题名

Histone Deacetylases in Stroke

DOI

10.4103/CJP.CJP_22_19

作者

Mei-Han Kao；Teng-Nan Lin

关键词

Acetylation ； cerebral ischemia ； epigenetic regulation ； histone acetyl transferases

期刊名称

The Chinese Journal of Physiology

卷期/出版年月

62卷3期（2019 / 06 / 30）

页次

95 - 107

内容语文

英文
中文摘要

Stroke is the second leading cause of death and the leading cause of adult disability worldwide. Despite an impressive amount of neuroprotective agents that has been identified in experimental stroke, none of them proved efficient in clinical trials. There is a general consensus that an effective treatment requires the ability to interact with not one, but multiple pathophysiological cascades at different levels that induced by the insult - cocktail therapy. Luckily, recent progress in the field of epigenetics revealed that epigenetic modifications had influence on many known pathways involved in the complex course of ischemic disease development. The fact that epigenetic molecules, by altering transcriptional regulation, may simultaneously act on different levels of ischemic brain injury makes them promising candidates for clinical use. These modifications arise typically owing to deoxyribonucleic acid methylation and histone acetylation. The aim of this review is to give a comprehensive overview of current advances in stroke epigenetics, in particular, the physiological and pathological functions of the 11 classical histone deacetylases.
主题分类 醫藥衛生 > 基礎醫學
参考文献
  1. Bao, MH,Szeto, V,Yang, BB,Zhu, SZ,Sun, HS,Feng, ZP(2018).Long non‑coding RNAs in ischemic stroke.Cell Death Dis,9,281.
  2. Belzeaux, R,Formisano‑Tréziny, C,Loundou, A,Boyer, L,Gabert, J,Samuelian, JC(2010).Clinical variations modulate patterns of gene expression and define blood biomarkers in major depression.J Psychiatr Res,44,1205-1213.
  3. Benjamin, EJ,Blaha, MJ,Chiuve, SE,Cushman, M,Das, SR,Deo, R(2017).Heart disease and stroke statistics‑2017 update: A report from the American Heart Association.Circulation,135,e146-e603.
  4. Bhaskara, S,Chyla, BJ,Amann, JM,Knutson, SK,Cortez, D,Sun, ZW(2008).Deletion of histone deacetylase 3 reveals critical roles in S phase progression and DNA damage control.Mol Cell,30,61-72.
  5. Bottai, D,Spreafico, M,Pistocchi, A,Fazio, G,Adami, R,Grazioli, P(2019).Modeling cornelia de lange syndrome in vitro and in vivo reveals a role for cohesin complex in neuronal survival and differentiation.Hum Mol Genet,28,64-73.
  6. Broide, RS,Redwine, JM,Aftahi, N,Young, W,Bloom, FE,Winrow, CJ(2007).Distribution of histone deacetylases 1‑11 in the rat brain.J Mol Neurosci,31,47-58.
  7. Brookes, RL,Crichton, S,Wolfe, CD,Yi, Q,Li, L,Hankey, GJ(2018).Sodium valproate, a histone deacetylase inhibitor, is associated with reduced stroke risk after previous ischemic stroke or transient ischemic attack.Stroke,49,54-61.
  8. Brouns, R,De Deyn, PP(2009).The complexity of neurobiological processes in acute ischemic stroke.Clin Neurol Neurosurg,111,483-495.
  9. Cao, Q,Rong, S,Repa, JJ,St Clair, R,Parks, JS,Mishra, N(2014).Histone deacetylase 9 represses cholesterol efflux and alternatively activated macrophages in atherosclerosis development.Arterioscler Thromb Vasc Biol,34,1871-1879.
  10. Chang, S,McKinsey, TA,Zhang, CL,Richardson, JA,Hill, JA,Olson, EN(2004).Histone deacetylases 5 and 9 govern responsiveness of the heart to a subset of stress signals and play redundant roles in heart development.Mol Cell Biol,24,8467-8476.
  11. Chang, S,Young, BD,Li, S,Qi, X,Richardson, JA,Olson, EN(2006).Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10.Cell,126,321-334.
  12. Chen, YT,Zang, XF,Pan, J,Zhu, XL,Chen, F,Chen, ZB(2012).Expression patterns of histone deacetylases in experimental stroke and potential targets for neuroprotection.Clin Exp Pharmacol Physiol,39,751-758.
  13. Christopherson, KS,Ullian, EM,Stokes, CC,Mullowney, CE,Hell, JW,Agah, A(2005).Thrombospondins are astrocyte‑secreted proteins that promote CNS synaptogenesis.Cell,120,421-433.
  14. Cox, MN,Lehninger, AL(2015).Lehninger Principles of Biochemistry.San Francisco:W.H. Freeman.
  15. Dahiya, S,Wang, L,Beier, UH,Angelin, A,Han, R,Wallace, DC(2016).Deletion of a class IIb histone/protein deacetylase (HDAC), HDAC10, enhances FoxP3+T‑regulatory (Treg) cell suppressive function, gene expression and metabolism, and promotes allograft survival.J Immunol,196(Suppl 1),140.5.
  16. Dahiya, S,Wang, L,Beier, UH,Han, R,Hancock, WW(2018).HDAC10 Targeting regulates Foxp3 promoter, enhances t‑regulatory (treg) function and suppresses autoimmune colitis.J Immunol,2000(Suppl),54.11.
  17. de Ruijter, AJ,van Gennip, AH,Caron, HN,Kemp, S,van Kuilenburg, AB(2003).Histone deacetylases (HDACs): Characterization of the classical HDAC family.Biochem J,370,737-749.
  18. Demyanenko, S,Neginskaya, M,Berezhnaya, E(2018).Expression of class I histone deacetylases in ipsilateral and contralateral hemispheres after the focal photothrombotic infarction in the mouse brain.Transl Stroke Res,9,471-483.
  19. Dong, E,Chen, Y,Gavin, DP,Grayson, DR,Guidotti, A(2010).Valproate induces DNA demethylation in nuclear extracts from adult mouse brain.Epigenetics,5,730-735.
  20. Duan, B,Ye, D,Zhu, S,Jia, W,Lu, C,Wang, G(2017).HDAC10 promotes angiogenesis in endothelial cells through the PTPN22/ERK axis.Oncotarget,8,61338-61349.
  21. Endres, M,Engelhardt, B,Koistinaho, J,Lindvall, O,Meairs, S,Mohr, JP(2008).Improving outcome after stroke: Overcoming the translational roadblock.Cerebrovasc Dis,25,268-278.
  22. Endres, M,Fan, G,Meisel, A,Dirnagl, U,Jaenisch, R(2001).Effects of cerebral ischemia in mice lacking DNA methyltransferase 1 in post‑mitotic neurons.Neuroreport,12,3763-3766.
  23. Endres, M,Meisel, A,Biniszkiewicz, D,Namura, S,Prass, K,Ruscher, K(2000).DNA methyltransferase contributes to delayed ischemic brain injury.J Neurosci,20,3175-3181.
  24. Fan, J,Alsarraf, O,Dahrouj, M,Platt, KA,Chou, CJ,Rice, DS(2013).Inhibition of HDAC2 protects the retina from ischemic injury.Invest Ophthalmol Vis Sci,54,4072-4080.
  25. Faraco, G,Pancani, T,Formentini, L,Mascagni, P,Fossati, G,Leoni, F(2006).Pharmacological inhibition of histone deacetylases by suberoylanilide hydroxamic acid specifically alters gene expression and reduces ischemic injury in the mouse brain.Mol Pharmacol,70,1876-1884.
  26. Feng, L,Zhou, D,Zhang, Z,Liu, Y,Yang, Y(2014).Exome sequencing identifies a de novo mutation in HDAC8 associated with cornelia de lange syndrome.J Hum Genet,59,536-539.
  27. Fessler, EB,Chibane, FL,Wang, Z,Chuang, DM(2013).Potential roles of HDAC inhibitors in mitigating ischemia‑induced brain damage and facilitating endogenous regeneration and recovery.Curr Pharm Des,19,5105-5120.
  28. Fonseca, PA,Dos Santos, FC,Lam, S,Suárez‑Vega, A,Miglior, F,Schenkel, FS(2018).Genetic mechanisms underlying spermatic and testicular traits within and among cattle breeds: Systematic review and prioritization of GWAS results.J Anim Sci,96,4978-4999.
  29. Fukada, M,Hanai, A,Nakayama, A,Suzuki, T,Miyata, N,Rodriguiz, RM(2012).Loss of deacetylation activity of Hdac6 affects emotional behavior in mice.PLoS One,7,e30924.
  30. Fukada, M,Nakayama, A,Mamiya, T,Yao, TP,Kawaguchi, Y(2016).Dopaminergic abnormalities in Hdac6‑deficient mice.Neuropharmacology,110,470-479.
  31. Glozak, MA,Sengupta, N,Zhang, X,Seto, E(2005).Acetylation and deacetylation of non‑histone proteins.Gene,363,15-23.
  32. Haberland, M,Mokalled, MH,Montgomery, RL,Olson, EN(2009).Epigenetic control of skull morphogenesis by histone deacetylase 8.Genes Dev,23,1625-1630.
  33. Haberland, M,Montgomery, RL,Olson, EN(2009).The many roles of histone deacetylases in development and physiology: Implications for disease and therapy.Nat Rev Genet,10,32-42.
  34. He, M,Zhang, B,Wei, X,Wang, Z,Fan, B,Du, P(2013).HDAC4/5‑HMGB1 signalling mediated by NADPH oxidase activity contributes to cerebral ischaemia/reperfusion injury.J Cell Mol Med,17,531-542.
  35. Hu, CJ,Chen, SD,Yang, DI,Lin, TN,Chen, CM,Huang, TH(2006).Promoter region methylation and reduced expression of thrombospondin‑1 after oxygen‑glucose deprivation in murine cerebral endothelial cells.J Cereb Blood Flow Metab,26,1519-1526.
  36. Hwang, JY,Aromolaran, KA,Zukin, RS(2017).The emerging field of epigenetics in neurodegeneration and neuroprotection.Nat Rev Neurosci,18,347-361.
  37. International Stroke Genetics Consortium,Wellcome Trust Case Control Consortium 2,Bellenguez, C,Bevan, S,Gschwendtner, A,Spencer, CC(2012).Genome‑wide association study identifies a variant in HDAC9 associated with large vessel ischemic stroke.Nat Genet,44,328-333.
  38. Jaenisch, R,Bird, A(2003).Epigenetic regulation of gene expression: How the genome integrates intrinsic and environmental signals.Nat Genet,33(Suppl),245-254.
  39. Jhelum, P,Karisetty, BC,Kumar, A,Chakravarty, S(2017).Implications of epigenetic mechanisms and their targets in cerebral ischemia models.Curr Neuropharmacol,15,815-830.
  40. Jin, K,Mao, XO,Simon, RP,Greenberg, DA(2001).Cyclic AMP response element binding protein (CREB) and CREB binding protein (CBP) in global cerebral ischemia.J Mol Neurosci,16,49-56.
  41. Kaluza, D,Kroll, J,Gesierich, S,Yao, TP,Boon, RA,Hergenreider, E(2011).Class IIb HDAC6 regulates endothelial cell migration and angiogenesis by deacetylation of cortactin.EMBO J,30,4142-4156.
  42. Kassis, H,Shehadah, A,Chopp, M,Roberts, C,Zhang, ZG(2015).Stroke induces nuclear shuttling of histone deacetylase 4.Stroke,46,1909-1915.
  43. Kazantsev, AG,Thompson, LM(2008).Therapeutic application of histone deacetylase inhibitors for central nervous system disorders.Nat Rev Drug Discov,7,854-868.
  44. Kebir, O,Chaumette, B,Fatjó‑Vilas, M,Ambalavanan, A,Ramoz, N,Xiong, L(2014).Family‑based association study of common variants, rare mutation study and epistatic interaction detection in HDAC genes in schizophrenia.Schizophr Res,160,97-103.
  45. Kim, D,Frank, CL,Dobbin, MM,Tsunemoto, RK,Tu, W,Peng, PL(2008).Deregulation of HDAC1 by p25/Cdk5 in neurotoxicity.Neuron,60,803-817.
  46. Kim, JI,Jung, KJ,Jang, HS,Park, KM(2013).Gender‑specific role of HDAC11 in kidney ischemia – And reperfusion‑induced PAI‑1 expression and injury.Am J Physiol Renal Physiol,305,F61-F70.
  47. Kim, MH,Kim, SH,Kim, YK,Hong, SJ,Min, KU,Cho, SH(2013).A polymorphism in the histone deacetylase 1 gene is associated with the response to corticosteroids in asthmatics.Korean J Intern Med,28,708-714.
  48. Kim, T,Park, JK,Kim, HJ,Chung, JH,Kim, JW(2010).Association of histone deacetylase genes with schizophrenia in Korean population.Psychiatry Res,178,266-269.
  49. Kong, Q,Hao, Y,Li, X,Wang, X,Ji, B,Wu, Y(2018).HDAC4 in ischemic stroke: Mechanisms and therapeutic potential.Clin Epigenetics,10,117.
  50. Krupinski, J,Carrera, C,Muiño, E,Torres, N,Al‑Baradie, R,Cullell, N(2018).DNA methylation in stroke. Update of latest advances.Comput Struct Biotechnol J,16,1-5.
  51. Kwon, S,Zhang, Y,Matthias, P(2007).The deacetylase HDAC6 is a novel critical component of stress granules involved in the stress response.Genes Dev,21,3381-3394.
  52. Lagger, G,O’Carroll, D,Rembold, M,Khier, H,Tischler, J,Weitzer, G(2002).Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression.EMBO J,21,2672-2681.
  53. Lang, B,Alrahbeni, TM,Clair, DS,Blackwood, DH,International Schizophrenia Consortium,McCaig, CD(2012).HDAC9 is implicated in schizophrenia and expressed specifically in post‑mitotic neurons but not in adult neural stem cells.Am J Stem Cells,1,31-41.
  54. Lee, HA,Hong, SH,Kim, JW,Jang, IS(2010).Possible involvement of DNA methylation in NKCC1 gene expression during postnatal development and in response to ischemia.J Neurochem,114,520-529.
  55. Legube, G,Trouche, D(2003).Regulating histone acetyltransferases and deacetylases.EMBO Rep,4,944-947.
  56. Li, N,Yuan, Q,Cao, XL,Zhang, Y,Min, ZL,Xu, SQ(2017).Opposite effects of HDAC5 and p300 on MRTF‑A‑related neuronal apoptosis during ischemia/reperfusion injury in rats.Cell Death Dis,8,e2624.
  57. Li, Y,Zhou, Y,Zhu, L,Liu, G,Wang, X,Wang, X(2018).Genome‑wide analysis reveals that altered methylation in specific CpG loci is associated with childhood obesity.J Cell Biochem,119,7490-7497.
  58. Liesz, A,Zhou, W,Na, SY,Hämmerling, GJ,Garbi, N,Karcher, S(2013).Boosting regulatory T cells limits neuroinflammation in permanent cortical stroke.J Neurosci,33,17350-17362.
  59. Lin, TN,Kim, GM,Chen, JJ,Cheung, WM,He, YY,Hsu, CY(2003).Differential regulation of thrombospondin‑1 and thrombospondin‑2 after focal cerebral ischemia/reperfusion.Stroke,34,177-186.
  60. Lin, YH,Dong, J,Tang, Y,Ni, HY,Zhang, Y,Su, P(2017).Opening a new time window for treatment of stroke by targeting HDAC2.J Neurosci,37,6712-6728.
  61. Liu, H,Hu, Q,Kaufman, A,D’Ercole, AJ,Ye, P(2008).Developmental expression of histone deacetylase 11 in the murine brain.J Neurosci Res,86,537-543.
  62. Liu, J,Zhou, X,Li, Q,Zhou, SM,Hu, B,Hu, GW(2017).Role of phosphorylated HDAC4 in stroke‑induced angiogenesis.Biomed Res Int,2017,2957538.
  63. Liu, X,Yamashita, T,Shang, J,Shi, X,Morihara, R,Huang, Y(2018).Molecular switching from ubiquitin‑proteasome to autophagy pathways in mice stroke model.J Cereb Blood Flow Metab,2018,271678X18810617.
  64. Lloyd‑Jones, D,Adams, RJ,Brown, TM,Carnethon, M,Dai, S,De Simone, G(2010).Executive summary: Heart disease and stroke statistics‑2010 update: A report from the American Heart Association.Circulation,121,948-954.
  65. Lu, S,Li, H,Li, K,Fan, XD(2018).HDAC9 promotes brain ischemic injury by provoking iκBα/NF‑κB and MAPKs signaling pathways.Biochem Biophys Res Commun,503,1322-1329.
  66. Lucio‑Eterovic, AK,Cortez, MA,Valera, ET,Motta, FJ,Queiroz, RG,Machado, HR(2008).Differential expression of 12 histone deacetylase (HDAC) genes in astrocytomas and normal brain tissue: Class II and IV are hypoexpressed in glioblastomas.BMC Cancer,8,243.
  67. Matsushima, S,Sadoshima, J(2015).The role of sirtuins in cardiac disease.Am J Physiol Heart Circ Physiol,309,H1375-H1389.
  68. Mehta, SL,Manhas, N,Raghubir, R(2007).Molecular targets in cerebral ischemia for developing novel therapeutics.Brain Res Rev,54,34-66.
  69. Mews, P,Donahue, G,Drake, AM,Luczak, V,Abel, T,Berger, SL(2017).Acetyl‑coA synthetase regulates histone acetylation and hippocampal memory.Nature,546,381-386.
  70. Mihaylova, MM,Shaw, RJ(2013).Metabolic reprogramming by class I and II histone deacetylases.Trends Endocrinol Metab,24,48-57.
  71. Montgomery, RL,Davis, CA,Potthoff, MJ,Haberland, M,Fielitz, J,Qi, X(2007).Histone deacetylases 1 and 2 redundantly regulate cardiac morphogenesis, growth, and contractility.Genes Dev,21,1790-1802.
  72. Moskowitz, MA,Lo, EH,Iadecola, C(2010).The science of stroke: Mechanisms in search of treatments.Neuron,67,181-198.
  73. O’Collins, VE,Macleod, MR,Donnan, GA,Horky, LL,van der Worp, BH,Howells, DW(2006).1,026 experimental treatments in acute stroke.Ann Neurol,20(59),467-477.
  74. Pan, Y,Yang, J,Wei, Y,Wang, H,Jiao, R,Moraga, A(2018).Histone deacetylase 7‑derived peptides play a vital role in vascular repair and regeneration.Adv Sci,5,1800006.
  75. Park, BL,Kim, YJ,Cheong, HS,Lee, SO,Han, CS,Yoon, JH(2007).HDAC10 promoter polymorphism associated with development of HCC among chronic HBV patients.Biochem Biophys Res Commun,363,776-781.
  76. Rajabi, N,Galleano, I,Madsen, AS,Olsen, CA(2018).Targeting sirtuins: Substrate specificity and inhibitor design.Prog Mol Biol Transl Sci,154,25-69.
  77. Raz, L,Zhang, QG,Han, D,Dong, Y,De Sevilla, L,Brann, DW(2011).Acetylation of the pro‑apoptotic factor, p53 in the hippocampus following cerebral ischemia and modulation by estrogen.PLoS One,6,e27039.
  78. Ree, R,Varland, S,ArnesenT(2018).Spotlight on protein N‑terminal acetylation.Exp Mol Med,50,90.
  79. Rivadeneira, F,Styrkársdottir, U,Estrada, K,Halldórsson, BV,Hsu, YH,Richards, JB(2009).Twenty bone‑mineral‑density loci identified by large‑scale meta‑analysis of genome‑wide association studies.Nat Genet,41,1199-1206.
  80. Sadakierska‑Chudy, A,Kostrzewa, RM,Filip, M(2015).A comprehensive view of the epigenetic landscape part I: DNA methylation, passive and active DNA demethylation pathways and histone variants.Neurotox Res,27,84-97.
  81. Sadoul, K,Boyault, C,Pabion, M,Khochbin, S.(2008).Regulation of protein turnover by acetyltransferases and deacetylases.Biochimie,12,306-312.
  82. Sahakian, E,Powers, JJ,Chen, J,Deng, SL,Cheng, F,Distler, A(2015).Histone deacetylase 11: A novel epigenetic regulator of myeloid derived suppressor cell expansion and function.Mol Immunol,63,579-585.
  83. Schweizer, S,Meisel, A,Märschenz, S(2013).Epigenetic mechanisms in cerebral ischemia.J Cereb Blood Flow Metab,33,1335-1346.
  84. Seto, E,Yoshida, M(2014).Erasers of histone acetylation: The histone deacetylase enzymes.Cold Spring Harb Perspect Biol,6,a018713.
  85. Shaffer, JR,Orlova, E,Lee, MK,Leslie, EJ,Raffensperger, ZD,Heike, CL(2016).Genome‑wide association study reveals multiple loci influencing normal human facial morphology.PLoS Genet,12,e1006149.
  86. Shakespear, MR,Hohenhaus, DM,Kelly, GM,Kamal, NA,Gupta, P,Labzin, LI(2013).Histone deacetylase 7 promotes toll‑like receptor 4‑dependent proinflammatory gene expression in macrophages.J Biol Chem,288,25362-25374.
  87. Sheikh, BN.(2014).Crafting the brain – Role of histone acetyltransferases in neural development and disease.Cell Tissue Res,356,553-573.
  88. Shi, W,Wei, X,Wang, Z,Han, H,Fu, Y,Liu, J(2016).HDAC9 exacerbates endothelial injury in cerebral ischaemia/reperfusion injury.J Cell Mol Med,20,1139-1149.
  89. Sleiman, SF,Olson, DE,Bourassa, MW,Karuppagounder, SS,Zhang, YL,Gale, J(2014).Hydroxamic acid‑based histone deacetylase (HDAC) inhibitors can mediate neuroprotection independent of HDAC inhibition.J Neurosci,34,14328-14337.
  90. Soriano‑Tárraga, C,Jiménez‑Conde, J,Giralt‑Steinhauer, E,Mola, M,Ois, A,Rodríguez‑Campello, A(2014).Global DNA methylation of ischemic stroke subtypes.PLoS One,9,e96543.
  91. Starheim, KK,Gevaert, K,Arnesen, T(2012).Protein N‑terminal acetyltransferases: When the start matters.Trends Biochem Sci,37,152-161.
  92. Symmank, J,Zimmer, G(2017).Regulation of neuronal survival by DNA methyltransferases.Neural Regen Res,12,1768-1775.
  93. Thiagarajan, D,Vedantham, S,Ananthakrishnan, R,Schmidt, AM,Ramasamy, R(2016).Mechanisms of transcription factor acetylation and consequences in hearts.Biochim Biophys Acta,1862,2221-2231.
  94. Thomas, EA,D’Mello, SR(2018).Complex neuroprotective and neurotoxic effects of histone deacetylases.J Neurochem,145,96-110.
  95. Traylor, M,Farrall, M,Holliday, EG,Sudlow, C,Hopewell, JC,Cheng, YC(2012).Genetic risk factors for ischaemic stroke and its subtypes (the METASTROKE collaboration): A meta‑analysis of genome‑wide association studies.Lancet Neurol,11,951-962.
  96. Tsai, HD,Wu, JS,Kao, MH,Chen, JJ,Sun, GY,Ong, WY(2016).Clinacanthus nutans protects cortical neurons against hypoxia‑induced toxicity by downregulating HDAC1/6.Neuromolecular Med,18,274-282.
  97. Vega, RB,Matsuda, K,Oh, J,Barbosa, AC,Yang, X,Meadows, E(2004).Histone deacetylase 4 controls chondrocyte hypertrophy during skeletogenesis.Cell,119,555-566.
  98. Wang, DB,Kinoshita, C,Kinoshita, Y,Sopher, BL,Uo, T,Lee, RJ(2019).Neuronal susceptibility to beta‑amyloid toxicity and ischemic injury involves histone deacetylase‑2 regulation of endophilin‑B1.Brain Pathol,29,164-175.
  99. Wang, J,Hodes, GE,Zhang, H,Zhang, S,Zhao, W,Golden, SA(2018).Epigenetic modulation of inflammation and synaptic plasticity promotes resilience against stress in mice.Nat Commun,9,477.
  100. Wang, J,Zhao, H,Fan, Z,Li, G,Ma, Q,Tao, Z(2017).Long noncoding RNA H19 promotes neuroinflammation in ischemic stroke by driving histone deacetylase 1‑dependent M1 microglial polarization.Stroke,48,2211-2221.
  101. Wang, J,Zibetti, C,Shang, P,Sripathi, SR,Zhang, P,Cano, M(2018).ATAC‑seq analysis reveals a widespread decrease of chromatin accessibility in age‑related macular degeneration.Nat Commun,9,1364.
  102. Wang, Z,Leng, Y,Wang, J,Liao, HM,Bergman, J,Leeds, P(2016).Tubastatin A, an HDAC6 inhibitor, alleviates stroke‑induced brain infarction and functional deficits: Potential roles of α‑tubulin acetylation and FGF‑21 up‑regulation.Sci Rep,6,19626.
  103. Watson, LA,Tsai, LH(2017).Molecular biology: Local metabolites linked to memory.Nature,546,361-362.
  104. Xiang, B,Liu, K,Yu, M,Liang, X,Zhang, J,Lei, W(2018).Systematic genetic analyses of genome‑wide association study data reveal an association between the key nucleosome remodeling and deacetylase complex and bipolar disorder development.Bipolar Disord,20,370-380.
  105. Xiong, XY,Liu, L,Yang, QW(2018).Refocusing neuroprotection in cerebral reperfusion era: New challenges and strategies.Front Neurol,9,249.
  106. Yang, X,Wu, Q,Zhang, L,Feng, L(2016).Inhibition of histone deacetylase 3 (HDAC3) mediates ischemic preconditioning and protects cortical neurons against ischemia in rats.Front Mol Neurosci,9,131.
  107. Yang, Z,Zhou, L,Wu, LM,Xie, HY,Zhang, F,Zheng, SS(2010).Combination of polymorphisms within the HDAC1 and HDAC3 gene predict tumor recurrence in hepatocellular carcinoma patients that have undergone transplant therapy.Clin Chem Lab Med,48,1785-1791.
  108. Yuan, H,Denton, K,Liu, L,Li, XJ,Benashski, S,McCullough, L(2016).Nuclear translocation of histone deacetylase 4 induces neuronal death in stroke.Neurobiol Dis,91,182-193.
  109. Zeng, Z,Liao, R,Yao, Z,Zhou, W,Ye, P,Zheng, X(2014).Three single nucleotide variants of the HDAC gene are associated with type 2 diabetes mellitus in a Chinese population: A community‑based case‑control study.Gene,533,427-433.
  110. Zhang, CC,Lu, F,Liang, JQ,Zhou, YF(2018).Research progress of histone deacetylase 6 inhibitors in the therapy of ischemic stroke.Sheng Li Xue Bao,70,301-309.
  111. Zhang, CL,McKinsey, TA,Chang, S,Antos, CL,Hill, JA,Olson, EN(2002).Class II histone deacetylases act as signal‑responsive repressors of cardiac hypertrophy.Cell,110,479-488.
  112. Zhang, L,Zhang, ZG,Chopp, M.(2012).The neurovascular unit and combination treatment strategies for stroke.Trends Pharmacol Sci,33,415-422.
  113. Zhang, QY,Wang, ZJ,Sun, DM,Wang, Y,Xu, P,Wu, WJ(2017).Novel therapeutic effects of leonurine on ischemic stroke: New mechanisms of BBB integrity.Oxid Med Cell Longev,2017,7150376.
  114. Zhang, Y,Kwon, S,Yamaguchi, T,Cubizolles, F,Rousseaux, S,Kneissel, M(2008).Mice lacking histone deacetylase 6 have hyperacetylated tubulin but are viable and develop normally.Mol Cell Biol,28,1688-1701.
  115. Zhao, BQ,Wang, S,Kim, HY,Storrie, H,Rosen, BR,Mooney, DJ(2006).Role of matrix metalloproteinases in delayed cortical responses after stroke.Nat Med,12,441-445.
  116. Ziemka‑Nalecz, M,Zalewska, T(2014).Neuroprotective effects of histone deacetylase inhibitors in brain ischemia.Acta Neurobiol Exp,74,383-395.
print cancel