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Research Paper

Comprehensive mapping of 5-hydroxymethylcytosine epigenetic dynamics in axon regeneration

, , , , &
Pages 77-92 | Received 31 Aug 2016, Accepted 17 Nov 2016, Published online: 06 Jan 2017

References

  • Jaenisch R, Bird A. Epigenetic regulation of gene expression: how the genome integrates intrinsic and environmental signals. Nat Genet 2003; 33(Suppl):245-54; PMID:12610534; http://dx.doi.org/10.1038/ng1089
  • 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; PMID:23828890; http://dx.doi.org/10.1126/science.1237905
  • Day JJ, Sweatt JD. DNA methylation and memory formation. Nat Neurosci 2010; 13:1319-23; PMID:20975755; http://dx.doi.org/10.1038/nn.2666
  • Gräff J, Kim D, Dobbin MM, Tsai LH. Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol Rev 2011; 91:603-49; PMID:21527733; http://dx.doi.org/10.1152/physrev.00012.2010
  • Kinde B, Gabel HW, Gilbert CS, Griffith EC, Greenberg ME. Reading the unique DNA methylation landscape of the brain: Non-CpG methylation, hydroxymethylation, and MeCP2. Proc Natl Acad Sci U S A 2015; 112:6800-6; PMID:25739960; http://dx.doi.org/10.1073/pnas.1411269112
  • Wu SC, Zhang Y. Active DNA demethylation: many roads lead to Rome. Nat Rev Mol Cell Biol 2010; 11:607-20; PMID:20683471; http://dx.doi.org/10.1038/nrm2950
  • 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; PMID:23403289; http://dx.doi.org/10.1016/j.celrep.2013.01.011
  • Globisch D, Munzel M, Muller M, Michalakis S, Wagner M, Koch S, Bruckl T, Biel M, Carell T. Tissue distribution of 5-hydroxymethylcytosine and search for active demethylation intermediates. PloS One 2010; 5:e15367; PMID:21203455; http://dx.doi.org/10.1371/journal.pone.0015367
  • 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; PMID:21151123; http://dx.doi.org/10.1038/nbt.1732
  • 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; PMID:19372391; http://dx.doi.org/10.1126/science.1170116
  • 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; PMID:21460836; http://dx.doi.org/10.1038/nature10008
  • 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; PMID:22037496; http://dx.doi.org/10.1038/nn.2959
  • Feng J, Shao N, Szulwach KE, Vialou V, Huynh J, Zhong C, Le T, Ferguson D, Cahill ME, Li Y, et al. Role of Tet1 and 5-hydroxymethylcytosine in cocaine action. Nat Neurosci 2015; 18:536-44; PMID:25774451; http://dx.doi.org/10.1038/nn.3976
  • Iskandar BJ, Rizk E, Meier B, Hariharan N, Bottiglieri T, Finnell RH, Jarrard DF, Banerjee RV, Skene JHP, Nelson A, et al. Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest 2010; 120:1603-16; PMID:20424322; http://dx.doi.org/10.1172/JCI40000
  • Puttagunta R, Tedeschi A, Soria MG, Hervera A, Lindner R, Rathore KI, Gaub P, Joshi Y, Nguyen T, Schmandke A, et al. PCAF-dependent epigenetic changes promote axonal regeneration in the central nervous system. Nat Commun 2014; 5:3527; PMID:24686445; http://dx.doi.org/10.1038/ncomms4527
  • Goldberg JL. How does an axon grow? Genes Dev 2003; 17:941-58; PMID:12704078; http://dx.doi.org/10.1101/gad.1062303
  • Zhou FQ, Snider WD. Intracellular control of developmental and regenerative axon growth. Philos Trans R Soc Lond B Biol Sci 2006; 361:1575-92; PMID:16939976; http://dx.doi.org/10.1098/rstb.2006.1882
  • Wong JK, Zou H. Reshaping the chromatin landscape after spinal cord injury. Front Biol (Beijing) 2014; 9:356-66; PMID:25554728; http://dx.doi.org/10.1007/s11515-014-1329-8
  • Neumann S, Woolf CJ. Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron 1999; 23:83-91; PMID:10402195; http://dx.doi.org/10.1016/S0896-6273(00)80755-2
  • Richardson PM, Issa VM. Peripheral injury enhances central regeneration of primary sensory neurones. Nature 1984; 309:791-3; PMID:6204205; http://dx.doi.org/10.1038/309791a0
  • Smith DS, Pate Skene JH. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J Neurosci 1997; 17:646-58; PMID:8987787
  • Blesch A, Lu P, Tsukada S, Alto LT, Roet K, Coppola G, Geschwind D, Tuszynski MH. Conditioning lesions before or after spinal cord injury recruit broad genetic mechanisms that sustain axonal regeneration: superiority to camp-mediated effects. Exp Neurol 2012; 235:162-73; PMID:22227059; http://dx.doi.org/10.1016/j.expneurol.2011.12.037
  • Bonilla IE, Tanabe K, Strittmatter SM. Small proline-rich repeat protein 1A is expressed by axotomized neurons and promotes axonal outgrowth. J Neurosci 2002; 22:1303-15; PMID:11850458
  • Costigan M, Befort K, Karchewski L, Griffin RS, D'Urso D, Allchorne A, Sitarski J, Mannion JW, Pratt RE, Woolf CJ. Replicate high-density rat genome oligonucleotide microarrays reveal hundreds of regulated genes in the dorsal root ganglion after peripheral nerve injury. BMC Neurosci 2002; 3:16; PMID:12401135; http://dx.doi.org/10.1186/1471-2202-3-16
  • Michaelevski I, Segal-Ruder Y, Rozenbaum M, Medzihradszky KF, Shalem O, Coppola G, Horn-Saban S, Ben-Yaakov K, Dagan SY, Rishal I, et al. Signaling to transcription networks in the neuronal retrograde injury response. Sci Signal 2010; 3:ra53; PMID:20628157; http://dx.doi.org/10.1126/scisignal.2000952
  • Finelli MJ, Wong JK, Zou H. Epigenetic regulation of sensory axon regeneration after spinal cord injury. J Neurosci 2013; 33:19664-76; PMID:24336730; http://dx.doi.org/10.1523/JNEUROSCI.0589-13.2013
  • Ma DK, Guo JU, Ming GL, Song H. DNA excision repair proteins and Gadd45 as molecular players for active DNA demethylation. Cell Cycle 2009; 8:1526-31; PMID:19377292; http://dx.doi.org/10.4161/cc.8.10.8500
  • Befort K, Karchewski L, Lanoue C, Woolf CJ. Selective up-regulation of the growth arrest DNA damage-inducible gene Gadd45 alpha in sensory and motor neurons after peripheral nerve injury. Eur J Neurosci 2003; 18:911-22; PMID:12925017; http://dx.doi.org/10.1046/j.1460-9568.2003.02827.x
  • Doron-Mandel E, Fainzilber M, Terenzio M. Growth control mechanisms in neuronal regeneration. FEBS Lett 2015; 589:1669-77; PMID:25937120; http://dx.doi.org/10.1016/j.febslet.2015.04.046
  • Frey E, Valakh V, Karney-Grobe S, Shi Y, Milbrandt J, DiAntonio A. An in vitro assay to study induction of the regenerative state in sensory neurons. Exp Neurol 2015; 263:350-63; PMID:25447942; http://dx.doi.org/10.1016/j.expneurol.2014.10.012
  • Zou H, Ho C, Wong K, Tessier-Lavigne M. Axotomy-induced Smad1 activation promotes axonal growth in adult sensory neurons. J Neurosci 2009; 29:7116-23; PMID:19494134; http://dx.doi.org/10.1523/JNEUROSCI.5397-08.2009
  • 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; PMID:21892189; http://dx.doi.org/10.1038/nature10443
  • Li X, Wei W, Zhao QY, Widagdo J, Baker-Andresen D, Flavell CR, D'Alessio A, Zhang Y, Bredy TW. Neocortical Tet3-mediated accumulation of 5-hydroxymethylcytosine promotes rapid behavioral adaptation. Proc Natl Acad Sci U S A 2014; 111:7120-5; PMID:24757058; http://dx.doi.org/10.1073/pnas.1318906111
  • Xu Y, Xu C, Kato A, Tempel W, Abreu JG, Bian C, Hu Y, Hu D, Zhao B, Cerovina T, et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 2012; 151:1200-13; PMID:23217707; http://dx.doi.org/10.1016/j.cell.2012.11.014
  • Santos F, Peat J, Burgess H, Rada C, Reik W, Dean W. Active demethylation in mouse zygotes involves cytosine deamination and base excision repair. Epigenetics Chromatin 2013; 6:39; PMID:24279473; http://dx.doi.org/10.1186/1756-8935-6-39
  • Shen L, Shao NY, Liu X, Maze I, Feng J, Nestler EJ. diffReps: detecting differential chromatin modification sites from ChIP-seq data with biological replicates. PloS One 2013; 8:e65598; PMID:23762400; http://dx.doi.org/10.1371/journal.pone.0065598
  • Liu K, Lu Y, Lee JK, Samara R, Willenberg R, Sears-Kraxberger I, Tedeschi A, Park KK, Jin D, Cai B, et al. PTEN deletion enhances the regenerative ability of adult corticospinal neurons. Nat Neurosci 2010; 13:1075-81; PMID:20694004; http://dx.doi.org/10.1038/nn.2603
  • Parikh P, Hao Y, Hosseinkhani M, Patil SB, Huntley GW, Tessier-Lavigne M, Zou H. Regeneration of axons in injured spinal cord by activation of bone morphogenetic protein/Smad1 signaling pathway in adult neurons. Proc Natl Acad Sci 2011; 108:E99–E107; PMID:21518886; http://dx.doi.org/10.1073/pnas.1100426108
  • Seijffers R, Mills CD, Woolf CJ. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci 2007; 27:7911-20; PMID:17652582; http://dx.doi.org/10.1523/JNEUROSCI.5313-06.2007
  • Cohen-Cory S, Kidane AH, Shirkey NJ, Marshak S. Brain-derived neurotrophic factor and the development of structural neuronal connectivity. Dev Neurobiol 2010; 70:271-88; PMID:20186709; http://dx.doi.org/10.1002/dneu.20774
  • Shim SO, Cafferty WB, Schmidt EC, Kim BG, Fujisawa H, Strittmatter SM. PlexinA2 limits recovery from corticospinal axotomy by mediating oligodendrocyte-derived Sema6A growth inhibition. Mol Cell Neurosci 2012; 50:193-200; PMID:22564823; http://dx.doi.org/10.1016/j.mcn.2012.04.007
  • Suto F, Tsuboi M, Kamiya H, Mizuno H, Kiyama Y, Komai S, Shimizu M, Sanbo M, Yagi T, Hiromi Y, et al. Interactions between plexin-A2, plexin-A4, and semaphorin 6A control lamina-restricted projection of hippocampal mossy fibers. Neuron 2007; 53:535-47; PMID:17296555; http://dx.doi.org/10.1016/j.neuron.2007.01.028
  • Miao T, Wu D, Zhang Y, Bo X, Subang MC, Wang P, Richardson PM. Suppressor of cytokine signaling-3 suppresses the ability of activated signal transducer and activator of transcription-3 to stimulate neurite growth in rat primary sensory neurons. J Neurosci 2006; 26:9512-9; PMID:16971535; http://dx.doi.org/10.1523/JNEUROSCI.2160-06.2006
  • Colbran RJ, Brown AM. Calcium/calmodulin-dependent protein kinase II and synaptic plasticity. Curr Opin Neurobiol 2004; 14:318-27; PMID:15194112; http://dx.doi.org/10.1016/j.conb.2004.05.008
  • Graef IA, Wang F, Charron F, Chen L, Neilson J, Tessier-Lavigne M, Crabtree GR. Neurotrophins and netrins require calcineurin/NFAT signaling to stimulate outgrowth of embryonic axons. Cell 2003; 113:657-70; PMID:12787506; http://dx.doi.org/10.1016/S0092-8674(03)00390-8
  • Ma TC, Barco A, Ratan RR, Willis DE. cAMP-responsive element-binding protein (CREB) and cAMP co-regulate activator protein 1 (AP1)-dependent regeneration-associated gene expression and neurite growth. J Biol Chem 2014; 289:32914-25; PMID:25296755; http://dx.doi.org/10.1074/jbc.M114.582460
  • Finelli MJ, Murphy KJ, Chen L, Zou H. Differential phosphorylation of Smad1 integrates BMP and neurotrophin pathways through Erk/Dusp in axon development. Cell Rep 2013; 3:1592-606; PMID:23665221; http://dx.doi.org/10.1016/j.celrep.2013.04.011
  • Wu H, D'Alessio AC, Ito S, Wang Z, Cui K, Zhao K, Sun YE, Zhang Y. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev 2011; 25:679-84; PMID:21460036; http://dx.doi.org/10.1101/gad.2036011
  • Bareyre FM, Garzorz N, Lang C, Misgeld T, Buning H, Kerschensteiner M. In vivo imaging reveals a phase-specific role of STAT3 during central and peripheral nervous system axon regeneration. Proc Natl Acad Sci U S A 2011; 108:6282-7; PMID:21447717; http://dx.doi.org/10.1073/pnas.1015239108
  • Martinowich K, Hattori D, Wu H, Fouse S, He F, Hu Y, Fan G, Sun YE. DNA methylation-related chromatin remodeling in activity-dependent BDNF gene regulation. Science 2003; 302:890-3; PMID:14593184; http://dx.doi.org/10.1126/science.1090842
  • Yu NK, Baek SH, Kaang BK. DNA methylation-mediated control of learning and memory. Mol Brain 2011; 4:5; PMID:21247469; http://dx.doi.org/10.1186/1756-6606-4-5
  • Nan X, Ng HH, Johnson CA, Laherty CD, Turner BM, Eisenman RN, Bird A. Transcriptional repression by the methyl-CpG-binding protein MeCP2 involves a histone deacetylase complex. Nature 1998; 393:386-9; PMID:9620804; http://dx.doi.org/10.1038/30764
  • 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; PMID:23260135; http://dx.doi.org/10.1016/j.cell.2012.11.022
  • Lister R, Pelizzola M, Dowen RH, Hawkins RD, Hon G, Tonti-Filippini J, Nery JR, Lee L, Ye Z, Ngo QM, et al. Human DNA methylomes at base resolution show widespread epigenomic differences. Nature 2009; 462:315-22; PMID:19829295; http://dx.doi.org/10.1038/nature08514
  • Cho Y, Sloutsky R, Naegle KM, Cavalli V. Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell 2013; 155:894-908; PMID:24209626; http://dx.doi.org/10.1016/j.cell.2013.10.004
  • Afshari FT, Kappagantula S, Fawcett JW. Extrinsic and intrinsic factors controlling axonal regeneration after spinal cord injury. Expert Rev Mol Med 2009; 11:e37; PMID:19968910; http://dx.doi.org/10.1017/S1462399409001288
  • Cho Y, Shin JE, Ewan EE, Oh YM, Pita-Thomas W, Cavalli V. Activating Injury-Responsive Genes with Hypoxia Enhances Axon Regeneration through Neuronal HIF-1alpha. Neuron 2015; 88:720-34; PMID:26526390; http://dx.doi.org/10.1016/j.neuron.2015.09.050
  • Chandran V, Coppola G, Nawabi H, Omura T, Versano R, Huebner EA, Zhang A, Costigan M, Yekkirala A, Barrett L, et al. A Systems-Level Analysis of the Peripheral Nerve Intrinsic Axonal Growth Program. Neuron 2016; 89:956-70; PMID:26898779; http://dx.doi.org/10.1016/j.neuron.2016.01.034
  • Andrews S. FastQC: a quality control tool for high throughput sequence data. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc
  • Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10:R25; PMID:19261174; http://dx.doi.org/10.1186/gb-2009-10-3-r25
  • Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, Genome Project Data Processing S. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009; 25:2078-9; PMID:19505943; http://dx.doi.org/10.1093/bioinformatics/btp352
  • 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; PMID:18798982; http://dx.doi.org/10.1186/gb-2008-9-9-r137
  • Shen L, Shao N, Liu X, Nestler E. ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 2014; 15:284; PMID:24735413; http://dx.doi.org/10.1186/1471-2164-15-284
  • McLeay RC, Bailey TL. Motif Enrichment Analysis: a unified framework and an evaluation on ChIP data. BMC Bioinformatics 2010; 11:165; PMID:20356413; http://dx.doi.org/10.1186/1471-2105-11-165

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