Selective distribution and dynamic modulation of miRNAs in the synapse and its possible role in Alzheimer's Disease

Brain Research

Volumn 1584, Issue , 2014, Pages 80-93

  Garza Manero, Sylvia ^a   Pichardo Casas, Israel ^b   Arias, Clorinda ^a   Vaca, Luis ^b   Zepeda, Angélica ^a  

^a UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

^b INSTITUTO DE FISIOLOGÍA CELULAR   (Mexico)

Author keywords

Brain; Hippocampus; Hyperexcitation; Neural plasticity; Neurodegeneration; Posttransciptional modification; Synaptoneurosome

Indexed keywords

ARGONAUTE 2 PROTEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; EXONUCLEASE; HEAT SHOCK COGNATE PROTEIN 70; HEAT SHOCK PROTEIN 90; MESSENGER RNA; MICRORNA; MICRORNA 125A; MICRORNA 132; MICRORNA 134; MICRORNA 138; MICRORNA 145; MICRORNA 150; MICRORNA 34A; MICRORNA 9; SINGLE STRANDED RNA; UNCLASSIFIED DRUG;

3' UNTRANSLATED REGION; ACTIN POLYMERIZATION; ALZHEIMER DISEASE; ARTICLE; BRAIN CORTEX; BRAIN STEM; CEREBELLUM; GENE SILENCING; HIPPOCAMPUS; NERVE CELL PLASTICITY; OLFACTORY BULB; POSTTRANSCRIPTIONAL GENE SILENCING; PROTEIN SYNTHESIS; RNA DEGRADATION; RNA PROCESSING; SYNAPSE; BRAIN; GENETICS; HUMAN; METABOLISM; PATHOLOGY; PHYSIOLOGY; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ALZHEIMER DISEASE; BRAIN; HUMANS; MICRORNAS; NEURONAL PLASTICITY; RNA INTERFERENCE; RNA PROCESSING, POST-TRANSCRIPTIONAL; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84907680730     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2013.12.009     Document Type: Article

References (129)

1. V. Ambros The functions of animal microRNAs Nature 431 2004 350 355
2. S.L. Ameres, and P.D. Zamore Diversifying microRNA sequence and function Nat. Rev. Mol. Cell Biol. 14 2013 475 488
3. T. Arendt Synaptic degeneration in Alzheimer's disease Acta Neuropathol. 118 2009 167 179
4. S.I. Ashraf, A.L. McLoon, S.M. Sclarsic, and S. Kunes Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila Cell 124 2006 191 205
5. M. Bak, A. Silahtaroglu, M. Moller, M. Christensen, M.F. Rath, B. Skryabin, N. Tommerup, and S. Kauppinen MicroRNA expression in the adult mouse central nervous system RNA 14 2008 432 444
6. S. Banerjee, P. Neveu, and K.S. Kosik A coordinated local translational control point at the synapse involving relief from silencing and MOV10 degradation Neuron 64 2009 871 884
7. D.P. Bartel MicroRNAs: target recognition and regulatory functions Cell 136 2009 215 233
8. G.J. Bassell, and S.T. Warren Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function Neuron 60 2008 201 214
9. E.M. Batassa, M. Costanzi, D. Saraulli, R. Scardigli, C. Barbato, C. Cogoni, and V. Cestari RISC activity in hippocampus is essential for contextual memory Neurosci. Lett. 471 2010 185 188
10. S.N. Bhattacharyya, R. Habermacher, U. Martine, E.I. Closs, and W. Filipowicz Relief of microRNA-mediated translational repression in human cells subjected to stress Cell 125 2006 1111 1124
11. 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 Dev. 27 2013 991 996
12. A. Blichenberg, B. Schwanke, M. Rehbein, C.C. Garner, D. Richter, and S. Kindler Identification of a cis-acting dendritic targeting element in MAP2 mRNAs J. Neurosci. 19 1999 8818 8829
13. T.M. Bockers, M. Segger-Junius, P. Iglauer, J. Bockmann, E.D. Gundelfinger, M.R. Kreutz, D. Richter, S. Kindler, and H.J. Kreienkamp Differential expression and dendritic transcript localization of Shank family members: identification of a dendritic targeting element in the 3' untranslated region of Shank1 mRNA Mol. Cell Neurosci. 26 2004 182 190
14. H. Braak, E. Braak, J. Peter, and J.H. Morrison Temporal sequence of Alzheimer's disease related pathology A. Peters, J.H. Morrison, Cerebral Cortex. Vol. Neurodegenerative and Age-Related Changes in Structure and Function of Cerebral Cortex 1999 Kluwer Academic, Plenum Publishers New York 475 512
15. M. Brengues, D. Teixeira, and R. Parker Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies Science 310 2005 486 489
16. J.P. Cogswell, J. Ward, I.A. Taylor, M. Waters, Y. Shi, B. Cannon, K. Kelnar, J. Kemppainen, D. Brown, C. Chen, R.K. Prinjha, J.C. Richardson, A.M. Saunders, A.D. Roses, and C.A. Richards Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways J. Alzheimers Dis. 14 2008 27 41
17. B. Connor, D. Young, Q. Yan, R.L. Faull, B. Synek, and M. Dragunow Brain-derived neurotrophic factor is reduced in Alzheimer's disease Brain Res. Mol. Brain Res. 49 1997 71 81
18. H.A. Cook, B.S. Koppetsch, J. Wu, and W.E. Theurkauf The Drosophila SDE3 homolog armitage is required for oskar mRNA and embryonic axis specification Cell 116 2004 817 829
19. N. Cougot, S.N. Bhattacharyya, L. Tapia-Arancibia, R. Bordonne, W. Filipowicz, E. Bertrand, and F. Rage Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation J Neurosci. 28 2008 13793 13804
20. S.E. Counts, M. Nadeem, S.P. Lad, J. Wuu, and E.J. Mufson Differential expression of synaptic proteins in the frontal and temporal cortex of elderly subjects with mild cognitive impairment J. Neuropathol. Exp. Neurol. 65 2006 592 601
21. V. Chandrasekar, and J.L. Dreyer microRNAs miR-124, let-7d and miR-181a regulate cocaine-induced plasticity Mol. Cell Neurosci. 42 2009 350 362
22. 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
23. J.C. Chuang, and P.A. Jones Epigenetics and microRNAs Pediatr. Res. 61 2007 24R 29R
24. C.A. Davies, D.M. Mann, P.Q. Sumpter, and P.O. Yates A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease J. Neurol. Sci. 78 1987 151 164
25. C.J. Davis, S.G. Bohnet, J.M. Meyerson, and J.M. Krueger Sleep loss changes microRNA levels in the brain: a possible mechanism for state-dependent translational regulation Neurosci. Lett. 422 2007 68 73
26. S.T. DeKosky, and S.W. Scheff Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity Ann. Neurol. 27 1990 457 464
27. S.T. DeKosky, S.W. Scheff, and S.D. Styren Structural correlates of cognition in dementia: quantification and assessment of synapse change Neurodegeneration 5 1996 417 421
28. J.G. Doench, and P.A. Sharp Specificity of microRNA target selection in translational repression Genes Dev. 18 2004 504 511
29. D. Edbauer, J.R. Neilson, K.A. Foster, C.F. Wang, D.P. Seeburg, M.N. Batterton, T. Tada, B.M. Dolan, P.A. Sharp, and M. Sheng Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132 Neuron 65 2010 373 384
30. M.R. Fabian, N. Sonenberg, and W. Filipowicz Regulation of mRNA translation and stability by microRNAs Annu. Rev. Biochem. 79 2010 351 379
31. Y. Feng, C.A. Gutekunst, D.E. Eberhart, H. Yi, S.T. Warren, and S.M. Hersch Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes J. Neurosci. 17 1997 1539 1547
32. W. Filipowicz, L. Jaskiewicz, F.A. Kolb, and R.S. Pillai Post-transcriptional gene silencing by siRNAs and miRNAs Curr. Opin. Struct. Biol. 15 2005 331 341
33. R. Fiore, S. Khudayberdiev, M. Christensen, G. Siegel, S.W. Flavell, T.K. Kim, M.E. Greenberg, and G. Schratt Mef2-mediated transcription of the miR379-410 cluster regulates activity-dependent dendritogenesis by fine-tuning Pumilio2 protein levels EMBO J. 28 2009 697 710
34. J. Gao, W.Y. Wang, Y.W. Mao, J. Graff, J.S. Guan, L. Pan, G. Mak, D. Kim, S.C. Su, and L.H. Tsai A novel pathway regulates memory and plasticity via SIRT1 and miR-134 Nature 466 2010 1105 1109
35. A. Ghosh, J. Carnahan, and M.E. Greenberg Requirement for BDNF in activity-dependent survival of cortical neurons Science 263 1994 1618 1623
36. 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
37. A.M. Gurtan, and P.A. Sharp The role of miRNAs in regulating gene expression networks J. Mol. Biol. 425 2013 3582 3600
38. J.E. Hamos, L.J. DeGennaro, and D.A. Drachman Synaptic loss in Alzheimer's disease and other dementias Neurology 39 1989 355 361
39. 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 5 2010 e15497
40. J. Hardy, and D.J. Selkoe The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics Science 297 2002 353 356
41. Y. Harigaya, M. Shoji, T. Shirao, and S. Hirai Disappearance of actin-binding protein, drebrin, from hippocampal synapses in Alzheimer's disease J. Neurosci. Res. 43 1996 87 92
42. K. Hatanpaa, K.R. Isaacs, T. Shirao, D.R. Brady, and S.I. Rapoport Loss of proteins regulating synaptic plasticity in normal aging of the human brain and in Alzheimer disease J. Neuropathol. Exp. Neurol. 58 1999 637 643
43. M. He, Y. Liu, X. Wang, M.Q. Zhang, G.J. Hannon, and Z.J. Huang Cell-type-based analysis of microRNA profiles in the mouse brain Neuron 73 2012 35 48
44. O. Heinonen, H. Soininen, H. Sorvari, O. Kosunen, L. Paljarvi, E. Koivisto, and P.J. Riekkinen Sr. Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease Neuroscience 64 1995 375 384
45. A. Helwak, G. Kudla, T. Dudnakova, and D. Tollervey Mapping the human miRNA interactome by CLASH reveals frequent noncanonical binding Cell 153 2013 654 665
46. U. Hengst, L.J. Cox, E.Z. Macosko, and S.R. Jaffrey Functional and selective RNA interference in developing axons and growth cones J. Neurosci. 26 2006 5727 5732
47. K. Hernandez-Ortega, R. Quiroz-Baez, and C. Arias Cell cycle reactivation in mature neurons: a link with brain plasticity, neuronal injury and neurodegenerative diseases? Neurosci. Bull. 27 2011 185 196
48. H.Y. Hu, S. Guo, J. Xi, Z. Yan, N. Fu, X. Zhang, C. Menzel, H. Liang, H. Yang, M. Zhao, R. Zeng, W. Chen, S. Paabo, and P. Khaitovich MicroRNA expression and regulation in human, chimpanzee, and macaque brains PLoS Genet. 7 2011 e1002327
49. E. Huntzinger, and E. Izaurralde Gene silencing by microRNAs: contributions of translational repression and mRNA decay Nat. Rev. Genet. 12 2011 99 110
50. S. Impey, M. Davare, A. Lesiak, D. Fortin, H. Ando, O. Varlamova, K. Obrietan, T.R. Soderling, R.H. Goodman, and G.A. Wayman An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling Mol. Cell Neurosci. 43 2012 146 156
51. S. Iwasaki, M. Kobayashi, M. Yoda, Y. Sakaguchi, S. Katsuma, T. Suzuki, and Y. Tomari Hsc70/Hsp90 chaperone machinery mediates ATP-dependent RISC loading of small RNA duplexes Mol. Cell. 39 2010 292 299
52. P. Jin, R.S. Alisch, and S.T. Warren RNA and microRNAs in fragile X mental retardation Nat. Cell Biol. 6 2004 1048 1053
53. P. Jin, D.C. Zarnescu, S. Ceman, M. Nakamoto, J. Mowrey, T.A. Jongens, D.L. Nelson, K. Moses, and S.T. Warren Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway Nat. Neurosci. 7 2004 113 117
54. M. Johnston, M.C. Geoffroy, A. Sobala, R. Hay, and G. Hutvagner HSP90 protein stabilizes unloaded argonaute complexes and microscopic P-bodies in human cells Mol. Biol. Cell. 21 2010 1462 1469
55. H. Jung, B.C. Yoon, and C.E. Holt Axonal mRNA localization and local protein synthesis in nervous system assembly, maintenance and repair Nat. Rev. Neurosci. 13 2012 308 324
56. A. Junker Pathophysiology of translational regulation by microRNAs in multiple sclerosis FEBS Lett. 585 2011 3738 3746
57. H. Kang, and E.M. Schuman A requirement for local protein synthesis in neurotrophin-induced hippocampal synaptic plasticity Science 273 1996 1402 1406
58. M. Katakowski, B. Buller, X. Wang, T. Rogers, and M. Chopp Functional microRNA is transferred between glioma cells Cancer Res. 70 2010 8259 8263
59. S. Kindler, H. Wang, D. Richter, and H. Tiedge RNA transport and local control of translation Annu. Rev. Cell Dev. Biol. 21 2005 223 245
60. 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 Nat. Neurosci. 10 2007 1513 1514
61. A. Konecna, J.E. Heraud, L. Schoderboeck, A.A. Raposo, and M.A. Kiebler What are the roles of microRNAs at the mammalian synapse? Neurosci. Lett 466 2009 63 68
62. W. Konopka, A. Kiryk, M. Novak, M. Herwerth, J.R. Parkitna, M. Wawrzyniak, A. Kowarsch, P. Michaluk, J. Dzwonek, T. Arnsperger, G. Wilczynski, M. Merkenschlager, F.J. Theis, G. Kohr, L. Kaczmarek, and G. Schutz MicroRNA loss enhances learning and memory in mice J. Neurosci. 30 2010 14835 14842
63. M. Korte, P. Carroll, E. Wolf, G. Brem, H. Thoenen, and T. Bonhoeffer Hippocampal long-term potentiation is impaired in mice lacking brain-derived neurotrophic factor Proc. Natl. Acad. Sci. USA 92 1995 8856 8860
64. K.S. Kosik The neuronal microRNA system Nat. Rev. Neurosci. 7 2006 911 920
65. A.M. Krichevsky, K.S. King, C.P. Donahue, K. Khrapko, and K.S. Kosik A microRNA array reveals extensive regulation of microRNAs during brain development RNA 9 2003 1274 1281
66. M.J. Kye, T. Liu, S.F. Levy, N.L. Xu, B.B. Groves, R. Bonneau, K. Lao, and K.S. Kosik Somatodendritic microRNAs identified by laser capture and multiplex RT-PCR RNA 13 2007 1224 1234
67. G. Lachenal, K. Pernet-Gallay, M. Chivet, F.J. Hemming, A. Belly, G. Bodon, B. Blot, G. Haase, Y. Goldberg, and R. Sadoul Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity Mol. Cell Neurosci. 46 2011 409 418
68. M. Lagos-Quintana, R. Rauhut, A. Yalcin, J. Meyer, W. Lendeckel, and T. Tuschl Identification of tissue-specific microRNAs from mouse Curr. Biol. 12 2002 735 739
69. P. Landgraf, M. Rusu, R. Sheridan, A. Sewer, N. Iovino, A. Aravin, S. Pfeffer, A. Rice, A.O. Kamphorst, M. Landthaler, C. Lin, N.D. Socci, L. Hermida, V. Fulci, S. Chiaretti, R. Foa, J. Schliwka, U. Fuchs, A. Novosel, R.U. Muller, B. Schermer, U. Bissels, J. Inman, Q. Phan, M. Chien, D.B. Weir, R. Choksi, G. De Vita, D. Frezzetti, H.I. Trompeter, V. Hornung, G. Teng, G. Hartmann, M. Palkovits, R. Di Lauro, P. Wernet, G. Macino, C.E. Rogler, J.W. Nagle, J. Ju, F.N. Papavasiliou, T. Benzing, P. Lichter, W. Tam, M.J. Brownstein, A. Bosio, A. Borkhardt, J.J. Russo, C. Sander, M. Zavolan, and T. Tuschl A mammalian microRNA expression atlas based on small RNA library sequencing Cell 129 2007 1401 1414
70. H. Lassmann, R. Weiler, P. Fischer, C. Bancher, K. Jellinger, E. Floor, W. Danielczyk, F. Seitelberger, and H. Winkler Synaptic pathology in Alzheimer's disease: immunological data for markers of synaptic and large dense-core vesicles Neuroscience 46 1992 1 8
71. R.C. Lee, R.L. Feinbaum, and V. Ambros The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14 Cell 75 1993 843 854
72. G. Leuba, A. Savioz, A. Vernay, B. Carnal, R. Kraftsik, E. Tardif, I. Riederer, and B.M. Riederer Differential changes in synaptic proteins in the Alzheimer frontal cortex with marked increase in PSD-95 postsynaptic protein J. Alzheimers Dis. 15 2008 139 151
73. H. Li, X. Zhong, K.F. Chau, E.C. Williams, and Q. Chang Loss of activity-induced phosphorylation of MeCP2 enhances synaptogenesis, LTP and spatial memory Nat. Neurosci. 14 2011 1001 1008
74. X. Li, A. Khanna, N. Li, and E. Wang Circulatory miR34a as an RNAbased, noninvasive biomarker for brain aging Aging (Albany, NY) 3 2011 985 1002
75. Q. Lin, W. Wei, C.M. Coelho, X. Li, D. Baker-Andresen, K. Dudley, V.S. Ratnu, Z. Boskovic, M.S. Kobor, Y.E. Sun, and T.W. Bredy The brain-specific microRNA miR-128b regulates the formation of fear-extinction memory Nat. Neurosci. 14 2011 1115 1117
76. G. Lippi, J.R. Steinert, E.L. Marczylo, S. D'Oro, R. Fiore, I.D. Forsythe, G. Schratt, M. Zoli, P. Nicotera, and K.W. Young Targeting of the Arpc3 actin nucleation factor by miR-29a/b regulates dendritic spine morphology J. Cell Biol. 194 2011 889 904
77. N. Liu, M. Landreh, K. Cao, M. Abe, G.J. Hendriks, J.R. Kennerdell, Y. Zhu, L.S. Wang, and N.M. Bonini The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila Nature 482 2012 519 523
78. G. Lugli, J. Larson, M.E. Martone, Y. Jones, and N.R. Smalheiser Dicer and eIF2c are enriched at postsynaptic densities in adult mouse brain and are modified by neuronal activity in a calpain-dependent manner J. Neurochem. 94 2005 896 905
79. G. Lugli, V.I. Torvik, J. Larson, and N.R. Smalheiser Expression of microRNAs and their precursors in synaptic fractions of adult mouse forebrain J. Neurochem. 106 2008 650 661
80. W. Lukiw Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus Neuroreport 18 2007 297 300
81. K.C. Martin, A. Casadio, H. Zhu, E. Yaping, J.C. Rose, M. Chen, C.H. Bailey, and E.R. Kandel Synapse-specific, long-term facilitation of aplysia sensory to motor synapses: a function for local protein synthesis in memory storage Cell 91 1997 927 938
82. K.C. Martin, and R.S. Zukin RNA trafficking and local protein synthesis in dendrites: an overview J. Neurosci. 26 2006 7131 7134
83. E. Masliah, R.D. Terry, R.M. DeTeresa, and L.A. Hansen Immunohistochemical quantification of the synapse-related protein synaptophysin in Alzheimer disease Neurosci. Lett. 103 1989 234 239
84. E. Masliah, M. Mallory, L. Hansen, R. DeTeresa, M. Alford, and R. Terry Synaptic and neuritic alterations during the progression of Alzheimer's disease Neurosci. Lett. 174 1994 67 72
85. E. Masliah, M. Mallory, M. Alford, R. DeTeresa, L.A. Hansen, D.W. McKeel Jr., and J.C. Morris Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease Neurology 56 2001 127 129
86. M. Mayford, D. Baranes, K. Podsypanina, and E.R. Kandel The 3'-untranslated region of CaMKII alpha is a cis-acting signal for the localization and translation of mRNA in dendrites Proc. Natl. Acad. Sci. USA 93 1996 13250 13255
87. E. McNeill, and D. Van Vactor MicroRNAs shape the neuronal landscape Neuron 75 2012 363 379
88. P. Merino-Serrais, S. Knafo, L. Alonso-Nanclares, I. Fernaud-Espinosa, and J. DeFelipe Layer-specific alterations to CA1 dendritic spines in a mouse model of Alzheimer's disease Hippocampus 21 2011 1037 1044
89. R.S. Muddashetty, V.C. Nalavadi, C. Gross, X. Yao, L. Xing, O. Laur, S.T. Warren, and G.J. Bassell Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling Mol. Cell 42 2011 673 688
90. A.K. Murashov, V. Chintalgattu, R.R. Islamov, T.E. Lever, E.S. Pak, P.L. Sierpinski, L.C. Katwa, and M.R. Van Scott RNAi pathway is functional in peripheral nerve axons FASEB J. 21 2007 656 670
91. O. Natera-Naranjo, A. Aschrafi, A.E. Gioio, and B.B. Kaplan Identification and quantitative analyses of microRNAs located in the distal axons of sympathetic neurons RNA 16 2010 1516 1529
92. P.T. Nelson, and W.X. Wang MiR-107 is reduced in Alzheimer's disease brain neocortex: validation study J. Alzheimers Dis. 21 2010 75 79
93. A.S. Nudelman, D.P. DiRocco, T.J. Lambert, M.G. Garelick, J. Le, N.M. Nathanson, and D.R. Storm Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo Hippocampus 20 2010 492 498
94. L. Olsen, M. Klausen, L. Helboe, F.C. Nielsen, and T. Werge MicroRNAs show mutually exclusive expression patterns in the brain of adult male rats PLoS One 4 2009 e7225
95. U.A. Orom, F.C. Nielsen, and A.H. Lund MicroRNA-10a binds the 5'UTR of ribosomal protein mRNAs and enhances their translation Mol. Cell 30 2008 460 471
96. C.S. Park, and S.J. Tang Regulation of microRNA expression by induction of bidirectional synaptic plasticity J. Mol. Neurosci. 38 2009 50 56
97. S.L. Patterson, T. Abel, T.A. Deuel, K.C. Martin, J.C. Rose, and E.R. Kandel Recombinant BDNF rescues deficits in basal synaptic transmission and hippocampal LTP in BDNF knockout mice Neuron 16 1996 1137 1145
98. S. Peng, J. Wuu, E.J. Mufson, and M. Fahnestock Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer's disease J. Neurochem. 93 2005 1412 1421
99. I. Pichardo-Casas, L.A. Goff, M.R. Swerdel, A. Athie, J. Davila, M. Ramos-Brossier, M. Lapid-Volosin, W.J. Friedman, R.P. Hart, and L. Vaca Expression profiling of synaptic microRNAs from the adult rat brain identifies regional differences and seizure-induced dynamic modulation Brain Res. 1436 2012 20 33
100. P. Rajasethupathy, F. Fiumara, R. Sheridan, D. Betel, S.V. Puthanveettil, J.J. Russo, C. Sander, T. Tuschl, and E. Kandel Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB Neuron 63 2009 803 817
101. N. Rudinskiy, J.M. Hawkes, R.A. Betensky, M. Eguchi, S. Yamaguchi, T.L. Spires-Jones, and B.T. Hyman Orchestrated experience-driven Arc responses are disrupted in a mouse model of Alzheimer's disease Nat. Neurosci. 15 2012 1422 1429
102. R. Saba, P.H. Storchel, A. Aksoy-Aksel, F. Kepura, G. Lippi, T.D. Plant, and G.M. Schratt Dopamine-regulated microRNA MiR-181a controls GluA2 surface expression in hippocampal neurons Mol. Cell Biol. 32 2012 619 632
103. C.A. Saura, S.Y. Choi, V. Beglopoulos, S. Malkani, D. Zhang, B.S. Shankaranarayana Rao, S. Chattarji, R.J. Kelleher III, E.R. Kandel, K. Duff, A. Kirkwood, and J. Shen Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration Neuron 42 2004 23 36
104. S.W. Scheff, S.T. DeKosky, and D.A. Price Quantitative assessment of cortical synaptic density in Alzheimer's disease Neurobiol. Aging 11 1990 29 37
105. S.W. Scheff, D.A. Price, F.A. Schmitt, and E.J. Mufson Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment Neurobiol. Aging 27 2006 1372 1384
106. S.W. Scheff, D.A. Price, F.A. Schmitt, S.T. DeKosky, and E.J. Mufson Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment Neurology 68 2007 1501 1508
107. G. Schratt microRNAs at the synapse Nat. Rev. Neurosci. 10 2009 842 849
108. G.M. Schratt, F. Tuebing, E.A. Nigh, C.G. Kane, M.E. Sabatini, M. Kiebler, and M.E. Greenberg A brain-specific microRNA regulates dendritic spine development Nature 439 2006 283 289
109. D.J. Selkoe Alzheimer's disease is a synaptic failure Science 298 2002 789 791
110. L.F. Sempere, S. Freemantle, I. Pitha-Rowe, E. Moss, E. Dmitrovsky, and V. Ambros Expression profiling of mammalian microRNAs uncovers a subset of brain-expressed microRNAs with possible roles in murine and human neuronal differentiation Genome Biol. 5 2004 R13
111. K.S. Sheinerman, V.G. Tsivinsky, F. Crawford, M.J. Mullan, L. Abdullah, and S.R. Umansky Plasma microRNA biomarkers for detection of mild cognitive impairment Aging (Albany, NY) 4 2012 590 605
112. G. Siegel, G. Obernosterer, R. Fiore, M. Oehmen, S. Bicker, M. Christensen, S. Khudayberdiev, P.F. Leuschner, C.J. Busch, C. Kane, K. Hubel, F. Dekker, C. Hedberg, B. Rengarajan, C. Drepper, H. Waldmann, S. Kauppinen, M.E. Greenberg, A. Draguhn, M. Rehmsmeier, J. Martinez, and G.M. Schratt A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis Nat. Cell Biol. 11 2009 705 716
113. N.R. Smalheiser, and G. Lugli microRNA regulation of synaptic plasticity Neuromol, Med. 11 2009 133 140
114. T. Spires-Jones, and S. Knafo Spines, plasticity, and cognition in Alzheimer's model mice Neural Plast. 2012 2012 319836
115. M.A. Sutton, and E.M. Schuman Dendritic protein synthesis, synaptic plasticity, and memory Cell 127 2006 49 58
116. C.I. Sze, J.C. Troncoso, C. Kawas, P. Mouton, D.L. Price, and L.J. Martin Loss of the presynaptic vesicle protein synaptophysin in hippocampus correlates with cognitive decline in Alzheimer disease J. Neuropathol. Exp. Neurol. 56 1997 933 944
117. R.E. Tanzi, and L. Bertram Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective Cell 120 2005 545 555
118. R.D. Terry, E. Masliah, D.P. Salmon, N. Butters, R. DeTeresa, R. Hill, L.A. Hansen, and R. Katzman Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment Ann. Neurol. 30 1991 572 580
119. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 9 2007 654 659
120. A. Vazdarjanova, V. Ramirez-Amaya, N. Insel, T.K. Plummer, S. Rosi, S. Chowdhury, D. Mikhael, P.F. Worley, J.F. Guzowski, and C.A. Barnes Spatial exploration induces ARC, a plasticity-related immediate-early gene, only in calcium/calmodulin-dependent protein kinase II-positive principal excitatory and inhibitory neurons of the rat forebrain J. Comp. Neurol. 498 2006 317 329
121. J. Viosca, G. Malleret, R. Bourtchouladze, E. Benito, S. Vronskava, E.R. Kandel, and A. Barco Chronic enhancement of CREB activity in the hippocampus interferes with the retrieval of spatial information Learn. Mem. 16 2009 198 209
122. N. Vo, M.E. Klein, O. Varlamova, D.M. Keller, T. Yamamoto, R.H. Goodman, and S. Impey A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis Proc. Natl. Acad. Sci. USA 102 2005 16426 16431
123. L.L. Wang, Z. Zhang, Q. Li, R. Yang, X. Pei, Y. Xu, J. Wang, S.F. Zhou, and Y. Li Ethanol exposure induces differential microRNA and target gene expression and teratogenic effects which can be suppressed by folic acid supplementation Hum. Reprod. 24 2009 562 579
124. G.A. Wayman, M. Davare, H. Ando, D. Fortin, O. Varlamova, H.Y. Cheng, D. Marks, K. Obrietan, T.R. Soderling, R.H. Goodman, and S. Impey An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP Proc. Natl. Acad. Sci. USA 105 2008 9093 9098
125. K. Wibrand, D. Panja, A. Tiron, M.L. Ofte, K.O. Skaftnesmo, C.S. Lee, J.T. Pena, T. Tuschl, and C.R. Bramham Differential regulation of mature and precursor microRNA expression by NMDA and metabotropic glutamate receptor activation during LTP in the adult dentate gyrus in vivo Eur. J. Neurosci. 31 2010 636 645
126. K. Wibrand, B. Pai, T. Siripornmongcolchai, M. Bittins, B. Berentsen, M.L. Ofte, A. Weigel, K.O. Skaftnesmo, and C.R. Bramham MicroRNA regulation of the synaptic plasticity-related gene Arc PLoS One 7 2012 e41688
127. J. Xu, Q. Chen, K. Zen, C. Zhang, and Q. Zhang Synaptosomes secrete and uptake functionally active microRNAs via exocytosis and endocytosis pathways J. Neurochem. 124 2013 15 25
128. L.A. Yates, C.J. Norbury, and R.J. Gilbert The long and short of microRNA Cell 153 2013 516 519
129. F. Zalfa, M. Giorgi, B. Primerano, A. Moro, A. Di Penta, S. Reis, B. Oostra, and C. Bagni The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses Cell 112 2003 317 327