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CNS & Neurological Disorders - Drug Targets

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ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

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Research Article

Conifer Essential Oils Reversed Amyloid Beta1-42 Action by Modulating BDNF and ARC Expression in The Rat Hippocampus

Author(s): Paula Alexandra Postu, Adrian Tiron, Crina Elena Tiron, Dragoș Lucian Gorgan, Marius Mihasan and Lucian Hritcu*

Volume 21, Issue 1, 2022

Published on: 02 March, 2021

Page: [85 - 94] Pages: 10

DOI: 10.2174/1871527320666210303111537

Price: $65

Abstract

Background: The conifer species Pinus halepensis (Pinaceae) and Tetraclinis articulata (Cupressaceae) are widely used in traditional medicine due to their beneficial health properties.

Objective: This study aimed to investigate the mechanisms by which P. halepensis and T. articulata essential oils (1% and 3%) could exhibit neuroprotective effects in an Alzheimer's disease (AD) rat model, induced by intracerebroventricular (i.c.v.) administration of amyloid beta1-42 (Aβ1-42).

Methods: The essential oils were administered by inhalation to the AD rat model, once daily, for 21 days. DNA fragmentation was assessed through a Cell Death Detection ELISA kit. Brainderived neurotrophic factor (BDNF), activity-regulated cytoskeleton-associated protein (ARC), and interleukin-1β (IL-1β) gene expressions were determined by RT-qPCR analysis, while BDNF and ARC protein expressions were assessed using immunohistochemistry technique.

Results: Our data showed that both essential oils substantially attenuated memory impairments, with P. halepensis mainly stimulating ARC expression and T. articulata mostly enhancing BDNF expression. Also, the inhalation of essential oils reduced IL-1β expression and induced positive effects against DNA fragmentation associated with Aβ1-42-induced toxicity, further contributing to the cognitive improvement in the rats with the AD-like model

Conclusion: Our findings provide further evidence that these essential oils and their chemical constituents could be natural agents of therapeutic interest against Aβ1-42-induced neurotoxicity.

Keywords: Pinus halepensis, Tetraclinis articulata, amyloid-beta peptide, memory, neuroprotection, Alzheimer’s disease.

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[1]
Johnston MV, Alemi L, Harum KH. Learning, memory, and transcription factors. Pediatr Res 2003; 53(3): 369-74.
[http://dx.doi.org/10.1203/01.PDR.0000049517.47493.E9] [PMID: 12595582]
[2]
Camina E, Güell F. The Neuroanatomical, Neurophysiological and Psychological Basis of Memory: Current Models and Their Origins. Front Pharmacol 2017; 8(438): 438.
[http://dx.doi.org/10.3389/fphar.2017.00438] [PMID: 28713278]
[3]
Bisaz R, Travaglia A, Alberini CM. The neurobiological bases of memory formation: from physiological conditions to psychopathology. Psychopathology 2014; 47(6): 347-56.
[http://dx.doi.org/10.1159/000363702] [PMID: 25301080]
[4]
Tadi M, Allaman I, Lengacher S, Grenningloh G, Magistretti PJ. Learning-induced gene expression in the hippocampus reveals a role of neuron -astrocyte metabolic coupling in long term memory. PloS one 2015; 10: e0141568.
[5]
Alonso M, Vianna MR, Depino AM, et al. BDNF-triggered events in the rat hippocampus are required for both short- and long-term memory formation. Hippocampus 2002; 12(4): 551-60.
[http://dx.doi.org/10.1002/hipo.10035] [PMID: 12201640]
[6]
Bekinschtein P, Cammarota M, Katche C, et al. BDNF is essential to promote persistence of long-term memory storage. Proc Natl Acad Sci USA 2008; 105(7): 2711-6.
[http://dx.doi.org/10.1073/pnas.0711863105] [PMID: 18263738]
[7]
Lu Y, Christian K, Lu B. BDNF: a key regulator for protein synthesis-dependent LTP and long-term memory? Neurobiol Learn Mem 2008; 89(3): 312-23.
[http://dx.doi.org/10.1016/j.nlm.2007.08.018] [PMID: 17942328]
[8]
Miranda M, Morici JF, Zanoni MB, Bekinschtein P. Brain-Derived Neurotrophic Factor: A Key Molecule for Memory in the Healthy and the Pathological Brain. Front Cell Neurosci 2019; 13: 363.
[http://dx.doi.org/10.3389/fncel.2019.00363] [PMID: 31440144]
[9]
Panja D, Bramham CR. BDNF mechanisms in late LTP formation: A synthesis and breakdown. Neuropharmacology 2014; 76(Pt C): 664-76.
[http://dx.doi.org/10.1016/j.neuropharm.2013.06.024] [PMID: 23831365]
[10]
Bermúdez-Rattoni F. Frontiers in Neuroscience Neural Plasticity and Memory: From Genes to Brain Imaging Boca Raton (FL). Boca Raton, FL: CRC Press/Taylor & Francis, LLC 2007.
[http://dx.doi.org/10.1201/9781420008418]
[11]
Farris S, Lewandowski G, Cox CD, Steward O. Selective localization of arc mRNA in dendrites involves activity- and translation-dependent mRNA degradation. J Neurosci 2014; 34(13): 4481-93.
[http://dx.doi.org/10.1523/JNEUROSCI.4944-13.2014] [PMID: 24671994]
[12]
Kuipers SD, Trentani A, Tiron A, Mao X, Kuhl D, Bramham CR. BDNF-induced LTP is associated with rapid Arc/Arg3.1-dependent enhancement in adult hippocampal neurogenesis. Sci Rep 2016; 6(1): 21222.
[http://dx.doi.org/10.1038/srep21222] [PMID: 26888068]
[13]
Zheng F, Luo Y, Wang H. Regulation of brain-derived neurotrophic factor-mediated transcription of the immediate early gene Arc by intracellular calcium and calmodulin. J Neurosci Res 2009; 87(2): 380-92.
[http://dx.doi.org/10.1002/jnr.21863] [PMID: 18798281]
[14]
Yin Y, Edelman GM, Vanderklish PW. The brain-derived neurotrophic factor enhances synthesis of Arc in synaptoneurosomes. Proc Natl Acad Sci USA 2002; 99(4): 2368-73.
[http://dx.doi.org/10.1073/pnas.042693699] [PMID: 11842217]
[15]
Chen GF, Xu TH, Yan Y, et al. Amyloid beta: structure, biology and structure-based therapeutic development. Acta Pharmacol Sin 2017; 38(9): 1205-35.
[http://dx.doi.org/10.1038/aps.2017.28] [PMID: 28713158]
[16]
Gouras GK, Olsson TT, Hansson O. β-Amyloid peptides and amyloid plaques in Alzheimer’s disease. Neurotherapeutics 2015; 12(1): 3-11.
[http://dx.doi.org/10.1007/s13311-014-0313-y] [PMID: 25371168]
[17]
Sadigh-Eteghad S, Sabermarouf B, Majdi A, Talebi M, Farhoudi M, Mahmoudi J. Amyloid-beta: a crucial factor in Alzheimer’s disease. Med Princ Pract 2015; 24(1): 1-10.
[http://dx.doi.org/10.1159/000369101] [PMID: 25471398]
[18]
Palop JJ, Chin J, Bien-Ly N, et al. Vulnerability of dentate granule cells to disruption of arc expression in human amyloid precursor protein transgenic mice. J Neurosci 2005; 25(42): 9686-93.
[http://dx.doi.org/10.1523/JNEUROSCI.2829-05.2005] [PMID: 16237173]
[19]
Wang DC, Chen SS, Lee YC, Chen TJ. Amyloid-beta at sublethal level impairs BDNF-induced arc expression in cortical neurons. Neurosci Lett 2006; 398(1-2): 78-82.
[http://dx.doi.org/10.1016/j.neulet.2005.12.057] [PMID: 16412575]
[20]
Tong L, Balazs R, Thornton PL, Cotman CW. Beta-amyloid peptide at sublethal concentrations downregulates brain-derived neurotrophic factor functions in cultured cortical neurons. J Neurosci 2004; 24(30): 6799-809.
[http://dx.doi.org/10.1523/JNEUROSCI.5463-03.2004] [PMID: 15282285]
[21]
Zhang L, Fang Y, Xu Y, Lian Y, Xie N, Wu T, et al. Curcumin Improves Amyloid β-Peptide (1-42) Induced Spatial Memory Deficits through BDNF-ERK Signaling Pathway. PloS one 2015; 10(6): e0131525-.
[22]
Peng S, Garzon DJ, Marchese M, et al. Decreased brain-derived neurotrophic factor depends on amyloid aggregation state in transgenic mouse models of Alzheimer’s disease. J Neurosci 2009; 29(29): 9321-9.
[http://dx.doi.org/10.1523/JNEUROSCI.4736-08.2009] [PMID: 19625522]
[23]
Peng S, Wuu J, Mufson EJ, Fahnestock M. Precursor form of brain-derived neurotrophic factor and mature brain-derived neurotrophic factor are decreased in the pre-clinical stages of Alzheimer’s disease. J Neurochem 2005; 93(6): 1412-21.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03135.x] [PMID: 15935057]
[24]
Garzon D, Yu G, Fahnestock M. A new brain-derived neurotrophic factor transcript and decrease in brain-derived neurotrophic factor transcripts 1, 2 and 3 in Alzheimer’s disease parietal cortex. J Neurochem 2002; 82(5): 1058-64.
[http://dx.doi.org/10.1046/j.1471-4159.2002.01030.x] [PMID: 12358753]
[25]
Takada E, Okubo K, Yano Y, et al. Molecular Mechanism of Apoptosis by Amyloid β-Protein Fibrils Formed on Neuronal Cells. ACS Chem Neurosci 2020; 11(5): 796-805.
[http://dx.doi.org/10.1021/acschemneuro.0c00011] [PMID: 32056421]
[26]
Awasthi A, Matsunaga Y, Yamada T. Amyloid-beta causes apoptosis of neuronal cells via caspase cascade, which can be prevented by amyloid-beta-derived short peptides. Exp Neurol 2005; 196(2): 282-9.
[http://dx.doi.org/10.1016/j.expneurol.2005.08.001] [PMID: 16137679]
[27]
Han X-J, Hu Y-Y, Yang Z-J, et al. Amyloid β-42 induces neuronal apoptosis by targeting mitochondria. Mol Med Rep 2017; 16(4): 4521-8.
[http://dx.doi.org/10.3892/mmr.2017.7203] [PMID: 28849115]
[28]
Kim JH. Brain-derived neurotrophic factor exerts neuroprotective actions against amyloid β-induced apoptosis in neuroblastoma cells. Exp Ther Med 2014; 8(6): 1891-5.
[http://dx.doi.org/10.3892/etm.2014.2033] [PMID: 25371750]
[29]
Sun Z, Ma X, Yang H, Zhao J, Zhang J. Brain-derived neurotrophic factor prevents beta- amyloid-induced apoptosis of pheochromocytoma cells by regulating Bax/Bcl-2 expression. Neural Regen Res 2012; 7(5): 347-51.
[http://dx.doi.org/10.3969/j.issn.1673-5374.2012.05.004] [PMID: 25774173]
[30]
Alasmari F, Alshammari MA, Alasmari AF, Alanazi WA, Alhazzani K. Neuroinflammatory Cytokines Induce Amyloid Beta Neurotoxicity through Modulating Amyloid Precursor Protein Levels/Metabolism. BioMed Res Int 2018; 2018: 3087475.
[http://dx.doi.org/10.1155/2018/3087475] [PMID: 30498753]
[31]
Zheng C, Zhou X-W, Wang J-Z. The dual roles of cytokines in Alzheimer’s disease: update on interleukins, TNF-α, TGF-β and IFN-γ. Transl Neurodegener 2016; 5: 7-7.
[http://dx.doi.org/10.1186/s40035-016-0054-4] [PMID: 27054030]
[32]
Martini AC, Gomez-Arboledas A, Forner S, et al. Amyloid-beta impairs TOM1-mediated IL-1R1 signaling. Proc Natl Acad Sci USA 2019; 116(42): 21198-206.
[http://dx.doi.org/10.1073/pnas.1914088116] [PMID: 31570577]
[33]
Kitazawa M, Cheng D, Tsukamoto MR, et al. Blocking IL-1 signaling rescues cognition, attenuates tau pathology, and restores neuronal β-catenin pathway function in an Alzheimer’s disease model. J Immunol 2011; 187(12): 6539-49.
[http://dx.doi.org/10.4049/jimmunol.1100620] [PMID: 22095718]
[34]
Song C, Zhang Y, Dong Y. Acute and subacute IL-1β administrations differentially modulate neuroimmune and neurotrophic systems: possible implications for neuroprotection and neurodegeneration. J Neuroinflammation 2013; 10(1): 59.
[http://dx.doi.org/10.1186/1742-2094-10-59] [PMID: 23651534]
[35]
Tong L, Prieto GA, Kramár EA, et al. Brain-derived neurotrophic factor-dependent synaptic plasticity is suppressed by interleukin-1β via p38 mitogen-activated protein kinase. J Neurosci 2012; 32(49): 17714-24.
[http://dx.doi.org/10.1523/JNEUROSCI.1253-12.2012] [PMID: 23223292]
[36]
Hein AM, Stasko MR, Matousek SB, et al. Sustained hippocampal IL-1beta overexpression impairs contextual and spatial memory in transgenic mice. Brain Behav Immun 2010; 24(2): 243-53.
[http://dx.doi.org/10.1016/j.bbi.2009.10.002] [PMID: 19825412]
[37]
Scuteri D, Morrone LA, Rombolà L, et al. Aromatherapy and Aromatic Plants for the Treatment of Behavioural and Psychological Symptoms of Dementia in Patients with Alzheimer’s Disease: Clinical Evidence and Possible Mechanisms. Evid Based Complement Alternat Med 2017; 2017: 9416305-5.
[http://dx.doi.org/10.1155/2017/9416305] [PMID: 28465709]
[38]
Ballard CG, O’Brien JT, Reichelt K, Perry EK. Aromatherapy as a safe and effective treatment for the management of agitation in severe dementia: the results of a double-blind, placebo-controlled trial with Melissa. J Clin Psychiatry 2002; 63(7): 553-8.
[http://dx.doi.org/10.4088/JCP.v63n0703] [PMID: 12143909]
[39]
Burns A, Perry E, Holmes C, et al. A double-blind placebo-controlled randomized trial of Melissa officinalis oil and donepezil for the treatment of agitation in Alzheimer’s disease. Dement Geriatr Cogn Disord 2011; 31(2): 158-64.
[http://dx.doi.org/10.1159/000324438] [PMID: 21335973]
[40]
Jimbo D, Kimura Y, Taniguchi M, Inoue M, Urakami K. Effect of aromatherapy on patients with Alzheimer’s disease. Psychogeriatrics 2009; 9(4): 173-9.
[http://dx.doi.org/10.1111/j.1479-8301.2009.00299.x] [PMID: 20377818]
[41]
Birks J, Grimley Evans J. Ginkgo biloba for cognitive impairment and dementia. Cochrane Database Syst Rev 2007; (2): CD003120.
[http://dx.doi.org/10.1002/14651858.CD003120.pub2] [PMID: 17443523]
[42]
Bouzenna H, Samout N, Amani E, et al. Protective Effects of Pinus halepensis L. Essential Oil on Aspirin-induced Acute Liver and Kidney Damage in Female Wistar Albino Rats. J Oleo Sci 2016; 65(8): 701-12.
[http://dx.doi.org/10.5650/jos.ess15287] [PMID: 27430382]
[43]
Daoudi A, Aarab L, Abdel-Sattar E. Screening of immunomodulatory activity of total and protein extracts of some Moroccan medicinal plants. Toxicol Ind Health 2013; 29(3): 245-53.
[http://dx.doi.org/10.1177/0748233711430972] [PMID: 22301818]
[44]
Süntar I, Tumen I, Ustün O, Keleş H, Akkol EK. Appraisal on the wound healing and anti-inflammatory activities of the essential oils obtained from the cones and needles of Pinus species by in vivo and in vitro experimental models. J Ethnopharmacol 2012; 139(2): 533-40.
[http://dx.doi.org/10.1016/j.jep.2011.11.045] [PMID: 22155393]
[45]
Djouahri A, Saka B, Boudarene L, Benseradj F, Aberrane S, Aitmoussa S, et al. In vitro synergistic/antagonistic antibacterial and anti-inflammatory effect of various extracts/essential oil from cones of Tetraclinis articulata (Vahl) Masters with antibiotic and anti-inflammatory agents. Ind Crops Prod 2014; 56: 60-6.
[http://dx.doi.org/10.1016/j.indcrop.2014.02.035]
[46]
El Jemli M, Kamal R, Marmouzi I, et al. Chemical composition, acute toxicity, antioxidant and anti-inflammatory activities of Moroccan Tetraclinis articulata L. J Tradit Complement Med 2016; 7(3): 281-7.
[http://dx.doi.org/10.1016/j.jtcme.2016.06.006] [PMID: 28725621]
[47]
Ustun O, Senol FS, Kurkcuoglu M, Orhan IE, Kartal M, Baser KHC. Investigation on chemical composition, anticholinesterase and antioxidant activities of extracts and essential oils of Turkish Pinus species and pycnogenol. Ind Crops Prod 2012; 38: 115-23.
[http://dx.doi.org/10.1016/j.indcrop.2012.01.016]
[48]
Dhibi M, Issaoui M, Brahmi F, et al. Nutritional quality of fresh and heated Aleppo pine (Pinus halepensis Mill.) seed oil: trans-fatty acid isomers profiles and antioxidant properties. J Food Sci Technol 2014; 51(8): 1442-52.
[http://dx.doi.org/10.1007/s13197-012-0664-5] [PMID: 25114334]
[49]
Emami SA, Shahani A, Hassanzadeh Khayyat M. Antioxidant activity of leaves and fruits of cultivated conifers in iran. Jundishapur J Nat Pharm Prod 2013; 8(3): 113-7.
[http://dx.doi.org/10.17795/jjnpp-9670] [PMID: 24624199]
[50]
Chikhoune AHM, Kerbouche L, Baaliouamer A, Aissat K. Tetraclinis articulata (Vahl) Masters essential oils: chemical composition and biological activities. J Essent Oil Res 2013; 25(4): 300-7.
[http://dx.doi.org/10.1080/10412905.2013.774625]
[51]
Jemia MB, Chaabane S, Senatore F, Bruno M, Kchouk ME. Studies on the antioxidant activity of the essential oil and extract of Tunisian Tetraclinis articulata (Vahl) Mast. (Cupressaceae). Nat Prod Res 2013; 27(16): 1419-30.
[http://dx.doi.org/10.1080/14786419.2012.717289] [PMID: 23082942]
[52]
Postu PA, Sadiki FZ, El Idrissi M, et al. Pinus halepensis essential oil attenuates the toxic Alzheimer’s amyloid beta (1-42)-induced memory impairment and oxidative stress in the rat hippocampus. Biomed Pharmacother 2019; 112: 108673.
[http://dx.doi.org/10.1016/j.biopha.2019.108673] [PMID: 30784941]
[53]
Sadiki FZ, Idrissi ME, Cioanca O, et al. Tetraclinis articulata essential oil mitigates cognitive deficits and brain oxidative stress in an Alzheimer’s disease amyloidosis model. Phytomedicine 2019; 56: 57-63.
[http://dx.doi.org/10.1016/j.phymed.2018.10.032] [PMID: 30668354]
[54]
Paxinos G, Watson C. The rat brain in stereotaxiccoordinates. 6th ed. San Diego, CA, USA: Academic Press 2005.
[55]
Aydin E, Hritcu L, Dogan G, Hayta S, Bagci E. The Effects of Inhaled Pimpinella peregrina Essential Oil on Scopolamine-Induced Memory Impairment, Anxiety, and Depression in Laboratory Rats. Mol Neurobiol 2016; 53(9): 6557-67.
[http://dx.doi.org/10.1007/s12035-016-9693-9] [PMID: 26768430]
[56]
Postu PA, Gorgan DL, Cioanca O, et al. Memory-Enhancing Effects of Origanum majorana Essential Oil in an Alzheimer’s Amyloid beta1-42 Rat Model: A Molecular and Behavioral Study. Antioxidants 2020; 9(10): 919.
[http://dx.doi.org/10.3390/antiox9100919] [PMID: 32993114]
[57]
Postu PA, Noumedem JAK, Cioanca O, et al. Lactuca capensis reverses memory deficits in Aβ1-42-induced an animal model of Alzheimer’s disease. J Cell Mol Med 2018; 22(1): 111-22.
[http://dx.doi.org/10.1111/jcmm.13299] [PMID: 28816008]
[58]
Mizuno M, Yamada K, Olariu A, Nawa H, Nabeshima T. Involvement of brain-derived neurotrophic factor in spatial memory formation and maintenance in a radial arm maze test in rats. J Neurosci 2000; 20(18): 7116-21.
[http://dx.doi.org/10.1523/JNEUROSCI.20-18-07116.2000] [PMID: 10995859]
[59]
Palasz E, Wysocka A, Gasiorowska A, Chalimoniuk M, Niewiadomski W, Niewiadomska G. BDNF as a Promising Therapeutic Agent in Parkinson’s Disease. Int J Mol Sci 2020; 21(3): 1170.
[http://dx.doi.org/10.3390/ijms21031170] [PMID: 32050617]
[60]
Zhang L, Fang Y, Lian Y, Chen Y, Wu T, Zheng 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.
[http://dx.doi.org/10.1371/journal.pone.0122415]
[61]
Moghbelinejad S, Nassiri-Asl M, Farivar TN, et al. Rutin activates the MAPK pathway and BDNF gene expression on beta-amyloid induced neurotoxicity in rats. Toxicol Lett 2014; 224(1): 108-13.
[http://dx.doi.org/10.1016/j.toxlet.2013.10.010] [PMID: 24148604]
[62]
Khodadad A, Adelson PD, Lifshitz J, Thomas TC. The time course of activity-regulated cytoskeletal (ARC) gene and protein expression in the whisker-barrel circuit using two paradigms of whisker stimulation. Behav Brain Res 2015; 284: 249-56.
[http://dx.doi.org/10.1016/j.bbr.2015.01.032] [PMID: 25682931]
[63]
Guzowski JF, Setlow B, Wagner EK, McGaugh JL. Experience-dependent gene expression in the rat hippocampus after spatial learning: a comparison of the immediate-early genes Arc, c- fos, and zif268. J Neurosci 2001; 21(14): 5089-98.
[http://dx.doi.org/10.1523/JNEUROSCI.21-14-05089.2001] [PMID: 11438584]
[64]
Nikbakht N, Zarei B, Shirani E, Moshtaghian J, Esmaeili A, Habibian S. Experience-dependent expression of rat hippocampal Arc and Homer 1a after spatial learning on 8-arm and 12-arm radial mazes. Neuroscience 2012; 218: 49-55.
[http://dx.doi.org/10.1016/j.neuroscience.2012.05.025] [PMID: 22617701]
[65]
Ramírez-Amaya V, Vazdarjanova A, Mikhael D, Rosi S, Worley PF, Barnes CA. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 2005; 25(7): 1761-8.
[http://dx.doi.org/10.1523/JNEUROSCI.4342-04.2005] [PMID: 15716412]
[66]
Wegenast-Braun BM, Fulgencio Maisch A, Eicke D, et al. Independent effects of intra- and extracellular Abeta on learning-related gene expression. Am J Pathol 2009; 175(1): 271-82.
[http://dx.doi.org/10.2353/ajpath.2009.090044] [PMID: 19556514]
[67]
Dickey CA, Gordon MN, Mason JE, et al. Amyloid suppresses induction of genes critical for memory consolidation in APP + PS1 transgenic mice. J Neurochem 2004; 88(2): 434-42.
[http://dx.doi.org/10.1111/j.1471-4159.2004.02185.x] [PMID: 14690531]
[68]
Budni J, Feijó DP, Batista-Silva H, et al. Lithium and memantine improve spatial memory impairment and neuroinflammation induced by β-amyloid 1-42 oligomers in rats. Neurobiol Learn Mem 2017; 141: 84-92.
[http://dx.doi.org/10.1016/j.nlm.2017.03.017] [PMID: 28359852]
[69]
Shen W-X, Chen J-H, Lu J-H, Peng Y-P, Qiu Y-H. TGF-β1 protection against Aβ1-42-induced neuroinflammation and neurodegeneration in rats. Int J Mol Sci 2014; 15(12): 22092-108.
[http://dx.doi.org/10.3390/ijms151222092] [PMID: 25470026]
[70]
Kotroni E, Simirioti E, Kikionis S, et al. In vivo evaluation of the anti-inflammatory activity of electrospun micro/nanofibrous patches loaded with Pinus halepensis bark extract on hairless mice skin. Materials (Basel) 2019; 12(16): 2596.
[http://dx.doi.org/10.3390/ma12162596] [PMID: 31443178]
[71]
Rached W, Zeghada FZ, Bennaceur M, Barros L, Calhelha RC, Heleno S, et al. Phytochemical analysis and assessment of antioxidant, antimicrobial, anti-inflammatory and cytotoxic properties of Tetraclinis articulata (Vahl) Masters leaves. Ind Crops Prod 2018; 112: 460-6.
[http://dx.doi.org/10.1016/j.indcrop.2017.12.037]
[72]
Colurso GJ, Nilson JE, Vervoort LG. Quantitative assessment of DNA fragmentation and beta-amyloid deposition in insular cortex and midfrontal gyrus from patients with Alzheimer’s disease. Life Sci 2003; 73(14): 1795-803.
[http://dx.doi.org/10.1016/S0024-3205(03)00512-5] [PMID: 12888118]
[73]
Mota SI, Ferreira IL, Pereira C, Oliveira CR, Rego AC. Amyloid- beta peptide 1-42 causes microtubule deregulation through N-methyl-D-aspartate receptors in mature hippocampal cultures. Curr Alzheimer Res 2012; 9(7): 844-56.
[http://dx.doi.org/10.2174/156720512802455322] [PMID: 22631440]

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