Genome-wide alteration of 5-hydroxymenthylcytosine in a mouse model of Alzheimer's disease

BMC Genomics

Volumn 17, Issue 1, 2016, Pages

  Shu, Liqi ^a   Sun, Wenjia ^b   Li, Liping ^c   Xu, Zihui ^a,d   Lin, Li ^a   Xie, Pei ^c   Shen, Hui ^c   Huang, Luoxiu ^a   Xu, Qi ^e   Jin, Peng ^a   Li, Xuekun ^c  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b ZHEJIANG UNIVERSITY   (China)

^c ZHEJIANG UNIVERSITY SCHOOL OF MEDICINE   (China)

^d WUHAN CENTRAL HOSPITAL   (China)

^e PEKING UNION MEDICAL COLLEGE   (China)

Author keywords

5 hydroxymethylcytosine; Alzheimer's disease; Amyloid peptide; DNA demethylation

Indexed keywords

5 HYDROXYMETHYLCYTOSINE; AMYLOID BETA PROTEIN[1-42]; 5 METHYLCYTOSINE; 5-HYDROXYMETHYLCYTOSINE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN;

ADULT; AGED; AGING; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN CORTEX; CELL FUNCTION; CELL SURVIVAL; CEREBELLUM; CONTROLLED STUDY; DEMETHYLATION; DIFFERENTIALLY HYDROXYMETHYLATED REGION; DNA STRUCTURE; EPIGENETICS; EXON; GENE ONTOLOGY; GENOME; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; INTRON; MOUSE; MOUSE MODEL; NERVE CELL DIFFERENTIATION; NONHUMAN; PATHOGENESIS; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; CELL LINE; DISEASE MODEL; DNA METHYLATION; GENETIC EPIGENESIS; GENETICS; GENOME-WIDE ASSOCIATION STUDY; HUMAN; METABOLISM; TRANSGENIC MOUSE;

5-METHYLCYTOSINE; AGING; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CELL LINE; DISEASE MODELS, ANIMAL; DNA METHYLATION; EPIGENESIS, GENETIC; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MICE; MICE, TRANSGENIC;

EID: 84974602567     PISSN: None     EISSN: 14712164     Source Type: Journal    
DOI: 10.1186/s12864-016-2731-1     Document Type: Article

References (51)

1. Duyckaerts C, Delatour B, Potier MC. Classification and basic pathology of Alzheimer disease. Acta Neuropathol. 2009;118:5-36.
2. Finder VH. Alzheimer's disease: a general introduction and pathomechanism. J Alzheimers Dis. 2010;22 Suppl 3:5-19.
3. Gapp K, Woldemichael BT, Bohacek J, Mansuy IM. Epigenetic regulation in neurodevelopment and neurodegenerative diseases. Neuroscience. 2014;264:99-111.
4. Chouliaras L, Rutten BP, Kenis G, Peerbooms O, Visser PJ, Verhey F, van Os J, Steinbusch HW, van den Hove DL. Epigenetic regulation in the pathophysiology of Alzheimer's disease. Prog Neurobiol. 2010;90:498-510.
5. Bergman Y, Cedar H. DNA methylation dynamics in health and disease. Nat Struct Mol Biol. 2013;20:274-81.
6. Jakovcevski M, Akbarian S. Epigenetic mechanisms in neurological disease. Nat Med. 2012;18:1194-204.
7. Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet. 2003;33(Suppl):245-54.
8. Chouliaras L, Mastroeni D, Delvaux E, Grover A, Kenis G, Hof PR, Steinbusch, HW, Coleman PD, Rutten BP, van den Hove DL. Consistent decrease in global DNA methylation and hydroxymethylation in the hippocampus of Alzheimer's disease patients. Neurobiol Aging. 2013;34:2091-9.
9. Coppieters N, Dragunow M. Epigenetics in Alzheimer's disease: a focus on DNA modifications. Curr Pharm Des. 2011;17:3398-412.
10. 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.
11. De Jager PL, Srivastava G, Lunnon K, Burgess J, Schalkwyk LC, Yu L, Eaton ML, Keenan BT, Ernst J, McCabe C, et al. Alzheimer's disease: early alterations in brain DNA methylation at ANK1, BIN1, RHBDF2 and other loci. Nat Neurosci. 2014;17:1156-63.
12. Lunnon K, Smith R, Hannon E, De Jager PL, Srivastava G, Volta M, Troakes C, Al-Sarraj S, Burrage J, Macdonald R, et al. Methylomic profiling implicates cortical deregulation of ANK1 in Alzheimer's disease. Nat Neurosci. 2014;17:1164-70.
13. Siegmund KD, Connor CM, Campan M, Long TI, Weisenberger DJ, Biniszkiewicz D, Jaenisch R, Laird PW, Akbarian S. DNA methylation in the human cerebral cortex is dynamically regulated throughout the life span and involves differentiated neurons. PLoS One. 2007;2:e895.
14. Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J. Epigenetic changes in Alzheimer's disease: decrements in DNA methylation. Neurobiol Aging. 2010;31:2025-37.
15. Bakulski KM, Dolinoy DC, Sartor MA, Paulson HL, Konen JR, Lieberman AP, Albin RL, Hu H, Rozek LS. 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.
16. Barrachina M, Ferrer I. DNA methylation of Alzheimer disease and tauopathy-related genes in postmortem brain. J Neuropathol Exp Neurol. 2009;68:880-91.
17. Wang SC, Oelze B, Schumacher A. Age-specific epigenetic drift in late-onset Alzheimer's disease. PLoS One. 2008;3:e2698.
18. Fuso A, Seminara L, Cavallaro RA, D'Anselmi F, Scarpa S. S-adenosylmethionine/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.
19. Kriaucionis S, Heintz N. The nuclear DNA base 5-hydroxymethylcytosine is present in Purkinje neurons and the brain. Science. 2009;324:929-30.
20. Szulwach KE, Li X, Li Y, Song CX, Wu H, Dai Q, Irier H, Upadhyay AK, Gearing M, Levey AI, et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat Neurosci. 2011;14:1607-16.
21. Jin SG, Wu X, Li AX, Pfeifer GP. Genomic mapping of 5-hydroxymethylcytosine in the human brain. Nucleic Acids Res. 2011;39:5015-24.
22. Gu TP, Guo F, Yang H, Wu HP, Xu GF, Liu W, Xie ZG, Shi L, He X, Jin SG, et al. The role of Tet3 DNA dioxygenase in epigenetic reprogramming by oocytes. Nature. 2011;477:606-10.
23. Ito S, Shen L, Dai Q, Wu SC, Collins LB, Swenberg JA, He C, Zhang Y. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science. 2011;333:1300-3.
24. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, Agarwal S, Iyer LM, Liu DR, Aravind L, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science. 2009;324:930-5.
25. Wang T, Pan Q, Lin L, Szulwach KE, Song CX, He C, Wu H, Warren ST, Jin P, Duan R, et al. Genome-wide DNA hydroxymethylation changes are associated with neurodevelopmental genes in the developing human cerebellum. Hum Mol Genet. 2012;21:5500-10.
26. Song CX, Szulwach KE, Fu Y, Dai Q, Yi C, Li X, Li Y, Chen CH, Zhang W, Jian X, et al. Selective chemical labeling reveals the genome-wide distribution of 5-hydroxymethylcytosine. Nat Biotechnol. 2011;29:68-72.
27. Ficz G, Branco MR, Seisenberger S, Santos F, Krueger F, Hore TA, Marques CJ, Andrews S, Reik W. Dynamic regulation of 5-hydroxymethylcytosine in mouse ES cells and during differentiation. Nature. 2011;473:398-402.
28. Pastor WA, Pape UJ, Huang Y, Henderson HR, Lister R, Ko M, McLoughlin EM, Brudno Y, Mahapatra S, Kapranov P, et al. Genome-wide mapping of 5-hydroxymethylcytosine in embryonic stem cells. Nature. 2011;473:394-7.
29. Wu H, Zhang Y. Mechanisms and functions of Tet protein-mediated 5-methylcytosine oxidation. Genes Dev. 2011;25:2436-52.
30. Szulwach KE, Li X, Li Y, Song CX, Han JW, Kim S, Namburi S, Hermetz K, Kim JJ, Rudd MK, et al. Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet. 2011;7:e1002154.
31. Etchegaray JP, Chavez L, Huang Y, Ross KN, Choi J, Martinez-Pastor B, Walsh RM, Sommer CA, Lienhard M, Gladden A, et al. The histone deacetylase SIRT6 controls embryonic stem cell fate via TET-mediated production of 5-hydroxymethylcytosine. Nat Cell Biol. 2015;17:545-57.
32. Choi I, Kim R, Lim HW, Kaestner KH, Won KJ. 5-hydroxymethylcytosine represses the activity of enhancers in embryonic stem cells: a new epigenetic signature for gene regulation. BMC Genomics. 2014;15:670.
33. Hahn MA, Qiu R, Wu X, Li AX, Zhang H, Wang J, Jui J, Jin SG, Jiang Y, Pfeifer GP, et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell Rep. 2013;3:291-300.
34. Deplus R, Delatte B, Schwinn MK, Defrance M, Mendez J, Murphy N, Dawson MA, Volkmar M, Putmans P, Calonne E, et al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J. 2013;32:645-55.
35. Mellen M, Ayata P, Dewell S, Kriaucionis S, Heintz N. MeCP2 binds to 5hmC enriched within active genes and accessible chromatin in the nervous system. Cell. 2012;151:1417-30.
36. Wang F, Yang Y, Lin X, Wang JQ, Wu YS, Xie W, Wang D, Zhu S, Liao YQ, Sun Q, et al. Genome-wide loss of 5-hmC is a novel epigenetic feature of Huntington's disease. Hum Mol Genet. 2013;22:3641-53.
37. Yao B, Lin L, Street RC, Zalewski ZA, Galloway JN, Wu H, Nelson DL, Jin P. Genome-wide alteration of 5-hydroxymethylcytosine in a mouse model of fragile X-associated tremor/ataxia syndrome. Hum Mol Genet. 2013; in press.
38. Condliffe D, Wong A, Troakes C, Proitsi P, Patel Y, Chouliaras L, Fernandes C, Cooper J, Lovestone S, Schalkwyk L, et al. Cross-region reduction in 5-hydroxymethylcytosine in Alzheimer's disease brain. Neurobiol Aging. 2014;35:1850-4.
39. Bradley-Whitman MA, Lovell MA. Epigenetic changes in the progression of Alzheimer's disease. Mech Ageing Dev. 2013;134:486-95.
40. 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;35:1334-44.
41. Cadena-Del-Castillo C, Valdes-Quezada C, Carmona-Aldana F, Arias C, Bermudez-Rattoni F, Recillas-Targa F. Age-dependent increment of hydroxymethylation in the brain cortex in the triple-transgenic mouse model of Alzheimer's disease. J Alzheimers Dis. 2014; in press.
42. Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, et al. Model-based analysis of ChIP-Seq (MACS). Genome Biol. 2008;9:R137.
43. Mastroeni D, McKee A, Grover A, Rogers J, Coleman PD. Epigenetic differences in cortical neurons from a pair of monozygotic twins discordant for Alzheimer's disease. PLoS One. 2009;4:e6617.
44. Van den Hove DL, Kompotis K, Lardenoije R, Kenis G, Mill J, Steinbusch HW, Lesch KP, Fitzsimons CP, De Strooper B, Rutten BP. Epigenetically regulated microRNAs in Alzheimer's disease. Neurobiol Aging. 2014;35:731-45.
45. Bennett DA, Yu L, Yang J, Srivastava GP, Aubin C, De Jager PL. Epigenomics of Alzheimer's disease. Transl Res. 2014; in press.
46. Lister R, Mukamel EA, Nery JR, Urich M, Puddifoot CA, Johnson ND, Lucero J, Huang Y, Dwork AJ, Schultz MD, et al. Global epigenomic reconfiguration during mammalian brain development. Science. 2013;341:1237905.
47. Colquitt BM, Allen WE, Barnea G, Lomvardas S. Alteration of genic 5-hydroxymethylcytosine patterning in olfactory neurons correlates with changes in gene expression and cell identity. Proc Natl Acad Sci U S A. 2013;110:14682-7.
48. Kummer MP, Hammerschmidt T, Martinez A, Terwel D, Eichele G, Witten A, Figura S, Stoll M, Schwartz S, Pape HC, et al. Ear2 deletion causes early memory and learning deficits in APP/PS1 mice. J Neurosci. 2014;34:8845-54.
49. Li X, Barkho BZ, Luo Y, Smrt RD, Santistevan NJ, Liu C, Kuwabara T, Gage FH, Zhao X. Epigenetic regulation of the stem cell mitogen Fgf-2 by Mbd1 in adult neural stem/progenitor cells. J Biol Chem. 2008;283:27644-52.
50. Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell. 2010;38:576-89.
51. Zhang B, Kirov S, Snoddy J. WebGestalt: an integrated system for exploring gene sets in various biological contexts. Nucleic Acids Res. 2005;33:W741-8.