Reshaping the chromatin landscape after spinal cord injury

Frontiers in Biology

Volumn 9, Issue 5, 2014, Pages 356-366

  Wong, Jamie K ^a   Zou, Hongyan ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

axon regeneration; chromatin; epigenetics; neural repair; spinal cord injury

Indexed keywords

EID: 85027938008     PISSN: 16747984     EISSN: 16747992     Source Type: Journal    
DOI: 10.1007/s11515-014-1329-8     Document Type: Review

References (83)

1. 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
2. Aguzzi A, Barres B A, Bennett M L (2013). Microglia: scapegoat, saboteur, or something else?. Science, 339(6116): 156–161
3. 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
4. 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
5. 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
6. 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
7. 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
8. 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
9. 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
10. 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
11. 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
12. 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
13. 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
14. Cho Y, Cavalli V (2012). HDAC5 is a novel injury-regulated tubulin deacetylase controlling axon regeneration. EMBO J, 31(14): 3063–3078
15. Cho Y, Cavalli V (2014). HDAC signaling in neuronal development and axon regeneration. Curr Opin Neurobiol, 27C: 118–126
16. 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
17. David S, Kroner A (2011). Repertoire of microglial and macrophage responses after spinal cord injury. Nat Rev Neurosci, 12(7): 388–399
18. 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
19. 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
20. 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
21. 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
22. 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
23. 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
24. 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
25. 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
26. 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
27. 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
28. Gordon S, Martinez F O (2010). Alternative activation of macrophages: mechanism and functions. Immunity, 32(5): 593–604
29. 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
30. 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
31. 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
32. 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
33. 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
34. 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
35. 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
36. 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
37. 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
38. Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693–705
39. 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
40. 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
41. 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
42. Liu K, Tedeschi A, Park K K, He Z (2011). Neuronal intrinsic mechanisms of axon regeneration. Annu Rev Neurosci, 34(1): 131–152
43. 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
44. 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
45. 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
46. 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
47. 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
48. 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
49. Monti B, Polazzi E, Contestabile A (2009). Biochemical, molecular and epigenetic mechanisms of valproic acid neuroprotection. Curr Mol Pharmacol 2: 95–109
50. 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
51. 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
52. 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
53. 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
54. 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
55. Peleg S (2010). Memory impairment in mice altered histone acetylation is associated with age-dependent. Science, 328: 753–756
56. 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
57. 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
58. Popovich P G, Longbrake E E (2008). Can the immune system be harnessed to repair the CNS?. Nat Rev Neurosci, 9: 481–493
59. 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
60. 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
61. Richardson P M, Issa V M (1984). Peripheral injury enhances central regeneration of primary sensory neurones. Nature, 309(5971): 791–793
62. 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
63. 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
64. 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
65. Silver J, Miller J H (2004). Regeneration beyond the glial scar. Nat Rev Neurosci, 5(2): 146–156
66. 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
67. 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
68. 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
69. 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
70. Tang B L (2014). Class II HDACs and neuronal regeneration. J Cell Biochem, 115(7): 1225–1233
71. 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
72. 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
73. Totoiu M O, Keirstead H S (2005). Spinal cord injury is accompanied by chronic progressive demyelination. J Comp Neurol, 486(4): 373–383
74. Trakhtenberg E F, Goldberg J L (2012). Epigenetic regulation of axon and dendrite growth. Front Mol Neurosci, 5: 24
75. 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
76. 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
77. 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
78. 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
79. 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
80. York E M, Petit A, Roskams A J (2013). Epigenetics of neural repair following spinal cord injury. Neurotherapeutics, 10(4): 757–770
81. 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
82. Zhong J, Zou H (2014). BMP signaling in axon regeneration. Curr Opin Neurobiol, 27C: 127–134
83. 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