MiR-24 Is Required for Hematopoietic Differentiation of Mouse Embryonic Stem Cells

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Studies of mouse embryos and embryonic stem cells (ESCs) have defined the ontogeny of mammalian embryonic hematopoietic cells. The ESC differentiation system has been valuable for dissecting the molecular regulation of the development of mesoderm into HPCs. Extracellular signals regulate a complex network of transcription factors to direct embryonic hematopoietic development. Mammalian miRNAs have previously not been described to regulate this genetic network during embryonic hematopoiesis. However, a role for miRNAs in producing the hemangioblast, and hemogenic endothelium in Xenopus has been described. Our work with ESCs demonstrates a specific requirement for the miRNA, miR-24, in the development of hematopoietic progenitors cells (HPCs). Antagonizing miR-24 in ESCs does not affect generation of BL-CFCs, the in vitro equivalent of the hemangioblast, but does compromise the ability of those BL-CFCs to produced HPCs. Expression of transcription factors required for HPC production downstream of the hemangioblast, Scl, and Runx1, is greatly reduced by antagonizing miR-24. These results identify miR-24, as a mammalian miRNA required for the development of blood from newly formed mesoderm.

Vyšlo v časopise: MiR-24 Is Required for Hematopoietic Differentiation of Mouse Embryonic Stem Cells. PLoS Genet 11(1): e32767. doi:10.1371/journal.pgen.1004959
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1004959

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Zdroje

1. Bushati N, Cohen SM (2007) microRNA Functions. Annu Rev Cell Dev Biol 23: 175–205. doi: 10.1146/annurev.cellbio.23.090506.123406 17506695

2. Havelange V, Garzon R (2010) MicroRNAs: emerging key regulators of hematopoiesis. Am J Hematol 85: 935–942. doi: 10.1002/ajh.21863 20941782

3. Kong KY, Owens KS, Rogers JH, Mullenix J, Velu CS, et al. (2010) MIR-23A microRNA cluster inhibits B-cell development. Exp Hematol 38: 629–640 e621. doi: 10.1016/j.exphem.2010.04.004 20399246

4. Taganov KD, Boldin MP, Baltimore D (2007) MicroRNAs and immunity: tiny players in a big field. Immunity 26: 133–137. doi: 10.1016/j.immuni.2007.02.005 17307699

5. Lancrin C, Sroczynska P, Stephenson C, Allen T, Kouskoff V, et al. (2009) The haemangioblast generates haematopoietic cells through a haemogenic endothelium stage. Nature 457: 892–895. doi: 10.1038/nature07679 19182774

6. Hirschi KK (2012) Hemogenic endothelium during development and beyond. Blood 119: 4823–4827. doi: 10.1182/blood-2011-12-353466 22415753

7. Medvinsky A, Rybtsov S, Taoudi S (2011) Embryonic origin of the adult hematopoietic system: advances and questions. Development 138: 1017–1031. doi: 10.1242/dev.040998 21343360

8. Sabin FR (1920) Studies on the origin of blood vessels and of red corpuscules as seen in the living blastoderm of the chick during the second day of incubation: contributions to embryology. Contrib Embryol 9: 213–262.

9. Murray PDF (1932) The development in vitro of the blood of the early chick embryo. Proc R Soc Lond 11: 497–521. doi: 10.1098/rspb.1932.0070

10. Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125: 725–732. 9435292

11. Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, et al. (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130: 4217–4227. doi: 10.1242/dev.00589 12874139

12. Huber TL, Kouskoff V, Fehling HJ, Palis J, Keller G (2004) Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432: 625–630. doi: 10.1038/nature03122 15577911

13. Jaffredo T, Gautier R, Eichmann A, Dieterlen-Lievre F (1998) Intraaortic hemopoietic cells are derived from endothelial cells during ontogeny. Development 125: 4575–4583. 9778515

14. Nishikawa SI, Nishikawa S, Kawamoto H, Yoshida H, Kizumoto M, et al. (1998) In vitro generation of lymphohematopoietic cells from endothelial cells purified from murine embryos. Immunity 8: 761–769. doi: 10.1016/S1074-7613(00)80581-6 9655490

15. Soderberg SS, Karlsson G, Karlsson S (2009) Complex and context dependent regulation of hematopoiesis by TGF-beta superfamily signaling. Ann N Y Acad Sci 1176: 55–69. doi: 10.1111/j.1749-6632.2009.04569.x 19796233

16. Moroni E, Dell′Era P, Rusnati M, Presta M (2002) Fibroblast growth factors and their receptors in hematopoiesis and hematological tumors. J Hematother Stem Cell Res 11: 19–32. doi: 10.1089/152581602753448513 11847001

17. Baron MH (2003) Embryonic origins of mammalian hematopoiesis. Exp Hematol 31: 1160–1169. doi: 10.1016/j.exphem.2003.08.019 14662321

18. Bigas A, Robert-Moreno A, Espinosa L (2010) The Notch pathway in the developing hematopoietic system. Int J Dev Biol 54: 1175–1188. doi: 10.1387/ijdb.093049ab 20711994

19. Liu F, Patient R (2008) Genome-wide analysis of the zebrafish ETS family identifies three genes required for hemangioblast differentiation or angiogenesis. Circ Res 103: 1147–1154. doi: 10.1161/CIRCRESAHA.108.179713 18832752

20. Sumanas S, Gomez G, Zhao Y, Park C, Choi K, et al. (2008) Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111: 4500–4510. doi: 10.1182/blood-2007-09-110569 18270322

21. Lee D, Park C, Lee H, Lugus JJ, Kim SH, et al. (2008) ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2: 497–507. doi: 10.1016/j.stem.2008.03.008 18462699

22. Wareing S, Eliades A, Lacaud G, Kouskoff V (2012) ETV2 expression marks blood and endothelium precursors, including hemogenic endothelium, at the onset of blood development. Dev Dyn 241: 1454–1464. doi: 10.1002/dvdy.23825 22733530

23. Wareing S, Mazan A, Pearson S, Gottgens B, Lacaud G, et al. (2012) The Flk1-Cre-mediated deletion of ETV2 defines its narrow temporal requirement during embryonic hematopoietic development. Stem Cells 30: 1521–1531. doi: 10.1002/stem.1115 22570122

24. D′Souza SL, Elefanty AG, Keller G (2005) SCL/Tal-1 is essential for hematopoietic commitment of the hemangioblast but not for its development. Blood 105: 3862–3870. doi: 10.1182/blood-2004-09-3611 15677567

25. Lacaud G, Gore L, Kennedy M, Kouskoff V, Kingsley P, et al. (2002) Runx1 is essential for hematopoietic commitment at the hemangioblast stage of development in vitro. Blood 100: 458–466. doi: 10.1182/blood-2001-12-0321 12091336

26. Beck D, Thoms JA, Perera D, Schutte J, Unnikrishnan A, et al. (2013) Genome-wide analysis of transcriptional regulators in human HSPCs reveals a densely interconnected network of coding and noncoding genes. Blood 122: e12–22. doi: 10.1182/blood-2013-03-490425 23974199

27. Ben-Ami O, Pencovich N, Lotem J, Levanon D, Groner Y (2009) A regulatory interplay between miR-27a and Runx1 during megakaryopoiesis. Proc Natl Acad Sci U S A 106: 238–243. doi: 10.1073/pnas.0811466106 19114653

28. Mansour MR, Sanda T, Lawton LN, Li X, Kreslavsky T, et al. (2013) The TAL1 complex targets the FBXW7 tumor suppressor by activating miR-223 in human T cell acute lymphoblastic leukemia. J Exp Med 210: 1545–1557. doi: 10.1084/jem.20122516 23857984

29. Wang Q, Huang Z, Xue H, Jin C, Ju XL, et al. (2007) MicroRNA miR-24 inhibits erythropoiesis by targeting activin type I receptor ALK4. Blood.

30. Nimmo R, Ciau-Uitz A, Ruiz-Herguido C, Soneji S, Bigas A, et al. (2013) MiR-142-3p controls the specification of definitive hemangioblasts during ontogeny. Dev Cell 26: 237–249. doi: 10.1016/j.devcel.2013.06.023 23911199

31. Chan MC, Hilyard AC, Wu C, Davis BN, Hill NS, et al. (2010) Molecular basis for antagonism between PDGF and the TGFbeta family of signalling pathways by control of miR-24 expression. EMBO J 29: 559–573. doi: 10.1038/emboj.2009.370 20019669

32. Chan MC, Nguyen PH, Davis BN, Ohoka N, Hayashi H, et al. (2007) A novel regulatory mechanism of the bone morphogenetic protein (BMP) signaling pathway involving the carboxyl-terminal tail domain of BMP type II receptor. Mol Cell Biol 27: 5776–5789. doi: 10.1128/MCB.00218-07 17576816

33. Cook BD, Liu S, Evans T (2011) Smad1 signaling restricts hematopoietic potential after promoting hemangioblast commitment. Blood 117: 6489–6497. doi: 10.1182/blood-2010-10-312389 21515822

34. Liu B, Sun Y, Jiang F, Zhang S, Wu Y, et al. (2003) Disruption of Smad5 gene leads to enhanced proliferation of high-proliferative potential precursors during embryonic hematopoiesis. Blood 101: 124–133. doi: 10.1182/blood-2002-02-0398 12393578

35. McReynolds LJ, Gupta S, Figueroa ME, Mullins MC, Evans T (2007) Smad1 and Smad5 differentially regulate embryonic hematopoiesis. Blood 110: 3881–3890. doi: 10.1182/blood-2007-04-085753 17761518

36. Zafonte BT, Liu S, Lynch-Kattman M, Torregroza I, Benvenuto L, et al. (2007) Smad1 expands the hemangioblast population within a limited developmental window. Blood 109: 516–523. doi: 10.1182/blood-2006-02-004564 16990609

37. Dahl R, Walsh JC, Lancki D, Laslo P, Iyer SR, et al. (2003) Regulation of macrophage and neutrophil cell fates by the PU.1:C/EBPalpha ratio and granulocyte colony-stimulating factor. Nat Immunol 4: 1029–1036. doi: 10.1038/ni973 12958595

38. Mikkola HK, Fujiwara Y, Schlaeger TM, Traver D, Orkin SH (2003) Expression of CD41 marks the initiation of definitive hematopoiesis in the mouse embryo. Blood 101: 508–516. doi: 10.1182/blood-2002-06-1699 12393529

39. Sakurai H, Era T, Jakt LM, Okada M, Nakai S, et al. (2006) In vitro modeling of paraxial and lateral mesoderm differentiation reveals early reversibility. Stem Cells 24: 575–586. doi: 10.1634/stemcells.2005-0256 16339996

40. Takakura N, Yoshida H, Ogura Y, Kataoka H, Nishikawa S, et al. (1997) PDGFR alpha expression during mouse embryogenesis: immunolocalization analyzed by whole-mount immunohistostaining using the monoclonal anti-mouse PDGFR alpha antibody APA5. The journal of histochemistry and cytochemistry: official journal of the Histochemistry Society 45: 883–893. doi: 10.1177/002215549704500613

41. Feraud O, Cao Y, Vittet D (2001) Embryonic stem cell-derived embryoid bodies development in collagen gels recapitulates sprouting angiogenesis. Lab Invest 81: 1669–1681. doi: 10.1038/labinvest.3780380 11742037

42. Faloon P, Arentson E, Kazarov A, Deng CX, Porcher C, et al. (2000) Basic fibroblast growth factor positively regulates hematopoietic development. Development 127: 1931–1941. 10751181

43. Robertson SM, Kennedy M, Shannon JM, Keller G (2000) A transitional stage in the commitment of mesoderm to hematopoiesis requiring the transcription factor SCL/tal-1. Development 127: 2447–2459. 10804185

44. Ismailoglu I, Yeamans G, Daley GQ, Perlingeiro RC, Kyba M (2008) Mesodermal patterning activity of SCL. Exp Hematol 36: 1593–1603. doi: 10.1016/j.exphem.2008.07.005 18809240

45. Van Handel B, Montel-Hagen A, Sasidharan R, Nakano H, Ferrari R, et al. (2012) Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 150: 590–605. doi: 10.1016/j.cell.2012.06.026 22863011

46. Du K, Herzig S, Kulkarni RN, Montminy M (2003) TRB3: a tribbles homolog that inhibits Akt/PKB activation by insulin in liver. Science 300: 1574–1577. doi: 10.1126/science.1079817 12791994

47. Liu L, Zhu S, Gong Z, Low BC (2008) K-ras/PI3K-Akt signaling is essential for zebrafish hematopoiesis and angiogenesis. PLoS One 3: e2850. doi: 10.1371/journal.pone.0002850 18682746

48. Okita K, Ichisaka T, Yamanaka S (2007) Generation of germline-competent induced pluripotent stem cells. Nature 448: 313–317. doi: 10.1038/nature05934 17554338

49. Meissner A, Wernig M, Jaenisch R (2007) Direct reprogramming of genetically unmodified fibroblasts into pluripotent stem cells. Nat Biotechnol 25: 1177–1181. doi: 10.1038/nbt1335 17724450

50. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126: 663–676. doi: 10.1016/j.cell.2006.07.024 16904174

51. Pereira TC, Lopes-Cendes I (2012) Emerging RNA-based drugs: siRNAs, microRNAs and derivates. Central nervous system agents in medicinal chemistry 12: 217–232. doi: 10.2174/187152412802430138 22697266