Isolated Hoxa9 overexpression predisposes to the development of lymphoid but not myeloid leukemia

Experimental Hematology

Volumn 41, Issue 6, 2013, Pages 518-529.e5

  Beachy, Sarah H ^a   Onozawa, Masahiro ^a   Silverman, Deborah ^a   Chung, Yang Jo ^a   Rivera, Mariela Martinez ^a   Aplan, Peter D ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MIR196B; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR HOXA9; UNCLASSIFIED DRUG; VAV PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CANCER SUSCEPTIBILITY; CONTROLLED STUDY; FEMALE; GENE; GENE MUTATION; GENE OVEREXPRESSION; HEMATOPOIETIC TISSUE; HOXA9 GENE; LYMPHATIC LEUKEMIA; LYMPHOBLASTOMA; MALE; MALIGNANT TRANSFORMATION; MEIS1 GENE; MOUSE; MYELOID LEUKEMIA; NONHUMAN; NOTCH1 GENE; NUCLEOTIDE SEQUENCE; PBX3 GENE; PRIORITY JOURNAL; VAV GENE;

MURINAE; MUS; MUS MUSCULUS;

EID: 84878183730     PISSN: 0301472X     EISSN: 18732399     Source Type: Journal    
DOI: 10.1016/j.exphem.2013.02.006     Document Type: Article

References (54)

1. Argiropoulos B., Humphries R.K. Hox genes in hematopoiesis and leukemogenesis. Oncogene 2007, 26:6766-6776.
2. Gehring W.J., Muller M., Affolter M., et al. The structure of the homeodomain and its functional implications. Trends Genet 1990, 6:323-329.
3. Kawagoe H., Humphries R.K., Blair A., Sutherland H.J., Hogge D.E. Expression of HOX genes, HOX cofactors, and MLL in phenotypically and functionally defined subpopulations of leukemic and normal human hematopoietic cells. Leukemia 1999, 13:687-698.
4. Moretti P., Simmons P., Thomas P., et al. Identification of homeobox genes expressed in human haemopoietic progenitor cells. Gene 1994, 144:213-219.
5. Pineault N., Helgason C.D., Lawrence H.J., Humphries R.K. Differential expression of Hox, Meis1, and Pbx1 genes in primitive cells throughout murine hematopoietic ontogeny. Exp Hematol 2002, 30:49-57.
6. Sauvageau G., Lansdorp P.M., Eaves C.J., et al. Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci U S A 1994, 91:12223-12227.
7. Lawrence H.J., Christensen J., Fong S., et al. Loss of expression of the Hoxa-9 homeobox gene impairs the proliferation and repopulating ability of hematopoietic stem cells. Blood 2005, 106:3988-3994.
8. Lawrence H.J., Helgason C.D., Sauvageau G., et al. Mice bearing a targeted interruption of the homeobox gene HOXA9 have defects in myeloid, erythroid, and lymphoid hematopoiesis. Blood 1997, 89:1922-1930.
9. Kroon E., Krosl J., Thorsteinsdottir U., Baban S., Buchberg A.M., Sauvageau G. Hoxa9 transforms primary bone marrow cells through specific collaboration with Meis1a but not Pbx1b. EMBO J 1998, 17:3714-3725.
10. Nakamura T., Largaespada D.A., Shaughnessy J.D., Jenkins N.A., Copeland N.G. Cooperative activation of Hoxa and Pbx1-related genes in murine myeloid leukaemias. Nat Genet 1996, 12:149-153.
11. Borrow J., Shearman A.M., Stanton V.P., et al. The t(7;11)(p15;p15) translocation in acute myeloid leukaemia fuses the genes for nucleoporin NUP98 and class I homeoprotein HOXA9. Nat Genet 1996, 12:159-167.
12. Golub T.R., Slonim D.K., Tamayo P., et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science 1999, 286:531-537.
13. Harper D.P., Aplan P.D. Chromosomal rearrangements leading to MLL gene fusions: clinical and biological aspects. Cancer Res 2008, 68:10024-10027.
14. Gough S.M., Slape C.I., Aplan P.D. NUP98 gene fusions and hematopoietic malignancies: common themes and new biologic insights. Blood 2011, 118:6247-6257.
15. Caudell D., Aplan P.D. The role of CALM-AF10 gene fusion in acute leukemia. Leukemia 2008, 22:678-685.
16. Armstrong S.A., Staunton J.E., Silverman L.B., et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 2002, 30:41-47.
17. Faber J., Krivtsov A.V., Stubbs M.C., et al. HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood 2009, 113:2375-2385.
18. Rozovskaia T., Feinstein E., Mor O., et al. Upregulation of Meis1 and HoxA9 in acute lymphocytic leukemias with the t(4:11) abnormality. Oncogene 2001, 20:874-878.
19. Asnafi V., Radford-Weiss I., Dastugue N., et al. CALM-AF10 is a common fusion transcript in T-ALL and is specific to the TCRgammadelta lineage. Blood 2003, 102:1000-1006.
20. Speleman F., Cauwelier B., Dastugue N., et al. A new recurrent inversion, inv(7)(p15q34), leads to transcriptional activation of HOXA10 and HOXA11 in a subset of T-cell acute lymphoblastic leukemias. Leukemia 2005, 19:358-366.
21. Choi C.W., Chung Y.J., Slape C., Aplan P.D. A NUP98-HOXD13 fusion gene impairs differentiation of B and T lymphocytes and leads to expansion of thymocytes with partial TCRB gene rearrangement. J Immunol 2009, 183:6227-6235.
22. Gough S.M., Lee F., Chung Y.J., et al. A NUP98-PHF23 transgenic mouse model develops AML and T-ALL. Blood 2011, 118:1058.
23. Thorsteinsdottir U., Krosl J., Kroon E., Haman A., Hoang T., Sauvageau G. The oncoprotein E2A-Pbx1a collaborates with Hoxa9 to acutely transform primary bone marrow cells. Mol Cell Biol 1999, 19:6355-6366.
24. Thorsteinsdottir U., Mamo A., Kroon E., et al. Overexpression of the myeloid leukemia-associated Hoxa9 gene in bone marrow cells induces stem cell expansion. Blood 2002, 99:121-129.
25. Ogilvy S., Metcalf D., Gibson L., Bath M.L., Harris A.W., Adams J.M. Promoter elements of vav drive transgene expression in vivo throughout the hematopoietic compartment. Blood 1999, 94:1855-1863.
26. Caudell D., Zhang Z., Chung Y.J., Aplan P.D. Expression of a CALM-AF10 fusion gene leads to Hoxa cluster overexpression and acute leukemia in transgenic mice. Cancer Res 2007, 67:8022-8031.
27. Morse H.C., Anver M.R., Fredrickson T.N., et al. Bethesda proposals for classification of lymphoid neoplasms in mice. Blood 2002, 100:246-258.
28. Holmes R., Zuniga-Pflucker J.C. The OP9-DL1 system: generation of T-lymphocytes from embryonic or hematopoietic stem cells in vitro. Cold Spring Harb Protoc 2009, 2009:pdb.prot5156.
29. Pineault N., Buske C., Feuring-Buske M., et al. Induction of acute myeloid leukemia in mice by the human leukemia-specific fusion gene NUP98-HOXD13 in concert with Meis1. Blood 2003, 101:4529-4538.
30. Lin Y.W., Slape C., Zhang Z., Aplan P.D. NUP98-HOXD13 transgenic mice develop a highly penetrant, severe myelodysplastic syndrome that progresses to acute leukemia. Blood 2005, 106:287-295.
31. Calvo K.R., Sykes D.B., Pasillas M., Kamps M.P. Hoxa9 immortalizes a granulocyte-macrophage colony-stimulating factor-dependent promyelocyte capable of biphenotypic differentiation to neutrophils or macrophages, independent of enforced meis expression. Mol Cell Biol 2000, 20:3274-3285.
32. Schnabel C.A., Jacobs Y., Cleary M.L. HoxA9-mediated immortalization of myeloid progenitors requires functional interactions with TALE cofactors Pbx and Meis. Oncogene 2000, 19:608-616.
33. Krivtsov A.V., Twomey D., Feng Z., et al. Transformation from committed progenitor to leukaemia stem cell initiated by MLL-AF9. Nature 2006, 442:818-822.
34. Popovic R., Riesbeck L.E., Velu C.S., et al. Regulation of mir-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood 2009, 113:3314-3322.
35. Schotte D., Lange-Turenhout E.A., Stumpel D.J., et al. Expression of miR-196b is not exclusively MLL-driven but is especially linked to activation of HOXA genes in pediatric acute lymphoblastic leukemia. Haematologica 2010, 95:1675-1682.
36. Lin Y.W., Aplan P.D. Gene expression profiling of precursor T-cell lymphoblastic leukemia/lymphoma identifies oncogenic pathways that are potential therapeutic targets. Leukemia 2007, 21:1276-1284.
37. Novak R.L., Harper D.P., Caudell D., Slape C., Beachy S.H., Aplan P.D. Gene expression profiling and candidate gene resequencing identifies pathways and mutations important for malignant transformation caused by leukemogenic fusion genes. Exp Hematol 2012, 40:1016-1027.
38. Armstrong F., Brunet de la Grange P., Gerby B., et al. NOTCH is a key regulator of human T-cell acute leukemia initiating cell activity. Blood 2009, 113:1730-1740.
39. Morgado E., Albouhair S., Lavau C. Flt3 is dispensable to the Hoxa9/Meis1 leukemogenic cooperation. Blood 2007, 109:4020-4022.
40. Somervaille T.C., Cleary M.L. Identification and characterization of leukemia stem cells in murine MLL-AF9 acute myeloid leukemia. Cancer Cell 2006, 10:257-268.
41. Heuser M., Yun H., Berg T., et al. Cell of origin in AML: susceptibility to MN1-induced transformation is regulated by the MEIS1/AbdB-like HOX protein complex. Cancer Cell 2011, 20:39-52.
42. Van Vlierberghe P., van Grotel M., Tchinda J., et al. The recurrent SET-NUP214 fusion as a new HOXA activation mechanism in pediatric T-cell acute lymphoblastic leukemia. Blood 2008, 111:4668-4680.
43. Soulier J., Clappier E., Cayuela J.M., et al. HOXA genes are included in genetic and biologic networks defining human acute T-cell leukemia (TALL). Blood 2005, 106:274-286.
44. Ferrando A.A., Armstrong S.A., Neuberg D.S., et al. Gene expression signatures in MLL-rearranged T-lineage and B-precursor acute leukemias: dominance of HOX dysregulation. Blood 2003, 102:262-268.
45. Cauwelier B., Cave H., Gervais C., et al. Clinical, cytogenetic and molecular characteristics of 14 T-ALL patients carrying the TCRbeta-HOXA rearrangement: a study of the Groupe Francophone de Cytogenetique Hematologique. Leukemia 2007, 21:121-128.
46. Lin Y.W., Nichols R.A., Letterio J.J., Aplan P.D. Notch1 mutations are important for leukemic transformation in murine models of precursor-T leukemia/lymphoma. Blood 2006, 107:2540-2543.
47. O'Neil J., Calvo J., McKenna K., et al. Activating Notch1 mutations in mouse models of T-ALL. Blood 2006, 107:781-785.
48. Weng A.P., Ferrando A.A., Lee W., et al. Activating mutations of NOTCH1 in human T cell acute lymphoblastic leukemia. Science 2004, 306:269-271.
49. Pear W.S., Aster J.C., Scott M.L., et al. Exclusive development of T cell neoplasms in mice transplanted with bone marrow expressing activated Notch alleles. J Exp Med 1996, 183:2283-2291.
50. Kumar A.R., Hudson W.A., Chen W., Nishiuchi R., Yao Q., Kersey J.H. Hoxa9 influences the phenotype but not the incidence of Mll-AF9 fusion gene leukemia. Blood 2004, 103:1823-1828.
51. Wang G.G., Song J., Wang Z., et al. Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 2009, 459:847-851.
52. Trivedi C.M., Patel R.C., Patel C.V. Differential regulation of HOXA9 expression by nuclear factor kappa B (NF-kappaB) and HOXA9. Gene 2008, 408:187-195.
53. Horton S.J., Grier D.G., McGonigle G.J., et al. Continuous MLL-ENL expression is necessary to establish a " Hox Code" and maintain immortalization of hematopoietic progenitor cells. Cancer Res 2005, 65:9245-9252.
54. Wong P., Iwasaki M., Somervaille T.C., So C.W., Cleary M.L. Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev 2007, 21:2762-2774.