The epigenetic dimension of Alzheimer's disease: Causal, consequence, or curiosity?

Dialogues in Clinical Neuroscience

Volumn 16, Issue 3, 2014, Pages 373-393

  Millan, Mark J ^a  

^a INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

Author keywords

Acetylation; Apoptosis; Bcl2; Beta amyloid methylation; Cell cycle reentry; HDAC; Histone; Inflammation; MicroRNA; Microtubule; miR; miRNA; Oxidative stress; Phosphorylation; Secretase; Tau

Indexed keywords

AMYLOID BETA PROTEIN[1-42]; LONG UNTRANSLATED RNA; MICRORNA; SMALL UNTRANSLATED RNA; TAU PROTEIN; UNTRANSLATED RNA; AMYLOID BETA PROTEIN;

ALZHEIMER DISEASE; APOPTOSIS; ARTICLE; BEHAVIOR DISORDER; BRAIN TISSUE; CELL CYCLE; CELL LOSS; COGNITIVE DEFECT; DEREGULATION; DISEASE COURSE; DNA METHYLATION; EPIGENETICS; GENE EXPRESSION; GENETIC RISK; HISTONE ACETYLATION; HISTONE METHYLATION; HUMAN; INTERACTIONS WITH RNA; NERVOUS SYSTEM INFLAMMATION; NONHUMAN; OXIDATIVE STRESS; PROTEIN PROCESSING; RISK FACTOR; SYNAPSE; ANIMAL; BRAIN CORTEX; GENETIC EPIGENESIS; GENETICS; METABOLISM; MOUSE; PATHOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; CEREBRAL CORTEX; EPIGENESIS, GENETIC; EPIGENOMICS; HUMANS; MICE; MICE, TRANSGENIC; MICRORNAS;

EID: 84911447251     PISSN: 12948322     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (185)

1. Reitz C, Brayne C, Mayeux R. Epidemiology of Alzheimer disease. Nat Rev Neurol. 2011;7:137.
2. Adwan L, Zawia NH. Epigenetics: a novel therapeutic approach for the treatment of Alzheimer's disease. Pharmacol Ther. 2013;139:41-50.
3. Anand R, Gill KD, Mahdi AA. Therapeutics of Alzheimer's disease: past, present and future. Neuropharmacology. 2014;76:27-50.
4. Jacobs HI, Radua J, Lückmann HC, Sack AT. Meta-analysis of functional network alterations in Alzheimer's disease: toward a network biomarker. Neurosci Biobehav Rev. 2013;37:753-765.
5. Jack CR, Knopman DS, Jagust WJ, et al. Tracking pathophysiological processes in Alzheimer's disease: an updated hypothetical model of dynamic biomarkers. Lancet Neurol. 2013;12:207-216.
6. Benilova I, Karran E, De Strooper B.The toxic Aβ oligomer and Alzheimer's disease: an emperor in need of clothes. Nat Neurosci. 2012;15:349-357.
7. Karran E, Mercken M, De Strooper B. The amyloid cascade hypothesis for Alzheimer's disease: an appraisal for the development of therapeutics. Nat Rev Drug Discov. 2011;10:698-712.
8. Martin L, Latypova X, Terro F. Post-translational modifications of tau protein: implications for Alzheimer's disease. Neurochem Int. 2011;58:458-471.
9. Spillantini MG, Goedert M. Tau pathology and neurodegeneration. Lancet Neurol. 2013;12:609-622.
10. Khandelwal PJ, Herman AM, Moussa CE. Inflammation in the early stages of neurodegenerative pathology. J Neuroimmunol. 2011;238:1-11.
11. Swerdlow RH, Burns JM, Khan SM. The Alzheimer's disease mitochondrial cascade hypothesis: Progress and perspectives. Biochim Biophys Acta. 2014;1842:1219-1231.
12. Ghavami S, Shojaei S, Yeganeh B, et al. Autophagy and apoptosis dysfunction in neurodegenerative disorders. Prog Neurobiol. 2014;112:24-49.
13. Mukhopadhyay S, Panda PK, Sinha N, Das DN, Bhutia SK. Autophagy and apoptosis: where do they meet? Apoptosis. 2014;19:555-566.
14. Swiss VA, Casaccia P. Cell-context specific role of the E2F/Rb pathway in development and disease. Glia. 2010;58:377-390.
15. Haass C, Kaether C, Thinakaran G, Sisodia S. Trafficking and proteolytic processing of APP. Cold Spring Harb Perspect Med. 2012;2:a006270.
16. Chavez-Gutierrez, L, Bammens L, Benilova I, et al. The mechanism of γ-secretase dysfunction in familial Alzheimer disease. EMBO J. 2012;31:2261-2268.
17. Huang Y. Abeta-independent roles of apolipoprotein E4 in the pathogenesis of Alzheimer's disease. Trends Mol Med. 2010;16:287-294.
18. Kanekiyo T, Xu H, Bu G. ApoE and Aβ in Alzheimer's disease: accidental encounters or partners? Neuron. 2014;81:740-754.
19. Lambert JC, Amouyel P. Genetics of Alzheimer's disease: new evidence for an old hypothesis? Genet Dev. 2011;21:295-301.
20. Lu H, Liu X, Deng Y, Qing H. DNA methylation, a hand behind neurodegenerative diseases. Front Aging Neurosci. 2013;5:85.
21. Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J. Epigenetic mechanisms in Alzheimer's disease. Neurobiol Aging. 2011;32:1161-1180.
22. Wang J, Yu JT, Tan MS, Jiang T, Tan L. Epigenetic mechanisms in Alzheimer's disease: Implications for pathogenesis and therapy. Ageing Res Rev. 2013;12:1024-1041.
23. Bihaqi SW, Schumacher A, Maloney B, Lahiri DK, Zawia NH. Do epigenetic pathways initiate late onset Alzheimer disease (LOAD): towards a new paradigm. Curr Alzheimer Res. 2012;9:574-588.
24. Bradley-Whitman MA, Lovell MA. Epigenetic changes in the progression of Alzheimer's disease. Mech Ageing Dev. 2013;134:486-495.
25. Cencioni C, Spallotta F, Martelli F, Valente S, Mai A, Zeiher AM, Gaetano C. Oxidative stress and epigenetic regulation in ageing and age-related diseases. Int J Mol Sci. 2013;14:17643-17663.
26. Walker MP, LaFerla FM, Oddo SS, Brewer GJ. Reversible epigenetic histone modifications and Bdnf expression in neurons with aging and from a mouse model of Alzheimer's disease. Age (Disorder). 2013;35:519- 531.
27. Millan MJ. An epigenetic framework for neurodevelopmental disorders: from pathogenesis to potential therapy. Neuropharmacology. 2013;68:2-82.
28. Deaton AM, Bird A. CpG islands and the regulation of transcription. Genes Dev. 2011;25:1010-1022.
29. Grayson DR, Guidotti A. The dynamics of DNA methylation in schizophrenia and related psychiatric disorders. Neuropsychopharmacology. 2013;38:138-166.
30. Fleming JL, Phiel CJ, Toland AE. The role for oxidative stress in aberrant DNA methylation in Alzheimer's disease. Curr Alzheimer Res. 2012;9:1077-1096.
31. Bakulski KM, Dolinoy DC, Sartor MA, et al. Genome-wide DNA methylation differences between late-onset Alzheimer's disease and cognitively normal controls in human frontal cortex. J Alzheimers Dis. 2012;29:571-88.
32. Chouliaras L, Mastroeni D, Delvaux E, et al Consistent decrease in global DNA methylation and hydroxymethylation in the hippocampus of Alzheimer's disease patients. Neurobiol Aging. 2013;34:2091-2099.
33. Coppieters N, Dieriks BV, Lill C, Faull RL, Curtis MA, Dragunow M. Global changes in DNA methylation and hydroxymethylation in Alzheimer's disease human brain. Neurobiol Aging. 2014;35:1334-1344
34. Iwata A, Nagata K, Hatsuta H, et al. Altered CpG methylation in sporadic Alzheimer's disease is associated with APP and MAPT dysregulation. Hum Mol Genet. 2014;23:648-656.
35. Fuso A, Cavallaro RA, Nicolia V, Scarpa S. PSEN1 promoter demethylation in hyperhomocysteinemic TgCRND8 mice is the culprit, not the consequence. Curr Alzheimer Res. 2012;9:527-535.
36. Fuso A, Seminara L, Cavallaro RA, D'Anselmi F, Scarpa S. S-adenosyl- methionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Mol Cell Neurosci. 2005;28:195-204.
37. Guo X, Wu X, Ren L, Liu G, Li L. Epigenetic mechanisms of amyloid-β production in anisomycin-treated SH-SY5Y cells. Neurocience. 2011;194:272-281.
38. Rao JS, Keleshian VL, Klein S, Rapoport SI. Epigenetic modifications in frontal cortex from Alzheimer's disease and bipolar disorder patients. Transl Psychiatry. 2012;2:e132
39. Gu X, Sun J, Li S, Wu X, Li L. Oxidative stress induces DNA demethylation and histone acetylation in SH-SY5Y cells: potential epigenetic mechanisms in gene transcription in Aβ production. Neurobiol Aging. 2013;34:1069-1079.
40. Chen KL, Wang SS, Yang YY, Yuan RY, Chen RM, Hu CJ. The epigenetic effects of amyloid-beta(1-40) on global DNA and neprilysin genes in murine cerebral endothelial cells. Biochem Biophys Res Commun. 2009;378:57-61.
41. Taher N, McKenzie C, Garrett R, Baker M, Fox N, Isaacs GD. Amyloid-β alters the DNA methylation status of cell-fate genes in an Alzheimer's disease model. J Alzheimers Dis. 2014;38:831-844.
42. Van den Hove DL, Kompotis K, Lardenoije R, et al. Epigenetically regulated microRNAs in Alzheimer's disease. Neurobiol Aging. 2014;35:731- 745.
43. Cogswell JP, Ward J, Taylor IA, et al. Identification of miRNA changes in Alzheimer's disease brain and CSF yields putative biomarkers and insights into disease pathways. J Alzheimers Dis. 2008;14:27-41.
44. Xu B, Hsu PK, Karayiorgou M, Gogos JA. MicroRNA dysregulation in neuropsychiatric disorders and cognitive dysfunction. Neurobiol Dis. 2012;46:291-301.
45. Sun G, Ye P, Murai K, Lang MF, et al. MiR-137 forms a regulatory loop with nuclear receptor TLX and LSD1 in neural stem cells. Nat Commun. 2011;2:529.
46. Li X, Wei W, Ratnu VS, Bredy TW. On the potential role of active DNA demethylation in establishing epigenetic states associated with neural plasticity and memory. Neurobiol Learn Mem. 2013;105:125-132.
47. Kouzarides T. Chromatin modifications and their function. Cell. 2007;128:693-705.
48. Gräff J, Rei D, Guan JS, et al. An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature. 2012;483:222-226.
49. Day JJ, Sweatt JD.Epigenetic mechanisms in cognition. Neuron. 2011;70:813-829.
50. Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH. Recovery of learning and memory is associated with chromatin remodelling. Nature. 2007;447:178-182.
51. Jarome TJ, Lubin FD. Histone lysine methylation: critical regulator of memory and behavior. Rev Neurosci. 2013;24:375-387.
52. Zhang K, Schrag M, Crofton A, Trivedi R, Vinters H, Kirsch W. Targeted proteomics for quantification of histone acetylation in Alzheimer's disease. Proteomics. 2012;12:1261-1268.
53. Ricobaraza A, Cuadrado-Tejedor M, Pérez-Mediavilla A, Frechilla D, Del Río J, García-Osta A. Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology. 2009;34:1721-1732.
54. Francis YI, Fà M, Ashraf H, et al. Dysregulation of histone acetylation in the APP/PS1 mouse model of Alzheimer's disease. J Alzheimers Dis. 2009;18:131-139.
55. Zhang ZY, Schluesener HJ. Oral administration of histone deacetylase inhibitor MS-275 ameliorates neuroinflammation and cerebral amyloidosis and improves behavior in a mouse model. J Neuropathol Exp Neurol. 2013;72:178-185.
56. Bie B, Wu J, Yang H, Xu JJ, Brown DL, Naguib M. Epigenetic suppression of neuroligin 1 underlies amyloid-induced memory deficiency. Nat Neurosci. 2014;17:223-231.
57. Lithner CU Lacor PN, Zhao WQ, et al. Disruption of neocortical histone H3 homeostasis by soluble Aβ: implications for Alzheimer's disease. Neurobiol Aging. 2013;34:2081-2090.
58. Wang Z, Yang D, Zhang X, et al. Hypoxia-induced downregulation of neprilysin by histone modification in mouse primary cortical and hippocampal neurons. PLoS One. 201;6:e19229.
59. Barry G. Integrating the roles of long and small non-coding RNA in brain function and disease. Mol Psychiatry. 2014;19:410-416.
60. Bartel, DP. MicroRNAs: target recognition and regulatory functions. Cell. 2009;136:215-233.
61. ENCODE Project Consortium, Bernstein BE, Birney E, et al. An integrated encyclopedia of DNA elements in the human genome. Nature. 2012;489:57-74.
62. Qureshi IA, Mehler MF. Long non-coding RNAs: novel targets for nervous system disease diagnosis and therapy. Neurotherapeutics. 2013;10:632-646.
63. Millan MJ. MicroRNA in the regulation and expression of serotonergic transmission in the brain and other tissues. Curr Opin Pharmacol. 2011;11:11-22.
64. Goodall EF, Heath PR, Bandmann O, Kirby J, Shaw PJ. Neuronal dark matter: the emerging of microRNAs in neurodegeneration. Front Cell Neurosci. 2013;7:178.
65. Lau P, Sala Frigerio C, 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. 2014:17C:43-53.
66. Satoh J. Molecular network of microRNA targets in Alzheimer's disease brains. Exp Neurol. 2012;235:436-446.
67. Wang WX, Huang Q, Hu Y, Stromberg AJ, Nelson PT. Patterns of microRNA expression in normal and early Alzheimer's disease human temporal cortex: white matter versus gray matter. Acta Neuropathol. 2011;121:193-205.
68. Long JM, Lahiri DK. Advances in microRNA experimental approaches to study physiological regulation of gene products implicated in CNS disorders. Exp Neurol. 2012;235:402-418.
69. Lukiw WJ. Micro-RNA speciation in fetal, adult and Alzheimer's disease hippocampus. Neuroreport. 2007;18:297-300.
70. Müller M, Kuiperij HB, Claassen JA, Küsters B, Verbeek MM. MicroRNAs in Alzheimer's disease: differential expression in hippocampus and cell-free cerebrospinal fluid. Neurobiol Aging. 2014;35:152-158.
71. Chai S, Cambronne XA, Eichhorn SW, Goodman RH. MicroRNA-134 activity in somatostatin interneurons regulates H-Ras localization by repressing the palmitoylation enzyme, DHHC9. Proc Natl Acad Sci U S A. 2013;110:17898-17903.
72. Cui JG, Li YY, Zhao Y, Bhattacharjee S, Lukiw WJ. Differential regulation of interleukin-1 receptor-associated kinase-1 (IRAK-1) and IRAK-2 by microRNA-146a and NF-kappaB in stressed human astroglial cells and in Alzheimer disease. J Biol Chem. 2010;285:38951-38960.
73. Sethi P, Lukiw WJ. Micro-RNA abundance and stability in human brain: specific alterations in Alzheimer's disease temporal lobe neocortex. Neurosci Lett. 2009;459:100-104.
74. Lau P, Bossers K, Janky R, et al. Alteration of the microRNA network during the progression of Alzheimer's disease. EMBO Mol Med. 2013;5:1613-1634.
75. Smith PY, Delay C, Girard J, et al MicroRNA-132 loss is associated with tau exon 10 inclusion in progressive supranuclear palsy. Hum Mol Genet. 2011;20:4016-4024.
76. Smith P, Al Hashimi A, Girard J, Delay C, Hébert SS. In vivo regulation of amyloid precursor protein neuronal splicing by microRNAs. J Neurochem. 2011;116:240-247.
77. Nelson PT, Wang WX. MiR-107 is reduced in Alzheimer's disease brain neocortex: validation study. J Alzheimers Dis. 2010;21:75-79.
78. Wang WX, Rajeev BW, Stromberg AJ, et al. 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. 2008;28:1213-1223.
79. Geekiyanage H, Chan C. MicroRNA-137/181c regulates serine palmitoyltransferase and in turn amyloid β, novel targets in sporadic Alzheimer's disease. J Neurosci. 2011;31:14820-14830.
80. Hébert SS, Horré K, Nicolaï L, et al. Loss of microRNA cluster miR- 29a/b-1 in sporadic Alzheimer's disease correlates with increased BACE1/β- secretase expression. Proc Natl Acad Sci U S A. 2008;105:6415-6422.
81. Schonrock N, Humphreys DT, Preiss T, Götz J. Target gene repression mediated by miRNAs miR-181c and miR-9 both of which are down-regulated by amyloid-β. J Mol Neurosci. 2012;46:324-335.
82. Schonrock N, Ke YD, Humphreys D, et al. Neuronal microRNA deregulation in response to Alzheimer's disease amyloid-beta. PLoS One. 2010;5:e11070.
83. Absalon S, Kochanek DM, Raghavan V, Krichevsky AM. MiR-26b, upregulated in Alzheimer's disease, activates cell cycle entry, tau-phosphorylation, and apoptosis in postmitotic neurons. J Neurosci. 2013;33:14645- 14659.
84. Long JM, Ray B, Lahiri DK. MicroRNA-153 physiologically inhibits expression of amyloid-β precursor protein in cultured human fetal brain cells and is dysregulated in a subset of Alzheimer disease patients. J Biol Chem. 2012;287:31298-31310.
85. Zovoilis A, Agbemenyah HY, Agis-Balboa RC, et al. MicroRNA-34c is a novel target to treat dementias. EMBO J. 2011;30:4299-4308.
86. Lukiw WJ, Zhao Y, Cui JG. An NF-kappaB-sensitive micro RNA-146amediated inflammatory circuit in Alzheimer disease and in stressed human brain cells. J Biol Chem. 2008;283:31315-31322.
87. Long JM, Ray B, Lahiri DK. MicroRNA-339-5p down-regulates protein expression of β-site amyloid precursor protein-cleaving enzyme 1 (BACE1) in human primary brain cultures and is reduced in brain tissue specimens of Alzheimer disease subjects. J Biol Chem. 2014;289:5184-5198.
88. Nunez-Iglesias J, Liu CC, Morgan TE, Finch CE, Zhou XJ. Joint genomewide profiling of miRNA and mRNA expression in Alzheimer's disease cortex reveals altered miRNA regulation. PLoS One. 2010;5:e8898.
89. Persengiev S, Kondova I, Otting N, Koeppen AH, Bontrop RE. Genome- wide analysis of miRNA expression reveals a potential role for miR- 144 in brain aging and spinocerebellar ataxia pathogenesis. Neurobiol Aging. 2011;32:2316.e17-27.
90. Shioya M, Obayashi S, Tabunoki, H, et al. Aberrant microRNA expression in the brains of neurodegenerative diseases: miR-29a decreased in Alzheimer disease brains targets neurone navigator 3. Neuropathol Appl Neurobiol. 2010;36:320-330.
91. Geekiyanage H, Jicha GA, Nelson PT, Chan C. Blood serum miRNA: non-invasive biomarkers for Alzheimer's disease. Exp Neurol. 2012;235:491- 496.
92. Braidy N, Jayasena T, Poljak A, Sachdev PS. Sirtuins in cognitive ageing and Alzheimer's disease. Curr Opin Psychiatry. 2012;25:226-230.
93. Min SW, Sohn PD, Cho SH, Swanson RA, Gan L. Sirtuins in neurodegenerative diseases: an update on potential mechanism. Front Aging Neurosci. 2013;5:1.
94. Moon JM, Xu L, Giffard RG. Inhibition of microRNA-181 reduces forebrain ischemia-induced neuronal loss. J Cereb Blood Flow Metab. 2013;33:1976-1982.
95. Ouyang YB, Lu Y, Yue S, Giffard RG. MiR-181 targets multiple Bcl-2 family members and influences apoptosis and mitochondrial function in astrocytes. Mitochondrion. 2012;12:213-219.
96. Zhang L, Dong LY, Li YJ, Hong Z, Wei WS. The microRNA miR-181c controls microglia-mediated neuronal apoptosis by suppressing tumor necrosis factor. J Neuroinflammation. 2012;9:211.
97. Barak B, Shvarts-Serebro I, Modai S, et al. Opposing actions of environmental enrichment and Alzheimer's disease on the expression of hippocampal microRNAs in mouse models. Transl Psychiatry. 2013;3:e304.
98. Delay C, Hébert SS. MicroRNAs and Alzheimer's disease mouse models: current insights and future research avenues. Int J Alzheimer's Disease. 2011; ID894938.
99. Wang X, Liu P, Zhu H, et al. MiR-34a, a microRNA up-regulated in a double transgenic mouse model of Alzheimer's disease, inhibits bcl2 translation. Brain Res Bull. 2009;80:268-273.
100. Boissoneault V, Plante I, Rivest S, Provost P. MicroRNA-298 and microRNA- 328 regulate expression of mouse beta-amyloid precursor protein- converting enzyme 1. J Biol Chem. 2009;284:1971-1981.
101. Li YY, Cui JG, Hill JM, Bhattacharjee S, Zhao Y, Lukiw WJ. Increased expression of miRNA-146a in Alzheimer's disease transgenic mouse models. Neurosci Lett. 2011;487:94-98.
102. Liu W, Liu C, Zhu J, et al. MicroRNA-16 targets amyloid precursor protein to potentially modulate Alzheimer's-associated pathogenesis in SAMP8 mice. Neurobiol Aging. 2012;33:522-534.
103. Zhang R, Zhang Q, Niu J. Screening of microRNAs associated with Alzheimer's disease using oxidative stress cell model and different strains of senescence accelerated mice. J Neurol Sci. 2014;338:57-64.
104. Caraci F, Spampinato S, Sortino MA, et al. Dysfunction of TGF-β1 signaling in Alzheimer's disease: perspectives for neuroprotection. Cell Tissue Res. 2012;347:291-301.
105. Li JJ, Dolios G, Wang R, Liao FF. Soluble beta-amyloid peptides, but not insoluble fibrils, have specific effect on neuronal microRNA expression. PLoS One. 2014;9:e90770.
106. Tackenberg C, Grinschgl S, Trutzel A, et al. NMDA receptor subunit composition determines beta-amyloid-induced neurodegeneration and synaptic loss. Cell Death Dis. 2013;4:e608.
107. Xu S, Zhang R, Niu J, Cui D, et al. Oxidative stress mediated-alterations of the microRNA expression profile in mouse hippocampal neurons. Int J Mol Sci. 2012;13:16945-169-160.
108. Chio CC, Lin JW, Cheng HA, et al. MicroRNA-210 targets antiapoptotic Bcl-2 expression and mediates hypoxia-induced apoptosis of neuroblastoma cells. Arch Toxicol. 2013;87:459-468.
109. Lukiw WJ, Andreeva TV, Grigorenko AP, Rogaev EI. Studying microRNA function and dysfunction in Alzheimer's disease. Front Genet. 2013;3:327.
110. Wang LL, Huang Y, Wang G, Chen SD. The potential role of microRNA- 146 in Alzheimer's disease: biomarker or therapeutic target? Med Hypotheses. 2012;78:398-401.
111. Boldin MP, Baltimore D. MicroRNAs, new effectors and regulators of NF-ΚB. Immunol Rev. 2012;246:205-220.
112. Lukiw WJ, Alexandrov PN. Regulation of complement factor H (CFH) by multiple miRNAs in Alzheimer's disease (AD) brain. Mol Neurobiol. 2012;46:11-19.
113. Zhao Y, Bhattacharjee S, Jones BM, Hill J, Dua P, Lukiw WJ. Regulation of neurotropic signaling by the inducible, NF-kB-Sensitive miRNA-125b in Alzheimer's disease (AD) and in primary human neuronal-glial (HNG) cells. Mol Neurobiol. In press.
114. Toh H, Chitramuthu BP, Bennett HP, Bateman A. Structure, function, and mechanism of progranulin; the brain and beyond. J Mol Neurosci. 2011; 45:538-548.
115. Wang WX, Wilfred BR, Madathil SK. MiR-107 regulates granulin/progranulin with implications for traumatic brain injury and neurodegenerative disease. Am J Pathol. 2010;177:334-345.
116. Lukiw WJ, Alexandrov PN, Zhao Y, Hill JM, Bhattacharjee S. Spreading of Alzheimer's disease inflammatory signaling through soluble micro- RNA. Neuroreport. 2012;23:621-626.
117. Lehmann SM, Krüger C, Park B, et al. An unconventional role for miRNA: let-7 activates Toll-like receptor 7 and causes neurodegeneration. Nat Neurosci. 2012;15:827-835.
118. Liang C, Zhu H, Xu Y, et al. MicroRNA-153 negatively regulates the expression of amyloid precursor protein and amyloid precursor-like protein 2. Brain Res. 2012;1455:103-113.
119. Hébert SS, Horré K, Nicolaï L, et al. MicroRNA regulation of Alzheimer's amyloid precursor protein expression. Neurobiol Disease. 2009;33:422- 428.
120. Patel N, Hoang D, Miller N, et al. MicroRNAs can regulate human APP levels. Mol Neurodegen. 2008;3:10.
121. Roshan R, Ghosh T, Gadgil M, Pillai B. Regulation of BACE1 by miR-29a/b in a cellular model of Spinocerebellar Ataxia 17. RNA Biol. 2012;9:891-899.
122. Faghihi MA, Zhang M, Huang J, et al. Evidence for natural antisense transcript-mediated inhibition of microRNA function. Genome Biol. 2010;11:R56.
123. Fang, M, Wang J, Zhang X, et al. The miR-124 regulates the expression of BACE1/β-secretase correlated with cell death in Alzheimer's disease. Toxicol Lett. 2012;209:94-105.
124. Sala Frigerio C, Lau P, Salta E, et al. Reduced expression of hsa-miR- 27a-3p in CSF of patients with Alzheimer disease. Neurology. 2013;81:2103- 2106.
125. Zhang C, Browne A, Child D, Divito JR, Stevenson JA, Tanzi RE. Loss of function of ATXN1 increases amyloid beta-protein levels by potentiating beta-secretase processing of beta-amyloid precursor protein. J Biol Chem. 2010;285:8515-8526.
126. Augustin R, Endres K, Reinhardt S, Kuhn PH, Lichtenthaler SF, Hansen J. Computational identification and experimental validation of microRNAs binding to the Alzheimer-related gene ADAM10. BMC Med Genet. 2012;13:35.
127. Cheng C, Li W, Zhang Z. MicroRNA-144 is regulated by activator protein-1 (AP-1) and decreases expression of Alzheimer disease-related alpha-disintegrin and metalloprotease 10 (ADAM10). J Biol Chem. 2013;288:13748-13761.
128. Xu D, Sharma C, Hemler ME. Tetraspanin12 regulates ADAM10-dependent cleavage of amyloid precursor protein. FASEB J. 2009;23:3674-3681.
129. Lukiw WJ. NF-kB-regulated microRNAs (miRNAs) in primary human brain cells. Exp Neurol. 2012;235:484-490.
130. Irwin DJ, Cohen TJ, Grossman M, et al. Acetylated tau, a novel pathological signature in Alzheimer's disease and other tauopathies. Brain. 2012;135:807-818.
131. Dickson JR, Kruse C, Montagna DR, Finsen B, Wolfe MS. Alternative polyadenylation and miR-34 family members regulate tau expression. J Neurochem. 2013;127:739-749.
132. Hébert SS, Papadopoulou AS, Smith P, et al. Genetic ablation of Dicer in adult forebrain neurons results in abnormal tau hyperphosphorylation and neurodegeneration. Hum Mol Genet. 2010;19:3959-3969.
133. Moncini S, Salvi A, Zuccotti P, et al. The role of miR-103 and miR-107 in regulation of CDK5R1 expression and in cellular migration. PloS One. 2011;6:e20038.
134. Aranha MM, Santos DM, Solá S, Steer CJ, Rodrigues CM. miR-34a regulates mouse neural stem cell differentiation. PLoS One. 2011;6:e21396.
135. Im HI, Kenny PJ. MicroRNAs in neuronal function and dysfunction. Trends Neurosci. 2012;35:325-334.
136. Yamakuchi M, Ferlito M, Lowenstein CJ. MiR-34a repression of SIRT1 regulates apoptosis. Proc Natl Acad Sci U S A. 2008;105:13421-13426.
137. Dajas-Bailador F, Bonev B, Garcez P, Stanley P, Guillemot F, Papalopulu N. MicroRNA-9 regulates axon extension and branching by targeting Map1b in mouse cortical neurons. Nat Neurosci. 2012 ;15 :697-699.
138. Haramati S, Chapnik E, Sztainberg Y miRNA malfunction causes spinal motor neuron disease. Proc Natl Acad Sci U S A. 2010;107:13111-13116.
139. Cohen JE, Lee PR, Chen S, Li W, Fields RD. MicroRNA regulation of homeostatic synaptic plasticity. Proc Natl Acad Sci U S A. 2011;108:11650- 11655.
140. Ouyang YB, Xu L, Yue S, Liu S, Giffard RG. Neuroprotection by astrocytes in brain ischemia: Importance of microRNAs. Neurosci Lett. 2014;565:53-58.
141. Wei C, Thatcher EJ, Olena AF miR-153 regulates SNAP-25, synaptic transmission, and neuronal development. PLoS One. 2013;8:e57080.
142. Edbauer D, Neilson JR, Foster KA, et al. Regulation of synaptic structure and function by FMRP-associated microRNAs miR-125b and miR-132. Neuron. 2010; 65:373-384.
143. Muddashetty RS, Nalavadi VC, Gross C. Reversible inhibition of PSD- 95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol Cell. 2011; 42;673-688.
144. Wibrand K, Pai B, Siripornmongcolchai T. MicroRNA regulation of the synaptic plasticity-related gene Arc. PLoS One. 2012;7:e41688.
145. Follert P, Cremer H, Béclin C. MicroRNAs in brain development and function: a matter of flexibility and stability. Front Mol Neurosci. 2014;7:5.
146. Gao J, Wang WY, Mao YW, et al. A novel pathway regulates memory and plasticity via SIRT1 and miR-134. Nature. 2010;466:1105-1109.
147. Mellios N, Huang HS, Grigorenko A, Rogaev E, Akbarian S. A set of differentially expressed miRNAs, including miR-30a-5p, act as posttranscriptional inhibitors of BDNF in prefrontal cortex. Hum Mol Genet. 2008;17:3030-3042.
148. Schratt GM, Tuebing F, Nigh EA. A brain-specific microRNA regulates dendritic spine development. Nature. 2006;439:283-289.
149. Garza-Manero S, Pichardo-Casas I, Arias C, Vaca L, Zepeda A. Selective distribution and dynamic modulation of miRNAs in the synapse and its possible role in Alzheimer's Disease. Brain Res. 2014. In press.
150. Bamburg JR, Bernstein BW, Davis RC, et al. ADF/Cofilin-actin rods in neurodegenerative diseases. Curr Alzheimer Res. 2010;7:241-250.
151. Impey S, Davare M, Lesiak A. An activity-induced microRNA controls dendritic spine formation by regulating Rac1-PAK signaling. Mol Cell Neurosci. 2010;43:146-156.
152. Siegel G, Obernosterer G, Fiore R, et al. A functional screen implicates microRNA-138-dependent regulation of the depalmitoylation enzyme APT1 in dendritic spine morphogenesis. Nat Cell Biol. 2009;11:705-716.
153. Yao J, Hennessey T, Flynt A, Lai E, Beal MF, Lin MT. MicroRNA-related cofilin abnormality in Alzheimer's disease. PLoS One. 2010;5:e15546.
154. Tian N, Cao Z, Zhang Y. MiR-206 decreases brain-derived neurotrophic factor levels in a transgenic mouse model of Alzheimer's disease. Neurosci Bull. 2014;30:191-187.
155. Lee ST, Chu K, Jung KH, et al. MiR-206 regulates brain-derived neurotrophic factor in Alzheimer disease model. Ann Neurol. 2012;72:269-77.
156. Ji G, Lv K, Chen H, et al. MiR-146a regulates SOD2 expression in H2O2 stimulated PC12 cells. PLoS One. 2013;8:e69351.
157. He M, Lu Y, Xu S, et al. MiRNA-210 modulates a nickel-induced cellular energy metabolism shift by repressing the iron-sulfur cluster assembly proteins ISCU1/2 in Neuro-2a cells. Cell Death Dis. 2014;5:e1090.
158. Isaya G. Mitochondrial iron-sulfur cluster dysfunction in neurodegenerative disease. Front Pharmacol. 2014;5:29.
159. Akhter R, Sanphui P, Biswas SC. The essential role of p53-up-regulated modulator of apoptosis (Puma) and its regulation by FoxO3a transcription factor in β-amyloid-induced neuron death. J Biol Chem. 2014;289:10812- 10822.
160. Wong HK, Veremeyko T, Patel N, et al. De-repression of FOXO3a death axis by microRNA-132 and -212 causes neuronal apoptosis in Alzheimer's disease. Hum Mol Genet. 2013;22:3077-3092.
161. Kole AJ, Swahari V, Hammond SM, Deshmukh M. MiR-29b is activated during neuronal maturation and targets BH3-only genes to restrict apoptosis. Genes Development. 2011;25:125-130.
162. Ouyang YB, Xu L, Lu Y. Astrocyte-enriched miR-29a targets PUMA and reduces neuronal vulnerability to forebrain ischemia. Glia. 2013;61:1784- 1794.
163. Hutchison ER, Kawamoto EM, Taub DD. Evidence for miR-181 involvement in neuroinflammatory responses of astrocytes. Glia. 2013; 61:1018- 10128.
164. Truettner JS, Motti D, Dietrich WD. MicroRNA overexpression increases cortical neuronal vulnerability to injury. Brain Res. 2013;1533:122- 130.
165. Bonda DJ, Lee HP, Kudo W, Zhu X, Smith MA, Lee HG. Pathological implications of cell cycle re-entry in Alzheimer disease. J Alzheimers Dis. 2001;3:377-385.
166. Seward ME, Swanson E, Norambuena A, et al. Amyloid-β signals through tau to drive ectopic neuronal cell cycle re-entry in Alzheimer's disease. J Cell Sci. 2013;126:1278-1286.
167. Ranganathan S, Scudiere S, Bowser R. Hyperphosphorylation of the retinoblastoma gene product and altered subcellular distribution of E2F-1 during Alzheimer's disease and amyotrophic lateral sclerosis. J Alzheimers Dis. 2001;3:377-385.
168. Riba A, Bosia C, El Baroudi M, Ollino L, Caselle M. A combination of transcriptional and microRNA regulation improves the stability of the relative concentrations of target genes. PLoS Comput Biol. 2014; Feb 27;10:e1003490.
169. Trompeter HI, Abbad H, Iwaniuk KM. MicroRNAs MiR-17, MiR-20a, and MiR-106b act in concert to modulate E2F activity on cell cycle arrest during neuronal lineage differentiation of USSC. PLoS One. 2011;6:e16138.
170. Ueberham U, Hilbrich I, Ueberham E, et al. Transcriptional control of cell cycle-dependent kinase 4 by Smad proteins-implications for Alzheimer's disease. Neurobiol Aging. 2012;33:2827-2840.
171. Wang H, Liu J, Zong Y, et al. MiR-106b aberrantly expressed in a double trangenic mouse model for Alzheimer's disease targets TGF-β type II receptor. Brain Res. 2010;1357:166-174.
172. Füllgrabe J, Klionsky DJ, Joseph B. The return of the nucleus: transcriptional and epigenetic control of autophagy. Nat Rev Mol Cell Biol. 2014;15:65-74.
173. Lee MJ, Lee JH, Rubinsztein DC. Tau degradation: the ubiquitin-proteasome system versus the autophagy-lysosome system. Prog Neurobiol. 2013;105:49-59.
174. Fenn AM, Smith KM, Lovett-Racke AE, Guerau-de-Arellano M, Whitacre CC, Godbout JP. Increased micro-RNA 29b in the aged brain correlates with the reduction of insulin-like growth factor-1 and fractalkine ligand. Neurobiol Aging. 2013;34:2748-2758.
175. Salminen A, Kaarniranta K, Kauppinen A, et al. Impaired autophagy and APP processing in Alzheimer's disease: the potential role of Beclin 1 interactome. Prog Neurobiol. 2013;106:33-54.
176. Tiribuzi R, Crispoltoni L, Porcellati S, et al. MiR128 up-regulation correlates with impaired amyloid β(1-42) degradation in monocytes from patients with sporadic Alzheimer's disease. Neurobiol Aging. 2014;35:345-356.
177. Carrettiero DC, Hernandez I, Neveu P, Papagiannakopoulos T, Kosik KS. The co-chaperone BAG2 sweeps paired helical filament-insoluble Tau from the microtubule. J Neurosci. 2009;29:2151-2161.
178. Massone S, Vassallo I, Fiorino G. 17A, a novel non-coding RNA, regulates GABA B alternative splicing and signaling in response to inflammatory stimuli and in Alzheimer disease. Neurobiol Dis. 2011;41:308-317.
179. Lukiw WJ Circular RNA (circRNA) in Alzheimer's disease (AD). Front Genet. 2013;4:307.
180. Landry CD, Kandel ER, Rajasethupathy P. New mechanisms in memory storage: piRNAs and epigenetics. Trends Neurosci. 2013;36:535-542.
181. Mus E, Hof PR, Tiedge H. Dendritic BC200 RNA in aging and in Alzheimer's disease. Proc Natl Acad Sci U S A. 2007;104:10679-10684.
182. Salta E, De Strooper B. Non-coding RNAs with essential roles in neurodegenerative disorders. Lancet Neurol. 2012;11:189-200.
183. Dorval V, Nelson PT, Hébert SS. Circulating microRNAs in Alzheimer's disease: the search for novel biomarkers. Front Mol Neurosci. 2013;6:24.
184. Sheinerman KS, Umansky SR. Circulating cell-free microRNA as biomarkers for screening, diagnosis and monitoring of neurodegenerative diseases and other neurologic pathologies. Front Cell Neurosci. 2013,7:150.
185. Wahlestedt C. Targeting long non-coding RNA to therapeutically upregulate gene expression. Nat Rev Drug Discov. 2013;12:433-446.