Inactivation of HOXA genes by hypermethylation in myeloid and lymphoid malignancy is frequent and associated with poor prognosis

Clinical Cancer Research

Volumn 13, Issue 17, 2007, Pages 5048-5055

  Strathdee, Gordon ^a,i   Holyoake, Tessa L ^b   Sim, Alyson ^a   Parker, Anton ^d   Oscier, David G ^d   Melo, Junia V ^e   Meyer, Stefan ^f,g   Eden, Tim ^g   Dickinson, Anne M ^h   Mountford, Joanne C ^b   Jorgensen, Heather G ^b   Soutar, Richard ^c   Brown, Robert ^a  

^a BEATSON INSTITUTE FOR CANCER RESEARCH   (United Kingdom)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

^c WESTERN INFIRMARY   (United Kingdom)

^d ROYAL BOURNEMOUTH HOSPITAL   (United Kingdom)

^e HAMMERSMITH HOSPITAL   (United Kingdom)

^f UNIVERSITY OF MANCHESTER   (United Kingdom)

^g UNIVERSITY OF MANCHESTER   (United Kingdom)

^h NEWCASTLE UNIVERSITY   (United Kingdom)

ⁱ NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

HOX PROTEIN; PROTEIN HOX A; PROTEIN HOX A4; PROTEIN HOX A5; PROTEIN HOX B; UNCLASSIFIED DRUG; HOMEODOMAIN PROTEIN; HOXA4 PROTEIN, HUMAN; HOXA5 PROTEIN, HUMAN;

ARTICLE; CELL DIFFERENTIATION; CELL SELECTION; CONTROLLED STUDY; DNA METHYLATION; GENE EXPRESSION; GENE SEQUENCE; GENE SILENCING; GRANULOCYTE; HUMAN; HUMAN CELL; HUMAN TISSUE; LEUKEMIA; LYMPHATIC LEUKEMIA; MAJOR CLINICAL STUDY; MYELOID LEUKEMIA; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; BLAST CELL CRISIS; CPG ISLAND; GENETICS; MORTALITY; PATHOLOGY; PROGNOSIS;

BLAST CRISIS; CPG ISLANDS; DNA METHYLATION; HOMEODOMAIN PROTEINS; HUMANS; LEUKEMIA; LEUKEMIA, LYMPHOCYTIC; LEUKEMIA, MYELOID; PROGNOSIS;

EID: 34548819044     PISSN: 10780432     EISSN: None     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-07-0919     Document Type: Article

References (35)

1. Cillo C, Cantile M, Faiella A, Boncinelli E. Homeobox genes in normal and malignant cells. J Cell Physiol 2001;188:161-9.
2. Abramovich C, Humphries RK. Hox regulation of normal and leukemic hematopoietic stem cells. Curr Opin Hematol 2005;12:210-6.
3. Crooks GM, Fuller J, Petersen D, et al. Constitutive HOXA5 expression inhibits erythropoiesis and increases myelopoiesis from human hematopoietic progenitors. Blood1999;94:519-28.
4. Fuller JF, McAdara J, Yaron Y, Sakaguchi M, Fraser JK, Gasson JC. Characterization of HOX gene expression during myelopoiesis: role of HOX A5 in lineage commitment and maturation. Blood 1999;93:3391-400.
5. Buske C, Humphries RK. Homeobox genes in leukemogenesis. Int J Hematol 2000;71:301-8.
6. Borrow J, Shearman AM, Stanton VP, Jr., 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;12:159-67.
7. 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;12:154-8.
8. 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;19:6355-66.
9. Grier DG, Thompson A, Kwasniewska A, McGonigle GJ, Halliday HL, Lappin TR. The pathophysiology of HOX genes and their role in cancer. J Pathol 2005;205:154-71.
10. Mitterbauer-Hohendanner G, Mannhalter C. The biological and clinical significance of MLL abnormalities in haematological malignancies. Eur J Clin Invest 2004;34 Suppl 2:12-24.
11. Debernardi S, Lillington DM, Chaplin T, et al. Genomewide 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;37:149-58.
12. Armstrong SA, Staunton JE, Silverman LB, et al. MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 2002;30:41-7.
13. Strathdee G, Brown R. Aberrant DNA methylation in cancer: potential clinical interventions. Expert Rev Mol Med 2002.
14. Esteller M. Profiling aberrant DNA methylation in hematologic neoplasms: a view from the tip of the iceberg. Clin Immunol 2003;109:80-8.
15. Herman JG, Baylin SB. Gene silencing in cancer in association with promoter hypermethylation. N Engl J Med 2003;349:2042-54.
16. Strathdee G, Sim A, Parker A, Oscier D, Brown R. Promoter hypermethylation silences expression of the HoxA4 gene and correlates with IgVh mutational status in CLL. Leukemia 2006;20:1326-9.
17. Strathdee G, Sim A, Brown R. Control of gene expression by CpG island methylation in normal cells. Biochem Soc Trans 2004;32:913-5.
18. Strathdee G, Sim A, Soutar R, Holyoake TL, Brown R. HOXA5 is targeted by cell-type-specific CpG island methylation in normal cells and during the development of acute myeloid leukaemia. Carcinogenesis 2007;28:299-309.
19. Hasford J, Pfirrmann M, Hehlmann R, et al. A new prognostic score for survival of patients with chronic myeloid leukemia treated with interferon alfa. Writing Committee for the Collaborative CML Prognostic Factors Project Group. J Natl Cancer Inst 1998;90:850-8.
20. Sokal JE, Cox EB, Baccarani M, et al. Prognostic discrimination in "good-risk" chronic granulocytic leukemia. Blood 1984;63:789-99.
21. Guilhot F. Sustained durability of responses plus high rates of cytogenetic responses result in long term benefit for newly diagnosed chronic-phase chronic myeloid leukemia (CML-CP) treated with imatinib (IM) therapy: update from the IRIS study. Blood 2004;104:21.
22. Huntly BJ, Reid AG, Bench AJ, et al. Deletions of the derivative chromosome 9 occur at the time of the Philadelphia translocation and provide a powerful and independent prognostic indicator in chronic myeloid leukemia. Blood 2001;98:1732-8.
23. Grimwade D, Walker H, Oliver F, et al. The importance of diagnostic cytogenetics on outcome in AML: analysis of 1,612 patients entered into the MRC AML 10 trial. The Medical Research Council Adult and Children's Leukaemia Working Parties. Blood 1998;92:2322-33.
24. Xiong Z, Laird PW. COBRA: a sensitive and quantitative DNA methylation assay. Nucleic Acids Res 1997;25:2532-4.
25. Colella S, Shen L, Baggerly KA, Issa JP, Krahe R. Sensitive and quantitative universal pyrosequencing methylation analysis of CpG sites. Biotechniques 2003;35:146-50.
26. Dupont JM, Tost J, Jammes H, Gut IG. De novo quantitative bisulfite sequencing using the pyrosequencing technology. Anal Biochem 2004;333:119-27.
27. Calabretta B, Perrotti D. The biology of CML blast crisis. Blood 2004;103:4010-22.
28. Bird A, Wolffe AP. Methylation-induced repression - belts, braces and chromatin. Cell 1999;99:451-4.
29. Friedman AD. Transcriptional regulation of granulocyte and monocyte development. Oncogene 2002;21:3377-90.
30. Tavor S, Park DJ, Gery S, Vuong PT, Gombart AF, Koeffler HP. Restoration of C/EBPα expression in a BCR-ABL+ cell line induces terminal granulocytic differentiation. J Biol Chem 2003;278:52651-9.
31. Ayton PM, Cleary ML. Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 2003;17:2298-307.
32. Okada Y, Feng Q, Lin Y, et al. hDOT1L links histone methylation to leukemogenesis. Cell 2005;121:167-78.
33. Okada Y, Jiang Q, Lemieux M, Jeannotte L, Su L, Zhang Y. Leukaemic transformation by CALM-AF10 involves upregulation of Hoxa5 by hDOT1L. Nat Cell Biol 2006;8:1017-24.
34. Toyota M, Issa JP. CpG island methylator phenotypes in aging and cancer. Semin Cancer Biol 1999;9:349-57.
35. Roman-Gomez J, Jimenez-Velasco A, Castillejo JA, et al. Promoter hypermethylation of cancer-related genes: a strong independent prognostic factor in acute lymphoblastic leukemia. Blood 2004;104:2492-8.