Neuroprotective effects of histone deacetylase inhibitors in brain ischemia

• Autorzy: Ziemka-Nalecz M. , Zalewska T.
• Języki publikacji: EN

Abstrakty

EN

Stroke resulting from cerebral ischemia or haemorrhage is a common cause of the death of neuronal cells and neurological dysfunction in humans. Finding therapeutics to improve outcome from brain ischemic injury has proved to be challenging. The efficacy of neuroprotective compounds identified in experimental brain ischemia models thus far have failed to successfully translate in clinical human trials. Recent experimental evidence indicates that inhibition of zinc-dependent histone deacetylases can protect neuronal and oligodendroglial cells from the damaging effects of ischemic insult, which may contribute to improved functional outcome. In this review we briefly highlight the current data supporting a beneficial role of histone deacetylation in experimental brain ischemia. We also discuss the molecular mechanism of neuroprotection.

• Wydawca: -
• Czasopismo: Acta Neurobiologiae Experimentalis
• Rocznik: 2014
• Tom: 74
• Numer: 4
• Opis fizyczny: p.383-395,fig.,ref.

Twórcy

autor

Ziemka-Nalecz M.

• NeuroRepair Department, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

autor

Zalewska T.

• NeuroRepair Department, Mossakowski Medical Research Centre, Polish Academy of Sciences, Warsaw, Poland

Bibliografia

• Akhtar MW, Raingo J, Nelson ED, Montgomery RL, Olson EN, Kavalali ET, Monteggia LM (2009) Histone deacety- lases 1 and 2 form a developmental switch that controls excitatory synapse maturation and function. J Neurosci 29: 8288-8297.
• Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8: 963-970.
• Baltan S, Bachleda A, Morrison RS, Murphy SP (2011a) Expression of histone deacetylases in cellular compart¬ments of the mouse brain and the effects of ischemia. Transl Stroke Res 2: 411-423.
• Baltan S, Murphy SP, Danilov CA, Bachleda A, Morrison RS (2011b) Histone deacetylase inhibitors preserve white matter structure and function during ischemia by conserv¬ing ATP and reducing excitotoxicity. J Neurosci 31: 3990-3999.
• Baltan S, Morrison RS, Murphy SP (2013) Novel protective effects of histone deacetylase inhibition on stroke and white matter ischemic injury. Neurotherapeutics 10: 798-807.
• Baur JA, Ungvari Z, Minor RK, Le Couteur DG, de Cabo R (2012) Are sirtuins viable targets for improving health- span and lifespan? Nat Rev Drug Discov 11: 443-461.
• Bieliauskas AV, Pflum MK (2008) Isoform-selective histone deacetylase inhibitors. Chem Soc Rev 37: 1402-1413.
• Bolger TA, Yao TP (2005) Intracellular trafficking of histone deacetylase 4 regulates neuronal cell death. J Neurosci 25: 9544-9553.
• Boutillier AL, Trinh E, Loeffler JP (2002) Constitutive repression of E2F1 transcriptional activity through HDAC proteins is essential for neuronal survival. Ann N Y Acad Sci 973: 438-442.
• Brochier C, Dennis G, Rivieccio MA, McLaughlin K, Coppola G, Ratan RR, Langley B (2013) Specific acety¬lation of p53 by HDAC inhibition prevents DNA damage- induced apoptosis in neurons. J Neurosci 33: 8621¬8632.
• Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Sauerbeck L, Spilker J, Duldner J, Khoury J (1997) Early hemorrhage growth in patients with intracerebral hemor¬rhage. Stroke 28: 1-5.
• Brunmeir R, Lagger S, Seiser C (2009) Histone deacetylase HDAC1/HDAC2-controlled embryonic development and cell differentiation. Int J Dev Biol 53: 275-289.
• Chen PS, Peng GS, Li G, Yang S, Wu X, Wang CC, Wilson B, Lu RB, Gean PW, Chuang DM, Hong JS (2006) Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neu- rotrophic factors from astrocytes. Mol Psychiatry 11: 1116-1125.
• Cheng Y, Gidday JM, Yan Q, Shah AR, Holtzman DM (1997) Marked age-dependent neuroprotection by brain- derived neurotrophic factor against neonatal hypoxic- ischemic brain injury. Ann Neurol 41: 521-529.
• Chiaramello S, Dalmasso G, Bezin L, Marcel D, Jourdan F, Peretto P, Fasolo A, De Marchis S (2007) BDNF/ TrkB interaction regulates migration of SVZ precursor cells via PI3-K and MAP-K signalling pathways. Eur J Neurosci 26: 1780-1790.
• Chiu SP, Wu MJ, Chen PY, Ho YR, Tai MH, Ho CT, Yen JH (2013) Neurotrophic action of 5-hydroxylated polymethoxyflavones: 5-demethylnobiletin and gardenin A stimulate neuritogenesis in PC12 cells. J Agric Food Chem 61: 9453-9463.
• Chuang DM, Leng Y, Marinova Z, Kim HJ, Chiu CT (2009) Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 32: 591-601.
• Covington EC (1998) Anticonvulsants for neuropathic pain and detoxification. Cleve Clin J Med 65 Suppl 1: SI21-9; discussion SI45-7.
• Dallavalle S, Pisano C, Zunino F (2012) Development and therapeutic impact of HDAC6-selective inhibitors. Biochem Pharmacol 84: 756-765.
• Di Daniel E, Mudge AW, Maycox PR (2005) Comparative analysis of the effects of four mood stabilizers in SH-SY5Y cells and in primary neurons. Bipolar Disord 7: 33-41.
• Drummond DC, Noble CO, Kirpotin DB, Guo Z, Scott GK, Benz CC (2005) Clinical development of histone deacety- lase inhibitors as anticancer agents. Annu Rev Pharmacol Toxicol 45: 495-528.
• Du G, Jiao R (2011) To prevent neurodegeneration: HDAC6 uses different strategies for different challenges. Commun Integr Biol 4: 139-142.
• Duvic M, Vu J (2007) Update on the treatment of cutaneous T-cell lymphoma (CTCL): Focus on vorinostat. Biologics 1: 377-392.
• Emrich HM, von Zerssen D, Kissling W, Möller HJ, Windorfer A (1980) Effect of sodium valproate on mania. The GABA-hypothesis of affective disorders. Arch Psychiatr Nervenkr 229: 1-16.
• Faraco G, Pancani T, Formentini L, Mascagni P, Fossati G, Leoni F, Moroni F, Chiarugi A (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.
• Ferrante RJ, Kubilus JK, Lee J, Ryu H, Beesen A, Zucker B, Smith K, Kowall NW, Ratan RR, Luthi-Carter R, Hersch SM (2003) Histone deacetylase inhibition by sodium butyrate chemotherapy ameliorates the neurodegenera¬tive phenotype in Huntington's disease mice. J Neurosci 23: 9418-9427.
• Fischer A, Sananbenesi F, Wang X, Dobbin M, Tsai LH (2007) Recovery of learning and memory is associated with chromatin remodelling. Nature 447: 178-182.
• Fleiss B, Nilsson MK, Blomgren K, Mallard C (2012) Neuroprotection by the histone deacetylase inhibitor trichostatin A in a model of lipopolysaccharide-sensitised neonatal hypoxic-ischaemic brain injury. J Neuroinflammation 9: 70.
• Foti SB, Chou A, Moll AD, Roskams AJ (2013) HDAC inhibitors dysregulate neural stem cell activity in the postnatal mouse brain. Int J Dev Neurosci 31: 434-447.
• Fukumoto T, Morinobu S, Okamoto Y, Kagaya A, Yamawaki S (2001) Chronic lithium treatment increases the expres¬sion of brain-derived neurotrophic factor in the rat brain. Psychopharmacology (Berl) 158: 100-106.
• George S, Kadam SD, Irving ND, Markowitz GJ, Raja S, Kwan A, Tu Y, Chen H, Rohde C, Smith DR, Comi AM (2013) Impact of trichostatin A and sodium valproate treatment on post-stroke neurogenesis and behavioral outcomes in immature mice. Front Cell Neurosci 7: 123.
• Glozak MA, Sengupta N, Zhang X, Seto E (2005) Acetylation and deacetylation of non-histone proteins. Gene 363: 15-23.
• Göttlicher M, Minucci S, Zhu P, Krämer OH, Schimpf A, Giavara S, Sleeman JP, Lo Coco F, Nervi C, Pelicci PG, Heinzel T (2001) Valproic acid defines a novel class of HDAC inhibitors inducing differentiation of transformed cells. EMBO J 20: 6969-6978.
• Gräff J, Rei D, Guan JS, Wang WY, Seo J, Hennig KM, Nieland TJ, Fass DM, Kao PF, Kahn M, Su SC, Samiei A, Joseph N, Haggarty SJ, Delalle I, Tsai LH (2012) An epigenetic blockade of cognitive functions in the neuro¬degenerating brain. Nature 483: 222-226.
• Graham B, Gibson SB (2005) The two faces of NFkappaB in cell survival responses. Cell Cycle 4: 1342-1345.
• Gurvich N, Klein PS (2002) Lithium and valproic acid: par¬allels and contrasts in diverse signaling contexts. Pharmacol Ther 96: 45-66.
• Gurvich N, Tsygankova OM, Meinkoth JL, Klein PS (2004) Histone deacetylase is a target of valproic acid-mediated cellular differentiation. Cancer Res 64: 1079-1086.
• Haberland M, Montgomery RL, Olson EN (2009) The many roles of histone deacetylases in development and physiol¬ogy: implications for disease and therapy. Nat Rev Genet 10: 32-42.
• Halili MA, Andrews MR, Sweet MJ, Fairlie DP (2009) Histone deacetylase inhibitors in inflammatory disease. Curr Top Med Chem 9: 309-319.
• Hao Y, Creson T, Zhang L, Li P, Du F, Yuan P, Gould TD, Manji HK, Chen G (2004) Mood stabilizer valproate pro¬motes ERK pathway-dependent cortical neuronal growth and neurogenesis. J Neurosci 24: 6590-6599.
• Hasan MR, Kim JH, Kim YJ, Kwon KJ, Shin CY, Kim HY, Han SH, Choi DH, Lee J (2013) Effect of HDAC inhibi¬tors on neuroprotection and neurite outgrowth in primary rat cortical neurons following ischemic insult. Neurochem Res 38: 1921-1934.
• Hashimoto R, Hough C, Nakazawa T, Yamamoto T, Chuang DM (2002) Lithium protection against glutamate excito- toxicity in rat cerebral cortical neurons: involvement of NMDA receptor inhibition possibly by decreasing NR2B tyrosine phosphorylation. J Neurochem 80: 589-597.
• Hildmann C, Riester D, Schwienhorst A (2007) Histone deacetylases - an important class of cellular regulators with a variety of functions. Appl Microbiol Biotechnol 75: 487-497.
• Hockly E, Richon VM, Woodman B, Smith DL, Zhou X, Rosa E, Sathasivam K, Ghazi-Noori S, Mahal A, Lowden PA, Steffan JS, Marsh JL, Thompson LM, Lewis CM, Marks PA, Bates GP (2003) Suberoylanilide hydroxamic acid, a histone deacetylase inhibitor, ameliorates motor deficits in a mouse model of Huntington's disease. Proc Natl Acad Sci U S A 100: 2041-2046.
• Hoehn B, Ringer TM, Xu L, Giffard RG, Sapolsky RM, Steinberg GK, Yenari MA (2001) Overexpression of HSP72 after induction of experimental stroke protects neurons from ischemic damage. J Cereb Blood Flow Metab 21: 1303-1309.
• Houtkooper RH, Pirinen E, Auwerx J (2012) Sirtuins as regulators of metabolism and healthspan. Nat Rev Mol Cell Biol 13: 225-238.
• Hsieh J, Nakashima K, Kuwabara T, Mejia E, Gage FH (2004) Histone deacetylase inhibition-mediated neuronal differentiation of multipotent adult neural progenitor cells. Proc Natl Acad Sci U S A 101: 16659-16664.
• Jacob C, Christen CN, Pereira JA, Somandin C, Baggiolini A, Lötscher P, Ozgelik M, Tricaud N, Meijer D, Yamaguchi
• T, Matthias P, Suter U (2011) HDAC1 and HDAC2 con¬trol the transcriptional program of myelination and the survival of Schwann cells. Nat Neurosci 14: 429-436.
• Jawerka M, Colak D, Dimou L, Spiller C, Lagger S, Montgomery RL, Olson EN, Wurst W, Göttlicher M, Götz M (2010) The specific role of histone deacetylase 2 in adult neurogenesis. Neuron Glia Biol 6: 93-107.
• Jeong MR, Hashimoto R, Senatorov VV, Fujimaki K, Ren M, Lee MS, Chuang DM (2003) Valproic acid, a mood stabilizer and anticonvulsant, protects rat cerebral cortical neurons from spontaneous cell death: a role of histone deacetylase inhibition. FEBS Lett 542: 74-78.
• Jin K, Minami M, Lan JQ, Mao XO, Batteur S, Simon RP, Greenberg DA (2001) Neurogenesis in the dentate sub- granular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci U S A 98: 4710-4715.
• Kabakus N, Ay I, Aysun S, Söylemezoglu F, Ozcan A, Celasun B (2005) Protective effects of valproic acid against hypoxic-ischemic brain injury in neonatal rats. J Child Neurol 20: 582-587.
• Kahle MP, Bix GJ (2013) Neuronal restoration following ischemic stroke: influences, barriers, and therapeutic potential. Neurorehabil Neural Repair 27: 469-478.
• Kazantsev AG, Thompson LM (2008) Therapeutic applica¬tion of histone deacetylase inhibitors for central nervous system disorders. Nat Rev Drug Discov 7: 854-868.
• Khan N, Jeffers M, Kumar S, Hackett C, Boldog F, Khramtsov N, Qian X, Mills E, Berghs SC, Carey N, Finn PW, Collins LS, Tumber A, Ritchie JW, Jensen PB, Lichenstein HS, Sehested M (2008) Determination of the class and isoform selectivity of small-molecule histone deacetylase inhibitors. Biochem J 409: 581¬589.
• Khochbin S, Verdel A, Lemercier C, Seigneurin-Berny D (2001) Functional significance of histone deacetylase diversity. Curr Opin Genet Dev 11: 162-166.
• Kim HJ, Chuang DM (2014) HDAC inhibitors mitigate ischemia-induced oligodendrocyte damage: potential roles of oligodendrogenesis, VEGF, and anti-inflamma¬tion. Am J Transl Res 6: 206-223.
• Kim HJ, Rowe M, Ren M, Hong JS, Chen PS, Chuang DM (2007) Histone deacetylase inhibitors exhibit anti-inflam¬matory and neuroprotective effects in a rat permanent ischemic model of stroke: multiple mechanisms of action. J Pharmacol Exp Ther 321: 892-901.
• Kim HJ, Leeds P, Chuang DM (2009) The HDAC inhibitor, sodium butyrate, stimulates neurogenesis in the ischemic brain. J Neurochem 110: 1226-1240.Kozikowski AP, Chen Y, Gaysin A, Chen B, D'Annibale MA, Suto CM, Langley BC (2007) Functional differences in epigenetic modulators-superiority of mercaptoacet- amide-based histone deacetylase inhibitors relative to hydroxamates in cortical neuron neuroprotection studies. J Med Chem 50: 3054-3061.
• Kristensen LS, Nielsen HM, Hansen LL (2009) Epigenetics and cancer treatment. Eur J Pharmacol 625: 131-142.
• Langley B, Gensert JM, Beal MF, Ratan RR (2005) Remodeling chromatin and stress resistance in the central nervous system: histone deacetylase inhibitors as novel and broadly effective neuroprotective agents. Curr Drug Targets CNS Neurol Disord 4: 41-50.
• Langley B, D'Annibale MA, Suh K, Ayoub I, Tolhurst A, Bastan B, Yang L, Ko B, Fisher M, Cho S, Beal MF, Ratan RR (2008) Pulse inhibition of histone deacetylases induces complete resistance to oxidative death in cortical neurons without toxicity and reveals a role for cytoplas- mic p21(waf1/cip1) in cell cycle-independent neuropro¬tection. J Neurosci 28: 163-176.
• Langley B, Brochier C, Rivieccio MA (2009) Targeting his- tone deacetylases as a multifaceted approach to treat the diverse outcomes of stroke. Stroke 40: 2899-2905.
• Lawless MW, Norris S, O'Byrne KJ, Gray SG (2009) Targeting histone deacetylases for the treatment of dis¬ease. J Cell Mol Med 13: 826-852.
• Liesz A, Zhou W, Na S-Y, Hammerling GJ, Garbi N, Karcher S, Mracsko E, Backs J, Rivest S, Veltkamp R (2013) Boosting Regulatory T Cells Limits Neuroinflammation in Permanent Cortical Stroke. J Neurosci 33: 17350-17362.
• Liu H, Wu H, Wang Y, Wang Y, Wu X, Ju S, Wang X (2012a) Inhibition of class II histone deacetylase blocks prolifera¬tion and promotes neuronal differentiation of the embry¬onic rat neural progenitor cells. Acta Neurobiol Exp (Wars) 72: 365-376.
• Liu XS, Chopp M, Kassis H, Jia LF, Hozeska-Solgot A, Zhang RL, Chen C, Cui YS, Zhang ZG (2012b) Valproic acid increases white matter repair and neurogenesis after stroke. Neuroscience 220: 313-321.
• Lyssiotis CA, Walker J, Wu C, Kondo T, Schultz PG, Wu X (2007) Inhibition of histone deacetylase activity induces developmental plasticity in oligodendrocyte precursor cells. Proc Natl Acad Sci U S A 104: 14982-14987.
• Marks PA, Breslow R (2007) Dimethyl sulfoxide to vorinos- tat: development of this histone deacetylase inhibitor as an anticancer drug. Nat Biotechnol 25: 84-90.
• Martin-Montalvo A, Villalba JM, Navas P, de Cabo R (2011) NRF2, cancer and calorie restriction. Oncogene 30: 505-520.
• Miller TA, Witter DJ, Belvedere S (2003). Histone deacety¬lase inhibitors. J Med Chem 46: 5097-5116.
• Minucci S, Pelicci PG (2006) Histone deacetylase inhibitors and the promise of epigenetic (and more) treatments for cancer. Nat Rev Cancer 6: 38-51.
• Morrison RS, Kinoshita Y, Johnson MD, Guo W, Garden GA (2003) p53-dependent cell death signaling in neurons. Neurochem Res 28: 15-27.
• Moxon-Emre I, Schlichter LC (2010) Evolution of inflam¬mation and white matter injury in a model of transient focal ischemia.J Neuropathol Exp Neurol 69: 1-15.
• Murphy SP, Lee RJ, McClean ME, Pemberton HE, Uo T, Morrison RS, Bastian C, Baltan S (2014) MS-275, a Class I histone deacetylase inhibitor, protects the p-53- deficient mouse against ischemic injury. J Neurochem 129: 509-515.
• Nau H, Hauck RS, Ehlers K (1991) Valproic acid-induced neural tube defects in mouse and human: aspects of chi- rality, alternative drug development, pharmacokinetics and possible mechanisms. Pharmacol Toxicol 69: 310¬321.
• Ocker M (2010) Deacetylase inhibitors - focus on non-his- tone targets and effects. World J Biol Chem 1: 55-61.
• Pandey P, Saleh A, Nakazawa A Kumar S, Srinivasula SM, Kumar V, Weichselbaum R, Nalin C, Alnemri ES, Kufe D, Kharbanda S (2000) Negative regulation of cyto- chrome c-mediated oligomerization of Apaf-1 and activa¬tion of procaspase-9 by heat shock protein 90. EMBO J 19: 4310-4322.
• Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM (2002) Rat forebrain neurogenesis and striatal neuronal replacement after focal stroke. Ann Neurol 52: 802-813.
• Phiel CJ, Zhang F, Huang EY, Guenther MG, Lazar MA, Klein PS (2001) Histone deacetylase is a direct target of valproic acid, a potent anticonvulsant, mood stabilizer, and teratogen. J Biol Chem 276: 36734-36741.
• Rajdev S, Hara K, Kokubo Y, Mestril R, Dillmann W, Weinstein PR, Sharp FR (2000) Mice overexpressing rat heat shock protein 70 are protected against cerebral infarction. Ann Neurol 47: 782-791.
• Ravagnan L, Gurbuxani S, Susin SA, Maisse C, Daugas E, Zamzami N, Mak T, Jäättelä M, Penninger JM, Garrido C, Kroemer G (2001) Heat-shock protein 70 antagonizes apoptosis-inducing factor. Nat Cell Biol 3: 839-843.
• Reckling JC (2003) Neuroprotective effects of anticonvul¬sants in rat hippocampal slice culture exposed to oxygen/ glucose deprivation. Neurosci Lett 335: 167-170.