Mitochondrial involvement in memory impairment induced by scopolamine in rats

References

• Suh YH, Checler F. Amyloid precursor protein, presenilins, and alpha-synuclein: molecular pathogenesis and pharmacological applications in Alzheimer’s disease. Pharmacol Rev. 2002;54(3):469–525.10.1124/pr.54.3.469
   PubMed Web of Science ®Google Scholar
• Cabezas-Opazo FA, Vergara-Pulgar K, Perez MJ, et al. Mitochondrial dysfunction contributes to the pathogenesis of Alzheimer’s disease. Oxid Med Cell Longev. 2015;2015:509–654.
   Web of Science ®Google Scholar
• Doraiswamy PM. Non-cholinergic strategies for treating and preventing Alzheimer’s disease. CNS Drugs. 2002;16(12):811–824.10.2165/00023210-200216120-00003
   PubMed Web of Science ®Google Scholar
• Selkoe DJ. The molecular pathology of Alzheimer’s disease. Neuron. 1991;6(4):487–498.10.1016/0896-6273(91)90052-2
   PubMed Web of Science ®Google Scholar
• Citron M. Alzheimer’s disease: strategies for disease modification. Nat Rev Drug Discovery. 2010;9(5):387–398.10.1038/nrd2896
   PubMed Web of Science ®Google Scholar
• Shineman DW, Basi GS, Bizon JL, et al. Accelerating drug discovery for Alzheimer’s disease: best practices for preclinical animal studies. Alzheimer’s Res Ther. 2011;3(5):1–13.10.1186/alzrt90
   Web of Science ®Google Scholar
• Wallace TL, Ballard TM, Glavis-Bloom C. Animal paradigms to assess cognition with translation to humans. Handb Exp Pharmacol. 2015;228:27–57.
   PubMedGoogle Scholar
• Lee B, Sur B, Shim I, et al. Phellodendron amurense and its major alkaloid compound, berberine ameliorates scopolamine-induced neuronal impairment and memory dysfunction in rats. Korean J Physiol Pharmacol. 2012;16(2):79–89.10.4196/kjpp.2012.16.2.79
   PubMed Web of Science ®Google Scholar
• Jeong EJ, Lee KY, Kim SH, et al. Cognitive-enhancing and antioxidant activities of iridoid glycosides from Scrophularia buergeriana in scopolamine-treated mice. Eur J Pharmacol. 2008;588(1):78–84.10.1016/j.ejphar.2008.04.015
   PubMed Web of Science ®Google Scholar
• Jahanshahi M, Nickmahzar EG, Babakordi F. The effect of Ginkgo biloba extract on scopolamine-induced apoptosis in the hippocampus of rats. Anat Sci Int. 2013;88(4):217–222.10.1007/s12565-013-0188-8
   PubMed Web of Science ®Google Scholar
• Demirci K, Naziroglu M, Ovey IS, et al. Selenium attenuates apoptosis, inflammation and oxidative stress in the blood and brain of aged rats with scopolamine-induced dementia. Metab Brain Dis. 2017;32:321–329.
   PubMed Web of Science ®Google Scholar
• Balaban H, Naziroglu M, Demirci K, et al. 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. 2016. doi: 10.1007/s12035-016-9835-0.
   PubMed Web of Science ®Google Scholar
• Ishola IO, Tota S, Adeyemi OO, et al. Protective effect of Cnestis ferruginea and its active constituent on scopolamine-induced memory impairment in mice: a behavioral and biochemical study. Pharm Biol. 2013;51(7):825–835.10.3109/13880209.2013.767360
   PubMed Web of Science ®Google Scholar
• Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature. 2006;443(7113):787–795.10.1038/nature05292
   PubMed Web of Science ®Google Scholar
• Gorlach A, Bertram K, Hudecova S, et al. Calcium and ROS: a mutual interplay. Redox Biol. 2015;6:260–271.10.1016/j.redox.2015.08.010
   PubMed Web of Science ®Google Scholar
• Bhosale G, Sharpe JA, Sundier SY, et al. Calcium signaling as a mediator of cell energy demand and a trigger to cell death. Ann NY Acad Sci. 2015;1350:107–116.10.1111/nyas.2015.1350.issue-1
   PubMed Web of Science ®Google Scholar
• Jang YJ, Kim J, Shim J, et al. Decaffeinated coffee prevents scopolamine-induced memory impairment in rats. Behav Brain Res. 2013;245:113–119. Epub 2013/02/19.10.1016/j.bbr.2013.02.003
   PubMed Web of Science ®Google Scholar
• de Bruin NM, Prickaerts J, van Loevezijn A, et al. Two novel 5-HT6 receptor antagonists ameliorate scopolamine-induced memory deficits in the object recognition and object location tasks in Wistar rats. Neurobiol Learn Memory. 2011;96(2):392–402. Epub 2011/07/16.10.1016/j.nlm.2011.06.015
   PubMed Web of Science ®Google Scholar
• Han RW, Zhang RS, Xu HJ, et al. Neuropeptide S enhances memory and mitigates memory impairment induced by MK801, scopolamine or Aβ1–42 in mice novel object and object location recognition tasks. Neuropharmacology. 2013;70:261–267. Epub 2013/03/05.10.1016/j.neuropharm.2013.02.002
   PubMed Web of Science ®Google Scholar
• Willi R, Winter C, Wieske F, et al. Loss of EphA4 impairs short-term spatial recognition memory performance and locomotor habituation. Genes Brain Behav. 2012;11(8):1020–1031.
   PubMed Web of Science ®Google Scholar
• Akwa Y, Ladurelle N, Covey DF, et al. The synthetic enantiomer of pregnenolone sulfate is very active on memory in rats and mice, even more so than its physiological neurosteroid counterpart: distinct mechanisms? Proc Natl Acad Sci USA. 2001;98(24):14033–14037.10.1073/pnas.241503698
   PubMed Web of Science ®Google Scholar
• Hidaka N, Suemaru K, Takechi K, et al. Inhibitory effects of valproate on impairment of Y-maze alternation behavior induced by repeated electroconvulsive seizures and c-Fos protein levels in rat brains. Acta Med Okayama. 2011;65(4):269–277.
   PubMed Web of Science ®Google Scholar
• Tucci P, Mhillaj E, Morgese MG, et al. Memantine prevents memory consolidation failure induced by soluble beta amyloid in rats. Front Behav Neurosci. 2014;8:1–11.
   PubMed Web of Science ®Google Scholar
• Milic M, Timic T, Joksimovic S, et al. PWZ-029, an inverse agonist selective for α5 GABAA receptors, improves object recognition, but not water-maze memory in normal and scopolamine-treated rats. Behav Brain Res. 2013;241:206–213.10.1016/j.bbr.2012.12.016
   PubMed Web of Science ®Google Scholar
• Lowry OH, Rosebrough NJ, Farr AL, et al. Protein measurement with the Folin phenol reagent. J Biol Chem. 1951;193(1):265–275.
   PubMed Web of Science ®Google Scholar
• Ellman GL, Courtney KD, Andres Jr V. A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol. 1961;7:88–95.10.1016/0006-2952(61)90145-9
   PubMed Web of Science ®Google Scholar
• Kono Y. Generation of superoxide radical during autoxidation of hydroxylamine and an assay for superoxide dismutase. Arch Biochem Biophys. 1978;186(1):189–195.10.1016/0003-9861(78)90479-4
   PubMed Web of Science ®Google Scholar
• Kumar A, Dogra S, Prakash A. Protective effect of curcumin (Curcuma longa), against aluminium toxicity: possible behavioral and biochemical alterations in rats. Behav Brain Res. 2009;205(2):384–390.10.1016/j.bbr.2009.07.012
   PubMed Web of Science ®Google Scholar
• Wills ED. Lipid peroxide formation in microsomes. General considerations. Biochem J. 1969;113(2):315–324.
   PubMed Web of Science ®Google Scholar
• Ellman G. Tissue sulfhydryl groups. Arch Biochem Biophys. 1959;82:48670–48677.
   Web of Science ®Google Scholar
• Mirandola SR, Melo DR, Saito A, et al. 3-Nitropropionic acid-induced mitochondrial permeability transition: comparative study of mitochondria from different tissues and brain regions. J Neurosci Res. 2010;88(3):630–639.
   PubMed Web of Science ®Google Scholar
• Nunez-Figueredo Y, Ramirez-Sanchez J, Hansel G, et al. A novel multi-target ligand (JM-20) protects mitochondrial integrity, inhibits brain excitatory amino acid release and reduces cerebral ischemia injury in vitro and in vivo. Neuropharmacology. 2014;85:517–527.10.1016/j.neuropharm.2014.06.009
   PubMed Web of Science ®Google Scholar
• Nuñez-Figueredo Y, Pardo-Andreu GL, Ramírez-Sánchez J, et al. Antioxidant effects of JM-20 on rat brain mitochondria and synaptosomes: mitoprotection against Ca2+-induced mitochondrial impairment. Brain Res Bull. 2014;109:68–76.10.1016/j.brainresbull.2014.10.001
   PubMed Web of Science ®Google Scholar
• Zanotti A, Azzone GF. Safranine as membrane potential probe in rat liver mitochondria. Arch Biochem Biophys. 1980;201(1):255–265.10.1016/0003-9861(80)90510-X
   PubMed Web of Science ®Google Scholar
• Votyakova TV, Reynolds IJ. DeltaPsi(m)-dependent and -independent production of reactive oxygen species by rat brain mitochondria. J Neurochem. 2001;79(2):266–277.
   PubMed Web of Science ®Google Scholar
• Zhou M, Diwu Z, Panchuk-Voloshina N, et al. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem. 1997;253:162–168.10.1006/abio.1997.2391
   PubMed Web of Science ®Google Scholar
• Rajdev S, Reynolds IJ. Calcium green-5N, a novel fluorescent probe for monitoring high intracellular free Ca2+ concentrations associated with glutamate excitotoxicity in cultured rat brain neurons. Neuroscience Letters. 1993;162(1–2):149–152.10.1016/0304-3940(93)90582-6
   PubMed Web of Science ®Google Scholar
• Rajdev S, Reynolds IJ. Calcium green-5N, a novel fluorescent probe for monitoring high intracellular free Ca2+ concentrations associated with glutamate excitotoxicity in cultured rat brain neurons. Neurosci Lett. 1993;162(1–2):149–152.10.1016/0304-3940(93)90582-6
   PubMed Web of Science ®Google Scholar
• Paredes RM, Etzler JC, Watts LT, et al. Chemical calcium indicators. Methods. 2008;46(3):143–151.10.1016/j.ymeth.2008.09.025
   PubMed Web of Science ®Google Scholar
• Eberhard M, Erne P. Calcium binding to fluorescent calcium indicators: calcium green, calcium orange and calcium crimson. Biochem Biophys Res Commun. 1991;180:209–215.10.1016/S0006-291X(05)81278-1
   PubMed Web of Science ®Google Scholar
• Gold PE. Acetylcholine: cognitive and brain functions. Neurobiol Learn Memory. 2003;80(3):177.10.1016/j.nlm.2003.07.002
   PubMed Web of Science ®Google Scholar
• Cuartero M, Ortuno JA, Garcia MS, et al. Assay of acetylcholinesterase activity by potentiometric monitoring of acetylcholine. Anal Biochem. 2012;421(1):208–212.
   PubMed Web of Science ®Google Scholar
• Budzynska B, Boguszewska-Czubara A, Kruk-Slomka M, et al. Effects of imperatorin on scopolamine-induced cognitive impairment and oxidative stress in mice. Psychopharmacology. 2015;232(5):931–942.10.1007/s00213-014-3728-6
   PubMed Web of Science ®Google Scholar
• Foyet HS, Abaissou HH, Wado E, et al. Emilia coccinae (SIMS) G Extract improves memory impairment, cholinergic dysfunction, and oxidative stress damage in scopolamine-treated rats. BMC Complementary Altern Med. 2015;15:1–12.10.1186/s12906-015-0864-4
   Web of Science ®Google Scholar
• Ciobica A, Hritcu L, Artenie V, et al. The effects of some cholinergic drugs on cognitive processes and oxidative stress in rat. Rev Med Chir Soc Med Nat Iasi. 2009;113(3):832–837.
   PubMedGoogle Scholar
• Chaturvedi RK, Flint Beal M. Mitochondrial diseases of the brain. Free Radic Biol Med. 2013;63:1–29.10.1016/j.freeradbiomed.2013.03.018
   PubMed Web of Science ®Google Scholar
• Ruszkiewicz J, Albrecht J. Changes in the mitochondrial antioxidant systems in neurodegenerative diseases and acute brain disorders. Neurochem Int. 2015;88:66–72.10.1016/j.neuint.2014.12.012
   PubMed Web of Science ®Google Scholar
• Simoncini C, Orsucci D, Caldarazzo Ienco E, et al. Alzheimer’s pathogenesis and its link to the mitochondrion. Oxid Med Cell Longev. 2015;2015:1–8.
   PubMed Web of Science ®Google Scholar
• Ferreira-Vieira TH, Guimaraes IM, Silva FR, et al. Alzheimer’s disease: targeting the cholinergic system. Curr Neuropharmacol. 2016;14(1):101–115.10.2174/1570159X13666150716165726
   PubMed Web of Science ®Google Scholar
• Carvalho AN, Firuzi O, Gama MJ, et al. Oxidative stress and antioxidants in neurological diseases: is there still hope? Curr Drug Targets. 2016;18:705–718.
   PubMed Web of Science ®Google Scholar
• Chen C, Li XH, Zhang S, et al. 7,8-dihydroxyflavone ameliorates scopolamine-induced Alzheimer-like pathologic dysfunction. Rejuvenation Res. 2014;17(3):249–254.10.1089/rej.2013.1519
   PubMed Web of Science ®Google Scholar
• Pachauri SD, Tota S, Khandelwal K, et al. Protective effect of fruits of Morinda citrifolia L. on scopolamine induced memory impairment in mice: a behavioral, biochemical and cerebral blood flow study. J Ethnopharmacol. 2012;139(1):34–41.10.1016/j.jep.2011.09.057
   PubMed Web of Science ®Google Scholar
• Chaudhaery SS, Roy KK, Shakya N, et al. Novel carbamates as orally active acetylcholinesterase inhibitors found to improve scopolamine-induced cognition impairment: pharmacophore-based virtual screening, synthesis, and pharmacology. J Med Chem. 2010;53(17):6490–6505.
   PubMed Web of Science ®Google Scholar
• Gutierres JM, Carvalho FB, Schetinger MR, et al. Neuroprotective effect of anthocyanins on acetylcholinesterase activity and attenuation of scopolamine-induced amnesia in rats. Int J Dev Neurosci. 2014;33:88–97.10.1016/j.ijdevneu.2013.12.006
   PubMed Web of Science ®Google Scholar
• Kwon SH, Lee HK, Kim JA, et al. Neuroprotective effects of chlorogenic acid on scopolamine-induced amnesia via anti-acetylcholinesterase and anti-oxidative activities in mice. Eur J Pharmacol. 2010;649(1–3):210–217.10.1016/j.ejphar.2010.09.001
   PubMed Web of Science ®Google Scholar
• Snyder PJ, Bednar MM, Cromer JR, et al. Reversal of scopolamine-induced deficits with a single dose of donepezil, an acetylcholinesterase inhibitor. Alzheimer’s Dementia. 2005;1(2):126–135.10.1016/j.jalz.2005.09.004
   PubMedGoogle Scholar
• Wang X, Wang W, Li L, et al. Oxidative stress and mitochondrial dysfunction in Alzheimer’s disease. Biochim Biophys Acta. 2014;1842(8):1240–1247.10.1016/j.bbadis.2013.10.015
   PubMed Web of Science ®Google Scholar
• Klinkenberg I, Blokland A. The validity of scopolamine as a pharmacological model for cognitive impairment: a review of animal behavioral studies. Neurosci Biobehav Rev. 2010;34(8):1307–1350.10.1016/j.neubiorev.2010.04.001
   PubMed Web of Science ®Google Scholar
• Marcello E, Epis R, Saraceno C, et al. Synaptic dysfunction in Alzheimer’s disease. Adv Exp Med Biol. 2012;970:573–601.10.1007/978-3-7091-0932-8
   PubMed Web of Science ®Google Scholar
• Sullivan PG, Rabchevsky AG, Waldmeier PC, et al. Mitochondrial permeability transition in CNS trauma: cause or effect of neuronal cell death? J Neurosci Res. 2005;79:231–239.10.1002/(ISSN)1097-4547
   PubMed Web of Science ®Google Scholar
• Zoratti M, Szabo I. The mitochondrial permeability transition. Biochim Biophys Acta. 1995;1241:139–176.10.1016/0304-4157(95)00003-A
   PubMed Web of Science ®Google Scholar
• Venkatesan R, Subedi L, Yeo EJ, et al. Lactucopicrin ameliorates oxidative stress mediated by scopolamine-induced neurotoxicity through activation of the NRF2 pathway. Neurochem Int. 2016;99:133–146 . Epub 2016/06/28.10.1016/j.neuint.2016.06.010
   PubMed Web of Science ®Google Scholar
• Fišar Z, Hroudová J, Hansíková H, et al. Mitochondrial respiration in the platelets of patients with Alzheimer’s disease. Curr Alzheimer Res. 2016;13(8):930–941.
   PubMed Web of Science ®Google Scholar
• Rönnbäck A, Pavlov PF, Mansory M, et al. Mitochondrial dysfunction in a transgenic mouse model expressing human amyloid precursor protein (APP) with the Arctic mutation. J Neurochem. 2016;136(3):497–502.10.1111/jnc.2016.136.issue-3
   PubMed Web of Science ®Google Scholar
• Bobba A, Amadoro G, Valenti D, et al. Mitochondrial respiratory chain Complexes I and IV are impaired by β-amyloid via direct interaction and through Complex I-dependent ROS production, respectively. Mitochondrion. 2013;13(4):298–311.10.1016/j.mito.2013.03.008
   PubMed Web of Science ®Google Scholar
• Sun L, Zang WJ, Wang H, et al. Acetylcholine promotes ROS detoxification against hypoxia/reoxygenation-induced oxidative stress through FoxO3a/PGC-1α dependent superoxide dismutase. Cell Physiol Biochem. 2014;34(5):1614–1625.10.1159/000366364
   PubMed Web of Science ®Google Scholar
• De Sarno P, Shestopal SA, King TD, et al. Muscarinic receptor activation protects cells from apoptotic effects of DNA damage, oxidative stress, and mitochondrial inhibition. J Biol Chem. 2003;278(13):11086–11093.10.1074/jbc.M212157200
   PubMed Web of Science ®Google Scholar
• Leloup C, Michaelson DM, Fisher A, et al. M1 muscarinic receptors block caspase activation by phosphoinositide 3-kinase- and MAPK/ERK-independent pathways. Cell Death Differ. 2000;7(9):825–833.10.1038/sj.cdd.4400713
   PubMed Web of Science ®Google Scholar
• Urrunaga NH, Jadeja RN, Rachakonda V, et al. M1 muscarinic receptors modify oxidative stress response to acetaminophen-induced acute liver injury. Free Radicals Biol Med. 2015;78:66–81.10.1016/j.freeradbiomed.2014.09.032
   PubMed Web of Science ®Google Scholar
• Nazıroğlu M. Molecular role of catalase on oxidative stress-induced Ca2+ signaling and TRP cation channel activation in nervous system. J Recept Signal Transduct Res. 2012;32(3):134–141.
   PubMed Web of Science ®Google Scholar