MicroRNA-153 Regulates the Acquisition of Gliogenic Competence by Neural Stem Cells

Stem Cell Reports

Volumn 5, Issue 3, 2015, Pages 365-377

  Tsuyama, Jun ^a   Bunt, Jens ^b   Richards, Linda J ^b   Iwanari, Hiroko ^c   Mochizuki, Yasuhiro ^c   Hamakubo, Takao ^c   Shimazaki, Takuya ^a   Okano, Hideyuki ^a  

^a KEIO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MICRORNA; MICRORNA 153; NUCLEAR FACTOR I; NUCLEAR FACTOR IA; NUCLEAR FACTOR IB; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG; MIRN153 MICRORNA, MOUSE; NFIA PROTEIN, MOUSE; NFIB PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BINDING SITE; CELL MIGRATION; CONTROLLED STUDY; EMBRYO; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; GENE OVEREXPRESSION; GENE TARGETING; GENETIC TRANSFORMATION; GLIA CELL; GLIOGENESIS; GLIOGENIC COMPETENCE; IMMUNOCYTOCHEMISTRY; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; IN VITRO STUDY; MOUSE; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPORTER GENE; ANIMAL; BRAIN CORTEX; CELL DIFFERENTIATION; CYTOLOGY; GENETICS; GLIA; METABOLISM; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; CEREBRAL CORTEX; MICE; MICRORNAS; NEURAL STEM CELLS; NEUROGLIA; NFI TRANSCRIPTION FACTORS;

EID: 84941170340     PISSN: 22136711     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.stemcr.2015.06.006     Document Type: Article

References (65)

1. A. Alvarez-Buylla, M. Kohwi, T.M. Nguyen, and F.T. Merkle The heterogeneity of adult neural stem cells and the emerging complexity of their niche Cold Spring Harb. Symp. Quant. Biol. 73 2008 357 365
2. E. Balzer, C. Heine, Q. Jiang, V.M. Lee, and E.G. Moss LIN28 alters cell fate succession and acts independently of the let-7 microRNA during neurogliogenesis in vitro Development 137 2010 891 900
3. F. Barnabé-Heider, J.A. Wasylnka, K.J. Fernandes, C. Porsche, M. Sendtner, D.R. Kaplan, and F.D. Miller Evidence that embryonic neurons regulate the onset of cortical gliogenesis via cardiotrophin-1 Neuron 48 2005 253 265
4. G. Barry, M. Piper, C. Lindwall, R. Moldrich, S. Mason, E. Little, A. Sarkar, S. Tole, R.M. Gronostajski, and L.J. Richards Specific glial populations regulate hippocampal morphogenesis J. Neurosci. 28 2008 12328 12340
5. D.P. Bartel MicroRNAs: Genomics, biogenesis, mechanism, and function Cell 116 2004 281 297
6. D.P. Bartel MicroRNAs: Target recognition and regulatory functions Cell 136 2009 215 233
7. J.D. Cahoy, B. Emery, A. Kaushal, L.C. Foo, J.L. Zamanian, K.S. Christopherson, Y. Xing, J.L. Lubischer, P.A. Krieg, S.A. Krupenko, and et al. A transcriptome database for astrocytes, neurons, and oligodendrocytes: A new resource for understanding brain development and function J. Neurosci. 28 2008 264 278
8. S.W. Chi, J.B. Zang, A. Mele, and R.B. Darnell Argonaute HITS-CLIP decodes microRNA-mRNA interaction maps Nature 460 2009 479 486
9. F. Cimadamore, A. Amador-Arjona, C. Chen, C.T. Huang, and A.V. Terskikh SOX2-LIN28/let-7 pathway regulates proliferation and neurogenesis in neural precursors Proc. Natl. Acad. Sci. USA 110 2013 E3017 E3026
10. L. das Neves, C.S. Duchala, F. Tolentino-Silva, M.A. Haxhiu, C. Colmenares, W.B. Macklin, C.E. Campbell, K.G. Butz, and R.M. Gronostajski Disruption of the murine nuclear factor I-A gene (Nfia) results in perinatal lethality, hydrocephalus, and agenesis of the corpus callosum Proc. Natl. Acad. Sci. USA 96 1999 11946 11951
11. B. Deneen, R. Ho, A. Lukaszewicz, C.J. Hochstim, R.M. Gronostajski, and D.J. Anderson The transcription factor NFIA controls the onset of gliogenesis in the developing spinal cord Neuron 52 2006 953 968
12. E. Doxakis Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153 J. Biol. Chem. 285 2010 12726 12734
13. J.C. Dugas, T.L. Cuellar, A. Scholze, B. Ason, A. Ibrahim, B. Emery, J.L. Zamanian, L.C. Foo, M.T. McManus, and B.A. Barres Dicer1 and miR-219 Are required for normal oligodendrocyte differentiation and myelination Neuron 65 2010 597 611
14. M.S. Ebert, and P.A. Sharp Roles for microRNAs in conferring robustness to biological processes Cell 149 2012 515 524
15. C. Englund, A. Fink, C. Lau, D. Pham, R.A.M. Daza, A. Bulfone, T. Kowalczyk, and R.F. Hevner Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex J. Neurosci. 25 2005 247 251
16. R.C. Friedman, K.K. Farh, C.B. Burge, and D.P. Bartel Most mammalian mRNAs are conserved targets of microRNAs Genome Res. 19 2009 92 105
17. W. Ge, K. Martinowich, X. Wu, F. He, A. Miyamoto, G. Fan, G. Weinmaster, and Y.E. Sun Notch signaling promotes astrogliogenesis via direct CSL-mediated glial gene activation J. Neurosci. Res. 69 2002 848 860
18. L. Grandbarbe, J. Bouissac, M. Rand, M. Hrabé de Angelis, S. Artavanis-Tsakonas, and E. Mohier Delta-Notch signaling controls the generation of neurons/glia from neural stem cells in a stepwise process Development 130 2003 1391 1402
19. R.E. Gross, M.F. Mehler, P.C. Mabie, Z. Zang, L. Santschi, and J.A. Kessler Bone morphogenetic proteins promote astroglial lineage commitment by mammalian subventricular zone progenitor cells Neuron 17 1996 595 606
20. H. Guo, N.T. Ingolia, J.S. Weissman, and D.P. Bartel Mammalian microRNAs predominantly act to decrease target mRNA levels Nature 466 2010 835 840
21. T. Haraguchi, H. Nakano, T. Tagawa, T. Ohki, Y. Ueno, T. Yoshida, and H. Iba A potent 2′-O-methylated RNA-based microRNA inhibitor with unique secondary structures Nucleic Acids Res. 40 2012 e58
22. S.V. Hegarty, G.W. O'Keeffe, and A.M. Sullivan BMP-Smad 1/5/8 signalling in the development of the nervous system Prog. Neurobiol. 109 2013 28 41
23. Y. Hirabayashi, N. Suzki, M. Tsuboi, T.A. Endo, T. Toyoda, J. Shinga, H. Koseki, M. Vidal, and Y. Gotoh Polycomb limits the neurogenic competence of neural precursor cells to promote astrogenic fate transition Neuron 63 2009 600 613
24. L.I. Hudish, A.J. Blasky, and B. Appel miR-219 regulates neural precursor differentiation by direct inhibition of apical par polarity proteins Dev. Cell 27 2013 387 398
25. E. Huntzinger, and E. Izaurralde Gene silencing by microRNAs: Contributions of translational repression and mRNA decay Nat. Rev. Genet. 12 2011 99 110
26. P. Kang, H.K. Lee, S.M. Glasgow, M. Finley, T. Donti, Z.B. Gaber, B.H. Graham, A.E. Foster, B.G. Novitch, R.M. Gronostajski, and B. Deneen Sox9 and NFIA coordinate a transcriptional regulatory cascade during the initiation of gliogenesis Neuron 74 2012 79 94
27. A. Kawaguchi, T. Miyata, K. Sawamoto, N. Takashita, A. Murayama, W. Akamatsu, M. Ogawa, M. Okabe, Y. Tano, S.A. Goldman, and H. Okano Nestin-EGFP transgenic mice: Visualization of the self-renewal and multipotency of CNS stem cells Mol. Cell. Neurosci. 17 2001 259 273
28. H. Kawahara, T. Imai, and H. Okano MicroRNAs in Neural Stem Cells and Neurogenesis Front. Neurosci. 6 2012 30
29. Y. Kishi, Y. Fujii, Y. Hirabayashi, and Y. Gotoh HMGA regulates the global chromatin state and neurogenic potential in neocortical precursor cells Nat. Neurosci. 15 2012 1127 1133
30. S.A. Koblar, A.M. Turnley, B.J. Classon, K.L. Reid, C.B. Ware, S.S. Cheema, M. Murphy, and P.F. Bartlett Neural precursor differentiation into astrocytes requires signaling through the leukemia inhibitory factor receptor Proc. Natl. Acad. Sci. USA 95 1998 3178 3181
31. X.K. Li, and P. Jin Roles of small regulatory RNAs in determining neuronal identity Nat. Rev. Neurosci. 11 2010 329
32. W. Li, C.A. Cogswell, and J.J. LoTurco Neuronal differentiation of precursors in the neocortical ventricular zone is triggered by BMP J. Neurosci. 18 1998 8853 8862
33. C. Liang, H. Zhu, Y. Xu, L. Huang, C. Ma, W. Deng, Y. Liu, and C. Qin MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2 Brain Res. 1455 2012 103 113
34. F.D. Miller, and A.S. Gauthier Timing is everything: Making neurons versus glia in the developing cortex Neuron 54 2007 357 369
35. K. Miura, Y. Okada, T. Aoi, A. Okada, K. Takahashi, K. Okita, M. Nakagawa, M. Koyanagi, K. Tanabe, M. Ohnuki, and et al. Variation in the safety of induced pluripotent stem cell lines Nat. Biotechnol. 27 2009 743 745
36. H. Naka, S. Nakamura, T. Shimazaki, and H. Okano Requirement for COUP-TFI and II in the temporal specification of neural stem cells in CNS development Nat. Neurosci. 11 2008 1014 1023
37. H. Naka-Kaneda, S. Nakamura, M. Igarashi, H. Aoi, H. Kanki, J. Tsuyama, S. Tsutsumi, H. Aburatani, T. Shimazaki, and H. Okano The miR-17/106-p38 axis is a key regulator of the neurogenic-to-gliogenic transition in developing neural stem/progenitor cells Proc. Natl. Acad. Sci. USA 111 2014 1604 1609
38. K. Nakashima, S. Wiese, M. Yanagisawa, H. Arakawa, N. Kimura, T. Hisatsune, K. Yoshida, T. Kishimoto, M. Sendtner, and T. Taga Developmental requirement of gp130 signaling in neuronal survival and astrocyte differentiation J. Neurosci. 19 1999 5429 5434
39. K. Nakashima, T. Takizawa, W. Ochiai, M. Yanagisawa, T. Hisatsune, M. Nakafuku, K. Miyazono, T. Kishimoto, R. Kageyama, and T. Taga BMP2-mediated alteration in the developmental pathway of fetal mouse brain cells from neurogenesis to astrocytogenesis Proc. Natl. Acad. Sci. USA 98 2001 5868 5873
40. M. Namihira, J. Kohyama, K. Semi, T. Sanosaka, B. Deneen, T. Taga, and K. Nakashima Committed neuronal precursors confer astrocytic potential on residual neural precursor cells Dev. Cell 16 2009 245 255
41. W.H. Neo, K. Yap, S.H. Lee, L.S. Looi, P. Khandelia, S.X. Neo, E.V. Makeyev, and I.H. Su MicroRNA miR-124 controls the choice between neuronal and astrocyte differentiation by fine-tuning Ezh2 expression J. Biol. Chem. 289 2014 20788 20801
42. Y. Okada, T. Shimazaki, G. Sobue, and H. Okano Retinoic-acid-concentration-dependent acquisition of neural cell identity during in vitro differentiation of mouse embryonic stem cells Dev. Biol. 275 2004 124 142
43. Y. Okada, A. Matsumoto, T. Shimazaki, R. Enoki, A. Koizumi, S. Ishii, Y. Itoyama, G. Sobue, and H. Okano Spatiotemporal recapitulation of central nervous system development by murine embryonic stem cell-derived neural stem/progenitor cells Stem Cells 26 2008 3086 3098
44. H. Okano, and S. Temple Cell types to order: Temporal specification of CNS stem cells Curr. Opin. Neurobiol. 19 2009 112 119
45. T. Papagiannakopoulos, and K.S. Kosik MicroRNA-124: Micromanager of neurogenesis Cell Stem Cell 4 2009 375 376
46. J.D. Pereira, S.N. Sansom, J. Smith, M.W. Dobenecker, A. Tarakhovsky, and F.J. Livesey Ezh2, the histone methyltransferase of PRC2, regulates the balance between self-renewal and differentiation in the cerebral cortex Proc. Natl. Acad. Sci. USA 107 2010 15957 15962
47. M. Piper, G. Barry, J. Hawkins, S. Mason, C. Lindwall, E. Little, A. Sarkar, A.G. Smith, R.X. Moldrich, G.M. Boyle, and et al. NFIA controls telencephalic progenitor cell differentiation through repression of the Notch effector Hes1 J. Neurosci. 30 2010 9127 9139
48. M. Piper, G. Barry, T.J. Harvey, R. McLeay, A.G. Smith, L. Harris, S. Mason, B.W. Stringer, B.W. Day, N.R. Wray, and et al. NFIB-mediated repression of the epigenetic factor Ezh2 regulates cortical development J. Neurosci. 34 2014 2921 2930
49. C. Plachez, K. Cato, R.C. McLeay, Y.H. Heng, T.L. Bailey, R.M. Gronostajski, L.J. Richards, A.C. Puche, and M. Piper Expression of nuclear factor one A and -B in the olfactory bulb J. Comp. Neurol. 520 2012 3135 3149
50. I.A. Qureshi, and M.F. Mehler Emerging roles of non-coding RNAs in brain evolution, development, plasticity and disease Nat. Rev. Neurosci. 13 2012 528 541
51. M. Shibata, H. Nakao, H. Kiyonari, T. Abe, and S. Aizawa MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors J. Neurosci. 31 2011 3407 3422
52. T. Shu, K.G. Butz, C. Plachez, R.M. Gronostajski, and L.J. Richards Abnormal development of forebrain midline glia and commissural projections in Nfia knock-out mice J. Neurosci. 23 2003 203 212
53. A. Sparmann, Y. Xie, E. Verhoeven, M. Vermeulen, C. Lancini, G. Gargiulo, D. Hulsman, M. Mann, J.A. Knoblich, and M. van Lohuizen The chromodomain helicase Chd4 is required for Polycomb-mediated inhibition of astroglial differentiation EMBO J. 32 2013 1598 1612
54. G. Steele-Perkins, C. Plachez, K.G. Butz, G. Yang, C.J. Bachurski, S.L. Kinsman, E.D. Litwack, L.J. Richards, and R.M. Gronostajski The transcription factor gene Nfib is essential for both lung maturation and brain development Mol. Cell. Biol. 25 2005 685 698
55. T. Takizawa, K. Nakashima, M. Namihira, W. Ochiai, A. Uemura, M. Yanagisawa, N. Fujita, M. Nakao, and T. Taga DNA methylation is a critical cell-intrinsic determinant of astrocyte differentiation in the fetal brain Dev. Cell 1 2001 749 758
56. S. Tanaka, Y. Kamachi, A. Tanouchi, H. Hamada, N. Jing, and H. Kondoh Interplay of SOX and POU factors in regulation of the Nestin gene in neural primordial cells Mol. Cell. Biol. 24 2004 8834 8846
57. P.C. Tsai, S. Bake, S. Balaraman, J. Rawlings, R.R. Holgate, D. Dubois, and R.C. Miranda MiR-153 targets the nuclear factor-1 family and protects against teratogenic effects of ethanol exposure in fetal neural stem cells Biol. Open 3 2014 741 758
58. J. Visvanathan, S. Lee, B. Lee, J.W. Lee, and S.K. Lee The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development Genes Dev. 21 2007 744 749
59. C. Wei, E.J. Thatcher, A.F. Olena, D.J. Cha, A.L. Perdigoto, A.F. Marshall, B.D. Carter, K. Broadie, and J.G. Patton miR-153 regulates SNAP-25, synaptic transmission, and neuronal development PLoS ONE 8 2013 e57080
60. H.B. Wood, and V. Episkopou Comparative expression of the mouse Sox1, Sox2 and Sox3 genes from pre-gastrulation to early somite stages Mech. Dev. 86 1999 197 201
61. Z. Wu, B. He, J. He, and X. Mao Upregulation of miR-153 promotes cell proliferation via downregulation of the PTEN tumor suppressor gene in human prostate cancer Prostate 73 2013 596 604
62. A.S. Yoo, B.T. Staahl, L. Chen, and G.R. Crabtree MicroRNA-mediated switching of chromatin-remodelling complexes in neural development Nature 460 2009 642 646
63. C. Zhao, G. Sun, S. Li, and Y. Shi A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination Nat. Struct. Mol. Biol. 16 2009 365 371
64. X. Zhao, X. He, X. Han, Y. Yu, F. Ye, Y. Chen, T. Hoang, X. Xu, Q.S. Mi, M. Xin, and et al. MicroRNA-mediated control of oligodendrocyte differentiation Neuron 65 2010 612 626
65. S. Zhao, Y. Deng, Y. Liu, X. Chen, G. Yang, Y. Mu, D. Zhang, J. Kang, and Z. Wu MicroRNA-153 is tumor suppressive in glioblastoma stem cells Mol. Biol. Rep. 40 2013 2789 2798