Alterations in 5hmC Level and Genomic Distribution in Aging-Related Epigenetic Drift in Human Adipose Stem Cells

References

• Fantuzzi G . Adipose tissue, adipokines, and inflammation. J. Allergy Clin. Immunol.115(5), 911–919 (2005).
   PubMed Web of Science ®Google Scholar
• Jonas MI , KurylowiczA , BartoszewiczZet al. Interleukins 6 and 15 levels are higher in subcutaneous adipose tissue, but obesity is associated with their increased content in visceral fat depots. Int. J. Mol. Sci.16(10), 25817–25830 (2015).
   PubMed Web of Science ®Google Scholar
• Park MH , KimDH , LeeEKet al. Age-related inflammation and insulin resistance: a review of their intricate interdependency. Arch. Pharm. Res.37(12), 1507–1514 (2014).
   PubMed Web of Science ®Google Scholar
• Arner E , WestermarkPO , SpaldingKLet al. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes59(1), 105–109 (2010).
   PubMed Web of Science ®Google Scholar
• Tchkonia T , MorbeckDE , Von ZglinickiTet al. Fat tissue, aging, and cellular senescence. Aging Cell9(5), 667–684 (2010).
   PubMed Web of Science ®Google Scholar
• Putiri E , RobertsonKD. Epigenetic mechanisms and genome stability. Clin. Epigenetics2(2), 299–314 (2011).
   PubMed Web of Science ®Google Scholar
• Kim M , CostelloJ. DNA methylation: an epigenetic mark of cellular memory. Exp. Mol. Med.49(4), e322 (2017).
   PubMedGoogle Scholar
• Maeder ML , AngstmanJF , RichardsonMEet al. Targeted DNA demethylation and activation of endogenous genes using programmable TALE-TET1 fusion proteins. Nat. Biotechnol.31(12), 1137–1142 (2013).
   PubMed Web of Science ®Google Scholar
• Bestor TH , EdwardsJR , BoulardM. Notes on the role of dynamic DNA methylation in mammalian development. Proc. Natl Acad. Sci. USA112(22), 6796–6799 (2015).
   PubMed Web of Science ®Google Scholar
• Wilkinson MF . Evidence that DNA methylation engenders dynamic gene regulation. Proc. Natl Acad. Sci. USA112(17), e2116 (2015).
   PubMed Web of Science ®Google Scholar
• Liu XS , WuH , JiXet al. Editing DNA methylation in the mammalian genome. Cell167(1), 233–247.e17 (2016).
   PubMed Web of Science ®Google Scholar
• Marttila S , KananenL , HäyrynenSet al. Ageing-associated changes in the human DNA methylome: genomic locations and effects on gene expression. BMC Genomics16(1), 179 (2015).
   PubMedGoogle Scholar
• Sun D , YiSV. Impacts of chromatin states and long-range genomic segments on aging and DNA methylation. PLoS ONE10(6), e0128517 (2015).
   PubMed Web of Science ®Google Scholar
• Grönniger E , WeberB , HeilOet al. Aging and chronic sun exposure cause distinct epigenetic changes in human skin. PLoS Genet6(5), e1000971 (2010).
   PubMed Web of Science ®Google Scholar
• Szarc Vel Szic K , DeclerckK , VidakovićM , Vanden BergheW. From inflammaging to healthy aging by dietary lifestyle choices: is epigenetics the key to personalized nutrition?Clin. Epigenetics7(1), 33 (2015).
   PubMedGoogle Scholar
• Ling C , RönnT. Epigenetic adaptation to regular exercise in humans. Drug Discov. Today19(7), 1015–1018 (2014).
   PubMed Web of Science ®Google Scholar
• Shah S , McRaeAF , MarioniRet al. Genetic and environmental exposures constrain epigenetic drift over the human life course. Genome Res.24(11), 1725–1733 (2014).
   PubMed Web of Science ®Google Scholar
• Yeh S , LiuC , ChangR , WuC , LinC , YangK. Aging-dependent DNA hypermethylation and gene expression of GSTM1 involved in T cell differentiation. Oncotarget8(30), 48591–48602 (2017).
   PubMedGoogle Scholar
• Mendelsohn AR , LarrickJW. The DNA methylome as a biomarker for epigenetic instability and human aging. Rejuvenation Res.16(1), 74–77 (2013).
   PubMed Web of Science ®Google Scholar
• Ciccarone F , TagliatestaS , CaiafaP , ZampieriM. DNA methylation dynamics in aging: how far are we from understanding the mechanisms?Mech. Ageing Dev.174, 3–17 (2018).
   PubMed Web of Science ®Google Scholar
• Ciccarone F , MalavoltaM , CalabreseRet al. Age-dependent expression of DNMT1 and DNMT3B in PBMCs from a large European population enrolled in the MARK-AGE study. Aging Cell15(4), 755–765 (2016).
   PubMed Web of Science ®Google Scholar
• Lorsback RB , MooreJ , MathewSC , RaimondiSC , MukatiraST , DowningJR. TET1, a member of a novel protein family, is fused to MLL in acute myeloid leukemia containing the t(10;11)(q22;23). Leukemia17(3), 637–641 (2003).
   PubMed Web of Science ®Google Scholar
• Tahiliani M , KohKP , ShenYet al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science324(5929), 930–935 (2009).
   PubMed Web of Science ®Google Scholar
• Kohli RM , ZhangY. TET enzymes, TDG and the dynamics of DNA demethylation. Nature502(7472), 472–479 (2013).
   PubMed Web of Science ®Google Scholar
• Kagiwada S , KurimotoK , HirotaT , YamajiM , SaitouM. Replication-coupled passive DNA demethylation for the erasure of genome imprints in mice. EMBO J.32(3), 340–353 (2013).
   PubMed Web of Science ®Google Scholar
• Yamaguchi S , HongK , LiuRet al. Dynamics of 5-methylcytosine and 5-hydroxymethylcytosine during germ cell reprogramming. Cell Res.23(3), 329–339 (2013).
   PubMed Web of Science ®Google Scholar
• Hahn MA , SzabóPE , PfeiferGP. 5-Hydroxymethylcytosine: astable or transient DNA modification?Genomics104(5), 314–323 (2014).
   PubMed Web of Science ®Google Scholar
• Wiehle L , RaddatzG , MuschTet al. Tet1 and Tet2 protect DNA methylation canyons against hypermethylation. Mol. Cell. Biol.36(3), 452–461 (2016).
   PubMed Web of Science ®Google Scholar
• Williams K , ChristensenJ , PedersenMTet al. TET1 and hydroxymethylcytosine in transcription and DNA methylation fidelity. Nature473(7347), 343–349 (2011).
   PubMed Web of Science ®Google Scholar
• Cartron PF , NadaradjaneA , LePapeF , LalierL , GardieB , ValletteFM. Identification of TET1 partners that control its DNA-demethylating function. Genes Cancer4(5–6), 235–241 (2013).
   PubMedGoogle Scholar
• Zhong J , LiX , CaiWet al. TET1 modulates H4K16 acetylation by controlling auto-acetylation of hMOF to affect gene regulation and DNA repair function. Nucleic Acids Res.45(2), 672–684 (2017).
   PubMed Web of Science ®Google Scholar
• Deplus R , DelatteB , SchwinnMKet al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J.32(5), 645–655 (2013).
   PubMed Web of Science ®Google Scholar
• Dawlaty MM , BreilingA , LeTet al. Loss of tet enzymes compromises proper differentiation of embryonic stem cells. Dev. Cell29(1), 102–111 (2014).
   PubMed Web of Science ®Google Scholar
• Sajic T , HopfgartnerG , SzantoI , VaresioE. Comparison of three detergent-free protein extraction protocols for white adipose tissue. Anal. Biochem.415(2), 215–217 (2011).
   PubMed Web of Science ®Google Scholar
• Stark R , BrownG. DiffBind: differential binding analysis of ChIP-Seq peak data. Bioconductor1–29 (2016). http://bioconductor.org/packages/release/bioc/vignettes/DiffBind/inst/doc/DiffBind.pdf
   Google Scholar
• Lienhard M , GrimmC , MorkelM , HerwigR , ChavezL. MEDIPS: genome-wide differential coverage analysis of sequencing data derived from DNA enrichment experiments. Bioinformatics30(2), 284–286 (2014).
   PubMed Web of Science ®Google Scholar
• James Kent W , SugnetCW , FureyTet al. The human genome browser at UCSC. Genome Res.12(6), 996–1006 (2002).
   PubMed Web of Science ®Google Scholar
• Heinz S , BennerC , SpannNet al. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol. Cell38(4), 576–589 (2010).
   PubMed Web of Science ®Google Scholar
• Cavalcante RG , SartorMA. Annotatr: genomic regions in context. Bioinformatics33(15), 2381–2383 (2017).
   PubMed Web of Science ®Google Scholar
• Carlson M . Annotation package for TxDb object(s). R Packag. version 3.4.0. (2015).
   Google Scholar
• Zerbino DR , WilderSP , JohnsonN , JuettemannT , FlicekP. The Ensembl regulatory build. Genome Biol.16(1), 56 (2015).
   PubMedGoogle Scholar
• Gel B , Díez-VillanuevaA , SerraE , BuschbeckM , PeinadoMA , MalinverniR. RegioneR: an R/Bioconductor package for the association analysis of genomic regions based on permutation tests. Bioinformatics32(2), 289–291 (2016).
   PubMed Web of Science ®Google Scholar
• Puzianowska-Kuznicka M , OwczarzM , Wieczorowska-TobisKet al. Interleukin-6 and C-reactive protein, successful aging, and mortality: the PolSenior study. Immun. Ageing13(1), 21 (2016).
   PubMedGoogle Scholar
• Reas DL , NygårdJF , SvenssonE , SørensenT , SandangerI. Changes in body mass index by age, gender, and socio-economic status among a cohort of Norwegian men and women (1990–2001). BMC Public Health7, 269 (2007).
   PubMed Web of Science ®Google Scholar
• Schellenberg A , LinQ , SchülerHet al. Replicative senescence of mesenchymal stem cells causes DNA-methylation changes which correlate with repressive histone marks. Aging3(9), 873–888 (2011).
   PubMedGoogle Scholar
• Yu P , JiL , LeeKJet al. Subsets of visceral adipose tissue nuclei with distinct levels of 5-hydroxymethylcytosine. PLoS ONE11(5), e0154949 (2016).
   PubMed Web of Science ®Google Scholar
• Rohde K , KellerM , StumvollM , DietrichA , BlüherM , BöttcherY. DNA 5-hydroxymethylation in human adipose tissue differs between subcutaneous and visceral adipose tissue depots. Epigenomics7(6), 911–920 (2015).
   PubMed Web of Science ®Google Scholar
• Chouliaras L , vanden Hove D , KenisGet al. Age-related increase in levels of 5-hydroxymethylcytosine in mouse hippocampus is prevented by caloric restriction. Curr. Alzheimer Res.9(5), 536–544 (2014).
   Web of Science ®Google Scholar
• Chen H , DzitoyevaS , ManevH. Effect of aging on 5-hydroxymethylcytosine in the mouse hippocampus. Restor. Neurol. Neurosci.30(3), 237–245 (2012).
   PubMed Web of Science ®Google Scholar
• Szulwach KE , LiX , LiYet al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci.14(12), 1607–1616 (2011).
   PubMed Web of Science ®Google Scholar
• Valentini E , ZampieriM , MalavoltaMet al. Analysis of the machinery and intermediates of the 5hmC-mediated DNA demethylation pathway in aging on samples from the MARK-AGE Study. Aging8(9), 1896–1922 (2016).
   PubMedGoogle Scholar
• Daniunaite K , SerenaiteI , MisgirdaiteRet al. Epigenetic regulation of human adipose-derived stem cells differentiation. Mol. Cell. Biochem.410(1–2), 111–120 (2015).
   PubMed Web of Science ®Google Scholar
• Shen Y , ChowJ , WangZ , FanG. Abnormal CpG island methylation occurs during in vitro differentiation of human embryonic stem cells. Hum. Mol. Genet.15(17), 2623–2635 (2006).
   PubMed Web of Science ®Google Scholar
• Meissner A , MikkelsenTS , GuHet al. Genome-scale DNA methylation maps of pluripotent and differentiated cells. Nature454(7205), 766–770 (2008).
   PubMed Web of Science ®Google Scholar
• Boraldi F , AnnoviG , TiozzoR , SommerP , QuaglinoD. Comparison of ex vivo and in vitro human fibroblast ageing models. Mech. Ageing Dev.131(10), 625–635 (2010).
   PubMed Web of Science ®Google Scholar
• Garitaonandia I , AmirH , BoscoloFSet al. Increased risk of genetic and epigenetic instability in human embryonic stem cells associated with specific culture conditions. PLoS ONE10(2), e0118307 (2015).
   PubMed Web of Science ®Google Scholar
• Xiao M , YangH , XuWet al. Inhibition of α-KG-dependent histone and DNA demethylases by fumarate and succinate that are accumulated in mutations of FH and SDH tumor suppressors. Genes Dev.26(12), 1326–1338 (2012).
   PubMed Web of Science ®Google Scholar
• Salminen A , KauppinenA , KaarnirantaK. 2-Oxoglutarate-dependent dioxygenases are sensors of energy metabolism, oxygen availability, and iron homeostasis: potential role in the regulation of aging process. Cell. Mol. Life Sci.72(20), 3897–3914 (2015).
   PubMed Web of Science ®Google Scholar
• Bauer C , GöbelK , NagarajNet al. Phosphorylation of TET proteins is regulated via O-GlcNAcylation by the O-Linked N-acetylglucosamine transferase (OGT). J. Biol. Chem.290(8), 4801–4812 (2015).
   PubMed Web of Science ®Google Scholar
• Ciccarone F , ValentiniE , ZampieriM , CaiafaP. 5 mC-hydroxylase activity is influenced by the PARylation of TET1 enzyme. Oncotarget6(27), 24333–24347 (2015).
   PubMedGoogle Scholar
• Jones MJ , GoodmanSJ , KoborM. DNA methylation and healthy human aging. Aging Cell14(6), 924–932 (2015).
   PubMed Web of Science ®Google Scholar
• Bacalini MG , D’AquilaP , MarascoEet al. The methylation of nuclear and mitochondrial DNA in ageing phenotypes and longevity. Mech. Ageing Dev.165, 156–161 (2017).
   PubMed Web of Science ®Google Scholar
• Toraño EG , BayónGF , delReal Áet al. Age-associated hydroxymethylation in human bone-marrow mesenchymal stem cells. J. Transl. Med.14(1), 207 (2016).
   PubMedGoogle Scholar
• Stroud H , FengS , MoreyKinney S , PradhanS , JacobsenS. 5-Hydroxymethylcytosine is associated with enhancers and gene bodies in human embryonic stem cells. Genome Biol.12(6), R54 (2011).
   PubMed Web of Science ®Google Scholar
• Sérandour AA , AvnerS , OgerFet al. Dynamic hydroxymethylation of deoxyribonucleic acid marks differentiation-associated enhancers. Nucleic Acids Res.40(17), 8255–8265 (2012).
   PubMed Web of Science ®Google Scholar
• Hon GC , SongCX , DuTet al. 5 mC oxidation by Tet2 modulates enhancer activity and timing of transcriptome reprogramming during differentiation. Mol. Cell.56(2), 286–297 (2014).
   PubMed Web of Science ®Google Scholar
• Valinluck V , TsaiHH , RogstadDK , BurdzyA , BirdA , SowersLC. Oxidative damage to methyl-CpG sequences inhibits the binding of the methyl-CpG binding domain (MBD) of methyl-CpG binding protein 2 (MeCP2). Nucleic Acids Res.32(14), 4100–4108 (2004).
   PubMed Web of Science ®Google Scholar
• Feldmann A , IvanekR , MurrR , GaidatzisD , BurgerL , SchübelerD. Transcription factor occupancy can mediate active turnover of DNA methylation at regulatory regions. PLoS Genet.9(12), e1003994 (2013).
   PubMed Web of Science ®Google Scholar
• Szulwach KE , LiX , LiYet al. Integrating 5-hydroxymethylcytosine into the epigenomic landscape of human embryonic stem cells. PLoS Genet.7(6), e1002154 (2011).
   PubMed Web of Science ®Google Scholar
• Lin IH , ChenYF , HsuMT. Correlated 5-hydroxymethylcytosine (5hmC) and gene expression profiles underpin gene and organ-specific epigenetic regulation in adult mouse brain and liver. PLoS ONE12(1), e0170779 (2017).
   PubMed Web of Science ®Google Scholar
• Marina RJ , SturgillD , BaillyMAet al. TET-catalyzed oxidation of intragenic 5-methylcytosine regulates CTCF-dependent alternative splicing. EMBO J.35(3), 335–355 (2016).
   PubMed Web of Science ®Google Scholar
• Filippova GN , ThienesCP , PennBHet al. CTCF-binding sites flank CTG/CAG repeats and form a methylation-sensitive insulator at the DM1 locus. Nat. Genet.28(4), 335–343 (2001).
   PubMed Web of Science ®Google Scholar
• Hashimoto H , WangD , HortonJR , ZhangX , CorcesVG , ChengX. Structural basis for the versatile and methylation-dependent binding of CTCF to DNA. Mol. Cell.66(5), 711–720 (2017).
   PubMed Web of Science ®Google Scholar
• Dubois-Chevalier J , OgerF , DehondtHet al. A dynamic CTCF chromatin binding landscape promotes DNA hydroxymethylation and transcriptional induction of adipocyte differentiation. Nucleic Acids Res.42(17), 10943–10959 (2014).
   PubMed Web of Science ®Google Scholar
• Tu S , ShaoZ. An introduction to computational tools for differential binding analysis with ChIP-seq data. Quant. Biol.5, 226 (2017).
   Google Scholar
• Steinhauser S , KurzawaN , EilsR , HerrmannCA. Comprehensive comparison of tools for differential ChIP-seq analysis. Brief Bioinform.17(6), 953–966 (2016).
   PubMed Web of Science ®Google Scholar