 121, 2117-2125.
18. Hassan, H.T. and Drexler, H.G. (1995) Interleukins and colony stimulating factors in human myeloid leukemia cell lines. Leuk. Lymphoma, 20, 1-15.
19. Hawley, R.G., Fong, A.Z., Reis, M.D., Zhang, N., Lu, M. and Hawley, T.S. (1997) Transforming function of the HOX11/TCL3 homeobox gene. Cancer Res., 57, 337-345.
20. Humphries, R.K., Eaves, A.C. and Eaves, C.J. (1981) Self-renewal of hemopoietic stem cells during mixed colony formation in vitro. Proc. Natl Acad. Sci. USA, 76, 3629-3633.
21. Kamps, M.P. and Baltimore, D. (1993) E2A-Pbx1, the t(1;19) translocation protein of human pre-B-cell acute lymphocytic leukemia, causes acute myeloid leukemia in mice. Mol. Cell. Biol., 13, 351-357.
22. Kamps, M.P., Murre, C. Sun, X.H. and Baltimore, D. (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.
23. Knoepfler, P.S., Calvo, K.R., Chen, H., Antonarakis, S.E. and Kamps, M.P. (1997) Meis 1 and pKnox 1 bind DNA cooperatively with Pbx 1 utilizing an interaction surface disrupted in oncoprotein E2a-Pbxl. Proc. Natl Acad. Sci. USA, 94, 14553-14558.
24. Krosl, J., Baban, S., Krosl, G., Rozenfeld, S., Largman, C. and Sauvageau, G. (1998) Proliferation and transformation by HOXB4 and HOXB3 genes involves cooperation with PBX. Oncogene, in press.
25. Krumlauf, R. (1994) Hox genes in vertebrate development. Cell, 78, 191-201.
26. Lapidot, T. et al. (1994) A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature, 367, 645-648.
27. Lawrence, H.J., Sauvageau, G., Ahmadi, A., Lau, T., Lopez, A.R., Le Beau, M.M., Link, M. and Largman, C. (1995) Stage and lineage-specific expression of the HOXA10 homeobox gene in normal and leukemic hematopoietic cells. Exp. Hematol., 23, 1160-1166.
28. Lawrence, H.J., Helgason, C.D., Sauvageau, G., Fong, S.T., Peterson, C.L., Capecchi, M.R., Humphries, R.K. and Largman, C. (1997) Mice homozygous for a targeted disruption of the homeobox gene HOXA9 have defects in lymphoid and myeloid hematopoiesis. Blood, 89, 1922-1930.
29. Maconochie, M.K., Nonchev, S., Studr, M., Chan, S.K., Poepperl, H., Sham, M.H., Mann, R.S. and Krumlauf, R. (1997) Cross-regulation in the mouse HoxB complex: the expression of Hoxb2 in rhobdomere 4 is regulated by Hoxb1. Genes Dev., 11, 1885-1895.
30. Mann, R.S. and Chan, S.K. (1996) Extra specificity from extradenticle: the partnership between HOX and PBX/EXD homeodomain proteins. Trends Genet., 12, 258-262.
31. Markowitz, D., Goff, S. and Bank, A. (1988a) A safe packaging line for gene transfer: separarting viral genes on two different plasmids. J. Virol., 62, 1120-1124.
32. Markowitz, D., Goff, S. and Bank A. (1988b) Construction and use of a safe and efficient amphotropic packaging cell line. Virology, 167, 400-406.
33. Monica, K., Galili, N., Nourse, J., Saltman, D. and Cleary, M.L. (1991) PBX2 and PBX3, new homeobox genes with extensive homology to the human proto-oncogene PBX1. Mol. Cell. Biol., 11, 6149-6157.
34. Moskow, J.J., Bullrich, F., Huebner, K., Daar, I.O. and Buchberg, A.M. (1995) Meis1, a PBX1-related homeobox gene involved in myeloid leukemia in BXH-2 mice. Mol. Cell. Biol., 15, 5434-5443.
35. Nakamura, T., Largaespada, D.A., Shaughnessy, J.D., Jenkins, N.A. and Copeland, N.G. (1996) Cooperative activation of Hoxa and Pbx1-related genes in murine myeloid leukaemias. Nature Genet., 12, 149-153.
36. Pai, C.Y., Kuo, T.S., Jaw, T.J., Kurant, E., Chen, C.T., Bessarab, D.A., Salzberg, A. and Sun, Y.H. (1998) The Homothorax homeoprotein activates the nuclear localization of another homeoprotein, Extradenticle and suppresses eye development in Drosophila. Genes Dev., 12, 435-446.
37. Pawliuk, R., Kay, R., Lansdorp, P. and Humphries, R.K. (1994) Selection of retrovirally transduced hematopoietic cells using CD24 as a marker of gene transfer. Blood, 84, 2868-2876.
38. Peers, B., Sharma, S., Johnson, T., Kamps, M. and Monteminy, M. (1995) The pancreatic islet factor STF-1 binds cooperatively with Pbx to a regulatory element in the somatostatin promoter: importance of the FPWMK motif and of the homeodomain. Mol. Cell. Biol., 15, 7091-7097.
39. Peifer, M. and Wieschaus, E. (1990) Mutations in the Drosophila gene extradenticle affect the way specific homeo domain proteins regulate segmental identity. Genes Dev., 4, 1209-1223.
40. 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.
41. 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.
42. Quaranta, M.T. Petrini, M., Tritarelli, E., Samoggia, P., Caré, A., Bottero, L., Testa, U. and Peschle, C. (1996) HOXB cluster genes in activated natural killer lymphocytes. J. Immunol., 157, 2462-2469.
43. Rauskolb, C., Smith, K.M., Peifer, M. and Weischaus, E. (1995) Extradenticle determines segmental identities throughout Drosophila development. Development, 121, 3663-3673.
44. Rieckhof, G.E., Casares, F., Don Ryoo, H., Abu-Shaar, M. and Mann, R.S. (1997) Nuclear translocation of extradenticle requires homothorax, which encodes and extradenticle-related homeodomain protein. Cell, 91, 171-183.
45. Rocco, G.D., Mavilio, F. and Zappavigna, V. (1997) Functional dissection of a transcriptionally active, target-specific Hox-Pbx complex. EMBO J., 16, 3644-3654.
46. Rodriguez-Cimadevilla, J.C., Beauchemin, V., Villeneuve, L., Letendre, F., Shaw, A. and Hoang, T. (1990) Coordinate secretion of interleukin-1 beta and granulocyte-macrophage colony-stimulating factor by the blast cells of acute myeloblastic leukemia: role of interleukin-1 as an endogenous inducer. Blood, 76, 1481-1489.
47. + subpopulations of human bone marrow cells. Proc. Natl Acad. Sci. USA, 91, 12223-12227.
48. 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.
49. Sauvageau, G., Thorsteinsdottir, U., Hough, M.R., Hugo, P., Lawrence, H.J., Largman, C. and Humphries, R.K. (1997) Overexpression of HOXB3 in hematopoietic cells causes defective lymphoid development and progressive myeloproliferation. Immunity, 6, 13-22.
50. Shen, W.F., Montgomery, J.C., Rozenfeld, S., Moskow, J.J., Lawrence, H.J., Buchberg, A.M. and Largman, C. (1997a) The AbdB-like proteins stabilize DNA binding by the Meisl homeodomain proteins. Mol. Cell. Biol., 17, 6448-6458.
51. Shen, W.F., Rozenfeld, S., Lawrence, H.J. and Largman, C. (1997b) The Abd-B-like Hox homeodomain proteins can be subdivided by the ability to form complexes with Pbx1a on a novel DNA target. J. Biol. Chem., 272, 8198-8206.
52. Steelman, S., Moskow, J.J., Muzynski, K., North, C., Druck, T., Montgomery, J.C., Huebner, K., Daar, I.O. and Buchberg, A.M. (1997) Identification of a conserved family of Meis-1-related homeobox genes. Genome Res., 7, 142-156.
53. Sun, B., Hursh, D.A., Jackson, D. and Beachy, P.A. (1995) Ultrabithorax protein is necessary but not sufficient for full activation of decapentaplegic expression in the visceral mesoderm. EMBO J., 14, 520-535.
54. Thomas, K.R. and Capecchi, M.R. (1987) Site-directed mutagenesis by gene targeted in mouse embryo-derived stem cell. Cell, 51, 503-512.
55. Thorsteinsdottir, U., Sauvageau, G., Hough, M.R., 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 leukemia. Mol. Cell. Biol., 17, 495-505.
56. Watrin, F. and Wolgemuth, D.J. (1993) Conservation and divergence of patterns of expression and lineage-specific transcripts in orthogues and paralogues of the mouse Hox-1.4 gene. Dev. Biol., 156, 136-145.
57. Zhang, P., Benson, G.V., Rhoades, K.L., Maas, R.L. and Tenen, D.G. (1996) HOXA-10 deficient mice exhibit increased myelopoiesis and overproliferation of myeloid colony forming units. Blood, 88, 631a.