The Role of Post-Translational Protein Acetylation and Deacetylation in the Apoptosis of Neurons of the Peripheral Nervous System

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Abstract

Neurotrauma is among the main causes of human disability and mortality. However, the mechanisms that mediate the survival and death of cells in the peripheral nervous system are still not fully understood. The transcription factors p53 and E2F1 are the master regulators of basic cellular functions, including DNA repair, cell cycle, metabolism, and apoptosis. Overexpression of p53 and E2F1, shown in a number of experimental models of peripheral nerve injury, suggests an important role of these proteins in the pathogenesis of neurotrauma. This review discusses the epigenetic mechanisms of p53 and E2F1 activation and regulation, which may contribute to the survival or death of neurons and glial cells after traumatic injury. Prospects for further studies of the mechanisms of regulation of the p53 and E2F1 proteins, including those involving histone deacetylases, for the development of neuroprotectors are considered.

About the authors

V. A. Dzreyan

Laboratory of Molecular Neurobiology, Academy of Biology and Biotechnology, Southern Federal University

Author for correspondence.
Email: dzreyan2016@mail.ru
Russia, 344090, Rostov-on-Don

S. V. Demyanenko

Laboratory of Molecular Neurobiology, Academy of Biology and Biotechnology, Southern Federal University

Email: dzreyan2016@mail.ru
Russia, 344090, Rostov-on-Don

References

  1. Demyanenko S., Sharifulina S. 2021. The role of post-translational acetylation and deacetylation of signaling proteins and transcription factors after cerebral ischemia: Facts and hypotheses. Int. J. Mol. Sci. 22 (15), 7947.
  2. Spange S., Wagner T., Heinzel T., Krämer O.H. 2009. Acetylation of non-histone proteins modulates cellular signalling at multiple leve ls. Int. J. Biochem. Cell Biol. 41 (1), 185–198.
  3. Mrakovcic M., Kleinheinz J., Fröhlich L.F. 2019. p53 at the crossroads between different types of HDAC inhibitor-mediated cancer cell death. Int. J. Mol. Sci. 20 (10), 2415.
  4. Alseksek R.K., Ramadan W.S., Saleh E., El-Awady R. 2022. The role of HDACs in the response of cancer cells to cellular stress and the potential for therapeutic intervention. Int. J. Mol. Sci. 23 (15), 8141.
  5. Kao M.H., Lin T.N. 2019. Histone deacetylases in stroke. Chin. J. Physiol. 62 (3), 95–107.
  6. Demyanenko S., Dzreyan V., Sharifulina S. 2021. Histone deacetylases and their isoform-specific inhibitors in ischemic stroke. Biomedicines. 9 (10), 1445.
  7. Li Y., Gu Z., Lin S., Chen L., Dzreyan V., Eid M., Demyanenko S., He B. 2022. Histone deacetylases as epigenetic targets for treating Parkinson’s disease. Brain Sci. 12 (5), 672.
  8. Athira K.V., Sadanandan P., Chakravarty S. 2021. Repurposing vorinostat for the treatment of disorders affecting brain. Neuromolecular Med. 23 (4), 449–465.
  9. Casas C., Isus L., Herrando-Grabulosa M., Mancuso F.M., Borrás E., Sabidó E., Forés J., Aloy P. 2015. Network-based proteomic approaches reveal the neurodegenerative, neuroprotective and pain-related mechanisms involved after retrograde axonal damage. Sci. Rep. 5, 9185.
  10. Abe N., Cavalli V. 2008. Nerve injury signaling. Curr. Opin. Neurobiol. 18 (3), 276–283.
  11. Batulan Z., Nalbantoglu J., Durham H.D. 2005. Nonsteroidal anti-inflammatory drugs differentially affect the heat shock response in cultured spinal cord cells. Cell Stress Chaperones. 10 (3), 185–196.
  12. Richardson P.M., Miao T., Wu D., Zhang Y., Yeh J., Bo X. 2009. Responses of the nerve cell body to axotomy. Neurosurgery. 65 (4 Suppl), A74–A79.
  13. Weng Y.L., Joseph J., An R., Song H., Ming G.L. 2016. Epigenetic regulation of axonal regenerative capacity. Epigenomics. 8 (10), 1429–1442.
  14. Shin J.E., Cho Y. 2017. Epigenetic regulation of axon regeneration after neural injury. Mol. Cells. 40 (1), 10–16.
  15. Rishal I., Fainzilber M. 2014. Axon-soma communication in neuronal injury. Nat. Rev. Neurosci. 15 (1), 32–42.
  16. Wahane S., Halawani D., Zhou X., Zou H. 2019. Epigenetic regulation of axon regeneration and glial activation in injury responses. Front. Genet. 10, 640.
  17. Berry K.P., Lu Q.R. 2020. Chromatin modification and epigenetic control in functional nerve regeneration. Semin. Cell Dev. Biol. 97, 74–83.
  18. Mar F.M., Bonni A., Sousa M.M. 2014. Cell intrinsic control of axon regeneration. EMBO Rep. 15 (3), 254–263.
  19. Bomze H.M., Bulsara K.R., Iskandar B.J., Caroni P., Skene J.H. 2001. Spinal axon regeneration evoked by replacing two growth cone proteins in adult neurons. Nat. Neurosci. 4 (1), 38–43.
  20. Kameda T., Imamura T., Nakashima K. 2018. Epigenetic regulation of neural stem cell differentiation towards spinal cord regeneration. Cell Tissue. Res. 371 (1), 189–199.
  21. Saha A., Tiwari S., Dharmarajan S., Otteson D.C., Belecky-Adams T.L. 2018. Class I histone deacetylases in retinal progenitors and differentiating ganglion cells. Gene Expr. Patterns. 30, 37–48.
  22. Schmitt H.M., Schlamp C.L., Nickells R.W. 2016. Role of HDACs in optic nerve damage-induced nuclear atrophy of retinal ganglion cells. Neurosci. Lett. 625, 11–15.
  23. Wong V.S., Langley B. 2016. Epigenetic changes following traumatic brain injury and their implications for outcome, recovery and therapy. Neurosci. Lett. 625, 26–33.
  24. Zhong J., Zou H. 2014. BMP signaling in axon regeneration. Curr. Opin. Neurobiol. 27, 127–134.
  25. Phan M.L., Gergues M.M., Mahidadia S., Jimenez-Castillo J., Vicario D.S., Bieszczad K.M. 2017. HDAC3 inhibitor RGFP966 modulates neuronal memory for vocal communication signals in a songbird model. Front. Syst. Neurosci. 11, 65.
  26. Thomas E.A., D’Mello S.R. 2018. Complex neuroprotective and neurotoxic effects of histone deacetylases. J. Neurochem. 145 (2), 96–110.
  27. Wong J.K., Zou H. 2014. Reshaping the chromatin landscape after spinal cord injury. Front. Biol. (Beijing). 9 (5), 356–366.
  28. Schmitt H.M., Pelzel H.R., Schlamp C.L., Nickells R.W. 2014. Histone deacetylase 3 (HDAC3) plays an important role in retinal ganglion cell death after acute optic nerve injury. Mol. Neurodegener. 9, 39.
  29. Marmorstein R., Roth S.Y. 2001. Histone acetyltransferases: Function, structure, and catalysis. Curr. Opin. Genet. Dev. 11 (2), 155–161.
  30. Kimura A., Matsubara K., Horikoshi M. 2005. A decade of histone acetylation: Marking eukaryotic chromosomes with specific codes. J. Biochem. 138 (6), 647–662.
  31. Yamauchi T., Yamauchi J., Kuwata T., Tamura T., Yamashita T., Bae N., Westphal H., Ozato K., Nakatani Y. 2000. Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAF-B/ GCN5 in mouse embryogenesis. Proc. Natl. Acad. Sci. USA. 97 (21), 11303–11306.
  32. Bardai F.H., Price V., Zaayman M., Wang L., D’Mello S.R. 2012. Histone deacetylase-1 (HDAC1) is a molecular switch between neuronal survival and death. J. Biol. Chem. 287 (42), 35444–35453.
  33. Nagalakshmi B., Sagarkar S., Sakharkar A.J. 2018. Epigenetic mechanisms of traumatic brain injuries. Prog. Mol. Biol. Transl. Sci. 157, 263–298.
  34. Chen Y.T., Zang X.F., Pan J., Zhu X.L., Chen F., Chen Z.B., Xu Y. 2012. Expression patterns of histone deacetylases in experimental stroke and potential targets for neuroprotection. Clin. Exp. Pharmacol. Physiol. 39 (9), 751–758.
  35. Sun J., Ji Y., Liang Q., Ming M., Chen Y., Zhang Q., Zhou S., Shen M., Ding F. 2022. Expression of protein acetylation regulators during peripheral nerve development, injury, and regeneration. Front. Mol. Neurosci. 15, 888523.
  36. Gomis-Coloma C., Velasco-Aviles S., Gomez-Sanchez J.A., Casillas-Bajo A., Backs J., Cabedo H. 2018. Class IIa histone deacetylases link cAMP signaling to the myelin transcriptional program of schwann cells. J. Cell Biol. 217, 1249–1268.
  37. He X., Zhang L., Queme L.F., Liu X., Lu A., Waclaw R.R., Dong X., Zhou W., Kidd G., Yoon S.O., Buonanno A., Rubin J.B., Xin M., Nave K.A., Trapp B.D., Jankowski M.P., Lu Q.R. 2018. A histone deacetylase 3-dependent pathway delimits peripheral myelin growth and functional regeneration. Nat. Med. 24, 338–351.
  38. Brügger V., Duman M., Bochud M., Münger E., Heller M., Ruff S., Jacob C. 2017. Delaying histone deacetylase response to injury accelerates conversion into repair Schwann cells and nerve regeneration. Nat. Commun. 8, 14272.
  39. Dzreyan V.A., Rodkin S.V., Pitinova M.A., Uzdensky A.B. 2021. HDAC1 expression, histone deacetylation, and protective role of sodium valproate in the rat dorsal root ganglia after sciatic nerve transection. Mol. Neurobiol. 58 (1), 217–228.
  40. Chen Y., Wang H., Yoon S.O., Xu X., Hottiger M.O., Svaren J. 2011. HDAC-mediated deacetylation of NF-kappaB is critical for Schwann cell myelination. Nat. Neurosci. 14, 437–441.
  41. Duman M., Vaquié A., Nocera G., Heller M., Stumpe M., Siva Sankar D., Dengjel J., Meijer D., Yamaguchi T., Matthias P., Zeis T., Schaeren-Wiemers N., Hayoz A., Ruff S., Jacob C. 2020. EEF1A1 deacetylation enables transcriptional activation of remyelination. Nat. Commun. 11 (1), 3420.
  42. He X.T., Hu X.F., Zhu C., Zhou K.X., Zhao W.J., Zhang C., Han X., Wu C.L., Wei Y.Y., Wang W., Deng J.P., Chen F.M., Gu Z.X., Dong Y.L. 2020. Suppression of histone deacetylases by SAHA relieves bone cancer pain in rats via inhibiting activation of glial cells in spinal dorsal horn and dorsal root ganglia. J. Neuroinflammation. 17 (1), 125.
  43. Schmitt H.M., Fehrman R.L., Maes M.E., Yang H., Guo L.W., Schlamp C.L., Pelzel H.R., Nickells R.W. 2021. Increased susceptibility and intrinsic apoptotic signaling in neurons by induced HDAC3 expression. Invest. Ophthalmol. Vis. Sci. 62 (10), 14.
  44. Schmitt H.M., Grosser J.A., Schlamp C.L., Nickells R.W. 2020. Targeting HDAC3 in the DBA/2J spontaneous mouse model of glaucoma. Exp. Eye Res. 200, 108244.
  45. Hervera A., Zhou L., Palmisano I., McLachlan E., Kong G., Hutson T.H., Danzi M. C., Lemmon V.P., Bixby J.L., Matamoros-Angles A., Forsberg K., De Virgiliis F., Matheos D.P., Kwapis J., Wood M.A., Puttagunta R., Del Río J.A., Di Giovanni, S. 2019. PP4-dependent HDAC3 dephosphorylation discriminates between axonal regeneration and regenerative failure. EMBO J. 38 (13), e101032.
  46. Zaidi S.A.H., Guzman W., Singh S., Mehrotra S., Husain S. 2020. Changes in class I and IIb HDACs by δ-opioid in chronic rat glaucoma model. Invest. Ophthalmol. Vis. Sci. 61 (14), 4.
  47. Lebrun-Julien F., Suter U. 2015. Combined HDAC1 and HDAC2 depletion promotes retinal ganglion cell survival after injury through reduction of p53 target gene expression. ASN Neuro. 7 (3), 1759091415593066.
  48. Pelzel H.R., Schlamp C.L., Nickells R. W. 2010. Histone H4 deacetylation plays a critical role in early gene silencing during neuronal apoptosis. BMC Neurosci. 11, 62.
  49. Schlüter A., Aksan B., Fioravanti R., Valente S., Mai A., Mauceri D. 2019. Histone deacetylases contribute to excitotoxicity-triggered degeneration of retinal ganglion cells in vivo. Mol. Neurobiol. 56 (12), 8018–8034.
  50. Demyanenko S., Dzreyan V., Uzdensky A. 2019. Axotomy-induced changes of the protein profile in the crayfish ventral cord ganglia. Mol. Neurosci. 68 (4), 667–678.
  51. Simões-Pires C., Zwick V., Nurisso A., Schenker E., Carrupt P. A., Cuendet M. 2013. HDAC6 as a target for neurodegenerative diseases: What makes it different from the other HDACs? Mol. Neurodegener. 8, 7.
  52. d’Ydewalle C., Bogaert E., Van Den Bosch L. 2012. HDAC6 at the intersection of neuroprotection and neurodegeneration. Traffic. 13 (6), 771–779.
  53. Yuan H., Li H., Yu P., Fan Q., Zhang X., Huang W., Shen J., Cui Y., Zhou W. 2018. Involvement of HDAC6 in ischaemia and reperfusion-induced rat retinal injury. BMC Ophthalmol. 18 (1), 300.
  54. Cho Y., Sloutsky R., Naegle K.M., Cavalli V. 2015. Injury-induced HDAC5 nuclear export is essential for axon regeneration. Cell. 161 (3), 894–908.
  55. She D.T., Jo D.G., Arumugam T.V. 2017. Emerging roles of sirtuins in ischemic stroke. Transl. Stroke Res. https://doi.org/10.1007/s12975-017-0544-4
  56. Ng F., Wijaya L., Tang B.L. 2015. SIRT1 in the brain-connections with aging-associated disorders and lifespan. Front. Cell Neurosci. 9, 64.
  57. Hernández-Jiménez M., Hurtado O., Cuartero M.I., Ballesteros I., Moraga A., Pradillo J.M., McBurney M.W., Lizasoain I., Moro M.A. 2013. Silent information regulator 1 protects the brain against cerebral ischemic damage. Stroke. 44 (8), 2333–2337.
  58. Hattori Y., Okamoto Y., Nagatsuka K., Takahashi R., Kalaria R.N., Kinoshita M., Ihara M. 2015. SIRT1 attenuates severe ischemic damage by preserving cerebral blood flow. Neuroreport. 26 (3), 113–117.
  59. Li Z., Pang L., Fang F., Zhang G., Zhang J., Xie M., Wang L. 2012. Resveratrol attenuates brain damage in a rat model of focal cerebral ischemia via up-regulation of hippocampal Bcl-2. Brain Res. 1450, 116–124.
  60. Nie H., Hong Y., Lu X. Zhang J., Chen H., Li Y., Ma Y., Ying W. 2014. SIRT2 mediates oxidative stress-induced apoptosis of differentiated PC12 cells. Neuroreport. 25 (11), 838–842.
  61. Krey L., Lühder F., Kusch K., Czech-Zechmeister B., Könnecke B., Fleming Outeiro T., Trendelenburg G. 2015. Knockout of silent information regulator 2 SIRT2 preserves neurological function after experimental stroke in mice. J. Cereb. Blood Flow Metab. 35 (12), 2080–2088.
  62. Joshi P., Greco T.M., Guise A.J., Luo Y., Yu, F., Nesvizhskii A.I., Cristea I.M. 2013. The functional interactome landscape of the human histone deacetylase family. Mol. Syst. Biol. 9, 672.
  63. Dzreyan V., Rodkin S., Nikul V., Pitinova M., Uzdensky A. 2021. The expression of E2F1, p53, and caspase 3 in the rat dorsal root ganglia after sciatic nerve transection. J. Mol. Neurosci. 71 (4), 826–835.
  64. Демьяненко С.В., Дзреян В.А., Узденский А.Б. 2022. Эпигенетические механизмы повреждения и защиты клеток центральной и периферической нервных систем. Ростов-на-Дону: Изд-во Южного федерального университета. 179 с.
  65. Rodkin S., Khaitin A., Pitinova M., Dzreyan V., Guzenko V., Rudkovskii M., Sharifulina S., Uzdensky A. 2020. The localization of p53 in the crayfish mechanoreceptor neurons and its role in axotomy-induced death of satellite glial cells remote from the axon transection site. J. Mol. Neurosci. 70 (4), 532–541.
  66. Kim S.C., Sprung R., Chen Y., Xu Y., Ball H., Pei J., Cheng T., Kho Y., Xiao H., Xiao L., Grishin N.V., White M., Yang X. J., Zhao Y. 2006. Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell. 23 (4), 607–618.
  67. Uzdensky A. 2020. Multifunctional proteins. Biophysics. 65, 390–403.
  68. Родькин С.В., Дзреян В.А. Демьяненко С.В., Узденский А.Б. 2021. Роль p53-зависимых сигнальных путей в выживании и гибели нейронов и глиальных клеток при повреждении периферической нервной системы. Биол. мембраны. 38 (6), 402–417.
  69. Nijboer C.H., Heijnen C.J., van der Kooij M.A., Zijlstra J., van Velthoven C.T., Culmsee C., van Bel F., Hagberg H., Kavelaars A. 2011. Targeting the p53 pathway to protect the neonatal ischemic brain. Ann. Neurol. 70 (2), 255–264.
  70. Xie B., Gao X., Huang Y., Zhang Y., Zhu S. 2021. Remote ischemic postconditioning inhibits hippocampal neuronal apoptosis and mitophagy after cardiopulmonary resuscitation in rats. Shock. 55 (1), 74–82.
  71. Endo H., Kamada H., Nito C., Nishi T., Chan P.H. 2006. Mitochondrial translocation of p53 mediates release of cytochrome c and hippocampal CA1 neuronal death after transient global cerebral ischemia in rats. J. Neurosci. 26 (30), 7974–7983.
  72. Gu W., Roeder R.G. 1997. Activation of p53 sequence-specific DNA binding by acetylation of the p53 C-terminal domain. Cell. 90 (4), 595–606.
  73. Eid M., Dzreyan V., Demyanenko S. 2022. Sirtuins 1 and 2 in the acute period after photothrombotic stroke: Expression, localization and involvement in apoptosis. Front. Physiol. 13, 782684.
  74. Uo T., Veenstra T.D., Morrison R.S. 2009. Histone deacetylase inhibitors prevent p53-dependent and p53-independent Bax-mediated neuronal apoptosis through two distinct mechanisms. J. Neurosci. 29 (9), 2824–2832.
  75. Brochier C., Dennis G., Rivieccio M.A., McLaughlin K., Coppola G., Ratan R.R., Langley B. 2013. Specific acetylation of p53 by HDAC inhibition prevents DNA damage-induced apoptosis in neurons. J. Neurosci. 33 (20), 8621–8632.
  76. Di Giovanni S., Knights C.D., Rao M., Yakovlev A., Beers J., Catania J., Avantaggiati M.L., Faden A.I. 2006. The tumor suppressor protein p53 is required for neurite outgrowth and axon regeneration. EMBO J. 25 (17), 4084–4096.
  77. Hasegawa K., Yoshikawa K. 2008. Necdin regulates p53 acetylation via Sirtuin1 to modulate DNA damage response in cortical neurons. J. Neurosci. 28 (35), 8772–8784.
  78. 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.
  79. Iida S., Mashimo T., Kurosawa T., Hojo H., Muta H., Goto Y., Fukunishi Y., Nakamura H., Higo J. 2016. Variation of free-energy landscape of the p53 C-terminal domain induced by acetylation: Enhanced conformational sampling. J. Comput. Chem. 37 (31), 2687–2700.
  80. Knights C.D., Catania J., Di Giovanni S., Muratoglu S., Perez, R., Swartzbeck A., Quong A.A., Zhang X., Beerman T., Pestell R.G., Avantaggiati M.L. 2006. Distinct p53 acetylation cassettes differentially influence gene-expression patterns and cell fate. J. Cell Biol. 173 (4), 533–544.
  81. 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.
  82. Wilson A.M., Morquette B., Abdouh M., Unsain N., Barker P.A., Feinstein E., Di Polo A. 2013. ASPP1/2 regulate p53-dependent death of retinal ganglion cells through PUMA and Fas/CD95 activation in vivo. J. Neurosci. 33, 2205–2216.
  83. Meng P., Ghosh R. 2014. Transcription addiction: Can we garner the Yin and Yang functions of E2F1 for cancer therapy? Cell Death Dis. 5 (8), e1360.
  84. Folch J., Junyent F., Verdaguer E., Auladell C., Pizarro J.G., Beas-Zarate C., Pallàs M., Camins A. 2012. Role of cell cycle re-entry in neurons: a common apoptotic mechanism of neuronal cell death. Neurotox. Res. 22 (3), 195–207.
  85. Bretones G., Delgado M.D., León J. 2015. Myc and cell cycle control. Biochim. Biophys. Acta. 1849 (5), 506–516.
  86. Camins A., Verdaguer E., Folch J., Beas-Zarate C., Canudas A.M., Pallàs M. 2007. Inhibition of ataxia telangiectasia-p53-E2F-1 pathway in neurons as a target for the prevention of neuronal apoptosis. Curr. Drug Metab. 8 (7), 709–715.
  87. Dzreyan V., Eid M., Rodkin S., Pitinova M., Demyanenko S. 2022. E2F1 Expression and apoptosis initiation in crayfish and rat peripheral neurons and glial cells after axonal injury. Int. J. Mol. Sci. 23 (8), 4451.
  88. Ma L., Yu H.J., Gan S.W., Gong R., Mou K.J., Xue J., Sun S.Q. 2017. p53-Mediated oligodendrocyte apoptosis initiates demyelination after compressed spinal cord injury by enhancing ER-mitochondria interaction and E2F1 expression. Neurosci. Lett. 644, 55–61.
  89. Raimundo N., Song L., Shutt T.E., McKay S.E., Cotney J., Guan M.X., Gilliland T. C., Hohuan D., Santos-Sacchi J., Shadel G.S. 2012. Mitochondrial stress engages E2F1 apoptotic signaling to cause deafness. Cell. 148 (4), 716–726.
  90. Inoue K., Fry E. A., Frazier D.P. 2016. Transcription factors that interact with p53 and Mdm2. Int. J. Cancer. 138 (7), 1577–1585.
  91. Fogal V., Hsieh J.K., Royer C., Zhong S., Lu X. 2005. Cell cycle-dependent nuclear retention of p53 by E2F1 requires phosphorylation of p53 at Ser315. EMBO J. 24 (15), 2768–2782.
  92. Martínez-Balbás M.A., Bauer U.M., Nielsen S.J., Brehm A., Kouzarides T. 2000. Regulation of E2F1 activity by acetylation. EMBO J. 19 (4), 662–671.
  93. Boutillier A.L., Trinh E., Loeffler J.P. 2003. Selective E2F-dependent gene transcription is controlled by histone deacetylase activity during neuronal apoptosis. J. Neurochem. 84 (4), 814–828.
  94. Tariot P.N., Schneider L.S., Cummings J., Thomas R.G., Raman R., Jakimovich L.J., Loy R., Bartocci B., Fleisher A., Ismail M.S., Porsteinsson A., Weiner M., Jack C.R. Jr., Thal L., Aisen P.S. 2011. Chronic divalproex sodium to attenuate agitation and clinical progression of Alzheimer disease. Arch. Gen. Psychiatry. 68 (8), 853–861.
  95. Piepers S., Veldink J.H., de Jong S.W., van der Tweel I., van der Pol W.L., Uijtendaal E.V., Schelhaas H.J., Scheffer H., de Visser M., de Jong J.M., Wokke J.H., Groeneveld G.J., van den Berg L.H. 2009. Randomized sequential trial of valproic acid in amyotrophic lateral sclerosis. Ann. Neurol. 66 (2), 227–234.
  96. Ho T.C.S., Chan A.H.Y., Ganesan A. 2020. Thirty years of HDAC inhibitors: 2020 insight and hindsight. J. Med. Chem. 63 (21), 12460–12484.
  97. Wang C., Zheng C., Wang H., Zhang L., Liu Z., Xu P. 2022. The state of the art of PROTAC technologies for drug discovery. Eur. J. Med. Chem. 5 (235), 114290.
  98. Kumar D., Hassan M.I. 2022. Targeted protein degraders march towards the clinic for neurodegenerative diseases. Ageing Res. Rev. 1 (78), 101616.
  99. Yang K., Zhao Y., Nie X., Wu H., Wang B., Almodovar-Rivera C.M, Xie H., Tang W. 2020. A cell-based target engagement assay for the identification of cereblon E3 ubiquitin ligase ligands and their application in HDAC6 degraders. Cell Chem. Biol. 27 (7), 866–876.
  100. Cao Z., Gu Z., Lin S., Chen D., Wang J., Zhao Y., Li Y., Liu T., Li Y., Wang Y., Lin H., He B. 2021. Attenuation of NLRP3 inflammasome activation by indirubin-derived PROTAC targeting HDAC6. ACS Chem. Biol. 16 (12), 2746–2751.
  101. Hong J.Y., Jing H., Price I.R., Cao J., Bai J.J., Lin H. 2020. Simultaneous inhibition of SIRT2 deacetylase and defatty-acylase activities via a PROTAC strategy. ACS Med. Chem. Lett. 11 (11), 2305–2311.
  102. Schiedel M., Lehotzky A., Szunyogh S., Oláh J., Hammelmann S., Wössner N., Robaa D., Einsle O., Sippl W., Ovádi J., Jung M. 2020. HaloTag-targeted sirtuin-rearranging ligand (SirReal) for the development of proteolysis-targeting chimeras (PROTACs) against the lysine deacetylase sirtuin 2 (Sirt2). Chembiochem. 21 (23), 3371–3376.

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