Overexpression of CDX2 perturbs HOX gene expression in murine progenitors depending on its N-terminal domain and is closely correlated with deregulated HOX gene expression in human acute myeloid leukemia

Blood

Volumn 111, Issue 1, 2008, Pages 309-319

  Rawat, Vijay P S ^a,b   Thoene, Silvia ^a,b   Naidu, Vegi M ^a,b   Arseni, Natalia ^a,b   Heilmeier, Bernhard ^a   Metzeler, Klaus ^a   Petropoulos, Konstantin ^a,b   Deshpande, Aniruddha ^a,b   Quintanilla Martinez, Leticia ^b   Bohlander, Stefan K ^a,b   Spiekermann, Karsten ^a,b   Hiddemann, Wolfgang ^a,b   Feuring Buske, Michaela ^a,b   Buske, Christian ^a,b  

^a LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

^b INSTITUTE OF EPIDEMIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

TRANSCRIPTION FACTOR CDX2;

ACUTE GRANULOCYTIC LEUKEMIA; AMINO TERMINAL SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHROMOSOME TRANSLOCATION; CONTROLLED STUDY; GENE DELETION; GENE EXPRESSION REGULATION; GENE INACTIVATION; GENE OVEREXPRESSION; HOX GENE; HUMAN; HUMAN CELL; KARYOTYPE; MOUSE; NONHUMAN; PRIORITY JOURNAL; STEM CELL;

EID: 38049141542     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2007-04-085407     Document Type: Article

References (59)

1. Rowley JD. The critical role of chromosome translocations in human leukemias. Annu Rev Genet. 1998;32:495-519.
2. Golub TR, Slonim DK, Tamayo P, et al. Molecular classification of cancer: class discovery and class prediction by gene expression monitoring. Science. 1999;286:531-537.
3. Armstrong SA, Staunton JE, Silverman LB, et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet. 2002;30:41-47.
4. Debernardi S, Lillington DM, Chaplin T, et al. Genome-wide analysis of acute myeloid leukemia with normal karyotype reveals a unique pattern of homeobox gene expression distinct from those with translocation-mediated fusion events. Genes Chromosomes Cancer. 2003;37:149-158.
5. Buske C, Humphries RK. Homeobox genes in leukemogenesis. Int J Hematol. 2000;71:301-308.
6. Thorsteinsdottir U, Kroon E, Jerome L, Blasi F, Sauvageau G. Defining roles for HOX and MEIS1 genes in induction of acute myeloid leukemia. Mol Cell Biol. 2001;21:224-234.
7. Buske C, Feuring-Buske M, Antonchuk J, et al. Overexpression of HOXA10 perturbs human lymphomyelopoiesis in vitro and in vivo. Blood. 2001;97:2286-2292.
8. Sauvageau G, Lansdorp PM, Eaves CJ, 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.
9. Abramovich C, Pineault N, Ohta H, Humphries RK. Hox genes: from leukemia to hematopoietic stem cell expansion. Ann N Y Acad Sci. 2005;1044:109-116.
10. Okada Y, Jiang Q, Lemieux M, Jeannotte L, Su L, Zhang Y. Leukaemic transformation by CALMAF10 involves upregulation of Hoxa5 by hDOT1L. Nat Cell Biol. 2006;8:1017-1024.
11. Kohlmann A, Schoch C, Dugas M, et al. New insights into MLL gene rearranged acute leukemias using gene expression profiling: shared pathways, lineage commitment, and partner genes. Leukemia. 2005;19:953-964.
12. Alcalay M, Tiacci E, Bergomas R, et al. Acute myeloid leukemia bearing cytoplasmic nucleophosmin (NPMc+AML) shows a distinct gene expression profile characterized by up-regulation of genes involved in stem-cell maintenance. Blood. 2005;106:899-902.
13. Deshpande AJ, Cusan M, Rawat VP, et al. Acute myeloid leukemia is propagated by a leukemic stem cell with lymphoid characteristics in a mouse model of CALM/AF10-positive leukemia. Cancer Cell. 2006;10:363-374.
14. Slany RK. When epigenetics kills: MLL fusion proteins in leukemia. Hematol Oncol. 2005;23:1-9.
15. Verhaak RG, Goudswaard CS, van Putten W, et al. Mutations in nucleophosmin (NPM1) in acute myeloid leukemia (AML): association with other gene abnormalities and previously established gene expression signatures and their favorable prognostic significance. Blood. 2005;106:3747-3754.
16. Falini B, Nicoletti I, Martelli MF, Mecucci C. Acute myeloid leukemia carrying cytoplasmic/mutated nucleophosmin (NPMc+AML): biologic and clinical features. Blood. 2007;109:874-885.
17. Brooke NM, Garcia-Fernandez J, Holland PW. The ParaHox gene cluster is an evolutionary sister of the Hox gene cluster. Nature. 1998;392:920-922.
18. Chawengsaksophak K, de Graaff W, Rossant J, Deschamps J, Beck F. Cdx2 is essential for axial elongation in mouse development. Proc Natl Acad Sci U S A. 2004;101:7641-7645.
19. Mlodzik M, Gehring WJ. Expression of the caudal gene in the germ line of Drosophila: formation of an RNA and protein gradient during early embryogenesis. Cell. 1987;48:465-478.
20. Charite J, de Graaff W, Consten D, Reijnen MJ, Korving J, Deschamps J. Transducing positional information to the Hox genes: critical interaction of cdx gene products with position-sensitive regulatory elements. Development. 1998;125:4349-4358.
21. Gehring WJ. Homeo boxes in the study of development. Science. 1987;236:1245-1252.
22. Davidson AJ, Ernst P, Wang Y, et al. cdx4 mutants fail to specify blood progenitors and can be rescued by multiple hox genes. Nature. 2003;425:300-306.
23. Suh E, Traber PG. An intestine-specific homeobox gene regulates proliferation and differentiation. Mol Cell Biol. 1996;16:619-625.
24. Satoh K, Mutoh H, Eda A, et al. Aberrant expression of CDX2 in the gastric mucosa with and without intestinal metaplasia: effect of eradication of Helicobacter pylori. Helicobacter. 2002;7:192-198.
25. Ishikawa A, Sasaki M, Ohira S, et al. Aberrant expression of CDX2 is closely related to the intestinal metaplasia and MUC2 expression in intraductal papillary neoplasm of the liver in hepatolithiasis. Lab Invest. 2004;84:629-638.
26. Eda A, Osawa H, Satoh K, et al. Aberrant expression of CDX2 in Barrett's epithelium and inflammatory esophageal mucosa. J Gastroenterol. 2003;38:14-22.
27. Silberg DG, Sullivan J, Kang E, et al. Cdx2 ectopic expression induces gastric intestinal metaplasia in transgenic mice. Gastroenterology. 2002;122:689-696.
28. Chase A, Reiter A, Burci L, et al. Fusion of ETV6 to the caudal-related homeobox gene CDX2 in acute myeloid leukemia with the t(12;13)(p13;q12). Blood. 1999;93:1025-1031.
29. Rawat VP, Cusan M, Deshpande A, et al. Ectopic expression of the homeobox gene Cdx2 is the transforming event in a mouse model of t(12; 13)(p13;q12) acute myeloid leukemia. Proc Natl Acad Sci U S A. 2004;101:817-822.
30. Bennett JM, Catovsky D, Daniel MT, et al. Proposed revised criteria for the classification of acute myeloid leukemia: a report of the French-American-British Cooperative Group. Ann Intern Med. 1985;103:620-625.
31. Schnittger S, Weisser M, Schoch C, Hiddemann W, Haferlach T, Kern W. New score predicting for prognosis in PML-RARA+, AML1-ETO+, or CBFBMYH11+ acute myeloid leukemia based on quantification of fusion transcripts. Blood. 2003;102:2746-2755.
32. Schnittger S, Schoch C, Dugas M, et al. Analysis of FLT3 length mutations in 1003 patients with acute myeloid leukemia: correlation to cytogenetics, FAB subtype, and prognosis in the AMLCG study and usefulness as a marker for the detection of minimal residual disease. Blood. 2002;100:59-66.
33. Haferlach T, Kohlmann A, Schnittger S, et al. Global approach to the diagnosis of leukemia using gene expression profiling. Blood. 2005;106:1189-1198.
34. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5:R80.
35. Huber W, von Heydebreck A, Sultmann H, Poustka A, Vingron M. Variance stabilization applied to microarray data calibration and to the quantification of differential expression. Bioinformatics. 2002;18:S96-S104.
36. Scheid S, Spang R. A stochastic downhill search algorithm for estimating the local false discovery rate. IEEE/ACM Trans Comput Biol Bioinform. 2004;1:98-108.
37. Imren S, Fabry ME, Westerman KA, et al. High-level beta-globin expression and preferred intragenic integration after lentiviral transduction of human cord blood stem cells. J Clin Invest. 2004;114:953-962.
38. National Cancer Institute-Frederick. Retrovirus Tagged Cancer Gene database. http://RTCGD.ncifcrf.gov. Accessed February 2007.
39. Bansal D, Scholl C, Frohling S, et al. Cdx4 dysregulates Hox gene expression and generates acute myeloid leukemia alone and in cooperation with Meis1a in a murine model. Proc Natl Acad Sci U S A. 2006;103:16924-16929.
40. Passegue E, Weisman IL. Leukemic stem cells: where do they come from? Stem Cell Rev. 2005;1:181-188.
41. Armstrong SA, Golub TR, Korsmeyer SJ. MLL-rearranged leukemias: insights from gene expression profiling. Semin Hematol. 2003;40:268-273.
42. Nakamura T, Largaespada DA, Lee MP, et al. Fusion of the nucleoporin gene NUP98 to HOXA9 by the chromosome translocation t(7;11)(p15;p15) in human myeloid leukaemia. Nat Genet. 1996;12:154-158.
43. 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.
44. Knoepfler PS, Sykes DB, Pasillas M, Kamps MP. HoxB8 requires its Pbx-interaction motif to block differentiation of primary myeloid progenitors and of most cell line models of myeloid differentiation. Oncogene. 2001;20:5440-5448.
45. Crooks GM, Fuller J, Petersen D, et al. Constitutive HOXA5 expression inhibits erythropoiesis and increases myelopoiesis from human hematopoietic progenitors. Blood. 1999;94:519-528.
46. Sauvageau G, Thorsteinsdottir U, Hough MR, et al. Overexpression of HOXB3 in hematopoietic cells causes defective lymphoid development and progressive myeloproliferation. Immunity. 1997;6:13-22.
47. Thorsteinsdottir U, Sauvageau G, Hough MR, et al. Overexpression of HOXA10 in murine hematopoietic cells perturbs both myeloid and lymphoid differentiation and leads to acute myeloid leukemia. Mol Cell Biol. 1997;17:495-505.
48. Fischbach NA, Rozenfeld S, Shen W, et al. HOXB6 overexpression in murine bone marrow immortalizes a myelomonocytic precursor in vitro and causes hematopoietic stem cell expansion and acute myeloid leukemia in vivo. Blood. 2005;105:1456-1466.
49. Subramanian V, Meyer BI, Gruss P. Disruption of the murine homeobox gene Cdx1 affects axial skeletal identities by altering the mesodermal expression domains of Hox genes. Cell. 1995;83:641-653.
50. Suh E, Chen L, Taylor J, Traber PG. A homeodomain protein related to caudal regulates intestine-specific gene transcription. Mol Cell Biol. 1994;14:7340-7351.
51. Liu T, Zhang X, So CK, et al. Regulation of Cdx2 expression by promoter methylation, and effects of Cdx2 transfection on morphology and gene expression of human esophageal epithelial cells. Carcinogenesis. 2007;28:488-496.
52. Calon A, Gross I, Davidson I, et al. Functional interaction between the homeoprotein CDX1 and the transcriptional machinery containing the TATA-binding protein. Nucleic Acids Res. 2007;35:175-185.
53. Taylor JK, Levy T, Suh ER, Traber PG. Activation of enhancer elements by the homeobox gene Cdx2 is cell line specific. Nucleic Acids Res. 1997;25:2293-2300.
54. Lorentz O, Suh ER, Taylor JK, Boudreau F, Traber PG. CREB-binding protein interacts with the homeodomain protein Cdx2 and enhances transcriptional activity. J Biol Chem. 1999;274:7196-7199.
55. Scholl C, Bansal D, Dohner K, et al. The homeobox gene CDX2 is aberrantly expressed in most cases of acute myeloid leukemia and promotes leukemogenesis. J Clin Invest. 2007;117:1037-1048.
56. Takahashi O, Hamada J, Abe M, et al. Dysregulated expression of HOX and ParaHOX genes in human esophageal squamous cell carcinoma. Oncol Rep. 2007;17:753-760.
57. Simon M, Grandage VL, Linch DC, Khwaja A. Constitutive activation of the Wnt/beta-catenin signalling pathway in acute myeloid leukaemia. Oncogene. 2005;24:2410-2420.
58. Karajannis MA, Vincent L, Direnzo R, et al. Activation of FGFR1beta signaling pathway promotes survival, migration and resistance to chemotherapy in acute myeloid leukemia cells. Leukemia. 2006;20:979-986.
59. Piazza F, Gurrieri C, Pandolfi PP. The theory of APL. Oncogene. 2001;20:7216-7222.