MicroRNAs: Key triggers of neuronal cell fate

Frontiers in Cellular Neuroscience

Volumn 8, Issue JUN, 2014, Pages

  Meza Sosa, Karla F ^a   Pedraza Alva, Gustavo ^a   Pérez Martínez, Leonor ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Central nervous system; Development; MiRNAs; Neural progenitors; Neural stem cell; Neuronal cell fate; Neuronal differentiation

Indexed keywords

BETA CATENIN; CYCLIN D1; CYCLIN DEPENDENT KINASE 6; CYCLIN DEPENDENT KINASE INHIBITOR 1C; EOMESODERMIN; GUANOSINE TRIPHOSPHATASE; JAGGED1; KI 67 ANTIGEN; METHYL CPG BINDING PROTEIN 2; MICRORNA; MICRORNA 124; MICRORNA 134; MICRORNA 137; MICRORNA 25; MICRORNA 9; MINICHROMOSOME MAINTENANCE PROTEIN 7; ORPHAN NUCLEAR RECEPTOR; POLYPYRIMIDINE TRACT BINDING PROTEIN; PROTEIN P53; RETINOBLASTOMA BINDING PROTEIN 2; RNA POLYMERASE II; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR E2F3; TRANSCRIPTION FACTOR NANOG; TRANSCRIPTION FACTOR SOX2; TRANSCRIPTION FACTOR SOX9; TRANSFORMING GROWTH FACTOR BETA; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; UNTRANSLATED RNA; WNT PROTEIN;

3' UNTRANSLATED REGION; CAENORHABDITIS ELEGANS; CELL CYCLE; CELL FATE; CELL LINEAGE; CELL SURVIVAL; DOWN REGULATION; DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; GENE CONTROL; GENE OVEREXPRESSION; GENE REPRESSION; MRNA EXPRESSION ASSAY; NERVE CELL; NERVE CELL DIFFERENTIATION; NERVOUS SYSTEM DEVELOPMENT; NEURAL STEM CELL; NONHUMAN; PROTEIN EXPRESSION; REVIEW; XENOPUS TROPICALIS; ZEBRA FISH;

EID: 84906268446     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2014.00175     Document Type: Review

References (116)

1. Åkerblom, M., and Jakobsson, J. (2013). MicroRNAs as neuronal fate determinants. Neuroscientist 20, 235-242. doi: 10.1177/1073858413497265
2. Åkerblom, M., Sachdeva, R., Barde, I., Verp, S., Gentner, B., Trono, D., and Jakobsson, J. (2012). MicroRNA-124 is a subventricular zone neuronal fate determinant. J. Neurosci. 32, 8879-8889. doi: 10.1523/JNEUROSCI.0558-12.2012
3. Althoff, K., Beckers, A., Odersky, A., Mestdagh, P., Köster, J., Bray, I., et al. (2013). MiR-137 functions as a tumor suppressor in neuroblastoma by downregulating KDM1A. Int. J. Cancer 133, 1064-1073. doi: 10.1002/ijc.28091
4. Balaguer, F., Link, A., Lozano, J. J., Cuatrecasas, M., Nagasaka, T., Boland, C. R., et al. (2011). Epigenetic silencing of miR-137 is an early event in colorectal carcinogenesis. Cancer Res. 70, 6609-6618. doi: 10.1158/0008-5472.CAN-10-0622
5. Bartel, D. P., Lee, R., and Feinbaum, R. (2004). MicroRNAs: genomics, biogenesis, mechanism and function. Cell 116, 281-297. doi: 10.1016/S0092-8674(04)00045-5
6. Bertrand, N., Castro, D. S., and Guillemot, F. (2002). Proneural genes and the specification of neural cell types. Nat. Rev. Neurosci. 3, 517-530. doi: 10.1038/nrn874
7. Bier, A., Giladi, N., Kronfeld, N., Lee, H., Cazacu, S., Finniss, S., et al. (2013). MicroRNA-137 is downregulated in glioblastoma and inhibits the stemness of glioma stem cells by targeting RTVP-1. Oncotarget 4, 665-676.
8. Bonev, B., Pisco, A., and Papalopulu, N. (2011). MicroRNA-9 reveals regional diversity of neural progenitors along the anterior-posterior axis. Dev. Cell 20, 19-32. doi: 10.1016/j.devcel.2010.11.018
9. Brett, J. O., Renault, V. M., Rafalski, V. A., Webb, A. E., and Brunet, A. (2011). The microRNA cluster miR-106b~25 regulates adult neural stem/progenitor cell proliferation and neuronal differentiation. Aging (Albany. NY). 3, 108-124.
10. Cao, X., Yeo, G., Muotri, A. R., Kuwabara, T., and Gage, F. H. (2006). Noncoding RNAs in the mammalian central nervous system. Annu. Rev. Neurosci. 29, 77-103. doi: 10.1146/annurev.neuro.29.051605.112839
11. Chen, C.-Z., Li, L., Lodish, H. F., and Bartel, D. P. (2004). MicroRNAs modulate hematopoietic lineage differentiation. Science 303, 83-86. doi: 10.1126/science.1091903
12. Chen, J.-A., Huang, Y.-P., Mazzoni, E. O., Tan, G. C., Zavadil, J., and Wichterle, H. (2011a). Mir-17-3p controls spinal neural progenitor patterning by regulating Olig2/Irx3 cross-repressive loop. Neuron 69, 721-735. doi: 10.1016/j.neuron.2011.01.014
13. Chen, Q., Chen, X., Zhang, M., Fan, Q., Luo, S., and Cao, X. (2011b). miR-137 is frequently down-regulated in gastric cancer and is a negative regulator of Cdc42. Dig. Dis. Sci. 56, 2009-2016. doi: 10.1007/s10620-010-1536-3
14. Chen, X., Wang, J., Shen, H., Lu, J., Li, C., Hu, D.-N., et al. (2011c). Epigenetics, microRNAs, and carcinogenesis: functional role of microRNA-137 in uveal melanoma. Invest. Ophthalmol. Vis. Sci. 52, 1193-1199. doi: 10.1167/iovs.10-5272
15. Cheng, L.-C., Pastrana, E., Tavazoie, M., and Doetsch, F. (2009). miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12, 399-408. doi: 10.1038/nn.2294
16. Choudhury, N. R., de Lima Alves, F., de Andrés-Aguayo, L., Graf, T., Cáceres, J. F., Rappsilber, J., et al. (2013). Tissue-specific control of brain-enriched miR-7 biogenesis. Genes Dev. 27, 24-38. doi: 10.1101/gad.199190.112
17. Clark, A., Goldstein, L., Tevlin, M., Tavaré, S., Shaham, S., and Miska, E. (2010). The microRNA miR-124 controls gene expres-sion in the sensory nervous system of Caenorhabditis elegans. Nucleic Acids Res. 38, 3780-3793. doi: 10.1093/nar/gkq083
18. Conaco, C., Otto, S., Han, J.-J., and Mandel, G. (2006). Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. U.S.A. 103, 2422-2427. doi: 10.1073/pnas.0511041103
19. Coolen, M., and Bally-Cuif, L. (2009). MicroRNAs in brain development and physiology. Curr. Opin. Neurobiol. 19, 461-470. doi: 10.1016/j.conb.2009.09.006
20. Davis, T. H., Cuellar, T. L., Koch, S. M., Barker, A. J., Harfe, B. D., McManus, M. T., et al. (2008). Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28, 4322-4330. doi: 10.1523/JNEUROSCI.4815-07.2008
21. De Chevigny, A., Coré, N., Follert, P., Gaudin, M., Barbry, P., Béclin, C., et al. (2012). miR-7a regulation of Pax6 controls spatial origin of forebrain dopaminergic neurons. Nat. Neurosci. 15, 1120-1126. doi: 10.1038/nn.3142
22. Delaloy, C., Liu, L., Lee, J.-A., Su, H., Shen, F., Yang, G.-Y., et al. (2010). MicroRNA-9 coordinates proliferation and migration of human embryonic stem cell-derived neural progenitors. Cell Stem Cell 6, 323-335. doi: 10.1016/j.stem.2010.02.015
23. Denli, A. M., Cao, X., and Gage, F. H. (2009). miR-9 and TLX: chasing tails in neural stem cells. Nat. Struct. Mol. Biol. 16, 346-347. doi: 10.1038/nsmb0409-346
24. De Smaele, E., Ferretti, E., and Gulino, A. (2010). MiRNAs as biomarkers for CNS cancer and other disorders. Brain Res. 1338, 100-111. doi: 10.1016/j.brainres.2010.03.103
25. Diez del Corral, R., and Storey, K. G. (2001). Markers in vertebrate neurogenesis. Nat. Rev. Neurosci. 2, 835-839. doi: 10.1038/35097587
26. Du, T., and Zamore, P. D. (2005). microPrimer: the biogenesis and function of microRNA. Development 132, 4645-4652. doi: 10.1242/dev.02070
27. Faghihi, M. A., Zhang, M., Huang, J., Modarresi, F., Van Der Brug, M. P., Nalls, M. A., et al. (2010). Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 11, R56. doi: 10.1186/gb-2010-11-5-r56
28. Gage, F. H. (2000). Mammalian neural stem cells. Science 287, 1433-1438. doi: 10.1126/science.287.5457.1433
29. Gaughwin, P., Ciesla, M., Yang, H., Lim, B., and Brundin, P. (2011). Stage-specific modulation of cortical neuronal development by Mmu-miR-134. Cereb. Cortex 21, 1857-1869. doi: 10.1093/cercor/bhq262
30. Giraldez, A., Cinalli, R., Glasner, M., Enright, A., Thomson, J., Baskerville, S., et al. (2005). MicroRNAs regulate brain morphogenesis in zebrafish. Science 308, 833-838. doi: 10.1126/science.1109020
31. Guo, L., Xu, J., Qi, J., Zhang, L., Wang, J., Liang, J., et al. (2013). MicroRNA-17-92a upregulation by estrogen leads to Bim targeting and inhibition of osteoblast apoptosis. J. Cell Sci. 126, 978-988. doi: 10.1242/jcs.117515
32. Hansen, T. B., Jensen, T. I., Clausen, B. H., Bramsen, J. B., Finsen, B., Damgaard, C. K., et al. (2013). Natural RNA circles function as efficient microRNA sponges. Nature 495, 384-388. doi: 10.1038/nature11993
33. Helwak, A., Kudla, G., Dudnakova, T., and Tollervey, D. (2013). Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding. Cell 153, 654-665. doi: 10.1016/j.cell.2013.03.043
34. Herzer, S., Silahtaroglu, A., and Meister, B. (2012). Locked nucleic acid-based in situ hybridisation reveals miR-7a as a hypothalamus-enriched microRNA with a distinct expression pattern. J. Neuroendocrinol. 24, 1492-1504. doi: 10.1111/j.1365-2826.2012.02358.x
35. Hohjoh, H., and Fukushima, T. (2007). Expression profile analysis of microRNA (miRNA) in mouse central nervous system using a new miRNA detection system that examines hybridization signals at every step of washing. Gene 391, 39-44. doi: 10.1016/j.gene.2006.11.018
36. Hutvágner, G., McLachlan, J., Pasquinelli, A. E., Bálint, E., Tuschl, T., and Zamore, P. D. (2001). A cellular function for the RNA-interference enzyme Dicer in the maturation of the let-7 small temporal RNA. Science 293, 834-838. doi: 10.1126/science.1062961
37. Imayoshi, I., and Kageyama, R. (2011). The role of Notch signaling in adult neurogenesis. Mol. Neurobiol. 44, 7-12. doi: 10.1007/s12035-011-8186-0
38. Ivey, K. N., and Srivastava, D. (2010). MicroRNAs as regulators of differentiation and cell fate decisions. Cell Stem Cell 7, 36-41. doi: 10.1016/j.stem.2010.06.012
39. Jan, T., Fotaki, V., Pollock, A., Sun, T., Pratt, T., and Price, D. J. (2013). MicroRNA-92b regulates the development of intermediate cortical progenitors in embryonic mouse brain. Proc. Natl. Acad. Sci.U.S.A. 110, 7056-7061. doi: 10.1073/pnas.1219385110
40. Johnson, D. G., and Walker, C. L. (1999). Cyclins and cell cycle checkpoints. Annu. Rev. Pharmacol. Toxicol. 39, 295-312. doi: 10.1146/annurev.pharmtox.39.1.295
41. Kan, T., Sato, F., Ito, T., Matsumura, N., David, S., Agarwal, R., et al. (2010). The miR-106b-25 polycistron, activated by genomic amplification, functions as an oncogene by suppressing p21 and Bim. Gastroenterology 136, 1689-1700. doi: 10.1053/j.gastro.2009.02.002
42. Kawase-Koga, Y., Low, R., Otaegi, G., Pollock, A., Deng, H., Eisenhaber, F., et al. (2010). RNAase-III enzyme Dicer maintains signaling pathways for differentiation and survival in mouse cortical neural stem cells. J. Cell Sci. 123, 586-594. doi: 10.1242/jcs.059659
43. Kim, D., Song, J., and Jin, E.-J. (2010). MicroRNA-221 regulates chondrogenic differentiation through promoting proteosomal degradation of slug by targeting Mdm2. J. Biol. Chem. 285, 26900-26907. doi: 10.1074/jbc.M110.115105
44. Kim, Y.-K., Yu, J., Han, T. S., Park, S.-Y., Namkoong, B., Kim, D. H., et al. (2009). Functional links between clustered microRNAs: suppression of cell-cycle inhibitors by microRNA clusters in gastric cancer. Nucleic Acids Res. 37, 1672-1681. doi: 10.1093/nar/gkp002
45. Kohwi, M., Osumi, N., Rubenstein, J. L. R., and Alvarez-Buylla, A. (2005). Pax6 is required for making specific subpopulations of granule and periglomerular neurons in the olfactory bulb. J. Neurosci. 25, 6997-7003. doi: 10.1523/JNEUROSCI.1435-05.2005
46. Krichevsky, A., and Sonntag, K. (2006). Specific MicroRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24, 857-864. doi: 10.1634/stemcells.2005-0441
47. Lai, E. C. (2002). MicroRNAs are complementary to 3′ UTR sequence motifs that mediate negative post-transcriptional regulation. Nat. Genet. 30, 363-364. doi: 10.1038/ng865
48. Lal, A., Navarro, F., Maher, C. A., Maliszewski, L. E., Yan, N., O'Day, E., Chowdhury, D., et al. (2009). miR-24 Inhibits cell proliferation by targeting E2F2, MYC, and other cell-cycle genes via binding to "seedless" 3′UTR microRNA recognition elements. Mol. Cell 35, 610-625. doi: 10.1016/j.molcel.2009.08.020
49. Landgraf, P., Rusu, M., Sheridan, R., Sewer, A., Iovino, N., Aravin, A., et al. (2007). A mammalian microRNA expression atlas based on small RNA library sequencing. Cell 129, 1401-1414. doi: 10.1016/j.cell.2007.04.040
50. Lau, P., and de Strooper, B. (2010). Dysregulated microRNAs in neurodegenerative disorders. Semin. Cell Dev. Biol. 21, 768-773. doi: 10.1016/j.semcdb.2010.01.009
51. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., et al. (2003). The nuclear RNase III Drosha initiates microRNA processing. Nature 425, 415-419. doi: 10.1038/nature01957
52. Lee, Y., Jeon, K., Lee, J.-T., Kim, S., and Kim, V. N. (2002). MicroRNA maturation: stepwise processing and subcellular localization. EMBO J. 21, 4663-4670. doi: 10.1093/emboj/cdf476
53. Leucht, C., Stigloher, C., Wizenmann, A., Klafke, R., Folchert, A., and Bally-Cuif, L. (2008). MicroRNA-9 directs late organizer activity of the midbrain-hindbrain boundary. Nat. Neurosci. 11, 641-648. doi: 10.1038/nn.2115
54. Lewis, B. P., Shih, I., Jones-rhoades, M. W., Bartel, D. P., and Burge, C. B. (2003). Prediction of mammalian MicroRNA Targets. Cell 115, 787-798. doi: 10.1016/S0092-8674(03)01018-3
55. Li, H., and Yang, B. B. (2012). Stress response of glioblastoma cells mediated by miR-17-5p targeting PTEN and the passenger strand miR-17-3p targeting. Oncotarget 3, 1653-1668.
56. Li, W., Sun, G., Yang, S., Qu, Q., Nakashima, K., and Shi, Y. (2008). Nuclear receptor TLX regulates cell cycle progression in neural stem cells of the developing brain. Mol. Endocrinol. 22, 56-64. doi: 10.1210/me.2007-0290
57. Li, X., and Jin, P. (2010). Roles of small regulatory RNAs in determining neuronal identity. Nat. Rev. Neurosci. 11, 329-338. doi: 10.1038/nrn2739
58. Li, X., and Zhao, X. (2008). Epigenetic regulation of mammalian stem cells. Stem Cells Dev. 17, 1043-1052. doi: 10.1089/scd.2008.0036
59. Liu, M., Lang, N., Qiu, M., Xu, F., Li, Q., Tang, Q., et al. (2011a). miR-137 targets Cdc42 expression, induces cell cycle G1 arrest and inhibits invasion in colorectal cancer cells. Int. J. Cancer 128, 1269-1279. doi: 10.1002/ijc.25452
60. Liu, S.-P., Fu, R.-H., Yu, H.-H., Li, K.-W., Tsai, C.-H., Shyu, W.-C., et al. (2009). MicroRNAs regulation modulated self-renewal and lineage differentiation of stem cells. Cell Transplant. 18, 1039-1045. doi: 10.3727/096368909X471224
61. Liu, X., Chopp, M., Zhang, R., Tao, T., Wang, X., Kassis, H., et al. (2011b). MiR-124a regulates proliferation of neural progenitor cells through Notch signaling pathway. PLoS ONE 6:e23461. doi: 10.1371/journal.pone.0023461
62. Lopes, R., Verhey van Wijk, N., Neves, G., and Pachnis, V. (2012). Transcription factor LIM homeobox 7 (Lhx7) maintains subtype identity of cholinergic interneurons in the mammalian striatum. Proc. Natl. Acad. Sci. U.S.A. 109, 3119-3124. doi: 10.1073/pnas.1109251109
63. Maiorano, N., and Mallamaci, A. (2009). Promotion of embryonic cortico-cerebral neuronogenesis by miR-124. Neural Dev. 4:40. doi: 10.1186/1749-8104-4-40
64. Makeyev, E. V., Zhang, J., Carrasco, M. A., and Maniatis, T. (2007). The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27, 435-448. doi: 10.1016/j.molcel.2007.07.015
65. Markakis, E. A., Palmer, T. D., Randolph-Moore, L., Rakic, P., and Gage, F. H. (2004). Novel neuronal phenotypes from neural progenitor cells. J. Neurosci. 24, 2886-2897. doi: 10.1523/JNEUROSCI.4161-03.2004
66. Memczak, S., Jens, M., Elefsinioti, A., Torti, F., Krueger, J., Rybak, A., et al. (2013). Circular RNAs are a large class of animal RNAs with regulatory potency. Nature 495, 333-338. doi: 10.1038/nature11928
67. Meza-Sosa, K., Valle-García, D., Pedraza-Alva, G., and Pérez-Martínez, L. (2012). Role of microRNAs in central nervous system development and pathology. J. Neurosci. Res. 90, 1-12. doi: 10.1002/jnr.22701
68. Miska, E. A., Alvarez-Saavedra, E., Townsend, M., Yoshii, A., Sestan, N., Rakic, P., et al. (2004). Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol. 5:R68. doi: 10.1186/gb-2004-5-9-r68
69. Neves, G., Shah, M. M., Liodis, P., Achimastou, A., Denaxa, M., Roalfe, G., et al. (2013). The LIM homeodomain protein Lhx6 regulates maturation of interneurons and network excitability in the mammalian Cortex. Cereb. Cortex 23, 1811-1823. doi: 10.1093/cercor/bhs159
70. Nielsen, J. A., Lau, P., Maric, D., Barker, J. L., and Hudson, L. D. (2009). Integrating microRNA and mRNA expression profiles of neuronal progenitors to identify regulatory networks underlying the onset of cortical neurogenesis. BMC Neurosci. 10:98. doi: 10.1186/1471-2202-10-98
71. Niu, C. S., Yang, Y., and Cheng, C.-D. (2013). MiR-134 regulates the proliferation and invasion of glioblastoma cells by reducing Nanog expression. Int. J. Oncol. 42, 1533-1540. doi: 10.3892/ijo.2013.1844
72. Okamura, K., Hagen, J. W., Duan, H., Tyler, D. M., and Lai, E. C. (2007). The mirtron pathway generates microRNA-class regulatory RNAs in Drosophila. Cell 130, 89-100. doi: 10.1016/j.cell.2007.06.028
73. Olsen, L., Klausen, M., Helboe, L., Nielsen, F. C., and Werge, T. (2009). MicroRNAs show mutually exclusive expression patterns in the brain of adult male rats. PLoS ONE 4:e7225. doi: 10.1371/journal.pone.0007225
74. Otaegi, G., Pollock, A., Hong, J., and Sun, T. (2011). MicroRNA miR-9 modifies motor neuron columns by a tuning regulation of FoxP1 levels in developing spinal cords. J. Neurosci. 31, 809-818. doi: 10.1523/JNEUROSCI.4330-10.2011
75. Pelling, M., Anthwal, N., McNay, D., Gradwohl, G., Leiter, A. B., Guillemot, F., et al. (2011). Differential requirements for neurogenin 3 in the development of POMC and NPY neurons in the hypothalamus. Dev. Biol. 349, 406-416. doi: 10.1016/j.ydbio.2010.11.007
76. Peng, C., Li, N., Ng, Y.-K., Zhang, J., Meier, F., Theis, F. J., et al. (2012). A unilateral negative feedback loop between miR-200 microRNAs and Sox2/E2F3 controls neural progenitor cell-cycle exit and differentiation. J. Neurosci. 32, 13292-13308. doi: 10.1523/JNEUROSCI.2124-12.2012
77. Pérez-Martinez, L., and Charli, J. (2006). "Factors involved in the establishment of hypothalamic neuroendocrine phenotypes, " in Molecular Endocrinology, ed P. Joseph-Bravo (Trivandrum: Research Signpost), 127-147.
78. Pichiorri, F., Suh, S.-S., Rocci, A., De Luca, L., Taccioli, C., Santhanam, R., et al. (2010). Downregulation of p53-inducible microRNAs 192, 194, and 215 impairs the p53/MDM2 autoregulatory loop in multiple myeloma development. Cancer Cell 18, 367-381. doi: 10.1016/j.ccr.2010.09.005
79. Qin, S., Mol, C. Z., Ahead, P., and Feeds, R. S. S. (2012). Role of Krüppel-like factor 4 in neurogenesis and radial neuronal migration in the developing cerebral cortex. Mol. Cell. Biol. 32, 4297-4305. doi: 10.1128/MCB.00838-12
80. Qu, Q., Sun, G., Li, W., Yang, S., Ye, P., Zhao, C., et al. (2010). Orphan nuclear receptor TLX activates Wnt/beta-catenin signalling to stimulate neural stem cell proliferation and self-renewal. Nat. Cell Biol. 12, 31-40. doi: 10.1038/ncb2001
81. Rago, L., Beattie, R., Taylor, V., and Winter, J. (2014). miR379-410 cluster miRNAs regulate neurogenesis and neuronal migration by fine-tuning N-cadherin. EMBO J. 33, 906-920. doi: 10.1002/embj.201386591
82. Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S. V., Russo, J. J., et al. (2009). Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63, 803-817. doi: 10.1016/j.neuron.2009.05.029
83. Renault, V. M., Rafalski, V. A., Morgan, A. A., Salih, D. A. M., Jamie, O., Webb, A. E., et al. (2009). FoxO3 regulates neural stem cell homeostasis. Cell Stem Cell 5, 527-539. doi: 10.1016/j.stem.2009.09.014
84. Rodríguez-Aznar, E., Barrallo-Gimeno, A., and Nieto, M. (2013). Scratch2 prevents cell cycle re-entry by repressing miR-25 in postmitotic primary neurons. J. Neurosci. 33, 5095-5105. doi: 10.1523/JNEUROSCI.4459-12.2013
85. Roese-Koerner, B., Stappert, L., Koch, P., Brüstle, O., and Borghese, L. (2013). Pluripotent stem cell-derived somatic stem cells as tool to study the role of microRNAs in early human neural development. Curr. Mol. Med. 13, 707-722. doi: 10.2174/1566524011313050003
86. Rybak, A., Fuchs, H., Smirnova, L., Brandt, C., Pohl, E. E., Nitsch, R., et al. (2008). A feedback loop comprising lin-28 and let-7 controls pre-let-7 maturation during neural stem-cell commitment. Nat. Cell Biol. 10, 987-993. doi: 10.1038/ncb1759
87. Schratt, G. (2009). Fine-tuning neural gene expression with microRNAs. Curr. Opin. Neurobiol. 19, 213-219. doi: 10.1016/j.conb.2009.05.015
88. Schratt, G., Tuebing, F., Nigh, E., Kane, C., Sabatini, M., Kiebler, M., et al. (2006). A brain-specific microRNA regulates dendritic spine development. Nature 441, 902. doi: 10.1038/nature04367
89. Sempere, L. F., Freemantle, S., Pitha-Rowe, I., Moss, E., Dmitrovsky, E., and Ambros, V. (2004). Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation. Genome Biol. 5, R13. doi: 10.1186/gb-2004-5-3-r13
90. Shibata, M., Nakao, H., Kiyonari, H., Abe, T., and Aizawa, S. (2011). MicroRNA-9 regulates neurogenesis in mouse telencephalon by targeting multiple transcription factors. J. Neurosci. 31, 3407-3422. doi: 10.1523/JNEUROSCI.5085-10.2011
91. Shikanai, M., Nakajima, K., and Kawauchi, T. (2011). N-cadherin regulates radial glial fiber-dependent migration of cortical locomoting neurons. Commun. Integr. Biol. 4, 326-330. doi: 10.4161/cib.4.3.14886
92. Silber, J., Lim, D. A., Petritsch, C., Persson, A. I., Maunakea, A. K., Yu, M., Vandenberg, S. R., et al. (2008). miR-124 and miR-137 inhibit proliferation of glioblastoma multiforme cells and induce differentiation of brain tumor stem cells. BMC Med. 6:14. doi: 10.1186/1741-7015-6-14
93. Singh, S. K. (2007). miRNAs: from neurogeneration to neurodegeneration. Pharmacogenomics 8, 971-978. doi: 10.2217/14622416.8.8.971
94. Smirnova, L., Gräfe, A., Seiler, A., Schumacher, S., Nitsch, R., and Wulczyn, F. G. (2005). Regulation of miRNA expression during neural cell specification. Eur. J. Neurosci. 21, 1469-1477. doi: 10.1111/j.1460-9568.2005.03978.x
95. Smrt, R. D., Szulwach, K. E., Pfeiffer, R. L., Li, X., Guo, W., Pathania, M., et al. (2011). MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1. Stem Cells 28, 1060-1070. doi: 10.1002/stem.431
96. Sun, G., Ye, P., Murai, K., Lang, M., Li, S., and Zhang, H. (2012). miR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat. Commun. 2, 1-20. doi: 10.1038/ncomms1532
97. Szulwach, K., Li, X., Smrt, R., Li, Y., Luo, Y., Lin, L., et al. (2010). Cross talk between microRNA and epigenetic regulation in adult neurogenesis. J. Cell Biol. 189, 127-141. doi: 10.1083/jcb.200908151
98. Tanzer, A., and Stadler, P. (2004). Molecular evolution of a microRNA cluster. J. Mol. Biol. 339, 327-335. doi: 10.1016/j.jmb.2004.03.065
99. Tarantino, C., Paolella, G., Cozzuto, L., Minopoli, G., Pastore, L., Parisi, S., et al. (2010). miRNA 34a, 100, and 137 modulate differentiation of mouse embryonic stem cells. FASEB J. 24, 3255-3263. doi: 10.1096/fj.09-152207
100. Tay, Y., Tam, W., Ang, Y., Gaughwin, P., Yang, H., Wang, W., et al. (2008). MicroRNA-134 modulates the differentiation of mouse embryonic stem cells, where it causes post-transcriptional attenuation of Nanog and LRH1. Stem Cells 26, 17-29. doi: 10.1634/stemcells.2007-0295
101. Tsai, N., Lin, Y., and Wei, L. (2009). MicroRNA mir-346 targets the 5′-untranslated region of receptor-interacting protein 140 (RIP140) mRNA and up-regulates its protein expression. Biochem. J. 424, 411-418. doi: 10.1042/BJ20090915
102. Visvanathan, J., Lee, S., Lee, B., Lee, J. W., and Lee, S.-K. (2007). The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 21, 744-749. doi: 10.1101/gad.1519107
103. Wang, Y., Vogel, G., Yu, Z., and Richard, S. (2013). The QKI-5 and QKI-6 RNA binding proteins regulate the expression of microRNA 7 in glial cells. Mol. Cell. Biol. 33, 1233-1243. doi: 10.1128/MCB.01604-12
104. Weng, R., and Cohen, S. (2012). Drosophila miR-124 regulates neuroblast proliferation through its target anachronism. Development 139, 1427-1434. doi: 10.1242/dev.075143
105. Westholm, J. O., and Lai, E. C. (2011). Mirtrons: microRNA biogenesis via splicing. Biochimie 93, 1897-1904. doi: 10.1016/j.biochi.2011.06.017
106. Xu, N., Papagiannakopoulos, T., Pan, G., Thomson, J. A., and Kosik, K. S. (2009). MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137, 647-658. doi: 10.1016/j.cell.2009.02.038
107. Yi, R., Qin, Y., Macara, I. G., and Cullen, B. R. (2003). Exportin-5 mediates the nuclear export of pre-microRNAs and short hairpin RNAs. Genes Dev. 17, 3011-3016. doi: 10.1101/gad.1158803
108. Yoo, A. S., Staahl, B. T., Chen, L., and Crabtree, G. R. (2009). MicroRNA-mediated switching of chromatin-remodelling complexes in neural development. Nature 460, 642-646. doi: 10.1038/nature08139
109. Yu, J., Chung, K., Deo, M., Thompson, R. C., and Turner, D. L. (2008). MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp. Cell Res. 314, 2618-2633. doi: 10.1016/j.yexcr.2008.06.002
110. Yuva-Aydemir, Y., Simkin, A., Gascon, E., and Gao, F.-B. (2011). MicroRNA-9: functional evolution of a conserved small regulatory RNA. RNA Biol. 8, 557-564. doi: 10.4161/rna.8.4.16019
111. Zhang, X., Wang, H., Zhang, S., Song, J., Zhang, Y., Wei, X., et al. (2012). MiR-134 functions as a regulator of cell proliferation, apoptosis, and migration involving lung septation. In Vitro Cell. Dev. Biol. Anim. 48, 131-136. doi: 10.1007/s11626-012-9482-3
112. Zhao, C., Sun, G., Li, S., Lang, M., Yang, S., Li, W., et al. (2010). MicroRNA let-7b regulates neural stem cell proliferation and differentiation by targeting nuclear receptor TLX signaling. Proc. Natl. Acad. Sci.U.S.A. 107, 1876-1881. doi: 10.1073/pnas.0908750107
113. Zhao, C., Sun, G., Li, S., and Shi, Y. (2009). A feedback regulatory loop involving microRNA-9 and nuclear receptor TLX in neural stem cell fate determination. Nat. Struct. Mol. Biol. 16, 365-371. doi: 10.1038/nsmb.1576
114. Zhao, C., Sun, G., Ye, P., Li, S., and Shi, Y. (2013). MicroRNA let-7d regulates the TLX/microRNA-9 cascade to control neural cell fate and neurogenesis. Sci. Rep. 3, 1-7. doi: 10.1038/srep01329
115. Zhao, Y., and Srivastava, D. (2007). A developmental view of microRNA function. Trends Biochem. Sci. 32, 189-197. doi: 10.1016/j.tibs.2007.02.006
116. Zheng, L., Qi, T., Yang, D., Qi, M., Li, D., Xiang, X., et al. (2013). microRNA-9 suppresses the proliferation, invasion and metastasis of gastric cancer cells through targeting cyclin D1 and Ets1. PLoS ONE 8:e55719. doi: 10.1371/journal.pone.0055719