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ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

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Review Article

β-amyloid and Oxidative Stress: Perspectives in Drug Development

Author(s): Giuseppe Caruso, Simona F. Spampinato, Vincenzo Cardaci, Filippo Caraci, Maria A. Sortino* and Sara Merlo*

Volume 25, Issue 45, 2019

Page: [4771 - 4781] Pages: 11

DOI: 10.2174/1381612825666191209115431

Price: $65

Abstract

Alzheimer’s Disease (AD) is a slow-developing neurodegenerative disorder in which the main pathogenic role has been assigned to β-amyloid protein (Aβ) that accumulates in extracellular plaques. The mechanism of action of Aβ has been deeply analyzed and several membrane structures have been identified as potential mediators of its effect. The ability of Aβ to modify neuronal activity, receptor expression, signaling pathways, mitochondrial function, and involvement of glial cells have been analyzed. In addition, extensive literature deals with the involvement of oxidative stress in Aβ effects. Herein we focus more specifically on the reciprocal regulation of Aβ, that causes oxidative stress, that favors Aβ aggregation and toxicity and negatively affects the peptide clearance. Analysis of this strict interaction may offer novel opportunities for therapeutic intervention. Both common and new molecules endowed with antioxidant properties deserve attention in this regard.

Keywords: Alzheimer’s disease, reactive oxygen species, reactive nitrogen species, neurodegeneration, antioxidants, carnosine.

« Previous Next »
[1]
Cummings J, Lee G, Ritter A, Zhong K. Alzheimer’s disease drug development pipeline: 2018. Alzheimers Dement (N Y) 2018; 4: 195-214.
[http://dx.doi.org/10.1016/j.trci.2018.03.009] [PMID: 29955663]
[2]
Frozza RL, Lourenco MV, De Felice FG. Challenges for Alzheimer’s Disease therapy: insights from novel mechanisms beyond memory defects. Front Neurosci 2018; 12: 37.
[http://dx.doi.org/10.3389/fnins.2018.00037] [PMID: 29467605]
[3]
Sperling R, Mormino E, Johnson K. The evolution of preclinical Alzheimer’s disease: implications for prevention trials. Neuron 2014; 84(3): 608-22.
[http://dx.doi.org/10.1016/j.neuron.2014.10.038] [PMID: 25442939]
[4]
De Strooper B, Karran E. The Cellular Phase of Alzheimer’s Disease. Cell 2016; 164(4): 603-15.
[http://dx.doi.org/10.1016/j.cell.2015.12.056] [PMID: 26871627]
[5]
Merlo S, Spampinato SF, Beneventano M, Sortino MA. The contribution of microglia to early synaptic compensatory responses that precede β-amyloid-induced neuronal death. Sci Rep 2018; 8(1): 7297.
[http://dx.doi.org/10.1038/s41598-018-25453-1] [PMID: 29740062]
[6]
Merlo S, Spampinato SF, Sortino MA. Early compensatory responses against neuronal injury: a new therapeutic window of opportunity for Alzheimer’s Disease?. CNS Neurosci Ther 2019; 25(1): 5-13.
[http://dx.doi.org/10.1111/cns.13050] [PMID: 30101571]
[7]
Counts SE, Ikonomovic MD, Mercado N, Vega IE, Mufson EJ. Biomarkers for the early detection and progression of Alzheimer’s Disease. Neurotherapeutics 2017; 14(1): 35-53.
[http://dx.doi.org/10.1007/s13311-016-0481-z] [PMID: 27738903]
[8]
Knowles TP, Vendruscolo M, Dobson CM. The amyloid state and its association with protein misfolding diseases. Nat Rev Mol Cell Biol 2014; 15(6): 384-96.
[http://dx.doi.org/10.1038/nrm3810] [PMID: 24854788]
[9]
Chiti F, Dobson CM. Protein misfolding, amyloid formation, and human disease: a summary of progress over the last decade. Annu Rev Biochem 2017; 86: 27-68.
[http://dx.doi.org/10.1146/annurev-biochem-061516-045115] [PMID: 28498720]
[10]
Caruso G, Distefano DA, Parlascino P, et al. Receptor-mediated toxicity of human amylin fragment aggregated by short- and long-term incubations with copper ions. Mol Cell Biochem 2017; 425(1-2): 85-93.
[http://dx.doi.org/10.1007/s11010-016-2864-1] [PMID: 27804051]
[11]
Chong FP, Ng KY, Koh RY, Chye SM. Tau proteins and tauopathies in Alzheimer’s Disease. Cell Mol Neurobiol 2018; 38(5): 965-80.
[http://dx.doi.org/10.1007/s10571-017-0574-1] [PMID: 29299792]
[12]
Hardy J, Selkoe DJ. The amyloid hypothesis of Alzheimer’s disease: progress and problems on the road to therapeutics. Science 2002; 297(5580): 353-6.
[http://dx.doi.org/10.1126/science.1072994] [PMID: 12130773]
[13]
Cline EN, Bicca MA, Viola KL, Klein WL. The Amyloid-β oligomer hypothesis: beginning of the third decade. J Alzheimers Dis 2018; 64(Suppl. 1): S567-610.
[http://dx.doi.org/10.3233/JAD-179941] [PMID: 29843241]
[14]
Liu L, Ding L, Rovere M, Wolfe MS, Selkoe DJ. A cellular complex of BACE1 and γ-secretase sequentially generates Aβ from its full-length precursor. J Cell Biol 2019; 218(2): 644-63.
[http://dx.doi.org/10.1083/jcb.201806205] [PMID: 30626721]
[15]
Thinakaran G, Koo EH. Amyloid precursor protein trafficking, processing, and function. J Biol Chem 2008; 283(44): 29615-9.
[http://dx.doi.org/10.1074/jbc.R800019200] [PMID: 18650430]
[16]
Sun J, Roy S. The physical approximation of APP and BACE-1: a key event in alzheimer’s disease pathogenesis. Dev Neurobiol 2018; 78(3): 340-7.
[http://dx.doi.org/10.1002/dneu.22556] [PMID: 29106038]
[17]
Tan JZA, Gleeson PA. The role of membrane trafficking in the processing of amyloid precursor protein and production of amyloid peptides in Alzheimer’s disease. Biochim Biophys Acta Biomembr 2019; 1861(4): 697-712.
[http://dx.doi.org/10.1016/j.bbamem.2018.11.013] [PMID: 30639513]
[18]
Selkoe DJ. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 2008; 192(1): 106-13.
[http://dx.doi.org/10.1016/j.bbr.2008.02.016] [PMID: 18359102]
[19]
Caruso G, Fresta CG, Lazzarino G, et al. Sub-Toxic human amylin fragment concentrations promote the survival and proliferation of SH-SY5Y cells via the release of VEGF and HspB5 from endothelial RBE4 Cells. Int J Mol Sci 2018; 19(11): 19.
[http://dx.doi.org/10.3390/ijms19113659] [PMID: 30463298]
[20]
Kayed R, Lasagna-Reeves CA. Molecular mechanisms of amyloid oligomers toxicity. J Alzheimers Dis 2013; 33(Suppl. 1): S67-78.
[http://dx.doi.org/10.3233/JAD-2012-129001] [PMID: 22531422]
[21]
Sun X, Chen WD, Wang YD. β-Amyloid: the key peptide in the pathogenesis of Alzheimer’s disease. Front Pharmacol 2015; 6: 221.
[http://dx.doi.org/10.3389/fphar.2015.00221] [PMID: 26483691]
[22]
Bisceglia F, Natalello A, Serafini MM, et al. An integrated strategy to correlate aggregation state, structure and toxicity of Aß 1-42 oligomers. Talanta 2018; 188: 17-26.
[http://dx.doi.org/10.1016/j.talanta.2018.05.062] [PMID: 30029360]
[23]
Takahashi RH, Almeida CG, Kearney PF, et al. Oligomerization of Alzheimer’s beta-amyloid within processes and synapses of cultured neurons and brain. J Neurosci 2004; 24(14): 3592-9.
[http://dx.doi.org/10.1523/JNEUROSCI.5167-03.2004] [PMID: 15071107]
[24]
Gaspar RC, Villarreal SA, Bowles N, Hepler RW, Joyce JG, Shughrue PJ. Oligomers of beta-amyloid are sequestered into and seed new plaques in the brains of an AD mouse model. Exp Neurol 2010; 223(2): 394-400.
[http://dx.doi.org/10.1016/j.expneurol.2009.09.001] [PMID: 19744481]
[25]
Marttinen M, Takalo M, Natunen T, et al. Molecular mechanisms of synaptotoxicity and neuroinflammation in Alzheimer’s Disease. Front Neurosci 2018; 12: 963.
[http://dx.doi.org/10.3389/fnins.2018.00963] [PMID: 30618585]
[26]
Reddy PH, Manczak M, Mao P, Calkins MJ, Reddy AP, Shirendeb U. Amyloid-beta and mitochondria in aging and Alzheimer’s disease: implications for synaptic damage and cognitive decline. J Alzheimers Dis 2010; 20(Suppl. 2): S499-512.
[http://dx.doi.org/10.3233/JAD-2010-100504] [PMID: 20413847]
[27]
Cerpa W, Dinamarca MC, Inestrosa NC. Structure-function implications in Alzheimer’s disease: effect of abeta oligomers at central synapses. Curr Alzheimer Res 2008; 5(3): 233-43.
[http://dx.doi.org/10.2174/156720508784533321] [PMID: 18537540]
[28]
Guntupalli S, Widagdo J, Anggono V. Amyloid-β-Induced dysregulation of AMPA receptor trafficking. Neural Plast 2016; 2016: 3204519.
[http://dx.doi.org/10.1155/2016/3204519] [PMID: 27073700]
[29]
Coleman PD, Yao PJ. Synaptic slaughter in Alzheimer’s disease. Neurobiol Aging 2003; 24(8): 1023-7.
[http://dx.doi.org/10.1016/j.neurobiolaging.2003.09.001] [PMID: 14643374]
[30]
Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. Natural oligomers of the Alzheimer amyloid-beta protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 2007; 27(11): 2866-75.
[http://dx.doi.org/10.1523/JNEUROSCI.4970-06.2007] [PMID: 17360908]
[31]
Klyubin I, Betts V, Welzel AT, et al. Amyloid beta protein dimercontaining human CSF disrupts synaptic plasticity: prevention by systemic passive immunization. J Neurosci 2008; 28(16): 4231-7.
[http://dx.doi.org/10.1523/JNEUROSCI.5161-07.2008 ] [PMID: 18417702]
[32]
Huang S, Tong H, Lei M, et al. Astrocytic glutamatergic transporters are involved in Aβ-induced synaptic dysfunction. Brain Res 2018; 1678: 129-37.
[http://dx.doi.org/10.1016/j.brainres.2017.10.011] [PMID: 29066369]
[33]
Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: implications for neurodegenerative disorders. Nat Rev Neurosci 2010; 11(10): 682-96.
[http://dx.doi.org/10.1038/nrn2911] [PMID: 20842175]
[34]
Mroczko B, Groblewska M, Litman-Zawadzka A, Kornhuber J, Lewczuk P. Cellular receptors of amyloid β oligomers (AβOs) in Alzheimer’s Disease. Int J Mol Sci 2018; 19(7): 19.
[http://dx.doi.org/10.3390/ijms19071884] [PMID: 29954063]
[35]
Canale C, Seghezza S, Vilasi S, et al. Different effects of Alzheimer’s peptide Aβ(1-40) oligomers and fibrils on supported lipid membranes. Biophys Chem 2013; 182: 23-9.
[http://dx.doi.org/10.1016/j.bpc.2013.07.010] [PMID: 23998637]
[36]
Kagan BL, Hirakura Y, Azimov R, Azimova R, Lin MC. The channel hypothesis of Alzheimer’s disease: current status. Peptides 2002; 23(7): 1311-5.
[http://dx.doi.org/10.1016/S0196-9781(02)00067-0] [PMID: 12128087]
[37]
Bode DC, Baker MD, Viles JH. Ion channel formation by amyloid-β42 oligomers but not Amyloid-β40 in cellular membranes. J Biol Chem 2017; 292(4): 1404-13.
[http://dx.doi.org/10.1074/jbc.M116.762526] [PMID: 27927987]
[38]
Drolle E, Hane F, Lee B, Leonenko Z. Atomic force microscopy to study molecular mechanisms of amyloid fibril formation and toxicity in Alzheimer’s disease. Drug Metab Rev 2014; 46(2): 207-23.
[http://dx.doi.org/10.3109/03602532.2014.882354] [PMID: 24495298]
[39]
Mouillet-Richard S, Ermonval M, Chebassier C, et al. Signal transduction through prion protein. Science 2000; 289(5486): 1925-8.
[http://dx.doi.org/10.1126/science.289.5486.1925] [PMID: 10988071]
[40]
Lee G, Thangavel R, Sharma VM, et al. Phosphorylation of tau by fyn: implications for Alzheimer’s disease. J Neurosci 2004; 24(9): 2304-12.
[http://dx.doi.org/10.1523/JNEUROSCI.4162-03.2004] [PMID: 14999081]
[41]
Ohnishi T, Yanazawa M, Sasahara T, et al. Na, K-ATPase α3 is a death target of Alzheimer patient amyloid-β assembly. Proc Natl Acad Sci USA 2015; 112(32): E4465-74.
[http://dx.doi.org/10.1073/pnas.1421182112] [PMID: 26224839]
[42]
DiChiara T, DiNunno N, Clark J, et al. Alzheimer’s Toxic amyloid beta oligomers: unwelcome visitors to the Na/K ATPase alpha3 docking station. Yale J Biol Med 2017; 90(1): 45-61.
[PMID: 28356893]
[43]
De Felice FG, Vieira MN, Bomfim TR, et al. Protection of synapses against Alzheimer’s-linked toxins: insulin signaling prevents the pathogenic binding of Abeta oligomers. Proc Natl Acad Sci USA 2009; 106(6): 1971-6.
[http://dx.doi.org/10.1073/pnas.0809158106] [PMID: 19188609]
[44]
Zhao WQ, De Felice FG, Fernandez S, et al. Amyloid beta oligomers induce impairment of neuronal insulin receptors. FASEB J 2008; 22(1): 246-60.
[http://dx.doi.org/10.1096/fj.06-7703com] [PMID: 17720802]
[45]
Texidó L, Martín-Satué M, Alberdi E, Solsona C, Matute C. Amyloid β peptide oligomers directly activate NMDA receptors. Cell Calcium 2011; 49(3): 184-90.
[http://dx.doi.org/10.1016/j.ceca.2011.02.001] [PMID: 21349580]
[46]
Costa RO, Lacor PN, Ferreira IL, et al. Endoplasmic reticulum stress occurs downstream of GluN2B subunit of N-methyl-d-aspartate receptor in mature hippocampal cultures treated with amyloid-β oligomers. Aging Cell 2012; 11(5): 823-33.
[http://dx.doi.org/10.1111/j.1474-9726.2012.00848.x] [PMID: 22708890]
[47]
Ferreira IL, Ferreiro E, Schmidt J, et al. Aβ and NMDAR activation cause mitochondrial dysfunction involving ER calcium release. Neurobiol Aging 2015; 36(2): 680-92.
[http://dx.doi.org/10.1016/j.neurobiolaging.2014.09.006] [PMID: 25442114]
[48]
De Felice FG, Velasco PT, Lambert MP, et al. Abeta oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 2007; 282(15): 11590-601.
[http://dx.doi.org/10.1074/jbc.M607483200] [PMID: 17308309]
[49]
Copani A, Hoozemans JJ, Caraci F, et al. DNA polymerase-beta is expressed early in neurons of Alzheimer’s disease brain and is loaded into DNA replication forks in neurons challenged with beta-amyloid. J Neurosci 2006; 26(43): 10949-57.
[http://dx.doi.org/10.1523/JNEUROSCI.2793-06.2006] [PMID: 17065437]
[50]
Merlo S, Basile L, Giuffrida ML, Sortino MA, Guccione S, Copani A. Identification of 5-Methoxyflavone as a novel DNA polymerase-beta inhibitor and neuroprotective agent against beta-amyloid toxicity. J Nat Prod 2015; 78(11): 2704-11.
[http://dx.doi.org/10.1021/acs.jnatprod.5b00621] [PMID: 26517378]
[51]
Copani A, Guccione S, Giurato L, et al. The cell cycle molecules behind neurodegeneration in Alzheimer’s disease: perspectives for drug development. Curr Med Chem 2008; 15(24): 2420-32.
[http://dx.doi.org/10.2174/092986708785909030] [PMID: 18855671]
[52]
Frasca G, Carbonaro V, Merlo S, Copani A, Sortino MA. Integrins mediate beta-amyloid-induced cell-cycle activation and neuronal death. J Neurosci Res 2008; 86(2): 350-5.
[http://dx.doi.org/10.1002/jnr.21487] [PMID: 17828768]
[53]
D’Andrea MR, Nagele RG, Wang HY, Peterson PA, Lee DH. Evidence that neurones accumulating amyloid can undergo lysis to form amyloid plaques in Alzheimer’s disease. Histopathology 2001; 38(2): 120-34.
[http://dx.doi.org/10.1046/j.1365-2559.2001.01082.x] [PMID: 11207825]
[54]
Wirths O, Multhaup G, Czech C, et al. Intraneuronal Abeta accumulation precedes plaque formation in beta-amyloid precursor protein and presenilin-1 double-transgenic mice. Neurosci Lett 2001; 306(1-2): 116-20.
[http://dx.doi.org/10.1016/S0304-3940(01)01876-6] [PMID: 11403971]
[55]
Nagele RG, D’Andrea MR, Anderson WJ, Wang HY. Intracellular accumulation of beta-amyloid(1-42) in neurons is facilitated by the alpha 7 nicotinic acetylcholine receptor in Alzheimer’s disease. Neuroscience 2002; 110(2): 199-211.
[http://dx.doi.org/10.1016/S0306-4522(01)00460-2] [PMID: 11958863]
[56]
Deane R, Du Yan S, Submamaryan RK, et al. RAGE mediates amyloid-beta peptide transport across the blood-brain barrier and accumulation in brain. Nat Med 2003; 9(7): 907-13.
[http://dx.doi.org/10.1038/nm890] [PMID: 12808450]
[57]
Zerbinatti CV, Wahrle SE, Kim H, et al. Apolipoprotein E and low density lipoprotein receptor-related protein facilitate intraneuronal Abeta42 accumulation in amyloid model mice. J Biol Chem 2006; 281(47): 36180-6.
[http://dx.doi.org/10.1074/jbc.M604436200] [PMID: 17012232]
[58]
Nishioka C, Liang HF, Barsamian B, Sun SW. Amyloid-beta induced retrograde axonal degeneration in a mouse tauopathy model. Neuroimage 2019; 189: 180-91.
[http://dx.doi.org/10.1016/j.neuroimage.2019.01.007] [PMID: 30630081]
[59]
Orr ME, Oddo S. Autophagic/lysosomal dysfunction in Alzheimer’s disease. Alzheimers Res Ther 2013; 5(5): 53.
[http://dx.doi.org/10.1186/alzrt217] [PMID: 24171818]
[60]
Yang AJ, Chandswangbhuvana D, Margol L, Glabe CG. Loss of endosomal/lysosomal membrane impermeability is an early event in amyloid Abeta1-42 pathogenesis. J Neurosci Res 1998; 52(6): 691-8.
[http://dx.doi.org/10.1002/(SICI)1097-4547(19980615)52:6<691:AID-JNR8>3.0.CO;2-3] [PMID: 9669318]
[61]
Kundra R, Ciryam P, Morimoto RI, Dobson CM, Vendruscolo M. Protein homeostasis of a metastable subproteome associated with Alzheimer’s disease. Proc Natl Acad Sci USA 2017; 114(28): E5703-11.
[http://dx.doi.org/10.1073/pnas.1618417114] [PMID: 28652376]
[62]
Casley CS, Canevari L, Land JM, Clark JB, Sharpe MA. Beta-amyloid inhibits integrated mitochondrial respiration and key enzyme activities. J Neurochem 2002; 80(1): 91-100.
[http://dx.doi.org/10.1046/j.0022-3042.2001.00681.x] [PMID: 11796747]
[63]
Sirk D, Zhu Z, Wadia JS, et al. Chronic exposure to sub-lethal betaamyloid (Abeta) inhibits the import of nuclear-encoded proteins to mitochondria in differentiated PC12 cells. J Neurochem 2007; 103(5): 1989-2003.
[http://dx.doi.org/10.1111/j.1471-4159.2007.04907.x] [PMID: 17868329]
[64]
Caspersen C, Wang N, Yao J, et al. Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer’s disease. FASEB J 2005; 19(14): 2040-1.
[http://dx.doi.org/10.1096/fj.05-3735fje] [PMID: 16210396]
[65]
Mastroeni D, Nolz J, Khdour OM, et al. Oligomeric amyloid β preferentially targets neuronal and not glial mitochondrial-encoded mRNAs. Alzheimers Dement 2018; 14(6): 775-86.
[http://dx.doi.org/10.1016/j.jalz.2017.12.005] [PMID: 29396107]
[66]
Kim J, Yang Y, Song SS, et al. Beta-amyloid oligomers activate apoptotic BAK pore for cytochrome C release. Biophys J 2014; 107(7): 1601-8.
[http://dx.doi.org/10.1016/j.bpj.2014.07.074] [PMID: 25296312]
[67]
Moreira PI, Santos MS, Oliveira CR. Alzheimer’s disease: a lesson from mitochondrial dysfunction. Antioxid Redox Signal 2007; 9(10): 1621-30.
[http://dx.doi.org/10.1089/ars.2007.1703] [PMID: 17678440]
[68]
Medeiros R, LaFerla FM. Astrocytes: conductors of the Alzheimer disease neuroinflammatory symphony. Exp Neurol 2013; 239: 133-8.
[http://dx.doi.org/10.1016/j.expneurol.2012.10.007] [PMID: 23063604]
[69]
Narayan P, Holmström KM, Kim DH, et al. Rare individual amyloid-β oligomers act on astrocytes to initiate neuronal damage. Biochemistry 2014; 53(15): 2442-53.
[http://dx.doi.org/10.1021/bi401606f] [PMID: 24717093]
[70]
Spampinato SF, Merlo S, Sano Y, Kanda T, Sortino MA. Astrocytes contribute to Aβ-induced blood-brain barrier damage through activation of endothelial MMP9. J Neurochem 2017; 142(3): 464-77.
[http://dx.doi.org/10.1111/jnc.14068] [PMID: 28488764]
[71]
Zhao J, O’Connor T, Vassar R. The contribution of activated astrocytes to Aβ production: implications for Alzheimer’s disease pathogenesis. J Neuroinflammation 2011; 8: 150.
[http://dx.doi.org/10.1186/1742-2094-8-150] [PMID: 22047170]
[72]
Wyss-Coray T, Rogers J. Inflammation in Alzheimer disease-a brief review of the basic science and clinical literature. Cold Spring Harb Perspect Med 2012; 2(1): a006346.
[http://dx.doi.org/10.1101/cshperspect.a006346] [PMID: 22315714]
[73]
Benatti C, Blom JM, Rigillo G, et al. Disease-induced neuroinflammation and depression. CNS Neurol Disord Drug Targets 2016; 15(4): 414-33.
[http://dx.doi.org/10.2174/1871527315666160321104749] [PMID: 26996176]
[74]
Lee CY, Landreth GE. The role of microglia in amyloid clearance from the AD brain. J Neural Transm (Vienna) 2010; 117(8): 949-60.
[http://dx.doi.org/10.1007/s00702-010-0433-4] [PMID: 20552234]
[75]
Cheignon C, Tomas M, Bonnefont-Rousselot D, Faller P, Hureau C, Collin F. Oxidative stress and the amyloid beta peptide in Alzheimer’s disease. Redox Biol 2018; 14: 450-64.
[http://dx.doi.org/10.1016/j.redox.2017.10.014] [PMID: 29080524]
[76]
Caruso G, Caraci F, Jolivet RB. Pivotal role of carnosine in the modulation of brain cells activity: multimodal mechanism of action and therapeutic potential in neurodegenerative disorders. Prog Neurobiol 2019.; 175: 35-53.
[PMID: 30593839]
[77]
Birben E, Sahiner UM, Sackesen C, Erzurum S, Kalayci O. Oxidative stress and antioxidant defense. World Allergy Organ J 2012; 5(1): 9-19.
[http://dx.doi.org/10.1097/WOX.0b013e3182439613] [PMID: 23268465]
[78]
de Campos RP, Siegel JM, Fresta CG, Caruso G, da Silva JA, Lunte SM. Indirect detection of superoxide in RAW 264.7 macrophage cells using microchip electrophoresis coupled to laser-induced fluorescence. Anal Bioanal Chem 2015; 407(23): 7003-12.
[http://dx.doi.org/10.1007/s00216-015-8865-1] [PMID: 26159570]
[79]
Mainz ER, Gunasekara DB, Caruso G, et al. Monitoring intracellular nitric oxide production using microchip electrophoresis and laser-induced fluorescence detection. Anal Methods 2012; 4: 414-20.
[http://dx.doi.org/10.1039/c2ay05542b]
[80]
Maes M, Galecki P, Chang YS, Berk M. A review on the oxidative and nitrosative stress (O&NS) pathways in major depression and their possible contribution to the (neuro) degenerative processes in that illness. Prog Neuropsychopharmacol Biol Psychiatry 2011; 35(3): 676-92.
[http://dx.doi.org/10.1016/j.pnpbp.2010.05.004] [PMID: 20471444]
[81]
Beckman JS, Crow JP. Pathological implications of nitric oxide, superoxide and peroxynitrite formation. Biochem Soc Trans 1993; 21(2): 330-4.
[http://dx.doi.org/10.1042/bst0210330] [PMID: 8395426]
[82]
Lushchak VI. Free radicals, reactive oxygen species, oxidative stress and its classification. Chem Biol Interact 2014; 224: 164-75.
[http://dx.doi.org/10.1016/j.cbi.2014.10.016] [PMID: 25452175]
[83]
Serini S, Calviello G. Reduction of oxidative/nitrosative stress in brain and its involvement in the neuroprotective effect of n-3 PUFA in Alzheimer’s disease. Curr Alzheimer Res 2016; 13(2): 123-34.
[http://dx.doi.org/10.2174/1567205012666150921101147] [PMID: 26391044]
[84]
Huang WJ, Zhang X, Chen WW. Role of oxidative stress in Alzheimer’s disease. Biomed Rep 2016; 4(5): 519-22.
[http://dx.doi.org/10.3892/br.2016.630] [PMID: 27123241]
[85]
Gelain DP, Antonio Behr G, Birnfeld de Oliveira R, Trujillo M. Antioxidant therapies for neurodegenerative diseases: mechanisms, current trends, and perspectives. Oxid Med Cell Longev 2012; 2012: 895153.
[http://dx.doi.org/10.1155/2012/895153] [PMID: 23304258]
[86]
Varadarajan S, Yatin S, Aksenova M, Butterfield DA. Review: Alzheimer’s amyloid beta-peptide-associated free radical oxidative stress and neurotoxicity. J Struct Biol 2000; 130(2-3): 184-208.
[http://dx.doi.org/10.1006/jsbi.2000.4274] [PMID: 10940225]
[87]
Zhao Y, Zhao B. Oxidative stress and the pathogenesis of Alzheimer’s disease. Oxid Med Cell Longev 2013; 2013: 316523.
[http://dx.doi.org/10.1155/2013/316523]
[88]
Usui K, Hulleman JD, Paulsson JF, Siegel SJ, Powers ET, Kelly JW. Site-specific modification of Alzheimer’s peptides by cholesterol oxidation products enhances aggregation energetics and neurotoxicity. Proc Natl Acad Sci USA 2009; 106(44): 18563-8.
[http://dx.doi.org/10.1073/pnas.0804758106] [PMID: 19841277]
[89]
Duce JA, Bush AI. Biological metals and Alzheimer’s disease: implications for therapeutics and diagnostics. Prog Neurobiol 2010; 92(1): 1-18.
[http://dx.doi.org/10.1016/j.pneurobio.2010.04.003] [PMID: 20444428]
[90]
Kanti Das T, Wati MR, Fatima-Shad K. Oxidative stress gated by Fenton and Haber Weiss reactions and its association with Alzheimer’s disease. Arch Neurosci 2014; 2(3): e20078.
[http://dx.doi.org/10.5812/archneurosci.20078]
[91]
Bush AI. The metal theory of Alzheimer’s disease. J Alzheimers Dis 2013; 33(Suppl. 1): S277-81.
[http://dx.doi.org/10.3233/JAD-2012-129011] [PMID: 22635102]
[92]
Myhre O, Utkilen H, Duale N, Brunborg G, Hofer T. Metal dyshomeostasis and inflammation in Alzheimer’s and Parkinson’s diseases: possible impact of environmental exposures. Oxid Med Cell Longev 2013; 2013: 726954.
[http://dx.doi.org/10.1155/2013/726954]
[93]
Bagheri S, Squitti R, Haertlé T, Siotto M, Saboury AA. Role of copper in the onset of Alzheimer’s disease compared to other metals. Front Aging Neurosci 2018; 9: 446.
[http://dx.doi.org/10.3389/fnagi.2017.00446] [PMID: 29472855]
[94]
Faller P, Hureau C. A bioinorganic view of Alzheimer’s disease: when misplaced metal ions (re)direct the electrons to the wrong target. Chemistry 2012; 18(50): 15910-20.
[http://dx.doi.org/10.1002/chem.201202697] [PMID: 23180511]
[95]
Cassagnes LE, Hervé V, Nepveu F, Hureau C, Faller P, Collin F. The catalytically active copper-amyloid-Beta state: coordination site responsible for reactive oxygen species production. Angew Chem Int Ed Engl 2013; 52(42): 11110-3.
[http://dx.doi.org/10.1002/anie.201305372] [PMID: 24038998]
[96]
Kanekiyo T, Bu G. The low-density lipoprotein receptor-related protein 1 and amyloid-β clearance in Alzheimer’s disease. Front Aging Neurosci 2014; 6: 93.
[http://dx.doi.org/10.3389/fnagi.2014.00093] [PMID: 24904407]
[97]
Kanekiyo T, Cirrito JR, Liu CC, et al. Neuronal clearance of amyloid-β by endocytic receptor LRP1. J Neurosci 2013; 33(49): 19276-83.
[http://dx.doi.org/10.1523/JNEUROSCI.3487-13.2013] [PMID: 24305823]
[98]
Kanekiyo T, Liu CC, Shinohara M, Li J, Bu G. LRP1 in brain vascular smooth muscle cells mediates local clearance of Alzheimer’s amyloid-β. J Neurosci 2012; 32(46): 16458-65.
[http://dx.doi.org/10.1523/JNEUROSCI.3987-12.2012] [PMID: 23152628]
[99]
Liu CC, Hu J, Zhao N, et al. Astrocytic LRP1 Mediates brain Aβ clearance and impacts amyloid deposition. J Neurosci 2017; 37(15): 4023-31.
[http://dx.doi.org/10.1523/JNEUROSCI.3442-16.2017] [PMID: 28275161]
[100]
Owen JB, Sultana R, Aluise CD, et al. Oxidative modification to LDL receptor-related protein 1 in hippocampus from subjects with Alzheimer disease: implications for Aβ accumulation in AD brain. Free Radic Biol Med 2010; 49(11): 1798-803.
[http://dx.doi.org/10.1016/j.freeradbiomed.2010.09.013] [PMID: 20869432]
[101]
Reddy PH. Amyloid precursor protein-mediated free radicals and oxidative damage: implications for the development and progression of Alzheimer’s disease. J Neurochem 2006; 96(1): 1-13.
[http://dx.doi.org/10.1111/j.1471-4159.2005.03530.x] [PMID: 16305625]
[102]
Smith DG, Cappai R, Barnham KJ. The redox chemistry of the Alzheimer’s disease amyloid beta peptide. Biochim Biophys Acta 2007; 1768(8): 1976-90.
[http://dx.doi.org/10.1016/j.bbamem.2007.02.002] [PMID: 17433250]
[103]
Grasso G, Giuffrida ML, Rizzarelli E. Metallostasis and amyloid β-degrading enzymes. Metallomics 2012; 4(9): 937-49.
[http://dx.doi.org/10.1039/c2mt20105d] [PMID: 22832870]
[104]
Grasso G, Pietropaolo A, Spoto G, et al. Copper(I) and copper(II) inhibit Aβ peptides proteolysis by insulin-degrading enzyme differently: implications for metallostasis alteration in Alzheimer’s disease. Chemistry 2011; 17(9): 2752-62.
[http://dx.doi.org/10.1002/chem.201002809] [PMID: 21274957]
[105]
Tamagno E, Guglielmotto M, Aragno M, et al. Oxidative stress activates a positive feedback between the gamma- and beta-secretase cleavages of the beta-amyloid precursor protein. J Neurochem 2008; 104(3): 683-95.
[PMID: 18005001]
[106]
Behl C, Davis J, Cole GM, Schubert D. Vitamin E protects nerve cells from amyloid beta protein toxicity. Biochem Biophys Res Commun 1992; 186(2): 944-50.
[http://dx.doi.org/10.1016/0006-291X(92)90837-B] [PMID: 1497677]
[107]
Butterfield DA, Hensley K, Harris M, Mattson M, Carney J. beta-Amyloid peptide free radical fragments initiate synaptosomal lipoperoxidation in a sequence-specific fashion: implications to Alzheimer’s disease. Biochem Biophys Res Commun 1994; 200(2): 710-5.
[http://dx.doi.org/10.1006/bbrc.1994.1508] [PMID: 8179604]
[108]
Harris ME, Hensley K, Butterfield DA, Leedle RA, Carney JM. Direct evidence of oxidative injury produced by the Alzheimer’s beta-amyloid peptide (1-40) in cultured hippocampal neurons. Exp Neurol 1995; 131(2): 193-202.
[http://dx.doi.org/10.1016/0014-4886(95)90041-1] [PMID: 7895820]
[109]
Bruce AJ, Malfroy B, Baudry M. beta-Amyloid toxicity in organotypic hippocampal cultures: protection by EUK-8, a synthetic catalytic free radical scavenger. Proc Natl Acad Sci USA 1996; 93(6): 2312-6.
[http://dx.doi.org/10.1073/pnas.93.6.2312] [PMID: 8637869]
[110]
Mark RJ, Lovell MA, Markesbery WR, Uchida K, Mattson MP. A role for 4-hydroxynonenal, an aldehydic product of lipid peroxidation, in disruption of ion homeostasis and neuronal death induced by amyloid beta-peptide. J Neurochem 1997; 68(1): 255-64.
[http://dx.doi.org/10.1046/j.1471-4159.1997.68010255.x] [PMID: 8978733]
[111]
Ebenezer PJ, Weidner AM, LeVine H III, et al. Neuron specific toxicity of oligomeric amyloid-β: role for JUN-kinase and oxidative stress. J Alzheimers Dis 2010; 22(3): 839-48.
[http://dx.doi.org/10.3233/JAD-2010-101161] [PMID: 20858948]
[112]
Xie H, Hou S, Jiang J, Sekutowicz M, Kelly J, Bacskai BJ. Rapid cell death is preceded by amyloid plaque-mediated oxidative stress. Proc Natl Acad Sci USA 2013; 110(19): 7904-9.
[http://dx.doi.org/10.1073/pnas.1217938110] [PMID: 23610434]
[113]
Abramov AY, Canevari L, Duchen MR. Beta-amyloid peptides induce mitochondrial dysfunction and oxidative stress in astrocytes and death of neurons through activation of NADPH oxidase. J Neurosci 2004; 24(2): 565-75.
[http://dx.doi.org/10.1523/JNEUROSCI.4042-03.2004] [PMID: 14724257]
[114]
Smith DP, Smith DG, Curtain CC, et al. Copper-mediated amyloid-beta toxicity is associated with an intermolecular histidine bridge. J Biol Chem 2006; 281(22): 15145-54.
[http://dx.doi.org/10.1074/jbc.M600417200] [PMID: 16595673]
[115]
Lecanu L, Greeson J, Papadopoulos V. Beta-amyloid and oxidative stress jointly induce neuronal death, amyloid deposits, gliosis, and memory impairment in the rat brain. Pharmacology 2006; 76(1): 19-33.
[http://dx.doi.org/10.1159/000088929] [PMID: 16224201]
[116]
Celsi F, Svedberg M, Unger C, et al. Beta-amyloid causes downregulation of calcineurin in neurons through induction of oxidative stress. Neurobiol Dis 2007; 26(2): 342-52.
[http://dx.doi.org/10.1016/j.nbd.2006.12.022] [PMID: 17344052]
[117]
Amir Aslani B, Ghobadi S. Studies on oxidants and antioxidants with a brief glance at their relevance to the immune system. Life Sci 2016; 146: 163-73.
[http://dx.doi.org/10.1016/j.lfs.2016.01.014] [PMID: 26792059]
[118]
Carocho M, Ferreira IC. A review on antioxidants, prooxidants and related controversy: natural and synthetic compounds, screening and analysis methodologies and future perspectives. Food Chem Toxicol 2013; 51: 15-25.
[http://dx.doi.org/10.1016/j.fct.2012.09.021] [PMID: 23017782]
[119]
Valko M, Rhodes CJ, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chem Biol Interact 2006; 160(1): 1-40.
[http://dx.doi.org/10.1016/j.cbi.2005.12.009] [PMID: 16430879]
[120]
Vendemiale G, Grattagliano I, Altomare E. An update on the role of free radicals and antioxidant defense in human disease. Int J Clin Lab Res 1999; 29(2): 49-55.
[http://dx.doi.org/10.1007/s005990050063] [PMID: 10436261]
[121]
Singh M, Saini HK. Resident cardiac mast cells and ischemia-reperfusion injury. J Cardiovasc Pharmacol Ther 2003; 8(2): 135-48.
[http://dx.doi.org/10.1177/107424840300800207] [PMID: 12808487]
[122]
Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. Int J Biomed Sci 2008; 4(2): 89-96.
[PMID: 23675073]
[123]
Sepand MR, Razavi-Azarkhiavi K, Omidi A, et al. Effect of Acetyl-l-carnitine on antioxidant status, lipid peroxidation, and oxidative damage of arsenic in rat. Biol Trace Elem Res 2016; 171(1): 107-15.
[http://dx.doi.org/10.1007/s12011-015-0436-y] [PMID: 26349760]
[124]
Celsi F, Ferri A, Casciati A, et al. Overexpression of superoxide dismutase 1 protects against beta-amyloid peptide toxicity: effect of estrogen and copper chelators. Neurochem Int 2004; 44(1): 25-33.
[http://dx.doi.org/10.1016/S0197-0186(03)00101-3] [PMID: 12963085]
[125]
Chilumuri A, Odell M, Milton N. The neuroprotective role of catalase overexpression in SH-SY5Y cells against beta-amyloid and H2O2 toxicity. Alzheimers Dement 2013; 9: 361.
[http://dx.doi.org/10.1016/j.jalz.2013.05.691]
[126]
Barkats M, Millecamps S, Abrioux P, Geoffroy MC, Mallet J. Overexpression of glutathione peroxidase increases the resistance of neuronal cells to Abeta-mediated neurotoxicity. J Neurochem 2000; 75(4): 1438-46.
[http://dx.doi.org/10.1046/j.1471-4159.2000.0751438.x] [PMID: 10987823]
[127]
Deshmukh P, Unni S, Krishnappa G, Padmanabhan B. The Keap1-Nrf2 pathway: promising therapeutic target to counteract ROS-mediated damage in cancers and neurodegenerative diseases. Biophys Rev 2017; 9(1): 41-56.
[http://dx.doi.org/10.1007/s12551-016-0244-4] [PMID: 28510041]
[128]
Taguchi K, Motohashi H, Yamamoto M. Molecular mechanisms of the Keap1-Nrf2 pathway in stress response and cancer evolution. Genes Cells 2011; 16(2): 123-40.
[http://dx.doi.org/10.1111/j.1365-2443.2010.01473.x] [PMID: 21251164]
[129]
Branca C, Ferreira E, Nguyen TV, Doyle K, Caccamo A, Oddo S. Genetic reduction of Nrf2 exacerbates cognitive deficits in a mouse model of Alzheimer’s disease. Hum Mol Genet 2017; 26(24): 4823-35.
[http://dx.doi.org/10.1093/hmg/ddx361] [PMID: 29036636]
[130]
Simoni E, Serafini MM, Caporaso R, et al. Targeting the Nrf2/amyloid-beta liaison in Alzheimer’s disease: a rational approach. ACS Chem Neurosci 2017; 8(7): 1618-27.
[http://dx.doi.org/10.1021/acschemneuro.7b00100] [PMID: 28421738]
[131]
Kerr F, Sofola-Adesakin O, Ivanov DK, et al. Direct Keap1-Nrf2 disruption as a potential therapeutic target for Alzheimer’s disease. PLoS Genet 2017; 13(3): e1006593.
[http://dx.doi.org/10.1371/journal.pgen.1006593] [PMID: 28253260]
[132]
Kanninen K, White AR, Koistinaho J, Malm T. Targeting glycogen synthase kinase-3β for therapeutic benefit against oxidative stress in Alzheimer’s disease: involvement of the Nrf2-ARE Pathway. Int J Alzheimers Dis 2011; 2011: 985085.
[http://dx.doi.org/10.4061/2011/985085] [PMID: 21629716]
[133]
Pocernich CB, Butterfield DA. Elevation of glutathione as a therapeutic strategy in Alzheimer disease. Biochim Biophys Acta 2012; 1822(5): 625-30.
[http://dx.doi.org/10.1016/j.bbadis.2011.10.003] [PMID: 22015471]
[134]
Mecocci P, Polidori MC. Antioxidant clinical trials in mild cognitive impairment and Alzheimer’s disease. Biochim Biophys Acta 2012; 1822(5): 631-8.
[http://dx.doi.org/10.1016/j.bbadis.2011.10.006] [PMID: 22019723]
[135]
Calabrese V, Sultana R, Scapagnini G, et al. Nitrosative stress, cellular stress response, and thiol homeostasis in patients with Alzheimer’s disease. Antioxid Redox Signal 2006; 8(11-12): 1975-86.
[http://dx.doi.org/10.1089/ars.2006.8.1975] [PMID: 17034343]
[136]
Lloret A, Badía MC, Mora NJ, Pallardó FV, Alonso MD, Viña J. Vitamin E paradox in Alzheimer’s disease: it does not prevent loss of cognition and may even be detrimental. J Alzheimers Dis 2009; 17(1): 143-9.
[http://dx.doi.org/10.3233/JAD-2009-1033] [PMID: 19494439]
[137]
Anderson ME, Meister A. Transport and direct utilization of gamma-glutamylcyst(e)ine for glutathione synthesis. Proc Natl Acad Sci USA 1983; 80(3): 707-11.
[http://dx.doi.org/10.1073/pnas.80.3.707] [PMID: 6572362]
[138]
Le WD, Jankovic J, Xie W, Appel SH. Antioxidant property of pramipexole independent of dopamine receptor activation in neuroprotection. J Neural Transm (Vienna) 2000; 107(10): 1165-73.
[http://dx.doi.org/10.1007/s007020070030] [PMID: 11129106]
[139]
Pocernich CB, La Fontaine M, Butterfield DA. In-vivo glutathione elevation protects against hydroxyl free radical-induced protein oxidation in rat brain. Neurochem Int 2000; 36(3): 185-91.
[http://dx.doi.org/10.1016/S0197-0186(99)00126-6] [PMID: 10676851]
[140]
Koppal T, Drake J, Butterfield DA. In vivo modulation of rodent glutathione and its role in peroxynitrite-induced neocortical synaptosomal membrane protein damage. Biochim Biophys Acta 1999; 1453(3): 407-11.
[http://dx.doi.org/10.1016/S0925-4439(99)00014-9] [PMID: 10101259]
[141]
Pocernich CB, Cardin AL, Racine CL, Lauderback CM, Butterfield DA. Glutathione elevation and its protective role in acrolein-induced protein damage in synaptosomal membranes: relevance to brain lipid peroxidation in neurodegenerative disease. Neurochem Int 2001; 39(2): 141-9.
[http://dx.doi.org/10.1016/S0197-0186(01)00012-2] [PMID: 11408093]
[142]
Fu AL, Dong ZH, Sun MJ. Protective effect of N-acetyl-L-cysteine on amyloid beta-peptide-induced learning and memory deficits in mice. Brain Res 2006; 1109(1): 201-6.
[http://dx.doi.org/10.1016/j.brainres.2006.06.042] [PMID: 16872586]
[143]
Berezhnoy DS, Stvolinsky SL, Lopachev AV, et al. Carnosine as an effective neuroprotector in brain pathology and potential neuromodulator in normal conditions. Amino Acids 2018.
[PMID: 30353356]
[144]
Gorbunov NV, Erin AN. [Mechanism of antioxidant action of carnosine]. Biull Eksp Biol Med 1991; 111(5): 477-8.
[http://dx.doi.org/10.1007/BF00840997] [PMID: 1878559]
[145]
Caruso G, Fresta CG, Siegel JM, Wijesinghe MB, Lunte SM. Microchip electrophoresis with laser-induced fluorescence detection for the determination of the ratio of nitric oxide to superoxide production in macrophages during inflammation. Anal Bioanal Chem 2017; 409(19): 4529-38.
[http://dx.doi.org/10.1007/s00216-017-0401-z] [PMID: 28555342]
[146]
Chan WK, Decker EA, Chow CK, Boissonneault GA. Effect of dietary carnosine on plasma and tissue antioxidant concentrations and on lipid oxidation in rat skeletal muscle. Lipids 1994; 29(7): 461-6.
[http://dx.doi.org/10.1007/BF02578242] [PMID: 7968266]
[147]
Reddy VP, Garrett MR, Perry G, Smith MA. Carnosine: a versatile antioxidant and antiglycating agent. Sci SAGE KE 2005; 2005(18): pe12.
[http://dx.doi.org/10.1126/sageke.2005.18.pe12] [PMID: 15872311]
[148]
Fresta CG, Chakraborty A, Wijesinghe MB, et al. Non-toxic engineered carbon nanodiamond concentrations induce oxidative/nitrosative stress, imbalance of energy metabolism, and mitochondrial dysfunction in microglial and alveolar basal epithelial cells. Cell Death Dis 2018; 9(2): 245.
[http://dx.doi.org/10.1038/s41419-018-0280-z] [PMID: 29445138]
[149]
Tsai SJ, Kuo WW, Liu WH, Yin MC. Antioxidative and antiinflammatory protection from carnosine in the striatum of MPTPtreated mice. J Agric Food Chem 2010; 58(21): 11510-6.
[http://dx.doi.org/10.1021/jf103258p] [PMID: 20925384]
[150]
Caruso G, Fresta CG, Martinez-Becerra F, et al. Carnosine modulates nitric oxide in stimulated murine RAW 264.7 macrophages. Mol Cell Biochem 2017; 431(1-2): 197-210.
[http://dx.doi.org/10.1007/s11010-017-2991-3] [PMID: 28290048]
[151]
Aldini G, Facino RM, Beretta G, Carini M. Carnosine and related dipeptides as quenchers of reactive carbonyl species: from structural studies to therapeutic perspectives. Biofactors 2005; 24(1-4): 77-87.
[http://dx.doi.org/10.1002/biof.5520240109] [PMID: 16403966]
[152]
Hipkiss AR, Preston JE, Himsworth DT, et al. Pluripotent protective effects of carnosine, a naturally occurring dipeptide. Ann N Y Acad Sci 1998; 854: 37-53.
[http://dx.doi.org/10.1111/j.1749-6632.1998.tb09890.x] [PMID: 9928418]
[153]
Baran EJ. Metal complexes of carnosine. Biochemistry (Mosc) 2000; 65(7): 789-97.
[PMID: 10951097]
[154]
Choi SY, Kwon HY, Kwon OB, Kang JH. Hydrogen peroxide-mediated Cu,Zn-superoxide dismutase fragmentation: protection by carnosine, homocarnosine and anserine. Biochim Biophys Acta 1999; 1472(3): 651-7.
[http://dx.doi.org/10.1016/S0304-4165(99)00189-0] [PMID: 10564779]
[155]
Ukeda H, Hasegawa Y, Harada Y, Sawamura M. Effect of carnosine and related compounds on the inactivation of human Cu,Zn-superoxide dismutase by modification of fructose and glycolaldehyde. Biosci Biotechnol Biochem 2002; 66(1): 36-43.
[http://dx.doi.org/10.1271/bbb.66.36] [PMID: 11866117]
[156]
Zhao J, Shi L, Zhang LR. Neuroprotective effect of carnosine against salsolinol-induced Parkinson’s disease. Exp Ther Med 2017; 14(1): 664-70.
[http://dx.doi.org/10.3892/etm.2017.4571] [PMID: 28672983]
[157]
Fresta CG, Hogard ML, Caruso G, Melo Costa EE, Lazzarino G, Lunte SM. Monitoring carnosine uptake by RAW 264.7 macrophage cells using microchip electrophoresis with fluorescence detection. Anal Methods 2017; 9(3): 402-8.
[http://dx.doi.org/10.1039/C6AY03009B] [PMID: 29104617]
[158]
Caruso G, Fresta CG, Musso N, et al. Carnosine prevents Aβ-induced oxidative stress and inflammation in microglial cells: a key role of TGF-β1. Cells 2019; 8(1): 8.
[http://dx.doi.org/10.3390/cells8010064] [PMID: 30658430]
[159]
Caraci F, Spampinato SF, Morgese MG, et al. Neurobiological links between depression and AD: the role of TGF-β1 signaling as a new pharmacological target. Pharmacol Res 2018; 130: 374-84.
[http://dx.doi.org/10.1016/j.phrs.2018.02.007] [PMID: 29438781]
[160]
Butterfield DA, Swomley AM, Sultana R. Amyloid β-peptide (1-42)-induced oxidative stress in Alzheimer disease: importance in disease pathogenesis and progression. Antioxid Redox Signal 2013; 19(8): 823-35.
[http://dx.doi.org/10.1089/ars.2012.5027] [PMID: 23249141]
[161]
Corona C, Frazzini V, Silvestri E, et al. Effects of dietary supplementation of carnosine on mitochondrial dysfunction, amyloid pathology, and cognitive deficits in 3xTg-AD mice. PLoS One 2011; 6(3): e17971.
[http://dx.doi.org/10.1371/journal.pone.0017971] [PMID: 21423579]
[162]
Herculano B, Tamura M, Ohba A, Shimatani M, Kutsuna N, Hisatsune T. β-alanyl-L-histidine rescues cognitive deficits caused by feeding a high fat diet in a transgenic mouse model of Alzheimer’s disease. J Alzheimers Dis 2013; 33(4): 983-97.
[http://dx.doi.org/10.3233/JAD-2012-121324] [PMID: 23099816]
[163]
Gallant S, Kukley M, Stvolinsky S, Bulygina E, Boldyrev A. Effect of carnosine on rats under experimental brain ischemia. Tohoku J Exp Med 2000; 191(2): 85-99.
[http://dx.doi.org/10.1620/tjem.191.85] [PMID: 10946918]
[164]
Min J, Senut MC, Rajanikant K, et al. Differential neuroprotective effects of carnosine, anserine, and N-acetyl carnosine against permanent focal ischemia. J Neurosci Res 2008; 86(13): 2984-91.
[http://dx.doi.org/10.1002/jnr.21744] [PMID: 18543335]

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