Browse > Article
http://dx.doi.org/10.5483/BMBRep.2016.49.12.184

Age-related epigenetic regulation in the brain and its role in neuronal diseases  

Kim-Ha, Jeongsil (Department of Integrative Bioscience and Biotechnology, College of Life Sciences, Sejong University)
Kim, Young-Joon (Department of Integrated Omics for Biomedical Science, Graduate School, Yonsei University)
Publication Information
BMB Reports / v.49, no.12, 2016 , pp. 671-680 More about this Journal
Abstract
Accumulating evidence indicates many brain functions are mediated by epigenetic regulation of neural genes, and their dysregulations result in neuronal disorders. Experiences such as learning and recall, as well as physical exercise, induce neuronal activation through epigenetic modifications and by changing the noncoding RNA profiles. Animal models, brain samples from patients, and the development of diverse analytical methods have broadened our understanding of epigenetic regulation in the brain. Diverse and specific epigenetic changes are suggested to correlate with neuronal development, learning and memory, aging and age-related neuronal diseases. Although the results show some discrepancies, a careful comparison of the data (including methods, regions and conditions examined) would clarify the problems confronted in understanding epigenetic regulation in the brain.
Keywords
Epigenetics; Learning and memory; Neurodegenerative diseases;
Citations & Related Records
연도 인용수 순위
  • Reference
1 Feng J, Fouse S and Fan G (2007) Epigenetic regulation of neural gene expression and neuronal function. Pediatr Res 61, 58R-63R   DOI
2 Graff J and Tsai LH (2013) The potential of HDAC inhibitors as cognitive enhancers. Annu Rev Pharmacol Toxicol 53, 311-330   DOI
3 Fischer A, Sananbenesi F, Wang XY, Dobbin M and Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447, 178-182   DOI
4 Graff J, Kim D, Dobbin MM and Tsai LH (2011) Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol Rev 91, 603-649   DOI
5 Kempermann G, Song H and Gage FH (2015) Neuro-genesis in the Adult Hippocampus. Cold Spring Harb Perspect Biol 7, a018812   DOI
6 Feng J, Zhou Y, Campbell SL et al (2010) Dnmt1 and Dnmt3a maintain DNA methylation and regulate synaptic function in adult forebrain neurons. Nat Neurosci 13, 423-430   DOI
7 Ma DK, Jang MH, Guo JU et al (2009) Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323, 1074-1077   DOI
8 Oh G, Ebrahimi S, Wang SC et al (2016) Epigenetic assimilation in the aging human brain. Genome Biol 17, 76   DOI
9 Bollati V, Schwartz J, Wright R et al (2009) Decline in genomic DNA methylation through aging in a cohort of elderly subjects. Mech Ageing Dev 130, 234-239   DOI
10 Chouliaras L, van den Hove DL, Kenis G et al (2012) Age-related increase in levels of 5-hydroxymethylcytosine in mouse hippocampus is prevented by caloric restriction. Curr Alzheimer Res 9, 536-544   DOI
11 Maegawa S, Hinkal G, Kim HS et al (2010) Widespread and tissue specific age-related DNA methylation changes in mice. Genome Res 20, 332-340   DOI
12 Geekiyanage H, Jicha GA, Nelson PT and Chan C (2012) Blood serum miRNA: non-invasive biomarkers for Alzheimer's disease. Exp Neurol 235, 491-496   DOI
13 Marques SC, Lemos R, Ferreiro E et al (2012) Epigenetic regulation of BACE1 in Alzheimer's disease patients and in transgenic mice. Neuroscience 220, 256-266   DOI
14 Lithner CU, Lacor PN, Zhao WQ et al (2013) Disruption of neocortical histone H3 homeostasis by soluble $A{\beta}$: implications for Alzheimer's disease. Neurobiol Aging 34, 2081-2090   DOI
15 Ogawa O, Zhu X, Lee HG et al (2003) Ectopic localization of phosphorylated histone H3 in Alzheimer's disease: a mitotic catastrophe? Acta Neuropathol 105, 524-528
16 Galimberti D, Villa C, Fenoglio C et al (2014) Circulating miRNAs as potential biomarkers in Alzheimer's disease. J Alzheimers Dis 42, 1261-1267   DOI
17 Kumar S and Reddy PH (2016) Are circulating microRNAs peripheral biomarkers for Alzheimer's disease? Biochim Biophys Acta 1862, 1617-1627   DOI
18 Modi PK, Jaiswal S and Sharma P (2015) Regulation of Neuronal Cell Cycle and Apoptosis by MicroRNA 34a. Mol Cell Biol 36, 84-94
19 Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C and Kubo M (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 41, 1303-1307   DOI
20 Ai SX, Xu Q, Hu YC et al (2014) Hypomethylation of SNCA in blood of patients with sporadic Parkinson's disease. J Neurol Sci 337, 123-128   DOI
21 Tan YY, Wu L, Zhao ZB et al (2014) Methylation of ${\alpha}$-synuclein and leucine-rich repeat kinase 2 in leukocyte DNA of Parkinson's disease patients. Parkinsonism Relat Disord 20, 308-313   DOI
22 Pedreira ME, Dimant B and Maldonado H (1996) Inhibitors of protein and RNA synthesis block context memory and long-term habituation in the crab Chas-magnathus. Pharmacol Biochem Behav 54, 611-617   DOI
23 Choudhuri S (2011) From Waddington's epigenetic land-scape to small noncoding RNA: some important milestones in the history of epigenetics research. Toxicol Mech Methods 21, 252-274   DOI
24 Lee SM, Kim-Ha J, Choi WY et al (2016) Interplay of genetic and epigenetic alterations in hepatocellular carcinoma. Epigenomics 8, 993-1005   DOI
25 Fischer A (2014) Epigenetic memory: the Lamarckian brain. EMBO J 33, 945-967   DOI
26 Maharana C, Sharma KP and Sharma SK (2010) Depolarization induces acetylation of histone H2B in the hippocampus. Neuroscience 167, 354-360   DOI
27 Guo JU, Ma DK, Mo H et al (2011) Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat Neurosci 14, 1345-1351   DOI
28 Tan M, Luo H, Lee S et al (2011) Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 146, 1016-1028   DOI
29 Chwang WB, Arthur JS, Schumacher A and Sweatt JD (2007) The nuclear kinase mitogen-and stress-activated protein kinase 1 regulates hippocampal chromatin remodeling in memory formation. J Neurosci 27, 12732-12742   DOI
30 Peters MJ, Joehanes R, Pilling LC et al (2015) The transcriptional landscape of age in human peripheral blood. Nat Commun 6, 8570   DOI
31 Peleg S, Sananbenesi F, Zovoilis A et al (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328, 753-756   DOI
32 Chouliaras L, van den Hove DL, Kenis G et al (2013) Histone deacetylase 2 in the mouse hippocampus: attenuation of age-related increase by caloric restriction. Curr Alzheimer Res 10, 868-876   DOI
33 Persengiev S, Kondova I, Otting N, Koeppen AH and Bontrop RE (2011) Genome-wide analysis of miRNA expression reveals a potential role for miR-144 in brain aging and spinocerebellar ataxia pathogenesis. Neurobiol Aging 32, 2316.e17-27   DOI
34 Inukai S, de Lencastre A, Turner M and Slack F (2012) Novel microRNAs differentially expressed during aging in the mouse brain. PLoS One 7, e40028   DOI
35 Noren Hooten N, Abdelmohsen K, Gorospe M, Ejiogu N, Zonderman AB and Evans MK (2010) microRNA expression patterns reveal differential expression of target genes with age. PLoS One 5, e10724   DOI
36 Kontopoulos E, Parvin JD and Feany MB (2006) Alpha-synuclein acts in the nucleus to inhibit histone acetylation and promote neurotoxicity. Hum Mol Genet 15, 3012-3023   DOI
37 Desplats P, Spencer B, Coffee E et al (2011) Alpha-synuclein sequesters Dnmt1 from the nucleus: a novel mechanism for epigenetic alterations in Lewy body diseases. J Biol Chem 286, 9031-9037   DOI
38 Coupland KG, Mellick GD, Silburn PA et al (2014) DNA methylation of the MAPT gene in Parkinson's disease cohorts and modulation by vitamin E in vitro. Mov Disord 29, 1606-1614   DOI
39 Goers J, Manning-Bog AB, McCormack AL et al (2003) Nuclear localization of alpha-synuclein and its interaction with histones. Biochemistry 42, 8465-8471   DOI
40 Song C, Kanthasamy A, Anantharam V, Sun F and Kanthasamy AG (2010) Environmental neurotoxic pesticide increases histone acetylation to promote apoptosis in dopaminergic neuronal cells: relevance to epigenetic mechanisms of neurodegeneration. Mol Pharmacol 77, 621-632   DOI
41 Doxakis E (2010) Post-transcriptional regulation of alpha-synuclein expression by mir-7 and mir-153. J Biol Chem 285, 12726-12734   DOI
42 Junn E, Lee KW, Jeong BS, Chan TW, Im JY and Mouradian MM (2009) Repression of alpha-synuclein expression and toxicity by microRNA-7. Proc Natl Acad Sci U S A 106, 13052-13057   DOI
43 Xu W, Tan L and Yu JT (2015) Link between the SNCA gene and parkinsonism. Neurobiol Aging 36, 1505-1518   DOI
44 Adlakha YK and Saini N (2014) Brain microRNAs and insights into biological functions and therapeutic potential of brain enriched miRNA-128. Mol Cancer 13, doi: 10.1186/1476-4598-13-33   DOI
45 Arguello AA, Ye X, Bozdagi O et al (2013) CCAAT enhancer binding protein ${\delta}$ plays an essential role in memory consolidation and reconsolidation. J Neurosci 33, 3646-3658   DOI
46 Alberini CM and Kandel ER (2014) The regulation of transcription in memory consolidation. Cold Spring Harb Perspect Biol 7, a021741
47 Nott A, Watson PM, Robinson JD, Crepaldi L and Riccio A (2008) S-Nitrosylation of histone deacetylase 2 induces chromatin remodelling in neurons. Nature 455, 411-415   DOI
48 Tweedie-Cullen RY, Brunner AM, Grossmann J et al (2012) Identification of combinatorial patterns of post-translational modifications on individual histones in the mouse brain. PLoS One 7, e36980   DOI
49 Graff J and Tsai LH (2013) Histone acetylation: molecular mnemonics on the chromatin. Nat Rev Neurosci 14, 97-111   DOI
50 Hsieh J and Zhao X (2016) Genetics and Epigenetics in Adult Neurogenesis. Cold Spring Harb Perspect Biol 8, pii: a018911   DOI
51 Lungu G, Stoica G and Ambrus A (2013) MicroRNA profiling and the role of microRNA-132 in neuro-degeneration using a rat model. Neurosci Lett 553, 153-158   DOI
52 Yin L, Sun Y, Wu J et al (2015) Discovering novel microRNAs and age-related nonlinear changes in rat brains using deep sequencing. Neurobiol Aging 36, 1037-1044   DOI
53 Kim J, Yoon H, Chung DE, Brown JL, Belmonte KC and Kim J (2016) miR-186 is decreased in aged brain and suppresses BACE1 expression. J Neurochem 137, 436-445   DOI
54 Chouliaras L, Mastroeni D, Delvaux E et al (2013) Consistent decrease in global DNA methylation and hydroxymethylation in the hippocampus of Alzheimer's disease patients. Neurobiol Aging 34, 2091-2099   DOI
55 Kanagaraj N, Beiping H, Dheen ST and Tay SS (2014) 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, 167-179   DOI
56 Kim J, Inoue K, Ishii J et al (2007) A MicroRNA feedback circuit in midbrain dopamine neurons. Science 317, 1220-1224   DOI
57 Margis R, Margis R and Rieder CRM (2011) Identification of blood microRNAs associated to Parkinson's disease. J Biotechnol 152, 96-101   DOI
58 Cardo LF, Coto E, de Mena L et al (2013) Profile of microRNAs in the plasma of Parkinson's disease patients and healthy controls. J Neurol 260, 1420-1422   DOI
59 Hoss AG, Labadorf A, Beach TG, Latourelle JC and Myers RH (2016) microRNA Profiles in Parkinson's Disease Prefrontal Cortex. Front Aging Neurosci 8, 36
60 Cheng LC, Pastrana E, Tavazoie M and Doetsch F (2009) miR-124 regulates adult neurogenesis in the subventri-cular zone stem cell niche. Nat Neurosci 12, 399-408   DOI
61 Santos MC, Tegge AN, Correa BR et al (2016) miR-124, -128, and -137 Orchestrate Neural Differentiation by Acting on Overlapping Gene Sets Containing a Highly Connected Transcription Factor Network. Stem Cells 34, 220-232   DOI
62 Kim SN, Rhee JH, Song YH et al (2005) Age-dependent changes of gene expression in the Drosophila head. Neurobiol Aging 26, 1083-1091   DOI
63 Berchtold NC, Sabbagh MN, Beach TG, Kim RC, Cribbs DH and Cotman CW (2014) Brain gene expression patterns differentiate mild cognitive impairment from normal aged and Alzheimer's disease. Neurobiol Aging 35, 1961-1972   DOI
64 Talens RP, Christensen K, Putter H et al (2012) Epigenetic variation during the adult lifespan: cross-sectional and longitudinal data on monozygotic twin pairs. Aging Cell 11, 694-703   DOI
65 West RL, Lee JM and Maroun LE (1995) Hypomethylation of the amyloid precursor protein gene in the brain of an Alzheimer's disease patient. J Mol Neurosci 6, 141-146   DOI
66 Morrison LD, Smith DD and Kish SJ (1996) Brain S-adenosylmethionine levels are severely decreased in Alzheimer's disease. J Neurochem 67, 1328-1331
67 Coppieters N, Dieriks BV, Lill C, Faull RL, Curtis MA and Dragunow M (2014) Global changes in DNA methylation and hydroxymethylation in Alzheimer's disease human brain. Neurobiol Aging 35, 1334-1344   DOI
68 Sanchez-Mut JV and Graff J (2015) Epigenetic Alterations in Alzheimer's Disease. Front Behav Neurosci 9, 347
69 Barrachina M and Ferrer I (2009) DNA methylation of Alzheimer disease and tauopathy-related genes in postmortem brain. J Neuropathol Exp Neurol 68, 880-891   DOI
70 Wang SC, Oelze B and Schumacher A (2008) Age-specific epigenetic drift in late-onset Alzheimer's disease. PLoS One 3, e2698   DOI
71 De Jager PL, Srivastava G, Lunnon K et al (2014) Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci 17, 1156-1163   DOI
72 Lunnon K, Smith R, Hannon E et al (2014) Methylomic profiling implicates cortical deregulation of ANK1 in Alzheimer's disease. Nat Neurosci 17, 1164-1170   DOI
73 Hu Y, Chopra V, Chopra R et al (2011) Transcriptional modulator H2A histone family, member Y (H2AFY) marks Huntington disease activity in man and mouse. Proc Natl Acad Sci U S A 108, 17141-17146   DOI
74 Nucifora FC Jr, Sasaki M, Peters MF et al (2001) Interference by huntingtin and atrophin-1 with cbp-mediated transcription leading to cellular toxicity. Science 291, 2423-2428   DOI
75 Steffan JS, Bodai L, Pallos J et al (2001) Histone deacetylase inhibitors arrest polyglutamine-dependent neurodegeneration in Drosophila. Nature 413, 739-743   DOI
76 Sadri-Vakili G, Bouzou B, Benn CL et al (2007) Histones associated with downregulated genes are hypo-acetylated in Huntington's disease models. Hum Mol Genet 16, 1293-1306   DOI
77 Ng CW, Yildirim F, Yap YS et al (2013) Extensive changes in DNA methylation are associated with expression of mutant huntingtin. Proc Natl Acad Sci U S A 110, 2354-2359   DOI
78 Ricobaraza A, Cuadrado-Tejedor M, Perez-Mediavilla A, Frechilla D, Del Rio J and Garcia-Osta A (2009) Phenylbutyrate ameliorates cognitive deficit and reduces tau pathology in an Alzheimer's disease mouse model. Neuropsychopharmacology 34, 1721-1732   DOI
79 Graff J, Rei D, Guan JS et al (2012) An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 483, 222-226   DOI
80 Ryu H, Lee J, Hagerty SW et al (2006) ESET/SETDB1 gene expression and histone H3 (K9) trime-thylation in Huntington's disease. Proc Natl Acad Sci U S A 103, 19176-19181   DOI
81 De Souza RA, Islam SA, McEwen LM et al (2016) DNA methylation profiling in human Huntington's disease brain. Hum Mol Genet 25, 2013-2030   DOI
82 Diez-Planelles C, Sanchez-Lozano P, Crespo MC et al (2016) Circulating microRNAs in Huntington's disease: Emerging mediators in metabolic impairment. Pharmacol Res 108, 102-110   DOI
83 Conaco C, Otto S, Han JJ and Mandel G (2006) Reciprocal actions of REST and microRNA promote neuronal identity. Proc Natl Acad Sci U S A 103, 2422-2427   DOI
84 Jung HJ and Suh Y (2014) Circulating miRNAs in ageing and ageing-related diseases. J Genet Genomics 41, 465-472   DOI
85 Soldati C, Bithell A, Johnston C, Wong KY, Stanton LW and Buckley NJ (2013) Dysregulation of REST-regulated coding and non-coding RNAs in a cellular model of Huntington's disease. J Neurochem 124, 418-430   DOI
86 Savas JN, Makusky A, Ottosen S et al (2008) Huntington's disease protein contributes to RNA-mediated gene silencing through association with Argonaute and P bodies. Proc Natl Acad Sci U S A 105, 10820-10825   DOI
87 Machida T, Tomofuji T, Ekuni D et al (2015) MicroRNAs in Salivary Exosome as Potential Biomarkers of Aging. Int J Mol Sci 16, 21294-21309   DOI