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Original Articles

An adenoviral vector encoded with the GPx-1 gene attenuates memory impairments induced by β-amyloid (1-42) in GPx-1 KO mice via activation of M1 mAChR-mediated signalling

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Pages 11-25 | Received 27 May 2020, Accepted 18 Nov 2020, Published online: 10 Dec 2020

References

  • Behl C, Davis JB, Lesley R, et al. Hydrogen peroxide mediates amyloid beta protein toxicity. Cell. 1994;77(6):817–827.
  • Butterfield DA. Amyloid β-peptide (1-42)-induced oxidative stress and neurotoxicity: Implications for neurodegeneration in Alzheimer’s disease brain. A review. Free Radic Res. 2002;36:1307–1313.
  • Jhoo JH, Kim HC, Nabeshima T, et al. Beta-amyloid (1-42)-induced learning and memory deficits in mice: involvement of oxidative burdens in the hippocampus and cerebral cortex. Behav Brain Res. 2004;155(2):185–196.
  • Kim HC, Yamada K, Nitta A, et al. Immunocytochemical evidence that amyloid beta (1-42) impairs endogenous antioxidant systems in vivo. Neuroscience. 2003;119(2):399–419.
  • Wang WT, Tailor BA, Cohen DS, et al. Alzheimer’s pathogenesis, metal-mediated redox stress, and potential nanotheranostics. EC Pharmacol Toxicol. 2019;7:547–558.
  • Butterfield DA. The 2013 SFRBM discovery award: Selected discoveries from the butterfield laboratory of oxidative stress and its sequela in brain in cognitive disorders exemplified by Alzheimer disease and chemotherapy induced cognitive impairment. Free Radic Biol Med. 2014;74:157–174.
  • Butterfield DA. Perspectives on oxidative stress in Alzheimer's disease and predictions of future research emphases. J Alzheimers Dis. 2018;64(s1):S469–S479.
  • Butterfield DA, Drake J, Pocernich C, et al. Evidence of oxidative damage in Alzheimer’s disease brain: central role for amyloid beta-peptide. Trends Mol Med. 2001;7(12):548–554.
  • Mattson MP. Free radicals and disruption of neuronal ion homeostasis in AD: A role for amyloid beta-peptide? Neurobiol Aging. 1995;16(4):679–682.
  • Behl C, Davis J, Cole GM, et al. Vitamin E protects nerve cells from amyloid beta protein toxicity. Biochem Biophys Res Commun. 1992;186(2):944–950.
  • Li MH, Jang JH, Sun B, et al. Protective effects of oligomers of grape seed polyphenols against beta-amyloid-induced oxidative cell death. Ann N Y Acad Sci. 2004;1030:317–329.
  • Jang JH, Surh YJ. Protective effect of resveratrol on β-amyloid-induced oxidative PC12 cell death. Free Radic Biol Med. 2003;34(8):1100–1110.
  • Shin E-J, Oh K-W, Kim K-W, et al. Attenuation of cocaine-induced conditioned place preference by Polygala tenuifolia root extract. Life Sci. 2004;75(23):2751–2764.
  • Li Z-Y, Chung YH, Shin E-J, et al. YY-1224, a terpene trilactone-strengthened Ginkgo biloba, attenuates neurodegenerative changes induced by β-amyloid (1-42) or double transgenic overexpression of APP and PS1 via inhibition of cyclooxygenase-2. J Neuroinflammation. 2017;14(1):94.
  • Halliwell B. Reactive oxygen species and the central nervous system. J Neurochem. 1992;59(5):1609–1623.
  • Sani M, Sebaï H, Gadacha W, et al. Catalase activity and rhythmic patterns in mouse brain, kidney and liver. Comp Biochem Physiol B Biochem Mol Biol. 2006;145(3-4):331–337.
  • Power JHT, Blumbergs PC. Cellular glutathione peroxidase in human brain: Cellular distribution, and its potential role in the degradation of Lewy bodies in Parkinson's disease and dementia with Lewy bodies. Acta Neuropathol. 2009;117(1):63–73.
  • Margis R, Dunand C, Teixeira FK, et al. Glutathione peroxidase family - an evolutionary overview. Febs J. 2008;275(15):3959–3970.
  • Hampel H, Mesulam MM, Cuello AC, et al. The cholinergic system in the pathophysiology and treatment of Alzheimer's disease. Brain. 2018;141(7):1917–1933.
  • Bartus RT. On neurodegenerative diseases, models, and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp Neurol. 2000;163(2):495–529.
  • Kihara T, Shimohama S. Alzheimer’s disease and acetylcholine receptors. Acta Neurobiol Exp (Wars)). 2004;64(1):99–105.
  • Fisher A. M1 muscarinic agonists target major hallmarks of Alzheimer's disease-the pivotal role of brain M1 receptors. Neurodegener Dis. 2008;5(3–4):237–240.
  • Jiang S, Li Y, Zhang C, et al. M1 muscarinic acetylcholine receptor in Alzheimer's disease. Neurosci Bull. 2014;30(2):295–307.
  • Lu B, Nagappan G, Lu Y. BDNF and synaptic plasticity, cognitive function, and dysfunction. Handb Exp Pharmacol. 2015;220:223–250.
  • Nabeshima T, Yamada K. Neurotrophic factor strategies for the treatment of Alzheimer disease. Alzheimer Dis Assoc Disord. 2000;14:S39–S46.
  • Schindowski K, Belarbi K, Buée L. Neurotrophic factors in Alzheimer’s disease: role of axonal transport. Genes, Brain Behav. 2008;7:43–56.
  • Tuszynski MH. Nerve growth factor gene therapy in Alzheimer disease. Alzheimer Dis Assoc Disord. 2007;21(2):179–189.
  • Einoch R, Weinreb O, Mandiuk N, et al. The involvement of BDNF-CREB signaling pathways in the pharmacological mechanism of combined SSRI- antipsychotic treatment in schizophrenia. Eur Neuropsychopharmacol. 2017;27(5):470–483.
  • Pizzorusso T, Ratto GM, Putignano E, et al. Brain-derived neurotrophic factor causes cAMP response element-binding protein phosphorylation in absence of calcium increases in slices and cultured neurons from rat visual cortex. J Neurosci. 2000;20(8):2809–2816.
  • Alonso M, Bekinschtein P, Cammarota M, et al. Endogenous BDNF is required for long-term memory formation in the rat parietal cortex. Learn Mem. 2005;12(5):504–510.
  • Gooney M, Messaoudi E, Maher FO, et al. BDNF-induced LTP in dentate gyrus is impaired with age: analysis of changes in cell signaling events. Neurobiol Aging. 2004;25(10):1323–1331.
  • Ying SW, Futter M, Rosenblum K, et al. Brain-derived neurotrophic factor induces long-term potentiation in intact adult hippocampus: Requirement for ERK activation coupled to CREB and upregulation of Arc synthesis. J Neurosci. 2002;22(5):1532–1540.
  • Gil-Bea FJ, Solas M, Mateos L, et al. Cholinergic hypofunction impairs memory acquisition possibly through hippocampal Arc and BDNF downregulation. Hippocampus. 2011;21(9):999–1009.
  • Ho YS, Magnenat JL, Bronson RT, et al. Mice deficient in cellular glutathione peroxidase develop normally and show no increased sensitivity to hyperoxia. J Biol Chem. 1997;272(26):16644–16651.
  • Cheng WH, Ho YS, Ross DA, et al. Cellular glutathione peroxidase knockout mice express normal levels of selenium-dependent plasma and phospholipid hydroperoxide glutathione peroxidases in various tissues. J Nutr. 1997;127(8):1445–1450.
  • Pham DT, Chung YH, Mai HN, et al. Glutathione peroxidase-1 gene rescues cocaine-induced conditioned place preference in mice by inhibiting σ-1 receptor expression. Clin Exp Pharmacol Physiol. 2019;46(9):791–797.
  • Nguyen LTT, Nguyen TXK, Bach JH, et al. Glutathione peroxidase-1 gene depletion potentiates cognitive impairments induced by β-amyloid (1-42). Proceedings of the spring international convention of the pharmaceutical society of Korea [April 21-22, Busan Exhibition & Convention Center (BEXCO)]. 2011; P168.
  • Yoo MH, Gu X, Xu XM, et al. Delineating the role of glutathione peroxidase 4 in protecting cells against lipid hydroperoxide damage and in Alzheimer's disease. Antioxid Redox Signal. 2010;12(7):819–827.
  • Zhang L, Fang Y, Lian Y, et al. Brain-derived neurotrophic factor ameliorates learning deficits in a rat model of Alzheimer's disease induced by aβ1-42. PLoS One. 2015;10(4):e0122415
  • Zhang L, Fang Y, Xu Y, et al. Curcumin improves amyloid β-peptide (1-42) induced spatial memory deficits through BDNF-ERK signaling pathway. PLoS One. 2015;10(6):e0131525.
  • Zhang T, Chen D, Lee TH. Molecular sciences phosphorylation signaling in APP processing in Alzheimer’s disease. IJMS. 2019;21(1):209.
  • Zhang T, Chen D, Lee TH. Phosphorylation signaling in APP processing in Alzheimer’s disease. Int J Mol Sci. 2020;21:209.
  • Shin E-J, Jhoo JH, Nabeshima T, et al. Growth hormone releaser attenuates beta-amyloid (1–42)-induced memory impairment in mice. J Pharmacol Sci. 2005;99(1):117–120.
  • Shin EJ, Chae JS, Park SJ, et al. Growth hormone-releaser diet attenuates beta-amyloid(1-42)-induced cognitive impairment via stimulation of the insulin-like growth factor (IGF)-1 receptor in mice. J Pharmacol Sci. 2009;109(1):139–143.
  • Yeung JHY, Palpagama TH, Tate WP, et al. The acute effects of amyloid-beta1–42 on glutamatergic receptor and transporter expression in the mouse hippocampus. Front Neurosci. 2020;13:1427.
  • Calvo-Flores Guzmán B, Elizabeth Chaffey T, Hansika Palpagama T, et al. The interplay between beta-amyloid 1–42 (Aβ1–42)-induced hippocampal inflammatory response, p-tau, vascular pathology, and their synergistic contributions to neuronal death and behavioral deficits. Front Mol Neurosci. 2020;13:196.
  • He TC, Zhou S, Da Costa LT, et al. A simplified system for generating recombinant adenoviruses. Proc Natl Acad Sci USA. 1998;95(5):2509–2514.
  • Jin CH, Shin EJ, Park JB, et al. Fustin flavonoid attenuates beta-amyloid (1-42)-induced learning impairment. J Neurosci Res. 2009;87(16):3658–3670.
  • Kim HJ, Shin EJ, Lee BH, et al. Oral administration of gintonin attenuates cholinergic impairments by scopolamine, amyloid-β protein, and mouse model of Alzheimer's disease. Mol Cells. 2015;38(9):796–805.
  • Chao LP, Wolfgram F. Spectrophotometric assay for choline acetyltransferase. Anal Biochem. 1972;46(1):114–118.
  • Mai HN, Sharma N, Shin E-J, et al. Exposure to far-infrared rays attenuates methamphetamine-induced recognition memory impairment via modulation of the muscarinic M1 receptor, Nrf2, and PKC. Neurochem Int. 2018;116:63–76.
  • Tran T-V, Shin E-J, Jeong JH, et al. Protective potential of the glutathione peroxidase-1 gene in abnormal behaviors induced by phencyclidine in mice. Mol Neurobiol. 2017;54(9):7042–7062.
  • Shin EJ, Nam Y, Tu THT, et al. Protein kinase Cδ mediates trimethyltin-induced neurotoxicity in mice in vivo via inhibition of glutathione defense mechanism. Arch Toxicol. 2016;90(4):937–953.
  • Nguyen BT, Sharma N, Shin E-J, et al. Theanine attenuates memory impairments induced by klotho gene depletion in mice. Food Funct. 2019;10(1):325–332.
  • Mai HN, Sharma N, Shin E-J, et al. Exposure to far-infrared ray attenuates methamphetamine-induced impairment in recognition memory through inhibition of protein kinase C δ in male mice: Comparison with the antipsychotic clozapine. J Neurosci Res. 2018;96:1294–1310.
  • Tran TV, Shin EJ, Nguyen LTT, et al. Protein kinase Cδ gene depletion protects against methamphetamine-induced impairments in recognition memory and ERK1/2 signaling via upregulation of glutathione peroxidase-1 gene. Mol Neurobiol. 2018;55(5):4136–4159.
  • Nagai T, Yamada K, Kim HC, et al. Cognition impairment in the genetic model of aging klotho gene mutant mice: a role of oxidative stress. Faseb J. 2003;17(1):50–52.
  • Castro MG, Candolfi M, Wilson TJ, et al. Adenoviral vector-mediated gene therapy for gliomas: coming of age. Expert Opin Biol Ther. 2014;14(9):1241–1257.
  • Kantor B, Bailey RM, Wimberly K, et al. Methods for gene transfer to the central nervous system. Advances in genetics. 2014; 125–197.
  • Lentz TB, Gray SJ, Samulski RJ. Viral vectors for gene delivery to the central nervous system. Neurobiol Dis. 2012;48(2):179–188.
  • Nakajima A, Aoyama Y, Shin EJ, et al. Nobiletin, a citrus flavonoid, improves cognitive impairment and reduces soluble Aβ levels in a triple transgenic mouse model of Alzheimer's disease (3XTg-AD)). Behav Brain Res. 2015;289:69–77.
  • Ma X-H, Zhong P, Gu Z, et al. Muscarinic potentiation of GABA(A) receptor currents is gated by insulin signaling in the prefrontal cortex. J Neurosci. 2003;23(4):1159–1168.
  • Levey AI, Kitt CA, Simonds WF, et al. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci. 1991;11(10):3218–3226.
  • Lebois EP, Thorn C, Edgerton JR, et al. Muscarinic receptor subtype distribution in the central nervous system and relevance to aging and Alzheimer's disease. Neuropharmacology. 2018;136(Pt C):362–373.
  • Wolf BA, Wertkin AM, Jolly YC, et al. Muscarinic regulation of Alzheimer's disease amyloid precursor protein secretion and amyloid beta-protein production in human neuronal NT2N cells. J Biol Chem. 1995;270(9):4916–4922.
  • Nitsch RM, Slack BE, Wurtman RJ, et al. Release of Alzheimer amyloid precursor derivatives stimulated by activation of muscarinic acetylcholine receptors. Science. 1992;258(5080):304–307.
  • Haring R, Fisher A, Marciano D, et al. Mitogen-activated protein kinase-dependent and protein kinase C-dependent pathways link the m1 Muscarinic receptor to beta-amyloid precursor protein secretion. J Neurochem. 1998;71(5):2094–2103.
  • Farías GG, Godoy JA, Hernández F, et al. M1 muscarinic receptor activation protects neurons from beta-amyloid toxicity. A role for Wnt signaling pathway. Neurobiol Dis. 2004;17(2):337–348.
  • Caccamo A, Oddo S, Billings LM, et al. M1 receptors play a central role in modulating AD-like pathology in transgenic mice. Neuron. 2006;49(5):671–682.
  • Chintamaneni PK, Krishnamurthy PT, Rao PV, et al. Surface modified nano-lipid drug conjugates of positive allosteric modulators of M1 muscarinic acetylcholine receptor for the treatment of Alzheimer's disease. Med Hypotheses. 2017;101:17–22.
  • Fisher A. M1 muscarinic agonists target major hallmarks of Alzheimer's disease-an update. Curr Alzheimer Res. 2007;4(5):577–580.
  • Tzavara ET, Bymaster FP, Felder CC, et al. Dysregulated hippocampal acetylcholine neurotransmission and impaired cognition in M2, M4 and M2/M4 muscarinic receptor knockout mice. Mol Psychiatry. 2003;8(7):673–679.
  • Mulugeta E, Karlsson E, Islam A, et al. Loss of muscarinic M4 receptors in hippocampus of Alzheimer patients. Brain Res. 2003;960(1-2):259–262.
  • Kihara T, Shimohama S, Urushitani M, et al. Stimulation of alpha4beta2 nicotinic acetylcholine receptors inhibits beta-amyloid toxicity. Brain Res. 1998;792(2):331–334.
  • Levin ED, Bradley A, Addy N, et al. Hippocampal α7 and α4β2 nicotinic receptors and working memory. Neuroscience. 2002;109(4):757–765.
  • Corrigan FM, Van Rhijn AG, Ijomah G, et al. Tin and fatty acids in dementia. Prostaglandins, Leukot Essent Fat Acids. 1991;43(4):229–238.
  • Martin F, Corrigan FM, Donard OF, et al. Organotin compounds in trimethyltin-treated rats and in human brain in Alzheimer's disease. Hum Exp Toxicol. 1997;16(9):512–515.
  • Liu M, Sun A, Shin E-J, et al. Expression of microsomal epoxide hydrolase is elevated in Alzheimer's hippocampus and induced by exogenous beta-amyloid and trimethyl-tin. Eur J Neurosci. 2006;23(8):2027–2034.
  • Andjus PR, Bataveljić D, Vanhoutte G, et al. In vivo morphological changes in animal models of amyotrophic lateral sclerosis and Alzheimer's-like disease: MRI approach. Anat Rec (Hoboken)). 2009;292(12):1882–1892.
  • Kassed CA, Butler TL, Navidomskis MT, et al. Mice expressing human mutant presenilin-1 exhibit decreased activation of NF-κB p50 in hippocampal neurons after injury. Brain Res Mol Brain Res. 2003;110(1):152–157.
  • Kim BK, Tran HYP, Shin EJ, et al. IL-6 attenuates trimethyltin-induced cognitive dysfunction via activation of JAK2/STAT3, M1 mAChR and ERK signaling network. Cell Signal. 2013;25(6):1348–1360.
  • Park SJ, Shin EJ, Min SS, et al. Inactivation of JAK2/STAT3 signaling axis and downregulation of m1 mAChR cause cognitive impairment in klotho mutant mice, a genetic model of aging. Neuropsychopharmacology. 2013;38(8):1426–1437.
  • Kuro-O M, Matsumura Y, Aizawa H, et al. Mutation of the mouse klotho gene leads to a syndrome resembling ageing. Nature. 1997;390(6655):45–51.
  • Hellweg R, Jockers-Scherübl M. Neurotrophic factors in memory disorders. Life Sci. 1994;55(25-26):2165–2169.
  • Thöne J, Ellrichmann G, Seubert S, et al. Modulation of autoimmune demyelination by laquinimod via induction of brain-derived neurotrophic factor. Am J Pathol. 2012;180(1):267–274.
  • Tong L, Thornton PL, Balazs R, et al. Beta -amyloid-(1-42) impairs activity-dependent cAMP-response element-binding protein signaling in neurons at concentrations in which cell survival Is not compromised. J Biol Chem. 2001;276(20):17301–17306.
  • Cheng WH, Ho YS, Valentine BA, et al. Cellular glutathione peroxidase is the mediator of body selenium to protect against paraquat lethality in transgenic mice. J Nutr. 1998;128(7):1070–1076.
  • Martini F, Rosa SG, Klann IP, et al. A multifunctional compound ebselen reverses memory impairment, apoptosis and oxidative stress in a mouse model of sporadic Alzheimer's disease. J Psychiatr Res. 2019;109:107–117.
  • Martini F, Pesarico AP, Brüning CA, et al. Ebselen inhibits the activity of acetylcholinesterase globular isoform G4 in vitro and attenuates scopolamine-induced amnesia in mice. J Cell Biochem. 2018;119(7):5598–5608.
  • Xie Y, Tan Y, Zheng Y, et al. Ebselen ameliorates β-amyloid pathology, tau pathology, and cognitive impairment in triple-transgenic Alzheimer's disease mice. J Biol Inorg Chem. 2017;22(6):851–865.

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