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Front. Biol.    2014, Vol. 9 Issue (5) : 356-366    https://doi.org/10.1007/s11515-014-1329-8
REVIEW
Reshaping the chromatin landscape after spinal cord injury
Jamie K. WONG1,Hongyan ZOU1,2,*()
1. Fishberg Department of Neuroscience, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
2. Department of Neurosurgery, Friedman Brain Institute, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
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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.
Keywords epigenetics      chromatin      spinal cord injury      axon regeneration      neural repair     
Corresponding Author(s): Hongyan ZOU   
Just Accepted Date: 13 August 2014   Online First Date: 02 September 2014    Issue Date: 11 October 2014
 Cite this article:   
Jamie K. WONG,Hongyan ZOU. Reshaping the chromatin landscape after spinal cord injury[J]. Front. Biol., 2014, 9(5): 356-366.
 URL:  
https://academic.hep.com.cn/fib/EN/10.1007/s11515-014-1329-8
https://academic.hep.com.cn/fib/EN/Y2014/V9/I5/356
Fig.1  Histone and DNA modifications. The covalent addition or removal of acetyl groups to the lysine residues on histone N-terminal tails is catalyzed by histone acetyltransferases (HATs) and histone deacetylases (HDACs), respectively. The covalent addition or removal of methyl groups to the lysine residues on histone tails is catalyzed by histone methyltransferases (HMTs) and histone demethylases (HDMs), respectively. The covalent addition of methyl groups to cytosine residues on DNA is catalyzed by DNA methytransferases (DNMTs), whereas the initial step of active DNA demethylation is catalyzed by the TET family of enzymes that convert the 5-methylcytosine (5-mC) to 5-hydroxymethylcytosine (5-hmC). Different colors of histone acetylation (depicted by round shapes) or histone methylation (depicted by star shapes) denote modifications on different lysine residues.
AgentsInjury modelSpeciesTargetTreatmentIn vivo effects
Valproic acidT8 moderate contusionRatClass I HDACs300 mg/kg i.p., twice daily immediately after injury for 2 wks- ↑ AcH3, AcH4, Bcl-2, HSP-70- Decreased apoptosis- Improved functional recovery(Lv et al., 2011)
Valproic acidT9 moderate contusionRatClass I HDACs300 mg/kg i.p., twice daily, starting 8 h post injury for 1 wk- ↑?AcH3, BDNF, GDNF- Reduced apoptosis- Smaller lesion volume- Improved functional recovery(Lv et al., 2012)
Valproic acidT9-T10 moderate contusionRatClass I HDACs150 or 300 mg/kg s.c., immediately after injury then every 12 h for 5 d- ↑? H3K9Ac-??↓ MMP-9, blood-spinal cord barrier breakdown, inflammation, apoptosis, lesion volume- Improved functional recovery(Lee et al., 2012)
Valproic acidT9 clip compressionRatClass I HDACs200 mg/kg i.p., twicedaily for 1 wk- ↑?AcH3K, AcH3K18- ↓?ED-1+ macrophages- Smaller lesion volume- Improved functional recovery(Yu et al., 2012)
Valproic acidT9-T10 very severe contusionRatClass I HDACs500 ng/d, osmotic pump for 3 d- ↑?SOD-??↓ macrophages/microglia, astrocytes, P2X4R- Preserved tissue and nerve fibers- Improved functional recovery(Lu et al., 2013)
MS-275C5 dorsal column transectionMouseHDAC1 & 312.5 mg/kg s.c., immediately after injury, then daily for 4 d- ↑? AcH4- ↑?RAG transcription- Enhanced sensory axon regeneration(Finelli et al., 2013)
AAVP/CAFT9-T10 dorsal hemi-crushMousePCAFSciatic nerve injection, 2 wks prior to injury- ↑?H3K9Ac- ↑?RAG expression- Enhanced sensory axon regeneration(Puttagunta et al., 2014)
AVp300Optic nerve crushRatp300Intraocular injection at time of injury- ↑ Ac-p53, -C/EBP, H3K18Ac- ↑? RAG expression- Enhanced optic nerve regeneration- No effect on RGC survival(Gaub et al., 2011)
TSAOptic nerve crushRatClass I/II HDACs1, 10 or 100 ng/mL, injected into the vitreous at the time of injury.- Improved RGC survival- No effect on axon regeneration(Gaub et al., 2011)
Tab.1  Summary of studies employing epigenetic modulators in spinal cord or optic nerve injury models
Fig.2  Nuclear epigenetic events for RAGs induction. In mature neurons in the CNS, pro-growth genes are generally downregulated by a repressive transcriptional complex, which may encompass transcription factor (TF), histone-modifying enzyme (HME) and chromatin remodeler (CR), to compact local chromatin. Upon stimulation, activated proregenerative transcription factors, such as Smad1, are recruited to the respective regulatory elements on specific genomic loci, and orchestrate recruitment of regeneration-associated HMEs and CRs to relax local chromatin, which further facilitates promoter occupancy of TFs, leading to a chromatin landscape favorable for expression of regeneration-associated genes (RAGs).
Fig.3  Injury responses of neurons and glia after SCI. Axon regeneration is controlled by intrinsic proregenerative transcriptional programs and influenced by environmental signals. Myelin debris from demyelinating oligodendrocytes and chondroitin sulfate proteoglycans (CSPG) secreted from reactive astrocytes constitute a roadblock for axonal regeneration. M2 macrophages can promote axonal regrowth. A nuclear program is activated by peripheral axotomy of DRG neurons, leading to increased histone acetylation and induction of RAGs. Histone-modifying enzymes participate in various aspects of injury responses in neurons and glial cells. Note that the epigenetic regulators controlling macrophage polarization have only been demonstrated in non-spinal cord injury settings.
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