In vitro and in vivo Biological Evaluation of Newly Tacrine-Selegiline Hybrids as Multi-Target Inhibitors of Cholinesterases and Monoamine Oxidases for Alzheimer’s Disease

References

• Alzheimer’s A. 2016 Alzheimer’s disease facts and figures. Alzheimers Dement. 2016;12:459–509. doi:10.1016/j.jalz.2016.03.001
   PubMedGoogle Scholar
• Scheltens P, De Strooper B, Kivipelto M, et al. Alzheimer’s disease. Lancet. 2021;397:1577–1590. doi:10.1016/S0140-6736(20)32205-4
   PubMed Web of Science ®Google Scholar
• Collaborators GDF. Estimation of the global prevalence of dementia in 2019 and forecasted prevalence in 2050: an analysis for the global burden of disease study 2019. Lancet Public Health. 2022;7:105–125. doi:10.1016/s2468-2667(21)00249-8
   Web of Science ®Google Scholar
• Levey AI. Progress with Treatments for Alzheimer’s Disease. N Engl J Med. 2021;384:1762–1763. doi:10.1056/NEJMe2103722
   PubMed Web of Science ®Google Scholar
• Li Q, Xing S, Chen Y, et al. Discovery and biological evaluation of a novel highly potent selective butyrylcholinsterase inhibitor. J Med Chem. 2020;63:10030–10044. doi:10.1021/acs.jmedchem.0c01129
   PubMed Web of Science ®Google Scholar
• Scarpini E, Scheltens P, Feldman H. Treatment of Alzheimer’s disease: current status and new perspectives. Lancet Neurol. 2003;2:539–547. doi:10.1016/s1474-4422(03)00502-7
   PubMed Web of Science ®Google Scholar
• Ballard C, Gauthier S, Corbett A, Brayne C, Aarsland D, Jones E. Alzheimer’s disease. Lancet. 2011;377:1019–1031. doi:10.1016/s0140-6736(10)61349-9
   PubMed Web of Science ®Google Scholar
• Chun H, Im H, Kang YJ, et al. Severe reactive astrocytes precipitate pathological hallmarks of Alzheimer’s disease via H(2)O(2)(-) production. Nat Neurosci. 2020;23:1555–1566. doi:10.1038/s41593-020-00735-y
   PubMed Web of Science ®Google Scholar
• Simunkova M, Alwasel SH, Alhazza IM, et al. Management of oxidative stress and other pathologies in Alzheimer’s disease. Arch Toxicol. 2019;93:2491–2513. doi:10.1007/s00204-019-02538-y
   PubMed Web of Science ®Google Scholar
• Vaz M, Silvestre S. Alzheimer’s disease: recent treatment strategies. Eur J Pharmacol. 2020;887:173554. doi:10.1016/j.ejphar.2020.173554
   PubMed Web of Science ®Google Scholar
• Høilund-Carlsen PF, Revheim ME, Costa T, et al. Passive Alzheimer’s immunotherapy: a promising or uncertain option? Ageing Res Rev. 2023;90:101996. doi:10.1016/j.arr.2023.101996
   PubMed Web of Science ®Google Scholar
• Przybyłowska M, Kowalski S, Dzierzbicka K, Inkielewicz-Stepniak I. Therapeutic Potential of Multifunctional Tacrine Analogues. Curr Neuropharmacol. 2019;17:472–490. doi:10.2174/1570159x16666180412091908
   PubMed Web of Science ®Google Scholar
• Perry EK, Tomlinson BE, Blessed G, Bergmann K, Gibson PH, Perry RH. Correlation of cholinergic abnormalities with senile plaques and mental test scores in senile dementia. Br Med J. 1978;2:1457–1459. doi:10.1136/bmj.2.6150.1457
   PubMed Web of Science ®Google Scholar
• Kucukoglu K, Gul HI, Taslimi P, Gulcin I, Supuran CT. Investigation of inhibitory properties of some hydrazone compounds on hCA I, hCA II and AChE enzymes. Bioorg Chem. 2019;86:316–321. doi:10.1016/j.bioorg.2019.02.008
   PubMed Web of Science ®Google Scholar
• Li Q, Yang H, Chen Y, Sun H. Recent progress in the identification of selective butyrylcholinesterase inhibitors for Alzheimer’s disease. Eur J Med Chem. 2017;132:294–309. doi:10.1016/j.ejmech.2017.03.062
   PubMed Web of Science ®Google Scholar
• Gómez-Ramos P, Morán MA. Ultrastructural localization of butyrylcholinesterase in senile plaques in the brains of aged and Alzheimer disease patients. Mol Chem Neuropathol. 1997;30:161–173. doi:10.1007/bf02815095
   PubMedGoogle Scholar
• Dogterom P, Nagelkerke JF, Mulder GJ. Hepatotoxicity of tetrahydroaminoacridine in isolated rat hepatocytes: effect of glutathione and vitamin E. Biochem Pharmacol. 1988;37:2311–2313. doi:10.1016/0006-2952(88)90356-5
   PubMed Web of Science ®Google Scholar
• Zemek F, Drtinova L, Nepovimova E, et al. Outcomes of Alzheimer’s disease therapy with acetylcholinesterase inhibitors and memantine. Expert Opin Drug Saf. 2014;13:759–774. doi:10.1517/14740338.2014.914168
   PubMed Web of Science ®Google Scholar
• Nepovimova E, Korabecny J, Dolezal R, et al. Tacrine-trolox hybrids: a novel class of centrally active, nonhepatotoxic multi-target-directed ligands exerting anticholinesterase and antioxidant activities with low in vivo toxicity. J Med Chem. 2015;58:8985–9003. doi:10.1021/acs.jmedchem.5b01325
   PubMed Web of Science ®Google Scholar
• Tumiatti V, Minarini A, Bolognesi ML, Milelli A, Rosini M, Melchiorre C. Tacrine derivatives and Alzheimer’s disease. Curr Med Chem. 2010;17:1825–1838. doi:10.2174/092986710791111206
   PubMed Web of Science ®Google Scholar
• Lu C, Zhou Q, Yan J, Du Z, Huang L, Li X. A novel series of tacrine-selegiline hybrids with cholinesterase and monoamine oxidase inhibition activities for the treatment of Alzheimer’s disease. Eur J Med Chem. 2013;62:745–753. doi:10.1016/j.ejmech.2013.01.039
   PubMed Web of Science ®Google Scholar
• Finberg JP. Update on the pharmacology of selective inhibitors of MAO-A and MAO-B: focus on modulation of CNS monoamine neurotransmitter release. Pharmacol Ther. 2014;143:133–152. doi:10.1016/j.pharmthera.2014.02.010
   PubMed Web of Science ®Google Scholar
• Chen JJ, Wilkinson JR. The monoamine oxidase type B inhibitor rasagiline in the treatment of Parkinson disease: is tyramine a challenge? J Clin Pharmacol. 2012;52:620–628. doi:10.1177/0091270011406279
   PubMed Web of Science ®Google Scholar
• Kalgutkar AS, Dalvie DK, Castagnoli N, Taylor TJ. Interactions of nitrogen-containing xenobiotics with monoamine oxidase (MAO) isozymes A and B: SAR studies on MAO substrates and inhibitors. Chem Res Toxicol. 2001;14:1139–1162. doi:10.1021/tx010073b
   PubMed Web of Science ®Google Scholar
• Boppana K, Dubey PK, Jagarlapudi SA, Vadivelan S, Rambabu G. Knowledge based identification of MAO-B selective inhibitors using pharmacophore and structure based virtual screening models. Eur J Med Chem. 2009;44:3584–3590. doi:10.1016/j.ejmech.2009.02.031
   PubMed Web of Science ®Google Scholar
• Gottfries CG. Alzheimer’s disease and senile dementia: biochemical characteristics and aspects of treatment. Psychopharmacology. 1985;86:245–252. doi:10.1007/bf00432208
   PubMed Web of Science ®Google Scholar
• Naoi M, Maruyama W. Monoamine oxidase inhibitors as neuroprotective agents in age-dependent neurodegenerative disorders. Curr Pharm Des. 2010;16:2799–2817. doi:10.2174/138161210793176527
   PubMed Web of Science ®Google Scholar
• Zhang P, Xu S, Zhu Z, Xu J. Multi-target design strategies for the improved treatment of Alzheimer’s disease. Eur J Med Chem. 2019;176:228–247. doi:10.1016/j.ejmech.2019.05.020
   PubMed Web of Science ®Google Scholar
• Farina R, Pisani L, Catto M, et al. Structure-based design and optimization of multitarget-directed 2H-chromen-2-one derivatives as potent inhibitors of monoamine oxidase B and cholinesterases. J Med Chem. 2015;58:5561–5578. doi:10.1021/acs.jmedchem.5b00599
   PubMed Web of Science ®Google Scholar
• Schneider LS, Geffen Y, Rabinowitz J, et al. Low-dose ladostigil for mild cognitive impairment: a Phase 2 placebo-controlled clinical trial. Neurology. 2019;93:1474–1484. doi:10.1212/wnl.0000000000008239
   PubMed Web of Science ®Google Scholar
• Hiremathad A, Keri RS, Esteves AR, Cardoso SM, Chaves S, Santos MA. Novel tacrine-hydroxyphenylbenzimidazole hybrids as potential multitarget drug candidates for Alzheimer’s disease. Eur J Med Chem. 2018;148:255–267. doi:10.1016/j.ejmech.2018.02.023
   PubMed Web of Science ®Google Scholar
• Frantz MC, Pellissier LP, Pflimlin E, et al. LIT-001, the first nonpeptide oxytocin receptor agonist that improves social interaction in a mouse model of autism. J Med Chem. 2018;61:8670–8692. doi:10.1021/acs.jmedchem.8b00697
   PubMed Web of Science ®Google Scholar
• Bolea I, Juárez-Jiménez J, de Los Ríos C, et al. Synthesis, biological evaluation, and molecular modeling of donepezil and N-[(5-(benzyloxy)-1-methyl-1H-indol-2-yl)methyl]-N-methylprop-2-yn-1-amine hybrids as new multipotent cholinesterase/monoamine oxidase inhibitors for the treatment of Alzheimer’s disease. J Med Chem. 2011;54:8251–8270. doi:10.1021/jm200853t
   PubMed Web of Science ®Google Scholar
• Ellman GL, Courtney KD, Andres V, Feather-Stone RM. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961;7:88–95. doi:10.1016/0006-2952(61)90145-9
   PubMed Web of Science ®Google Scholar
• Matos MJ, Terán C, Pérez-Castillo Y, Uriarte E, Santana L, Viña D. Synthesis and study of a series of 3-arylcoumarins as potent and selective monoamine oxidase B inhibitors. J Med Chem. 2011;54:7127–7137. doi:10.1021/jm200716y
   PubMed Web of Science ®Google Scholar
• Jiang N, Huang Q, Liu J, et al. Design, synthesis and biological evaluation of new coumarin-dithiocarbamate hybrids as multifunctional agents for the treatment of Alzheimer’s disease. Eur J Med Chem. 2018;146:287–298. doi:10.1016/j.ejmech.2018.01.055
   PubMed Web of Science ®Google Scholar
• Di L, Kerns EH, Fan K, McConnell OJ, Carter GT. High throughput artificial membrane permeability assay for blood-brain barrier. Eur J Med Chem. 2003;38:223–232. doi:10.1016/s0223-5234(03)00012-6
   PubMed Web of Science ®Google Scholar
• Zhong GH, Guo J, Pang CY, et al. Novel AP2238-clorgiline hybrids as multi-target agents for the treatment of Alzheimer’s disease: design, synthesis, and biological evaluation. Bioorg Chem. 2023;130:106224. doi:10.1016/j.bioorg.2022.106224
   PubMed Web of Science ®Google Scholar
• He Q, Liu J, Lan JS, et al. Coumarin-dithiocarbamate hybrids as novel multitarget AChE and MAO-B inhibitors against Alzheimer’s disease: design, synthesis and biological evaluation. Bioorg Chem. 2018;81:512–528. doi:10.1016/j.bioorg.2018.09.010
   PubMed Web of Science ®Google Scholar
• Ukai M, Kobayashi T, Shinkai N, Shan-Wu X, Kameyama T. Dynorphin A-(1-13) potently improves scopolamine-induced impairment of passive avoidance response in mice. Eur J Pharmacol. 1995;274:89–93. doi:10.1016/0014-2999(94)00710-o
   PubMed Web of Science ®Google Scholar
• Sang Z, Pan W, Wang K, et al. Design, synthesis and evaluation of novel ferulic acid-O-alkylamine derivatives as potential multifunctional agents for the treatment of Alzheimer’s disease. Eur J Med Chem. 2017;130:379–392. doi:10.1016/j.ejmech.2017.02.039
   PubMed Web of Science ®Google Scholar
• Li Q, Meng L, Zhou S, et al. Rapid generation of novel benzoic acid-based xanthine derivatives as highly potent, selective and long acting DPP-4 inhibitors: scaffold-hopping and prodrug study. Eur J Med Chem. 2019;180:509–523. doi:10.1016/j.ejmech.2019.07.045
   PubMed Web of Science ®Google Scholar
• Xie SS, Liu J, Tang C, et al. Design, synthesis and biological evaluation of rasagiline-clorgyline hybrids as novel dual inhibitors of monoamine oxidase-B and amyloid-β aggregation against Alzheimer’s disease. Eur J Med Chem. 2020;202:112475. doi:10.1016/j.ejmech.2020.112475
   PubMed Web of Science ®Google Scholar
• Jiang N, Ding J, Liu J, et al. Novel chromanone-dithiocarbamate hybrids as multifunctional AChE inhibitors with β-amyloid anti-aggregation properties for the treatment of Alzheimer’s disease. Bioorg Chem. 2019;89:103027. doi:10.1016/j.bioorg.2019.103027
   PubMed Web of Science ®Google Scholar