196
Views
1
CrossRef citations to date
0
Altmetric
Research Articles

Computational design of new tacrine analogs: an in silico prediction of their cholinesterase inhibitory, antioxidant, and hepatotoxic activities

, & ORCID Icon
Pages 91-105 | Received 28 May 2021, Accepted 04 Nov 2021, Published online: 26 Nov 2021

References

  • Abraham, M. J., Murtola, T., Schulz, R., Páll, S., Smith, J. C., Hess, B., & Lindahl, E. (2015). GROMACS: High performance molecular simulations through multi-level parallelism from laptops to supercomputers. SoftwareX, 1–2, 19–25. https://doi.org/10.1016/j.softx.2015.06.001
  • Albertini, C., Salerno, A., de Sena Murteira Pinheiro, P., & Bolognesi, M. L. (2021). From combinations to multitarget-directed ligands: A continuum in Alzheimer's disease polypharmacology. Medicinal Research Reviews, 41(5), 2606–2633. https://doi.org/10.1002/med.21699
  • Amine Khodja, I., & Boulebd, H. (2020). Synthesis, biological evaluation, theoretical investigations, docking study and ADME parameters of some 1,4-bisphenylhydrazone derivatives as potent antioxidant agents and acetylcholinesterase inhibitors. Molecular Diversity, 25, 279–290. https://doi.org/10.1007/s11030-020-10064-8
  • Anand, P., & Singh, B. (2013). A review on cholinesterase inhibitors for Alzheimer's disease. Archives of Pharmacal Research, 36(4), 375–399. https://doi.org/10.1007/s12272-013-0036-3
  • Atri, A. (2019). Current and future treatments in Alzheimer's disease. Seminars in Neurology, 39(2), 227–240.
  • Ayton, S., Lei, P., & Bush, A. I. (2013). Metallostasis in Alzheimer's disease. Free Radical Biology & Medicine, 62, 76–89. https://doi.org/10.1016/j.freeradbiomed.2012.10.558
  • Bartolini, M., & Marco-Contelles, J. (2019). Tacrines as therapeutic agents for Alzheimer's disease. IV. The tacripyrines and related annulated tacrines. Chemical Record (New York, NY), 19(5), 927–937. https://doi.org/10.1002/tcr.201800155
  • Birla, H., Minocha, T., Kumar, G., Misra, A., & Singh, S. K. (2020). Role of oxidative stress and metal toxicity in the progression of Alzheimer's Disease. Current Neuropharmacology, 18(7), 552–562. https://doi.org/10.2174/1570159X18666200122122512
  • Boulebd, H. (2021a). Are thymol, rosefuran, terpinolene and umbelliferone good scavengers of peroxyl radicals? Phytochemistry, 184, 112670. https://doi.org/10.1016/j.phytochem.2021.112670
  • Boulebd, H. (2021b). Modeling the peroxyl radical scavenging behavior of Carnosic acid: Mechanism, kinetics, and effects of physiological environments. Phytochemistry, 192, 112950. https://doi.org/10.1016/j.phytochem.2021.112950
  • Boulebd, H. (2021c). Structure-activity relationship of antioxidant prenylated (iso)flavonoid-type compounds: quantum chemistry and molecular docking studies. Journal of Biomolecular Structure and Dynamics, 1–10. https://doi.org/10.1080/07391102.2021.1943529
  • Boulebd, H., & Amine Khodja, I. (2021). A detailed DFT-based study of the free radical scavenging activity and mechanism of daphnetin in physiological environments. Phytochemistry, 189, 112831. https://doi.org/10.1016/j.phytochem.2021.112831
  • Boulebd, H., Ismaili, L., Martin, H., Bonet, A., Chioua, M., Marco-Contelles, J., & Belfaitah, A. (2017). New (benz)imidazolopyridino tacrines as nonhepatotoxic, cholinesterase inhibitors for Alzheimer disease. Future Medicinal Chemistry, 9(8), 723–729. https://doi.org/10.4155/fmc-2017-0019
  • Cassidy, L., Fernandez, F., Johnson, J. B., Naiker, M., Owoola, A. G., & Broszczak, D. A. (2020). Oxidative stress in Alzheimer's disease: A review on emergent natural polyphenolic therapeutics. Complementary Therapies in Medicine, 49, 102294. https://doi.org/10.1016/j.ctim.2019.102294
  • Cavalli, A., Bolognesi, M. L., Minarini, A., Rosini, M., Tumiatti, V., Recanatini, M., & Melchiorre, C. (2008). Multi-target-directed ligands to combat neurodegenerative diseases. Journal of Medicinal Chemistry, 51(3), 347–372. https://doi.org/10.1021/jm7009364
  • Chen, J., Yang, J., Ma, L., Li, J., Shahzad, N., & Kim, C. K. (2020). Structure-antioxidant activity relationship of methoxy, phenolic hydroxyl, and carboxylic acid groups of phenolic acids. Scientific Reports, 10(1), 1–9. https://doi.org/10.1038/s41598-020-59451-z
  • Chioua, M., Buzzi, E., Moraleda, I., Iriepa, I., Maj, M., Wnorowski, A., Giovannini, C., Tramarin, A., Portali, F., Ismaili, L., López-Alvarado, P., Bolognesi, M. L., Jóźwiak, K., Menéndez, J. C., Marco-Contelles, J., & Bartolini, M. (2018). Tacripyrimidines, the first tacrine-dihydropyrimidine hybrids, as multi-target-directed ligands for Alzheimer's disease. European Journal of Medicinal Chemistry, 155, 839–846. https://doi.org/10.1016/j.ejmech.2018.06.044
  • Darvesh, S., Cash, M. K., Reid, G. A., Martin, E., Mitnitski, A., & Geula, C. (2012). Butyrylcholinesterase is associated with β-amyloid plaques in the transgenic APPSWE/PSEN1dE9 mouse model of Alzheimer disease. Journal of Neuropathology and Experimental Neurology, 71(1), 2–14. https://doi.org/10.1097/NEN.0b013e31823cc7a6
  • Davis, K. L., Mohs, R. C., Marin, D., Purohit, D. P., Perl, D. P., Lantz, M., Austin, G., & Haroutunian, V. (1999). Cholinergic markers in elderly patients with early signs of Alzheimer disease. JAMA, 281(15), 1401–1406. https://doi.org/10.1001/jama.281.15.1401
  • de los Ríos, C., & Marco-Contelles, J. (2019). Tacrines for Alzheimer's disease therapy. III. The PyridoTacrines. European Journal of Medicinal Chemistry, 166, 381–389. https://doi.org/10.1016/j.ejmech.2019.02.005
  • Eckroat, T. J., Manross, D. L., & Cowan, S. C. (2020). Merged tacrine-based, multitarget-directed acetylcholinesterase inhibitors 2015–present: Synthesis and biological activity. International Journal of Molecular Sciences, 21(17), 5965. https://doi.org/10.3390/ijms21175965
  • Fan, L., Mao, C., Hu, X., Zhang, S., Yang, Z., Hu, Z., Sun, H., Fan, Y., Dong, Y., Yang, J., Shi, C., & Xu, Y. (2019). New insights into the pathogenesis of Alzheimer's disease. Frontiers in Neurology, 10, 1312. https://doi.org/10.3389/fneur.2019.01312
  • Frisch, M. J., Trucks, G. W., Schlegel, H. B., Scuseria, G. E., Robb, M. A., Cheeseman, J. R., … Fox, D. J. (2009). Gaussian 09. Gaussian, Inc.
  • Galano, A. (2015). Free radicals induced oxidative stress at a molecular level: the current status, challenges and perspectives of computational chemistry based protocols. Journal of the Mexican Chemical Society, 59(4), 231–262.
  • Galano, A., & Alvarez-Idaboy, J. R. (2014). Kinetics of radical-molecule reactions in aqueous solution: A benchmark study of the performance of density functional methods. Journal of Computational Chemistry, 35(28), 2019–2026. https://doi.org/10.1002/jcc.23715
  • Gálvez, J., Polo, S., Insuasty, B., Gutiérrez, M., Cáceres, D., Alzate-Morales, J. H., De-la-Torre, P., & Quiroga, J. (2018). Design, facile synthesis, and evaluation of novel spiro- and pyrazolo[1,5-c]quinazolines as cholinesterase inhibitors: Molecular docking and MM/GBSA studies. Computational Biology and Chemistry, 74, 218–229. https://doi.org/10.1016/j.compbiolchem.2018.03.001
  • Guzior, N., Wieckowska, A., Panek, D., & Malawska, B. (2015). Recent development of multifunctional agents as potential drug candidates for the treatment of Alzheimer's disease. Current Medicinal Chemistry, 22(3), 373–404. https://doi.org/10.2174/0929867321666141106122628
  • Harel, M., Schalk, I., Ehret-Sabatier, L., Bouet, F., Goeldner, M., Hirth, C., Axelsen, P. H., Silman, I., & Sussman, J. L. (1993). Quaternary ligand binding to aromatic residues in the active-site gorge of acetylcholinesterase. Proceedings of the National Academy of Sciences of the United States of America, 90(19), 9031–9035. . https://doi.org/10.1073/pnas.90.19.9031
  • Huang, J., & MacKerell, A. D. Jr. (2013). CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data. Journal of Computational Chemistry, 34(25), 2135–2145. https://doi.org/10.1002/jcc.23354
  • Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14(1), 33–38. https://doi.org/10.1016/0263-7855(96)00018-5
  • Jasiecki, J., Targońska, M., & Wasąg, B. (2021). The role of Butyrylcholinesterase and iron in the regulation of cholinergic network and cognitive dysfunction in Alzheimer’s disease pathogenesis. International Journal of Molecular Sciences, 22(4), 2033. https://doi.org/10.3390/ijms22042033
  • Kabir, M. T., Uddin, M. S., Zaman, S., Begum, Y., Ashraf, G. M., Bin-Jumah, M. N., Bungau, S. G., Mousa, S. A., & Abdel-Daim, M. M. (2021). Molecular mechanisms of metal toxicity in the pathogenesis of Alzheimer’s disease. Molecular Neurobiology, 58(1), 1–20. https://doi.org/10.1007/s12035-020-02096-w
  • Kausar, N., Murtaza, S., Arshad, M. N., Munir, R., Saleem, R. S. Z., Rafique, H., & Tawab, A. (2021). Design, synthesis, structure activity relationship and molecular docking studies of thiophene-2-carboxamide Schiff base derivatives of benzohydrazide as novel acetylcholinesterase and butyrylcholinesterase inhibitors. Journal of Molecular Structure, 1244, 130983. https://doi.org/10.1016/j.molstruc.2021.130983
  • Kausar, N., Murtaza, S., Arshad, M. N., Rashid, R., Asiri, A. M., Javid, N., Asim, M. H., & Ashraf, Z. (2020). Synthesis, characterization, biological evaluation and molecular docking studies of N-functionalized derivatives of 2-aminobenzohydrazide. Journal of Molecular Structure, 1210, 128042. https://doi.org/10.1016/j.molstruc.2020.128042
  • Khachaturian, Z. S. (1985). Diagnosis of Alzheimer's disease. Archives of Neurology, 42(11), 1097–1105. https://doi.org/10.1001/archneur.1985.04060100083029
  • Leopoldini, M., Russo, N., & Toscano, M. (2011). The molecular basis of working mechanism of natural polyphenolic antioxidants. Food Chemistry, 125(2), 288–306. https://doi.org/10.1016/j.foodchem.2010.08.012
  • Lipinski, C. A., Lombardo, F., Dominy, B. W., & Feeney, P. J. (1997). Experimental and computational approaches to estimate solubility and permeability in drug discovery and development settings. Advanced Drug Delivery Reviews, 23(1–3), 3–25. https://doi.org/10.1016/S0169-409X(96)00423-1
  • Liu, G., Huang, W., Moir, R. D., Vanderburg, C. R., Lai, B., Peng, Z., Tanzi, R. E., Rogers, J. T., & Huang, X. (2006). Metal exposure and Alzheimer's pathogenesis. Journal of Structural Biology, 155(1), 45–51. https://doi.org/10.1016/j.jsb.2005.12.011
  • Marco-Contelles, J., Pérez-Mayoral, E., Samadi, A., Carreiras, M. d C., & Soriano, E. (2009). Recent advances in the Friedländer reaction. Chemical Reviews, 109(6), 2652–2671. https://doi.org/10.1021/cr800482c
  • Martínez-Grau, A., & Marco, J. (1997). Friedländer reaction on 2-amino-3-cyano-4H-pyrans: Synthesis of derivatives of 4H-pyran [2,3-b] quinoline, new tacrine analogues. Bioorganic & Medicinal Chemistry Letters, 7(24), 3165–3170. https://doi.org/10.1016/S0960-894X(97)10165-2
  • McEneny-King, A., Osman, W., Edginton, A. N., & Rao, P. P. N. (2017). Cytochrome P450 binding studies of novel tacrine derivatives: Predicting the risk of hepatotoxicity. Bioorganic & Medicinal Chemistry Letters, 27(11), 2443–2449. https://doi.org/10.1016/j.bmcl.2017.04.006
  • Mesulam, M. M., Guillozet, A., Shaw, P., Levey, A., Duysen, E. G., & Lockridge, O. (2002). Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience, 110(4), 627–639. https://doi.org/10.1016/S0306-4522(01)00613-3
  • Munir, R., Zia-Ur-Rehman, M., Murtaza, S., Zaib, S., Javid, N., Awan, S. J., Iftikhar, K., Athar, M. M., & Khan, I. (2021). Microwave-assisted synthesis of (piperidin-1-yl) quinolin-3-yl) methylene) hydrazinecarbothioamides as potent inhibitors of cholinesterases: A biochemical and in silico approach. Molecules, 26(3), 656. https://doi.org/10.3390/molecules26030656
  • Murtaza, S., Mir, K. Z., Tatheer, A., & Ullah, R. S. (2019). Synthesis and evaluation of chalcone and its derivatives as potential anticholinergic agents. Letters in Drug Design & Discovery, 16(3), 322–332. https://doi.org/10.2174/1570180815666180523085436
  • Nachon, F., Carletti, E., Ronco, C., Trovaslet, M., Nicolet, Y., Jean, L., & Renard, P.-Y. (2013). Crystal structures of human cholinesterases in complex with huprine W and tacrine: elements of specificity for anti-Alzheimer's drugs targeting acetyl- and butyryl-cholinesterase . The Biochemical Journal, 453(3), 393–399. https://doi.org/10.1042/BJ20130013
  • Nachon, F., Ehret-Sabatier, L., Loew, D., Colas, C., van Dorsselaer, A., & Goeldner, M. (1998). Trp82 and Tyr332 are involved in two quaternary ammonium binding domains of human butyrylcholinesterase as revealed by photoaffinity labeling with [3H]DDF. Biochemistry, 37(29), 10507–10513. https://doi.org/10.1021/bi980536l
  • O’Brien, P. J., Irwin, W., Diaz, D., Howard-Cofield, E., Krejsa, C. M., Slaughter, M. R., Gao, B., Kaludercic, N., Angeline, A., Bernardi, P., Brain, P., & Hougham, C. (2006). High concordance of drug-induced human hepatotoxicity with in vitro cytotoxicity measured in a novel cell-based model using high content screening. Archives of Toxicology, 80(9), 580–604. https://doi.org/10.1007/s00204-006-0091-3
  • Oset-Gasque, M. J., & Marco-Contelles, J. (2017). New tacrines as Anti-Alzheimer's disease agents. The (Benzo)Chromeno- PyranoTacrines. Current Topics in Medicinal Chemistry, 17(31), 3349–3360. https://doi.org/10.2174/1568026618666180112155928
  • Pandithavidana, D. R., & Jayawardana, S. B. (2019). Comparative study of antioxidant potential of selected dietary vitamins; computational insights. Molecules, 24(9), 1646. https://doi.org/10.3390/molecules24091646
  • Prior, R. L., Wu, X., & Schaich, K. (2005). Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. Journal of Agricultural and Food Chemistry, 53(10), 4290–4302. https://doi.org/10.1021/jf0502698
  • Proctor, G. R., & Harvey, A. L. (2000). Synthesis of tacrine analogues and their structure-activity relationships. Current Medicinal Chemistry, 7(3), 295–302. https://doi.org/10.2174/0929867003375218
  • Przybyłowska, M., Kowalski, S., Dzierzbicka, K., & Inkielewicz-Stepniak, I. (2019). Therapeutic potential of multifunctional tacrine analogues. Current Neuropharmacology, 17(5), 472–490. https://doi.org/10.2174/1570159X16666180412091908
  • Ramírez, D., & Caballero, J. (2016). Is it reliable to use common molecular docking methods for comparing the binding affinities of enantiomer pairs for their protein target? International Journal of Molecular Sciences, 17(4), 525. https://doi.org/10.3390/ijms17040525
  • Romero, A., & Marco-Contelles, J. (2017). Recent developments on multi-target-directed tacrines for Alzheimer's disease. I. The pyranotacrines. Current Topics in Medicinal Chemistry, 17(31), 3328–3335. https://doi.org/10.2174/1568026618666180112155639
  • Sameem, B., Saeedi, M., Mahdavi, M., & Shafiee, A. (2017). A review on tacrine-based scaffolds as multi-target drugs (MTDLs) for Alzheimer's disease. European Journal of Medicinal Chemistry, 128, 332–345. https://doi.org/10.1016/j.ejmech.2016.10.060
  • Sansen, S., Yano, J. K., Reynald, R. L., Schoch, G. A., Griffin, K. J., Stout, C. D., & Johnson, E. F. (2007). Adaptations for the oxidation of polycyclic aromatic hydrocarbons exhibited by the structure of human P450 1A2. The Journal of Biological Chemistry, 282(19), 14348–14355. https://doi.org/10.1074/jbc.M611692200
  • Serrano-Pozo, A., Frosch, M. P., Masliah, E., & Hyman, B. T. (2011). Neuropathological alterations in Alzheimer disease. Cold Spring Harbor Perspectives in Medicine, 1(1), a006189. https://doi.org/10.1101/cshperspect.a006189
  • Shang, Y., Zhou, H., Li, X., Zhou, J., & Chen, K. (2019). Theoretical studies on the antioxidant activity of viniferifuran. New Journal of Chemistry, 43(39), 15736–15742. https://doi.org/10.1039/C9NJ02735A
  • Spaldin, V., Madden, S., Pool, W. F., Woolf, T. F., & Park, B. K. (1994). The effect of enzyme inhibition on the metabolism and activation of tacrine by human liver microsomes. British Journal of Clinical Pharmacology, 38(1), 15–22. https://doi.org/10.1111/j.1365-2125.1994.tb04316.x
  • Sussman, J. L., Harel, M., Frolow, F., Oefner, C., Goldman, A., Toker, L., & Silman, I. (1991). Atomic structure of acetylcholinesterase from Torpedo californica: A prototypic acetylcholine-binding protein. Science (New York, N.Y.), 253(5022), 872–879. https://doi.org/10.1126/science.1678899
  • Trott, O., & Olson, A. J. (2010). AutoDock Vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. Journal of Computational Chemistry, 31(2), 455–461. . https://doi.org/10.1002/jcc.21334
  • Watkins, P. B., Zimmerman, H. J., Knapp, M. J., Gracon, S. I., & Lewis, K. W. (1994). Hepatotoxic effects of tacrine administration in patients with Alzheimer's disease. JAMA, 271(13), 992–998. https://doi.org/10.1001/jama.1994.03510370044030. https://doi.org/10.1001/jama.1994.03510370044030
  • Wright, J. S., Johnson, E. R., & DiLabio, G. A. (2001). Predicting the activity of phenolic antioxidants: Theoretical method, analysis of substituent effects, and application to major families of antioxidants. Journal of the American Chemical Society, 123(6), 1173–1183. https://doi.org/10.1021/ja002455u
  • Xiong, G., Wu, Z., Yi, J., Fu, L., Yang, Z., Hsieh, C., Yin, M., Zeng, X., Wu, C., Lu, A., Chen, X., Hou, T., & Cao, D. (2021). ADMETlab 2.0: An integrated online platform for accurate and comprehensive predictions of ADMET properties. Nucleic Acids Research, 49(W1), W5–W14. https://doi.org/10.1093/nar/gkab255
  • Zhao, Y., & Truhlar, D. G. (2008). The M06 suite of density functionals for main group thermochemistry, thermochemical kinetics, noncovalent interactions, excited states, and transition elements: Two new functionals and systematic testing of four M06-class functionals and 12 other functionals. Theoretical Chemistry Accounts, 120(1-3), 215–241. https://doi.org/10.1007/s00214-007-0310-x
  • Zhou, H., Li, X., Shang, Y., & Chen, K. (2019). Radical scavenging activity of puerarin: A theoretical study. Antioxidants, 8(12), 590. https://doi.org/10.3390/antiox8120590

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.