MicroRNAs underlying memory deficits in neurodegenerative disorders

Progress in Neuro-Psychopharmacology and Biological Psychiatry

Volumn 73, Issue , 2017, Pages 79-86

  Hernandez Rapp, Julia ^a,b   Rainone, Sara ^a,b   Hébert, Sébastien S ^a,b  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITÉ LAVAL   (Canada)

Author keywords

Dementia; miR 124; miR 132; miR 34; Neurodegenerative disorders

Indexed keywords

MICRORNA; MICRORNA 124; MICRORNA 132; MICRORNA 34; UNCLASSIFIED DRUG;

ALZHEIMER DISEASE; AMNESIA; CELL LOSS; CELL SURVIVAL; GENE EXPRESSION REGULATION; HUMAN; HUNTINGTON CHOREA; MOLECULAR PATHOLOGY; NONHUMAN; PARKINSON DISEASE; REVIEW; ANIMAL; COMPLICATION; DEGENERATIVE DISEASE; GENETICS; MEMORY DISORDERS; PHYSIOLOGY;

ANIMALS; HUMANS; MEMORY DISORDERS; MICRORNAS; NEURODEGENERATIVE DISEASES;

EID: 84975142776     PISSN: 02785846     EISSN: 18784216     Source Type: Journal    
DOI: 10.1016/j.pnpbp.2016.04.011     Document Type: Review

References (149)

1. Aarsland, D., Cognitive impairment in Parkinson's disease and dementia with Lewy bodies. Parkinsonism Relat. Disord. 22:Suppl. 1 (2016), S144–S148.
2. Adachi, N., Numakawa, T., Richards, M., Nakajima, S., Kunugi, H., New insight in expression, transport, and secretion of brain-derived neurotrophic factor: implications in brain-related diseases. World J. Biol. Chem. 5 (2014), 409–428.
3. Agostini, M., Tucci, P., Killick, R., Candi, E., Sayan, B.S., Rivetti di Val Cervo, P., Nicotera, P., McKeon, F., Knight, R.A., Mak, T.W., et al. Neuronal differentiation by TAp73 is mediated by microRNA-34a regulation of synaptic protein targets. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 21093–21098.
4. Akerblom, M., Sachdeva, R., Barde, I., Verp, S., Gentner, B., Trono, D., Jakobsson, J., MicroRNA-124 is a subventricular zone neuronal fate determinant. J. Neurosci. 32 (2012), 8879–8889.
5. Aksoy-Aksel, A., Zampa, F., Schratt, G., MicroRNAs and synaptic plasticity—a mutual relationship. Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci., 369, 2014.
6. Bae, B.I., Xu, H., Igarashi, S., Fujimuro, M., Agrawal, N., Taya, Y., Hayward, S.D., Moran, T.H., Montell, C., Ross, C.A., et al. p53 mediates cellular dysfunction and behavioral abnormalities in Huntington's disease. Neuron 47 (2005), 29–41.
7. Bailey, C.H., Kandel, E.R., Si, K., The persistence of long-term memory: a molecular approach to self-sustaining changes in learning-induced synaptic growth. Neuron 44 (2004), 49–57.
8. Baroukh, N.N., Van Obberghen, E., Function of microRNA-375 and microRNA-124a in pancreas and brain. FEBS J. 276 (2009), 6509–6521.
9. Basak, I., Patil, K.S., Alves, G., Larsen, J.P., Moller, S.G., microRNAs as neuroregulators, biomarkers and therapeutic agents in neurodegenerative diseases. Cell Mol. Life Sci., 2015.
10. Bernstein, E., Kim, S.Y., Carmell, M.A., Murchison, E.P., Alcorn, H., Li, M.Z., Mills, A.A., Elledge, S.J., Anderson, K.V., Hannon, G.J., Dicer is essential for mouse development. Nat. Genet. 35 (2003), 215–217.
11. Bommer, G.T., Gerin, I., Feng, Y., Kaczorowski, A.J., Kuick, R., Love, R.E., Zhai, Y., Giordano, T.J., Qin, Z.S., Moore, B.B., et al. p53-mediated activation of miRNA34 candidate tumor-suppressor genes. Curr. Biol. 17 (2007), 1298–1307.
12. Bozon, B., Davis, S., Laroche, S., A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40 (2003), 695–701.
13. Brennecke, J., Hipfner, D.R., Stark, A., Russell, R.B., Cohen, S.M., bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113 (2003), 25–36.
14. Briggs, C.E., Wang, Y., Kong, B., Woo, T.U., Iyer, L.K., Sonntag, K.C., Midbrain dopamine neurons in Parkinson's disease exhibit a dysregulated miRNA and target-gene network. Brain Res. 1618 (2015), 111–121.
15. Brunet, A., Bonni, A., Zigmond, M.J., Lin, M.Z., Juo, P., Hu, L.S., Anderson, M.J., Arden, K.C., Blenis, J., Greenberg, M.E., Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96 (1999), 857–868.
16. Cardo, L.F., Coto, E., Ribacoba, R., Menendez, M., Moris, G., Suarez, E., Alvarez, V., MiRNA profile in the substantia nigra of Parkinson's disease and healthy subjects. J. Mol. Neurosci. 54 (2014), 830–836.
17. Caviness, J.N., Driver-Dunckley, E., Connor, D.J., Sabbagh, M.N., Hentz, J.G., Noble, B., Evidente, V.G., Shill, H.A., Adler, C.H., Defining mild cognitive impairment in Parkinson's disease. Mov. Disord. 22 (2007), 1272–1277.
18. Cheng, L.C., Pastrana, E., Tavazoie, M., Doetsch, F., miR-124 regulates adult neurogenesis in the subventricular zone stem cell niche. Nat. Neurosci. 12 (2009), 399–408.
19. Cogswell, J.P., Ward, J., Taylor, I.A., Waters, M., Shi, Y., Cannon, B., Kelnar, K., Kemppainen, J., Brown, D., Chen, C., et al. 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.
20. Conaco, C., Otto, S., Han, J.J., Mandel, G., Reciprocal actions of REST and a microRNA promote neuronal identity. Proc. Natl. Acad. Sci. U. S. A. 103 (2006), 2422–2427.
21. Davis, T.H., Cuellar, T.L., Koch, S.M., Barker, A.J., Harfe, B.D., McManus, M.T., Ullian, E.M., Conditional loss of Dicer disrupts cellular and tissue morphogenesis in the cortex and hippocampus. J. Neurosci. 28 (2008), 4322–4330.
22. De Pietri Tonelli, D., Pulvers, J.N., Haffner, C., Murchison, E.P., Hannon, G.J., Huttner, W.B., miRNAs are essential for survival and differentiation of newborn neurons but not for expansion of neural progenitors during early neurogenesis in the mouse embryonic neocortex. Development 135 (2008), 3911–3921.
23. Dias, B.G., Goodman, J.V., Ahluwalia, R., Easton, A.E., Andero, R., Ressler, K.J., Amygdala-dependent fear memory consolidation via miR-34a and Notch signaling. Neuron 83 (2014), 906–918.
24. Dorval, V., Smith, P.Y., Delay, C., Calvo, E., Planel, E., Zommer, N., Buee, L., Hebert, S.S., Gene network and pathway analysis of mice with conditional ablation of Dicer in post-mitotic neurons. PLoS One, 7, 2012, e44060.
25. Duff, K., Paulsen, J., Mills, J., Beglinger, L.J., Moser, D.J., Smith, M.M., Langbehn, D., Stout, J., Queller, S., Harrington, D.L., et al. Mild cognitive impairment in prediagnosed Huntington disease. Neurology 75 (2010), 500–507.
26. Ebert, M.S., Sharp, P.A., Roles for microRNAs in conferring robustness to biological processes. Cell 149 (2012), 515–524.
27. Edbauer, D., Neilson, J.R., Foster, K.A., Wang, C.F., Seeburg, D.P., Batterton, M.N., Tada, T., Dolan, B.M., Sharp, P.A., Sheng, M., Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron 65 (2010), 373–384.
28. Femminella, G.D., Ferrara, N., Rengo, G., The emerging role of microRNAs in Alzheimer's disease. Front. Physiol., 6, 2015, 40.
29. Follert, P., Cremer, H., Beclin, C., MicroRNAs in brain development and function: a matter of flexibility and stability. Front. Mol. Neurosci., 7, 2014, 5.
30. Formosa, A., Lena, A.M., Markert, E.K., Cortelli, S., Miano, R., Mauriello, A., Croce, N., Vandesompele, J., Mestdagh, P., Finazzi-Agro, E., et al. DNA methylation silences miR-132 in prostate cancer. Oncogene 32 (2013), 127–134.
31. Fukuda, T., Itoh, M., Ichikawa, T., Washiyama, K., Goto, Y., Delayed maturation of neuronal architecture and synaptogenesis in cerebral cortex of Mecp2-deficient mice. J. Neuropathol. Exp. Neurol. 64 (2005), 537–544.
32. Gao, J., Wang, W.Y., Mao, Y.W., Graff, J., Guan, J.S., Pan, L., Mak, G., Kim, D., Su, S.C., Tsai, L.H., A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature 466 (2010), 1105–1109.
33. Gascon, E., Lynch, K., Ruan, H., Almeida, S., Verheyden, J.M., Seeley, W.W., Dickson, D.W., Petrucelli, L., Sun, D., Jiao, J., et al. Alterations in microRNA-124 and AMPA receptors contribute to social behavioral deficits in frontotemporal dementia. Nat. Med. 20 (2014), 1444–1451.
34. Gaughwin, P.M., Ciesla, M., Lahiri, N., Tabrizi, S.J., Brundin, P., Bjorkqvist, M., Hsa-miR-34b is a plasma-stable microRNA that is elevated in pre-manifest Huntington's disease. Hum. Mol. Genet. 20 (2011), 2225–2237.
35. Ghavami, S., Shojaei, S., Yeganeh, B., Ande, S.R., Jangamreddy, J.R., Mehrpour, M., Christoffersson, J., Chaabane, W., Moghadam, A.R., Kashani, H.H., et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog. Neurobiol. 112 (2014), 24–49.
36. Gillardon, F., Mack, M., Rist, W., Schnack, C., Lenter, M., Hildebrandt, T., Hengerer, B., MicroRNA and proteome expression profiling in early-symptomatic alpha-synuclein(A30P)-transgenic mice. Proteomics Clin. Appl. 2 (2008), 697–705.
37. Giraldez, A.J., Cinalli, R.M., Glasner, M.E., Enright, A.J., Thomson, J.M., Baskerville, S., Hammond, S.M., Bartel, D.P., Schier, A.F., MicroRNAs regulate brain morphogenesis in zebrafish. Science 308 (2005), 833–838.
38. Goodall, E.F., Heath, P.R., Bandmann, O., Kirby, J., Shaw, P.J., Neuronal dark matter: the emerging role of microRNAs in neurodegeneration. Front. Cell. Neurosci., 7, 2013, 178.
39. Grimes, D.A., Han, F., Panisset, M., Racacho, L., Xiao, F., Zou, R., Westaff, K., Bulman, D.E., Translated mutation in the Nurr1 gene as a cause for Parkinson's disease. Mov. Disord. 21 (2006), 906–909.
40. Guo, L., Sun, B., Sang, F., Wang, W., Lu, Z., Haplotype distribution and evolutionary pattern of miR-17 and miR-124 families based on population analysis. PLoS One, 4, 2009, e7944.
41. Ha, M., Kim, V.N., Regulation of microRNA biogenesis. Nat. Rev. Mol. Cell Biol. 15 (2014), 509–524.
42. Hammond, S.M., An overview of microRNAs. Adv. Drug Deliv. Rev. 87 (2015), 3–14.
43. Hancock, M.L., Preitner, N., Quan, J., Flanagan, J.G., MicroRNA-132 is enriched in developing axons, locally regulates Rasa1 mRNA, and promotes axon extension. J. Neurosci. 34 (2014), 66–78.
44. Hansen, K.F., Sakamoto, K., Wayman, G.A., Impey, S., Obrietan, K., Transgenic miR132 alters neuronal spine density and impairs novel object recognition memory. PLoS One, 5, 2010, e15497.
45. Hansen, K.F., Karelina, K., Sakamoto, K., Wayman, G.A., Impey, S., Obrietan, K., miRNA-132: a dynamic regulator of cognitive capacity. Brain Struct. Funct. 218 (2013), 817–831.
46. Hansen, K.F., Sakamoto, K., Aten, S., Snider, K.H., Loeser, J., Hesse, A.M., Page, C.E., Pelz, C., Arthur, J.S., Impey, S., et al. Targeted deletion of miR-132/-212 impairs memory and alters the hippocampal transcriptome. Learn. Mem. 23 (2016), 61–71.
47. Hebert, S.S., De Strooper, B., Molecular biology. miRNAs in neurodegeneration. Science 317 (2007), 1179–1180.
48. Hebert, S.S., De Strooper, B., Alterations of the microRNA network cause neurodegenerative disease. Trends Neurosci. 32 (2009), 199–206.
49. Hebert, S.S., Horre, K., Nicolai, L., Papadopoulou, A.S., Mandemakers, W., Silahtaroglu, A.N., Kauppinen, S., Delacourte, A., De Strooper, B., 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 (2008), 6415–6420.
50. Hebert, S.S., Papadopoulou, A.S., Smith, P., Galas, M.C., Planel, E., Silahtaroglu, A.N., Sergeant, N., Buee, L., De Strooper, B., Genetic ablation of Dicer in adult forebrain neurons results in abnormal tau hyperphosphorylation and neurodegeneration. Hum. Mol. Genet. 19 (2010), 3959–3969.
51. Hebert, S.S., Wang, W.X., Zhu, Q., Nelson, P.T., A study of small RNAs from cerebral neocortex of pathology-verified Alzheimer's disease, dementia with Lewy bodies, hippocampal sclerosis, frontotemporal lobar dementia, and non-demented human controls. J. Alzheimers Dis. 35 (2013), 335–348.
52. Hernandez-Rapp, J., Smith, P.Y., Filali, M., Goupil, C., Planel, E., Magill, S.T., Goodman, R.H., Hebert, S.S., Memory formation and retention are affected in adult miR-132/212. Behav. Brain Res. 287 (2015), 15–26.
53. Ho, V.M., Dallalzadeh, L.O., Karathanasis, N., Keles, M.F., Vangala, S., Grogan, T., Poirazi, P., Martin, K.C., GluA2 mRNA distribution and regulation by miR-124 in hippocampal neurons. Mol. Cell. Neurosci. 61 (2014), 1–12.
54. Hollander, J.A., Im, H.I., Amelio, A.L., Kocerha, J., Bali, P., Lu, Q., Willoughby, D., Wahlestedt, C., Conkright, M.D., Kenny, P.J., Striatal microRNA controls cocaine intake through CREB signalling. Nature 466 (2010), 197–202.
55. Hoss, A.G., Labadorf, A., Latourelle, J.C., Kartha, V.K., Hadzi, T.C., Gusella, J.F., MacDonald, M.E., Chen, J.F., Akbarian, S., Weng, Z., et al. miR-10b-5p expression in Huntington's disease brain relates to age of onset and the extent of striatal involvement. BMC Med. Genet., 8, 2015, 10.
56. Hoss, A.G., Labadorf, A., Beach, T.G., Latourelle, J.C., Myers, R.H., microRNA profiles in Parkinson's disease prefrontal cortex. Front. Aging Neurosci., 8, 2016, 36.
57. Hu, S., Wang, H., Chen, K., Cheng, P., Gao, S., Liu, J., Li, X., Sun, X., MicroRNA-34c downregulation ameliorates amyloid-beta-induced synaptic failure and memory deficits by targeting VAMP2. J. Alzheimers Dis. 48 (2015), 673–686.
58. Huang, E.J., Reichardt, L.F., Trk receptors: roles in neuronal signal transduction. Annu. Rev. Biochem. 72 (2003), 609–642.
59. Hwang, J.Y., Kaneko, N., Noh, K.M., Pontarelli, F., Zukin, R.S., The gene silencing transcription factor REST represses miR-132 expression in hippocampal neurons destined to die. J. Mol. Biol. 426 (2014), 3454–3466.
60. Impey, S., Davare, M., Lesiak, A., Fortin, D., Ando, H., Varlamova, O., Obrietan, K., Soderling, T.R., Goodman, R.H., Wayman, G.A., An activity-induced microRNA controls dendritic spine formation by regulating Rac1–PAK signaling. Mol. Cell. Neurosci. 43 (2010), 146–156.
61. Jasinska, M., Milek, J., Cymerman, I.A., Leski, S., Kaczmarek, L., Dziembowska, M., miR-132 regulates dendritic spine structure by direct targeting of matrix metalloproteinase 9 mRNA. Mol. Neurobiol., 2015.
62. Jessen, F., Wolfsgruber, S., Wiese, B., Bickel, H., Mosch, E., Kaduszkiewicz, H., Pentzek, M., Riedel-Heller, S.G., Luck, T., Fuchs, A., et al. AD dementia risk in late MCI, in early MCI, and in subjective memory impairment. Alzheimers Dement. 10 (2014), 76–83.
63. Johnson, R., Buckley, N.J., Gene dysregulation in Huntington's disease: REST, microRNAs and beyond. Neruomol. Med. 11 (2009), 183–199.
64. Johnson, R., Zuccato, C., Belyaev, N.D., Guest, D.J., Cattaneo, E., Buckley, N.J., A microRNA-based gene dysregulation pathway in Huntington's disease. Neurobiol. Dis. 29 (2008), 438–445.
65. Jugloff, D.G., Jung, B.P., Purushotham, D., Logan, R., Eubanks, J.H., Increased dendritic complexity and axonal length in cultured mouse cortical neurons overexpressing methyl-CpG-binding protein MeCP2. Neurobiol. Dis. 19 (2005), 18–27.
66. Kanagaraj, N., Beiping, H., Dheen, S.T., Tay, S.S., Downregulation of miR-124 in MPTP-treated mouse model of Parkinson's disease and MPP iodide-treated MN9D cells modulates the expression of the calpain/cdk5 pathway proteins. Neuroscience 272 (2014), 167–179.
67. Kim, J., Inoue, K., Ishii, J., Vanti, W.B., Voronov, S.V., Murchison, E., Hannon, G., Abeliovich, A., A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317 (2007), 1220–1224.
68. Kim, W., Lee, Y., McKenna, N.D., Yi, M., Simunovic, F., Wang, Y., Kong, B., Rooney, R.J., Seo, H., Stephens, R.M., et al. miR-126 contributes to Parkinson's disease by dysregulating the insulin-like growth factor/phosphoinositide 3-kinase signaling. Neurobiol. Aging 35 (2014), 1712–1721.
69. Klein, M.E., Lioy, D.T., Ma, L., Impey, S., Mandel, G., Goodman, R.H., Homeostatic regulation of MeCP2 expression by a CREB-induced microRNA. Nat. Neurosci. 10 (2007), 1513–1514.
70. Konopka, W., Kiryk, A., Novak, M., Herwerth, M., Parkitna, J.R., Wawrzyniak, M., Kowarsch, A., Michaluk, P., Dzwonek, J., Arnsperger, T., et al. MicroRNA loss enhances learning and memory in mice. J. Neurosci. 30 (2010), 14835–14842.
71. Krichevsky, A.M., King, K.S., Donahue, C.P., Khrapko, K., Kosik, K.S., A microRNA array reveals extensive regulation of microRNAs during brain development. RNA 9 (2003), 1274–1281.
72. Lagos, D., Pollara, G., Henderson, S., Gratrix, F., Fabani, M., Milne, R.S., Gotch, F., Boshoff, C., miR-132 regulates antiviral innate immunity through suppression of the p300 transcriptional co-activator. Nat. Cell Biol. 12 (2010), 513–519.
73. Lagos-Quintana, M., Rauhut, R., Yalcin, A., Meyer, J., Lendeckel, W., Tuschl, T., Identification of tissue-specific microRNAs from mouse. Curr. Biol. 12 (2002), 735–739.
74. Lau, P., Bossers, K., Janky, R., Salta, E., Frigerio, C.S., Barbash, S., Rothman, R., Sierksma, A.S., Thathiah, A., Greenberg, D., et al. Alteration of the microRNA network during the progression of Alzheimer's disease. EMBO Mol. Med. 5 (2013), 1613–1634.
75. Lau, P., Frigerio, C.S., De Strooper, B., Variance in the identification of microRNAs deregulated in Alzheimer's disease and possible role of lincRNAs in the pathology: the need of larger datasets. Ageing Res. Rev. 17 (2014), 43–53.
76. Lee, S.T., Chu, K., Im, W.S., Yoon, H.J., Im, J.Y., Park, J.E., Park, K.H., Jung, K.H., Lee, S.K., Kim, M., et al. Altered microRNA regulation in Huntington's disease models. Exp. Neurol. 227 (2011), 172–179.
77. Lim, L.P., Lau, N.C., Garrett-Engele, P., Grimson, A., Schelter, J.M., Castle, J., Bartel, D.P., Linsley, P.S., Johnson, J.M., Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs. Nature 433 (2005), 769–773.
78. Liu, N., Landreh, M., Cao, K., Abe, M., Hendriks, G.J., Kennerdell, J.R., Zhu, Y., Wang, L.S., Bonini, N.M., The microRNA miR-34 modulates ageing and neurodegeneration in Drosophila. Nature 482 (2012), 519–523.
79. Lodygin, D., Tarasov, V., Epanchintsev, A., Berking, C., Knyazeva, T., Korner, H., Knyazev, P., Diebold, J., Hermeking, H., Inactivation of miR-34a by aberrant CpG methylation in multiple types of cancer. Cell Cycle 7 (2008), 2591–2600.
80. Luikart, B.W., Bensen, A.L., Washburn, E.K., Perederiy, J.V., Su, K.G., Li, Y., Kernie, S.G., Parada, L.F., Westbrook, G.L., miR-132 mediates the integration of newborn neurons into the adult dentate gyrus. PLoS One, 6, 2011, e19077.
81. Lukiw, W.J., Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport 18 (2007), 297–300.
82. Lungu, G., Stoica, G., Ambrus, A., MicroRNA profiling and the role of microRNA-132 in neurodegeneration using a rat model. Neurosci. Lett. 553 (2013), 153–158.
83. Maciotta, S., Meregalli, M., Torrente, Y., The involvement of microRNAs in neurodegenerative diseases. Front. Cell. Neurosci., 7, 2013, 265.
84. Magill, S.T., Cambronne, X.A., Luikart, B.W., Lioy, D.T., Leighton, B.H., Westbrook, G.L., Mandel, G., Goodman, R.H., microRNA-132 regulates dendritic growth and arborization of newborn neurons in the adult hippocampus. Proc. Natl. Acad. Sci. U. S. A. 107 (2010), 20382–20387.
85. Makeyev, E.V., Zhang, J., Carrasco, M.A., Maniatis, T., The MicroRNA miR-124 promotes neuronal differentiation by triggering brain-specific alternative pre-mRNA splicing. Mol. Cell 27 (2007), 435–448.
86. Malmevik, J., Petri, R., Knauff, P., Brattas, P.L., Akerblom, M., Jakobsson, J., Distinct cognitive effects and underlying transcriptome changes upon inhibition of individual miRNAs in hippocampal neurons. Sci. Rep., 6, 2016, 19879.
87. Marti, E., Pantano, L., Banez-Coronel, M., Llorens, F., Minones-Moyano, E., Porta, S., Sumoy, L., Ferrer, I., Estivill, X., A myriad of miRNA variants in control and Huntington's disease brain regions detected by massively parallel sequencing. Nucleic Acids Res. 38 (2010), 7219–7235.
88. Minichiello, L., TrkB signalling pathways in LTP and learning. Nat. Rev. Neurosci. 10 (2009), 850–860.
89. Minones-Moyano, E., Porta, S., Escaramis, G., Rabionet, R., Iraola, S., Kagerbauer, B., Espinosa-Parrilla, Y., Ferrer, I., Estivill, X., Marti, E., MicroRNA profiling of Parkinson's disease brains identifies early downregulation of miR-34b/c which modulate mitochondrial function. Hum. Mol. Genet. 20 (2011), 3067–3078.
90. Mishima, T., Mizuguchi, Y., Kawahigashi, Y., Takizawa, T., Takizawa, T., RT-PCR-based analysis of microRNA (miR-1 and -124) expression in mouse CNS. Brain Res. 1131 (2007), 37–43.
91. Miska, E.A., Alvarez-Saavedra, E., Townsend, M., Yoshii, A., Sestan, N., Rakic, P., Constantine-Paton, M., Horvitz, H.R., Microarray analysis of microRNA expression in the developing mammalian brain. Genome Biol., 5, 2004, R68.
92. Motta, M.C., Divecha, N., Lemieux, M., Kamel, C., Chen, D., Gu, W., Bultsma, Y., McBurney, M., Guarente, L., Mammalian SIRT1 represses forkhead transcription factors. Cell 116 (2004), 551–563.
93. Mukilan, M., Ragu Varman, D., Sudhakar, S., Rajan, K.E., Activity-dependent expression of miR-132 regulates immediate-early gene induction during olfactory learning in the greater short-nosed fruit bat, Cynopterus sphinx. Neurobiol. Learn. Mem. 120 (2015), 41–51.
94. Nair, V.D., McNaught, K.S., Gonzalez-Maeso, J., Sealfon, S.C., Olanow, C.W., p53 mediates nontranscriptional cell death in dopaminergic cells in response to proteasome inhibition. J. Biol. Chem. 281 (2006), 39550–39560.
95. Nichols, W.C., Uniacke, S.K., Pankratz, N., Reed, T., Simon, D.K., Halter, C., Rudolph, A., Shults, C.W., Conneally, P.M., Foroud, T., et al. Evaluation of the role of Nurr1 in a large sample of familial Parkinson's disease. Mov. Disord. 19 (2004), 649–655.
96. Nudelman, A.S., DiRocco, D.P., Lambert, T.J., Garelick, M.G., Le, J., Nathanson, N.M., Storm, D.R., Neuronal activity rapidly induces transcription of the CREB-regulated microRNA-132, in vivo. Hippocampus 20 (2010), 492–498.
97. Numakawa, T., Suzuki, S., Kumamaru, E., Adachi, N., Richards, M., Kunugi, H., BDNF function and intracellular signaling in neurons. Histol. Histopathol. 25 (2010), 237–258.
98. Nunez-Iglesias, J., Liu, C.C., Morgan, T.E., Finch, C.E., Zhou, X.J., Joint genome-wide profiling of miRNA and mRNA expression in Alzheimer's disease cortex reveals altered miRNA regulation. PLoS One, 5, 2010, e8898.
99. Packer, A.N., Xing, Y., Harper, S.Q., Jones, L., Davidson, B.L., The bifunctional microRNA miR-9/miR-9* regulates REST and CoREST and is downregulated in Huntington's disease. J. Neurosci. 28 (2008), 14341–14346.
100. Pathania, M., Torres-Reveron, J., Yan, L., Kimura, T., Lin, T.V., Gordon, V., Teng, Z.Q., Zhao, X., Fulga, T.A., Van Vactor, D., et al. miR-132 enhances dendritic morphogenesis, spine density, synaptic integration, and survival of newborn olfactory bulb neurons. PLoS One, 7, 2012, e38174.
101. Paulsen, J.S., Long, J.D., Onset of Huntington's disease: can it be purely cognitive?. Mov. Disord. 29 (2014), 1342–1350.
102. Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R.C., Cota, P., Wittnam, J.L., Gogol-Doering, A., Opitz, L., et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328 (2010), 753–756.
103. Petri, R., Malmevik, J., Fasching, L., Akerblom, M., Jakobsson, J., miRNAs in brain development. Exp. Cell Res. 321 (2014), 84–89.
104. Qin, J., Ke, J., Xu, J., Wang, F., Zhou, Y., Jiang, Y., Wang, Z., Downregulation of microRNA-132 by DNA hypermethylation is associated with cell invasion in colorectal cancer. Onco Targets Ther. 8 (2015), 3639–3648.
105. Rajasethupathy, P., Fiumara, F., Sheridan, R., Betel, D., Puthanveettil, S.V., Russo, J.J., Sander, C., Tuschl, T., Kandel, E., Characterization of small RNAs in Aplysia reveals a role for miR-124 in constraining synaptic plasticity through CREB. Neuron 63 (2009), 803–817.
106. Reinhart, B.J., Slack, F.J., Basson, M., Pasquinelli, A.E., Bettinger, J.C., Rougvie, A.E., Horvitz, H.R., Ruvkun, G., The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans. Nature 403 (2000), 901–906.
107. Remenyi, J., Hunter, C.J., Cole, C., Ando, H., Impey, S., Monk, C.E., Martin, K.J., Barton, G.J., Hutvagner, G., Arthur, J.S., Regulation of the miR-212/132 locus by MSK1 and CREB in response to neurotrophins. Biochem. J. 428 (2010), 281–291.
108. Renaudineau, S., Poucet, B., Laroche, S., Davis, S., Save, E., Impaired long-term stability of CA1 place cell representation in mice lacking the transcription factor zif268/egr1. Proc. Natl. Acad. Sci. U. S. A. 106 (2009), 11771–11775.
109. Rohn, T.T., Vyas, V., Hernandez-Estrada, T., Nichol, K.E., Christie, L.A., Head, E., Lack of pathology in a triple transgenic mouse model of Alzheimer's disease after overexpression of the anti-apoptotic protein Bcl-2. J. Neurosci. 28 (2008), 3051–3059.
110. Rokavec, M., Li, H., Jiang, L., Hermeking, H., The p53/miR-34 axis in development and disease. J. Mol. Cell Biol. 6 (2014), 214–230.
111. Rossi, C., Angelucci, A., Costantin, L., Braschi, C., Mazzantini, M., Babbini, F., Fabbri, M.E., Tessarollo, L., Maffei, L., Berardi, N., et al. Brain-derived neurotrophic factor (BDNF) is required for the enhancement of hippocampal neurogenesis following environmental enrichment. Eur. J. Neurosci. 24 (2006), 1850–1856.
112. Russo, S.J., Mazei-Robison, M.S., Ables, J.L., Nestler, E.J., Neurotrophic factors and structural plasticity in addiction. Neuropharmacology 56:Suppl. 1 (2009), 73–82.
113. Sajan, F.D., Martiniuk, F., Marcus, D.L., Frey, W.H. 2nd, Hite, R., Bordayo, E.Z., Freedman, M.L., Apoptotic gene expression in Alzheimer's disease hippocampal tissue. Am. J. Alzheimers Dis. Other Demen. 22 (2007), 319–328.
114. Schaefer, A., O'Carroll, D., Tan, C.L., Hillman, D., Sugimori, M., Llinas, R., Greengard, P., Cerebellar neurodegeneration in the absence of microRNAs. J. Exp. Med. 204 (2007), 1553–1558.
115. Scharfman, H., Goodman, J., Macleod, A., Phani, S., Antonelli, C., Croll, S., Increased neurogenesis and the ectopic granule cells after intrahippocampal BDNF infusion in adult rats. Exp. Neurol. 192 (2005), 348–356.
116. Schipper, H.M., Maes, O.C., Chertkow, H.M., Wang, E., MicroRNA expression in Alzheimer blood mononuclear cells. Gene Regul. Syst. Biol. 1 (2007), 263–274.
117. Scott, H.L., Tamagnini, F., Narduzzo, K.E., Howarth, J.L., Lee, Y.B., Wong, L.F., Brown, M.W., Warburton, E.C., Bashir, Z.I., Uney, J.B., MicroRNA-132 regulates recognition memory and synaptic plasticity in the perirhinal cortex. Eur. J. Neurosci. 36 (2012), 2941–2948.
118. Shioya, M., Obayashi, S., Tabunoki, H., Arima, K., Saito, Y., Ishida, T., Satoh, J., Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol. Appl. Neurobiol. 36 (2010), 320–330.
119. Smith, P.Y., Hernandez-Rapp, J., Jolivette, F., Lecours, C., Bisht, K., Goupil, C., Dorval, V., Parsi, S., Morin, F., Planel, E., et al. miR-132/212 deficiency impairs tau metabolism and promotes pathological aggregation in vivo. Hum. Mol. Genet., 2015.
120. Sonntag, K.C., MicroRNAs and deregulated gene expression networks in neurodegeneration. Brain Res. 1338 (2010), 48–57.
121. Stambolic, V., Suzuki, A., de la Pompa, J.L., Brothers, G.M., Mirtsos, C., Sasaki, T., Ruland, J., Penninger, J.M., Siderovski, D.P., Mak, T.W., Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95 (1998), 29–39.
122. Su, M., Hong, J., Zhao, Y., Liu, S., Xue, X., MeCP2 controls hippocampal brain-derived neurotrophic factor expression via homeostatic interactions with microRNA132 in rats with depression. Mol. Med. Rep. 12 (2015), 5399–5406.
123. Tetreault, N., De Guire, V., miRNAs: their discovery, biogenesis and mechanism of action. Clin. Biochem. 46 (2013), 842–845.
124. Tognini, P., Pizzorusso, T., MicroRNA212/132 family: molecular transducer of neuronal function and plasticity. Int. J. Biochem. Cell Biol. 44 (2012), 6–10.
125. Visvanathan, J., Lee, S., Lee, B., Lee, J.W., Lee, S.K., The microRNA miR-124 antagonizes the anti-neural REST/SCP1 pathway during embryonic CNS development. Genes Dev. 21 (2007), 744–749.
126. Vo, N., Klein, M.E., Varlamova, O., Keller, D.M., Yamamoto, T., Goodman, R.H., Impey, S., A cAMP-response element binding protein-induced microRNA regulates neuronal morphogenesis. Proc. Natl. Acad. Sci. U. S. A. 102 (2005), 16426–16431.
127. Wanet, A., Tacheny, A., Arnould, T., Renard, P., miR-212/132 expression and functions: within and beyond the neuronal compartment. Nucleic Acids Res. 40 (2012), 4742–4753.
128. Wang, W.X., Rajeev, B.W., Stromberg, A.J., Ren, N., Tang, G., Huang, Q., Rigoutsos, I., Nelson, P.T., The expression of microRNA miR-107 decreases early in Alzheimer's disease and may accelerate disease progression through regulation of beta-site amyloid precursor protein-cleaving enzyme 1. J. Neurosci. 28 (2008), 1213–1223.
129. Wang, X., Liu, P., Zhu, H., Xu, Y., Ma, C., Dai, X., Huang, L., Liu, Y., Zhang, L., Qin, C., miR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain Res. Bull. 80 (2009), 268–273.
130. Wang, R.Y., Phang, R.Z., Hsu, P.H., Wang, W.H., Huang, H.T., Liu, I.Y., In vivo knockdown of hippocampal miR-132 expression impairs memory acquisition of trace fear conditioning. Hippocampus 23 (2013), 625–633.
131. Wang, H., Ye, Y., Zhu, Z., Mo, L., Lin, C., Wang, Q., Wang, H., Gong, X., He, X., Lu, G., et al. MiR-124 regulates apoptosis and autophagy process in MPTP model of Parkinson's disease by targeting to bim. Brain Pathol., 2015.
132. Wayman, G.A., Davare, M., Ando, H., Fortin, D., Varlamova, O., Cheng, H.Y., Marks, D., Obrietan, K., Soderling, T.R., Goodman, R.H., et al. An activity-regulated microRNA controls dendritic plasticity by down-regulating p250GAP. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 9093–9098.
133. Weinberg, R.B., Mufson, E.J., Counts, S.E., Evidence for a neuroprotective microRNA pathway in amnestic mild cognitive impairment. Front. Neurosci., 9, 2015, 430.
134. Welch, C., Chen, Y., Stallings, R.L., MicroRNA-34a functions as a potential tumor suppressor by inducing apoptosis in neuroblastoma cells. Oncogene 26 (2007), 5017–5022.
135. Wibrand, K., Pai, B., Siripornmongcolchai, T., Bittins, M., Berentsen, B., Ofte, M.L., Weigel, A., Skaftnesmo, K.O., Bramham, C.R., MicroRNA regulation of the synaptic plasticity-related gene Arc. PLoS One, 7, 2012, e41688.
136. Wienholds, E., Koudijs, M.J., van Eeden, F.J., Cuppen, E., Plasterk, R.H., The microRNA-producing enzyme Dicer1 is essential for zebrafish development. Nat. Genet. 35 (2003), 217–218.
137. Wong, H.K., Veremeyko, T., Patel, N., Lemere, C.A., Walsh, D.M., Esau, C., Vanderburg, C., Krichevsky, A.M., De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease. Hum. Mol. Genet. 22 (2013), 3077–3092.
138. Xie, B., Zhou, H., Zhang, R., Song, M., Yu, L., Wang, L., Liu, Z., Zhang, Q., Cui, D., Wang, X., et al. Serum miR-206 and miR-132 as potential circulating biomarkers for mild cognitive impairment. J. Alzheimers Dis. 45 (2015), 721–731.
139. Xue, Y., Ouyang, K., Huang, J., Zhou, Y., Ouyang, H., Li, H., Wang, G., Wu, Q., Wei, C., Bi, Y., et al. Direct conversion of fibroblasts to neurons by reprogramming PTB-regulated microRNA circuits. Cell 152 (2013), 82–96.
140. Yamakuchi, M., Lowenstein, C.J., MiR-34, SIRT1 and p53: the feedback loop. Cell Cycle 8 (2009), 712–715.
141. Yamakuchi, M., Ferlito, M., Lowenstein, C.J., miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. U. S. A. 105 (2008), 13421–13426.
142. Yang, D.S., Kumar, A., Stavrides, P., Peterson, J., Peterhoff, C.M., Pawlik, M., Levy, E., Cataldo, A.M., Nixon, R.A., Neuronal apoptosis and autophagy cross talk in aging PS/APP mice, a model of Alzheimer's disease. Am. J. Pathol. 173 (2008), 665–681.
143. Yang, D., Li, T., Wang, Y., Tang, Y., Cui, H., Tang, Y., Zhang, X., Chen, D., Shen, N., Le, W., miR-132 regulates the differentiation of dopamine neurons by directly targeting Nurr1 expression. J. Cell Sci. 125 (2012), 1673–1682.
144. Yang, Y., Shu, X., Liu, D., Shang, Y., Wu, Y., Pei, L., Xu, X., Tian, Q., Zhang, J., Qian, K., et al. EPAC null mutation impairs learning and social interactions via aberrant regulation of miR-124 and Zif268 translation. Neuron 73 (2012), 774–788.
145. Yu, J.Y., Chung, K.H., Deo, M., Thompson, R.C., Turner, D.L., MicroRNA miR-124 regulates neurite outgrowth during neuronal differentiation. Exp. Cell Res. 314 (2008), 2618–2633.
146. Zhang, S., Hao, J., Xie, F., Hu, X., Liu, C., Tong, J., Zhou, J., Wu, J., Shao, C., Downregulation of miR-132 by promoter methylation contributes to pancreatic cancer development. Carcinogenesis 32 (2011), 1183–1189.
147. Zhou, R., Yuan, P., Wang, Y., Hunsberger, J.G., Elkahloun, A., Wei, Y., Damschroder-Williams, P., Du, J., Chen, G., Manji, H.K., Evidence for selective microRNAs and their effectors as common long-term targets for the actions of mood stabilizers. Neuropsychopharmacology 34 (2009), 1395–1405.
148. Zocchi, L., Sassone-Corsi, P., SIRT1-mediated deacetylation of MeCP2 contributes to BDNF expression. Epigenetics 7 (2012), 695–700.
149. Zovoilis, A., Agbemenyah, H.Y., Agis-Balboa, R.C., Stilling, R.M., Edbauer, D., Rao, P., Farinelli, L., Delalle, I., Schmitt, A., Falkai, P., et al. microRNA-34c is a novel target to treat dementias. EMBO J. 30 (2011), 4299–4308.