An updated role of microRNA-124 in central nervous system disorders: A review

Frontiers in Cellular Neuroscience

Volumn 9, Issue MAY, 2015, Pages

  Sun, Yang ^a   Luo, Zhu Min ^a   Guo, Xiu Ming ^a   Su, Ding Feng ^a   Liu, Xia ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

Brain development; Brain tumor; CNS disorders; CNS stress; MicroRNA 124; Neurodegradation; Neuroimmunity; Stroke

Indexed keywords

AROMATIC HYDROCARBON RECEPTOR; BETA1 INTEGRIN; CYCLIN DEPENDENT KINASE 6; EPHRIN B1; JAGGED1; LAMININ GAMMA1; MICRORNA 124; MITOGEN ACTIVATED PROTEIN KINASE; MONOCARBOXYLATE TRANSPORTER 1; NEUROGENIC DIFFERENTIATION FACTOR; PROTEIN KINASE PIM 3; STAT3 PROTEIN; TRANSCRIPTION FACTOR DLX2; TRANSCRIPTION FACTOR LHX2; TRANSCRIPTION FACTOR SOX9; UNCLASSIFIED DRUG;

ADAPTIVE IMMUNITY; ARTICLE; BRAIN TUMOR; CELL DIFFERENTIATION; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; CELL SURVIVAL; CENTRAL NERVOUS SYSTEM DISEASE; CEREBROVASCULAR ACCIDENT; DOWN REGULATION; GENE EXPRESSION; HUMAN; NERVE CELL PLASTICITY; NERVE DEGENERATION; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; UPREGULATION;

EID: 84929603704     PISSN: 16625102     EISSN: None     Source Type: Journal    
DOI: 10.3389/fncel.2015.00193     Document Type: Article

References (84)

1. Akerblom, M., Sachdeva, R., Barde, I., Verp, S., Gentner, B., Trono, D., et al. (2012). MicroRNA-124 is a subventricular zone neuronal fate determinant. J. Neurosci. 32, 8879-8889. doi: 10.1523/JNEUROSCI.0558-12.2012
2. Ambros, V. (2004). The functions of animal microRNAs. Nature 431, 350-355. doi: 10.1038/nature02871
3. An, L., Liu, Y., Wu, A., and Guan, Y. (2013). MicroRNA-124 inhibits migration and invasion by down-regulating ROCK1 in glioma. PLoS ONE 8:e69478. doi: 10.1371/journal.pone.0069478
4. Arvanitis, D. N., Jungas, T., Behar, A., and Davy, A. (2010). Ephrin-B1 reverse signaling controls a posttranscriptional feedback mechanism via miR-124. Mol. Cell. Biol. 30, 2508-2517. doi: 10.1128/MCB.01620-09
5. Baroukh, N. N., and Van Obberghen, E. (2009). Function of microRNA-375 and microRNA-124a in pancreas and brain. FEBS J. 276, 6509-6521. doi: 10.1111/j.1742-4658.2009.07353.x
6. Bartel, D. P. (2004). MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116, 281-297. doi: 10.1016/S0092-8674(04)00045-5
7. Ben Assayag, E., Shenhar-Tsarfaty, S., Ofek, K., Soreq, L., Bova, I., Shopin, L., et al. (2010). Serum cholinesterase activities distinguish between stroke patients and controls and predict 12-month mortality. Mol. Med. 16, 278-286. doi: 10.2119/molmed.2010.00015
8. Bigl, M., Apelt, J., Luschekina, E. A., Lange-Dohna, C., Rossner, S., and Schliebs, R. (2000). Expression of beta-secretase mRNA in transgenic Tg2576 mouse brain with Alzheimer plaque pathology. Neurosci. Lett. 292, 107-110. doi: 10.1016/S0304-3940(00)01452-X
9. Cao, X., Pfaff, S. L., and Gage, F. H. (2007). A functional study of miR-124 in the developing neural tube. Genes Dev. 21, 531-536. doi: 10.1101/gad.1519207
10. Chandrasekar, V., and Dreyer, J. L. (2009). MicroRNAs miR-124, let-7d and miR- 181a regulate cocaine-induced plasticity. Mol. Cell. Neurosci. 42, 350-362. doi: 10.1016/j.mcn.2009.08.009
11. 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
12. 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
13. Conrad, A. T., and Dittel, B. N. (2011). Taming of macrophage and microglial cell activation by microRNA-124. Cell Res. 21, 213-216. doi: 10.1038/cr.2011.9
14. Conti, L., Crisafulli, L., Caldera, V., Tortoreto, M., Brilli, E., Conforti, P., et al. (2012). REST controls self-renewal and tumorigenic competence of human glioblastoma cells. PLoS ONE 7:e38486. doi: 10.1371/journal.pone.0038486
15. Deo, M., Yu, J. Y., Chung, K. H., Tippens, M., and Turner, D. L. (2006). Detection of mammalian microRNA expression by in situ hybridization with RNA oligonucleotides. Dev. Dyn. 235, 2538-2548. doi: 10.1002/dvdy.20847
16. Dharap, A., Bowen, K., Place, R., Li, L. C., and Vemuganti, R. (2009). Transient focal ischemia induces extensive temporal changes in rat cerebral microRNAome. J. Cereb. Blood Flow Metab. 29, 675-687. doi: 10.1038/jcbfm.2008.157
17. Doeppner, T. R., Doehring, M., Bretschneider, E., Zechariah, A., Kaltwasser, B., Muller, B., et al. (2013). MicroRNA-124 protects against focal cerebral ischemia via mechanisms involving Usp14-dependent REST degradation. Acta Neuropathol. 126, 251-265. doi: 10.1007/s00401-013-1142-5
18. Fang, M., Wang, J., Zhang, X., Geng, Y., Hu, Z., Rudd, J. A., et al. (2012). The miR-124 regulates the expression of BACE1/beta-secretase correlated with cell death in Alzheimer’s disease. Toxicol. Lett. 209, 94-105. doi: 10.1016/j.toxlet.2011.11.032
19. Farrell, B. C., Power, E. M., and Mc Dermott, K. W. (2011). Developmentally regulated expression of Sox9 and microRNAs 124, 128 and 23 in neuroepithelial stem cells in the developing spinal cord. Int. J. Dev. Neurosci. 29, 31-36. doi: 10.1016/j.ijdevneu.2010.10.001
20. Fischbach, S. J., and Carew, T. J. (2009). MicroRNAs in memory processing. Neuron 63, 714-716. doi: 10.1016/j.neuron.2009.09.007
21. Fowler, A., Thomson, D., Giles, K., Maleki, S., Mreich, E., Wheeler, H., et al. (2011). MiR-124a is frequently down-regulated in glioblastoma and is involved in migration and invasion. Eur. J. Cancer 47, 953-963. doi: 10.1016/j.ejca.2010.11.026
22. Glass, C. K., Saijo, K., Winner, B., Marchetto, M. C., and Gage, F. H. (2010). Mechanisms underlying inflammation in neurodegeneration. Cell 140, 918-934. doi: 10.1016/j.cell.2010.02.016
23. Godlewski, J., Newton, H. B., Chiocca, E. A., and Lawler, S. E. (2010). MicroRNAs and glioblastoma; the stem cell connection. Cell Death. Differ. 17, 221-228. doi: 10.1038/cdd.2009.71
24. Graham, S. H., Chen, J., and Clark, R. S. (2000). Bcl-2 family gene products in cerebral ischemia and traumatic brain injury. J. Neurotrauma 17, 831-841. doi: 10.1089/neu.2000.17.831
25. Hebert, S. S., Horre, K., Nicolai, L., Papadopoulou, A. S., Mandemakers, W., Silahtaroglu, A. N., et al. (2008). Loss of microRNA cluster miR-29a/b- 1 in sporadic Alzheimer’s disease correlates with increased BACE1/beta- secretase expression. Proc. Natl. Acad. Sci. U.S.A. 105, 6415-6420. doi: 10.1073/pnas.0710263105
26. Ho, C. Y., Bar, E., Giannini, C., Marchionni, L., Karajannis, M. A., Zagzag, D., et al. (2013). MicroRNA profiling in pediatric pilocytic astrocytoma reveals biologically relevanttargets, including PBX3, NFIB, and METAP2. Neuro Oncol. 15, 69-82. doi: 10.1093/neuonc/nos269
27. Hua, D., Mo, F., Ding, D., Li, L., Han, X., Zhao, N., et al. (2012). A catalogue of glioblastoma and brain MicroRNAs identified by deep sequencing. OMICS 16, 690-699. doi: 10.1089/omi.2012.0069
28. Huang, T. C., Chang, H. Y., Chen, C. Y., Wu, P. Y., Lee, H., Liao, Y. F., et al. (2011). Silencing of miR-124 induces neuroblastoma SK-N-SH cell differentiation, cell cycle arrest and apoptosis through promoting AHR. FEBS Lett. 585, 3582-3586. doi: 10.1016/j.febslet.2011.10.025
29. Jeyaseelan, K., Lim, K. Y., and Armugam, A. (2008). MicroRNA expression in the blood and brain of rats subjected to transient focal ischemia by middle cerebral artery occlusion. Stroke 39, 959-966. doi: 10.1161/STROKEAHA.107.500736
30. Kim, J., Inoue, K., Ishii, J., Vanti, W. B., Voronov, S. V., Murchison, E., et al. (2007). A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317, 1220-1224. doi: 10.1126/science.1140481
31. Krichevsky, A. M., Sonntag, K. C., Isacson, O., and Kosik, K. S. (2006). Specific microRNAs modulate embryonic stem cell-derived neurogenesis. Stem Cells 24, 857-864. doi: 10.1634/stemcells.2005-0441
32. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., and Tuschl, T. (2002). Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12, 735-739. doi: 10.1016/S0960-9822(02)00809-6
33. Lang, M. F., Yang, S., Zhao, C., Sun, G., Murai, K., Wu, X., et al. (2012). Genome- wide profiling identified a set of miRNAs that are differentially expressed in glioblastoma stem cells and normal neural stem cells. PLoS ONE 7:e36248. doi: 10.1371/journal.pone.0036248
34. Laterza, O. F., Lim, L., Garrett-Engele, P. W., Vlasakova, K., Muniappa, N., Tanaka, W. K., et al. (2009). Plasma MicroRNAs as sensitive and specific biomarkers of tissue injury. Clin. Chem. 55, 1977-1983. doi: 10.1373/clinchem.2009.131797
35. Laterza, O. F., Modur, V. R., Crimmins, D. L., Olander, J. V., Landt, Y., Lee, J. M., et al. (2006). Identification of novel brain biomarkers. Clin. Chem. 52, 1713-1721. doi: 10.1373/clinchem.2006.070912
36. Lawson, S. K., Dobrikova, E. Y., Shveygert, M., and Gromeier, M. (2013). P38alpha mitogen-activated protein kinase depletion and repression of signal transduction to translation machinery by miR-124 and -128 in neurons. Mol. Cell. Biol. 33, 127-135. doi: 10.1128/MCB.00695-12
37. Lee, H. K., Finniss, S., Cazacu, S., Bucris, E., Ziv-Av, A., Xiang, C., et al. (2013). Mesenchymalstem cells deliversynthetic microRNA mimics to glioma cells and glioma stem cells and inhibit their cell migration and self-renewal. Oncotarget 4, 346-361.
38. Lewis, B. P., Burge, C. B., and Bartel, D. P. (2005). Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 120, 15-20. doi: 10.1016/j.cell.2004.12.035
39. Li, K. K., Pang, J. C., Ching, A. K., Wong, C. K., Kong, X., Wang, Y., et al. (2009). MiR-124 is frequently down-regulated in medulloblastoma and is a negative regulator of SLC16A1. Hum. Pathol. 40, 1234-1243. doi: 10.1016/j.humpath.2009.02.003
40. Lim, L. P., Lau, N. C., Garrett-Engele, P., Grimson, A., Schelter, J. M., Castle, J., et al. (2005). Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433, 769-773. doi: 10.1038/nature03315
41. Liu, D. Z., Tian, Y., Ander, B. P., Xu, H., Stamova, B. S., Zhan, X., et al. (2010). Brain and blood microRNA expression profiling of ischemic stroke, intracerebral hemorrhage, and kainate seizures. J. Cereb. Blood Flow Metab. 30, 92-101. doi: 10.1038/jcbfm.2009.186
42. Liu, K., Liu, Y., Mo, W., Qiu, R., Wang, X., Wu, J. Y., et al. (2011a). MiR- 124 regulates early neurogenesis in the optic vesicle and forebrain, targeting NeuroD1. Nucleic Acids Res. 39, 2869-2879. doi: 10.1093/nar/gkq904
43. Liu, X. S., Chopp, M., Zhang, R. L., Tao, T., Wang, X. L., Kassis, H., et al. (2011b). MicroRNA profiling in subventricular zone after stroke: miR-124a regulates proliferation of neural progenitor cells through Notch signaling pathway. PLoS ONE 6:e23461. doi: 10.1371/journal.pone.0023461
44. Liu, X., Li, F., Zhao, S., Luo, Y., Kang, J., Zhao, H., et al. (2013). MicroRNA- 124-mediated regulation of inhibitory member of apoptosis-stimulating protein of p53 family in experimental stroke. Stroke 44, 1973-1980. doi: 10.1161/STROKEAHA.111.000613
45. Lukiw, W. J. (2007). Micro-RNA speciation in fetal, adult and Alzheimer’s disease hippocampus. Neuroreport 18, 297-300. doi: 10.1097/WNR.0b013e3280148e8b
46. 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
47. Manakov, S. A., Morton, A., Enright, A. J., and Grant, S. G. (2012). A Neuronal Transcriptome Response Involving Stress Pathways is Buffered by Neuronal microRNAs. Front. Neurosci. 6:156. doi: 10.3389/fnins.2012.00156
48. Martinou, J. C., Dubois-Dauphin, M., Staple, J. K., Rodriguez, I., Frankowski, H., Missotten, M., et al. (1994). Overexpression of BCL-2 in transgenic mice protects neurons from naturally occurring cell death and experimental ischemia. Neuron 13, 1017-1030. doi: 10.1016/0896-6273(94)90266-6
49. Mckennirey, P. (2011). The Effects of Stress on Mouse Prefrontal Cortex microRNA Expression. Ottawa: Carleton University.
50. Meerson, A., Cacheaux, L., Goosens, K. A., Sapolsky, R. M., Soreq, H., and Kaufer, D. (2010). Changes in brain MicroRNAs contribute to cholinergic stress reactions. J. Mol. Neurosci. 40, 47-55. doi: 10.1007/s12031-009-9252-1
51. Mishima, T., Mizuguchi, Y., Kawahigashi, Y., Takizawa, T., and Takizawa, T. (2007). RT-PCR-based analysis of microRNA (miR-1 and -124) expression in mouse CNS. Brain Res. 1131, 37-43. doi: 10.1016/j.brainres.2006.11.035
52. Mucaj, V., Lee, S. S., Skuli, N., Giannoukos, D. N., Qiu, B., Eisinger-Mathason, T. S., et al. (2014). MicroRNA-124 expression counteracts pro-survival stress responses in glioblastoma. Oncogene 34, 2204-2214. doi: 10.1038/onc.2014.168
53. Nadorp, B., and Soreq, H. (2014). Predicted overlapping microRNA regulators of acetylcholine packaging and degradation in neuroinflammation-related disorders. Front. Mol. Neurosci. 7:9. doi: 10.3389/fnmol.2014.00009
54. Noguchi, T., Makino, S., Matsumoto, R., Nakayama, S., Nishiyama, M., Terada, Y., et al. (2010). Regulation of glucocorticoid receptor transcription and nuclear translocation during single and repeated immobilization stress. Endocrinology 151, 4344-4355. doi: 10.1210/en.2010-0266
55. O’Connell, R. M., Rao, D. S., Chaudhuri, A. A., and Baltimore, D. (2010). Physiological and pathological roles for microRNAs in the immune system. Nat. Rev. Immunol. 10, 111-122. doi: 10.1038/nri2708
56. Pavlov, V. A., Wang, H., Czura, C. J., Friedman, S. G., and Tracey, K. J. (2003). The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol. Med. 9, 125-134.
57. Ponomarev, E. D., Veremeyko, T., Barteneva, N., Krichevsky, A. M., and Weiner, H. L. (2011). MicroRNA-124 promotes microglia quiescence and suppresses EAE by deactivating macrophages via the C/EBP-alpha-PU.1 pathway. Nat. Med. 17, 64-70. doi: 10.1038/nm.2266
58. 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
59. Sanuki, R., Onishi, A., Koike, C., Muramatsu, R., Watanabe, S., Muranishi, Y., et al. (2011). MiR-124a is required for hippocampal axogenesis and retinal cone survival through Lhx2 suppression. Nat. Neurosci. 14, 1125-1134. doi: 10.1038/nn.2897
60. Schumacher, S., and Franke, K. (2013). MiR-124-regulated RhoG: a conductor of neuronal process complexity. Small GTPases 4, 42-46. doi: 10.4161/sgtp.22922
61. Silber, J., Lim, D. A., Petritsch, C., Persson, A. I., Maunakea, A. K., Yu, M., 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
62. Smirnova, L., Grafe, 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
63. Smith, P., Al Hashimi, A., Girard, J., Delay, C., and Hebert, S. S. (2011). In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J. Neurochem. 116, 240-247. doi: 10.1111/j.1471-4159.2010.07097.x
64. Sonntag, K. C. (2010). MicroRNAs and deregulated gene expression networks in neurodegeneration. Brain Res. 1338, 48-57. doi: 10.1016/j.brainres.2010.03.106
65. Soreq, H., and Wolf, Y. (2011). NeurimmiRs: microRNAs in the neuroimmune interface. Trends Mol. Med. 17, 548-555. doi: 10.1016/j.molmed.2011.06.009
66. Sun, A., Koelsch, G., Tang, J., and Bing, G. (2002). Localization of beta-secretase memapsin 2 in the brain of Alzheimer’s patients and normal aged controls. Exp. Neurol. 175, 10-22. doi: 10.1006/exnr.2002.7875
67. Sun, Y., Gui, H., Li, Q., Luo, Z. M., Zheng, M. J., Duan, J. L., et al. (2013a). MicroRNA-124 protects neurons against apoptosis in cerebral ischemic stroke. CNS Neurosci. Ther. 19, 813-819. doi: 10.1111/cns.12142
68. Sun, Y., Li, Q., Gui, H., Xu, D. P., Yang, Y. L., Su, D. F., et al. (2013b). MicroRNA- 124 mediates the cholinergic anti-inflammatory action through inhibiting the production of pro-inflammatory cytokines. Cell Res. 23, 1270-1283. doi: 10.1038/cr.2013.116
69. Uchida, S., Hara, K., Kobayashi, A., Funato, H., Hobara, T., Otsuki, K., et al. (2010). Early life stress enhances behavioral vulnerability to stress through the activation of REST4-mediated gene transcription in the medial prefrontal cortex of rodents. J. Neurosci. 30, 15007-15018. doi: 10.1523/JNEUROSCI.1436-10.2010
70. 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
71. Vreugdenhil, E., Verissimo, C. S., Mariman, R., Kamphorst, J. T., Barbosa, J. S., Zweers, T., et al. (2009). MicroRNA 18 and 124a down-regulate the glucocorticoid receptor: implications for glucocorticoid responsiveness in the brain. Endocrinology 150, 2220-2228. doi: 10.1210/en.2008-1335
72. Wang, X., Wang, Z. H., Wu, Y. Y., Tang, H., Tan, L., Wang, X., et al. (2013). Melatonin attenuates scopolamine-induced memory/synaptic disorder by rescuing EPACs/miR-124/Egr1 pathway. Mol. Neurobiol. 47, 373-381. doi: 10.1007/s12035-012-8355-9
73. Weng, H., Shen, C., Hirokawa, G., Ji, X., Takahashi, R., Shimada, K., et al. (2011). Plasma miR-124 as a biomarker for cerebral infarction. Biomed. Res. 32, 135-141. doi: 10.2220/biomedres.32.135
74. Wiessner, C., Allegrini, P. R., Rupalla, K., Sauer, D., Oltersdorf, T., Mcgregor, A. L., et al. (1999). Neuron-specific transgene expression of Bcl-XL but not Bcl-2 genes reduced lesion size after permanent middle cerebral artery occlusion in mice. Neurosci. Lett. 268, 119-122. doi: 10.1016/S0304-3940(99)00392-4
75. Xia, H., Cheung, W. K., Ng, S. S., Jiang, X., Jiang, S., Sze, J., et al. (2012). Loss of brain-enriched miR-124 microRNA enhances stem-like traits and invasiveness of glioma cells. J. Biol. Chem. 287, 9962-9971. doi: 10.1074/jbc.M111.332627
76. Xie, Y. K., Huo, S. F., Zhang, G., Zhang, F., Lian, Z. P., Tang, X. L., et al. (2012). CDA-2 induces cell differentiation through suppressing Twist/SLUG signaling via miR-124 in glioma. J. Neurooncol. 110, 179-186. doi: 10.1007/s11060-012-0961-x
77. Xue, Y., Ouyang, K., Huang, J., Zhou, Y., Ouyang, H., Li, H., et al. (2013). Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits. Cell 152, 82-96. doi: 10.1016/j.cell.2012.11.045
78. Yang, L. B., Lindholm, K., Yan, R., Citron, M., Xia, W., Yang, X. L., et al. (2003). Elevated beta-secretase expression and enzymatic activity detected in sporadic Alzheimer disease. Nat. Med. 9, 3-4. doi: 10.1038/nm0103-3
79. Yang, Y., Shu, X., Liu, D., Shang, Y., Wu, Y., Pei, L., et al. (2012). EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73, 774-788. doi: 10.1016/j.neuron.2012.02.003
80. 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
81. Yu, J. Y., Chung, K. H., 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
82. Yuan, Y., Wang, J. Y., Xu, L. Y., Cai, R., Chen, Z., and Luo, B. Y. (2010). MicroRNA expression changes in the hippocampi of rats subjected to global ischemia. J. Clin. Neurosci. 17, 774-778. doi: 10.1016/j.jocn.2009.10.009
83. Zhang, P., Iwasaki-Arai, J., Iwasaki, H., Fenyus, M. L., Dayaram, T., Owens, B. M., et al. (2004). Enhancement of hematopoieticstem cell repopulatingcapacity and self-renewal in the absence of the transcription factor C/EBP alpha. Immunity 21, 853-863. doi: 10.1016/j.immuni.2004.11.006
84. Zhu, F., Liu, J. L., Li, J. P., Xiao, F., Zhang, Z. X., and Zhang, L. (2014). MicroRNA- 124 (miR-124) regulates Ku70 expression and is correlated with neuronal death induced by ischemia/reperfusion. J. Mol. Neurosci. 52, 148-155. doi: 10.1007/s12031-013-0155-9