Login Register Cart 0
Generic placeholder image

Current Medicinal Chemistry

Editor-in-Chief

ISSN (Print): 0929-8673
ISSN (Online): 1875-533X

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe Translate in Chinese
Research Article

Evaluation of the Therapeutic Effect of Lycoramine on Alzheimer’s Disease in Mouse Model

Author(s): Irem Kiris, Merve Karayel Basar, Betul Sahin, Busra Gurel, Julide Coskun, Tomasz Mroczek and Ahmet Tarik Baykal*

Volume 28, Issue 17, 2021

Published on: 16 November, 2020

Page: [3449 - 3473] Pages: 25

DOI: 10.2174/0929867327999201116193126

Price: $65

Abstract

Background: Alzheimer’s disease is one of the leading health problems characterized by the accumulation of Aβ and hyperphosphorylated tau that account for the senile plaque formations causing extensive cognitive decline. Many of the clinical diagnoses of Alzheimer’s disease are made in the late stages, when the pathological changes have already progressed.

Objective: The objective of this study is to evaluate the promising therapeutic effects of a natural compound, lycoramine, which has been shown to have therapeutic potential in several studies and to understand its mechanism of action on the molecular level via differential protein expression analyses.

Methods: Lycoramine and galantamine, an FDA approved drug used in the treatment of mild to moderate AD, were administered to 12 month-old 5xFAD mice. Effects of the compounds were investigated by Morris water maze, immunohistochemistry and label- free differential protein expression analyses.

Results: Here we demonstrated the reversal of cognitive decline via behavioral testing and the clearance of Aβ plaques. Proteomics analysis provided in-depth information on the statistically significant protein perturbations in the cortex, hippocampus and cerebellum sections to hypothesize the possible clearance mechanisms of the plaque formation and the molecular mechanism of the reversal of cognitive decline in a transgenic mouse model. Bioinformatics analyses showed altered molecular pathways that can be linked with the reversal of cognitive decline observed after lycoramine administration but not with galantamine.

Conclusion: Lycoramine shows therapeutic potential to halt and reverse cognitive decline at the late stages of disease progression, and holds great promise for the treatment of Alzheimer’s disease.

Keywords: Alzheimer's Disease, 5xFAD, Lycoramine, Galantamine, Label-free Proteomics, Neurodegeneration.

« Previous
[1]
Christina, P. World Alzheimer’s Report 2018. 2018, 1-48. Available at: https://www.alzint.org/resource/world- alzheimer-report-2018/ (Accessed date: 14.01.2020).
[2]
Dos Santos, T.C.; Gomes, T.M.; Pinto, B.A.S.; Camara, A.L.; Paes, A.M.A. Naturally occurring acetylcholinesterase inhibitors and their potential use for alzheimer’s disease therapy. Front. Pharmacol., 2018, 9, 1192.
[http://dx.doi.org/10.3389/fphar.2018.01192] [PMID: 30405413]
[3]
Yamada, K.; Nabeshima, T. Animal models of Alzheimer’s disease and evaluation of anti-dementia drugs. Pharmacol. Ther., 2000, 88(2), 93-113.
[http://dx.doi.org/10.1016/S0163-7258(00)00081-4] [PMID: 11150591]
[4]
Loy, C.; Schneider, L. Galantamine for Alzheimer’s disease and mild cognitive impairment. Cochrane Database Syst. Rev., 2006, 1(1), CD001747.
[http://dx.doi.org/10.1002/14651858.CD001747.pub3] [PMID: 16437436]
[5]
Burns, A.; Bernabei, R.; Bullock, R.; Cruz Jentoft, A.J.; Frölich, L.; Hock, C.; Raivio, M.; Triau, E.; Vandewoude, M.; Wimo, A.; Came, E.; Van Baelen, B.; Hammond, G.L.; van Oene, J.C.; Schwalen, S. Safety and efficacy of galantamine (Reminyl) in severe Alzheimer’s disease (the SERAD study): a randomised, placebo-controlled, double-blind trial. Lancet Neurol., 2009, 8(1), 39-47.
[http://dx.doi.org/10.1016/S1474-4422(08)70261-8] [PMID: 19042161]
[6]
Winblad, B.; Gauthier, S.; Scinto, L.; Feldman, H.; Wilcock, G.K.; Truyen, L.; Mayorga, A.J.; Wang, D.; Brashear, H.R.; Nye, J.S. Safety and efficacy of galantamine in subjects with mild cognitive impairment. Neurology, 2008, 70(22), 2024-2035.
[http://dx.doi.org/10.1212/01.wnl.0000303815.69777.26] [PMID: 18322263]
[7]
Tricco, A.C.; Soobiah, C.; Berliner, S.; Ho, J.M.; Ng, C.H.; Ashoor, H.M.; Chen, M.H.; Hemmelgarn, B.; Straus, S.E. Efficacy and safety of cognitive enhancers for patients with mild cognitive impairment: a systematic review and meta-analysis. CMAJ, 2013, 185(16), 1393-1401.
[http://dx.doi.org/10.1503/cmaj.130451] [PMID: 24043661]
[8]
Jin, B.R.; Liu, H.Y. Comparative efficacy and safety of cognitive enhancers for treating vascular cognitive impairment: systematic review and Bayesian network meta-analysis. Neural Regen. Res., 2019, 14(5), 805-816.
[http://dx.doi.org/10.4103/1673-5374.249228] [PMID: 30688266]
[9]
Wilcock, G.K.; Lilienfeld, S.; Gaens, E. Efficacy and safety of galantamine in patients with mild to moderate Alzheimer’s disease: multicentre randomised controlled trial. Galantamine International-1 Study Group. BMJ, 2000, 321(7274), 1445-1449.
[http://dx.doi.org/10.1136/bmj.321.7274.1445] [PMID: 11110737]
[10]
Ng, Y.P.; Or, T.C.T.; Ip, N.Y. Plant alkaloids as drug leads for Alzheimer’s disease. Neurochem. Int., 2015, 89, 260-270.
[http://dx.doi.org/10.1016/j.neuint.2015.07.018] [PMID: 26220901]
[11]
Jin, A.; Li, X.; Zhu, Y.Y.; Yu, H.Y.; Pi, H.F.; Zhang, P.; Ruan, H.L. Four new compounds from the bulbs of Lycoris aurea with neuroprotective effects against CoCl2 and H2O2-induced SH-SY5Y cell injuries. Arch. Pharm. Res., 2014, 37(3), 315-323.
[http://dx.doi.org/10.1007/s12272-013-0188-1] [PMID: 23775477]
[12]
Katoch, D.; Kumar, S.; Kumar, N.; Singh, B. Simultaneous quantification of Amaryllidaceae alkaloids from Zephyranthes grandiflora by UPLC-DAD/ESI-MS/MS. J. Pharm. Biomed. Anal., 2012, 71, 187-192.
[http://dx.doi.org/10.1016/j.jpba.2012.08.001] [PMID: 22939505]
[13]
Shawky, E.; El Sohafy, S.M.; de Andrade, J.P.; de Souza Borges, W. Profiling of acetylcholinesterase inhibitory alkaloids from some Crinum, Habranthus and Zephyranthes species by GC-MS combined with multivariate analyses and in silico studies. Nat. Prod. Res., 2021, 35(5), 807-814.
[http://dx.doi.org/10.1080/14786419.2019.1598989] [PMID: 30990078]
[14]
Cortes, N.; Alvarez, R.; Osorio, E.H.; Alzate, F.; Berkov, S.; Osorio, E. Alkaloid metabolite profiles by GC/MS and acetylcholinesterase inhibitory activities with binding- mode predictions of five Amaryllidaceae plants. J. Pharm. Biomed. Anal., 2015, 102, 222-228.
[http://dx.doi.org/10.1016/j.jpba.2014.09.022] [PMID: 25305596]
[15]
Mroczek, T. Highly efficient, selective and sensitive molecular screening of acetylcholinesterase inhibitors of natural origin by solid-phase extraction-liquid chromatography/electrospray ionisation-octopole-orthogonal acceleration time-of-flight-mass spectrometry and novel thin-layer chromatography-based bioautography. J. Chromatogr. A, 2009, 1216(12), 2519-2528.
[http://dx.doi.org/10.1016/j.chroma.2009.01.061] [PMID: 19203760]
[16]
Oakley, H.; Cole, S.L.; Logan, S.; Maus, E.; Shao, P.; Craft, J.; Guillozet-Bongaarts, A.; Ohno, M.; Disterhoft, J.; Van Eldik, L.; Berry, R.; Vassar, R. Intraneuronal β-amyloid aggregates, neurodegeneration, and neuron loss in transgenic mice with five familial Alzheimer’s disease mutations: potential factors in amyloid plaque formation. J. Neurosci., 2006, 26(40), 10129-10140.
[http://dx.doi.org/10.1523/JNEUROSCI.1202-06.2006] [PMID: 17021169]
[17]
Maarouf, C.L.; Kokjohn, T.A.; Whiteside, C.M.; Macias, M.P.; Kalback, W.M.; Sabbagh, M.N.; Beach, T.G.; Vassar, R.; Roher, A.E. Molecular differences and similarities between Alzheimer’s disease and the 5XFAD transgenic mouse model of amyloidosis. Biochem. Insights, 2013, 6, 1-10.
[http://dx.doi.org/10.4137/BCI.S13025] [PMID: 25210460]
[18]
O’Leary, T.P.; Robertson, A.; Chipman, P.H.; Rafuse, V.F.; Brown, R.E. Motor function deficits in the 12 month-old female 5xFAD mouse model of Alzheimer’s disease. Behav. Brain Res., 2018, 337, 256-263.
[http://dx.doi.org/10.1016/j.bbr.2017.09.009] [PMID: 28890389]
[19]
Gurel, B.; Cansev, M.; Sevinc, C.; Kelestemur, S.; Ocalan, B.; Cakir, A.; Aydin, S.; Kahveci, N.; Ozansoy, M.; Taskapilioglu, O.; Ulus, I.H.; Başar, M.K.; Sahin, B.; Tuzuner, M.B.; Baykal, A.T. Early stage alterations in CA1 extracellular region proteins indicate dysregulation of IL6 and iron homeostasis in the 5XFAD Alzheimer’s disease mouse model. J. Alzheimers Dis., 2018, 61(4), 1399-1410.
[http://dx.doi.org/10.3233/JAD-170329] [PMID: 29376847]
[20]
Jawhar, S.; Trawicka, A.; Jenneckens, C.; Bayer, T.A.; Wirths, O. Motor deficits, neuron loss, and reduced anxiety coinciding with axonal degeneration and intraneuronal Aβ aggregation in the 5XFAD mouse model of Alzheimer’s disease. Neurobiol. Aging, 2012, 33(1), 196.e29-196.e40.
[http://dx.doi.org/10.1016/j.neurobiolaging.2010.05.027] [PMID: 20619937]
[21]
Mroczek, T. Qualitative and quantitative two-dimensional thin-layer chromatography/high performance liquid chromatography/diode-array/electrospray-ionization-time-of-flight mass spectrometry of cholinesterase inhibitors. J. Pharm. Biomed. Anal., 2016, 129, 155-162.
[http://dx.doi.org/10.1016/j.jpba.2016.06.048] [PMID: 27424196]
[22]
Li, Z.; Liu, Y.; Wang, L.; Liu, X.; Chang, Q.; Guo, Z.; Liao, Y.; Pan, R.; Fan, T.P. Memory-enhancing effects of the crude extract of Polygala tenuifolia on aged mice. Evid. Based Complement. Alternat. Med., 2014, 2014, 392324.
[http://dx.doi.org/10.1155/2014/392324] [PMID: 24744810]
[23]
Wiśniewski, J.R.; Zougman, A.; Nagaraj, N.; Mann, M. Universal sample preparation method for proteome analysis. Nat. Methods, 2009, 6(5), 359-362.
[http://dx.doi.org/10.1038/nmeth.1322] [PMID: 19377485]
[24]
Moseley, M.A.; Hughes, C.J.; Juvvadi, P.R.; Soderblom, E.J.; Lennon, S.; Perkins, S.R.; Thompson, J.W.; Steinbach, W.J.; Geromanos, S.J.; Wildgoose, J.; Langridge, J.I.; Richardson, K.; Vissers, J.P.C. Scanning quadrupole data-independent acquisition, part a: qualitative and quantitative characterization. J. Proteome Res., 2018, 17(2), 770-779.
[http://dx.doi.org/10.1021/acs.jproteome.7b00464] [PMID: 28901143]
[25]
Gulyás, M.; Bencsik, N.; Pusztai, S.; Liliom, H.; Schlett, K. Animal tracker: an imagej-based tracking API to create a customized behaviour analyser program. Neuroinformatics, 2016, 14(4), 479-481.
[http://dx.doi.org/10.1007/s12021-016-9303-z] [PMID: 27166960]
[26]
Huang, W.; Sherman, B.T.; Lempicki, R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res., 2009, 37(1), 1-13.
[http://dx.doi.org/10.1093/nar/gkn923] [PMID: 19033363]
[27]
Huang, W.; Sherman, B.T.; Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc., 2009, 4(1), 44-57.
[http://dx.doi.org/10.1038/nprot.2008.211] [PMID: 19131956]
[28]
Metsalu, T.; Vilo, J. ClustVis: a web tool for visualizing clustering of multivariate data using Principal Component Analysis and heatmap. Nucleic Acids Res., 2015, 43(W1), W566-70.
[http://dx.doi.org/10.1093/nar/gkv468] [PMID: 25969447]
[29]
Holtzman, D.M.; Bales, K.R.; Wu, S.; Bhat, P.; Parsadanian, M.; Fagan, A.M.; Chang, L.K.; Sun, Y.; Paul, S.M. Expression of human apolipoprotein E reduces amyloid-β deposition in a mouse model of Alzheimer’s disease. J. Clin. Invest., 1999, 103(6), R15-R21.
[http://dx.doi.org/10.1172/JCI6179] [PMID: 10079115]
[30]
Kosik, K.S. The molecular and cellular biology of tau. Brain Pathol., 1993, 3(1), 39-43.
[http://dx.doi.org/10.1111/j.1750-3639.1993.tb00724.x] [PMID: 8269082]
[31]
Jackson, R.J.; Rose, J.; Tulloch, J.; Henstridge, C.; Smith, C.; Spires-Jones, T.L. Clusterin accumulates in synapses in Alzheimer’s disease and is increased in apolipoprotein E4 carriers. Brain Commun, 2019, 1(1), fcz003.
[http://dx.doi.org/10.1093/braincomms/fcz003] [PMID: 31853523]
[32]
Wu, Z.; Zhao, L.; Chen, X.; Cheng, X.; Zhang, Y. Galantamine attenuates amyloid-β deposition and astrocyte activation in APP/PS1 transgenic mice. Exp. Gerontol., 2015, 72, 244-250.
[http://dx.doi.org/10.1016/j.exger.2015.10.015] [PMID: 26521029]
[33]
Cavalli, A.; Bolognesi, M.L.; Mìnarini, A.; Rosini, M.; Tumiatti, V.; Recanatini, M.; Melchiorre, C. Multi-target-directed ligands to combat neurodegenerative diseases. J. Med. Chem., 2008, 51(3), 347-372.
[http://dx.doi.org/10.1021/jm7009364] [PMID: 18181565]
[34]
Alvarez, A.; Opazo, C.; Alarcón, R.; Garrido, J.; Inestrosa, N.C. Acetylcholinesterase promotes the aggregation of amyloid-β-peptide fragments by forming a complex with the growing fibrils. J. Mol. Biol., 1997, 272(3), 348-361.
[http://dx.doi.org/10.1006/jmbi.1997.1245] [PMID: 9325095]
[35]
Inestrosa, N.C.; Alarcón, R. Molecular interactions of acetylcholinesterase with senile plaques. J. Physiol. Paris, 1998, 92(5-6), 341-344.
[http://dx.doi.org/10.1016/S0928-4257(99)80002-3] [PMID: 9789834]
[36]
De Ferrari, G.V.; Canales, M.A.; Shin, I.; Weiner, L.M.; Silman, I.; Inestrosa, N.C. A structural motif of acetylcholinesterase that promotes amyloid β-peptide fibril formation. Biochemistry, 2001, 40(35), 10447-10457.
[http://dx.doi.org/10.1021/bi0101392] [PMID: 11523986]
[37]
Sabbagh, M.N.; Hendrix, S.; Harrison, J.E. FDA position statement “Early Alzheimer’s disease: Developing drugs for treatment, Guidance for Industry”. Alzheimers Dement. (N. Y.), 2019, 5, 13-19.
[http://dx.doi.org/10.1016/j.trci.2018.11.004] [PMID: 31650002]
[38]
Drug approval package, F.D.A. 2020 Available at: https://www.accessdata.fda.gov/drugsatfda_docs/nda/2004/021615s000_RazadyneTOC.cfm (Accessed date: 18.03.2020).
[39]
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.
[http://dx.doi.org/10.1111/j.1527-3458.2002.tb00221.x] [PMID: 12177686]
[40]
Mu, H.M.; Wang, R.; Li, X.D.; Jiang, Y.M.; Peng, F.; Xia, B. Alkaloid accumulation in different parts and ages of Lycoris chinensis. Z. Natforsch. C J. Biosci., 2010, 65(7-8), 458-462.
[http://dx.doi.org/10.1515/znc-2010-7-807] [PMID: 20737914]
[41]
Nair, J.J.; Rárová, L.; Strnad, M.; Bastida, J.; van Staden, J. Apoptosis-inducing effects of distichamine and narciprimine, rare alkaloids of the plant family Amaryllidaceae. Bioorg. Med. Chem. Lett., 2012, 22(19), 6195-6199.
[http://dx.doi.org/10.1016/j.bmcl.2012.08.005] [PMID: 22921081]
[42]
Sasaguri, H.; Nilsson, P.; Hashimoto, S.; Nagata, K.; Saito, T.; De Strooper, B.; Hardy, J.; Vassar, R.; Winblad, B.; Saido, T.C. APP mouse models for Alzheimer’s disease preclinical studies. EMBO J., 2017, 36(17), 2473-2487.
[http://dx.doi.org/10.15252/embj.201797397] [PMID: 28768718]
[43]
Park, J-C.; Ma, J.; Jeon, W.K.; Han, J-S. Fructus mume extracts alleviate cognitive impairments in 5XFAD transgenic mice. BMC Complement. Altern. Med., 2016, 16, 54.
[http://dx.doi.org/10.1186/s12906-016-1033-0] [PMID: 26852239]
[44]
Dineley, K.T.; Xia, X.; Bui, D.; Sweatt, J.D.; Zheng, H. Accelerated plaque accumulation, associative learning deficits, and up-regulation of alpha 7 nicotinic receptor protein in transgenic mice co-expressing mutant human presenilin 1 and amyloid precursor proteins. J. Biol. Chem., 2002, 277(25), 22768-22780.
[http://dx.doi.org/10.1074/jbc.M200164200] [PMID: 11912199]
[45]
Urano, T.; Tohda, C. Icariin improves memory impairment in Alzheimer’s disease model mice (5xFAD) and attenuates amyloid β-induced neurite atrophy. Phytother. Res., 2010, 24(11), 1658-1663.
[http://dx.doi.org/10.1002/ptr.3183] [PMID: 21031624]
[46]
Wang, D.; Fu, Q.; Zhou, Y.; Xu, B.; Shi, Q.; Igwe, B.; Matt, L.; Hell, J.W.; Wisely, E.V.; Oddo, S.; Xiang, Y.K. β2 adrenergic receptor, protein kinase A (PKA) and c-Jun N-terminal kinase (JNK) signaling pathways mediate tau pathology in Alzheimer disease models. J. Biol. Chem., 2013, 288(15), 10298-10307.
[http://dx.doi.org/10.1074/jbc.M112.415141] [PMID: 23430246]
[47]
Schneider, F.; Baldauf, K.; Wetzel, W.; Reymann, K.G. Behavioral and EEG changes in male 5xFAD mice. Physiol. Behav., 2014, 135, 25-33.
[http://dx.doi.org/10.1016/j.physbeh.2014.05.041] [PMID: 24907698]
[48]
Bouter, Y.; Kacprowski, T.; Weissmann, R.; Dietrich, K.; Borgers, H.; Brauß, A.; Sperling, C.; Wirths, O.; Albrecht, M.; Jensen, L.R.; Kuss, A.W.; Bayer, T.A. Deciphering the molecular profile of plaques, memory decline and neuron loss in two mouse models for Alzheimer’s disease by deep sequencing. Front. Aging Neurosci., 2014, 6, 75.
[http://dx.doi.org/10.3389/fnagi.2014.00075] [PMID: 24795628]
[49]
Landel, V.; Baranger, K.; Virard, I.; Loriod, B.; Khrestchatisky, M.; Rivera, S.; Benech, P.; Féron, F. Temporal gene profiling of the 5XFAD transgenic mouse model highlights the importance of microglial activation in Alzheimer’s disease. Mol. Neurodegener., 2014, 9, 33.
[http://dx.doi.org/10.1186/1750-1326-9-33] [PMID: 25213090]
[50]
French, K.L.; Bimonte-Nelson, H.A.; Granholm, A.C. Galantamine effects on memory, spatial cue utilization, and neurotrophic factors in aged female rats. Cell Transplant., 2007, 16(3), 197-205.
[http://dx.doi.org/10.3727/000000007783464759] [PMID: 17503733]
[51]
Hernandez, C.M.; Gearhart, D.A.; Parikh, V.; Hohnadel, E.J.; Davis, L.W.; Middlemore, M.L.; Warsi, S.P.; Waller, J.L.; Terry, A.V.Jr., Comparison of galantamine and donepezil for effects on nerve growth factor, cholinergic markers, and memory performance in aged rats. J. Pharmacol. Exp. Ther., 2006, 316(2), 679-694.
[http://dx.doi.org/10.1124/jpet.105.093047] [PMID: 16214877]
[52]
Barnes, C.A.; Meltzer, J.; Houston, F.; Orr, G.; McGann, K.; Wenk, G.L. Chronic treatment of old rats with donepezil or galantamine: effects on memory, hippocampal plasticity and nicotinic receptors. Neuroscience, 2000, 99(1), 17-23.
[http://dx.doi.org/10.1016/S0306-4522(00)00180-9] [PMID: 10924948]
[53]
Bhattacharya, S.; Haertel, C.; Maelicke, A.; Montag, D. Galantamine slows down plaque formation and behavioral decline in the 5XFAD mouse model of Alzheimer’s disease. PLoS One, 2014, 9(2), e89454.
[http://dx.doi.org/10.1371/journal.pone.0089454] [PMID: 24586789]
[54]
Lee, N.Y.; Kang, Y.S. The inhibitory effect of rivastigmine and galantamine on choline transport in brain capillary endothelial cells. Biomol. Ther. (Seoul), 2010, 18(1), 65-70.
[http://dx.doi.org/10.4062/biomolther.2010.18.1.065]
[55]
Matharu, B.; Gibson, G.; Parsons, R.; Huckerby, T.N.; Moore, S.A.; Cooper, L.J.; Millichamp, R.; Allsop, D.; Austen, B. Galantamine inhibits β-amyloid aggregation and cytotoxicity. J. Neurol. Sci., 2009, 280(1-2), 49-58.
[http://dx.doi.org/10.1016/j.jns.2009.01.024] [PMID: 19249060]
[56]
Takata, K.; Kitamura, Y.; Saeki, M.; Terada, M.; Kagitani, S.; Kitamura, R.; Fujikawa, Y.; Maelicke, A.; Tomimoto, H.; Taniguchi, T.; Shimohama, S. Galantamine-induced amyloid-β clearance mediated via stimulation of microglial nicotinic acetylcholine receptors. J. Biol. Chem., 2010, 285(51), 40180-40191.
[http://dx.doi.org/10.1074/jbc.M110.142356] [PMID: 20947502]
[57]
Foster, E.M.; Dangla-Valls, A.; Lovestone, S.; Ribe, E.M.; Buckley, N.J. Clusterin in Alzheimer’s disease: mechanisms, genetics, and lessons from other pathologies. Front. Neurosci., 2019, 13, 164.
[http://dx.doi.org/10.3389/fnins.2019.00164] [PMID: 30872998]
[58]
Grewal, R.P.; Morgan, T.E.; Finch, C.E. C1qB and clusterin mRNA increase in association with neurodegeneration in sporadic amyotrophic lateral sclerosis. Neurosci. Lett., 1999, 271(1), 65-67.
[http://dx.doi.org/10.1016/S0304-3940(99)00496-6] [PMID: 10471215]
[59]
Ingram, G.; Loveless, S.; Howell, O.W.; Hakobyan, S.; Dancey, B.; Harris, C.L.; Robertson, N.P.; Neal, J.W.; Morgan, B.P. Complement activation in multiple sclerosis plaques: an immunohistochemical analysis. Acta Neuropathol. Commun., 2014, 2, 53.
[http://dx.doi.org/10.1186/2051-5960-2-53] [PMID: 24887075]
[60]
Sasaki, K.; Doh-ura, K.; Wakisaka, Y.; Iwaki, T. Clusterin/apolipoprotein J is associated with cortical Lewy bodies: immunohistochemical study in cases with α-synucleinopathies. Acta Neuropathol., 2002, 104(3), 225-230.
[http://dx.doi.org/10.1007/s00401-002-0546-4] [PMID: 12172907]
[61]
Labadorf, A.; Hoss, A.G.; Lagomarsino, V.; Latourelle, J.C.; Hadzi, T.C.; Bregu, J.; MacDonald, M.E.; Gusella, J.F.; Chen, J.F.; Akbarian, S.; Weng, Z.; Myers, R.H. RNA sequence analysis of human huntington disease brain reveals an extensive increase in inflammatory and developmental gene expression. PLoS One, 2015, 10(12), e0143563.
[http://dx.doi.org/10.1371/journal.pone.0143563] [PMID: 26636579]
[62]
May, P.C.; Lampert-Etchells, M.; Johnson, S.A.; Poirier, J.; Masters, J.N.; Finch, C.E. Dynamics of gene expression for a hippocampal glycoprotein elevated in Alzheimer’s disease and in response to experimental lesions in rat. Neuron, 1990, 5(6), 831-839.
[http://dx.doi.org/10.1016/0896-6273(90)90342-D] [PMID: 1702645]
[63]
Martins, I.J.; Berger, T.; Sharman, M.J.; Verdile, G.; Fuller, S.J.; Martins, R.N. Cholesterol metabolism and transport in the pathogenesis of Alzheimer’s disease. J. Neurochem., 2009, 111(6), 1275-1308.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06408.x] [PMID: 20050287]
[64]
DeMattos, R.B.; O’dell, M.A.; Parsadanian, M.; Taylor, J.W.; Harmony, J.A.K.; Bales, K.R.; Paul, S.M.; Aronow, B.J.; Holtzman, D.M. Clusterin promotes amyloid plaque formation and is critical for neuritic toxicity in a mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 2002, 99(16), 10843-10848.
[http://dx.doi.org/10.1073/pnas.162228299] [PMID: 12145324]
[65]
Bales, K.R.; Verina, T.; Cummins, D.J.; Du, Y.; Dodel, R.C.; Saura, J.; Fishman, C.E.; DeLong, C.A.; Piccardo, P.; Petegnief, V.; Ghetti, B.; Paul, S.M.; Apolipoprotein, E. Apolipoprotein E is essential for amyloid deposition in the APP(V717F) transgenic mouse model of Alzheimer’s disease. Proc. Natl. Acad. Sci. USA, 1999, 96(26), 15233-15238.
[http://dx.doi.org/10.1073/pnas.96.26.15233] [PMID: 10611368]
[66]
Koistinaho, M.; Lin, S.; Wu, X.; Esterman, M.; Koger, D.; Hanson, J.; Higgs, R.; Liu, F.; Malkani, S.; Bales, K.R.; Paul, S.M.; Apolipoprotein, E. Apolipoprotein E promotes astrocyte colocalization and degradation of deposited amyloid-β peptides. Nat. Med., 2004, 10(7), 719-726.
[http://dx.doi.org/10.1038/nm1058] [PMID: 15195085]
[67]
Bales, K.R.; Verina, T.; Dodel, R.C.; Du, Y.; Altstiel, L.; Bender, M.; Hyslop, P.; Johnstone, E.M.; Little, S.P.; Cummins, D.J.; Piccardo, P.; Ghetti, B.; Paul, S.M. Lack of apolipoprotein E dramatically reduces amyloid β-peptide deposition. Nat. Genet., 1997, 17(3), 263-264.
[http://dx.doi.org/10.1038/ng1197-263] [PMID: 9354781]
[68]
Mak, A.C.Y.; Pullinger, C.R.; Tang, L.F.; Wong, J.S.; Deo, R.C.; Schwarz, J-M.; Gugliucci, A.; Movsesyan, I.; Ishida, B.Y.; Chu, C.; Poon, A.; Kim, P.; Stock, E.O.; Schaefer, E.J.; Asztalos, B.F.; Castellano, J.M.; Wyss-Coray, T.; Duncan, J.L.; Miller, B.L.; Kane, J.P.; Kwok, P-Y.; Malloy, M.J. Effects of the absence of apolipoprotein e on lipoproteins, neurocognitive function, and retinal function. JAMA Neurol., 2014, 71(10), 1228-1236.
[http://dx.doi.org/10.1001/jamaneurol.2014.2011] [PMID: 25111166]
[69]
Gottschalk, W.K.; Mihovilovic, M.; Roses, A.D.; Chiba-Falek, O. The role of upregulated APOE in Alzheimer’s disease etiology. J. Alzheimers Dis. Parkinsonism, 2016, 6(1), 209.
[http://dx.doi.org/10.4172/2161-0460.1000209] [PMID: 27104063]
[70]
JacksonLab. 5XFAD. 2020. Available at: https://www. jax.org/strain/006554 (Accessed date: 03.03.2020).
[71]
Mazi, A.R.; Arzuman, A.S.; Gurel, B.; Sahin, B.; Tuzuner, M.B.; Ozansoy, M.; Baykal, A.T. Neonatal neurodegeneration in Alzheimer’s disease transgenic mouse model. J Alzheimers Dis. J Alzheimers Dis Rep, 2018, 2(1), 79-91.
[http://dx.doi.org/10.3233/ADR-170049] [PMID: 30480251]
[72]
Creighton, S.D.; Mendell, A.L.; Palmer, D.; Kalisch, B.E.; MacLusky, N.J.; Prado, V.F.; Prado, M.A.M.; Winters, B.D. Dissociable cognitive impairments in two strains of transgenic Alzheimer’s disease mice revealed by a battery of object-based tests. Sci. Rep., 2019, 9(1), 57.
[http://dx.doi.org/10.1038/s41598-018-37312-0] [PMID: 30635592]
[73]
Kanno, T.; Tsuchiya, A.; Nishizaki, T. Hyperphosphorylation of Tau at Ser396 occurs in the much earlier stage than appearance of learning and memory disorders in 5XFAD mice. Behav. Brain Res., 2014, 274, 302-306.
[http://dx.doi.org/10.1016/j.bbr.2014.08.034] [PMID: 25172181]
[74]
Kang, S.; Ha, S.; Park, H.; Nam, E.; Suh, W.H.; Suh, Y.H.; Chang, K.A. Effects of a dehydroevodiamine-derivative on synaptic destabilization and memory impairment in the 5xFAD, Alzheimer’s disease mouse model. Front. Behav. Neurosci., 2018, 12, 273.
[http://dx.doi.org/10.3389/fnbeh.2018.00273] [PMID: 30483077]
[75]
Griñán-Ferré, C.; Sarroca, S.; Ivanova, A.; Puigoriol-Illamola, D.; Aguado, F.; Camins, A.; Sanfeliu, C.; Pallàs, M. Epigenetic mechanisms underlying cognitive impairment and Alzheimer disease hallmarks in 5XFAD mice. Aging (Albany NY), 2016, 8(4), 664-684.
[http://dx.doi.org/10.18632/aging.100906] [PMID: 27013617]
[76]
Roberson, E.D.; Scearce-Levie, K.; Palop, J.J.; Yan, F.; Cheng, I.H.; Wu, T.; Gerstein, H.; Yu, G.Q.; Mucke, L. Reducing endogenous tau ameliorates amyloid beta-induced deficits in an Alzheimer’s disease mouse model. Science, 2007, 316(5825), 750-754.
[http://dx.doi.org/10.1126/science.1141736] [PMID: 17478722]
[77]
Jackson, J.; Jambrina, E.; Li, J.; Marston, H.; Menzies, F.; Phillips, K.; Gilmour, G. Targeting the synapse in Alzheimer’s disease. Front. Neurosci., 2019, 13, 735.
[http://dx.doi.org/10.3389/fnins.2019.00735] [PMID: 31396031]
[78]
Davies, C.A.; Mann, D.M.A.; Sumpter, P.Q.; Yates, P.O. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer’s disease. J. Neurol. Sci., 1987, 78(2), 151-164.
[http://dx.doi.org/10.1016/0022-510X(87)90057-8] [PMID: 3572454]
[79]
Selkoe, D.J. Alzheimer’s disease is a synaptic failure. Science, 2002, 298(5594), 789-791.
[http://dx.doi.org/10.1126/science.1074069] [PMID: 12399581]
[80]
Limon, A.; Reyes-Ruiz, J.M.; Miledi, R. Loss of functional GABA(A) receptors in the Alzheimer diseased brain. Proc. Natl. Acad. Sci. USA, 2012, 109(25), 10071-10076.
[http://dx.doi.org/10.1073/pnas.1204606109] [PMID: 22691495]
[81]
Kwakowsky, A.; Calvo-Flores Guzmán, B.; Pandya, M.; Turner, C.; Waldvogel, H.J.; Faull, R.L. GABAA receptor subunit expression changes in the human Alzheimer’s disease hippocampus, subiculum, entorhinal cortex and superior temporal gyrus. J. Neurochem., 2018, 145(5), 374-392.
[http://dx.doi.org/10.1111/jnc.14325] [PMID: 29485232]
[82]
Srivastava, S.; Cohen, J.; Pevsner, J.; Aradhya, S.; McKnight, D.; Butler, E.; Johnston, M.; Fatemi, A. A novel variant in GABRB2 associated with intellectual disability and epilepsy. Am. J. Med. Genet. A., 2014, 164A(11), 2914-2921.
[http://dx.doi.org/10.1002/ajmg.a.36714] [PMID: 25124326]
[83]
Niesmann, K.; Breuer, D.; Brockhaus, J.; Born, G.; Wolff, I.; Reissner, C.; Kilimann, M.W.; Rohlmann, A.; Missler, M. Dendritic spine formation and synaptic function require neurobeachin. Nat. Commun., 2011, 2, 557.
[http://dx.doi.org/10.1038/ncomms1565] [PMID: 22109531]
[84]
Su, Y.; Balice-Gordon, R.J.; Hess, D.M.; Landsman, D.S.; Minarcik, J.; Golden, J.; Hurwitz, I.; Liebhaber, S.A.; Cooke, N.E. Neurobeachin is essential for neuromuscular synaptic transmission. J. Neurosci., 2004, 24(14), 3627-3636.
[http://dx.doi.org/10.1523/JNEUROSCI.4644-03.2004] [PMID: 15071111]
[85]
Twine, N.A.; Janitz, K.; Wilkins, M.R.; Janitz, M. Whole transcriptome sequencing reveals gene expression and splicing differences in brain regions affected by Alzheimer’s disease. PLoS One, 2011, 6(1), e16266.
[http://dx.doi.org/10.1371/journal.pone.0016266] [PMID: 21283692]
[86]
Repetto, D.; Brockhaus, J.; Rhee, H.J.; Lee, C.; Kilimann, M.W.; Rhee, J.; Northoff, L.M.; Guo, W.; Reissner, C.; Missler, M. Molecular dissection of neurobeachin function at excitatory synapses. Front. Synaptic Neurosci., 2018, 10, 28.
[http://dx.doi.org/10.3389/fnsyn.2018.00028] [PMID: 30158865]
[87]
Glavan, G.; Schliebs, R.; Zivin, M. Synaptotagmins in neurodegeneration. Anat. Rec. (Hoboken), 2009, 292(12), 1849-1862.
[http://dx.doi.org/10.1002/ar.21026] [PMID: 19943339]
[88]
Südhof, T.C. Calcium control of neurotransmitter release. Cold Spring Harb. Perspect. Biol., 2012, 4(1), a011353.
[http://dx.doi.org/10.1101/cshperspect.a011353] [PMID: 22068972]
[89]
Xu, J.; Mashimo, T.; Südhof, T.C. Synaptotagmin-1, -2, and -9: Ca(2+) sensors for fast release that specify distinct presynaptic properties in subsets of neurons. Neuron, 2007, 54(4), 567-581.
[http://dx.doi.org/10.1016/j.neuron.2007.05.004] [PMID: 17521570]
[90]
Craxton, M.; Goedert, M.; Synaptotagmin, V. Synaptotagmin V: a novel synaptotagmin isoform expressed in rat brain. FEBS Lett., 1995, 361(2-3), 196-200.
[http://dx.doi.org/10.1016/0014-5793(95)00176-A] [PMID: 7698322]
[91]
Gautam, V.; D’Avanzo, C.; Berezovska, O.; Tanzi, R.E.; Kovacs, D.M. Synaptotagmins interact with APP and promote Aβ generation. Mol. Neurodegener., 2015, 10, 31.
[http://dx.doi.org/10.1186/s13024-015-0028-5] [PMID: 26202512]
[92]
Bamburg, J.R.; Bloom, G.S. Cytoskeletal pathologies of Alzheimer disease. Cell Motil. Cytoskeleton, 2009, 66(8), 635-649.
[http://dx.doi.org/10.1002/cm.20388] [PMID: 19479823]
[93]
Martin, B.; Brenneman, R.; Becker, K.G.; Gucek, M.; Cole, R.N.; Maudsley, S. iTRAQ analysis of complex proteome alterations in 3xTgAD Alzheimer’s mice: understanding the interface between physiology and disease. PLoS One, 2008, 3(7), e2750.
[http://dx.doi.org/10.1371/journal.pone.0002750] [PMID: 18648646]
[94]
Bossenmeyer-Pourié, C.; Smith, A.D.; Lehmann, S.; Deramecourt, V.; Sablonnière, B.; Camadro, J.M.; Pourié, G.; Kerek, R.; Helle, D.; Umoret, R.; Guéant-Rodriguez, R.M.; Rigau, V.; Gabelle, A.; Sequeira, J.M.; Quadros, E.V.; Daval, J.L.; Guéant, J.L. N-homocysteinylation of tau and MAP1 is increased in autopsy specimens of Alzheimer’s disease and vascular dementia. J. Pathol., 2019, 248(3), 291-303.
[http://dx.doi.org/10.1002/path.5254] [PMID: 30734924]
[95]
Giasson, B.I.; Forman, M.S.; Higuchi, M.; Golbe, L.I.; Graves, C.L.; Kotzbauer, P.T.; Trojanowski, J.Q.; Lee, V.M-Y. Initiation and synergistic fibrillization of tau and alpha-synuclein. Science, 2003, 300(5619), 636-640.
[http://dx.doi.org/10.1126/science.1082324] [PMID: 12714745]
[96]
Yan, X.; Uronen, R.L.; Huttunen, H.J. The interaction of α-synuclein and Tau: A molecular conspiracy in neurodegeneration? Semin. Cell Dev. Biol., 2020, 99, 55-64.
[http://dx.doi.org/10.1016/j.semcdb.2018.05.005] [PMID: 29738880]
[97]
Wirths, O.; Bayer, T.A. α-synuclein, Abeta and Alzheimer’s disease. Prog. Neuropsychopharmacol. Biol. Psychiatry, 2003, 27(1), 103-108.
[http://dx.doi.org/10.1016/S0278-5846(02)00339-1] [PMID: 12551731]
[98]
Lehotzky, A.; Lau, P.; Tokési, N.; Muja, N.; Hudson, L.D.; Ovádi, J. Tubulin polymerization-promoting protein (TPPP/p25) is critical for oligodendrocyte differentiation. Glia, 2010, 58(2), 157-168.
[http://dx.doi.org/10.1002/glia.20909] [PMID: 19606501]
[99]
Oláh, J.; Vincze, O.; Virók, D.; Simon, D.; Bozsó, Z.; Tõkési, N.; Horváth, I.; Hlavanda, E.; Kovács, J.; Magyar, A.; Szũcs, M.; Orosz, F.; Penke, B.; Ovádi, J. Interactions of pathological hallmark proteins: tubulin polymerization promoting protein/p25, β-amyloid, and α-synuclein. J. Biol. Chem., 2011, 286(39), 34088-34100.
[http://dx.doi.org/10.1074/jbc.M111.243907] [PMID: 21832049]
[100]
Tirián, L.; Hlavanda, E.; Oláh, J.; Horváth, I.; Orosz, F.; Szabó, B.; Kovács, J.; Szabad, J.; Ovádi, J. TPPP/p25 promotes tubulin assemblies and blocks mitotic spindle formation. Proc. Natl. Acad. Sci. USA, 2003, 100(24), 13976-13981.
[http://dx.doi.org/10.1073/pnas.2436331100] [PMID: 14623963]
[101]
Grant, P.; Pant, H.C. Topographic regulation of kinase activity in Alzheimer’s disease brains. J. Alzheimers Dis., 2002, 4(4), 269-281.
[http://dx.doi.org/10.3233/JAD-2002-4402] [PMID: 12446929]
[102]
Maziuk, B.F.; Apicco, D.J.; Cruz, A.L.; Jiang, L.; Ash, P.E.A.; da Rocha, E.L.; Zhang, C.; Yu, W.H.; Leszyk, J.; Abisambra, J.F.; Li, H.; Wolozin, B. RNA binding proteins co-localize with small tau inclusions in tauopathy. Acta Neuropathol. Commun., 2018, 6(1), 71.
[http://dx.doi.org/10.1186/s40478-018-0574-5] [PMID: 30068389]
[103]
David, S.; Shoemaker, M.; Haley, B.E. Abnormal properties of creatine kinase in Alzheimer’s disease brain: correlation of reduced enzyme activity and active site photolabeling with aberrant cytosol-membrane partitioning. Brain Res. Mol. Brain Res., 1998, 54(2), 276-287.
[http://dx.doi.org/10.1016/S0169-328X(97)00343-4] [PMID: 9555058]
[104]
Dzeja, P.P.; Zeleznikar, R.J.; Goldberg, N.D. Adenylate kinase: kinetic behavior in intact cells indicates it is integral to multiple cellular processes. Mol. Cell. Biochem., 1998, 184(1-2), 169-182.
[http://dx.doi.org/10.1023/A:1006859632730] [PMID: 9746320]
[105]
Ianiski, F.R.; Rech, V.C.; Nishihira, V.S.K.; Alves, C.B.; Baldissera, M.D.; Wilhelm, E.A.; Luchese, C. Amyloid-β peptide absence in short term effects on kinase activity of energy metabolism in mice hippocampus and cerebral cortex. An. Acad. Bras. Cienc., 2016, 88(3 Suppl), 1829-1840.
[http://dx.doi.org/10.1590/0001-3765201620150776] [PMID: 27411072]
[106]
Park, H.; Kam, T.I.; Kim, Y.; Choi, H.; Gwon, Y.; Kim, C.; Koh, J.Y.; Jung, Y.K. Neuropathogenic role of adenylate kinase-1 in Aβ-mediated tau phosphorylation via AMPK and GSK3β. Hum. Mol. Genet., 2012, 21(12), 2725-2737.
[http://dx.doi.org/10.1093/hmg/dds100] [PMID: 22419736]
[107]
Strehler, E.E.; Thayer, S.A. Evidence for a role of plasma membrane calcium pumps in neurodegenerative disease: Recent developments. Neurosci. Lett., 2018, 663, 39-47.
[http://dx.doi.org/10.1016/j.neulet.2017.08.035] [PMID: 28827127]
[108]
Berrocal, M.; Marcos, D.; Sepúlveda, M.R.; Pérez, M.; Ávila, J.; Mata, A.M. Altered Ca2+ dependence of synaptosomal plasma membrane Ca2+-ATPase in human brain affected by Alzheimer’s disease. FASEB J., 2009, 23(6), 1826-1834.
[http://dx.doi.org/10.1096/fj.08-121459] [PMID: 19144698]
[109]
Naslavsky, N.; Caplan, S. EHD proteins: key conductors of endocytic transport. Trends Cell Biol., 2011, 21(2), 122-131.
[http://dx.doi.org/10.1016/j.tcb.2010.10.003] [PMID: 21067929]
[110]
Buggia-Prévot, V.; Fernandez, C.G.; Udayar, V.; Vetrivel, K.S.; Elie, A.; Roseman, J.; Sasse, V.A.; Lefkow, M.; Meckler, X.; Bhattacharyya, S.; George, M.; Kar, S.; Bindokas, V.P.; Parent, A.T.; Rajendran, L.; Band, H.; Vassar, R.; Thinakaran, G. A function for EHD family proteins in unidirectional retrograde dendritic transport of BACE1 and Alzheimer’s disease Aβ production. Cell Rep., 2013, 5(6), 1552-1563.
[http://dx.doi.org/10.1016/j.celrep.2013.12.006] [PMID: 24373286]
[111]
Jinwal, U.K.; O’Leary, J.C., III; Borysov, S.I.; Jones, J.R.; Li, Q.; Koren, J., III; Abisambra, J.F.; Vestal, G.D.; Lawson, L.Y.; Johnson, A.G.; Blair, L.J.; Jin, Y.; Miyata, Y.; Gestwicki, J.E.; Dickey, C.A. Hsc70 rapidly engages tau after microtubule destabilization. J. Biol. Chem., 2010, 285(22), 16798-16805.
[http://dx.doi.org/10.1074/jbc.M110.113753] [PMID: 20308058]
[112]
Dou, F.; Netzer, W.J.; Tanemura, K.; Li, F.; Hartl, F.U.; Takashima, A.; Gouras, G.K.; Greengard, P.; Xu, H. Chaperones increase association of tau protein with microtubules. Proc. Natl. Acad. Sci. USA, 2003, 100(2), 721-726.
[http://dx.doi.org/10.1073/pnas.242720499] [PMID: 12522269]
[113]
Evans, C.G.; Wisén, S.; Gestwicki, J.E. Heat shock proteins 70 and 90 inhibit early stages of amyloid β-(1-42) aggregation in vitro. J. Biol. Chem., 2006, 281(44), 33182-33191.
[http://dx.doi.org/10.1074/jbc.M606192200] [PMID: 16973602]
[114]
Bobkova, N.V.; Garbuz, D.G.; Nesterova, I.; Medvinskaya, N.; Samokhin, A.; Alexandrova, I.; Yashin, V.; Karpov, V.; Kukharsky, M.S.; Ninkina, N.N.; Smirnov, A.A.; Nudler, E.; Evgen’ev, M. Therapeutic effect of exogenous hsp70 in mouse models of Alzheimer’s disease. J. Alzheimers Dis., 2014, 38(2), 425-435.
[http://dx.doi.org/10.3233/JAD-130779] [PMID: 23985416]
[115]
Klucken, J.; Shin, Y.; Masliah, E.; Hyman, B.T.; McLean, P.J. Hsp70 Reduces α-synuclein aggregation and toxicity. J. Biol. Chem., 2004, 279(24), 25497-25502.
[http://dx.doi.org/10.1074/jbc.M400255200] [PMID: 15044495]
[116]
Eftekharzadeh, B.; Daigle, J.G.; Kapinos, L.E.; Coyne, A.; Schiantarelli, J.; Carlomagno, Y.; Cook, C.; Miller, S.J.; Dujardin, S.; Amaral, A.S.; Grima, J.C.; Bennett, R.E.; Tepper, K.; DeTure, M.; Vanderburg, C.R.; Corjuc, B.T.; DeVos, S.L.; Gonzalez, J.A.; Chew, J.; Vidensky, S.; Gage, F.H.; Mertens, J.; Troncoso, J.; Mandelkow, E.; Salvatella, X.; Lim, R.Y.H.; Petrucelli, L.; Wegmann, S.; Rothstein, J.D.; Hyman, B.T. Tau protein disrupts nucleocytoplasmic transport in Alzheimer’s disease. Neuron, 2018, 99(5), 925-940.e7.
[http://dx.doi.org/10.1016/j.neuron.2018.07.039] [PMID: 30189209]
[117]
Sultana, R.; Butterfield, D.A. Alterations of some membrane transport proteins in Alzheimer’s disease: role of amyloid β-peptide. Mol. Biosyst., 2008, 4(1), 36-41.
[http://dx.doi.org/10.1039/B715278G] [PMID: 18075672]
[118]
Stokin, G.B.; Goldstein, L.S.B. Axonal transport and Alzheimer’s disease. Annu. Rev. Biochem., 2006, 75, 607-627.
[http://dx.doi.org/10.1146/annurev.biochem.75.103004.142637] [PMID: 16756504]
[119]
Brown, J., III; Theisler, C.; Silberman, S.; Magnuson, D.; Gottardi-Littell, N.; Lee, J.M.; Yager, D.; Crowley, J.; Sambamurti, K.; Rahman, M.M.; Reiss, A.B.; Eckman, C.B.; Wolozin, B. Differential expression of cholesterol hydroxylases in Alzheimer’s disease. J. Biol. Chem., 2004, 279(33), 34674-34681.
[http://dx.doi.org/10.1074/jbc.M402324200] [PMID: 15148325]
[120]
Zerbinatti, C.V.; Cordy, J.M.; Chen, C.D.; Guillily, M.; Suon, S.; Ray, W.J.; Seabrook, G.R.; Abraham, C.R.; Wolozin, B. Oxysterol-binding protein-1 (OSBP1) modulates processing and trafficking of the amyloid precursor protein. Mol. Neurodegener., 2008, 3, 5.
[http://dx.doi.org/10.1186/1750-1326-3-5] [PMID: 18348724]
[121]
Lin, W-H.; Chiu, K.C.; Chang, H.M.; Lee, K.C.; Tai, T.Y.; Chuang, L.M. Molecular scanning of the human sorbin and SH3-domain-containing-1 (SORBS1) gene: positive association of the T228A polymorphism with obesity and type 2 diabetes. Hum. Mol. Genet., 2001, 10(17), 1753-1760.
[http://dx.doi.org/10.1093/hmg/10.17.1753] [PMID: 11532984]
[122]
Chang, T.J.; Wang, W.C.; Hsiung, C.A.; He, C.T.; Lin, M.W.; Sheu, W.H.H.; Chang, Y.C.; Quertermous, T.; Chen, Y.I.; Rotter, J.I.; Chuang, L.M.; Hwu, C.M.; Hung, Y.J.; Lee, W.J.; Te Lee, I. Genetic variation of SORBS1 gene is associated with glucose homeostasis and age at onset of diabetes: A SAPPHIRe Cohort Study. Sci. Rep., 2018, 8(1), 10574.
[http://dx.doi.org/10.1038/s41598-018-28891-z] [PMID: 30002559]
[123]
Zhang, Q.; Ma, C.; Gearing, M.; Wang, P.G.; Chin, L.S.; Li, L. Integrated proteomics and network analysis identifies protein hubs and network alterations in Alzheimer’s disease. Acta Neuropathol. Commun., 2018, 6(1), 19.
[http://dx.doi.org/10.1186/s40478-018-0524-2] [PMID: 29490708]
[124]
Hallock, P.T.; Chin, S.; Blais, S.; Neubert, T.A.; Glass, D.J. Sorbs1 and -2 interact with CrkL and are required for acetylcholine receptor cluster formation. Mol. Cell. Biol., 2015, 36(2), 262-270.
[http://dx.doi.org/10.1128/MCB.00775-15] [PMID: 26527617]
[125]
Limpert, A.S.; Karlo, J.C.; Landreth, G.E. Nerve growth factor stimulates the concentration of TrkA within lipid rafts and extracellular signal-regulated kinase activation through c-Cbl-associated protein. Mol. Cell. Biol., 2007, 27(16), 5686-5698.
[http://dx.doi.org/10.1128/MCB.01109-06] [PMID: 17548467]
[126]
Wan Nasri, W.N.; Makpol, S.; Mazlan, M.; Tooyama, I.; Wan Ngah, W.Z.; Damanhuri, H.A. Tocotrienol rich fraction supplementation modulate brain hippocampal gene expression in APPswe/PS1dE9 Alzheimer’s disease mouse model. J. Alzheimers Dis., 2019, 70(s1), S239-S254.
[http://dx.doi.org/10.3233/JAD-180496] [PMID: 30507571]
[127]
Liem, R.K.H.; Messing, A. Dysfunctions of neuronal and glial intermediate filaments in disease. J. Clin. Invest., 2009, 119(7), 1814-1824.
[http://dx.doi.org/10.1172/JCI38003] [PMID: 19587456]
[128]
Meda, L.; Baron, P.; Scarlato, G. Glial activation in Alzheimer’s disease: the role of Abeta and its associated proteins. Neurobiol. Aging, 2001, 22(6), 885-893.
[http://dx.doi.org/10.1016/S0197-4580(01)00307-4] [PMID: 11754995]
[129]
Vehmas, A.K.; Kawas, C.H.; Stewart, W.F.; Troncoso, J.C. Immune reactive cells in senile plaques and cognitive decline in Alzheimer’s disease. Neurobiol. Aging, 2003, 24(2), 321-331.
[http://dx.doi.org/10.1016/S0197-4580(02)00090-8] [PMID: 12498966]
[130]
Hertz, L.; Chen, Y.; Simon, S.A.; Gutierrez, R.; Tandon, S. Editorial: all 3 types of glial cells are important for memory formation. Front. Integr. Nuerosci., 2016, 10, 31.
[http://dx.doi.org/10.3389/fnint.2016.00031] [PMID: 27729851]
[131]
Glezer, I.; Simard, A.R.; Rivest, S. Neuroprotective role of the innate immune system by microglia. Neuroscience, 2007, 147(4), 867-883.
[http://dx.doi.org/10.1016/j.neuroscience.2007.02.055] [PMID: 17459594]
[132]
Kato, S.; Gondo, T.; Hoshii, Y.; Takahashi, M.; Yamada, M. Confocal observation of senile plaques in Alzheimer’s disease : Senile plaque morphology and relationship between senile plaques and astrocytes. 1998, 48(5), 332-340.
[http://dx.doi.org/10.1111/j.1440-1827.1998.tb03915.x] [PMID: 9704339]
[133]
Pekny, M.; Wilhelmsson, U.; Pekna, M. The dual role of astrocyte activation and reactive gliosis. Neurosci. Lett., 2014, 565, 30-38.
[http://dx.doi.org/10.1016/j.neulet.2013.12.071] [PMID: 24406153]
[134]
Fakhoury, M. Microglia and astrocytes in Alzheimer’s disease: implications for therapy. Curr. Neuropharmacol., 2018, 16(5), 508-518.
[http://dx.doi.org/10.2174/1570159X15666170720095240] [PMID: 28730967]
[135]
Porchet, R.; Probst, A.; Bouras, C.; Dráberová, E.; Dráber, P.; Riederer, B.M. Analysis of glial acidic fibrillary protein in the human entorhinal cortex during aging and in Alzheimer’s disease. Proteomics, 2003, 3(8), 1476-1485.
[http://dx.doi.org/10.1002/pmic.200300456] [PMID: 12923773]
[136]
Muramori, F.; Kobayashi, K.; Nakamura, I. A quantitative study of neurofibrillary tangles, senile plaques and astrocytes in the hippocampal subdivisions and entorhinal cortex in Alzheimer’s disease, normal controls and non-Alzheimer neuropsychiatric diseases. Psychiatry Clin. Neurosci., 1998, 52(6), 593-599.
[http://dx.doi.org/10.1111/j.1440-1819.1998.tb02706.x] [PMID: 9895207]
[137]
Oeckl, P.; Halbgebauer, S.; Anderl-Straub, S.; Steinacker, P.; Huss, A.M.; Neugebauer, H.; von Arnim, C.A.F.; Diehl-Schmid, J.; Grimmer, T.; Kornhuber, J.; Lewczuk, P.; Danek, A.; Ludolph, A.C.; Otto, M.; Otto, M. Consortium for frontotemporal lobar degeneration german. Glial fibrillary acidic protein in serum is increased in Alzheimer’s disease and correlates with cognitive impairment. J. Alzheimers Dis., 2019, 67(2), 481-488.
[http://dx.doi.org/10.3233/JAD-180325] [PMID: 30594925]
[138]
Giepmans, B.N.G. Gap junctions and connexin-interacting proteins. Cardiovasc. Res., 2004, 62(2), 233-245.
[http://dx.doi.org/10.1016/j.cardiores.2003.12.009] [PMID: 15094344]
[139]
Takeuchi, H.; Suzumura, A. Gap junctions and hemichannels composed of connexins: potential therapeutic targets for neurodegenerative diseases. Front. Cell. Neurosci., 2014, 8, 189.
[http://dx.doi.org/10.3389/fncel.2014.00189] [PMID: 25228858]
[140]
Xie, H.Y.; Cui, Y.; Deng, F.; Feng, J.C. Connexin: a potential novel target for protecting the central nervous system? Neural Regen. Res., 2015, 10(4), 659-666.
[http://dx.doi.org/10.4103/1673-5374.155444] [PMID: 26170830]
[141]
Koulakoff, A.; Mei, X.; Orellana, J.A.; Sáez, J.C.; Giaume, C. Glial connexin expression and function in the context of Alzheimer’s disease. Biochim. Biophys. Acta, 2012, 1818(8), 2048-2057.
[http://dx.doi.org/10.1016/j.bbamem.2011.10.001] [PMID: 22008509]
[142]
Nagy, J.I.; Li, W.; Hertzberg, E.L.; Marotta, C.A. Elevated connexin43 immunoreactivity at sites of amyloid plaques in Alzheimer’s disease. Brain Res., 1996, 717(1-2), 173-178.
[http://dx.doi.org/10.1016/0006-8993(95)01526-4] [PMID: 8738268]
[143]
Ren, R.; Zhang, L.; Wang, M. Specific deletion connexin43 in astrocyte ameliorates cognitive dysfunction in APP/PS1 mice. Life Sci., 2018, 208, 175-191.
[http://dx.doi.org/10.1016/j.lfs.2018.07.033] [PMID: 30031059]
[144]
Blanchard, V.; Moussaoui, S.; Czech, C.; Touchet, N.; Bonici, B.; Planche, M.; Canton, T.; Jedidi, I.; Gohin, M.; Wirths, O.; Bayer, T.A.; Langui, D.; Duyckaerts, C.; Tremp, G.; Pradier, L. Time sequence of maturation of dystrophic neurites associated with Abeta deposits in APP/PS1 transgenic mice. Exp. Neurol., 2003, 184(1), 247-263.
[http://dx.doi.org/10.1016/S0014-4886(03)00252-8] [PMID: 14637096]
[145]
Saul, A.; Sprenger, F.; Bayer, T.A.; Wirths, O. Accelerated tau pathology with synaptic and neuronal loss in a novel triple transgenic mouse model of Alzheimer’s disease. Neurobiol. Aging, 2013, 34(11), 2564-2573.
[http://dx.doi.org/10.1016/j.neurobiolaging.2013.05.003] [PMID: 23747045]

Rights & Permissions Print Cite
Article Metrics
42
1
World Chagas Disease
© 2024 Bentham Science Publishers | Privacy Policy