HSC commitment-associated epigenetic signature is prognostic in acute myeloid leukemia

Journal of Clinical Investigation

Volumn 124, Issue 3, 2014, Pages 1158-1167

  Bartholdy, Boris ^a   Christopeit, Maximilian ^a   Will, Britta ^a   Mo, Yongkai ^a   Barreyro, Laura ^a   Yu, Yiting ^a   Bhagat, Tushar D ^a   Okoye Okafor, Ujunwa C ^a   Todorova, Tihomira I ^a   Greally, John M ^a   Levine, Ross L ^b   Melnick, Ari ^c   Verma, Amit ^a,d   Steidl, Ulrich ^a,d  

^a ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^b MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

^d MONTEFIORE MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSINE; DNA; KRUPPEL LIKE FACTOR 4; MICRORNA; SMAD2 PROTEIN; TRANSCRIPTION FACTOR GATA; TRANSCRIPTION FACTOR MAF;

ACUTE GRANULOCYTIC LEUKEMIA; ADULT; ARTICLE; CANCER PROGNOSIS; CANCER SURVIVAL; CELL ASSAY; CELL DIFFERENTIATION; COHORT ANALYSIS; DNA DETERMINATION; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENE MUTATION; GENETIC ASSOCIATION; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; MEGAKARYOCYTE ERYTHROID PROGENITOR; MYELOID PROGENITOR CELL; NANOHELP ASSAY; NUCLEOTIDE SEQUENCE; OVERALL SURVIVAL; PRIORITY JOURNAL;

CELL DIFFERENTIATION; DNA METHYLATION; EPIGENESIS, GENETIC; HEMATOPOIETIC STEM CELLS; HUMANS; KAPLAN-MEIER ESTIMATE; LEUKEMIA, MYELOID, ACUTE; PROGNOSIS; PROPORTIONAL HAZARDS MODELS; TRANSCRIPTOME;

EID: 84896693269     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI71264     Document Type: Article

References (63)

1. Shih AH, Abdel-Wahab O, Patel JP, Levine RL. The role of mutations in epigenetic regulators in myeloid malignancies. Nat Rev Cancer. 2012; 12(9):599-612.
2. Cancer Genome Atlas Research Network. Genomic and epigenomic landscapes of adult de novo acute myeloid leukemia. N Engl J Med. 2013; 368(22):2059-2074.
3. Patel JP, et al. Prognostic relevance of integrated genetic profiling in acute myeloid leukemia. N Engl J Med. 2012;366(12):1079-1089.
4. Figueroa ME, et al. DNA methylation signatures identify biologically distinct subtypes in acute myeloid leukemia. Cancer Cell. 2010;17(1):13-27.
5. Ji H, et al. Comprehensive methylome map of lineage commitment from haematopoietic progenitors. Nature. 2010;467(7313):338-342.
6. Shearstone JR, Pop R, Bock C, Boyle P, Meissner A, Socolovsky M. Global DNA demethylation during mouse erythropoiesis in vivo. Science. 2011; 334(6057):799-802.
7. Bock C, et al. DNA methylation dynamics during in vivo differentiation of blood and skin stem cells. Mol Cell. 2012;47(4):633-647.
8. Broske AM, et al. DNA methylation protects hematopoietic stem cell multipotency from myeloerythroid restriction. Nat Genet. 2009;41(11):1207-1215.
9. Trowbridge JJ, Snow JW, Kim J, Orkin SH. DNA methyltransferase 1 is essential for and uniquely regulates hematopoietic stem and progenitor cells. Cell Stem Cell. 2009;5(4):442-449.
10. Challen GA, et al. Dnmt3a is essential for hematopoietic stem cell differentiation. Nat Genet. 2012; 44(1):23-31.
11. Sasaki M, et al. IDH1(R132H) mutation increases murine haematopoietic progenitors and alters epigenetics. Nature. 2012;488(7413):656-659.
12. Moran-Crusio K, et al. Tet2 loss leads to increased hematopoietic stem cell self-renewal and myeloid transformation. Cancer Cell. 2011;20(1):11-24.
13. Quivoron C, et al. TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell. 2011;20(1):25-38.
14. Li Z, et al. Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood. 2011;118(17):4509-4518.
15. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci U S A. 1992;89(7):2804-2808.
16. Craig W, Kay R, Cutler RL, Lansdorp PM. Expression of Thy-1 on human hematopoietic progenitor cells. J Exp Med. 1993;177(5):1331-1342.
17. Manz MG, Miyamoto T, Akashi K, Weissman IL. Prospective isolation of human clonogenic common myeloid progenitors. Proc Natl Acad Sci U S A. 2002;99(18):11872-11877.
18. Steidl U, et al. Essential role of Jun family transcription factors in PU.1 knockdown-induced leukemic stem cells. Nat Genet. 2006;38(11):1269-1277.
19. Steidl U, et al. A distal single nucleotide polymorphism alters long-range regulation of the PU.1 gene in acute myeloid leukemia. J Clin Invest. 2007;117(9):2611-2620.
20. Will B, Steidl U. Multi-parameter fluorescence-activated cell sorting and analysis of stem and progenitor cells in myeloid malignancies. Best Pract Res Clin Haematol. 2010;23(3):391-401.
21. Barreyro L, et al. Overexpression of IL-1 receptor accessory protein in stem and progenitor cells and outcome correlation in AML and MDS. Blood. 2012; 120(6):1290-1298.
22. Khulan B, et al. Comparative isoschizomer profiling of cytosine methylation: the HELP assay. Genome Res. 2006;16(8):1046-1055.
23. Figueroa ME, et al. An integrative genomic and epigenomic approach for the study of transcriptional regulation. PLoS ONE. 2008;3(3):e1882.
24. Oda M, et al. High-resolution genome-wide cytosine methylation profiling with simultaneous copy number analysis and optimization for limited cell numbers. Nucleic Acids Res. 2009;37(12):3829-3839.
25. Will B, et al. Stem and progenitor cells in myelodysplastic syndromes show aberrant stage-specific expansion and harbor genetic and epigenetic alterations. Blood. 2012;120(10):2076-2086.
26. Heuck CJ, et al. Myeloma is characterized by stagespecific alterations in DNA methylation that occur early during myelomagenesis. J Immunol. 2013; 190(6):2966-2975.
27. Behre G, et al. Ras signaling enhances the activity of C/EBP alpha to induce granulocytic differentiation by phosphorylation of serine 11. J Biol Chem. 2002; 277(29):26293-26299
28. Geletu M, et al. Target proteins of C/EBPalphap30 in AML: C/EBPalphap30 enhances sumoylation of C/EBPalphap42 via up-regulation of Ubc9. Blood. 2007;110(9):3301-3309.
29. Pulikkan JA, et al. C/EBPalpha regulated microRNA-34a targets E2F3 during granulopoiesis and is down-regulated in AML with CEBPA mutations. Blood. 2010;116(25):5638-5649.
30. Pulikkan JA, et al. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood. 2010;115(9):1768-1778.
31. Braun BS, Archard JA, Van Ziffle JA, Tuveson DA, Jacks TE, Shannon K. Somatic activation of a conditional KrasG12D allele causes ineffective erythropoiesis in vivo. Blood. 2006;108(6):2041-2044.
32. Zhang J, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012; 481(7380):157-163.
33. Porter CC, et al. Integrated genomic analyses identify WEE1 as a critical mediator of cell fate and a novel therapeutic target in acute myeloid leukemia. Leukemia. 2012;26(6):1266-1276.
34. Sun SM, et al. Transition of highly specific microRNA expression patterns in association with discrete maturation stages of human granulopoiesis. Br J Haematol. 2011;155(3):395-398.
35. Garzon R, Croce CM. MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol. 2008; 15(4):352-358.
36. Chen J, Odenike O, Rowley JD. Leukaemogenesis: more than mutant genes. Nat Rev Cancer. 2010; 10(1):23-36.
37. Jiang X, et al. Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-associated leukemia. Cancer Cell. 2012;22(4):524-535.
38. Li Z, et al. miR-196b directly targets both HOXA9/ MEIS1 oncogenes and FAS tumour suppressor in MLL-rearranged leukaemia. Nat Commun. 2012;3:688.
39. Valk PJ, et al. Prognostically useful gene-expression profiles in acute myeloid leukemia. N Engl J Med. 2004;350(16):1617-1628.
40. Verhaak RG, et al. Prediction of molecular subtypes in acute myeloid leukemia based on gene expression profiling. Haematologica. 2009;94(1):131-134.
41. Fernandez HF, et al. Anthracycline dose intensification in acute myeloid leukemia. N Engl J Med. 2009;361(13):1249-1259.
42. Figueroa ME, et al. Leukemic IDH1 and IDH2 mutations result in a hypermethylation phenotype, disrupt TET2 function, and impair hematopoietic differentiation. Cancer Cell. 2010;18(6):553-567.
43. Goeman JJ, van de Geer SA, de Kort F, van Houwelingen HC. A global test for groups of genes: testing association with a clinical outcome. Bioinformatics. 2004;20(1):93-99.
44. Cox DR. Regression models and life tables. J R Stat Soc B. 1972;34(2):187-220.
45. Gentles AJ, Plevritis SK, Majeti R, Alizadeh AA. Association of a leukemic stem cell gene expression signature with clinical outcomes in acute myeloid leukemia. JAMA. 2010;304(24):2706-2715.
46. Eppert K, et al. Stem cell gene expression programs influence clinical outcome in human leukemia. Nat Med. 2011;17(9):1086-1093.
47. Li Z, et al. Identification of a 24-gene prognostic signature that improves the European LeukemiaNet risk classification of acute myeloid leukemia: an international collaborative study. J Clin Oncol. 2013;31(9):1172-1181.
48. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25(10):1010-1022.
49. Suzuki M, et al. Late-replicating heterochromatin is characterized by decreased cytosine methylation in the human genome. Genome Res. 2011;21(11):1833-1840.
50. Heinz S, et al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38(4):576-589.
51. Bhagat TD, et al. miR-21 mediates hematopoietic suppression in MDS by activating TGF-beta signaling. Blood. 2013;121(15):2875-2881.
52. Zhou L, et al. Reduced SMAD7 leads to overactivation of TGF-beta signaling in MDS that can be reversed by a specific inhibitor of TGF-beta receptor I kinase. Cancer Res. 2011;71(3):955-963.
53. Zhou L, et al. Inhibition of the TGF-beta receptor I kinase promotes hematopoiesis in MDS. Blood. 2008;112(8):3434-3443.
54. Schubeler D. Molecular biology. Epigenetic islands in a genetic ocean. Science. 2012;338(6108):756-757.
55. Yu Y, et al. High resolution methylome analysis reveals widespread functional hypomethylation during adult human erythropoiesis. J Biol Chem. 2013;288(13):8805-8814.
56. Gonen M, et al. CD25 expression status improves prognostic risk classification in AML independent of established biomarkers: ECOG phase 3 trial, E1900. Blood. 2012;120(11):2297-2306.
57. Zhou L, et al. Aberrant epigenetic and genetic marks are seen in myelodysplastic leukocytes and reveal Dock4 as a candidate pathogenic gene on chromosome 7q. J Biol Chem. 2011; 286(28):25211-25223.
58. Nischal S, et al. Methylome profiling reveals distinct alterations in phenotypic and mutational subgroups of myeloproliferative neoplasms. Cancer Res. 2013;73(3):1076-1085.
59. Figueroa ME, et al. Integrated genetic and epigenetic analysis of childhood acute lymphoblastic leukemia. J Clin Invest. 2013;123(7):3099-3111.
60. Figueroa ME, et al. Genome-wide epigenetic analysis delineates a biologically distinct immature acute leukemia with myeloid/T-lymphoid features. Blood. 2009;113(12):2795-2804.
61. Thompson RF, et al. An analytical pipeline for genomic representations used for cytosine methylation studies. Bioinformatics. 2008;24(9):1161-1167.
62. Kaplan EL, Meier P. Nonparametric estimation from incomplete observations. J Am Stat Assoc. 1958; 53(282):457-481.
63. Kawahara M, et al. H2.0-like Homeobox regulates early hematopoiesis and promotes acute myeloid leukemia. Cancer Cell. 2012;22(2):194-208.