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Reshaping the chromatin landscape after spinal cord injury

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Frontiers in Biology

Abstract

The pathophysiology underlying spinal cord injury is complex. Mechanistic understanding of the adaptive responses to injury is critical for targeted therapy aimed at reestablishing lost connections between proximal and distal neurons. After injury, cell-type specific gene transcription programs govern distinct cellular behaviors, and chromatin regulators play a central role in shaping the chromatin landscape to adjust transcriptional profiles in a context-dependent manner. In this review, we summarize recent progress on the pleiotropic roles of chromatin regulators in mediating the diverse adaptive behaviors of neurons and glial cells after spinal cord injury, and wherever possible, discuss the underlying mechanisms and genomic targets. We specifically draw attention to the perspective that takes into consideration the impact of epigenetic modulation on axon growth potential, together with its effect on wound-healing properties of glial cells. Epigenetic modulation of chromatin state represents an emerging therapeutic direction to promote neural repair and axon regeneration after spinal cord injury.

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References

  • Abematsu M, Tsujimura K, Yamano M, Saito M, Kohno K, Kohyama J, Namihira M, Komiya S, Nakashima K (2010). Neurons derived from transplanted neural stem cells restore disrupted neuronal circuitry in a mouse model of spinal cord injury. J Clin Invest, 120(9): 3255–3266

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Aguzzi A, Barres B A, Bennett M L (2013). Microglia: scapegoat, saboteur, or something else?. Science, 339(6116): 156–161

    Article  PubMed  CAS  Google Scholar 

  • Ashburner B P, Westerheide S D, Baldwin A S Jr (2001). The p65 (RelA) subunit of NF-κB interacts with the histone deacetylase (HDAC) corepressors HDAC1 and HDAC2 to negatively regulate gene expression. Mol Cell Biol, 21(20): 7065–7077

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bardehle S, Krüger M, Buggenthin F, Schwausch J, Ninkovic J, Clevers H, Snippert H J, Theis F J, Meyer-Luehmann M, Bechmann I, Dimou L, Götz M (2013). Live imaging of astrocyte responses to acute injury reveals selective juxtavascular proliferation. Nat Neurosci, 16(5): 580–586

    Article  PubMed  CAS  Google Scholar 

  • Barnabé-Heider F, Göritz C, Sabelström H, Takebayashi H, Pfrieger F W, Meletis K, Frisén J (2010). Origin of new glial cells in intact and injured adult spinal cord. Cell Stem Cell, 7(4): 470–482

    Article  PubMed  Google Scholar 

  • Bartholdi D, Schwab M E (1997). Expression of pro-inflammatory cytokine and chemokine mRNA upon experimental spinal cord injury in mouse: an in situ hybridization study. Eur J Neurosci, 9(7): 1422–1438

    Article  PubMed  CAS  Google Scholar 

  • Beck K D, Nguyen H X, Galvan M D, Salazar D L, Woodruff T M, Anderson A J (2010). Quantitative analysis of cellular inflammation after traumatic spinal cord injury: evidence for a multiphasic inflammatory response in the acute to chronic environment. Brain, 133(Pt 2): 433–447

    Article  PubMed  PubMed Central  Google Scholar 

  • Bethea J R, Castro M, Keane RW, Lee T T, Dietrich WD, Yezierski R P (1998). Traumatic spinal cord injury induces nuclear factor-κB activation. J Neurosci, 18(9): 3251–3260

    PubMed  CAS  Google Scholar 

  • Broide R S, Redwine J M, Aftahi N, Young W, Bloom F E, Winrow C J (2007). Distribution of histone deacetylases 1–11 in the rat brain. J Mol Neurosci, 31(1): 47–58

    Article  PubMed  CAS  Google Scholar 

  • Buffo A, Rite I, Tripathi P, Lepier A, Colak D, Horn A P, Mori T, Götz M (2008). Origin and progeny of reactive gliosis: A source of multipotent cells in the injured brain. Proc Natl Acad Sci USA, 105(9): 3581–3586

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Carlson S L, Parrish M E, Springer J E, Doty K, Dossett L (1998). Acute inflammatory response in spinal cord following impact injury. Exp Neurol, 151(1): 77–88

    Article  PubMed  CAS  Google Scholar 

  • Carmel J B, Galante A, Soteropoulos P, Tolias P, Recce M, Young W, Hart R P (2001). Gene expression profiling of acute spinal cord injury reveals spreading inflammatory signals and neuron loss. Physiol Genomics, 7(2): 201–213

    PubMed  CAS  Google Scholar 

  • Chen L F, Fischle W, Verdin E, Greene WC (2001). Duration of nuclear NF-kappaB action regulated by reversible acetylation. Science, 293(5535): 1653–1657

    Article  CAS  Google Scholar 

  • Cho Y, Cavalli V (2012). HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J, 31(14): 3063–3078

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Cho Y, Cavalli V (2014). HDAC signaling in neuronal development and axon regeneration. Curr Opin Neurobiol, 27C: 118–126

    Article  Google Scholar 

  • Cho Y, Sloutsky R, Naegle K M, Cavalli V (2013). Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell, 155(4): 894–908

    Article  PubMed  CAS  Google Scholar 

  • David S, Kroner A (2011). Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci, 12(7): 388–399

    Article  PubMed  CAS  Google Scholar 

  • de Lima S, Koriyama Y, Kurimoto T, Oliveira J T, Yin Y, Li Y, Gilbert H Y, Fagiolini M, Martinez A M, Benowitz L (2012). Full-length axon regeneration in the adult mouse optic nerve and partial recovery of simple visual behaviors. Proc Natl Acad Sci USA, 109(23): 9149–9154

    Article  PubMed  PubMed Central  Google Scholar 

  • De Santa F, Narang V, Yap Z H, Tusi B K, Burgold T, Austenaa L, Bucci G, Caganova M, Notarbartolo S, Casola S, Testa G, Sung W K, WeiC L, Natoli G (2009). Jmjd3 contributes to the control of gene expression in LPS-activated macrophages. EMBO J, 28(21): 3341–3352

    Article  PubMed  PubMed Central  Google Scholar 

  • Elsharkawy A M, Oakley F, Lin F, Packham G, Mann D A, Mann J (2010). The NF-κB p50:p50:HDAC-1 repressor complex orchestrates transcriptional inhibition of multiple pro-inflammatory genes. J Hepatol, 53(3): 519–527

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ernst J, Kheradpour P, Mikkelsen T S, Shoresh N, Ward L D, Epstein C B, Zhang X, Wang L, Issner R, Coyne M, Ku M, Durham T, Kellis M, Bernstein B E (2011). Mapping and analysis of chromatin state dynamics in nine human cell types. Nature, 473(7345): 43–49

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Faraco G, Pittelli M, Cavone L, Fossati S, Porcu M, Mascagni P, Fossati G, Moroni F, Chiarugi A (2009). Histone deacetylase (HDAC) inhibitors reduce the glial inflammatory response in vitro and in vivo. Neurobiol Dis, 36(2): 269–279

    Article  PubMed  CAS  Google Scholar 

  • Faulkner J R, Herrmann J E, Woo M J, Tansey K E, Doan N B, Sofroniew M V (2004). Reactive astrocytes protect tissue and preserve function after spinal cord injury. J Neurosci, 24(9): 2143–22155

    Article  PubMed  CAS  Google Scholar 

  • Finelli M J, Wong J K, Zou H (2013). Epigenetic regulation of sensory axon regeneration after spinal cord injury. J Neurosci, 33(50): 19664–19676

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gaub P, Joshi Y, Wuttke A, Naumann U, Schnichels S, Heiduschka P, Di Giovanni S (2011). The histone acetyltransferase p300 promotes intrinsic axonal regeneration. Brain, 134(Pt 7): 2134–2148

    Article  PubMed  Google Scholar 

  • Gaub P, Tedeschi A, Puttagunta R, Nguyen T, Schmandke A, Di Giovanni S (2010). 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

    Article  PubMed  CAS  Google Scholar 

  • Gensel J C, Nakamura S, Guan Z, van Rooijen N, Ankeny D P, Popovich P G (2009). Macrophages promote axon regeneration with concurrent neurotoxicity. J Neurosci, 29(12): 3956–3968

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Gordon S, Martinez F O (2010). Alternative activation of macrophages: mechanism and functions. Immunity, 32(5): 593–604

    Article  PubMed  CAS  Google Scholar 

  • Göritz C, Dias D O, Tomilin N, Barbacid M, Shupliakov O, Frisén J (2011). A pericyte origin of spinal cord scar tissue. Science, 333(6039): 238–242

    Article  PubMed  Google Scholar 

  • Guo Z, Zhang L, Wu Z, Chen Y, Wang F, Chen G (2014). In Vivo directreprogramming of reactive glial cells into functional neurons afterbrain injury and in an Alzheimer’s disease model. Cell Stem Cell, 14(2): 188–202

    Article  PubMed  CAS  Google Scholar 

  • Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage F H (2004). Histone deacetylase inhibition-mediated neuronal differentiation of multipotentadult neural progenitor cells. Proc Natl Acad Sci USA, 101(47): 16659–16664

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Ishii K, Toda M, Nakai Y, Asou H, Watanabe M, Nakamura M, Yato Y, Fujimura Y, Kawakami Y, Toyama Y, Uyemura K (2001). Increase of oligodendrocyte progenitor cells after spinal cord injury. J Neurosci Res, 65(6): 500–507

    Article  PubMed  CAS  Google Scholar 

  • Iskandar B J, Rizk E, Meier B, Hariharan N, Bottiglieri T, Finnell R H, Jarrard D F, Banerjee R V, Skene J H, Nelson A, Patel N, Gherasim C, Simon K, Cook T D, Hogan K J (2010). Folate regulation of axonal regeneration in the rodent central nervous system through DNA methylation. J Clin Invest, 120(5): 1603–1616

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Karow M, Sánchez R, Schichor C, Masserdotti G, Ortega F, Heinrich C, Gascón S, Khan M A, Lie D C, Dellavalle A, Cossu G, Goldbrunner R, Götz M, Berninger B (2012). Reprogramming of pericyte-derived cells of the adult human brain into induced neuronal cells. Cell Stem Cell, 11(4): 471–476

    Article  PubMed  CAS  Google Scholar 

  • Kigerl K A, Gensel J C, Ankeny D P, Alexander J K, Donnelly D J, Popovich P G (2009). Identification of two distinct macrophage subsets with divergent effects causing either neurotoxicity or regeneration in the injured mouse spinal cord. J Neurosci, 29(43): 13435–13444

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Kim J Y, Shen S, Dietz K, He Y, Howell O, Reynolds R, Casaccia P (2010). HDAC1 nuclear export induced by pathological conditions is essential for the onset of axonal damage. Nat Neurosci, 13(2): 180–189

    Article  PubMed  PubMed Central  Google Scholar 

  • Konsoula Z, Barile F A (2012). Epigenetic histone acetylation and deacetylation mechanisms in experimental models of neurodegenerative disorders. J Pharmacol Toxicol Methods, 66(3): 215–220

    Article  PubMed  CAS  Google Scholar 

  • Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693–705

    Article  PubMed  CAS  Google Scholar 

  • Lee J Y, Kim H S, Choi H Y, Oh T H, Ju B G, Yune T Y (2012). Valproic acid attenuates blood-spinal cord barrier disruption by inhibiting matrix metalloprotease-9 activity and improves functional recovery after spinal cord injury. J Neurochem, 121(5): 818–829

    Article  PubMed  CAS  Google Scholar 

  • Lindner R, Puttagunta R, Di Giovanni S (2013). Epigenetic regulation of axon outgrowth and regeneration in CNS injury: the first steps forward. Neurotherapeutics, 10(4): 771–781

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Hu Q, D’ercole A J, Ye P (2009). Histone deacetylase 11 regulates oligodendrocyte-specific gene expression and cell development in OL-1 oligodendroglia cells. Glia, 57(1): 1–12

    Article  PubMed  PubMed Central  Google Scholar 

  • Liu K, Tedeschi A, Park K K, He Z (2011). Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci, 34(1): 131–152

    Article  PubMed  Google Scholar 

  • Lu P, Wang Y, Graham L, McHale K, Gao M, Wu D, Brock J, Blesch A, Rosenzweig E S, Havton L A, Zheng B, Conner J M, Marsala M, Tuszynski M H (2012). Long-distance growth and connectivity of neural stem cells after severe spinal cord injury. Cell, 150(6): 1264–1273

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lu W H, Wang C Y, Chen P S, Wang J W, Chuang D M, Yang C S, Tzeng S F (2013). Valproic acid attenuates microgliosis in injured spinal cord and purinergic P2X4 receptor expression in activated microglia. J Neurosci Res, 91(5): 694–705

    Article  PubMed  CAS  Google Scholar 

  • Lv L, Han X, Sun Y, Wang X, Dong Q (2012). Valproic acid improves locomotion in vivo after SCI and axonal growth of neurons in vitro. Exp Neurol, 233(2): 783–790

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Lv L, Sun Y, Han X, Xu C C, Tang Y P, Dong Q (2011). Valproic acid improves outcome after rodent spinal cord injury: potential roles of histone deacetylase inhibition. Brain Res, 1396: 60–68

    Article  PubMed  CAS  Google Scholar 

  • McTigue D M, Wei P, Stokes B T (2001). Proliferation of NG2-positive cells and altered oligodendrocyte numbers in the contused rat spinal cord. J Neurosci, 21(10): 3392–3400

    PubMed  CAS  Google Scholar 

  • Montgomery R L, Hsieh J, Barbosa A C, Richardson J A, Olson E N (2009). Histone deacetylases 1 and 2 control the progression of neural precursors to neurons during brain development. Proc Natl Acad Sci USA, 106(19): 7876–7881

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Monti B, Polazzi E, Contestabile A (2009). Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection. Curr Mol Pharmacol 2: 95–109

    Article  PubMed  CAS  Google Scholar 

  • Mullican S E, Gaddis C A, Alenghat T, Nair MG, Giacomin P R, EverettL J, Feng D, Steger D J, Schug J, Artis D, Lazar MA (2011). Histone deacetylase 3 is an epigenomic brake in macrophage alternative activation. Genes Dev, 25(23): 2480–2488

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Neumann S, Woolf C J (1999). Regeneration of dorsal column fibers into and beyond the lesion site following adult spinal cord injury. Neuron, 23(1): 83–91

    Article  PubMed  CAS  Google Scholar 

  • Niu W, Zang T, Zou Y, Fang S, Smith D K, Bachoo R, Zhang C L (2013). In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat Cell Biol, 15(10): 1164–1175

    Article  PubMed  CAS  Google Scholar 

  • Oakley F, Mann J, Nailard S, Smart D E, Mungalsingh N, Constandinou C, Ali S, Wilson S J, Millward-Sadler H, Iredale J P, Mann D A (2005). Nuclear factor-κB1 (p50) limits the inflammatory and fibrogenic responses to chronic injury. Am J Pathol, 166(3): 695–708

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Parikh P, Hao Y, Hosseinkhani M, Patil S B, Huntley G W, Tessier-Lavigne M, Zou H (2011). Regeneration of axons in injured spinal cord by activation of bone morphogenetic protein/Smad1 signaling pathway in adult neurons. Proc Natl Acad Sci USA, 108(19): E99–E107

    Article  PubMed  PubMed Central  Google Scholar 

  • Peleg S (2010). Memory impairment in mice altered histone acetylation is associated with age-dependent. Science, 328: 753–756

    Article  PubMed  CAS  Google Scholar 

  • Ponomarev E D, Maresz K, Tan Y, Dittel B N (2007). CNS-derived interleukin-4 is essential for the regulation of autoimmune inflammation and induces a state of alternative activation in microglial cells. J Neurosci, 27(40): 10714–10721

    Article  PubMed  CAS  Google Scholar 

  • Popovich P G, Jones T B (2003). Manipulating neuroinflammatory reactions in the injured spinal cord: back to basics. Trends Pharmacol Sci, 24(1): 13–17

    Article  PubMed  CAS  Google Scholar 

  • Popovich P G, Longbrake E E (2008). Can the immune system be harnessed to repair the CNS?. Nat Rev Neurosci, 9: 481–493

    Article  PubMed  CAS  Google Scholar 

  • Puttagunta R, Tedeschi A, Sória M G, Hervera A, Lindner R, Rathore K I, Gaub P, Joshi Y, Nguyen T, Schmandke A, Laskowski C J, Boutillier A L, Bradke F, Di Giovanni S (2014). PCAF-dependent epigenetic changes promote axonal regeneration in the central nervous system. Nat Commun, 5: 3527

    Article  PubMed  Google Scholar 

  • Ram O, Goren A, Amit I, Shoresh N, Yosef N, Ernst J, Kellis M, Gymrek M, Issner R, Coyne M, Durham T, Zhang X, Donaghey J, Epstein C B, Regev A, Bernstein B E (2011). Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells. Cell, 147(7): 1628–1639

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Richardson P M, Issa V M (1984). Peripheral injury enhances central regeneration of primary sensory neurones. Nature, 309(5971): 791–793

    Article  PubMed  CAS  Google Scholar 

  • Rivieccio M A, Brochier C, Willis D E, Walker B A, D’Annibale M A, McLaughlin K, Siddiq A, Kozikowski A P, Jaffrey S R, Twiss J L, Ratan R R, Langley B (2009). HDAC6 is a target for protection and regeneration following injury in the nervous system. Proc Natl Acad Sci USA, 106(46): 19599–19604

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Sabelström H, Stenudd M, Réu P, Dias D O, Elfineh M, Zdunek S, Damberg P, Göritz C, Frisén J (2013). Resident neural stem cells restrict tissue damage and neuronal loss after spinal cord injury in mice. Science, 342(6158): 637–640

    Article  PubMed  Google Scholar 

  • Shen S, Sandoval J, Swiss V A, Li J, Dupree J, Franklin R J, Casaccia-Bonnefil P (2008). Age-dependent epigenetic control of differentiation inhibitors is critical for remyelination efficiency. Nat Neurosci, 11(9): 1024–1034

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Silver J, Miller J H (2004). Regeneration beyond the glial scar. Nat Rev Neurosci, 5(2): 146–156

    Article  PubMed  CAS  Google Scholar 

  • Stolt C C, Rehberg S, Ader M, Lommes P, Riethmacher D, Schachner M, Bartsch U, Wegner M (2002). Terminal differentiation of myelinformingolig odendrocytes depends on the transcription factor Sox10. Genes Dev, 16(2): 165–170

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Su Z, Niu W, Liu M L, Zou Y, Zhang C L (2014). In vivo conversion of astrocytes to neurons in the injured adult spinal cord. Nat Commun, 5: 3338

    PubMed  PubMed Central  Google Scholar 

  • Su Z, Yuan Y, Chen J, Zhu Y, Qiu Y, Zhu F, Huang A, He C (2011). Reactive astrocytes inhibit the survival and differentiation of oligodendrocyte precursor cells by secreted TNF-α. J Neurotrauma, 28(6): 1089–1100

    Article  PubMed  Google Scholar 

  • Suyama K, Watanabe M, Sakai D, Osada T, Imai M, Mochida J (2007). Nkx2.2 expression in differentiation of oligodendrocyte precursor cells and inhibitory factors for differentiation of oligodendrocytes after traumatic spinal cord injury. J Neurotrauma, 24(6): 1013–1025

    Google Scholar 

  • Tang B L (2014). Class II HDACs and neuronal regeneration. J Cell Biochem, 115(7): 1225–1233

    Article  PubMed  CAS  Google Scholar 

  • Tedeschi A, Nguyen T, Puttagunta R, Gaub P, Di Giovanni S (2009). A p53-CBP/p300 transcription module is required for GAP-43 expression, axon outgrowth, and regeneration. Cell Death Differ, 16(4): 543–554

    Article  PubMed  CAS  Google Scholar 

  • Torper O, Pfisterer U, Wolf D A, Pereira M, Lau S, Jakobsson J, Björklund A, Grealish S, Parmar M (2013). Generation of induced neurons via direct conversion in vivo. Proc Natl Acad Sci USA, 110(17): 7038–7043

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Totoiu M O, Keirstead H S (2005). Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol, 486(4): 373–383

    Article  PubMed  Google Scholar 

  • Trakhtenberg E F, Goldberg J L (2012). Epigenetic regulation of axon and dendrite growth. Front Mol Neurosci, 5: 24

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wang Y, Cheng X, He Q, Zheng Y, Kim D H, Whittemore S R, Cao Q L (2011). Astrocytes from the contused spinal cord inhibit oligodendrocyte differentiation of adult oligodendrocyte precursor cells by increasing the expression of bone morphogenetic proteins. J Neurosci, 31(16): 6053–6058

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wanner I B, Anderson M A, Song B, Levine J, Fernandez A, Gray-Thompson Z, Ao Y, Sofroniew M V (2013). Glial scar borders are formed by newly proliferated, elongated astrocytes that interact to corral inflammatory and fibrotic cells via STAT3-dependent mechanisms after spinal cord injury. J Neurosci, 33(31): 12870–12886

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Wisniewski H M, Bloom B R (1975). Primary demyelination as a nonspecific consequence of a cell-mediated immune reaction. J Exp Med, 141(2): 346–359

    Article  PubMed  CAS  Google Scholar 

  • Xu J, Fan G, Chen S, Wu Y, Xu X M, Hsu C Y (1998). Methylprednisolone inhibition of TNF-α expression and NF-κB activation after spinal cord injury in rats. Brain Res Mol Brain Res, 59(2): 135–142

    Article  PubMed  CAS  Google Scholar 

  • Ye F, Chen Y, Hoang T, Montgomery R L, Zhao X H, Bu H, Hu T, Taketo M M, van Es J H, Clevers H, Hsieh J, Bassel-Duby R, Olson E N, Lu Q R (2009). HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the β-catenin-TCF interaction. Nat Neurosci, 12(7): 829–838

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • York E M, Petit A, Roskams A J (2013). Epigenetics of neural repair following spinal cord injury. Neurotherapeutics, 10(4): 757–770

    Article  PubMed  CAS  Google Scholar 

  • Zamanian J L, Xu L, Foo L C, Nouri N, Zhou L, Giffard R G, Barres B A (2012). Genomic analysis of reactive astrogliosis. J Neurosci, 32(18): 6391–6410

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Zhong J, Zou H (2014). BMP signaling in axon regeneration. Curr Opin Neurobiol, 27C: 127–134

    Article  Google Scholar 

  • Zou H, Ho C, Wong K, Tessier-Lavigne M (2009). Axotomy-induced Smad1 activation promotes axonal growth in adult sensory neurons. J Neurosci, 29(22): 7116–7123

    Article  PubMed  CAS  PubMed Central  Google Scholar 

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  1. Fishberg Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Jamie K. Wong & Hongyan Zou

  2. Department of Neurosurgery, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY, 10029, USA

    Hongyan Zou

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Wong, J.K., Zou, H. Reshaping the chromatin landscape after spinal cord injury. Front. Biol. 9, 356–366 (2014). https://doi.org/10.1007/s11515-014-1329-8

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