Abstract
Inhibitors of cholinesterases are a wide group of low molecular weight compounds with a significant role in the current pharmacology. Besides the pharmacological importance, they are also known as toxic compounds like military nerve agents. In the pharmacology, drugs for Alzheimer disease, myasthenia gravis and prophylaxis of poisoning by nerve agents can be mentioned as the relevant applications. Besides this, anti-inflammation and antiphrastic drugs are other pharmacological applications of these inhibitors. This review is focused on a survey of cholinesterase inhibitors with known or expected pharmacological impact and indications of their use. Recent literature with comments is provided here as well.
Keywords: Acetylcholinesterase, Alzheimer disease, butyrylcholinesterase, myasthenia gravis, cholinergic anti-inflammatory pathway, nerve agents, galantamine, rivastigmine, donepezil, huperzine.
Graphical Abstract
[1]
Masson, P.; Froment, M.T.; Fortier, P.L.; Visicchio, J.E.; Bartels, C.F.; Lockridge, O. Butyrylcholinesterase-catalysed hydrolysis of aspirin, a negatively charged ester, and aspirin-related neutral esters. Biochim. Biophys. Acta, 1998, 8, 1-2.
[2]
Shram, M.J.; Cohen-Barak, O.; Chakraborty, B.; Bassan, M.; Schoedel, K.A.; Hallak, H.; Eyal, E.; Weiss, S.; Gilgun-Serki, Y.; Sellers, E.M.; Faulknor, J.; Spiegelstein, O. Assessment of pharmacokinetic and pharmacodynamic interactions between albumin-fused mutated butyrylcholinesterase and intravenously administered cocaine in recreational cocaine users. J. Clin. Psychopharmacol., 2015, 35(4), 396-405.
[3]
Hyatt, J.L.; Moak, T.; Hatfield, M.J.; Tsurkan, L.; Edwards, C.C.; Wierdl, M.; Danks, M.K.; Wadkins, R.M.; Potter, P.M. Selective inhibition of carboxylesterases by isatins, indole-2,3-diones. J. Med. Chem., 2007, 50(8), 1876-1885.
[4]
Pohanka, M. Butyrylcholinesterase as a biochemical marker, a review. Brat. Med. J., 2013, 114(12), 726-734.
[5]
Pohanka, M. Cholinesterases, a target of pharmacology and toxicology. Biomed. Pap. Olomouc, 2011, 155(3), 219-229.
[6]
Klinkerberg, I.; Sambeth, A.; Blokland, A. Acetylcholine and attention. Behav. Brain Res., 2011, 221(2), 430-442.
[7]
Campoy, F.J.; Vidal, C.J.; Munoz-Delgado, E.; Montenegro, M.F.; Cabezas-Herrera, J.; Nieto-Ceron, S. Cholinergic system and cell proliferation. Chem. Biol. Interact., 2016, 259(Pt B), 257-265.
[8]
Lewartowski, B.; Mackiewicz, U. The non-neuronal heart’s acetylcholine in health and disease. J. Physiol. Pharmacol., 2015, 66(6), 773-778.
[9]
Pohanka, M. Alpha7 nicotinic acetylcholine receptor is a target in pharmacology and toxicology. Int. J. Mol. Sci., 2012, 13(2), 2219-2238.
[10]
Tessier, C.J.G.; Emlaw, J.R.; Cao, Z.Q.; Javier Perez-Areales, F.; Salameh, J.J.; Prinston, J.E.; McNulty, M.S.; daCosta, C.J.B. Back to the future: Rational maps for exploring acetylcholine receptor space and time. Biochim. Biophys. Acta, 2017, 24(17), 30186-30183.
[11]
Changeux, J.P. The nicotinic acetylcholine receptor: The founding father of the pentameric ligand-gated ion channel superfamily. J. Biol. Chem., 2012, 287(48), 40207-40215.
[12]
De Angelis, F.; Tata, A.M. Analgesic effects mediated by muscarinic receptors: Mechanisms and pharmacological approaches. Cent. Nerv. Syst. Agents Med. Chem., 2016, 16(3), 218-226.
[14]
Dutta, S.R.; Passi, D.; Singh, M.; Singh, P.; Sharma, S.; Sharma, A. Botulinum toxin the poison that heals: A brief review. Natl. J. Maxillofac. Surg., 2016, 7(1), 10-16.
[15]
Ramirez-Castaneda, J.; Jankovic, J.; Comella, C.; Dashtipour, K.; Fernandez, H.H.; Mari, Z. Diffusion, spread, and migration of botulinum toxin. Mov. Disord., 2013, 28(13), 1775-1783.
[16]
Wheeler, A.; Smith, H.S. Botulinum toxins: Mechanisms of action, antinociception and clinical applications. Toxicology, 2013, 306, 124-146.
[17]
Petroianu, G.A. Pharmacists adolf schall and ernst ratzlaff and the synthesis of tabun-like compounds: A brief history. Pharmazie, 2014, 69(10), 780-784.
[18]
Lopez-Munoz, F.; Garcia-Garcia, P.; Alamo, C. The pharmaceutical industry and the german national socialist regime: Ig farben and pharmacological research. J. Clin. Pharm. Ther., 2009, 34(1), 67-77.
[19]
Mashkovsky, M.D.; Kruglikova-Lvova, R.P. On the pharmacology of the new alkaloid galantamine. Farmakologiea Toxicologia (Moscow), 1951, 14, 27-30.
[20]
Rainer, M. Galanthamine in alzheimer’s disease - a new alternative to tacrine? CNS Drugs, 1997, 7(2), 89-97.
[21]
Crismon, M.L. Tacrine: First drug approved for alzheimer’s disease. Ann. Pharmacother., 1994, 28(6), 744-751.
[22]
Bell, C.; Gershon, S. Experimental anticholinergic psychoto-mimetics - antagonism of yohimbine + tacrine (tha). Med. Experiment., 1964, 10(1), 15.
[23]
Delalande, I.S.; Porter, R.B. Actions of tacrine and amiphenazole on acetylcholine metabolims in guinea pig ileum. Aust. J. Exp. Biol. Med. Sci., 1963, 41(2), 149.
[24]
Pope, C.N.; Brimijoin, S. Cholinesterases and the fine line between poison and remedy. Biochem. Pharmacol., 2018, 31(18), 30050-30059.
[25]
Triantafylidis, L.K.; Clemons, J.S.; Peron, E.P.; Roefaro, J.; Zimmerman, K.M. Brain over bladder: A systematic review of dual cholinesterase inhibitor and urinary anticholinergic use. Drugs Aging, 2018, 35(1), 27-41.
[26]
Bourne, Y.; Marchot, P. Hot spots for protein partnerships at the surface of cholinesterases and related alpha/beta hydrolase fold proteins or domains-a structural perspective. Molecules, 2017, 23(1), 35.
[27]
Sahoo, A.K.; Dandapat, J.; Dash, U.C.; Kanhar, S. Features and outcomes of drugs for combination therapy as multi-targets strategy to combat alzheimer’s disease. J. Ethnopharmacol., 2018, 215, 42-73.
[28]
Renn, B.N.; Asghar-Ali, A.A.; Thielke, S.; Catic, A.; Martini, S.R.; Mitchell, B.G.; Kunik, M.E. A systematic review of practice guidelines and recommendations for discontinuation of cholinesterase inhibitors in dementia. Am. J. Geriatr. Psychiatry, 2018, 26(2), 134-147.
[29]
Khoury, R.; Patel, K.; Gold, J.; Hinds, S.; Grossberg, G.T. Recent progress in the pharmacotherapy of alzheimer’s disease. Drugs Aging, 2017, 34(11), 811-820.
[30]
Panek, D.; Wichur, T.; Godyn, J.; Pasieka, A.; Malawska, B. Advances toward multifunctional cholinesterase and beta-amyloid aggregation inhibitors. Future Med. Chem., 2017, 9(15), 1835-1854.
[31]
Mehta, N.; Rodrigues, C.; Lamba, M.; Wu, W.; Bronskill, S.E.; Herrmann, N.; Gill, S.S.; Chan, A.W.; Mason, R.; Day, S.; Gurwitz, J.H.; Rochon, P.A. Systematic review of sex-specific reporting of data: Cholinesterase inhibitor example. J. Am. Geriatr. Soc., 2017, 65(10), 2213-2219.
[32]
Ramsay, R.R.; Tipton, K.F. Assessment of enzyme inhibition: A review with examples from the development of monoamine oxidase and cholinesterase inhibitory drugs. Molecules, 2017, 22(7), 1192.
[33]
Mohammad, D.; Chan, P.; Bradley, J.; Lanctot, K.; Herrmann, N. Acetylcholinesterase inhibitors for treating dementia symptoms - a safety evaluation. Expert Opin. Drug Saf., 2017, 16(9), 1009-1019.
[34]
Masson, P.; Nachon, F. Cholinesterase reactivators and bioscavengers for pre- and post-exposure treatments of organophosphorus poisoning. J. Neurochem., 2017, 2, 26-40.
[35]
Knez, D.; Sova, M.; Kosak, U.; Gobec, S. Dual inhibitors of cholinesterases and monoamine oxidases for alzheimer’s disease. Future Med. Chem., 2017, 9(8), 811-832.
[36]
Shafferman, A.; Kronman, C.; Flashner, Y.; Leitner, M.; Grosfeld, H.; Ordentlich, A.; Gozes, Y.; Cohen, S.; Ariel, N.; Barak, D.; Harel, M.; Silman, I.; Sussman, J.L.; Velan, B. Mutagenesis of human acetylcholinesterase. Identification of residues involved in catalytic activity and in polypeptide folding. J. Biol. Chem., 1992, 267(25), 17640-17648.
[37]
Massoulie, J.; Anselmet, A.; Bon, S.; Krejci, E.; Legay, C.; Morel, N.; Simon, S. The polymorphism of acetylcholinesterase: Post-translational processing, quaternary associations and localization. Chem. Biol. Interact., 1999, 120, 29-42.
[38]
Pezzementi, L.; Nachon, F.; Chatonnet, A. Evolution of acetylcholinesterase and butyrylcholinesterase in the vertebrates: An atypical butyrylcholinesterase from the medaka oryzias latipes. PLoS One, 2011, 6(2) 0017396.
[39]
Nawaz, S.A.; Ayaz, M.; Brandt, W.; Wessjohann, L.A.; Westermann, B. Cation-π and π-π stacking interactions allow selective inhibition of butyrylcholinesterase by modified quinine and cinchonidine alkaloids. Biochem. Biophys. Res. Commun., 2011, 404(4), 935-940.
[40]
Pohanka, M. Acetylcholinesterase inhibitors: A patent review (2008 - present). Expert Opin. Ther. Pat., 2012, 22(8), 871-886.
[41]
Johnson, G.; Moore, S.W. The peripheral anionic site of acetylcholinesterase: Structure, functions and potential role in rational drug design. Curr. Pharm. Des., 2006, 12(2), 217-225.
[42]
Saxena, A.; Redman, A.M.; Jiang, X.; Lockridge, O.; Doctor, B.P. Differences in active site gorge dimensions of cholinesterases revealed by binding of inhibitors to human butyrylcholinesterase. Biochemistry, 1997, 36(48), 14642-14651.
[43]
Cometa, M.F.; Lorenzini, P.; Fortuna, S.; Volpe, M.T.; Meneguz, A.; Palmery, M. In vitro inhibitory effect of aflatoxin b-1 on acetylcholinesterase activity in mouse brain. Toxicology, 2005, 206(1), 125-135.
[44]
Stepurska, K.V.; Soldatkin, O.O.; Arkhypova, V.M.; Soldatkin, A.P.; Lagarde, F.; Jaffrezic-Renault, N.; Dzyadevych, S.V. Development of novel enzyme potentiometric biosensor based on ph-sensitive field-effect transistors for aflatoxin b1 analysis in real samples. Talanta, 2015, 144, 1079-1084.
[45]
Cavalli, A.; Bottegoni, G.; Raco, C.; De Vivo, M.; Recanatini, M. A computational study of the binding of propidium to the peripheral anionic site of human acetylcholinesterase. J. Med. Chem., 2004, 47(16), 3991-3999.
[46]
Mazzanti, C.M.; Spanevello, R.M.; Obregon, A.; Pereira, L.B.; Streher, C.A.; Ahmed, M.; Mazzanti, A.; Graca, D.L.; Morsch, V.M.; Schetinger, M.R. Ethidium bromide inhibits rat brain acetylcholinesterase activity in vitro. Chem. Biol. Interact., 2006, 162(2), 121-127.
[47]
Holtje, H.D.; Kjier, L.B. Nature of anionic or alpha-site of cholinesterase. J. Pharm. Sci., 1975, 64(3), 418-420.
[48]
Gilson, M.K.; Straatsma, T.P.; McCammon, J.A.; Ripoll, D.R.; Faerman, C.H.; Axelsen, P.H.; Silman, I.; Sussman, J.L. Open “back door” in a molecular dynamics simulation of acetylcholinesterase. Science, 1994, 263(5151), 1276-1278.
[49]
Boopathy, R.; Rajesh, R.V.; Darvesh, S.; Layer, P.G. Human serum cholinesterase from liver pathological samples exhibit highly elevated aryl acylamidase activity. Clin. Chim. Acta, 2007, 380, 151-156.
[50]
Montenegro, M.F.; Maria, T.M.; de la Cadena, M.P.; Campoy, F.J.; Munoz-Delgado, E.; Vidal, C.J. Human butyrylcholinesterase components differ in aryl acylamidase activity. Biol. Chem., 2008, 389(4), 425-432.
[51]
Berg, L.; Andersson, C.D.; Artursson, E.; Hornberg, A.; Tunemalm, A.K.; Linusson, A.; Ekstrom, F. Targeting acetylcholinesterase: Identification of chemical leads by high throughput screening, structure determination and molecular modeling. PLoS One, 2011, 6(11) e26039.
[52]
Cheewakriengkrai, L.; Gauthier, S. A 10-year perspective on donepezil. Expert Opin. Pharmacother., 2013, 14(3), 331-338.
[53]
Rampa, A.; Belluti, F.; Gobbi, S.; Bisi, A. Hybrid-based multi-target ligands for the treatment of alzheimer’s disease. Curr. Top. Med. Chem., 2011, 11(22), 2716-2730.
[54]
Bai, D.L.; Tang, X.C.; He, X.C. Huperzine a, a potential therapeutic agent for treatment of alzheimer’s disease. Curr. Med. Chem., 2000, 7(3), 355-374.
[55]
Liu, J.; Zhang, H.Y.; Tang, X.C.; Wang, B.; He, X.C.; Bai, D.L. Effects of synthetic (-)-huperzine a on cholinesterase activities and mouse water maze performance. Zhongguo Yao Li Xue Bao, 1998, 19(5), 413-416.
[56]
Luo, W.; Li, Y.P.; He, Y.; Huang, S.L.; Li, D.; Gu, L.Q.; Huang, Z.S. Synthesis and evaluation of heterobivalent tacrine derivatives as potential multi-functional anti-alzheimer agents. Eur. J. Med. Chem., 2011, 46(6), 2609-2616.
[57]
Jogani, V.V.; Shah, P.J.; Mishra, P.; Mishra, A.K.; Misra, A.R. Nose-to-brain delivery of tacrine. J. Pharm. Pharmacol., 2007, 59(9), 1199-1205.
[58]
Knapp, M.J.; Gracon, S.I.; Davis, C.S.; Solomon, P.R.; Pendlebury, W.W.; Knopman, D.S. Efficacy and safety of high-dose tacrine - a 30 week evaluation Alzheimer Dis. Assoc. Dis., 1994, 8, S22-S31.
[59]
Davis, K.L.; Thal, L.J.; Gamzu, E.R.; Davis, C.S.; Woolson, R.F.; Gracon, S.I.; Drachman, D.A.; Schneider, L.S.; Whitehouse, P.J.; Hoover, T.M.; Morris, J.C.; Kawas, C.H.; Knopman, D.S.; Earl, N.L.; Kumar, V.; Doody, R.S. A double-blind, placebo-controlled multicenter study of tacrine for alzheimers-disease. N. Engl. J. Med., 1992, 327(18), 1253-1259.
[60]
Pohanka, M. Spectrophotomeric assay of aflatoxin b1 using acetylcholinesterase immobilized on standard microplates. Anal. Lett., 2013, 46(8), 1306-1315.
[61]
Arduini, F.; Amine, A.; Moscone, D.; Palleschi, G. Biosensors based on cholinesterase inhibition for insecticides, nerve agents and aflatoxin b-1 detection (review). Microchim. Acta, 2010, 170(3-4), 193-214.
[62]
Pohanka, M.; Dobes, P. Caffeine inhibits acetylcholinesterase, but not butyrylcholinesterase. Int. J. Mol. Sci., 2013, 14, 9873-9882.
[63]
Pohanka, M. The effects of caffeine on the cholinergic system. Mini Rev. Med. Chem., 2014, 16(6), 543-549.
[64]
da Silva, V.B.; de Andrade, P.; Kawano, D.F.; Morais, P.A.B.; de Almeida, J.R.; Carvalho, I.; Taft, C.A.; da Silva, C. In silico design and search for acetylcholinesterase inhibitors in alzheimer’s disease with a suitable pharmacokinetic profile and low toxicity. Future Med. Chem., 2011, 3(8), 947-960.
[65]
Lilienfeld, S. Galantamine - a novel cholinergic drug with a unique dual mode of action for the treatment of patients with alzheimer’s disease. CNS Drug. Rev., 2002, 8(2), 159-176.
[66]
Darreh-Shori, T.; Soininen, H. Effects of cholinesterase inhibitors on the activities and protein levels of cholinesterases in the cerebrospinal fluid of patients with alzheimer’s disease: A review of recent clinical studies. Curr. Alzheimer Res., 2010, 7(1), 67-73.
[67]
Thomsen, T.; Kewitz, H. Selective inhibition of human acetylcholinesterase by galanthamine in vitro and in vivo. Life Sci., 1990, 46(21), 1553-1558.
[68]
Jokanovic, M. Medical treatment of acute poisoning with organophosphorus and carbamate pesticides. Toxicol. Lett., 2009, 190(2), 107-115.
[69]
Colovic, M.B.; Krstic, D.Z.; Lazarevic-Pasti, T.D.; Bondzic, A.M.; Vasic, V.M. Acetylcholinesterase inhibitors: Pharmacology and toxicology. Curr. Neuropharmacol., 2013, 11(3), 315-335.
[70]
Darvesh, S.; Darvesh, K.V.; McDonald, R.S.; Mataija, D.; Walsh, R.; Mothana, S.; Lockridge, O.; Martin, E. Carbamates with differential mechanism of inhibition toward acetylcholinesterase and butyrylcholinesterase. J. Med. Chem., 2008, 51(14), 4200-4212.
[71]
Marrs, T.C.; Maynard, R.L. Neurotranmission systems as targets for toxicants: A review. Cell Biol. Toxicol., 2013, 29(6), 381-396.
[72]
Kalasz, H.; Nurulain, S.M.; Veress, G.; Antus, S.; Darvas, F.; Adeghate, E.; Adem, A.; Hashemi, F.; Tekes, K. Mini review on blood-brain barrier penetration of pyridinium aldoximes. J. Appl. Toxicol., 2015, 35(2), 116-123.
[73]
Costantino, H.R.; Leonard, A.K.; Brandt, G.; Johnson, P.H.; Quay, S.C. Intranasal administration of acetylcholinesterase inhibitors. BMC Neurosci., 2008, 10(9), 1471-2202.
[74]
Worek, F.; Thiermann, H. The value of novel oximes for treatment of poisoning by organophosphorus compounds. Pharmacol. Ther., 2013, 139(2), 249-259.
[75]
Alfirevic, A.; Mills, T.; Carr, D.; Barratt, B.J.; Jawaid, A.; Sherwood, J.; Smith, J.C.; Tugwood, J.; Hartkoorn, R.; Owen, A.; Park, K.B.; Pirmohamed, M. Tacrine-induced liver damage: An analysis of 19 candidate genes. Pharmacogenet. Genomics, 2007, 17(12), 1091-1100.
[77]
Crane, P.K.; Trittschuh, E.; Mukherjee, S.; Saykin, A.J.; Sanders, R.E.; Larson, E.B.; McCurry, S.M.; McCormick, W.; Bowen, J.D.; Grabowski, T.; Moore, M.; Bauman, J.; Gross, A.L.; Keene, C.D.; Bird, T.D.; Gibbons, L.E.; Mez, J. Incidence of cognitively defined late-onset alzheimer’s dementia subgroups from a prospective cohort study. Alzheimers Dement., 2017, 15(17), 30216-30219.
[78]
Kukull, W.A.; Higdon, R.; Bowen, J.D.; McCormick, W.C.; Teri, L.; Schellenberg, G.D.; van Belle, G.; Jolley, L.; Larson, E.B. Dementia and alzheimer disease incidence: A prospective cohort study. Arch. Neurol., 2002, 59(11), 1737-1746.
[79]
Lobo, A.; Lopez-Anton, R.; Santabarbara, J.; de-la-Camara, C.; Ventura, T.; Quintanilla, M.A.; Roy, J.F.; Campayo, A.J.; Lobo, E.; Palomo, T.; Rodriquez-Jimenez, R.; Saz, P.; Marcos, G. Incidence and lifetime risk of dementia and alzheimer’s disease in a southern european population. Acta Psychiatr. Scand., 2011, 124(5), 372-383.
[80]
Dimitrov, I.; Tzourio, C.; Milanov, I.; Deleva, N.; Traykov, L. Prevalence of dementia and mild cognitive impairment in a bulgarian urban population. Am. J. Alzheimers Dis. Other Demen., 2012, 27(2), 131-135.
[81]
Himmelstein, D.S.; Ward, S.M.; Lancia, J.K.; Patterson, K.R.; Binder, L.I. Tau as a therapeutic target in neurodegenerative disease. Pharmacol. Ther., 2012, 136(1), 8-22.
[82]
Pohanka, M. Alzheimer’s disease and oxidative stress. A review. Curr. Med. Chem., 2014, 21(3), 356-364.
[83]
Hamlett, E.D.; Ledreux, A.; Potter, H.; Chial, H.J.; Patterson, D.; Espinosa, J.M.; Bettcher, B.M.; Granholm, A.C. Exosomal biomarkers in down syndrome and alzheimer's disease. Free Radic. Biol. Med., 2017, 5(17), 028.
[84]
He, J.; Liao, T.; Zhong, G.X.; Zhang, J.D.; Chen, Y.P.; Wang, Q.; Zeng, Q.P. Alzheimer‘s disease-like early-phase brain pathogenesis: Self-curing amelioration of neurodegeneration from pro-inflammatory ’wounding’ to anti-inflammatory ‘healing’. Curr. Alzheimer Res., 2017, 17(10) 1567205014666170417111420.
[85]
Pouryamout, L.; Dams, J.; Wasem, J.; Dodel, R.; Neumann, A. Economic evaluation of treatment options in patients with alzheimer’s disease: A systematic review of cost-effectiveness analyses. Drugs, 2012, 72(6), 789-802.
[86]
Patel, L.; Grossberg, G.T. Combination therapy for alzheimer’s disease. Drugs Aging, 2011, 28(7), 539-546.
[87]
Ehret, M.J.; Chamberlin, K.W. Current practices in the treatment of alzheimer disease: Where is the evidence after the phase iii trials? Clin. Ther., 2015, 37(8), 1604-1616.
[88]
Deardorff, W.J.; Feen, E.; Grossberg, G.T. The use of cholinesterase inhibitors across all stages of alzheimer’s disease. Drugs Aging, 2015, 32(7), 537-547.
[89]
Pohanka, M. Vaccination to alzheimer disease. Is it a promising tool or a blind way? Curr. Med. Chem., 2016, 23(14), 1432-1441.
[90]
Sterner, R.M.; Takahashi, P.Y.; Yu Ballard, A.C. Active vaccines for alzheimer disease treatment. J. Am. Med. Dir. Assoc., 2016, 17(9), 25.
[91]
Hartig, W.; Saul, A.; Kacza, J.; Grosche, J.; Goldhammer, S.; Michalski, D.; Wirths, O. Immunolesion-induced loss of cholinergic projection neurones promotes beta-amyloidosis and tau hyperphosphorylation in the hippocampus of triple-transgenic mice. Neuropathol. Appl. Neurobiol., 2014, 40(2), 106-120.
[92]
Abdel-Salam, O.M. Stem cell therapy for alzheimer’s disease. CNS Neurol. Disord. Drug Targets, 2011, 10(4), 459-485.
[93]
Hiremathad, A.; Piemontese, L. Heterocyclic compounds as key structures for the interaction with old and new targets in alzheimer’s disease therapy. Neural Regen. Res., 2017, 12(8), 1256-1261.
[94]
Makhaeva, G.F.; Lushchekina, S.V.; Boltneva, N.P.; Serebryakova, O.G.; Rudakova, E.V.; Ustyugov, A.A.; Bachurin, S.O.; Shchepochkin, A.V.; Chupakhin, O.N.; Charushin, V.N.; Richardson, R.J. 9-substituted acridine derivatives as acetylcholinesterase and butyrylcholinesterase inhibitors possessing antioxidant activity for alzheimer’s disease treatment. Bioorg. Med. Chem., 2017, 20(17), 31509-31502.
[95]
Skibinski, R.; Czarnecka, K.; Girek, M.; Bilichowski, I.; Chufarova, N.; Mikiciuk-Olasik, E.; Szymanski, P. Novel tetrahydroacridine derivatives with iodobenzoic acid moiety as multifunctional acetylcholinesterase inhibitors. Chem. Biol. Drug Des., 2017, 25(10), 13111.
[96]
Teponnou, G.A.K.; Joubert, J.; Malan, S.F. Tacrine, trolox and tryptoline as lead compounds for the design and synthesis of multi-target agents for alzheimer’s disease therapy. Open Med. Chem. J., 2017, 11, 24-37.
[97]
Boulebd, H.; Ismaili, L.; Bartolini, M.; Bouraiou, A.; Andrisano, V.; Martin, H.; Bonet, A.; Moraleda, I.; Iriepa, I.; Chioua, M.; Belfaitah, A.; Marco-Contelles, J. Imidazopyranotacrines as non-hepatotoxic, selective acetylcholinesterase inhibitors, and antioxidant agents for alzheimer’s disease therapy. Molecules, 2016, 21(4), 400.
[98]
Unzeta, M.; Esteban, G.; Bolea, I.; Fogel, W.A.; Ramsay, R.R.; Youdim, M.B.; Tipton, K.F.; Marco-Contelles, J. Multi-target directed donepezil-like ligands for alzheimer’s disease. Front. Neurosci., 2016, 10, 205.
[99]
Bautista-Aguilera, O.M.; Esteban, G.; Bolea, I.; Nikolic, K.; Agbaba, D.; Moraleda, I.; Iriepa, I.; Samadi, A.; Soriano, E.; Unzeta, M.; Marco-Contelles, J. Design, synthesis, pharmacological evaluation, qsar analysis, molecular modeling and admet of novel donepezil-indolyl hybrids as multipotent cholinesterase/monoamine oxidase inhibitors for the potential treatment of alzheimer’s disease. Eur. J. Med. Chem., 2014, 75, 82-95.
[100]
Palanimuthu, D.; Poon, R.; Sahni, S.; Anjum, R.; Hibbs, D.; Lin, H.Y.; Bernhardt, P.V.; Kalinowski, D.S.; Richardson, D.R. A novel class of thiosemicarbazones show multi-functional activity for the treatment of alzheimer’s disease. Eur. J. Med. Chem., 2017, 139, 612-632.
[101]
Luo, L.; Li, Y.; Qiang, X.; Cao, Z.; Xu, R.; Yang, X.; Xiao, G.; Song, Q.; Tan, Z.; Deng, Y. Multifunctional thioxanthone derivatives with acetylcholinesterase, monoamine oxidases and beta-amyloid aggregation inhibitory activities as potential agents against alzheimer’s disease. Bioorg. Med. Chem., 2017, 25(6), 1997-2009.
[102]
Xiao, G.; Li, Y.; Qiang, X.; Xu, R.; Zheng, Y.; Cao, Z.; Luo, L.; Yang, X.; Sang, Z.; Su, F.; Deng, Y. Design, synthesis and biological evaluation of 4′-aminochalcone-rivastigmine hybrids as multifunctional agents for the treatment of alzheimer’s disease. Bioorg. Med. Chem., 2017, 25(3), 1030-1041.
[103]
Sturm, A.; Hansen, P. Altered cholinesterase and monooxygenase levels in daphnia magna and chironomus riparius exposed to environmental pollutants. Ecotoxicol. Environ. Saf., 1999, 42(1), 9-15.
[104]
Mutch, E.; Daly, A.K.; Leathart, J.B.; Blain, P.G.; Williams, F.M. Do multiple cytochrome p450 isoforms contribute to parathion metabolism in man? Arch. Toxicol., 2003, 77(6), 313-320.
[105]
Jan, Y.H.; Richardson, J.R.; Baker, A.A.; Mishin, V.; Heck, D.E.; Laskin, D.L.; Laskin, J.D. Novel approaches to mitigating parathion toxicity: Targeting cytochrome p450-mediated metabolism with menadione. Ann. N. Y. Acad. Sci., 2016, 1, 80-86.
[106]
Buratti, F.M.; Testai, E. Evidences for cyp3a4 autoactivation in the desulfuration of dimethoate by the human liver. Toxicology, 2007, 241(1-2), 33-46.
[108]
Pohanka, M.; Novotny, L.; Pikula, J. Metrifonate alters antioxidant levels and caspase activity in cerebral cortex of wistar rats. Toxicol. Mech. Method., 2011, 21(8), 585-590.
[109]
Nordberg, A.; Svensson, A.L. Cholinesterase inhibitors in the treatment of alzheimer’s disease - a comparison of tolerability and pharmacology. Drug Saf., 1998, 19(6), 465-480.
[110]
López-Arrieta, J.M.; Schneider, L. Metrifonate for alzheimer’s disease. Cochrane Database Syst. Rev., 2006, (2) CD003155.
[111]
Cummings, J.L.; Nadel, A.; Masterman, D.; Cyrus, P.A. Efficacy of metrifonate in improving the psychiatric and behavioral disturbances of patients with alzheimer’s disease. J. Geriatr. Psychiatry Neurol., 2001, 14(2), 101-108.
[112]
Mirck, M.H. Use of trichlorfon as an anthelmintic in horses. Tijdschr. Diergeneeskd., 1980, 105(14), 564-566.
[113]
Lopes, W.D.; dos Santos, T.R.; Borges Fde, A.; Sakamoto, C.A.; Soares, V.E.; Costa, G.H.; Camargo, G.; Pulga, M.E.; Bhushan, C.; da Costa, A.J. Anthelmintic efficacy of oral trichlorfon solution against ivermectin resistant nematode strains in cattle. Vet. Parasitol., 2009, 166(1-2), 98-102.
[114]
Fiel, C.; Guzman, M.; Steffan, P.; Rodriguez, E.; Prieto, O.; Bhushan, C. The efficacy of trichlorphon and naphthalophos against multiple anthelmintic-resistant nematodes of naturally infected sheep in argentina. Parasitol. Res., 2011, 109(1), 011-2410.
[115]
Lopez-Arias, A.; Villar-Argaiz, D.; Chaparro-Gutierrez, J.J.; Miller, R.J.; Perez de Leon, A.A. Reduced efficacy of commercial acaricides against populations of resistant cattle tick rhipicephalus microplus from two municipalities of antioquia, colombia. Environ. Health Insights, 2015, 8(Suppl. 2), 71-80.
[116]
Fernandes, L.S.; Emerick, G.L.; dos Santos, N.A.; de Paula, E.S.; Barbosa, F., Jr.; dos Santos, A.C. In vitro study of the neuropathic potential of the organophosphorus compounds trichlorfon and acephate. Toxicol. In Vitro, 2015, 29(3), 522-528.
[117]
Martin, R.J.; Puttachary, S.; Buxton, S.K.; Verma, S.; Robertson, A.P. The conqueror worm: Recent advances with cholinergic anthelmintics and techniques excite research for better therapeutic drugs. J. Helminthol., 2015, 89(4), 387-397.
[118]
Zinser, E.W.; Wolf, M.L.; Alexander-Bowman, S.J.; Thomas, E.M.; Davis, J.P.; Groppi, V.E.; Lee, B.H.; Thompson, D.P.; Geary, T.G. Anthelmintic paraherquamides are cholinergic antagonists in gastrointestinal nematodes and mammals. J. Vet. Pharmacol. Ther., 2002, 25(4), 241-250.
[119]
Aas, P. In vitro effects of toxogonin, hi-6 and hlö-7 on the release of [3h]acetylcholine from peripheral cholinergic nerves in rat airway smooth muscle. Eur. J. Pharmacol., 1996, 301(1-3), 59-66.
[120]
Cetkovic, S.; Cvetkovic, M.; Jandric, D.; Cosic, M.; Boskovic, B. Effect of pam-2 cl, hi-6, and hgg-12 in poisoning by tabun and its thiocholine-like analog in the rat. Fundam. Appl. Toxicol., 1984, 4(2), S116-S123.
[121]
Nyberg, A.G.; Cassel, G.; Jeneskog, T.; Karlsson, L.; Larsson, R.; Lundstrom, M.; Palmer, L.; Persson, S.A. Pharmacokinetics of hi-6 and atropine in anesthetized pigs after administration by a new autoinjector. Biopharm. Drug Dispos., 1995, 16(8), 635-651.
[122]
Crenshaw, M.D.; Hayes, T.L.; Miller, T.L.; Shannon, C.M. Comparison of the hydrolytic stability of s-(n,n-diethylaminoethyl) isobutyl methylphosphonothiolate with vx in dilute solution. J. Appl. Toxicol., 2001, 21, S3-S6.
[123]
Dejong, L.P.A.; Vandijk, C.; Berhitoe, D.; Benschop, H.P. Hydrolysis and binding of a toxic stereoisomer of soman in plasma and tissue-homogentaes from rat, guinea-pig and marmoset, and in human plasma. Biochem. Pharmacol., 1993, 46(8), 1413-1419.
[124]
Tuovinen, K.; Kaliste-Korhonen, E.; Raushel, F.M.; Hanninen, O. Success of pyridostigmine, physostigmine, eptastigmine and phosphotriesterase treatments in acute sarin intoxication. Toxicology, 1999, 134(2-3), 169-178.
[125]
Cho, Y.; Kim, W.S.; Hur, G.H.; Ha, Y.C. Minimum effective drug concentrations of a transdermal patch system containing procyclidine and physostigmine for prophylaxis against soman poisoning in rhesus monkeys. Environ. Toxicol. Pharmacol., 2012, 33(1), 1-8.
[126]
Lamproglou, I.; Barbier, L.; Diserbo, M.; Fauvelle, F.; Fauquette, W.; Amourette, C. Repeated stress in combination with pyridostigmine part i: Long-term behavioural consequences. Behav. Brain Res., 2009, 197(2), 301-310.
[127]
Gordon, R.K.; Haigh, J.R.; Garcia, G.E.; Feaster, S.R.; Riel, M.A.; Lenz, D.E.; Aisen, P.S.; Doctor, B.P. Oral administration of pyridostigmine bromide and huperzine a protects human whole blood cholinesterases from ex vivo exposure to soman. Chem. Biol. Interact., 2005, 157, 239-246.
[128]
Golomb, B.A. Acetylcholinesterase inhibitors and gulf war illnesses. Proc. Natl. Acad. Sci. U. S. A., 2008, 105(11), 4295-4300.
[129]
Auxemery, Y. The gulf war syndrome twenty years on. Enceph.-. Rev. Psychiatr. Clin. Biol. Ther., 2013, 39(5), 332-338.
[130]
Dubovicky, M.; Paton, S.; Morris, M.; Mach, M.; Lucot, J.B. Effects of combined exposure to pyridostigmine bromide and shaker stress on acoustic startle response, pre-pulse inhibition and open field behavior in mice. J. Appl. Toxicol., 2007, 27(3), 276-283.
[131]
Romi, F.; Hong, Y.; Gilhus, N.E. Pathophysiology and immunological profile of myasthenia gravis and its subgroups. Curr. Opin. Immunol., 2017, 49, 9-13.
[132]
Hehir, M.K.; Hobson-Webb, L.D.; Benatar, M.; Barnett, C.; Silvestri, N.J.; Howard, J.F., Jr; Howard, D.; Visser, A.; Crum, B.A.; Nowak, R.; Beekman, R.; Kumar, A.; Ruzhansky, K.; Chen, I.A.; Pulley, M.T.; LaBoy, S.M.; Fellman, M.A.; Greene, S.M.; Pasnoor, M.; Burns, T.M. Rituximab as treatment for anti-musk myasthenia gravis: Multicenter blinded prospective review. Neurology, 2017, 89(10), 1069-1077.
[133]
Muto, K.; Matsui, N.; Unai, Y.; Sakai, W.; Haji, S.; Udaka, K.; Miki, H.; Furukawa, T.; Abe, M.; Kaji, R. Memory b cell resurgence requires repeated rituximab in myasthenia gravis. Neuromuscul. Disord., 2017, 27(10), 918-922.
[134]
Alkhawajah, N.M.; Oger, J. Treatment of myasthenia gravis in the aged. Drugs Aging, 2015, 32(9), 689-697.
[135]
Khan, M.S.; Tiwari, A.; Khan, Z.; Sharma, H.; Taleb, M.; Hammersley, J. Pyridostigmine induced prolonged asystole in a patient with myasthenia gravis successfully treated with hyoscyamine. Case Rep. Cardiol., 2017, 6956298(10), 14.
[136]
Patil, S.A.; Bokoliya, S.C.; Nagappa, M.; Taly, A.B. Diagnosis of myasthenia gravis: Comparison of anti-nicotinic acetyl choline receptor antibodies, repetitive nerve stimulation and neostigmine tests at a tertiary neuro care centre in india, a ten year study. J. Neuroimmunol., 2016, 292, 81-84.
[137]
Nazari, F.; Abdi, S. Pyridostigmine-induced bradycardia in patient with musk-ab-positive myasthenia gravis and alopecia universalis. J. Clin. Neuromuscul. Dis., 2017, 19(1), 49-50.
[138]
Petrov, K. Macrocyclic derivatives of 6-methyluracil: New ligands of the peripheral anionic site of acetylcholinesterase. Int. J. Risk Saf. Med., 2015, 27(1) JRS-150695.
[139]
Kharlamova, A.D.; Lushchekina, S.V.; Petrov, K.A.; Kots, E.D.; Nachon, F.; Villard-Wandhammer, M.; Zueva, I.V.; Krejci, E.; Reznik, V.S.; Zobov, V.V.; Nikolsky, E.E.; Masson, P. Slow-binding inhibition of acetylcholinesterase by an alkylammonium derivative of 6-methyluracil: Mechanism and possible advantages for myasthenia gravis treatment. Biochem. J., 2016, 473(9), 1225-1236.
[140]
Feng, X.; Wang, X.; Liu, Y.; Di, X. Linarin inhibits the acetylcholinesterase activity in-vitro and ex-vivo. Iran. J. Pharm. Res., 2015, 14(3), 949-954.
[142]
Rosas-Ballina, M.; Tracey, K.J. Cholinergic control of inflammation. J. Intern. Med., 2009, 265(6), 663-679.
[143]
Zabrodskii, P.F.; Lim, V.G.; Shekhter, M.S.; Kuzmin, A.V. Role of nicotinic and muscarinic cholinoreceptors in the realization of the cholinergic anti-inflammatory pathway during the early phase of sepsis. Bull. Exp. Biol. Med., 2012, 153(5), 700-703.
[144]
Tonhajzerova, I.; Mokra, D.; Visnovcova, Z. Vagal function indexed by respiratory sinus arrhythmia and cholinergic anti-inflammatory pathway. Respir. Physiol. Neurobiol., 2013, 187(1), 78-81.
[145]
Noelker, C.; Stuckenholz, V.; Reese, J.P.; Alvarez-Fischer, D.; Sankowski, R.; Rausch, T.; Oertel, W.H.; Hartmann, A.; van Patten, S.; Al-Abed, Y.; Bacher, M. Cni-1493 attenuates neuroinflammation and dopaminergic neurodegeneration in the acute mptp mouse model of parkinson’s disease. Neurodegener. Dis., 2013, 12(2), 103-110.
[146]
Forsythe, P. The nervous system as a critical regulator of immune responses underlying allergy. Curr. Pharm. Des., 2012, 18(16), 2290-2304.
[147]
Song, F.; Zhao, L.; Zhu, R.; Song, Q.; Deng, J.; Tian, R.; Wang, F.; Qian, Y. Protective effect of an alpha 7 nicotinic acetylcholine receptor agonist against enterovirus 71 infection in neuronal cells. Antiviral Res., 2017, 9(17), 30451-30455.
[148]
Pohanka, M. Inhibitors of acetylcholinesterase and butyrylcho-linesterase meet immunity. Int. J. Mol. Sci., 2014, 15(6), 9809-9825.
[149]
Pohanka, M. Caffeine downregulates antibody production in a mouse model. J. Appl. Biomed., 2014. In press
[http://dx.doi.org/10.1016/j.jab.2014.09.001.]
[http://dx.doi.org/10.1016/j.jab.2014.09.001.]
[150]
Pohanka, M. Effect of hi-6 on cytokines production after immunity stimulation by keyhole limpet hemocyanin in a mouse model. Neuroendocrinol. Lett., 2014, 35, 155-157.
[151]
Pohanka, M. Hi-6 modulates immunization efficacy in a balb/c mouse model. Environ. Toxicol. Pharmacol., 2013, 36(3), 801-806.
[152]
Wang, Z.F.; Wang, J.; Zhang, H.Y.; Tang, X.C. Huperzine a exhibits anti-inflammatory and neuroprotective effects in a rat model of transient focal cerebral ischemia. J. Neurochem., 2008, 106(4), 1594-1603.
Related Books
Science of Spices and Culinary Herbs - Latest Laboratory, Pre-clinical, and Clinical Studies
Frontiers in Natural Product Chemistry
Therapeutic Use of Plant Secondary Metabolites
Therapeutic Implications of Natural Bioactive Compounds
Frontiers in Bioactive Compounds
Frontiers in Natural Product Chemistry
Frontiers in Natural Product Chemistry
Science of Spices and Culinary Herbs - Latest Laboratory, Pre-clinical, and Clinical Studies
Frontiers in Natural Product Chemistry
Frontiers in Natural Product Chemistry
Article Metrics
32