Histone demethylase KDM2B regulates lineage commitment in normal and malignant hematopoiesis

Journal of Clinical Investigation

Volumn 126, Issue 3, 2016, Pages 905-920

  Andricovich, Jaclyn ^a,b   Kai, Yan ^a,b,c   Peng, Weiqun ^c   Foudi, Adlen ^d   Tzatsos, Alexandros ^a,b  

^a Department of Anatomy and Regenerative Biology ^*  (United States)

^b GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^c GEORGE WASHINGTON UNIVERSITY   (United States)

^d HÔPITAL PAUL BROUSSE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD135 ANTIGEN; CD150 ANTIGEN; CD34 ANTIGEN; CD45 ANTIGEN; CYTOKINE; HISTONE DEMETHYLASE; HISTONE DEMETHYLASE KDM2B; HISTONE H3; INTERFERON; INTERFERON REGULATORY FACTOR 3; INTERFERON REGULATORY FACTOR 5; INTERFERON REGULATORY FACTOR 7; INTERLEUKIN 7 RECEPTOR; K RAS PROTEIN; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; STAT1 PROTEIN; STAT2 PROTEIN; T LYMPHOCYTE RECEPTOR; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR GATA 1; UNCLASSIFIED DRUG; F BOX PROTEIN; KDM2A PROTEIN, HUMAN; KRAS PROTEIN, HUMAN; PROTEIN P21;

ANIMAL EXPERIMENT; ARTICLE; CELL CYCLE; CELL DIFFERENTIATION; COLONY FORMING UNIT GM; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FLOW CYTOMETRY; HEMATOLOGIC MALIGNANCY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; LEUKEMIA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH; ANIMAL; C57BL MOUSE; CELL LINEAGE; CELL TRANSFORMATION; ENZYMOLOGY; GENE EXPRESSION REGULATION; GENETICS; HUMAN; KNOCKOUT MOUSE; LYMPHOMA; PATHOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL LINEAGE; CELL TRANSFORMATION, NEOPLASTIC; F-BOX PROTEINS; GENE EXPRESSION REGULATION, LEUKEMIC; HEMATOPOIESIS; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; LYMPHOMA; MICE, INBRED C57BL; MICE, KNOCKOUT; PROTO-ONCOGENE PROTEINS P21(RAS);

EID: 84959918639     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI84014     Document Type: Article

References (65)

1. Kiel MJ, Yilmaz OH, Iwashita T, Terhorst C, Morrison SJ. SLAM family receptors distinguish hematopoietic stem and progenitor cells and reveal endothelial niches for stem cells. Cell. 2005;121(7):1109-1121.
2. McKinney-Freeman S, et al. The transcriptional landscape of hematopoietic stem cell ontogeny. Cell Stem Cell. 2012;11(5):701-714.
3. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;132(4):631-644.
4. Dzierzak E, Speck NA. Of lineage and legacy: the development of mammalian hematopoietic stem cells. Nat Immunol. 2008;9(2):129-136.
5. Foudi A, et al. Analysis of histone 2B-GFP retention reveals slowly cycling hematopoietic stem cells. Nat Biotechnol. 2009;27(1):84-90.
6. Wilson A, et al. Hematopoietic stem cells reversibly switch from dormancy to selfrenewal during homeostasis and repair. Cell. 2008;135(6):1118-1129.
7. Schuettengruber B, Chourrout D, Vervoort M, Leblanc B, Cavalli G. Genome regulation by polycomb and trithorax proteins. Cell. 2007;128(4):735-745.
8. Gao Z, et al. PCGF homologs, CBX proteins, and RYBP define functionally distinct PRC1 family complexes. Mol Cell. 2012;45(3):344-356.
9. Meyer C, et al. The MLL recombinome of acute leukemias in 2013. Leukemia. 2013;27(11):2165-2176.
10. Lindsley RC, et al. Acute myeloid leukemia ontogeny is defined by distinct somatic mutations. Blood. 2015;125(9):1367-1376.
11. Zhang J, et al. The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature. 2012;481(7380):157-163.
12. Ntziachristos P, et al. Genetic inactivation of the polycomb repressive complex 2 in T cell acute lymphoblastic leukemia. Nat Med. 2012;18(2):298-301.
13. Simon C, et al. A key role for EZH2 and associ-ated genes in mouse and human adult T-cell acute leukemia. Genes Dev. 2012;26(7):651-656.
14. Caye A, et al. Juvenile myelomonocytic leukemia displays mutations in components of the RAS pathway and the PRC2 network. Nat Genet. 2015;47(11):1334-1340.
15. 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.
16. Sneeringer CJ, et al. Coordinated activities of wild-type plus mutant EZH2 drive tumor-associated hypertrimethylation of lysine 27 on histone H3 (H3K27) in human B-cell lymphomas. Proc Natl Acad Sci U S A. 2010;107(49):20980-20985.
17. Morin RD, et al. Somatic mutations altering EZH2 (Tyr641) in follicular diffuse large B-cell lymphomas of germinal-center origin. Nat Genet. 2010;42(2):181-185.
18. Yap DB, et al. Somatic mutations at EZH2 Y641 act dominantly through a mechanism of selectively altered PRC2 catalytic activity, to increase H3K27 trimethylation. Blood. 2011;117(8):2451-2459.
19. Tzatsos A, Pfau R, Kampranis SC, Tsichlis PN. Ndy1/KDM2B immortalizes mouse embryonic fibroblasts by repressing the Ink4a/Arf locus. Proc Natl Acad Sci U S A. 2009;106(8):2641-2646.
20. Pfau R, Tzatsos A, Kampranis SC, Serebrennikova OB, Bear SE, Tsichlis PN. Members of a family of JmjC domain-containing oncoproteins immortalize embryonic fibroblasts via a JmjC domain-dependent process. Proc Natl Acad Sci U S A. 2008;105(6):1907-1912.
21. He J, Nguyen AT, Zhang Y. KDM2b/JHDM1b, an H3K36me2-specific demethylase, is required for initiation maintenance of acute myeloid leukemia. Blood. 2011;117(14):3869-3880.
22. Tzatsos A, et al. KDM2B promotes pancreatic cancer via Polycomb-dependent-independent transcriptional programs. J Clin Invest. 2013;123(2):727-739.
23. Tzatsos A, et al. Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression senescence in primary cells. J Biol Chem. 2011;286(38):33061-33069.
24. Wang T, et al. The histone demethylases Jhdm1a/1b enhance somatic cell reprogramming in a vitamin-C-dependent manner. Cell Stem Cell. 2011;9(6):575-587.
25. Liang G, He J, Zhang Y. Kdm2b promotes induced pluripotent stem cell generation by facilitating gene activation early in reprogramming. Nat Cell Biol. 2012;14(5):457-466.
26. Wu X, Johansen JV, Helin K. Fbxl10/Kdm2b recruits polycomb repressive complex 1 to CpG islands regulates H2A ubiquitylation. Mol Cell. 2013;49(6):1134-1146.
27. He J, Shen L, Wan M, Taranova O, Wu H, Zhang Y. Kdm2b maintains murine embryonic stem cell status by recruiting PRC1 complex to CpG islands of developmental genes. Nat Cell Biol. 2013;15(4):373-384.
28. Mao X, Fujiwara Y, Orkin SH. Improved reporter strain for monitoring Cre recombinase-mediated DNA excisions in mice. Proc Natl Acad Sci U S A. 1999;96(9):5037-5042.
29. Koni PA, Joshi SK, Temann UA, Olson D, Burkly L, Flavell RA. Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med. 2001;193(6):741-754.
30. Huang HT, et al. A network of epigenetic regulators guides developmental haematopoiesis in vivo. Nat Cell Biol. 2013;15(12):1516-1525.
31. Stadtfeld M, Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development. 2005;132(1):203-213.
32. Adolfsson J, et al. Identification of Flt3+ lymphomyeloid stem cells lacking erythro-megakaryocytic potential a revised road map for adult blood lineage commitment. Cell. 2005;121(2):295-306.
33. Bracken AP, Dietrich N, Pasini D, Hansen KH, Helin K. Genome-wide mapping of Polycomb target genes unravels their roles in cell fate transitions. Genes Dev. 2006;20(9):1123-1136.
34. Zhou BO, Ding L, Morrison SJ. Hematopoietic stem and progenitor cells regulate the regeneration of their niche by secreting Angiopoietin-1. Elife. 2015;4:e05521.
35. Xu H, et al. Regulation of bifurcating B cell trajectories by mutual antagonism between transcription factors IRF4 and IRF8. Nat Immunol. 2015;16(12):1274-1281.
36. Wang S, He Q, Ma D, Xue Y, Liu F. Irf4 regulates the choice between T lymphoid-primed progenitor myeloid lineage fates during embryogenesis. Dev Cell. 2015;34(6):621-631.
37. Barretina J, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603-607.
38. Wilson BG, et al. Epigenetic antagonism between polycomb and SWI/SNF complexes during oncogenic transformation. Cancer Cell. 2010;18(4):316-328.
39. Gearhart MD, Corcoran CM, Wamstad JA, Bardwell VJ. Polycomb group and SCF ubiquitin ligases are found in a novel BCOR complex that is recruited to BCL6 targets. Mol Cell Biol. 2006;26(18):6880-6889.
40. Grossmann V, et al. Whole-exome sequencing identifies somatic mutations of BCOR in acute myeloid leukemia with normal karyotype. Blood. 2011;118(23):6153-6163.
41. Huether R, et al. The landscape of somatic mutations in epigenetic regulators across 1,000 paediatric cancer genomes. Nat Commun. 2014;5:3630.
42. Gentles AJ, et al. The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 2015;21(8):938-945.
43. Zhao Z, et al. p53 loss promotes acute myeloid leukemia by enabling aberrant self-renewal. Genes Dev. 2010;24(13):1389-1402.
44. McLean CY, et al. GREAT improves functional interpretation of cis-regulatory regions. Nat Biotechnol. 2010;28(5):495-501.
45. Herranz D, et al. A NOTCH1-driven MYC enhancer promotes T cell development, transformation acute lymphoblastic leukemia. Nat Med. 2014;20(10):1130-1137.
46. Ram O, et al. Combinatorial patterning of chromatin regulators uncovered by genomewide location analysis in human cells. Cell. 2011;147(7):1628-1639.
47. Blackledge NP, et al. Variant PRC1 complexdependent H2A ubiquitylation drives PRC2 recruitment polycomb domain formation. Cell. 2014;157(6):1445-1459.
48. Ernst J, Kellis M. ChromHMM: automating chromatin-state discovery and characterization. Nat Methods. 2012;9(3):215-216.
49. Fukuda T, Tokunaga A, Sakamoto R, Yoshida N. Fbxl10/Kdm2b deficiency accelerates neural progenitor cell death leads to exencephaly. Mol Cell Neurosci. 2011;46(3):614-624.
50. Boulard M, Edwards JR, Bestor TH. FBXL10 protects Polycomb-bound genes from hypermethylation. Nat Genet. 2015;47(5):479-485.
51. Mochizuki-Kashio M, et al. Dependency on the polycomb gene Ezh2 distinguishes fetal from adult hematopoietic stem cells. Blood. 2011;118(25):6553-6561.
52. Delgado-Olguin P, et al. Ezh2-mediated repression of a transcriptional pathway upstream of Mmp9 maintains integrity of the developing vasculature. Development. 2014;141(23):4610-4617.
53. Su IH, et al. Ezh2 controls B cell development through histone H3 methylation Igh rearrangement. Nat Immunol. 2003;4(2):124-131.
54. Lee SC, et al. Polycomb repressive complex 2 component Suz12 is required for hematopoietic stem cell function lymphopoiesis. Blood. 2015;126(2):167-175.
55. Hock H. A complex Polycomb issue: the two faces of EZH2 in cancer. Genes Dev. 2012;26(8):751-755.
56. Ernst T, et al. Inactivating mutations of the histone methyltransferase gene EZH2 in myeloid disorders. Nat Genet. 2010;42(8):722-726.
57. Nikoloski G, et al. Somatic mutations of the histone methyltransferase gene EZH2 in myelodysplastic syndromes. Nat Genet. 2010;42(8):665-667.
58. Ueda T, et al. Fbxl10 overexpression in murine hematopoietic stem cells induces leukemia involving metabolic activation and upregulation of Nsg2. Blood. 2015;125(22):3437-3446.
59. Van Vlierberghe P, Ferrando A. The molecular basis of T cell acute lymphoblastic leukemia. J Clin Invest. 2012;122(10):3398-3406.
60. Lobry C, et al. Notch pathway activation targets AML-initiating cell homeostasis and differentiation. J Exp Med. 2013;210(2):301-319.
61. Lu L, et al. Kdm2a/b lysine demethylases regulate canonical Wnt signaling by modulating the stability of nuclear catenin. Dev Cell. 2015;33(6):660-674.
62. Foudi A, et al. Distinct, strict requirements for Gfi-1b in adult bone marrow red cell platelet generation. J Exp Med. 2014;211(5):909-927.
63. Gurumurthy S, et al. The Lkb1 metabolic sensor maintains haematopoietic stem cell survival. Nature. 2010;468(7324):659-663.
64. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105-1111.
65. Trapnell C, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol. 2010;28(5):511-515.