Epigenetic silencing of the oncogenic miR-17-92 cluster during PU.1-directed macrophage differentiation

EMBO Journal

Volumn 30, Issue 21, 2011, Pages 4450-4464

  Pospisil, Vit ^a   Vargova, Karin ^a   Kokavec, Juraj ^a   Rybarova, Jana ^a   Savvulidi, Filipp ^b   Jonasova, Anna ^a   Necas, Emanuel ^a   Zavadil, Jiri ^c   Laslo, Peter ^d   Stopka, Tomas ^a,b  

^a CHARLES UNIVERSITY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d ST JAMES S UNIVERSITY HOSPITAL   (United Kingdom)

Author keywords

AML; chromatin modification; differentiation; miR 17 92; PU.1

Indexed keywords

BIM PROTEIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; EARLY GROWTH RESPONSE FACTOR 2; HISTONE DEMETHYLASE; HISTONE H3; LYSINE; MICRORNA; MIR 17 92; TRANSCRIPTION FACTOR PU 1; UNCLASSIFIED DRUG;

ARTICLE; CELL DIFFERENTIATION; CPG ISLAND; DEMETHYLATION; DOWN REGULATION; EPIGENETICS; GENE CONTROL; GENE EXPRESSION; GENE SILENCING; MACROPHAGE; MYELOID LEUKEMIA; MYELOID PROGENITOR CELL; ONCOGENE; PRIORITY JOURNAL; PROMOTER REGION; TRANSGENICS;

ANIMALS; BASE SEQUENCE; CELL DIFFERENTIATION; CELLS, CULTURED; EARLY GROWTH RESPONSE PROTEIN 2; EPIGENESIS, GENETIC; GENE SILENCING; GENE TRANSFER TECHNIQUES; HL-60 CELLS; HUMANS; JUMONJI DOMAIN-CONTAINING HISTONE DEMETHYLASES; MACROPHAGES; MICE; MICRORNAS; MODELS, BIOLOGICAL; MULTIGENE FAMILY; NIH 3T3 CELLS; NUCLEAR PROTEINS; PROTO-ONCOGENE PROTEINS; REPRESSOR PROTEINS; SEQUENCE HOMOLOGY, NUCLEIC ACID; TRANS-ACTIVATORS; TRANSFECTION;

EID: 80455164567     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2011.317     Document Type: Article

References (67)

1. Back J, Dierich A, Bronn C, Kastner P, Chan S (2004) PU.1 determines the self-renewal capacity of erythroid progenitor cells. Blood 103: 3615-3623 (Pubitemid 38596273)
2. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, Wang Z, Wei G, Chepelev I, Zhao K (2007) High-resolution profiling of histone methylations in the human genome. Cell 129: 823-837 (Pubitemid 46802390)
3. Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116: 281-297
4. Bernstein BE, Humphrey E.L, Erlich R.L, Schneider R, Bouman P, Liu J.S, Kouzarides T, Schreiber S.L. (2002) Methylation of histone H3 Lys 4 in coding regions of active genes. Proc Natl Acad Sci USA 99: 8695-8700 (Pubitemid 34693622)
5. Bernstein BE, Kamal M, Lindblad-Toh K, Bekiranov S, Bailey DK, Huebert DJ, McMahon S, Karlsson EK, Kulbokas 3rd EJ, Gingeras TR, Schreiber SL, Lander ES (2005) Genomic maps and comparative analysis of histone modifications in human and mouse. Cell 120: 169-181 (Pubitemid 40174761)
6. Dey BK, Stalker L, Schnerch A, Bhatia M, Taylor-Papidimitriou J, Wynder C (2008) The histone demethylase KDM5b/JARID1b plays a role in cell fate decisions by blocking terminal differentiation. Mol Cell Biol 28: 5312-5327
7. Dixon-McIver A, East P, Mein CA, Cazier JB, Molloy G, Chaplin T, Andrew Lister T, Young BD, Debernardi S (2008) Distinctive patterns of microRNA expression associated with karyotype in acute myeloid leukaemia. PLoS One 3: e2141
8. Fontana L, Fiori ME, Albini S, Cifaldi L, Giovinazzi S, Forloni M, Boldrini R, Donfrancesco A, Federici V, Giacomini P, Peschle C,Fruci D (2008) Antagomir-17-5p abolishes the growth of therapy-resistant neuroblastoma through p21 and BIM. PLoS One 3: e2236
9. Fontana L, Pelosi E, Greco P, Racanicchi S, Testa U, Liuzzi F, Croce CM, Brunetti E, Grignani F, Peschle C (2007) MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 9: 775-787 (Pubitemid 47019464)
10. Garzon R, Croce CM (2008) MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol 15: 352-358
11. Ghani S, Riemke P, Schonheit J, Lenze D, Stumm J, Hoogenkamp M, Lagendijk A, Heinz S, Bonifer C, Bakkers J, Abdelilah-Seyfried S, Hummel M, Rosenbauer F (2011) Macrophage development from hematopoietic stem cells requires PU.1 coordinated microRNA expression. Blood 118: 2275-2284
12. Grimson A, Farh KK, Johnston WK, Garrett-Engele P, Lim LP, Bartel DP (2007) MicroRNA targeting specificity in mammals: determinants beyond seed pairing. Mol Cell 27: 91-105 (Pubitemid 46991392)
13. Hayashita Y, Osada H, Tatematsu Y, Yamada H, Yanagisawa K, Tomida S, Yatabe Y, Kawahara K, Sekido Y, Takahashi T (2005) A polycistronic microRNA cluster, miR-17-92, is overexpressed in human lung cancers and enhances cell proliferation. Cancer Res 65: 9628-9632 (Pubitemid 41541436)
14. He L, Thomson JM, Hemann MT, Hernando-Monge E, Mu D, Goodson S, Powers S, Cordon-Cardo C, Lowe SW, Hannon GJ, Hammond SM (2005) A microRNA polycistron as a potential human oncogene. Nature 435: 828-833 (Pubitemid 40839734)
15. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576-589
16. Ivanovska I, Ball AS, Diaz RL, Magnus JF, Kibukawa M, Schelter JM, Kobayashi SV, Lim L, Burchard J, Jackson AL, Linsley PS, Cleary MA (2008) MicroRNAs in the miR-106b family regulate p21/CDKN1A and promote cell cycle progression. Mol Cell Biol 28: 2167-2174 (Pubitemid 351429964)
17. Kasashima K, Nakamura Y, Kozu T (2004) Altered expression profiles of microRNAs during TPA-induced differentiation of HL-60 cells. Biochem Biophys Res Commun 322: 403-410 (Pubitemid 39490318)
18. Koralov SB, Muljo SA, Galler GR, Krek A, Chakraborty T, Kanellopoulou C, Jensen K, Cobb BS, Merkenschlager M, Rajewsky N, Rajewsky K (2008) Dicer ablation affects antibody diversity and cell survival in the B lymphocyte lineage. [see comment]. Cell 132: 860-874 (Pubitemid 351312808)
19. Krishnaraju K, Nguyen HQ, Liebermann DA, Hoffman B (1995) The zinc finger transcription factor Egr-1 potentiates macrophage differentiation of hematopoietic cells. Mol Cell Biol 15: 5499-5507
20. Krysinska H, Hoogenkamp M, Ingram R, Wilson N, Tagoh H, Laslo P, Singh H, Bonifer C (2007) A two-step, PU.1-dependent mechanism for developmentally regulated chromatin remodeling and transcription of the c-fms gene. Mol Cell Biol 27: 878-887 (Pubitemid 46174553)
21. Laslo P, Spooner CJ, Warmflash A, Lancki DW, Lee HJ, Sciammas R, Gantner BN, Dinner AR, Singh H (2006) Multilineage transcrip-tional priming and determination of alternate hematopoietic cell fates. Cell 126: 755-766 (Pubitemid 44233633)
22. Li S, Symonds AL, Zhu B, Liu M, Raymond MV, Miao T, Wang P (2011) Early growth response gene-2 (Egr-2) regulates the development of B and T cells. PLoS One 6: e18498
23. Li Z, Lu J, Sun M, Mi S, Zhang H, Luo RT, Chen P, Wang Y, Yan M, Qian Z, Neilly MB, Jin J, Zhang Y, Bohlander SK, Zhang DE, Larson RA, Le Beau MM, Thirman MJ, Golub TR, Rowley JD et al (2008) Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci USA 105: 15535-15540
24. Lopez-Bigas N, Kisiel TA, Dewaal DC, Holmes KB, Volkert TL, Gupta S, Love J, Murray HL, Young RA, Benevolenskaya EV (2008) Genome-wide analysis of the H3K4 histone demethylase RBP2 reveals a transcriptional program controlling differentiation. Mol Cell 31 : 520-530
25. Lu Y, Thomson JM, Wong HY, Hammond SM, Hogan BL (2007) Transgenic over-expression of the microRNA miR-17-92 cluster promotes proliferation and inhibits differentiation of lung epithelial progenitor cells. Dev Biol 310 : 442-453 (Pubitemid 47483685)
26. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, Guenther MG, Johnston WK, Wernig M, Newman J, Calabrese JM, Dennis LM, Volkert TL, Gupta S, Love J, Hannett N, Sharp PA, Bartel DP, Jaenisch R, Young RA (2008) Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell 134: 521-533
27. Martinez NJ, Ow MC, Barrasa MI, Hammell M, Sequerra R, Doucette-Stamm L, Roth FP, Ambros VR, Walhout AJ (2008) A C. elegans genome-scale microRNA network contains composite feedback motifs with high flux capacity. Genes Dev 22: 2535-2549
28. McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, Baribault H, Klemsz M, Feeney AJ, Wu GE, Paige CJ, Maki RA (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15: 5647-5658 (Pubitemid 26385624)
29. Melnick A, Licht JD (2002) Histone deacetylases as therapeutic targets in hematologic malignancies. Curr Opin Hematol 9: 322-332 (Pubitemid 34596877)
30. Nerlov C, Graf T (1998) PU.1 induces myeloid lineage commitment in multipotent hematopoietic progenitors. Genes Dev 12: 2403-2412 (Pubitemid 28371359)
31. Nguyen HQ, Hoffman-Liebermann B, Liebermann DA (1993) The zinc finger transcription factor Egr-1 is essential for and restricts differentiation along the macrophage lineage. Cell 72: 197-209 (Pubitemid 23044935)
32. O'Donnell KA, Wentzel EA, Zeller KI, Dang CV, Mendell JT (2005) c-Myc-regulated microRNAs modulate E2F1 expression. [see comment]. Nature 435: 839-843 (Pubitemid 40839736)
33. Okuda T, van Deursen J, Hiebert SW, Grosveld G, Downing JR (1996) AML1, the target of multiple chromosomal translocations in human leukemia, is essential for normal fetal liver hemato-poiesis. Cell 84: 321-330 (Pubitemid 26042836)
34. Ooi SK, Qiu C, Bernstein E, Li K, Jia D, Yang Z, Erdjument-Bromage H, Tempst P, Lin SP, Allis CD, Cheng X, Bestor TH (2007) DNMT3L connects unmethylated lysine 4 of histone H3 to de novo methylation of DNA. Nature 448: 714-717 (Pubitemid 47236857)
35. Orkin SH, Zon LI (2002) Hematopoiesis and stem cells: plasticity versus developmental heterogeneity. Nat Immunol 3: 323-328 (Pubitemid 34308613)
36. Ota A, Tagawa H, Karnan S, Tsuzuki S, Karpas A, Kira S, Yoshida Y, Seto M (2004) Identification and characterization of a novel gene, C13orf25, as a target for 13q31-q32 amplification in malignant lymphoma. Cancer Res 64: 3087-3095 (Pubitemid 38581408)
37. Petrocca F, Vecchione A, Croce CM (2008a) Emerging role of miR-106b-25/miR-17-92 clusters in the control of transforming growth factor beta signaling. Cancer Res 68: 8191-8194
38. Petrocca F, Visone R, Onelli MR, Shah MH, Nicoloso MS, de Martino I, Iliopoulos D, Pilozzi E, Liu CG, Negrini M, Cavazzini L, Volinia S, Alder H, Ruco LP, Baldassarre G, Croce CM, Vecchione A (2008b) E2F1-regulated microRNAs impair TGFbeta-dependent cell-cycle arrest and apoptosis in gastric cancer. Cancer Cell 13: 272-286 (Pubitemid 351318375)
39. Pons A, Nomdedeu B, Navarro A, Gaya A, Gel B, Diaz T, Valera S, Rozman M, Belkaid M, Montserrat E, Monzo M (2009) Hematopoiesis-related microRNA expression in myelodysplastic syndromes. Leuk Lymphoma 50: 1854-1859
40. Reader JC, Meekins JS, Gojo I, Ning Y (2007) A novel NUP98-PHF23 fusion resulting from a cryptic translocation t(11;17) (p15;p13) in acute myeloid leukemia. Leukemia 21 : 842-844 (Pubitemid 46444583)
41. Rosa A, Ballarino M, Sorrentino A, Sthandier O, De Angelis FG, Marchioni M, Masella B, Guarini A, Fatica A, Peschle C, Bozzoni I (2007) The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation. Proc Natl Acad Sci USA 104: 19849-19854
42. Rosenbauer F, Tenen DG (2007) Transcription factors in myeloid development: balancing differentiation with transformation. Nat Rev Immunol 7: 105-117 (Pubitemid 46174858)
43. Rosenbauer F, Wagner K, Kutok JL, Iwasaki H, Le Beau MM, Okuno Y, Akashi K, Fiering S, Tenen DG (2004) Acute myeloid leukemia induced by graded reduction of a lineage-specific transcription factor, PU.1. Nat Genet 36: 624-630 (Pubitemid 38715991)
44. Schmeier S, MacPherson CR, Essack M, Kaur M, Schaefer U, Suzuki H, Hayashizaki Y, Bajic VB (2009) Deciphering the transcriptional circuitry of microRNA genes expressed during human monocytic differentiation. BMC Genomics 10 : 595
45. Schmidt M, Nagel S, Proba J, Thiede C, Ritter M, Waring JF, Rosenbauer F, Huhn D, Wittig B, Horak I, Neubauer A (1998) Lack of interferon consensus sequence binding protein (ICSBP) transcripts in human myeloid leukemias. Blood 91 : 22-29 (Pubitemid 28018725)
46. Scibetta AG, Santangelo S, Coleman J, Hall D, Chaplin T, Copier J, Catchpole S, Burchell J, Taylor-Papadimitriou J (2007) Functional analysis of the transcription repressor PLU-1/JARID1B. Mol Cell Biol 27: 7220-7235 (Pubitemid 47549757)
47. Scott EW, Simon MC, Anastasi J, Singh H (1994) Requirement of transcription factor PU.1 in the development of multiple hemato-poietic lineages. Science 265: 1573-1577
48. Secombe J, Eisenman RN (2007) The function and regulation of the JARID1 family of histone H3 lysine 4 demethylases: the Myc connection. Cell Cycle 6: 1324-1328 (Pubitemid 47327965)
49. Sims 3rd RJ, Millhouse S, Chen CF, Lewis BA, Erdjument-Bromage H, Tempst P, Manley JL, Reinberg D (2007) Recognition of trimethylated histone H3 lysine 4 facilitates the recruitment of transcription postinitiation factors and pre-mRNA splicing. Mol Cell 28: 665-676 (Pubitemid 350137805)
50. Stopka T, Amanatullah DF, Papetti M, Skoultchi AI (2005) PU.1 inhibits the erythroid program by binding to GATA-1 on DNA and creating a repressive chromatin structure. EMBO J 24: 3712-3723 (Pubitemid 41581688)
51. Srinivasan R, Mager GM, Ward RM, Mayer J, Svaren J (2006) NAB2 represses transcription by interacting with the CHD4 subunit of the nucleosome remodeling and deacetylase (NuRD) complex. J Biol Chem 281: 15129-15137 (Pubitemid 43855102)
52. Svaren J, Sevetson BR, Apel ED, Zimonjic DB, Popescu NC, Milbrandt J (1996) NAB2, a corepressor of NGFI-A (Egr-1) and Krox20, is induced by proliferative and differentiative stimuli. Mol Cell Biol 16: 3545-3553 (Pubitemid 26199873)
53. Sylvestre Y, De Guire V, Querido E, Mukhopadhyay UK, Bourdeau V, Major F, Ferbeyre G, Chartrand P (2007) An E2F/miR-20a auto-regulatory feedback loop. J Biol Chem 282: 2135-2143
54. Tagawa H, Seto M (2005) A microRNA cluster as a target of genomic amplification in malignant lymphoma. Leukemia 19: 2013-2016 (Pubitemid 41554018)
55. Tanzer A, Stadler PF (2004) Molecular evolution of a microRNA cluster. J Mol Biol 339: 327-335 (Pubitemid 38596952)
56. Tsang J, Zhu J, van Oudenaarden A (2007) MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 26: 753-767 (Pubitemid 46856248)
57. van Zutven LJ, Onen E, Velthuizen SC, van Drunen E, von Bergh AR, van den Heuvel-Eibrink MM, Veronese A, Mecucci C, Negrini M, de Greef GE, Beverloo HB (2006) Identification of NUP98 abnormalities in acute leukemia: JARID1A (12p13) as a new partner gene. Genes Chromosomes Cancer 45: 437-446
58. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, Newman J, Bronson RT, Crowley D, Stone JR, Jaenisch R, Sharp PA, Jacks T (2008) Targeted deletion reveals essential and overlapping functions of the miR-17 through 92 family of miRNA clusters. Cell 132: 875-886 (Pubitemid 351312807)
59. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Muckenthaler MU, Ganser A, Eder M, Scherr M (2007) Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood 109: 4399-4405 (Pubitemid 46743409)
60. Volinia S, Calin GA, Liu CG, Ambs S, Cimmino A, Petrocca F, Visone R, Iorio M, Roldo C, Ferracin M, Prueitt RL, Yanaihara N, Lanza G, Scarpa A, Vecchione A, Negrini M, Harris CC, Croce CM (2006) A microRNA expression signature of human solid tumors defines cancer gene targets. Proc Natl Acad Sci USA 10 3 : 2257-2261 (Pubitemid 43271657)
61. Volinia S, Galasso M, Costinean S, Tagliavini L, Gamberoni G, Drusco A, Marchesini J, Mascellani N, Sana ME, Abu Jarour R, Desponts C, Teitell M, Baffa R, Aqeilan R, Iorio MV, Taccioli C, Garzon R, Di Leva G, Fabbri M, Catozzi M et al (2010) Reprogramming of miRNA networks in cancer and leukemia. Genome Res 20: 589-599
62. Walsh JC, DeKoter RP, Lee HJ, Smith ED, Lancki DW, Gurish MF, Friend DS, Stevens RL, Anastasi J, Singh H (2002) Cooperative and antagonistic interplay between PU.1 and GATA-2 in the specification of myeloid cell fates. Immunity 17: 665-676 (Pubitemid 35351511)
63. Wang GG, Song J, Wang Z, Dormann HL, Casadio F, Li H, Luo JL, Patel DJ, Allis CD (2009) Haematopoietic malignancies caused by dysregulation of a chromatin-binding PHD finger. Nature 459: 847-851
64. Woods K, Thomson JM, Hammond SM (2007) Direct regulation of an oncogenic micro-RNA cluster by E2F transcription factors. J Biol Chem 282: 2130-2134 (Pubitemid 47076737)
65. Xiao C, Srinivasan L, Calado DP, Patterson HC, Zhang B, Wang J, Henderson JM, Kutok JL, Rajewsky K (2008) Lymphoproliferative disease and autoimmunity in mice with increased miR-17-92 expression in lymphocytes. Nat Immunol 9: 405-414 (Pubitemid 351405110)
66. Yan HL, Xue G, Mei Q, Wang YZ, Ding FX, Liu MF, Lu MH, Tang Y, Yu HY, Sun SH (2009) Repression of the miR-17-92 cluster by p53 has an important function in hypoxia-induced apoptosis. EMBO J 28: 2719-2732
67. Zhu B, Symonds AL, Martin JE, Kioussis D, Wraith DC, Li S, Wang P (2008) Early growth response gene 2 (Egr-2) controls the self-tolerance of T cells and prevents the development of lupuslike autoimmune disease. J Exp Med 205: 2295-2307