Epigenetic regulation of axonal regenerative capacity

References

• 1 Goldberg JL, Klassen MP, Hua Y, Barres BA. Amacrine-signaled loss of intrinsic axon growth ability by retinal ganglion cells. Science 296(5574), 1860–1864 (2002).
  Medline CASGoogle Scholar
• 2 Blackmore M, Letourneau PC. Changes within maturing neurons limit axonal regeneration in the developing spinal cord. J. Neurobiol. 66(4), 348–360 (2006).
  Medline CASGoogle Scholar
• 3 Dusart I, Airaksinen MS, Sotelo C. Purkinje cell survival and axonal regeneration are age dependent: an in vitro study. J. Neurosci. 17(10), 3710–3726 (1997).
  Medline CASGoogle Scholar
• 4 Chen DF, Jhaveri S, Schneider GE. Intrinsic changes in developing retinal neurons result in regenerative failure of their axons. Proc. Natl Acad. Sci. USA 92(16), 7287–7291 (1995).
  Medline CASGoogle Scholar
• 5 Wang JT, Kunzevitzky NJ, Dugas JC, Cameron M, Barres BA, Goldberg JL. Disease gene candidates revealed by expression profiling of retinal ganglion cell development. J. Neurosci. 27(32), 8593–8603 (2007).
  Medline CASGoogle Scholar
• 6 Moore DL, Blackmore MG, Hu Y et al. KLF family members regulate intrinsic axon regeneration ability. Science 326(5950), 298–301 (2009).
  Medline CASGoogle Scholar
• 7 Blackmore MG, Wang Z, Lerch JK et al. Kruppel-like Factor 7 engineered for transcriptional activation promotes axon regeneration in the adult corticospinal tract. Proc. Natl Acad. Sci. USA 109(19), 7517–7522 (2012).
  Medline CASGoogle Scholar
• 8 Perera A, Eisen D, Wagner M et al. TET3 is recruited by REST for context-specific hydroxymethylation and induction of gene expression. Cell Rep. 11(2), 283–294 (2015).
  Medline CASGoogle Scholar
• 9 Gaub P, Joshi Y, Wuttke A et al. The histone acetyltransferase p300 promotes intrinsic axonal regeneration. Brain 134, 2134–2148 (2011).
  MedlineGoogle Scholar
• 10 Rao RC, Tchedre KT, Malik MT et al. Dynamic patterns of histone lysine methylation in the developing retina. Invest. Ophthalmol. Vis. Sci. 51(12), 6784–6792 (2010).
  MedlineGoogle Scholar
• 11 Biermann J, Grieshaber P, Goebel U et al. Valproic acid-mediated neuroprotection and regeneration in injured retinal ganglion cells. Invest. Ophthalmol. Vis. Sci. 51(1), 526–534 (2010).
  MedlineGoogle Scholar
• 12 Ma TC, Willis DE. What makes a RAG regeneration associated? Front. Mol. Neurosci. 8, 43 (2015).
  MedlineGoogle Scholar
• 13 Smith DS, Skene JH. A transcription-dependent switch controls competence of adult neurons for distinct modes of axon growth. J. Neurosci. 17(2), 646–658 (1997).
  Medline CASGoogle Scholar
• 14 Chandran V, Coppola G, Nawabi H et al. A systems-level analysis of the Peripheral Nerve Intrinsic Axonal Growth Program. Neuron 89(5), 956–970 (2016).
  Medline CASGoogle Scholar
• 15 Stam FJ, MacGillavry HD, Armstrong NJ et al. Identification of candidate transcriptional modulators involved in successful regeneration after nerve injury. Eur. J. Neurosci. 25(12), 3629–3637 (2007).
  MedlineGoogle Scholar
• 16 Storer PD, Dolbeare D, Houle JD. Treatment of chronically injured spinal cord with neurotrophic factors stimulates β-II-tubulin and GAP-43 expression in rubrospinal tract neurons. J. Neurosci. Res. 74(4), 502–511 (2003).
  Medline CASGoogle Scholar
• 17 Bomze HM, Bulsara KR, Iskandar BJ, Caroni P, Skene JH. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat. Neurosci. 4(1), 38–43 (2001).
  Medline CASGoogle Scholar
• 18 Pernet V, Joly S, Jordi N et al. Misguidance and modulation of axonal regeneration by Stat3 and Rho/ROCK signaling in the transparent optic nerve. Cell Death Dis. 4, e734 (2013).
  Medline CASGoogle Scholar
• 19 Lindner R, Puttagunta R, Di Giovanni S. Epigenetic regulation of axon outgrowth and regeneration in CNS injury: the first steps forward. Neurotherapeutics 10(4), 771–781 (2013).
  Medline CASGoogle Scholar
• 20 Bannister AJ, Kouzarides T. Regulation of chromatin by histone modifications. Cell Res. 21(3), 381–395 (2011).
  Medline CASGoogle Scholar
• 21 Peixoto L, Abel T. The role of histone acetylation in memory formation and cognitive impairments. Neuropsychopharmacology 38(1), 62–76 (2013).
  Medline CASGoogle Scholar
• 22 Lee KK, Workman JL. Histone acetyltransferase complexes: one size doesn’t fit all. Nat. Rev. Mol. Cell Biol. 8(4), 284–295 (2007).
  Medline CASGoogle Scholar
• 23 Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat. Rev. Genet. 10(1), 32–42 (2009).
  Medline CASGoogle Scholar
• 24 Broide RS, Redwine JM, Aftahi N, Young W, Bloom FE, Winrow CJ. Distribution of histone deacetylases 1–11 in the rat brain. J. Mol. Neurosci. 31(1), 47–58 (2007).
  Medline CASGoogle Scholar
• 25 Gaub P, Tedeschi A, Puttagunta R, Nguyen T, Schmandke A, Di Giovanni S. HDAC inhibition promotes neuronal outgrowth and counteracts growth cone collapse through CBP/p300 and P/CAF-dependent p53 acetylation. Cell Death Differ. 17(9), 1392–1408 (2010).
  Medline CASGoogle Scholar
• 26 Chen J, Laramore C, Shifman MI. Differential expression of HDACs and KATs in high and low regeneration capacity neurons during spinal cord regeneration. Exp. Neurol. 280, 50–59 (2016).
  Medline CASGoogle Scholar
• 27 Puttagunta R, Tedeschi A, Soria MG et al. PCAF-dependent epigenetic changes promote axonal regeneration in the central nervous system. Nat. Commun. 5, 3527 (2014).
  MedlineGoogle Scholar
• 28 Finelli MJ, Wong JK, Zou H. Epigenetic regulation of sensory axon regeneration after spinal cord injury. J. Neurosci. 33(50), 19664–19676 (2013).
  Medline CASGoogle Scholar
• 29 Cho Y, Sloutsky R, Naegle KM, Cavalli V. Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell 155(4), 894–908 (2013).
  Medline CASGoogle Scholar
• 30 Cho Y, Cavalli V. HDAC signaling in neuronal development and axon regeneration. Curr. Opin. Neurobiol. 27, 118–126 (2014).
  Medline CASGoogle Scholar
• 31 Cho Y, Cavalli V. HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J. 31(14), 3063–3078 (2012).
  Medline CASGoogle Scholar
• 32 Cho Y, Park D, Cavalli V. Filamin A is required in injured axons for HDAC5 activity and axon regeneration. J. Biol. Chem. 290(37), 22759–22770 (2015).
  Medline CASGoogle Scholar
• 33 Rivieccio MA, Brochier C, Willis DE et al. HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc. Natl Acad. Sci. USA 106(46), 19599–19604 (2009).
  Medline CASGoogle Scholar
• 34 Abe N, Cavalli V. Nerve injury signaling. Curr. Opin. Neurobiol. 18(3), 276–283 (2008).
  Medline CASGoogle Scholar
• 35 Teng FY, Tang BL. Axonal regeneration in adult CNS neurons-signaling molecules and pathways. J. Neurochem. 96(6), 1501–1508 (2006).
  Medline CASGoogle Scholar
• 36 West AE, Griffith EC, Greenberg ME. Regulation of transcription factors by neuronal activity. Nat. Rev. Neurosci. 3(12), 921–931 (2002).
  Medline CASGoogle Scholar
• 37 Mar FM, Bonni A, Sousa MM. Cell intrinsic control of axon regeneration. EMBO Rep. 15(3), 254–263 (2014).
  Medline CASGoogle Scholar
• 38 Schmitt HM, Pelzel HR, Schlamp CL, Nickells RW. Histone deacetylase 3 (HDAC3) plays an important role in retinal ganglion cell death after acute optic nerve injury. Mol. Neurodegener. 9, 39 (2014).
  MedlineGoogle Scholar
• 39 Shin J, Ming GL, Song H. Decoding neural transcriptomes and epigenomes via high-throughput sequencing. Nat. Neurosci. 17(11), 1463–1475 (2014).
  Medline CASGoogle Scholar
• 40 Jones PA. Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat. Rev. Genet. 13(7), 484–492 (2012).
  Medline CASGoogle Scholar
• 41 Hellman A, Chess A. Gene body-specific methylation on the active X chromosome. Science 315(5815), 1141–1143 (2007).
  Medline CASGoogle Scholar
• 42 Shukla S, Kavak E, Gregory M et al. CTCF-promoted RNA polymerase II pausing links DNA methylation to splicing. Nature 479(7371), 74–79 (2011).
  Medline CASGoogle Scholar
• 43 Weng YL, An R, Shin J, Song H, Ming GL. DNA modifications and neurological disorders. Neurotherapeutics 10(4), 556–567 (2013).
  Medline CASGoogle Scholar
• 44 Guo JU, Su Y, Shin JH et al. Distribution, recognition and regulation of non-CpG methylation in the adult mammalian brain. Nat. Neurosci. 17(2), 215–222 (2014).
  Medline CASGoogle Scholar
• 45 Laplant Q, Vialou V, Covington HE 3rd et al. Dnmt3a regulates emotional behavior and spine plasticity in the nucleus accumbens. Nat. Neurosci. 13(9), 1137–1143 (2010).
  Medline CASGoogle Scholar
• 46 Pollema-Mays SL, Centeno MV, Apkarian AV, Martina M. Expression of DNA methyltransferases in adult dorsal root ganglia is cell-type specific and up regulated in a rodent model of neuropathic pain. Front. Cell. Neurosci. 8, 217 (2014).
  MedlineGoogle Scholar
• 47 Delree P, Leprince P, Schoenen J, Moonen G. Purification and culture of adult rat dorsal root ganglia neurons. J. Neurosci. Res. 23(2), 198–206 (1989).
  Medline CASGoogle Scholar
• 48 Iskandar BJ, Rizk E, Meier B et al. Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J. Clin. Invest. 120(5), 1603–1616 (2010).
  Medline CASGoogle Scholar
• 49 Ma DK, Guo JU, Ming GL, Song H. DNA excision repair proteins and Gadd45 as molecular players for active DNA demethylation. Cell Cycle 8(10), 1526–1531 (2009).
  Medline CASGoogle Scholar
• 50 Guo JU, Ma DK, Mo H et al. Neuronal activity modifies the DNA methylation landscape in the adult brain. Nat. Neurosci. 14(10), 1345–1351 (2011).
  Medline CASGoogle Scholar
• 51 Ito S, Shen L, Dai Q et al. TET proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333(6047), 1300–1303 (2011).
  Medline CASGoogle Scholar
• 52 Tahiliani M, Koh KP, Shen Y et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324(5929), 930–935 (2009).
  Medline CASGoogle Scholar
• 53 He YF, Li BZ, Li Z et al. Tet-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science 333(6047), 1303–1307 (2011).
  Medline CASGoogle Scholar
• 54 Yu H, Su Y, Shin J et al. Tet3 regulates synaptic transmission and homeostatic plasticity via DNA oxidation and repair. Nat. Neurosci. 18(6), 836–843 (2015).
  Medline CASGoogle Scholar
• 55 Rudenko A, Dawlaty MM, Seo J et al. Tet1 is critical for neuronal activity-regulated gene expression and memory extinction. Neuron 79(6), 1109–1122 (2013).
  Medline CASGoogle Scholar
• 56 Zhang RR, Cui QY, Murai K et al. Tet1 regulates adult hippocampal neurogenesis and cognition. Cell Stem Cell 13(2), 237–245 (2013).
  MedlineGoogle Scholar
• 57 Li T, Yang D, Li J, Tang Y, Yang J, Le W. Critical role of Tet3 in neural progenitor cell maintenance and terminal differentiation. Mol. Neurobiol. 51(1), 142–154 (2015).
  Medline CASGoogle Scholar
• 58 Papale LA, Zhang Q, Li S, Chen K, Keles S, Alisch RS. Genome-wide disruption of 5-hydroxymethylcytosine in a mouse model of autism. Hum. Mol. Genet. 24(24), 7121–7131 (2015).
  Medline CASGoogle Scholar
• 59 Hahn MA, Qiu R, Wu X et al. Dynamics of 5-hydroxymethylcytosine and chromatin marks in Mammalian neurogenesis. Cell Rep. 3(2), 291–300 (2013).
  Medline CASGoogle Scholar
• 60 Xu Y, Xu C, Kato A et al. Tet3 CXXC domain and dioxygenase activity cooperatively regulate key genes for Xenopus eye and neural development. Cell 151(6), 1200–1213 (2012).
  Medline CASGoogle Scholar
• 61 Szulwach KE, Li X, Li Y et al. 5-hmC-mediated epigenetic dynamics during postnatal neurodevelopment and aging. Nat. Neurosci. 14(12), 1607–1616 (2011).
  Medline CASGoogle Scholar
• 62 Wu H, D’Alessio AC, Ito S et al. Genome-wide analysis of 5-hydroxymethylcytosine distribution reveals its dual function in transcriptional regulation in mouse embryonic stem cells. Genes Dev. 25(7), 679–684 (2011).
  Medline CASGoogle Scholar
• 63 Endres M, Meisel A, Biniszkiewicz D et al. DNA methyltransferase contributes to delayed ischemic brain injury. J. Neurosci. 20(9), 3175–3181 (2000).
  Medline CASGoogle Scholar
• 64 Chestnut BA, Chang Q, Price A, Lesuisse C, Wong M, Martin LJ. Epigenetic regulation of motor neuron cell death through DNA methylation. J. Neurosci. 31(46), 16619–16636 (2011).
  Medline CASGoogle Scholar
• 65 Petell CJ, Alabdi L, He M, San MP, Rose R, Gowher H. An epigenetic switch regulates de novo DNA methylation at a subset of pluripotency gene enhancers during embryonic stem cell differentiation. Nucleic Acids Res. doi:10.1093/nar/gkw426 (2016) (Epub ahead of print).
  MedlineGoogle Scholar
• 66 Nakamura T, Liu YJ, Nakashima H et al. PGC7 binds histone H3K9me2 to protect against conversion of 5mC to 5hmC in early embryos. Nature 486(7403), 415–419 (2012).
  Medline CASGoogle Scholar
• 67 Rose NR, Klose RJ. Understanding the relationship between DNA methylation and histone lysine methylation. Biochim. Biophys. Acta 1839(12), 1362–1372 (2014).
  Medline CASGoogle Scholar
• 68 Im HI, Kenny PJ. MicroRNAs in neuronal function and dysfunction. Trends Neurosci. 35(5), 325–334 (2012).
  Medline CASGoogle Scholar
• 69 Li Z, Rana TM. Therapeutic targeting of microRNAs: current status and future challenges. Nat. Rev. Drug Discov. 13(8), 622–638 (2014).
  Medline CASGoogle Scholar
• 70 Liu CM, Wang RY, Saijilafu, Jiao ZX, Zhang BY, Zhou FQ. MicroRNA-138 and SIRT1 form a mutual negative feedback loop to regulate mammalian axon regeneration. Genes Dev. 27(13), 1473–1483 (2013).
  Medline CASGoogle Scholar
• 71 Lv L, Han X, Sun Y, Wang X, Dong Q. Valproic acid improves locomotion in vivo after SCI and axonal growth of neurons in vitro. Exp. Neurol. 233(2), 783–790 (2012).
  Medline CASGoogle Scholar
• 72 Strickland IT, Richards L, Holmes FE, Wynick D, Uney JB, Wong LF. Axotomy-induced miR-21 promotes axon growth in adult dorsal root ganglion neurons. PLoS ONE 6(8), e23423 (2011).
  Medline CASGoogle Scholar
• 73 Han F, Huo Y, Huang CJ, Chen CL, Ye J. MicroRNA-30b promotes axon outgrowth of retinal ganglion cells by inhibiting Semaphorin3A expression. Brain Res. 1611, 65–73 (2015).
  Medline CASGoogle Scholar
• 74 Jiang JJ, Liu CM, Zhang BY et al. MicroRNA-26a supports mammalian axon regeneration in vivo by suppressing GSK3beta expression. Cell Death Dis. 6, e1865 (2015).
  Medline CASGoogle Scholar
• 75 Lu XC, Zheng JY, Tang LJ et al. MiR-133b Promotes neurite outgrowth by targeting RhoA expression. Cell Physiol. Biochem. 35(1), 246–258 (2015).
  Medline CASGoogle Scholar
• 76 Hu YW, Jiang JJ, Yan G, Wang RY, Tu GJ. MicroRNA-210 promotes sensory axon regeneration of adult mice in vivo and in vitro. Neurosci. Lett. 622 61–66 (2016).
  Medline CASGoogle Scholar
• 77 Zhou S, Shen D, Wang Y et al. MicroRNA-222 targeting PTEN promotes neurite outgrowth from adult dorsal root ganglion neurons following sciatic nerve transection. PLoS ONE 7(9), e44768 (2012).
  Medline CASGoogle Scholar
• 78 Wu D, Murashov AK. MicroRNA-431 regulates axon regeneration in mature sensory neurons by targeting the Wnt antagonist Kremen1. Front. Mol. Neurosci. 6, 35 (2013).
  Medline CASGoogle Scholar
• 79 Zeng L, He X, Wang Y et al. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther. 21(1), 37–43 (2014).
  Medline CASGoogle Scholar
• 80 Zhou J, Wan J, Gao X, Zhang X, Jaffrey SR, Qian SB. Dynamic m(6)A mRNA methylation directs translational control of heat shock response. Nature 526(7574), 591–594 (2015).
  Medline CASGoogle Scholar
• 81 Li S, Wang X, Gu Y et al. Let-7 microRNAs regenerate peripheral nerve regeneration by targeting nerve growth factor. Mol. Ther. 23(3), 423–433 (2015).
  Medline CASGoogle Scholar
• 82 Ma DK, Jang MH, Guo JU et al. Neuronal activity-induced Gadd45b promotes epigenetic DNA demethylation and adult neurogenesis. Science 323(5917), 1074–1077 (2009).
  Medline CASGoogle Scholar
• 83 Hilton IB, D’Ippolito AM, Vockley CM et al. Epigenome editing by a CRISPR–Cas9-based acetyltransferase activates genes from promoters and enhancers. Nat. Biotechnol. 33(5), 510–517 (2015).
  Medline CASGoogle Scholar
• 84 Painter MW, Brosius Lutz A, Cheng YC et al. Diminished Schwann cell repair responses underlie age-associated impaired axonal regeneration. Neuron 83(2), 331–343 (2014).
  Medline CASGoogle Scholar
• 85 Varela-Rey M, Iruarrizaga-Lejarreta M, Lozano JJ et al. S-adenosylmethionine levels regulate the schwann cell DNA methylome. Neuron 81(5), 1024–1039 (2014).
  Medline CASGoogle Scholar
• 86 Hung HA, Sun G, Keles S, Svaren J. Dynamic regulation of Schwann cell enhancers after peripheral nerve injury. J. Biol. Chem. 290(11), 6937–6950 (2015).
  Medline CASGoogle Scholar
• 87 Fu Y, Dominissini D, Rechavi G, He C. Gene expression regulation mediated through reversible m(6)A RNA methylation. Nat. Rev. Genet. 15(5), 293–306 (2014).
  Medline CASGoogle Scholar
• 88 Dominissini D, Moshitch-Moshkovitz S, Schwartz S et al. Topology of the human and mouse m6A RNA methylomes revealed by m6A-seq. Nature 485(7397), 201–206 (2012).
  Medline CASGoogle Scholar