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01-04-2020 | Amnesia | Original Article

Amnesia-ameliorative effect of a quinoline derivative through regulation of oxidative/cholinergic systems and Na⁺/K⁺-ATPase activity in mice

Authors: Cristiane Luchese, Ane G. Vogt, Mikaela P. Pinz, Angélica S. dos Reis, Carolina B. Gomes, Diego Alves, Ethel A. Wilhelm

Published in: Metabolic Brain Disease | Issue 4/2020

Abstract

The present study evaluated the anti-amnesic activity of 1-(7-chloroquinolin-4-yl)-5-methyl-N-phenyl-1H-1,2,3-triazole-4-carboxamide (QTCA-1) against scopolamine (SCO)-induced amnesia in mice. It was evaluated cholinergic dysfunction, oxidative stress and Na⁺/K⁺-ATPase activity in cerebral cortex and hippocampus of mice. Male Swiss mice were treated with QTCA-1 (10 mg/kg, intragastrically (i.g.), daily) for nine days. Thirty minutes after the treatment with compound, the animals received a injection of SCO (0.4 mg/kg, intraperitoneally (i.p.)). Mice were submitted to the behavioral tasks 30 min after injection of SCO (Barnes maze, open-field, object recognition and location, and step-down inhibitory avoidance tasks) during nine days. In day 9, cerebral cortex and hippocampus of mice were removed to determine the thiobarbituric acid reactive species (TBARS) levels, and catalase (CAT), Na⁺/K⁺-ATPase and acetylcholinesterase (AChE) activities. SCO caused amnesia in mice for changing in step-down inhibitory avoidance, Barnes maze, and object recognition and object location tasks. QTCA-1 treatment attenuated the behavioral changes caused by SCO. Moreover, SCO increased AChE and CAT activities, decreased Na⁺/K⁺-ATPase activity and increased TBARS levels in the cerebral structures of mice. QTCA-1 protected against these brain changes. In conclusion, QTCA-1 had anti-amnesic action in the experimental model used in the present study, through the anticholinesterase effect, modulation of Na⁺/K⁺-ATPase activity and antioxidant action.

Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126. https://doi.org/10.1016/S0076-6879(84)05016-3 CrossRef

Ali EHA, Arafa NMS (2011) Comparative protective action of curcumin, memantine and diclofenac against scopolamine-induced memory dysfunction. Fitoterapia 82:601–608. https://doi.org/10.1016/j.fitote.2011.01.016 CrossRefPubMed

Azman KF, Zakaria R, Abdul-Aziz C, Othman Z, Al-Rahbi B (2015) Tualang honey improves memory performance and decreases depressive-like behavior in rats exposed to loud noise stress. Noise Health 17:83–89. https://doi.org/10.4103/1463-1741.153388 CrossRefPubMedPubMedCentral

Balaban H, Nazıroglu M, Demirci K, Övey IS (2016) The protective role of selenium on scopolamine-induced memory impairment, oxidative stress, and apoptosis in aged rats: the involvement of TRPM2 and TRPV1 channels. Mol Neurobiol 54:2852–2868. https://doi.org/10.1007/s12035-016-9835-0 CrossRefPubMed

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254. https://doi.org/10.1016/0003-2697(76)90527-3 CrossRef

Chen W, Cheng X, Chen J, Yi X, Nie D, Sun X (2014) Lycium barbarum polysaccharides prevent memory and neurogenesis impairments in scopolamine-treated rats. PLoS One 9(2):e88076. https://doi.org/10.1371/journal.pone.0088076 CrossRefPubMedPubMedCentral

Cruz R, Almaguer MW, Bergado RJ (2002) Glutathione in cognitive function and neurodegeneration. Rev Neurol 36:877–886. https://doi.org/10.33588/rn.3609.2002395 CrossRef

da Silva FD, Pinz MP, de Oliveira RL, Rodrigues KC, Ianiski FR, Bassaco MM, Silveira CC, Jesse CR, Roman SS, Wilhelm EA, Luchese C (2017) Organosulfur compound protects against memory decline induced by scopolamine through modulation of oxidative stress and Na+/K+ ATPase activity in mice. Metab Brain Dis 6:1819–1828. https://doi.org/10.1007/s11011-017-0067-4 CrossRef

Dix SL, Aggleton JP (1999) Extending the spontaneous preference test of recognition:evidence of object location and object-context recognition. Behav Brain Res 99:191–200. https://doi.org/10.1016/S0166-4328(98)00079-5 CrossRefPubMed

Eduviere AT, Umukoro S, Aderibigbe AO, Ajayi AM, Adewole FA (2015) Methyl jasmonate enhances memory performance through inhibition of oxidative stress and acetylcholinesterase activity in mice. Life Sci 132:20–26. https://doi.org/10.1016/j.lfs.2015.04.007 CrossRefPubMed

Ellman GL, Courtney KD, Andres JV, Featherstone MR (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. https://doi.org/10.1016/0006-2952(61)90145-9 CrossRefPubMed

Ferreira-Vieira HT, Guimaraes IM, Silva FR, Ribeiro FM (2016) Alzheimer's disease: targeting the cholinergic system. Curr Neuropharmacol 14:101–115. https://doi.org/10.2174/1570159X13666150716165726 CrossRefPubMedPubMedCentral

Fiske CH, Subbarow YJ (1925) The calorimetic determination of phosphorus. Biol Chem 66:375–381

Freeman SE, Dawson RM (1991) Tacrine: a pharmacological review. Prog Neurobiol 36:255–257. https://doi.org/10.1016/0301-0082(91)90002-I CrossRef

Fukuda T, Ayabe T, Ohya R, Ano Y (2019) Matured hop bitter acids improve spatial working and object recognition memory via nicotinic acetylcholine receptors. Psychopharmacology 236(9):2847–2854. https://doi.org/10.1007/s00213-019-05263-7 CrossRefPubMed

Guo C, Shen J, Meng Z, Yang X, Li F (2016) Neuroprotective effects of polygalacic acid on scopolamine-induced memory deficits in mice. Phytomedicine 23:149–155. https://doi.org/10.1016/j.phymed.2015.12.009 CrossRefPubMed

Gutierres JM, Carvalho FB, Schetinger MRC, Agostinho P, MariscoPC VJM, Spanevello R (2014) Neuroprotective effect of anthocyanins on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia in rats. Int J Dev Neurosci 33:88–97. https://doi.org/10.1016/j.ijdevneu.2013.12.006 CrossRefPubMed

Habiba R, Aamra M, Touqeer A (2017) Title: role of cholinergic receptors in memory retrieval. Depends on Gender and Age of Memory Behav Brain Res 331:233–240. https://doi.org/10.1016/j.bbr.2017.05.017 CrossRef

Jiang HL, Wang X, Huang L, Luo Z, Su T, Ding K, Li X (2011) Benzenediol-berberine hybrids: multifunctional agents for Alzheimer's disease. Bioorg Med Chem 19:7228–7235. https://doi.org/10.1016/j.bmc.2011.09.040 CrossRefPubMed

Kim MS, Lee DY, Lee J, Kim HW, Sung SH, Han JS, Jeon WK (2018) Terminalia chebula extract prevents scopolamine-induced amnesia via cholinergic modulation and anti-oxidative effects in mice. BMC Complement Altern Med 18:1–11. https://doi.org/10.1186/s12906-018-2212-y CrossRef

Kumar A, Singh A, Ekavali (2015) A review on Alzheimer’s disease pathophysiology and its management: an update. Pharmacol Rep 67:195–203. https://doi.org/10.1016/j.pharep.2014.09.004 CrossRef

Libro RGS, Rajan ST, Bramanti P, Mazzon E (2016) Natural phytochemicals in the treatment and prevention of dementia: an overview. Molecules 21:1–38. https://doi.org/10.3390/molecules21040518 CrossRef

Lin J, Ling H, Jie Y, Siying X, Jialing W, Jinrong Z, Xiaojun Y, Wei C, Shan H, Qinwen W (2016) Fucoxanthin, a marine carotenoid, reverses scopolamine-induced cognitive impairments in mice and inhibits acetylcholinesterase in vitro. Mar Drugs 14:1–17. https://doi.org/10.3390/md14040067 CrossRef

Lobo A, Launer LJ, Fratiglioni L, Andersen K, Di Carlo A, Breteler MMB, Soininen H (2000) Prevalence of dementia and major subtypes in Europe: a collaborative study of population-based cohorts. Neurology 54:4–9. https://doi.org/10.1186/1471-2377-9-55 CrossRef

Mancino AM, Hindo SS, Kochi A, Lim MH (2009) Effects of clioquinol on metal- triggered amyloid-b aggregation revisited. Inorg Chem 48:9596–9598. https://doi.org/10.1021/ic9014256 CrossRefPubMed

Martini F, Pesarico AP, Brüning CA, Zeni G, Nogueira CW (2018) Ebselen inhibits the activity of acetylcholinesterase globular isoform G4 in vitro and attenuates scopolamine-induced amnesia in mice. J Cell Biochem 119:5598–5608. https://doi.org/10.1002/jcb.26731 CrossRefPubMed

Mattson MP, Pedersen WA, Duan W, Culmsee C, Camandola S (1999) Cellular and molecular mechanisms underlying perturbed energy metabolism and neuronal degeneration in Alzheimer’s and Parkinson’s diseases. Ann N Y Acad Sci 893:154–175. https://doi.org/10.1111/j.1749-6632.1999.tb07824.x CrossRefPubMed

Mazumder MK, Choudhury S, Borah A (2019) An in silico investigation on the inhibitory potential of the constituents of pomegranate juice on antioxidant defense mechanism: relevance to neurodegenerative diseases. IBRO Rep 6:153–159. https://doi.org/10.1016/j.ibror.2019.05.003 CrossRefPubMedPubMedCentral

Mignani S, El Kazzouli S, Bousmina M, Majoral JP (2013) Expand classical drug administration ways by emerging routes using dendrimer drug delivery systems: a concise overview. Adv Drug Deliv Rev 10:1316–1330. https://doi.org/10.1016/j.addr.2013.01.001 CrossRef

Nath C, Agrawal R, Tyagi E, Saxena G (2009) Cholinergic influence on memory stages: a study on scopolamine amnesic mice. Indian J Pharmacol 41:192–196. https://doi.org/10.4103/0253-7613.56072 CrossRefPubMedPubMedCentral

Nelson PT, Head E, Schmitt FA, Davis PR, Neltner JH, Jicha GA, Abner EL, Smith CD, Van Eldik LJ, Kryscio RJ, Scheff SW (2011) Alzheimer’s disease is not “brain aging”: neuropathological, genetic, and epidemiological human studies. Acta Neuropathol 121:571–587. https://doi.org/10.1007/s00401-011-0826-y CrossRefPubMedPubMedCentral

Ngoupaye GT, Pahaye DB, Ngondi J, Moto FCO, Bum EN (2017) Gladiolus dalenii lyophilisate reverses scopolamineinduced amnesia and reduces oxidative stress in rat brain. Biomed Pharmacother 91:350–357. https://doi.org/10.1016/j.biopha.2017.04.061 CrossRefPubMed

Niedzielska E, Smaga I, Gawlik M, Moniczewski A, Stankowicz P, Pera J, Filip M (2016) Oxidative stress in neurodegenerative diseases. Mol Neurobiol 53:4094–4125. https://doi.org/10.1007/s12035-015-9337-5 CrossRefPubMed

Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358. https://doi.org/10.1016/0003-2697(79)90738-3 CrossRefPubMed

Oz M, Lorke DE, Petroianu GA (2009) Methylene blue and Alzheimer's disease. Biochem Pharmacol 78:927–932. https://doi.org/10.1016/j.bcp.2009 CrossRefPubMed

Pahaye DB, Bum EN, Taïwé GS, Ngoupaye GT, Sidiki S, Moto FCO, Kouemou N, Njapdounke NSJK, Nkantchoua G, Kandeda O, Mairaira V, Ojong JL (2017) Neuroprotective and antiamnesic effects of mitragyna inermis willd (Rubiaceae) on scopolamine-induced memory impairment in mice. Behav Neurol 2017:5952897. https://doi.org/10.1155/2017/595289 CrossRefPubMedPubMedCentral

Parent MB, Baxter MG (2004) Septohippocampal acetylcholine: involved in but not necessary for learning and memory? Learn Mem 11:9–20. https://doi.org/10.1101/lm.69104 CrossRefPubMedPubMedCentral

Pinz MP, Reis AS, Vogt AG, Krüger R, Alves D, Jesse CR, Roman SS, Soares MP, Wilhelm EA, Luchese C (2018) Current advances of pharmacological properties of 7-chloro-4-(phenylselanyl) quinoline: prevention of cognitive deficit and anxiety in Alzheimer’s disease model. Biomed Pharmacother 105:1006–1014. https://doi.org/10.1016/j.biopha.2018.06.049 CrossRefPubMed

Pompl PN, Mullan MJ, Bjugstad K, Arendash GW (1999) Adaptation of the circular platform spatial memory task for mice: use in detecting cognitive impairment in the APP(SW) transgenic mouse model for Alzheimer’s disease. J Neurosci Methods 87:87–95. https://doi.org/10.1016/S0165-0270(98)00169-1 CrossRefPubMed

Puri A, Srivastava P, Pandey P, Yadav RS, Bhatt PC (2014) Scopolamine induced behavioral and biochemical modifications and protective effect of Celastrus paniculatous and Angelica glauca in rats. Int J Nutr Pharmacol Neurol Dis 4:158–169. https://doi.org/10.4103/2231-0738.132675 CrossRef

Ritchie CW, Terrera GM, Quinn TJ (2015) Dementia trials and dementia tribulations: methodological and analytical challenges in dementia research. Alzheimers Res Ther 7:31–11. https://doi.org/10.1186/s13195-015-0113-6 CrossRefPubMedPubMedCentral

Russell WMS, Burch RL (1959) The principles of humane experimental technique. Methuen, London

Sakaguchi M, Koseki M, Wakamatsu M, Matsumura E (2006) Effects of systemic administration of beta-casomorphin-5 on learning and memory in mice. Eur J Pharmacol 530:81–87. https://doi.org/10.1016/j.ejphar.2005.11.014 CrossRefPubMed

Sambon M, Napp A, Demelenne A, Vignisse J, Wins P, Fillet M, Bettendorff L (2019) Thiamine and benfotiamine protect neuroblastoma cells against paraquat and β-amyloid toxicity by a coenzyme-independent mechanism. Heliyon. 5:e01710. https://doi.org/10.1016/j.heliyon.2019.e01710 CrossRefPubMedPubMedCentral

Souza MA, Magni DV, Guerra GP, Oliveira MS, Furian AF, Pereira L, Marquez SV, Ferreira J, Fighera MR, Roves LFF (2012) Involvement of hippocampal CAMKII/CREB signaling in the spatial memory retention induced by creatine. Amino Acids 43:2491–2503. https://doi.org/10.1007/s00726-012-1329-4 CrossRefPubMed

Souza ACG, Brüning CA, Leite MR, Zeni G, Nogueira CW (2010) Diphenyl diselenide improves scopolamine-induced memory impairment in mice. Behav Pharmacol 21:556–562. https://doi.org/10.1097/FBP.0b013e32833befcf CrossRefPubMed

Stangherlin EC, Rocha JBT, Nogueira CW (2009) Diphenyl ditelluride impairs short term memory and alters neurochemical parameters in young rats. Pharmacol Biochem Behav 91:430–435. https://doi.org/10.1016/j.pbb.2008.08.020 CrossRefPubMed

Tao S, Liu L, Shi L, Li X, Shen P, Xun Q, Guo X, Yu Z, Wang J (2015) Spatial learning and memory deficits in young adult mice exposed to a brief intense noise at postnatal age. J Otol 10:21–28. https://doi.org/10.1016/j.joto.2015.07.001 CrossRefPubMedPubMedCentral

Van de Vorst IE, Vaartjes I, Sinnecker LF, Beks LJM, Bots ML, Koel HL (2015) The validity of national hospital discharge register data on dementia: a comparative analysis using clinical data from a university medical Centre. Neth J Med 73:69–75PubMed

Walsh RN, Cummins RA (1976) Open-field test: critical review. Psychol Bull 83:482–504CrossRef

Weon JB, Jung YS, Ma CJ (2016) Cognitive-enhancing effect of Dianthus superbus Var. Longicalycinus on scopolamine-induced memory impairment in mice. Biomol Ther 24:298–304. https://doi.org/10.4062/biomolther.2015.083 CrossRef

Wilhelm EA, Machado NC, Pedroso AB, Goldani BS, Seus N, Moura S, Savegnago L, Jacob RG, Alves D (2014) Organocatalytic synthesis and evaluation of 7-chloroquinoline-1,2,3-triazoylcarboxamides as potential antinociceptive, anti-inflammatory and anticonvulsant agent. RSC Adv 04:41437–41445. https://doi.org/10.5935/0103-5053.20150239 CrossRef

World Health Organization (WHO) (2017). Global action plan on the public health response to dementia 2017–2025. Geneva: World Health Organization; 2017. Licence: CC BY-NC-SA 3.0 IGO

Zemek F, Drtinova L, Nepovimova E, Sepsova V, Korabecny J, Klimes J, Kuca K (2014) Outcomes of Alzheimer’s disease therapy with acetylcholinesterase inhibitors and memantine. Expert Opin Drug Saf 13:759–774. https://doi.org/10.1517/14740338.2014.914168 CrossRefPubMed

Zhang LN, Sun YJ, Pan S, Li JX, Qu YE, Li Y, Wang YL, Gao ZB (2013) Na⁺-K⁺-ATPase, a potent neuroprotective modulator against Alzheimer disease. Fundam Clin Pharmacol 27:96–103. https://doi.org/10.1111/fcp.12000 CrossRefPubMed

Title: Amnesia-ameliorative effect of a quinoline derivative through regulation of oxidative/cholinergic systems and Na+/K+-ATPase activity in mice
Authors: Cristiane Luchese
Ane G. Vogt
Mikaela P. Pinz
Angélica S. dos Reis
Carolina B. Gomes
Diego Alves
Ethel A. Wilhelm
Publication date: 01-04-2020
Publisher: Springer US
Keywords: Amnesia
Dementia
Dementia
Published in: Metabolic Brain Disease / Issue 4/2020
Print ISSN: 0885-7490
Electronic ISSN: 1573-7365
DOI: https://doi.org/10.1007/s11011-020-00535-0

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Amnesia-ameliorative effect of a quinoline derivative through regulation of oxidative/cholinergic systems and Na⁺/K⁺-ATPase activity in mice

Abstract

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Springer Medicine

Abstract

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