TET1 plays an essential oncogenic role in MLL-rearranged leukemia

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 29, 2013, Pages 11994-11999

  Huang, Hao ^a   Jiang, Xi ^a   Li, Zejuan ^a   Li, Yuanyuan ^a   Song, Chun Xiao ^b   He, Chunjiang ^a   Sun, Miao ^a   Chen, Ping ^a   Gurbuxani, Sandeep ^a   Wang, Jiapeng ^c   Hong, Gia Ming ^a   Elkahloun, Abdel G ^d   Arnovitz, Stephen ^a   Wang, Jinhua ^a   Szulwach, Keith ^e   Lin, Li ^e   Street, Craig ^e   Wunderlich, Mark ^f   Dawlaty, Meelad ^g   Neilly, Mary Beth ^a   Jaenisch, Rudolf ^g   Yang, Feng Chun ^c   Mulloy, James C ^f   Jin, Peng ^e   Liu, Paul P ^d   Rowley, Janet D ^a   Xu, Mingjiang ^c   He, Chuan ^b   Chen, Jianjun ^a   more..

^a UNIVERSITY OF CHICAGO   (United States)

^b UNIVERSITY OF CHICAGO   (United States)

^c INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^e EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^g WHITEHEAD INSTITUTE FOR BIOMEDICAL RESEARCH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; HOMEOBOX A9; HOMEODOMAIN PROTEIN; MIXED LINEAGE LEUKEMIA PROTEIN; TEN ELEVEN TRANSLOCATION 1; TRANSCRIPTION FACTOR PBX3; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ACUTE GRANULOCYTIC LEUKEMIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DOWN REGULATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LEUKEMIA CELL LINE; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR GENE;

CHROMATIN IMMUNOPRECIPITATION; CHROMATOGRAPHY, LIQUID; CYTOSINE; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, NEOPLASTIC; HOMEODOMAIN PROTEINS; HUMANS; IMMUNOBLOTTING; LEUKEMIA, MYELOID, ACUTE; MICROARRAY ANALYSIS; MYELOID-LYMPHOID LEUKEMIA PROTEIN; NEOPLASM PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTO-ONCOGENE PROTEINS; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY;

EID: 84880366679     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1310656110     Document Type: Article

References (59)

1. He YF, et al. (2011) Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333(6047):1303-1307.
2. Ito S, et al. (2011) Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333(6047):1300-1303.
3. Guo JU, Su Y, Zhong C, Ming GL, Song H (2011) Hydroxylation of 5-methylcytosine by TET1 promotes active DNA demethylation in the adult brain. Cell 145(3):423-434.
4. Tahiliani M, et al. (2009) Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324(5929):930-935.
5. Gu TP, et al. (2011) The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature 477(7366):606-610.
6. Dawlaty MM, et al. (2011) Tet1 is dispensable for maintaining pluripotency and its loss is compatible with embryonic and postnatal development. Cell Stem Cell 9(2):166-175.
7. Quivoron C, et al. (2011) TET2 inactivation results in pleiotropic hematopoietic abnormalities in mouse and is a recurrent event during human lymphomagenesis. Cancer Cell 20(1):25-38.
8. Moran-Crusio K, et al. (2011) Tet2 loss leads to increased hematopoietic stem cell selfrenewal and myeloid transformation. Cancer Cell 20(1):11-24.
9. Li Z, et al. (2011) Deletion of Tet2 in mice leads to dysregulated hematopoietic stem cells and subsequent development of myeloid malignancies. Blood 118(17):4509-4518.
10. Dawlaty MM, et al. (2013) Combined deficiency of Tet1 and Tet2 causes epigenetic abnormalities but is compatible with postnatal development. Dev Cell 24(3):310-323.
11. Yamaguchi S, et al. (2012) Tet1 controls meiosis by regulating meiotic gene expression. Nature 492(7429):443-447.
12. Ito S, et al. (2010) Role of Tet proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature 466(7310):1129-1133.
13. Koh KP, et al. (2011) Tet1 and Tet2 regulate 5-hydroxymethylcytosine production and cell lineage specification in mouse embryonic stem cells. Cell Stem Cell 8(2):200-213.
14. Wu H, et al. (2011) Dual functions of Tet1 in transcriptional regulation in mouse embryonic stem cells. Nature 473(7347):389-393.
15. Williams K, et al. (2011) TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature 473(7347):343-348.
16. Xu Y, et al. (2011) Genome-wide regulation of 5hmC, 5mC, and gene expression by Tet1 hydroxylase in mouse embryonic stem cells. Mol Cell 42(4):451-464.
17. Ono R, et al. (2002) LCX, leukemia-Associated protein with a CXXC domain, is fused to MLL in acute myeloid leukemia with trilineage dysplasia having t(10;11)(q22;q23). Cancer Res 62(14):4075-4080.
18. Lorsbach RB, et al. (2003) TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;q23). Leukemia 17(3):637-641.
19. Abdel-Wahab O, et al. (2009) Genetic characterization of TET1, TET2, and TET3 alterations in myeloid malignancies. Blood 114(1):144-147.
20. Delhommeau F, et al. (2009) Mutation in TET2 in myeloid cancers. N Engl J Med 360(22):2289-2301.
21. Ko M, et al. (2010) Impaired hydroxylation of 5-methylcytosine in myeloid cancers with mutant TET2. Nature 468(7325):839-843.
22. Haffner MC, et al. (2011) Global 5-hydroxymethylcytosine content is significantly reduced in tissue stem/progenitor cell compartments and in human cancers. Oncotarget 2(8):627-637.
23. Kudo Y, et al. (2012) Loss of 5-hydroxymethylcytosine is accompanied with malignant cellular transformation. Cancer Sci 103(4):670-676.
24. Yang H, et al. (2013) Tumor development is associated with decrease of TET gene expression and 5-methylcytosine hydroxylation. Oncogene 32(5):663-669.
25. Lian CG, et al. (2012) Loss of 5-hydroxymethylcytosine is an epigenetic hallmark of melanoma. Cell 150(6):1135-1146.
26. Hsu CH, et al. (2012) TET1 suppresses cancer invasion by activating the tissue inhibitors of metalloproteinases. Cell Rep 2(3):568-579.
27. Sun M, et al. (2013) HMGA2/TET1/HOXA9 signaling pathway regulates breast cancer growth and metastasis. Proc Natl Acad Sci USA 110(24):9920-9925.
28. Chen J, Odenike O, Rowley JD (2010) Leukaemogenesis: More than mutant genes. Nat Rev Cancer 10(1):23-36.
29. Krivtsov AV, Armstrong SA (2007) MLL translocations, histone modifications and leukaemia stem-cell development. Nat Rev Cancer 7(11):823-833.
30. Muntean AG, Hess JL (2012) The pathogenesis of mixed-lineage leukemia. Annu Rev Pathol 7:283-301.
31. Martin ME, et al. (2003) Dimerization of MLL fusion proteins immortalizes hematopoietic cells. Cancer Cell 4(3):197-207.
32. Eguchi M, Eguchi-Ishimae M, Greaves M (2004) The small oligomerization domain of gephyrin converts MLL to an oncogene. Blood 103(10):3876-3882.
33. Dobson CL, Warren AJ, Pannell R, Forster A, Rabbitts TH (2000) Tumorigenesis in mice with a fusion of the leukaemia oncogene Mll and the bacterial lacZ gene. EMBO J 19(5):843-851.
34. Baer MR, et al. (1998) Acute myeloid leukemia with 11q23 translocations: Myelomonocytic immunophenotype by multiparameter flow cytometry. Leukemia 12(3): 317-325.
35. Wei J, et al. (2008) Microenvironment determines lineage fate in a human model of MLL-AF9 leukemia. Cancer Cell 13(6):483-495.
36. Milne TA, et al. (2005) MLL associates specifically with a subset of transcriptionally active target genes. Proc Natl Acad Sci USA 102(41):14765-14770.
37. Okada Y, et al. (2005) hDOT1L links histone methylation to leukemogenesis. Cell 121(2):167-178.
38. Bernt KM, et al. (2011) MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 20(1):66-78.
39. Zeisig BB, et al. (2004) Hoxa9 and Meis1 are key targets for MLL-ENL-mediated cellular immortalization. Mol Cell Biol 24(2):617-628.
40. Mueller D, et al. (2009) Misguided transcriptional elongation causes mixed lineage leukemia. PLoS Biol 7(11):e1000249.
41. Li Z, et al. (2012) miR-196b directly targets both HOXA9/MEIS1 oncogenes and FAS tumour suppressor in MLL-rearranged leukaemia. Nat Commun 3:688.
42. Wong P, Iwasaki M, Somervaille TC, So CW, Cleary ML (2007) Meis1 is an essential and rate-limiting regulator of MLL leukemia stem cell potential. Genes Dev 21(21): 2762-2774.
43. Kumar AR, et al. (2009) A role for MEIS1 in MLL-fusion gene leukemia. Blood 113(8): 1756-1758.
44. Faber J, et al. (2009) HOXA9 is required for survival in human MLL-rearranged acute leukemias. Blood 113(11):2375-2385.
45. Ayton PM, Cleary ML (2003) Transformation of myeloid progenitors by MLL oncoproteins is dependent on Hoxa7 and Hoxa9. Genes Dev 17(18):2298-2307.
46. Orlovsky K, et al. (2011) Down-regulation of homeobox genes MEIS1 and HOXA in MLL-rearranged acute leukemia impairs engraftment and reduces proliferation. Proc Natl Acad Sci USA 108(19):7956-7961.
47. Li Z, et al. (2012) Up-regulation of a HOXA-PBX3 homeobox-gene signature following down-regulation of miR-181 is associated with adverse prognosis in patients with cytogenetically abnormal AML. Blood 119(10):2314-2324.
48. Li Z, et al. (2013) PBX3 is an important cofactor of HOXA9 in leukemogenesis. Blood 121(8):1422-1431.
49. Wang GG, Pasillas MP, Kamps MP (2006) Persistent transactivation by meis1 replaces hox function in myeloid leukemogenesis models: Evidence for co-occupancy of meis1-pbx and hox-pbx complexes on promoters of leukemia-Associated genes. Mol Cell Biol 26(10):3902-3916.
50. Jiang X, et al. (2012) Blockade of miR-150 maturation by MLL-fusion/MYC/LIN-28 is required for MLL-Associated leukemia. Cancer Cell 22(4):524-535.
51. Huang Y, et al. (2012) Identification and characterization of Hoxa9 binding sites in hematopoietic cells. Blood 119(2):388-398.
52. Slany RK (2009) The molecular biology of mixed lineage leukemia. Haematologica 94(7):984-993.
53. Mohan M, Lin C, Guest E, Shilatifard A (2010) Licensed to elongate: A molecular mechanism for MLL-based leukaemogenesis. Nat Rev Cancer 10(10):721-728.
54. Muntean AG, et al. (2010) The PAF complex synergizes with MLL fusion proteins at HOX loci to promote leukemogenesis. Cancer Cell 17(6):609-621.
55. Yokoyama A, LinM, Naresh A, Kitabayashi I, ClearyML (2010) A higher-order complex containing AF4 and ENL family proteins with P-TEFb facilitates oncogenic and physiologic MLL-dependent transcription. Cancer Cell 17(2):198-212.
56. Lin C, et al. (2010) AFF4, a component of the ELL/P-TEFb elongation complex and a shared subunit of MLL chimeras, can link transcription elongation to leukemia. Mol Cell 37(3):429-437.
57. Szulwach KE, et al. (2011) Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet 7(6):e1002154.
58. Szulwach KE, et al. (2011) 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci 14(12):1607-1616.
59. Yu M, et al. (2012) Base-resolution analysis of 5-hydroxymethylcytosine in the mammalian genome. Cell 149(6):1368-1380.