Role of MicroRNA in Governing Synaptic Plasticity

Neural Plasticity

Volumn 2016, Issue , 2016, Pages

  Ye, Yuqin ^a,b   Xu, Hongyu ^a   Su, Xinhong ^a   He, Xiaosheng ^a  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b HUNAN NORMAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACYL PROTEIN THIOESTERASE 1; BRAIN DERIVED NEUROTROPHIC FACTOR; CAMP RESPONSE ELEMENT BINDING PROTEIN; FRAGILE X MENTAL RETARDATION PROTEIN; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; LIM KINASE 1; METHYL CPG BINDING PROTEIN 2; MICRORNA; MICRORNA 124; MICRORNA 125A; MICRORNA 125B; MICRORNA 132; MICRORNA 134; MICRORNA 138; MICRORNA 188; MICRORNA 212; MICRORNA 9; P250 GTPASE ACTIVATING PROTEIN; SIRTUIN 1; THIOL ESTER HYDROLASE; UNCLASSIFIED DRUG;

BIOGENESIS; GENE CONTROL; HUMAN; NERVE CELL PLASTICITY; NONHUMAN; REVIEW; ANIMAL; BRAIN; DENDRITIC SPINE; METABOLISM; PHYSIOLOGY;

ANIMALS; BRAIN; DENDRITIC SPINES; HUMANS; MICRORNAS; NEURONAL PLASTICITY;

EID: 84962695377     PISSN: 20905904     EISSN: 16875443     Source Type: Journal    
DOI: 10.1155/2016/4959523     Document Type: Review

References (126)

1. J. Wondolowski and D. Dickman, "Emerging links between homeostatic synaptic plasticity and neurological disease, " Frontiers in Cellular Neuroscience, vol. 7, article 223, 2013.
2. G. Turrigiano, "Homeostatic synaptic plasticity: local and global mechanisms for stabilizing neuronal function, " Cold Spring Harbor Perspectives in Biology, vol. 4, no. 1, Article ID a5736, 2012.
3. J. D. Richter, "RNA and the synapse, " RNA, vol. 21, no. 4, pp. 716-717, 2015.
4. C. Straub and B. L. Sabatini, "How to grow a synapse, " Neuron, vol. 82, no. 2, pp. 256-257, 2014.
5. E. Huntzinger and E. Izaurralde, "Gene silencing by microRNAs: contributions of translational repression and mRNA decay, " Nature Reviews Genetics, vol. 12, no. 2, pp. 99-110, 2011.
6. C. E. Holt and E. M. Schuman, "The central dogma decentralized: new perspectives on RNA function and local translation in neurons, " Neuron, vol. 80, no. 3, pp. 648-657, 2013.
7. D. Lenkala, E. R. Gamazon, B. LaCroix, H. K. Im, and R. S. Huang, "MicroRNA biogenesis and cellular proliferation, " Translational Research, vol. 166, no. 2, pp. 145-151, 2015.
8. E. M. Jobe, A. L. McQuate, and X. Zhao, "Crosstalk among epigenetic pathways regulates neurogenesis, " Frontiers in Neuroscience, vol. 6, article 59, 2012.
9. J. E. Cohen, P. R. Lee, S. Chen, W. Li, and R. D. Fields, "MicroRNA regulation of homeostatic synaptic plasticity, " Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 28, pp. 11650-11655, 2011.
10. R. Fiore, G. Siegel, and G. Schratt, "MicroRNA function in neuronal development, plasticity and disease, " Biochimica et BiophysicaActa (BBA)-Gene RegulatoryMechanisms, vol. 1779, no. 8, pp. 471-478, 2008.
11. Y. Lee, C. Ahn, J. Han et al., "The nuclear RNase III Drosha initiates microRNA processing, " Nature, vol. 425, no. 6956, pp. 415-419, 2003.
12. P. J. Kenny, H. Zhou, M. Kim et al., "MOV10 and FMRP regulate AGO2 association with microRNA recognition elements, " Cell Reports, vol. 9, no. 5, pp. 1729-1742, 2014.
13. W. Filipowicz, S. N. Bhattacharyya, and N. Sonenberg, "Mechanisms of post-transcriptional regulation by microRNAs: are the answers in sight?" Nature Reviews Genetics, vol. 9, no. 2, pp. 102-114, 2008.
14. A. Wilczynska and M. Bushell, "The complexity of miRNAmediated repression, " Cell Death and Differentiation, vol. 22, no. 1, pp. 22-33, 2015.
15. G. Mathonnet, M. R. Fabian, Y. V. Svitkin et al., "MicroRNA inhibition of translation initiation in vitro by targeting the capbinding complex eIF4F, " Science, vol. 317, no. 5845, pp. 1764-1767, 2007.
16. M. Xie and J. A. Steitz, "Versatile microRNA biogenesis in animals and their viruses, " RNA Biology, vol. 11, no. 6, pp. 673-681, 2014.
17. M. A. Havens, A. A. Reich, D. M. Duelli, and M. L. Hastings, "Biogenesis of mammalian microRNAs by a non-canonical processing pathway, " Nucleic Acids Research, vol. 40, no. 10, pp. 4626-4640, 2012.
18. J. G. Ruby, C. H. Jan, and D. P. Bartel, "Intronic microRNA precursors that bypass Drosha processing, " Nature, vol. 448, no. 7149, pp. 83-86, 2007.
19. R. Martin, P. Smibert, A. Yalcin et al., "A drosophila pasha mutant distinguishes the canonical microRNA and mirtron pathways, "Molecular and Cellular Biology, vol. 29, no. 3, pp. 861-870, 2009.
20. E. Ladewig, K. Okamura, A. S. Flynt, J. O. Westholm, and E. C. Lai, "Discovery of hundreds of mirtrons in mouse and human small RNAdata, " Genome Research, vol. 22, no. 9, pp. 1634-1645, 2012.
21. C. R. Sibley, Y. Seow, S. Saayman et al., "The biogenesis and characterization of mammalian microRNAs of mirtron origin, " Nucleic Acids Research, vol. 40, no. 1, pp. 438-448, 2012.
22. S. Stefanovic, G. J. Bassell, and M. R. Mihailescu, "G quadruplex RNA structures in PSD-95 mRNA: potential regulators of miR-125a seed binding site accessibility, " RNA, vol. 21, no. 1, pp. 48-60, 2015.
23. A. Suzuki, H. Fukushima, T. Mukawa et al., "Upregulation of CREB-mediated transcription enhances both short-and longterm memory, " The Journal of Neuroscience, vol. 31, no. 24, pp. 8786-8802, 2011.
24. N. Vo, M. E. Klein, O. Varlamova et al., "A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis, " Proceedings of the National Academy of Sciences of the United States of America, vol. 102, no. 45, pp. 16426-16431, 2005.
25. A. S. Nudelman, D. P. Dirocco, T. J. Lambert et al., "Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo, " Hippocampus, vol. 20, no. 4, pp. 492-498, 2010.
26. J. Guo, H. Wang, Q. Wang, Y. Chen, and S. Chen, "Expression of p-CREB and activity-dependent miR-132 in temporal lobe epilepsy, " International Journal of Clinical and Experimental Medicine, vol. 7, no. 5, pp. 1297-1306, 2014.
27. Y. Huang, J. Guo, Q. Wang, and Y. Chen, "MicroRNA-132 silencing decreases the spontaneous recurrent seizures, " International Journal of Clinical and Experimental Medicine, vol. 7, no. 7, pp. 1639-1649, 2014.
28. K. F. Hansen, K. Karelina, K. Sakamoto, G. A. Wayman, S. Impey, and K. Obrietan, "miRNA-132: a dynamic regulator of cognitive capacity, " Brain Structure and Function, vol. 218, no. 3, pp. 817-831, 2013.
29. H. L. Scott, F. Tamagnini, K. E. Narduzzo et al., "MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex, " European Journal of Neuroscience, vol. 36, no. 7, pp. 2941-2948, 2012.
30. H. Kawashima, T. Numakawa, E. Kumamaru et al., "Glucocorticoid attenuates brain-derived neurotrophic factor-dependent upregulation of glutamate receptors via the suppression of microRNA-132 expression, " Neuroscience, vol. 165, no. 4, pp. 1301-1311, 2010.
31. E. Kumamaru, T. Numakawa, N. Adachi et al., "Glucocorticoid prevents brain-derived neurotrophic factor-mediated maturation of synaptic function in developing hippocampal neurons through reduction in the activity of mitogen-activated protein kinase, " Molecular Endocrinology, vol. 22, no. 3, pp. 546-558, 2008.
32. T. Numakawa, E. Kumamaru, N. Adachi, Y. Yagasaki, A. Izumi, and H. Kunugi, "Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC signaling for glutamate release via a glutamate transporter, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 2, pp. 647-652, 2009.
33. S. Vaynman, Z. Ying, and F. Gomez-Pinilla, "Hippocampal BDNF mediates the efficacy of exercise on synaptic plasticity and cognition, " European Journal of Neuroscience, vol. 20, no. 10, pp. 2580-2590, 2004.
34. K. J. Marler, P. Suetterlin, A. Dopplapudi et al., "BDNF promotes axon branching of retinal ganglion cells via miRNA-132 and p250GAP, " The Journal of Neuroscience, vol. 34, no. 3, pp. 969-979, 2014.
35. G. A. Wayman, M. Davare, et al., "An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP, " Proceedings of the National Academy of Sciences of the United States of America, vol. 105, no. 26, pp. 9093-9098, 2008.
36. S. Impey, M. Davare, A. Lasiek et al., "An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling, " Molecular and Cellular Neuroscience, vol. 43, no. 1, pp. 146-156, 2010.
37. G. Shaltiel, M. Hanan, Y. Wolf et al., "Hippocampal microRNA-132 mediates stress-inducible cognitive deficits through its acetylcholinesterase target, " Brain Structure and Function, vol. 218, no. 1, pp. 59-72, 2013.
38. S. J. Kempf, S. Buratovic, C. von Toerne et al., "Ionising radiation immediately impairs synaptic plasticity-associated cytoskeletal signalling pathways in HT22 cells and in mouse brain: an in vitro/in vivo comparison study, " PLoS ONE, vol. 9, no. 10, Article ID e110464, 2014.
39. M. Dhar, M. Zhu, S. Impey et al., "Leptin induces hippocampal synaptogenesis via CREB-regulated MicroRNA-132 suppression of p250GAP, " Molecular Endocrinology, vol. 28, no. 7, pp. 1073-1087, 2014.
40. A. Lesiak, M. Zhu, H. Chenet al., "The environmental neurotoxicant PCB 95 promotes synaptogenesis via ryanodine receptordependent miR132 upregulation, " Journal of Neuroscience, vol. 34, no. 3, pp. 717-725, 2014.
41. A. L. Degano, M. J. Park, J. Penati, Q. Li, and G. V. Ronnett, "MeCP2 is required for activity-dependent refinement of olfactory circuits, " Molecular and Cellular Neuroscience, vol. 59, pp. 63-75, 2014.
42. K. F. Hansen, K. Sakamoto, G. A. Wayman, S. Impey, and K. Obrietan, "Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory, " PLoS ONE, vol. 5, no. 11, Article ID e15497, 2010.
43. J. Hernandez-Rapp, P. Y. Smith, M. Filali et al., "Memory formation and retention are affected in adult miR-132/212 knockout mice, " Behavioural Brain Research, vol. 287, pp. 15-26, 2015.
44. T. Fukuda, M. Itoh, T. Ichikawa, K. Washiyama, and Y.-I. Goto, "Delayed maturation of neuronal architecture and synaptogenesis in cerebral cortex of Mecp2-deficient mice, " Journal of Neuropathology and Experimental Neurology, vol. 64, no. 6, pp. 537-544, 2005.
45. Q. Chang, G. Khare, V. Dani, S. Nelson, and R. Jaenisch, "The disease progression of Mecp2 mutant mice is affected by the level of BDNF expression, " Neuron, vol. 49, no. 3, pp. 341-348, 2006.
46. H. Wu, J. Tao, P. J. Chen et al., "Genome-wide analysis revealsmethyl-CpG-binding protein 2-dependent regulation of microRNAs in amouse model of Rett syndrome, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 42, pp. 18161-18166, 2010.
47. R. Zhang, M. Huang, Z. Cao, J. Qi, Z. Qiu, and L. Chiang, "MeCP2 plays an analgesic role in pain transmission through regulating CREB/miR-132 pathway, " Molecular Pain, vol. 11, no. 1, article 19, 2015.
48. M. E. Klein, D. T. Lioy, L. Ma, S. Impey, G. Mandel, and R. H. Goodman, "Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA, " Nature Neuroscience, vol. 10, no. 12, pp. 1513-1514, 2007.
49. P. Jin, D. C. Zarnescu, S. Ceman et al., "Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway, " Nature Neuroscience, vol. 7, no. 2, pp. 113-117, 2004.
50. I. Napoli, V. Mercaldo, P. P. Boyl et al., "The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP, " Cell, vol. 134, no. 6, pp. 1042-1054, 2008.
51. D. Edbauer, J. R. Neilson, K. A. Foster et al., "Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132, " Neuron, vol. 65, no. 3, pp. 373-384, 2010.
52. I. P. Sudhakaran, J. Hillebrand, A. Dervan et al., "FMRP and Ataxin-2 function together in long-term olfactory habituation and neuronal translational control, " Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 1, pp. E99-E108, 2014.
53. F. Sethna, C. Moon, and H. Wang, "From FMRP function to potential therapies for fragile X syndrome, " Neurochemical Research, vol. 39, no. 6, pp. 1016-1031, 2014.
54. P. Tognini and T. Pizzorusso, "MicroRNA212/132 family:molecular transducer of neuronal function and plasticity, " International Journal of Biochemistry & Cell Biology, vol. 44, no. 1, pp. 6-10, 2012.
55. K. Wibrand, D. Panja, A. Tiron et al., "Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo, " European Journal of Neuroscience, vol. 31, no. 4, pp. 636-645, 2010.
56. J. Remenyi, M. W. M. van den Bosch, O. Palygin et al., "MiR-132/212 knockout mice reveal roles for these miRNAs in regulating cortical synaptic transmission and plasticity, " PLoS ONE, vol. 8, no. 4, Article ID e62509, 2013.
57. S. T. Magill, X. A. Cambronne, B. W. Luikart et al., "MicroRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus, " Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 47, pp. 20382-20387, 2010.
58. B. W. Luikart, A. L. Bensen, E. K. Washburn et al., "MiR-132 mediates the integration of newborn neurons into the adult dentate gyrus, " PLoS ONE, vol. 6, no. 5, Article ID e19077, 2011.
59. J.-Y. Hwang, N. Kaneko, K.-M. Noh, F. Pontarelli, and R. S. Zukin, "The gene silencing transcription factor rest represses miR-132 expression in hippocampal neurons destined to die, " Journal of Molecular Biology, vol. 426, no. 20, pp. 3454-3466, 2014.
60. P. Tognini, E. Putignano, A. Coatti, and T. Pizzorusso, "Experience-dependent expression of miR-132 regulates ocular dominance plasticity, " Nature Neuroscience, vol. 14, no. 10, pp. 1237-1239, 2011.
61. N. Mellios, H. Sugihara, J. Castro et al., "MiR-132, an experiencedependent microRNA, is essential for visual cortex plasticity, " Nature Neuroscience, vol. 14, no. 10, pp. 1240-1242, 2011.
62. J. F. Maya-Vetencourt and T. Pizzorusso, "Molecular mechanisms at the basis of plasticity in the developing visual cortex: epigenetic processes and gene programs, " Journal of Experimental Neuroscience, vol. 7, pp. 75-83, 2013.
63. S. Bicker, S. Khudayberdiev, K. Weiß, K. Zocher, S. Baumeister, and G. Schratt, "The DEAH-box helicase DHX36 mediates dendritic localization of the neuronal precursor-microRNA-134, " Genes & Development, vol. 27, no. 9, pp. 991-996, 2013.
64. J. Gao, W.-Y. Wang, Y.-W. Mao et al., "A novel pathway regulates memory and plasticity via SIRT1 and miR-134, " Nature, vol. 466, no. 7310, pp. 1105-1109, 2010.
65. H. Siemen, D. Colas, H. C. Heller, O. Brüstle, and R. A. Pera, "Pumilio-2 function in the mouse nervous system, " PLoS ONE, vol. 6, no. 10, Article ID e25932, 2011.
66. G. M. Schratt, F. Tuebing, E. A. Nigh et al., "A brain-specific microRNA regulates dendritic spine development, " Nature, vol. 439, no. 7074, pp. 283-289, 2006.
67. M. Christensen, L. A. Larsen, S. Kauppinen, and G. Schratt, "Recombinant adeno-associated virus-mediated microRNA delivery into the postnatal mouse brain reveals a role for miR-134 in dendritogenesis in vivo, " Frontiers in Neural Circuits, vol. 3, article no. 16, 2010.
68. O. Bernard, "Lim kinases, regulators of actin dynamics, " The International Journal of Biochemistry & Cell Biology, vol. 39, no. 6, pp. 1071-1076, 2007.
69. Y. Meng, Y. Zhang, V. Tregoubov, D. L. Falls, and Z. Jia, "Regulation of spine morphology and synaptic function by LIMKand the actin cytoskeleton, " Reviews in the Neurosciences, vol. 14, no. 3, pp. 233-240, 2003.
70. Q. Dong, Y.-S. Ji, C. Cai, and Z.-Y. Chen, "LIM Kinase 1 (LIMK1) interacts with Tropomyosin-related Kinase B (TrkB) and mediates Brain-Derived Neurotrophic Factor (BDNF)-induced axonal elongation, " Journal of Biological Chemistry, vol. 287, no. 50, pp. 41720-41731, 2012.
71. G. Leal, D. Comprido, and C. B. Duarte, "BDNF-induced local protein synthesis and synaptic plasticity, " Neuropharmacology, vol. 76, pp. 639-656, 2014.
72. S. Chai, X. A. Cambronne, S. W. Eichhorn, andR. H. Goodman, "MicroRNA-134 activity in somatostatin interneurons regulates H-Ras localization by repressing the palmitoylation enzyme, DHHC9, " Proceedings of the National Academy of Sciences of the United States of America, vol. 110, no. 44, pp. 17898-17903, 2013.
73. T. Arendt, U. Gärtner, G. Seeger et al., "Neuronal activation of Ras regulates synaptic connectivity, " European Journal of Neuroscience, vol. 19, no. 11, pp. 2953-2966, 2004.
74. E. M. Jimenez-Mateos, T. Engel, P. Merino-Serrais et al., "Silencing microRNA-134 produces neuroprotective and prolonged seizure-suppressive effects, " Nature Medicine, vol. 18, no. 7, pp. 1087-1094, 2012.
75. J. Peng, A. Omran, M. U. Ashhab et al., "Expression patterns of miR-124, miR-134, miR-132, and miR-21 in an immature rat model and children with mesial temporal lobe epilepsy, " Journal of Molecular Neuroscience, vol. 50, no. 2, pp. 291-297, 2013.
76. Y. Zhu, C. Li, Y. Wang, and S. Zhou, "Change ofMicroRNA-134, CREB and p-CREB expression in epileptic rat, " Asian Pacific Journal of Tropical Medicine, vol. 8, no. 4, pp. 292-298, 2015.
77. G. Siegel, G. Obernosterer, R. Fiore et al., "A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis, " Nature Cell Biology, vol. 11, no. 6, pp. 705-716, 2009.
78. M. Bak, A. Silahtaroglu, M. Møller et al., "MicroRNAexpression in the adult mouse central nervous system, " RNA, vol. 14, no. 3, pp. 432-444, 2008.
79. J. Schröder, S. Ansaloni, M. Schilling et al., "MicroRNA-138 is a potential regulator of memory performance in humans, " Frontiers in Human Neuroscience, vol. 8, article 501, 2014.
80. E. T. Tatro, V. Risbrough, B. Soontornniyomkij et al., "Shorttermrecognitionmemory correlates with regional CNS expression of microRNA-138 in mice, " The American Journal of Geriatric Psychiatry, vol. 21, no. 5, pp. 461-473, 2013.
81. C.-M. Liu, R.-Y. Wang, Saijilafu, Z.-X. Jiao, B.-Y. Zhang, and F.-Q. Zhou, "MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration, " Genes & Development, vol. 27, no. 13, pp. 1473-1483, 2013.
82. S. A. Giusti, A. M. Vogl, M. M. Brockmann et al., "MicroRNA-9 controls dendritic development by targeting REST, " eLife, vol. 3, Article ID e02755, 2014.
83. G. Garaffo, D. Conte, P. Proveroet al., "TheDlx5 andFoxg1 transcription factors, linked via miRNA-9 and-200, are required for the development of the olfactory and GnRH system, "Molecular and Cellular Neuroscience, vol. 68, pp. 103-119, 2015.
84. M. C. Siomi, H. Siomi, W. H. Sauer, S. Srinivasan, R. L. Nussbaum, and G. Dreyfuss, "FXR1, an autosomal homolog of the fragile X mental retardation gene, " The EMBO Journal, vol. 14, no. 11, pp. 2401-2408, 1995.
85. X.-L. Xu, R. Zong, Z. Li et al., "Fxr1p but not fmrp regulates the levels of mammalian brain-specific microrna-9 and microrna-124, " Journal of Neuroscience, vol. 31, no. 39, pp. 13705-13709, 2011.
86. J. P. Cogswell, J. Ward, I. A. Taylor et al., "Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways, " Journal of Alzheimer's Disease, vol. 14, no. 1, pp. 27-41, 2008.
87. G. Mairet-Coello, J. Courchet, S. Pieraut, V. Courchet, A. Maximov, and F. Polleux, "The CAMKK2-AMPK kinase pathway mediates the synaptotoxic effects of A oligomers through Tau phosphorylation, " Neuron, vol. 78, no. 1, pp. 94-108, 2013.
88. A. Nakano and S. Takashima, "LKB1 andAMP-activated protein kinase: regulators of cell polarity, " Genes to Cells, vol. 17, no. 9, pp. 737-747, 2012.
89. F. Chang, L.-H. Zhang, W. U.-P. Xu, P. Jing, and P.-Y. Zhan, "microRNA-9 attenuates amyloid-induced synaptotoxicity by targeting calcium/calmodulin-dependent protein kinase kinase 2, "MolecularMedicine Reports, vol. 9, no. 5, pp. 1917-1922, 2014.
90. X. Wang, L. Tan, Y. Lu et al., "MicroRNA-138 promotes tau phosphorylation by targeting retinoic acid receptor alpha, " FEBS Letters, vol. 589, no. 6, pp. 726-729, 2015.
91. H. Soreq and Y. Wolf, "NeurimmiRs: microRNAs in the neuroimmune interface, " Trends in Molecular Medicine, vol. 17, no. 10, pp. 548-555, 2011.
92. P. Rajasethupathy, F. Fiumara, R. Sheridan et al., "Characterization of small RNAs in aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB, " Neuron, vol. 63, no. 6, pp. 803-817, 2009.
93. S. Schumacher and K. Franke, "miR-124-regulated RhoG: a conductor of neuronal process complexity, " Small GTPases, vol. 4, no. 1, pp. 42-46, 2013.
94. K. Franke, W. Otto, S. Johannes, J. Baumgart, R. Nitsch, and S. Schumacher, "miR-124-regulated RhoG reduces neuronal process complexity via ELMO/Dock180/Rac1 and Cdc42 signalling, " The EMBO Journal, vol. 31, no. 13, pp. 2908-2921, 2012.
95. H. Katoh and M. Negishi, "RhoG activates Rac1 by direct interaction with the Dock180-binding protein Elmo, " Nature, vol. 424, no. 6947, pp. 461-464, 2003.
96. L. Yang, R. Zhang, M. Li et al., "A functional MiR-124 bindingsite polymorphism in IQGAP1 affects human cognitive performance, " PLoS ONE, vol. 9, no. 9, Article ID e107065, 2014.
97. C. Gao, S. F. Frausto, A. L. Guedea et al., "IQGAP1 regulates NR2A signaling, spine density, and cognitive processes, " Journal of Neuroscience, vol. 31, no. 23, pp. 8533-8542, 2011.
98. R. Dutta, A. M. Chomyk, A. Chang et al., "Hippocampal demyelination and memory dysfunction are associated with increased levels of the neuronal microRNA miR-124 and reduced AMPA receptors, " Annals of Neurology, vol. 73, no. 5, pp. 637-645, 2013.
99. V. Chandrasekar and J.-L. Dreyer, "microRNAs miR-124, let-7d and miR-181a regulate Cocaine-induced Plasticity, " Molecular and Cellular Neuroscience, vol. 42, no. 4, pp. 350-362, 2009.
100. W. Xu, O. M. Schlüter, P. Steiner, B. L. Czervionke, B. Sabatini, and R. C. Malenka, "Molecular dissociation of the role of PSD-95 in regulating synaptic strength and LTD, " Neuron, vol. 57, no. 2, pp. 248-262, 2008.
101. R. S. Muddashetty, V. C. Nalavadi, C. Gross et al., "Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, andmGluR signaling, "Molecular Cell, vol. 42, no. 5, pp. 673-688, 2011.
102. F. Zalfa, B. Eleuteri, K. S. Dickson et al., "A new function for the fragile Xmental retardation protein in regulation of PSD-95 mRNAstability, " Nature Neuroscience, vol. 10, no. 5, pp. 578-587, 2007.
103. R. Anwyl, "Metabotropic glutamate receptor-dependent longterm potentiation, " Neuropharmacology, vol. 56, no. 4, pp. 735-740, 2009.
104. P. J. Yao, M. Zhu, E. I. Pyun et al., "Defects in expression of genes related to synaptic vesicle trafficking in frontal cortex of Alzheimer's disease, " Neurobiology of Disease, vol. 12, no. 2, pp. 97-109, 2003.
105. J. Banzhaf-Strathmann, E. Benito, S. May et al., "MicroRNA-125b induces tau hyperphosphorylation and cognitive deficits in Alzheimer's disease, " EMBO Journal, vol. 33, no. 15, pp. 1667-1680, 2014.
106. W. J. Lukiw and P. N. Alexandrov, "Regulation of complement factor H (CFH) by multiple miRNAs in Alzheimer's disease (AD) brain, " Molecular Neurobiology, vol. 46, no. 1, pp. 11-19, 2012.
107. R. P. Kruger, J. Aurandt, and K.-L. Guan, "Semaphorins command cells tomove, " Nature ReviewsMolecular Cell Biology, vol. 6, no. 10, pp. 789-800, 2005.
108. K. Lee, J.-H. Kim, O.-B. Kwon et al., "An activity-regulated microRNA, miR-188, controls dendritic plasticity and synaptic transmission by downregulating neuropilin-2, " The Journal of Neuroscience, vol. 32, no. 16, pp. 5678-5687, 2012.
109. J. Zhang, M. Hu, Z. Teng, Y.-P. Tang, and C. Chen, "Synaptic and cognitive improvements by inhibition of 2-AG metabolism are through upregulation of microRNA-188-3p in a mouse model of Alzheimer's disease, " Journal of Neuroscience, vol. 34, no. 45, pp. 14919-14933, 2014.
110. C. S. Lu, B. Zhai, A. Mauss, M. Landgraf, S. Gygi, and D. Van Vactor, "MicroRNA-8 promotes robust motor axon targeting by coordinate regulation of cell adhesion molecules during synapse development, " Philosophical Transactions of the Royal Society B: Biological Sciences, vol. 369, no. 1652, article 517, 2014.
111. C. M. Loya, E. M. McNeill, H. Bao, B. Zhang, andD. Van Vactor, "miR-8 controls synapse structure by repression of the actin regulator Enabled, " Development, vol. 141, no. 9, pp. 1864-1874, 2014.
112. Y. Gao, J. Su, W. Guo et al., "Inhibition of miR-15a promotes BDNF expression and rescues dendritic maturation deficits in MeCP2-deficient neurons, " Stem Cells, vol. 33, no. 5, pp. 1618-1629, 2015.
113. M. J. Kye, P. Neveu, Y.-S. Lee et al., "NMDAmediated contextual conditioning changes miRNAexpression, " PLoSONE, vol. 6, no. 9, Article ID e24682, 2011.
114. F. Fiumara, P. Rajasethupathy, I. Antonov, S. Kosmidis, W. S. Sossin, and E. R. Kandel, "MicroRNA-22 gates long-term heterosynaptic plasticity in aplysia through presynaptic regulation of CPEB and downstream targets, " Cell Reports, vol. 11, no. 12, pp. 1866-1875, 2015.
115. Q. Gu, D. Yu, Z. Hu et al., "miR-26a and miR-384-5p are required for LTP maintenance and spine enlargement, " Nature Communications, vol. 6, article 6789, 2015.
116. B. Li and H. Sun, "MiR-26a promotes neurite outgrowth by repressing PTEN expression, " Molecular Medicine Reports, vol. 8, no. 2, pp. 676-680, 2013.
117. G. Lippi, J. R. Steinert, E. L. Marczylo et al., "Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology, " The Journal of Cell Biology, vol. 194, no. 6, pp. 889-904, 2011.
118. V. O. Pustylnyak, P. D. Lisachev, and M. B. Shtark, "Expression of p53 target genes in the early phase of long-term potentiation in the rat hippocampal CA1 area, " Neural Plasticity, vol. 2015, Article ID 242158, 12 pages, 2015.
119. M. Agostini, P. Tucci, J. R. Steinert et al., "microRNA-34a regulates neurite outgrowth, spinal morphology, and function, " Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 52, pp. 21099-21104, 2011.
120. K. Wibrand, B. Pai, T. Siripornmongcolchai et al., "MicroRNA regulation of the synaptic plasticity-related gene Arc, " PLoS ONE, vol. 7, no. 7, Article ID e41688, 2012.
121. E. Franzoni, S. A. Booker, S. Parthasarathy et al., "miR-128 regulates neuronal migration, outgrowth and intrinsic excitability via the intellectual disability gene Phf6, " ELife, vol. 4, Article ID e04263, 2015.
122. R. D. Smrt, K. E. Szulwach, R. L. Pfeiffer et al., "MicroRNA miR-137 regulates neuronal maturation by targeting ubiquitin ligase mind bomb-1, " Stem Cells, vol. 28, no. 6, pp. 1060-1070, 2010.
123. E. M. Griggs, E. J. Young, G. Rumbaugh, and C. A. Miller, "MicroRNA-182 regulates amygdala-dependent memory formation, " The Journal of Neuroscience, vol. 33, no. 4, pp. 1734-1740, 2013.
124. Z. Hu, D. Yu, Q.-H. Gu et al., "MiR-191 and miR-135 are required for long-lasting spine remodelling associated with synaptic long-term depression, " Nature Communications, vol. 5, article 3263, 2014.
125. H. Rong, T. B. Liu, K. J. Yang et al., "MicroRNA-134 plasma levels before and after treatment for bipolar mania, " Journal of Psychiatric Research, vol. 45, no. 1, pp. 92-95, 2011.
126. D. W. Hwang, S. Son, J. Jang et al., "Abrain-targeted rabies virus glycoprotein-disulfide linked PEI nanocarrier for delivery of neurogenic microRNA, " Biomaterials, vol. 32, no. 21, pp. 4968-4975, 2011.