Leukemia Research
Volume 33, Issue 12 , Pages 1584-1593 , December 2009

MicroRNAs in normal and malignant myelopoiesis

Received 27 April 2009 ,Revised 27 April 2009 ,Accepted 28 April 2009.

References 

  1. Ventura A, Young AG, Winslow MM, Lintault L, Meissner A, Erkeland SJ, et al. Targeted deletion reveals essential functions of the miR-17 through 92 family of miRNA clusters. Cell. 2008;132:875–886
  2. Kim VN, Han J, Siomi MC. Biogenesis of small RNAs in animals. Nat Rev Mol Cell Biol. 2009;10:126–139
  3. Ruby JG, Jan CH, Bartel DP. Intronic microRNA precursors that bypass Drosha processing. Nature. 2007;448:83–86
  4. Filipowicz W, Batthacharyya SN, Sonenberg N. Mechanisms of post-transcriptional regulation by micro-RNAs: are the answer in sight?. Nat Rev Genet. 2008;9:102–114
  5. Selbach M, Schwanhausser B, Thierfelder N, Fang Z, Khenin R, Rjewsky N. Widespread changes in protein synthesis is induced by microRNAs. Nature. 2008;455:58–63
  6. Bartel DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215–233
  7. Friedman RC, Forh KKH, Burge CB, Bartel DP. Most mammalian mRNAs are conserved targets for microRNAs. Genome Res. 2009;19:92–105
  8. Lodish HF, Zhou B, Liu G, Chen CZ. Micromanagement of the immune system by microRNAs. Nat Rev Immunol. 2008;8:120–130
  9. Garzon R, Croce CM. MicroRNAs in normal and malignant hematopoiesis. Curr Opin Hematol. 2008;15:352–358
  10. Yendamuri S, Calin GA. The role of microRNA in human leukemia: a review. Leukemia (in press).
  11. Fabbri M, Garzon R, Andreef M, Kantarjian HM, Garcia-Manmero G, Calin GA. MicroRNAs and noncoding RNAs in hematological malignancies: molecular, clinical and therapeutic implications. Leukemia. 2008;22:1095–1105
  12. Bibikova M, Laurent LC, Ren B, Loring JF, Fan JB. Unraveling epigenetic regulation in embryonic stem cells. Cell Stem Cell. 2008;2:123–134
  13. Kim KS, Kim JS, Lee MR, Jeong HS, Kim J. A study of microRNAs in silico and in vivo: emerging regulators of embryonic stem cells. FEBS J. 2009;276:2140–2149
  14. Stadler BM, Ruohola-Baker H. Small RNAs: keeping stem cells in line. Cell. 2008; 132: 563–566.
  15. Murry CE, Keller G. Differentiation of embryonic stem cells to clinically relevant populations: lessons from embryonic development. Cell. 2008;132:661–680
  16. Irion S, Nostro MC, Kattman SJ, Keller GM. Directed differentiation of pluripotent stem cells: from developmental biology to therapeutic applications. Cold Spring Harb Symp Quant Biol (in press).
  17. Suh MR, Lee Y, Kim JY, Moon SH, Lee JY, Che KY, et al. Human embryonic stem cells express a unique set of microRNAs. Dev Biol. 2004;270:488–498
  18. Laurent LC, Chen J, Ulitsky I, Mueller FJ, Lu C, Shamir R, et al. Comprehensive microRNA profiling reveals a unique human embryonic stem cell signature dominated by a single seed sequence. Stem Cells. 2008;26:1506–1516
  19. Wang Y, Keys DN, Au-Young J, Chen C. MicroRNAs in embryonic stem cells. J Cell Physiol. 2009;218:251–255
  20. Gangaraju VK, Liu H. MicroRNAs: key regulators of stem cells. Nat Rev Mol Cell Biol. 2009;10:116–125
  21. Marson A, Levine SS, Cole MF, Frampton GM, Brambrink T, Johnstone S, et al. Connecting microRNA genes to the core transcriptional regulatory circuitry of embryonic stem cells. Cell. 2008;134:521–533
  22. Tay Y, Zhang J, Thomson AM, Lim B, Rigoutsos I. MicroRNAs to Nanog Oct4 and Sox2 coding regions modulate embryonic stem cell differentiation. Nature. 2008;455:1124–1128
  23. Landgraf P, Rusu M, Sheridan R, Sewer A, Iovino N, Aravin A, et al. A mammalian microRNA expression atlas based on small library sequencing. Cell. 2007;129:1401–1414
  24. Georgantas RW, Hildreth R, Morisot S, Alder J, Liu C, Heimfeld S, et al. CD34+ hematopoietic stem/progenitor cell microRNA expression and function: a circuit diagram of differentiation control. Proc Natl Acad Sci USA. 2007;104:2750–2755
  25. O’Connell RM, Rao D, Chaudhuri A, Boldin M, Taganov K, Nicoll J, et al. Sustained expression of microRNA-155 in hematopoietic stem cells causes a myeloproliferative disorder. J Exp Med. 2008;205:585–594
  26. O’Connell RM, Chaudhuri AA, Rao DS, Baltimore D. Inositol phosphatase SHIP1 is a primary target of miR-155. Proc Natl Acad Sci USA. 2009;106:7113–7118
  27. Popovic R, Riesbeck L, Velu C, Chaubey A, Zhang J, Achille N, et al. Regulation of miR-196b by MLL and its overexpression by MLL fusions contributes to immortalization. Blood. 2009;113:3314–3322
  28. Shen WF, Hu YL, Uttarwae L, Passegue E, Largman C. MicroRNA-126 regulates HOXA9 by binding to the homeobox. Mol Cell Biol. 2008;28:4609–4619
  29. Lu J, Guo S, Ebert B, Zhang H, Pao X, Bosco J, et al. MicroRNA-mediated control of cell fate in megakaryocyte-erythrocyte progenitors. Dev Cell. 2008;14:843–853
  30. Liao R, Sun J, Zhang L, Lou G, Chen M, Zhou D, et al. MicroRNAs play a role in the development of human hematopoietic stem cells. J Cell Biochem. 2008;104:805–817
  31. Goff LA, Boucher S, Ricupero CL, Fenstermacher S, Swerdel M, Chase LG, et al. Differentiating human multipotent mesenchymal stromal cells regulate microRNAs: prediction of microRNA regulation by PDGF during osteogenesis. Exp Hematol. 2008;36:1354–1369
  32. Lakshmipathy U, Hart RP. MicroRNA expression in multipotent mesenchymal stromal cells. Stem Cells. 2008;26:356–363
  33. Oskowitz AZ, Lu J, Penfornis P, Ylostalo J, McBride J, Flemington EK, et al. Human multipotent stromal cells from bone marrow and microRNA: regulation of differentiation and leukemia inhibitory factor expression. Proc Natl Acad Sci USA. 2008;105:18372–18377
  34. Akashi K, Traver D, Miyamoto T, Weissman IL. A clonogenic common myeloid progenitor that gives rise to all myeloid lineages. Nature. 2000;404:193–197
  35. Nakorn TN, Miyamoto T, Weissman IL. Characterization of mouse clonogenic megakaryocyte progenitors. Proc Natl Acad Sci USA. 2003;100:205–210
  36. Orkin SH, Zon LI. Hematopoiesis: an evolving paradigm for stem cell biology. Cell. 2008;22:631–644
  37. Garzon R, Pichiorri F, Palumbo T, Iuliano R, Cimmino A, Aqeilan R, et al. MicroRNA fingerprints during human megakaryocytopoiesis. Proc Natl Acad Sci USA. 2006;103:5078–5083
  38. Mukai HY, Motohashi H, Ohmeda O, Suzuki N, Nagano M, Yamamoto M. Transgene nsertion in proximity to thr c-myb gene disrupts erythroid-megakaryocytic lineage bifurcation. Mol Cell Biol. 2006;26:7953–7965
  39. Barroga CF, Pham H, Kaushansky K. Thrombopoietin regulates c-Myb expression by modulating micro RNA 150 expression. Exp Hematol. 2008;36:1585–1592
  40. Xiao C, Calado DP, Galler G, Thai TH, Patterson HC, Wang J, et al. MiR-150 controls B cell differentiation by targeting the transcription factor c-Myb. Cell. 2007;131:146–159
  41. Zhou B, Wang S, Mayr C, Bartel DP. Lodish HF. miR-150, a microRNA expressed in mature B and T cells, blocks early B cell development when expressed prematurely. Proc Natl Acad Sci USA. 2007;104:7080–7085
  42. Ben-Ami O, Pencovich N, Lotem J, Levanon D, Groner Y. A regulatory interplay between miR-27° and Runx1 during megakaryopoiesis. Proc Natl Acad Sci USA. 2009;106:238–243
  43. Romania P, Lulli V, Pelosi E, Biffoni M, Peschle C, Marziali G. MicroRNA155 modulates megakaryopoiesis at progenitor and precursor level by targeting Ets-1 and Meis1 transcription factors. Br J Haematol. 2008;143:570–580
  44. Labbaye C, Spinello I, Quaranta MT, Pelosi E, Pasquini L, Petrucci E, et al. A three-step pathway comprising PLZF/miR-146°/CXCR4 control megakaryopoiesis. Nat Cell Biol. 2008;10:788–801
  45. Bruchova H, Yoon D, Agarwal AM, Mendell J, Prchal JT. Regulated expression of microRNAs in normal and polycythemia vera erythropoiesis. Exp Hematol. 2007;35:1657–1667
  46. Zhan M, Miller CP, Papayannopoulou T, Stamatoyannopoulos G, Song CZ. MicroRNA expression dynamics during murine and human erythroid differentiation. Exp Hematol. 2007;35:1015–1025
  47. Kosaka N, Sugiura K, Yamamoto Y, Yoshioka Y, Miyazaki H, Komatsu N, et al. Identification of erythropoietin-induced microRNAs in hematopoietic cells during erythroid differentiation. Br J Haematol. 2008;142:293–300
  48. Choong ML, Yang HH, McNiece I. MicroRNA expression profiling during human cord blood-derived CD34 vcell erythropoiesis. Exp Hematol. 2007;35:551–564
  49. Felli N, Fontana L, Pelosi E, Botta R, Bonci D, Facchiano F, et al. MicroRNAs 221 and 222 inhibit normal erythropoiesis and erythropoiesis and erythroleukemic cell growth via kit receptor down modulation. Proc Natl Acad Sci USA. 2005;102:18081–18086
  50. Spinello I, Quaranta MT, Pasquini L, Pelosi E, Petrucci E, Pagliuca A, Castelli G, Mariani G, Diverio D, Foà R, Testa U, Labbaye C. PLZF-mediated control on c-kit expression in CD34+ cells and early erythropoiesis. Oncogene (in press).
  51. Dore L, Amigo JD, Dos Santos CO, Zhang Z, Gai X, Tobias JW, et al. A GATA-1 regulated miRNA locus essential for erythropoiesis. Proc Natl Acad Sci USA. 2008;105:3333–3338
  52. Pase L, Layton JE, Kloosterman WP, Carradice D, Waterhouse PM, Lieschke GJ. Mit-451 regulates zebrafish erythroid maturation in vivo via its target gata2. Blood. 2009;113:1794–1804
  53. Fu YF, Du TT, Dong M, Zhu KY, Jing CB, Zhang Y, et al. Mir-144 selectively regulates embryonic α-hemoglobin synthesis during primitive erythropoiesis. Blood. 2009;113:1340–1349
  54. Wang Q, Huang Z, Xue H, Jin C, Ju XL, Han JD, Chen YG. MicroRNA miR-24 inhibits erythropoiesis by targeting activin type receptor ALK4. Blood 111: 588–595.
  55. Zhao H, Kalota A, Jin S, Gewirtz AM. The c-myb proto-oncogene and microRNA-15a comprise an active autoregulatory feedback loop in human hematopoietic cells. Blood. 2009;113:505–516
  56. 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
  57. Nervi C, Fazi F, Rosa A, Fatica A, Bozzoni I. Emerging role for microRNAs in acute promyelocyic leukemia. Curr Top Microbiol Immunol. 2007;313:73–84
  58. Garzon R, Pichioirri F, Palumbo T, Visentini M, Aqeilan R, Cimmino A, Wang H, Sun H, Volinia S, Alder H, Calin GA, Liu CG, Andreef M, Croce CM. MicroRNA gene expression during retinoic acid-induced differentiation of human acute promyelocytic leukemia. Oncogene 26: 4148–4157.
  59. Fukuda Y, Kiga K, Shaarif J, Hino K, Enomoto Y, Kawamura A, et al. An evolutionary conserved mechanism for microRNA-223 expression revealed by microRNA gene profiling. Cell. 2007;129:617–631
  60. 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
  61. Stehling-Sun S, Dade J, Nutt SL, De Koter R, Camargo FD. Regulation of lymphoid versus myeloid fate “choice” by the transcription factor Mef2C. Nature Immunol. 2009;10:289–296
  62. Velu CS, Baktula AM, Grimes HL. Gfi1 regulates miR-21 and miR-196b to control myelopoiesis. Blood. 2009;113:4720–4728
  63. Feng J, Iwama A, Masanobu S, Kohu K. MicroRNA-27 enhances differentiation of myeloblasts into granulocytes by post-transcriptionally downregulating Runx1. Brit J Haematol 145: 412–423.
  64. Fontana L, Pelosi E, Greco P, Racanicchi S, Testa U, Liuzzi F, et al. MicroRNAs 17-5p-20°-106° control monocytopoiesis through AML1 targeting and M-CSF receptor upregulation. Nat Cell Biol. 2007;9:775–786
  65. Rosa A, Ballarino M, Sorrentino A, Sthandier O, De Angelis FG, Marchioni M, et al. The interplay between the master transcription factor PU.1 and miR-424 regulates human monocyte/macrophage differentiation.. Proc Natl Acad Sci USA. 2007;104:19849–19854
  66. Fujita S, Ito T, Mizutani T, Minogouchi S, Yamamichi N, Sakuraiu K, et al. miR-21 expression triggered by AP-1 is sustained through a double-negative feedback mechanism. J Mol Biol. 2008;278:429–504
  67. O’ Connell RM, Taganov KD, Boldin MP, Cheng G, Baltimore D. MicroRNA-155 is induced durino the macrophage inflammatory response. Proc Natl Acad Sci USA. 2007;104:1604–1609
  68. Ceppi M, Pereira PM, Dunand-Sauthier I, Barras E, Reith W, Santos MA, et al. MicroRNA-155 modulates the interleukin-1 signaling pathway in activated human monocyte-derived dendritic cells. Proc Natl Acad Sci USA. 2009;106:2735–2740
  69. Taganov KD, Boldin MP, Chang KJ, Baltimor D. NF-kappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signalling proteins of innate immune responses. Proc Natl Acad Sci USA. 2006;103:12481–12486
  70. Bazzoni F, Rossato M, Fabbri M, Gaudiosi D, Mirolo M, Mori L, et al. Induction and regulatory function of miR-9 in human monocytes and neutrophils exposed to proinflammatory signals. Proc Natl Acad Sci USA. 2009;106:5282–5287
  71. Croce CM. Oncogenes and cancer. N Engl J Med. 2008;358:502–511
  72. Venturini L, Battmer K, Castoldi M, Schultheis B, Hochhaus A, Machenthaler MU. Expression of the miR-17-92 polycistron in chronic myeloid leukemia (CML) CD34+ cells. Blood. 2007;109:4399–4405
  73. Bueno MJ, Perez de Castro I, Gomez de Cédron M, Santos J, Calin GA, Cigudosa JC, et al. Genetic and epigenetic silencing of microRNA-203 enhances ABL1 and BCR-ABL1 oncogene expression. Cancer Cell. 2008;13:496–506
  74. Agirre K, Jimenez-Velasco A, San José-Enériz E, Garate L, Bandrés E, Cordeu L, et al. Down-regulation of has-miR-10a in chronic myeloid leukemia CD34+ cells increases USF2-mediated cell growth. Mol Cancer Res. 2008;6:1830–1840
  75. Scholl S, Fricke HJ, Sayer HG, Hoffken K. Clinical implications of molecular genetic aberrations in acute myeloid leukemia. J Cancer Res Clin Oncol. 2009;135:491–505
  76. Baldus CD, Bullinger L. Gene expression with prognostic implications in cytogenetically normal acute myeloid leucemia. Semin Oncol. 2008;35:356–364
  77. Garzon R, Volinia S, Liu CG, Fernandez-Cymering C, Palumbo T, Pichiorri F. MicroRNA signatures associated with cytogenetics and prognosis in acute myeloid leukemia. Blood. 2008;111:3183–3189
  78. Garzon R, Garofalo M, Martelli MP, Briesewitz R, Wang L, Fernandez-Cyemering C, et al. Distinctive microRNA signature of acute myeloid leukemia bearing cytoplasmic mutated nucleophosmin. Proc Natl Acad Sci USA. 2008;105:3945–3950
  79. Jongen-Lavrencic M, Sun SM, Dijkstra MK, Valk P, Lowenberg B. MicroRNA expression profiling in relation to the genetic heterogeneity of acute myeloid leukemia. Blood. 2008;111:5078–5085
  80. Li Z, Luo RT, Mi S, Sun M, Chen P, Bao J, et al. Consistent deregulation of gene expression between human and murine rearrangement leukemias. Cancer Res. 2009;69:1109–1116
  81. Marcucci G, Maharry K, Rodmacher M, Mrozek K, Vukisavljeic T, Paschka P, et al. Prognostic significance of, and gene and microRNA expression signatures associated with CEBPA mutations in cytogenetically normal acute myeloid leukemia with high risk molecular features: a cancer and leukemia group B study. J Clin Oncol. 2008;26:5078–5086
  82. Hackanson B, Bennet K, Brena R, Jiang J, Claus R, Chen SS, et al. Epigenetic modification of CCAAT/Enhancer binding protein alpha expression in acute myeloid leukemia. Cancer Res. 2008;68:3142–3151
  83. Isken F, Steffen B, Merk S, Dugas M, Markus B, Tidow N, et al. Identification of acute myeloid leukemia associated microRNA expression patterns. Br J Haematol. 2008;140:153–161
  84. DeBernardis S, Skoulakis S, Molloy G, Chaplin T, Dixon MI, Young BD. MicroRNA miR-181a correlates with morphological sub-class of acute myeloid leukemia and the expression of its target genes in global genome-wide analysis. Leukemia. 2007;21:912–916
  85. Li Z, Lu J, Sun M, Mi S, Zhang H, Luo R, et al. Distinct microRNA expression profiles in acute myeloid leukemia with common translocations. Proc Natl Acad Sci USA. 2008;105:15535–15540
  86. Saumet A, Vetter G, Bouttier M, Portales-Casamar E, Wasserman W, Mourin T, et al. Transcriptional repression of microRNA genes by PML-RARA increases expression of key cancer proteins in acute promyelocytic leukemia. Blood. 2009;113:412–421
  87. De Marchis ML, Ballarino M, Salvatori B, Puzzolo MC, Bozzoni I, Fatica A. A new molecular network comprising PU.1, interferon regularoty factor proteins and miR-342 stimulates ATRA-mediated granulocytic differentiation of acute promyelocytic leukemia cells. Leukemia. 2009;23:856–862
  88. Careccia S, Mainardi S, Pelosi A, Gurtner A, Diverio D, Riccioni R, Testa U, Pelosi E, Sacchi A, Lavorgna S, Lo-Coco F, Blandino G, Levrero M, Rizzo MG. A restricted signature of miRNAs distinguishes APL blasts from normal promyelocytes. Oncogene (in press).
  89. Garzon R, Liu S, Fabbri M, Liu Z, Heaphy C, Callegari E, Schwind S, Pang J, Yu J, Mthusamy N, Havelange V, Volinia S, Blum W, Rush L, Perrotti D, Andreef M, Bloomfield C, Byrd J, Chan K, Wu LC, Croce CM, Marcucci G. Micro-RNA29b induces global DNA hypomethylation and tumor suppressor gene re-expression in acute myeloid leukemia by targeting directly DNMT3A and 3B and indirectly DNMT1. Blood (in press).
  90. Shankar DB, Cheng JC, Kinjo K. The role of CREB as proto-oncogene in hematopoiesis and in acute myeloid leukaemia. Cancer Cell. 2005;7:351–362
  91. Pigozzi M, Manara E, Baron E, Basso G. miR-34b targets cyclic AMP-responsive element binding protein in acute myeloid leukaemia. Cancer Res. 2009;69:2471–2478
  92. Bousquet M, Quelen C, Rosati R, Mansat-De Mas V, La Starza R, Dastugue N, et al. Myeloid cell differentiation arrest by miR-125b-1 in myelodysplasic syndrome and acute myeloid leukemia with the t(2;11)(p21;q23) translocation. J Exp Med. 2008;205:2499–2506

PII: S0145-2126(09)00247-1

doi: 10.1016/j.leukres.2009.04.039

Leukemia Research
Volume 33, Issue 12 , Pages 1584-1593 , December 2009