Transcriptional fine-tuning of microRNA-223 levels directs lineage choice of human hematopoietic progenitors

Cell Death and Differentiation

Volumn 21, Issue 2, 2014, Pages 290-301

  Vian, L ^a   Di Carlo, M ^b   Pelosi, E ^c   Fazi, F ^a   Santoro, S ^c   Cerio, A M ^c   Boe, A ^c   Rotilio, V ^a   Billi, M ^b   Racanicchi, S ^b   Testa, U ^c   Grignani, F ^b   Nervi, C ^a  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF PERUGIA   (Italy)

^c ISTITUTO SUPERIORE DI SANITÀ   (Italy)

Author keywords

hematopoietic lineage choice; microRNA; myelopoiesis; transcriptional regulation

Indexed keywords

CD34 ANTIGEN; MICRORNA 223; MICRORNA; MIRN223 MICRORNA, HUMAN;

ANTIGEN EXPRESSION; ARTICLE; CELL DIFFERENTIATION; CELL LINEAGE; GENE EXPRESSION; GENETIC TRANSCRIPTION; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; CYTOLOGY; GENETICS; METABOLISM; TRANSCRIPTION INITIATION;

ANTIGENS, CD34; CELL LINEAGE; HEMATOPOIETIC STEM CELLS; HUMANS; MICRORNAS; TRANSCRIPTION, GENETIC; TRANSCRIPTIONAL ACTIVATION;

EID: 84892442548     PISSN: 13509047     EISSN: 14765403     Source Type: Journal    
DOI: 10.1038/cdd.2013.145     Document Type: Article

References (51)

1. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell 2008; 132: 631-644. (Pubitemid 351260057)
2. Iwasaki H, Akashi K. Myeloid lineage commitment from the hematopoietic stem cell. Immunity 2007; 26: 726-740. (Pubitemid 46907674)
3. Tenen DG, Hromas R, Licht JD, Zhang DE. Transcription factors, normal myeloid development, and leukemia. Blood 1997; 90: 489-519. (Pubitemid 27299089)
4. Tenen DG. Disruption of differentiation in human cancer: AML shows the way. Nat Rev Cancer 2003; 3: 89-101. (Pubitemid 37328876)
5. O'Connell RM, Baltimore D. MicroRNAs and hematopoietic cell development. Curr Top Dev Biol 2012; 99: 145-174.
6. Alemdehy MF, Erkeland SJ. MicroRNAs: key players of normal and malignant myelopoiesis. Curr Opin Hematol 2012; 19: 261-267.
7. O'Connell RM, Zhao JL, Rao DS. MicroRNA function in myeloid biology. Blood 2011; 118: 2960-2969.
8. Chen C-Z, Li L, Lodish HF, Bartell DP. MicroRNAs modulate hematopoietic lineage differentiation. Science 2004; 303: 83-86. (Pubitemid 38055775)
9. Chen K, Rajewsky N. The evolution of gene regulation by transcription factors and microRNAs. Nat Rev Genet 2007; 8: 93-103. (Pubitemid 46122839)
10. Bartel DP. MicroRNAs: genomics, biogenesis, mechanism and function. Cell 2004; 116: 281-297.
11. Krol J, Loedige I, Filipowicz W. The widespread regulation of microRNA biogenesis, function and decay. Nat Rev Genet 2010; 11: 597-610.
12. Karp X, Ambros V. Developmental biology. Encountering microRNAs in cell fate signaling. Science 2005; 310: 1288-1289. (Pubitemid 41698853)
13. Ambros V. The function of animal miRNAs. Nature 2004; 431: 350-355.
14. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell 2009; 136: 215-233.
15. Mukherji S, Ebert MS, Zheng GX, Tsang JS, Sharp PA, van OA. MicroRNAs can generate thresholds in target gene expression. Nat Genet 2011; 43: 854-859.
16. Shin C, Nam JW, Farh KK, Chiang HR, Shkumatava A, Bartel DP. Expanding the microRNA targeting code: functional sites with centered pairing. Mol Cell 2010; 38: 789-802.
17. Baek D, Villen J, Shin C, Camargo FD, Gygi SP, Bartel DP. The impact of microRNAs on protein output. Nature 2008; 455: 64-71.
18. Zardo G, Ciolfi A, Vian L, Starnes LM, Billi M, Racanicchi S et al. Polycombs and microRNA-223 regulate human granulopoiesis by transcriptional control of target gene expression. Blood 2012; 119: 4034-4046.
19. Benhamed M, Herbig U, Ye T, Dejean A, Bischof O. Senescence is an endogenous trigger for microRNA-directed transcriptional gene silencing in human cells. Nat Cell Biol 2012; 14: 266-275.
20. Lee Y, Kim M, Han J, Yeom KH, Lee S, Baek SH et al. MicroRNA genes are transcribed by RNA polymerase II. EMBO J 2004; 23: 4051-4060. (Pubitemid 39472426)
21. Fazi F, Nervi C. MicroRNA: basic mechanisms and transcriptional regulatory networks for cell fate determination. Cardiovasc Res 2008; 79: 553-561.
22. Tsang J, Zhu J, van Oudenaarden A. MicroRNA-mediated feedback and feedforward loops are recurrent network motifs in mammals. Mol Cell 2007; 26: 753-767. (Pubitemid 46856248)
23. Fontana L, Pelosi E, Greco P, Racanicchi S, Testa U, Liuzzi F et al. MicroRNAs 17-5p-20a-106a control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol 2007; 9: 775-787. (Pubitemid 47019464)
24. Labbaye C, Spinello I, Quaranta MT, Pelosi E, Pasquini L, Petrucci E et al. A three-step pathway comprising PLZF/miR-146a/CXCR4 controls megakaryopoiesis. Nat Cell Biol 2008; 10: 788-801. (Pubitemid 351927708)
25. Fazi F, Rosa A, Fatica A, Gelmetti V, De Marchis ML, Nervi C et al. A minicircuitry comprised of microRNA-223 and transcription factors NFI-A and C/EBPalpha regulates human granulopoiesis. Cell 2005; 123: 819-831. (Pubitemid 41721029)
26. Lee J, Li Z, Brower-Sinning R, John B. Regulatory circuit of human microRNA biogenesis. PLoS Comput Biol 2007; 3: e67.
27. Saini HK, Griffiths-Jones S, Enright AJ. Genomic analysis of human microRNA transcripts. Proc Natl Acad Sci USA 2007; 104: 17719-17724. (Pubitemid 350210901)
28. Chien CH, Sun YM, Chang WC, Chiang-Hsieh PY, Lee TY, Tsai WC et al. Identifying transcriptional start sites of human microRNAs based on high-throughput sequencing data. Nucleic Acids Res 2011; 39: 9345-9356.
29. Nervi C, Fazi F, Rosa A, Fatica A, Bozzoni I. Emerging role for microRNAs in acute promyelocytic leukemia. Curr Top Microbiol Immunol 2007; 313: 73-84. (Pubitemid 47400333)
30. Fazi F, Racanicchi S, Zardo G, Starnes LM, Mancini M, Travaglini L et al. Epigenetic silencing of the myelopoiesis regulator microRNA-223 by the AML1/ETO oncoprotein. Cancer Cell 2007; 12: 457-466. (Pubitemid 350046404)
31. Fukao T, Fukuda Y, Kiga K, Sharif J, Hino K, Enomoto Y et al. An evolutionarily conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell 2007; 129: 617-631. (Pubitemid 46660972)
32. Birnie GD. The HL60 cell line: a model system for studying human myeloid cell differentiation. Br J Cancer Suppl 1988; 9: 41-45. (Pubitemid 19054738)
33. Luisi-DeLuca C, Mitchell T, Spriggs D, Kufe DW. Induction of terminal differentiation in human K562 erythroleukemia cells by arabinofuranosylcytosine. J Clin Invest 1984; 74: 821-827. (Pubitemid 14031017)
34. Lin FT, MacDougald OA, Diehl AM, Lane MD. A 30-kDa alternative translation product of the CCAAT/enhancer binding protein alpha message: transcriptional activator lacking antimitotic activity. Proc Natl Acad Sci USA 1993; 90: 9606-9610. (Pubitemid 23315834)
35. Quintana-Bustamante O, Lan-Lan SS, Griessinger E, Reyal Y, Vargaftig J, Lister TA et al. Overexpression of wild-type or mutants forms of CEBPA alter normal human hematopoiesis. Leukemia 2012; 26: 1537-1546.
36. Descombes P, Schibler U. A liver-enriched transcriptional activator protein, LAP, and a transcriptional inhibitory protein, LIP, are translated from the same mRNA. Cell 1991; 67: 569-579. (Pubitemid 121001471)
37. Li T, Morgan MJ, Choksi S, Zhang Y, Kim YS, Liu ZG. MicroRNAs modulate the noncanonical transcription factor NF-kappaB pathway by regulating expression of the kinase IKKalpha during macrophage differentiation. Nat Immunol 2010; 11: 799-805.
38. Chen Q, Wang H, Liu Y, Song Y, Lai L, Han Q et al. Inducible microRNA-223 down-regulation promotes TLR-triggered IL-6 and IL-1beta production in macrophages by targeting STAT3. PLoS One 2012; 7: e42971.
39. Vitelli L, Condorelli G, Lulli V, Hoang T, Luchetti L, Croce CM et al. A pentamer transcriptional complex including tal-1 and retinoblastoma protein downmodulates c-kit expression in normal erythroblasts. Mol Cell Biol 2000; 20: 5330-5342. (Pubitemid 30431586)
40. Zardo G, Ciolfi A, Vian L, Billi M, Racanicchi S, Grignani F et al. Transcriptional targeting by microRNA-Polycomb complexes: A novel route in cell fate determination. Cell Cycle 2012; 11: 3543-3549.
41. Johnnidis JB, Harris MH, Wheeler RT, Stehling-Sun S, Lam MH, Kirak O et al. Regulation of progenitor cell proliferation and granulocyte function by microRNA-223. Nature 2008; 451: 1125-1129. (Pubitemid 351317447)
42. Felli N, Pedini F, Romania P, Biffoni M, Morsilli O, Castelli G et al. MicroRNA 223-dependent expression of LMO2 regulates normal erythropoiesis. Haematologica 2009; 94: 479-486.
43. Eyholzer M, Schmid S, Schardt JA, Haefliger S, Mueller BU, Pabst T. Complexity of miR-223 regulation by CEBPA in human AML. Leuk Res 2010; 34: 672-676.
44. Pulikkan JA, Dengler V, Peramangalam PS, Peer Zada AA, Muller-Tidow C, Bohlander SK et al. Cell-cycle regulator E2F1 and microRNA-223 comprise an autoregulatory negative feedback loop in acute myeloid leukemia. Blood 2010; 115: 1768-1778.
45. Ayoubi TA, Van de Ven WJ. Regulation of gene expression by alternative promoters. FASEB J 1996; 10: 453-460. (Pubitemid 26120320)
46. Schanen BC, Li X. Transcriptional regulation of mammalian miRNA genes. Genomics 2011; 97: 1-6.
47. Gabbianelli M, Testa U, Massa A, Pelosi E, Sposi NM, Riccioni R et al. Hemoglobin switching in unicellular erythroid culture of sibling erythroid burst-forming units: kit ligand induces a dose-dependent fetal hemoglobin reactivation potentiated by sodium butyrate. Blood 2000; 95: 3555-3561. (Pubitemid 30428491)
48. Starnes LM, Sorrentino A, Pelosi E, Ballarino M, Morsilli O, Biffoni M et al. NFI-A directs the fate of hematopoietic progenitors to the erythroid or granulocytic lineage and controls beta-globin and G-CSF receptor expression. Blood 2009; 114: 1753-1763.
49. Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythroleukemic cell growth via kit receptor downmodulation. Proc Natl Acad Sci USA 2005; 102: 18081-18086. (Pubitemid 41798505)
50. Grabe N. AliBaba2: context specific identification of transcription factor binding sites. In Silico Biol 2002; 2: S1-S15. (Pubitemid 33138331)
51. Grignani F, Kinsella T, Mencarelli A, Valtieri M, Riganelli D, Grignani F et al. High-efficiency gene transfer and selection of human hematopoietic progenitor cells with a hybrid EBV/retroviral vector expressing the green fluorescence protein. Cancer Res 1998; 58: 14-19. (Pubitemid 28027708)