Synthesis and biological evaluation of C-4 substituted phenoxazine-bearing hydroxamic acids with potent class II histone deacetylase inhibitory activities

References

• Franceschi C, Garagnani P, Morsiani C, Conte M, Santoro A, Grignolio A, Monti D, Capri M, Salvioli S. The continuum of aging and age-related diseases: common mechanisms but different rates. Front Med). 2018;5:61.
   Web of Science ®Google Scholar
• 2020 Alzheimer’s disease facts and figures. Alzheimer’s Dement. 2020;16(3):391–460.
   Google Scholar
• Burns A, Iliffe S. Alzheimer’s disease. BMJ. 2009;338:b158.
   PubMed Web of Science ®Google Scholar
• Tagliapietra M. Aducanumab for the treatment of alzheimer’s disease. Drugs Today. 2022;58(10):465–477.
   PubMed Web of Science ®Google Scholar
• Leon R, Garcia AG, Marco-Contelles J. Recent advances in the multitarget-directed ligands approach for the treatment of alzheimer’s disease. Med Res Rev. 2013;33(1):139–189.
   PubMed Web of Science ®Google Scholar
• Yamakawa H, Cheng J, Penney J, Gao F, Rueda R, Wang J, Yamakawa S, Kritskiy O, Gjoneska E, Tsai LH. The transcription factor sp3 cooperates with HDAC2 to regulate synaptic function and plasticity in neurons. Cell Rep. 2017;20(6):1319–1334.
   PubMed Web of Science ®Google Scholar
• Li JL, Chen JM, Ricupero CL, Hart RP, Schwartz MS, Kusnecov A, Herrup K. Nuclear accumulation of HDAC4 in atm deficiency promotes neurodegeneration in ataxia telangiectasia. Nat Med. 2012;18(5):783–790.
   PubMed Web of Science ®Google Scholar
• Tseng JH, Xie L, Song S, Xie YM, Allen L, Ajit D, Hong JS, Chen X, Meeker RB, Cohen TJ. The deacetylase HDAC6 mediates endogenous neuritic tau pathology. Cell Rep. 2017;20(9):2169–2183.
   PubMed Web of Science ®Google Scholar
• Govindarajan N, Rao P, Burkhardt S, Sananbenesi F, Schluter OM, Bradke F, Lu JR, Fischer A. Reducing HDAC6 ameliorates cognitive deficits in a mouse model for alzheimer’s disease. EMBO Mol Med. 2013;5(1):52–63.
   PubMed Web of Science ®Google Scholar
• Ballatore C, Brunden KR, Trojanowski JQ, Lee VMY, Smith AB, Huryn DM. Modulation of protein-protein interactions as a therapeutic strategy for the treatment of neurodegenerative tauopathies. Curr Top Med Chem. 2011;11(3):317–330.
   PubMed Web of Science ®Google Scholar
• Foglietti C, Filocamo G, Cundari E, De Rinaldis E, Lahm A, Cortese R, Steinkuhler C. Dissecting the biological functions of drosophila histone deacetylases by RNA interference and transcriptional profiling. J Biol Chem. 2006;281(26):17968–17976.
   PubMed Web of Science ®Google Scholar
• Mazzocchi M, Goulding SR, Morales-Prieto N, Foley T, Collins LM, Sullivan AM, O'Keeffe GW. Peripheral administration of the class-IIa HDAC inhibitor mc1568 partially protects against nigrostriatal neurodegeneration in the striatal 6-ohda rat model of parkinson’s disease. Brain Behav Immun. 2022;102:151–160.
   PubMed Web of Science ®Google Scholar
• Tang BL. Class II HDACs and neuronal regeneration. J Cell Biochem. 2014;115(7):1225–1233.
   PubMed Web of Science ®Google Scholar
• Anderson KW, Chen JJ, Wang MY, Mast N, Pikuleva IA, Turko IV. Quantification of histone deacetylase isoforms in human frontal cortex, human retina, and mouse brain. PLOS One. 2015;10(5):e0126592.
   PubMed Web of Science ®Google Scholar
• Margariti A, Zampetaki A, Xiao QZ, Zhou BD, Karamariti E, Martin D, Yin XK, Mayr M, Li HL, Zhang ZY, et al. Histone deacetylase 7 controls endothelial cell growth through modulation of beta-catenin. Circ Res. 2010;106(7):1202–1211.
   PubMed Web of Science ®Google Scholar
• Vallee A, Lecarpentier Y. Alzheimer disease: crosstalk between the canonical wnt/beta-catenin pathway and ppars alpha and gamma. Front Neurosci. 2016;10:459.
   PubMed Web of Science ®Google Scholar
• Aizawa S, Teramoto K, Yamamuro Y. Histone deacetylase 9 as a negative regulator for choline acetyltransferase gene in ng108-15 neuronal cells. Neurosci. 2012;205:63–72.
   Web of Science ®Google Scholar
• Yu CW, Chang PT, Hsin LW, Chern JW. Quinazolin-4-one derivatives as selective histone deacetylase-6 inhibitors for the treatment of alzheimer’s disease. J Med Chem. 2013;56(17):6775–6791.
   PubMed Web of Science ®Google Scholar
• Ding H, Dolan PJ, Johnson GV. Histone deacetylase 6 interacts with the microtubule-associated protein tau. J Neurochem. 2008;106(5):2119–2130.
   PubMed Web of Science ®Google Scholar
• Yang SS, Zhang R, Wang G, Zhang YF. The development prospection of HDAC inhibitors as a potential therapeutic direction in Alzheimer’s disease. Transl Neurodegener. 2017;6:19.
   PubMed Web of Science ®Google Scholar
• Sung YM, Lee T, Yoon H, DiBattista AM, Song JM, Sohn Y, Moffat EI, Turner RS, Jung M, Kim J, et al. Mercaptoacetamide-based class II HDAC inhibitor lowers abeta levels and improves learning and memory in a mouse model of Alzheimer’s disease. Exp Neurol. 2013;239:192–201.
   PubMed Web of Science ®Google Scholar
• Hsu KC, Chu JC, Tseng HJ, Liu CI, Wang HC, Lin TE, Lee HS, Hsin LW, Wang AHJ, Lin CH, et al. Synthesis and biological evaluation of phenothiazine derivative-containing hydroxamic acids as potent class ii histone deacetylase inhibitors. Eur J Med Chem. 2021;219:113419.
   PubMed Web of Science ®Google Scholar
• Thimmaiah KN, Horton JK, Seshadri R, Israel M, Houghton JA, Harwood FC, Houghton PJ. Synthesis and chemical characterization of n-substituted phenoxazines directed toward reversing vinca alkaloid resistance in multidrug-resistant cancer-cells. J Med Chem. 1992;35(18):3358–3364.
   PubMed Web of Science ®Google Scholar
• Hernandez-Olmos V, Abdelrahman A, El-Tayeb A, Freudendahl D, Weinhausen S, Muller CE. N-substituted phenoxazine and acridone derivatives: Structure-activity relationships of potent p2x4 receptor antagonists. J Med Chem. 2012;55(22):9576–9588.
   PubMed Web of Science ®Google Scholar
• Behl C, Moosmann B. Oxidative nerve cell death in Alzheimer’s disease and stroke: antioxidants as neuroprotective compounds. Biol Chem. 2002;383(3-4):521–536.
   PubMed Web of Science ®Google Scholar
• Hajieva P, Mocko JB, Moosmann B, Behl C. Novel imine antioxidants at low nanomolar concentrations protect dopaminergic cells from oxidative neurotoxicity. J Neurochem. 2009;110(1):118–132.
   PubMed Web of Science ®Google Scholar
• Yue K, Sun S, Jia G, Qin M, Hou X, Chou CJ, Huang C, Li X. First-in-class hydrazide-based hdac6 selective inhibitor with potent oral anti-inflammatory activity by attenuating nlrp3 inflammasome activation. J Med Chem. 2022;65(18):12140–12162.
   PubMed Web of Science ®Google Scholar
• Chao SW, Chen LC, Yu CC, Liu CY, Lin TE, Guh JH, Wang CY, Chen CY, Hsu KC, Huang WJ. Discovery of aliphatic-chain hydroxamates containing indole derivatives with potent class I histone deacetylase inhibitory activities. Eur J Med Chem. 2018;143:792–805.
   PubMed Web of Science ®Google Scholar
• Chen LC, Tseng HJ, Liu CY, Huang YY, Yen CC, Weng JR, Lu YL, Hou WC, Lin TE, Pan IH, et al. Design of diarylheptanoid derivatives as dual inhibitors against class IIa histone deacetylase and beta-amyloid aggregation. Front Pharmacol. 2018;9:708.
   PubMed Web of Science ®Google Scholar
• Nepali K, Chang TY, Lai MJ, Hsu KC, Yen Y, Lin TE, Lee SB, Liou JP. Purine/purine isoster based scaffolds as new derivatives of benzamide class of HDAC inhibitors. Eur J Med Chem. 2020;196:112291.
   PubMed Web of Science ®Google Scholar
• LeadIT v2.3.2, 2019. Sankt Augustin, Germany: BiosolveIT GmBH. Available from http://www.biosolveit.de/LeadIT.
   Google Scholar
• Burley SK, Berman HM, Bhikadiya C, Bi C, Chen L, Di Costanzo L, Christie C, Dalenberg K, Duarte JM, Dutta S, et al. RCSB protein data bank: Biological macromolecular structures enabling research and education in fundamental biology, biomedicine, biotechnology and energy. Nucleic Acids Res. 2019;47(D1):D464–D474.
   PubMed Web of Science ®Google Scholar
• The PyMOL Molecular Graphics System, Version 2.2.1, Schrödinger, LLC.
   Google Scholar
• Moritomo A, Yamada H, Watanabe T, Itahana H, Koga Y, Akuzawa S, Okada M. Synthesis and structure-activity relationships of new carbonyl guanidine derivatives as novel dual 5-ht2b and 5-ht7 receptor antagonists. Part 2. Bioorg Med Chem. 2014;22(15):4323–4337.
   PubMed Web of Science ®Google Scholar
• Eastmond GC, Gilchrist TL, Paprotny J, Steiner A. Cyano-activated fluoro displacement reactions in the synthesis of cyanophenoxazines and related compounds. New J Chem. 2001;25(3):385–390.
   Web of Science ®Google Scholar
• Wu CC, Lee PT, Kao TJ, Chou SY, Su RY, Lee YC, Yeh SH, Liou JP, Hsu TI, Su TP, et al. Upregulation of znf179 acetylation by saha protects cells against oxidative stress. Redox Biol. 2018;19:74–80.
   PubMed Web of Science ®Google Scholar
• Peleg S, Sananbenesi F, Zovoilis A, Burkhardt S, Bahari-Javan S, Agis-Balboa RC, Cota P, Wittnam JL, Gogol-Doering A, Opitz L, et al. Altered histone acetylation is associated with age-dependent memory impairment in mice. Science. 2010;328(5979):753–756.
   PubMed Web of Science ®Google Scholar
• Benito E, Urbanke H, Ramachandran B, Barth J, Halder R, Awasthi A, Jain G, Capece V, Burkhardt S, Navarro-Sala M, et al. HDAC inhibitor-dependent transcriptome and memory reinstatement in cognitive decline models. J Clin Invest. 2015;125(9):3572–3584.
   PubMed Web of Science ®Google Scholar
• Skultetyova L, Ustinova K, Kutil Z, Novakova Z, Pavlicek J, Mikesova J, Trapl D, Baranova P, Havlinova B, Hubalek M, et al. Human histone deacetylase 6 shows strong preference for tubulin dimers over assembled microtubules. Sci Rep. 2017;7(1):11547.
   PubMedGoogle Scholar
• Wang X, Zhou Y, Gao Q, Ping D, Wang Y, Wu W, Lin X, Fang Y, Zhang J, Shao A. The role of exosomal micrornas and oxidative stress in neurodegenerative diseases. Oxid Med Cell Longev. 2020;2020:3232869.
   PubMed Web of Science ®Google Scholar
• Klein JA, Ackerman SL. Oxidative stress, cell cycle, and neurodegeneration. J Clin Invest. 2003;111(6):785–793.
   PubMed Web of Science ®Google Scholar
• Feng F, Daw JN, Chen QM. Histone deacetylase inhibitors prevent H2O2 from inducing stress granule formation. Curr Res Toxicol. 2020;1:141–148.
   PubMedGoogle Scholar