Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Review Article

Insights Into the Role of Copper in Neurodegenerative Diseases and the Therapeutic Potential of Natural Compounds

Author(s): Guangcheng Zhong, Xinyue Wang, Jiaqi Li, Zhouyuan Xie, Qiqing Wu, Jiaxin Chen, Yiyun Wang, Ziying Chen, Xinyue Cao, Tianyao Li, Jinman Liu* and Qi Wang*

Volume 22, Issue 10, 2024

Published on: 15 November, 2023

Page: [1650 - 1671] Pages: 22

DOI: 10.2174/1570159X22666231103085859

Price: $65

conference banner
Abstract

Neurodegenerative diseases encompass a collection of neurological disorders originating from the progressive degeneration of neurons, resulting in the dysfunction of neurons. Unfortunately, effective therapeutic interventions for these diseases are presently lacking. Copper (Cu), a crucial trace element within the human body, assumes a pivotal role in various biological metabolic processes, including energy metabolism, antioxidant defense, and neurotransmission. These processes are vital for the sustenance, growth, and development of organisms. Mounting evidence suggests that disrupted copper homeostasis contributes to numerous age-related neurodegenerative diseases, such as Alzheimer's disease (AD), Parkinson's disease (PD), Huntington's disease (HD), amyotrophic lateral sclerosis (ALS), Wilson's disease (WD), Menkes disease (MD), prion diseases, and multiple sclerosis (MS). This comprehensive review investigates the connection between the imbalance of copper homeostasis and neurodegenerative diseases, summarizing pertinent drugs and therapies that ameliorate neuropathological changes, motor deficits, and cognitive impairments in these conditions through the modulation of copper metabolism. These interventions include Metal-Protein Attenuating Compounds (MPACs), copper chelators, copper supplements, and zinc salts. Moreover, this review highlights the potential of active compounds derived from natural plant medicines to enhance neurodegenerative disease outcomes by regulating copper homeostasis. Among these compounds, polyphenols are particularly abundant. Consequently, this review holds significant implications for the future development of innovative drugs targeting the treatment of neurodegenerative diseases.

Keywords: Neurodegenerative diseases, cognitive impairments, copper chelators, metal-protein attenuating compounds, natural compounds, polyphenol.

Graphical Abstract
[1]
Hetz, C.; Saxena, S. ER stress and the unfolded protein response in neurodegeneration. Nat. Rev. Neurol., 2017, 13(8), 477-491.
[http://dx.doi.org/10.1038/nrneurol.2017.99] [PMID: 28731040]
[2]
Barnham, K.J.; Masters, C.L.; Bush, A.I. Neurodegenerative diseases and oxidative stress. Nat. Rev. Drug Discov., 2004, 3(3), 205-214.
[http://dx.doi.org/10.1038/nrd1330] [PMID: 15031734]
[3]
Nixon, R.A. The role of autophagy in neurodegenerative disease. Nat. Med., 2013, 19(8), 983-997.
[http://dx.doi.org/10.1038/nm.3232] [PMID: 23921753]
[4]
Ross, C.A.; Poirier, M.A. Protein aggregation and neurodegenerative disease. Nat. Med., 2004, 10(S7)(Suppl.), S10-S17.
[http://dx.doi.org/10.1038/nm1066] [PMID: 15272267]
[5]
Nguyen, P.H.; Ramamoorthy, A.; Sahoo, B.R.; Zheng, J.; Faller, P.; Straub, J.E.; Dominguez, L.; Shea, J.E.; Dokholyan, N.V.; De Simone, A.; Ma, B.; Nussinov, R.; Najafi, S.; Ngo, S.T.; Loquet, A.; Chiricotto, M.; Ganguly, P.; McCarty, J.; Li, M.S.; Hall, C.; Wang, Y.; Miller, Y.; Melchionna, S.; Habenstein, B.; Timr, S.; Chen, J.; Hnath, B.; Strodel, B.; Kayed, R.; Lesné, S.; Wei, G.; Sterpone, F.; Doig, A.J.; Derreumaux, P. Amyloid oligomers: a joint experimental/computational perspective on Alzheimer’s disease, Parkinson’s disease, Type II diabetes, and amyotrophic lateral sclerosis. Chem. Rev., 2021, 121(4), 2545-2647.
[http://dx.doi.org/10.1021/acs.chemrev.0c01122] [PMID: 33543942]
[6]
Arnal, N.; Castillo, O.; de Alaniz, M.J.T.; Marra, C.A. Effects of copper and/or cholesterol overload on mitochondrial function in a rat model of incipient neurodegeneration. Int. J. Alzheimers Dis., 2013, 2013, 1-14.
[http://dx.doi.org/10.1155/2013/645379] [PMID: 24363953]
[7]
Ke, Y.; Qian, Z.M. Iron misregulation in the brain: a primary cause of neurodegenerative disorders. Lancet Neurol., 2003, 2(4), 246-253.
[http://dx.doi.org/10.1016/S1474-4422(03)00353-3] [PMID: 12849213]
[8]
Chen, J.; Jiang, Y.; Shi, H.; Peng, Y.; Fan, X.; Li, C. The molecular mechanisms of copper metabolism and its roles in human diseases. Pflugers Arch., 2020, 472(10), 1415-1429.
[http://dx.doi.org/10.1007/s00424-020-02412-2] [PMID: 32506322]
[9]
Russell, K.; Gillanders, L.K.; Orr, D.W.; Plank, L.D. Dietary copper restriction in Wilson’s disease. Eur. J. Clin. Nutr., 2018, 72(3), 326-331.
[http://dx.doi.org/10.1038/s41430-017-0002-0] [PMID: 29235558]
[10]
Kolbaum, A.E.; Sarvan, I.; Bakhiya, N.; Spolders, M.; Pieper, R.; Schubert, J.; Jung, C.; Hackethal, C.; Sieke, C.; Grünewald, K.H.; Lindtner, O. Long-term dietary exposure to copper in the population in Germany – Results from the BfR MEAL study. Food Chem. Toxicol., 2023, 176, 113759.
[http://dx.doi.org/10.1016/j.fct.2023.113759] [PMID: 37028745]
[11]
Tokuşoǧlu, Ö.; Aycan, Ş.; Akalin, S.; Koçak, S.; Ersoy, N. Simultaneous differential pulse polarographic determination of cadmium, lead, and copper in milk and dairy products. J. Agric. Food Chem., 2004, 52(7), 1795-1799.
[http://dx.doi.org/10.1021/jf034860l] [PMID: 15053511]
[12]
Zheng, W.; Monnot, A.D. Regulation of brain iron and copper homeostasis by brain barrier systems: Implication in neurodegenerative diseases. Pharmacol. Ther., 2012, 133(2), 177-188.
[http://dx.doi.org/10.1016/j.pharmthera.2011.10.006] [PMID: 22115751]
[13]
Brewer, G. Copper-2 ingestion, plus increased meat eating leading to increased copper absorption, are major factors behind the current epidemic of Alzheimer’s disease. Nutrients, 2015, 7(12), 10053-10064.
[http://dx.doi.org/10.3390/nu7125513] [PMID: 26633489]
[14]
Ruiz, L.M.; Libedinsky, A.; Elorza, A.A. Role of copper on mitochondrial function and metabolism. Front. Mol. Biosci., 2021, 8, 711227.
[http://dx.doi.org/10.3389/fmolb.2021.711227] [PMID: 34504870]
[15]
Scheiber, I.F.; Mercer, J.F.B.; Dringen, R. Metabolism and functions of copper in brain. Prog. Neurobiol., 2014, 116, 33-57.
[http://dx.doi.org/10.1016/j.pneurobio.2014.01.002] [PMID: 24440710]
[16]
Arredondo, M.; Núñez, M.T. Iron and copper metabolism. Mol. Aspects Med., 2005, 26(4-5), 313-327.
[http://dx.doi.org/10.1016/j.mam.2005.07.010] [PMID: 16112186]
[17]
Gromadzka, G.; Tarnacka, B.; Flaga, A.; Adamczyk, A. Copper dyshomeostasis in neurodegenerative diseases-therapeutic implications. Int. J. Mol. Sci., 2020, 21(23), 9259.
[http://dx.doi.org/10.3390/ijms21239259] [PMID: 33291628]
[18]
Kaler, S.G. ATP7A-related copper transport diseases—emerging concepts and future trends. Nat. Rev. Neurol., 2011, 7(1), 15-29.
[http://dx.doi.org/10.1038/nrneurol.2010.180] [PMID: 21221114]
[19]
Rasoul, A.A.; Khudhur, Z.O.; Hamad, M.S.; Ismaeal, Y.S.; Smail, S.W.; Rasul, M.F.; Mohammad, K.A.; Bapir, A.A.; Omar, S.A.; Qadir, M.K.; Rajab, M.F.; Salihi, A.; Kaleem, M.; Rizwan, M.A.; Qureshi, A.S.; Iqbal, Z.M. Qudratullah. The role of oxidative stress and haematological parameters in relapsing-remitting multiple sclerosis in Kurdish population. Mult. Scler. Relat. Disord., 2021, 56, 103228.
[http://dx.doi.org/10.1016/j.msard.2021.103228] [PMID: 34492630]
[20]
Tsvetkov, P.; Coy, S.; Petrova, B.; Dreishpoon, M.; Verma, A.; Abdusamad, M.; Rossen, J.; Joesch-Cohen, L.; Humeidi, R.; Spangler, R.D.; Eaton, J.K.; Frenkel, E.; Kocak, M.; Corsello, S.M.; Lutsenko, S.; Kanarek, N.; Santagata, S.; Golub, T.R. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science, 2022, 375(6586), 1254-1261.
[http://dx.doi.org/10.1126/science.abf0529] [PMID: 35298263]
[21]
An, Y.; Li, S.; Huang, X.; Chen, X.; Shan, H.; Zhang, M. The role of copper homeostasis in brain disease. Int. J. Mol. Sci., 2022, 23(22), 13850.
[http://dx.doi.org/10.3390/ijms232213850] [PMID: 36430330]
[22]
Law, B.Y.K.; Wu, A.G.; Wang, M.J.; Zhu, Y.Z. Chinese medicine: a hope for neurodegenerative diseases? J. Alzheimers Dis., 2017, 60(s1), S151-S160.
[http://dx.doi.org/10.3233/JAD-170374] [PMID: 28671133]
[23]
Pei, H.; Ma, L.; Cao, Y.; Wang, F.; Li, Z.; Liu, N.; Liu, M.; Wei, Y.; Li, H. Traditional Chinese medicine for Alzheimer’s disease and other cognitive impairment: A review. Am. J. Chin. Med., 2020, 48(3), 487-511.
[http://dx.doi.org/10.1142/S0192415X20500251] [PMID: 32329645]
[24]
De Riccardis, L.; Buccolieri, A.; Muci, M.; Pitotti, E.; De Robertis, F.; Trianni, G.; Manno, D.; Maffia, M. Copper and ceruloplasmin dyshomeostasis in serum and cerebrospinal fluid of multiple sclerosis subjects. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(5), 1828-1838.
[http://dx.doi.org/10.1016/j.bbadis.2018.03.007] [PMID: 29524632]
[25]
Sheykhansari, S.; Kozielski, K.; Bill, J.; Sitti, M.; Gemmati, D.; Zamboni, P.; Singh, A.V. Redox metals homeostasis in multiple sclerosis and amyotrophic lateral sclerosis: A review. Cell Death Dis., 2018, 9(3), 348.
[http://dx.doi.org/10.1038/s41419-018-0379-2] [PMID: 29497049]
[26]
Hung, Y.H.; Bush, A.I.; La Fontaine, S. Links between copper and cholesterol in Alzheimer’s disease. Front. Physiol., 2013, 4, 111.
[http://dx.doi.org/10.3389/fphys.2013.00111] [PMID: 23720634]
[27]
Tokuda, E.; Okawa, E.; Ono, S. Dysregulation of intracellular copper trafficking pathway in a mouse model of mutant copper/zinc superoxide dismutase-linked familial amyotrophic lateral sclerosis. J. Neurochem., 2009, 111(1), 181-191.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06310.x] [PMID: 19656261]
[28]
Liu, Y.; Miao, J. An emerging role of defective copper metabolism in heart disease. Nutrients, 2022, 14(3), 700.
[http://dx.doi.org/10.3390/nu14030700] [PMID: 35277059]
[29]
Gil-Bea, F.J.; Aldanondo, G.; Lasa-Fernández, H.; López de Munain, A.; Vallejo-Illarramendi, A. Insights into the mechanisms of copper dyshomeostasis in amyotrophic lateral sclerosis. Expert Rev. Mol. Med., 2017, 19, e7.
[http://dx.doi.org/10.1017/erm.2017.9] [PMID: 28597807]
[30]
Davies, K.M.; Hare, D.J.; Cottam, V.; Chen, N.; Hilgers, L.; Halliday, G.; Mercer, J.F.B.; Double, K.L. Localization of copper and copper transporters in the human brain. Metallomics, 2013, 5(1), 43-51.
[http://dx.doi.org/10.1039/C2MT20151H] [PMID: 23076575]
[31]
Skjørringe, T.; Møller, L.B.; Moos, T. Impairment of interrelated iron- and copper homeostatic mechanisms in brain contributes to the pathogenesis of neurodegenerative disorders. Front. Pharmacol., 2012, 3, 169.
[http://dx.doi.org/10.3389/fphar.2012.00169] [PMID: 23055972]
[32]
Sweeney, M.D.; Sagare, A.P.; Zlokovic, B.V. Blood–brain barrier breakdown in Alzheimer disease and other neurodegenerative disorders. Nat. Rev. Neurol., 2018, 14(3), 133-150.
[http://dx.doi.org/10.1038/nrneurol.2017.188] [PMID: 29377008]
[33]
Haywood, S.; Vaillant, C. Overexpression of copper transporter CTR1 in the brain barrier of North Ronaldsay sheep: Implications for the study of neurodegenerative disease. J. Comp. Pathol., 2014, 150(2-3), 216-224.
[http://dx.doi.org/10.1016/j.jcpa.2013.09.002] [PMID: 24172593]
[34]
Hsu, H.W.; Bondy, S.C.; Kitazawa, M. Environmental and dietary exposure to copper and its cellular mechanisms linking to Alzheimer’s disease. Toxicol. Sci., 2018, 163(2), 338-345.
[http://dx.doi.org/10.1093/toxsci/kfy025] [PMID: 29409005]
[35]
Ijomone, O.M.; Ifenatuoha, C.W.; Aluko, O.M.; Ijomone, O.K.; Aschner, M. The aging brain: impact of heavy metal neurotoxicity. Crit. Rev. Toxicol., 2020, 50(9), 801-814.
[http://dx.doi.org/10.1080/10408444.2020.1838441] [PMID: 33210961]
[36]
Madsen, E.; Gitlin, J.D. Copper and iron disorders of the brain. Annu. Rev. Neurosci., 2007, 30(1), 317-337.
[http://dx.doi.org/10.1146/annurev.neuro.30.051606.094232] [PMID: 17367269]
[37]
Prasad, A.N.; Ojha, R. Menkes disease: What a multidisciplinary approach can do. J. Multidiscip. Healthc., 2016, 9, 371-385.
[http://dx.doi.org/10.2147/JMDH.S93454] [PMID: 27574440]
[38]
Goedert, M. Alzheimer’s and Parkinson’s diseases: The prion concept in relation to assembled Aβ tau, and α-synuclein. Science, 2015, 349(6248), 1255555.
[http://dx.doi.org/10.1126/science.1255555] [PMID: 26250687]
[39]
Sinyor, B.; Mineo, J.; Ochner, C. Alzheimer’s disease, inflammation, and the role of antioxidants. J. Alzheimers Dis. Rep., 2020, 4(1), 175-183.
[http://dx.doi.org/10.3233/ADR-200171] [PMID: 32715278]
[40]
Squitti, R.; Pasqualetti, P.; Dal Forno, G.; Moffa, F.; Cassetta, E.; Lupoi, D.; Vernieri, F.; Rossi, L.; Baldassini, M.; Rossini, P.M. Excess of serum copper not related to ceruloplasmin in Alzheimer disease. Neurology, 2005, 64(6), 1040-1046.
[http://dx.doi.org/10.1212/01.WNL.0000154531.79362.23] [PMID: 15781823]
[41]
Robert, A.; Liu, Y.; Nguyen, M.; Meunier, B. Regulation of copper and iron homeostasis by metal chelators: A possible chemotherapy for Alzheimer’s disease. Acc. Chem. Res., 2015, 48(5), 1332-1339.
[http://dx.doi.org/10.1021/acs.accounts.5b00119] [PMID: 25946460]
[42]
Lovell, M.A.; Robertson, J.D.; Teesdale, W.J.; Campbell, J.L.; Markesbery, W.R. Copper, iron and zinc in Alzheimer’s disease senile plaques. J. Neurol. Sci., 1998, 158(1), 47-52.
[http://dx.doi.org/10.1016/S0022-510X(98)00092-6] [PMID: 9667777]
[43]
Ejaz, H.W.; Wang, W.; Lang, M. Copper toxicity links to pathogenesis of Alzheimer’s disease and therapeutics approaches. Int. J. Mol. Sci., 2020, 21(20), 7660.
[http://dx.doi.org/10.3390/ijms21207660] [PMID: 33081348]
[44]
Deibel, M.A.; Ehmann, W.D.; Markesbery, W.R. Copper, iron, and zinc imbalances in severely degenerated brain regions in Alzheimer’s disease: Possible relation to oxidative stress. J. Neurol. Sci., 1996, 143(1-2), 137-142.
[http://dx.doi.org/10.1016/S0022-510X(96)00203-1] [PMID: 8981312]
[45]
Rivera-Mancía, S.; Pérez-Neri, I.; Ríos, C.; Tristán-López, L.; Rivera-Espinosa, L.; Montes, S. The transition metals copper and iron in neurodegenerative diseases. Chem. Biol. Interact., 2010, 186(2), 184-199.
[http://dx.doi.org/10.1016/j.cbi.2010.04.010] [PMID: 20399203]
[46]
Loeffler, D.A.; LeWitt, P.A.; Juneau, P.L.; Sima, A.A.F.; Nguyen, H.U.; DeMaggio, A.J.; Brickman, C.M.; Brewer, G.J.; Dick, R.D.; Troyer, M.D.; Kanaley, L. Increased regional brain concentrations of ceruloplasmin in neurodegenerative disorders. Brain Res., 1996, 738(2), 265-274.
[http://dx.doi.org/10.1016/S0006-8993(96)00782-2] [PMID: 8955522]
[47]
Choo, X.Y.; Alukaidey, L.; White, A.R.; Grubman, A. Neuroinflammation and copper in Alzheimer’s disease. Int. J. Alzheimers Dis., 2013, 2013, 1-12.
[http://dx.doi.org/10.1155/2013/145345] [PMID: 24369524]
[48]
Bagheri, S.; Squitti, R.; Haertlé, T.; Siotto, M.; Saboury, A.A. 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]
[49]
Zubčić K.; Hof, P.R.; Šimić G.; Jazvinšćak Jembrek, M. The role of copper in tau-related pathology in Alzheimer’s disease. Front. Mol. Neurosci., 2020, 13, 572308.
[http://dx.doi.org/10.3389/fnmol.2020.572308] [PMID: 33071757]
[50]
Voss, K.; Harris, C.; Ralle, M.; Duffy, M.; Murchison, C.; Quinn, J.F. Modulation of tau phosphorylation by environmental copper. Transl. Neurodegener., 2014, 3(1), 24.
[http://dx.doi.org/10.1186/2047-9158-3-24] [PMID: 25671100]
[51]
Singh, I.; Sagare, A.P.; Coma, M.; Perlmutter, D.; Gelein, R.; Bell, R.D.; Deane, R.J.; Zhong, E.; Parisi, M.; Ciszewski, J.; Kasper, R.T.; Deane, R. Low levels of copper disrupt brain amyloid-β homeostasis by altering its production and clearance. Proc. Natl. Acad. Sci. USA, 2013, 110(36), 14771-14776.
[http://dx.doi.org/10.1073/pnas.1302212110] [PMID: 23959870]
[52]
Busche, M.A.; Hyman, B.T. Synergy between amyloid-β and tau in Alzheimer’s disease. Nat. Neurosci., 2020, 23(10), 1183-1193.
[http://dx.doi.org/10.1038/s41593-020-0687-6] [PMID: 32778792]
[53]
Aaseth, J.; Skalny, A.V.; Roos, P.M.; Alexander, J.; Aschner, M.; Tinkov, A.A. Copper, iron, selenium and lipo-glycemic dysmetabolism in Alzheimer’s disease. Int. J. Mol. Sci., 2021, 22(17), 9461.
[http://dx.doi.org/10.3390/ijms22179461] [PMID: 34502369]
[54]
Pal, A. Copper toxicity induced hepatocerebral and neurodegenerative diseases: An urgent need for prognostic biomarkers. Neurotoxicology, 2014, 40, 97-101.
[http://dx.doi.org/10.1016/j.neuro.2013.12.001] [PMID: 24342654]
[55]
Pal, A.; Kumar, A.; Prasad, R. Predictive association of copper metabolism proteins with Alzheimer’s disease and Parkinson’s disease: a preliminary perspective. Biometals, 2014, 27(1), 25-31.
[http://dx.doi.org/10.1007/s10534-013-9702-7] [PMID: 24435851]
[56]
Bloem, B.R.; Okun, M.S.; Klein, C. Parkinson’s disease. Lancet, 2021, 397(10291), 2284-2303.
[http://dx.doi.org/10.1016/S0140-6736(21)00218-X] [PMID: 33848468]
[57]
Aaseth, J.; Dusek, P.; Roos, P.M. Prevention of progression in Parkinson’s disease. Biometals, 2018, 31(5), 737-747.
[http://dx.doi.org/10.1007/s10534-018-0131-5] [PMID: 30030679]
[58]
Tolosa, E.; Garrido, A.; Scholz, S.W.; Poewe, W. Challenges in the diagnosis of Parkinson’s disease. Lancet Neurol., 2021, 20(5), 385-397.
[http://dx.doi.org/10.1016/S1474-4422(21)00030-2] [PMID: 33894193]
[59]
Montes, S.; Rivera-Mancia, S.; Diaz-Ruiz, A.; Tristan-Lopez, L.; Rios, C. Copper and copper proteins in Parkinson’s disease. Oxid. Med. Cell. Longev., 2014, 2014, 1-15.
[http://dx.doi.org/10.1155/2014/147251] [PMID: 24672633]
[60]
Wang, Q.; Luo, Y.; Ray Chaudhuri, K.; Reynolds, R.; Tan, E.K.; Pettersson, S. The role of gut dysbiosis in Parkinson’s disease: mechanistic insights and therapeutic options. Brain, 2021, 144(9), 2571-2593.
[http://dx.doi.org/10.1093/brain/awab156] [PMID: 33856024]
[61]
Gangania, M.K.; Batra, J.; Kushwaha, S.; Agarwal, R. Role of iron and copper in the pathogenesis of Parkinson’s disease. Indian J. Clin. Biochem., 2017, 32(3), 353-356.
[http://dx.doi.org/10.1007/s12291-016-0614-5] [PMID: 28811697]
[62]
Raj, K.; Kaur, P.; Gupta, G.D.; Singh, S. Metals associated neurodegeneration in Parkinson’s disease: Insight to physiological, pathological mechanisms and management. Neurosci. Lett., 2021, 753, 135873.
[http://dx.doi.org/10.1016/j.neulet.2021.135873] [PMID: 33812934]
[63]
Cherny, R.A.; Ayton, S.; Finkelstein, D.I.; Bush, A.I.; McColl, G.; Massa, S.M. PBT2 reduces toxicity in a c. elegans model of polyQ aggregation and extends lifespan, reduces striatal atrophy and improves motor performance in the R6/2 mouse model of Huntington’s disease. J. Huntingtons Dis., 2012, 1(2), 211-219.
[http://dx.doi.org/10.3233/JHD-120029] [PMID: 25063332]
[64]
Hands, S.L.; Mason, R.; Sajjad, M.U.; Giorgini, F.; Wyttenbach, A. Metallothioneins and copper metabolism are candidate therapeutic targets in Huntington’s disease. Biochem. Soc. Trans., 2010, 38(2), 552-558.
[http://dx.doi.org/10.1042/BST0380552] [PMID: 20298220]
[65]
Dexter, D.T.; Carayon, A.; Javoy-Agid, F.; Agid, Y.; Wells, F.R.; Daniel, S.E.; Lees, A.J.; Jenner, P.; Marsden, C.D. Alterations in the levels of iron, ferritin and other trace metals in Parkinson’s disease and other neurodegenerative diseases affecting the basal ganglia. Brain, 1991, 114(4), 1953-1975.
[http://dx.doi.org/10.1093/brain/114.4.1953] [PMID: 1832073]
[66]
Scholefield, M.; Unwin, R.D.; Cooper, G.J.S. Shared perturbations in the metallome and metabolome of Alzheimer’s, Parkinson’s, Huntington’s, and dementia with Lewy bodies: A systematic review. Ageing Res. Rev., 2020, 63, 101152.
[http://dx.doi.org/10.1016/j.arr.2020.101152] [PMID: 32846222]
[67]
Grubman, A.; White, A.R.; Liddell, J.R. Mitochondrial metals as a potential therapeutic target in neurodegeneration. Br. J. Pharmacol., 2014, 171(8), 2159-2173.
[http://dx.doi.org/10.1111/bph.12513] [PMID: 24206195]
[68]
Maung, M.T.; Carlson, A.; Olea-Flores, M.; Elkhadragy, L.; Schachtschneider, K.M.; Navarro-Tito, N.; Padilla-Benavides, T. The molecular and cellular basis of copper dysregulation and its relationship with human pathologies. FASEB J., 2021, 35(9), e21810.
[http://dx.doi.org/10.1096/fj.202100273RR] [PMID: 34390520]
[69]
Fox, J.H.; Kama, J.A.; Lieberman, G.; Chopra, R.; Dorsey, K.; Chopra, V.; Volitakis, I.; Cherny, R.A.; Bush, A.I.; Hersch, S. Mechanisms of copper ion mediated Huntington’s disease progression. PLoS One, 2007, 2(3), e334.
[http://dx.doi.org/10.1371/journal.pone.0000334] [PMID: 17396163]
[70]
Clarke, B.E.; Patani, R. The microglial component of amyotrophic lateral sclerosis. Brain, 2020, 143(12), 3526-3539.
[http://dx.doi.org/10.1093/brain/awaa309] [PMID: 33427296]
[71]
Van Harten, A.C.M.; Phatnani, H.; Przedborski, S. Non-cell-autonomous pathogenic mechanisms in amyotrophic lateral sclerosis. Trends Neurosci., 2021, 44(8), 658-668.
[http://dx.doi.org/10.1016/j.tins.2021.04.008] [PMID: 34006386]
[72]
Gellein, K.; Garruto, R.M.; Syversen, T.; Sjøbakk, T.E.; Flaten, T.P. Concentrations of Cd, Co, Cu, Fe, Mn, Rb, V, and Zn in formalin-fixed brain tissue in amyotrophic lateral sclerosis and Parkinsonism-dementia complex of Guam determined by High-resolution ICP-MS. Biol. Trace Elem. Res., 2003, 96(1-3), 39-60.
[http://dx.doi.org/10.1385/BTER:96:1-3:39] [PMID: 14716085]
[73]
Kapaki, E.; Zournas, C.; Kanias, G.; Zambelis, T.; Kakami, A.; Papageorgiou, C. Essential trace element alterations in amyotrophic lateral sclerosis. J. Neurol. Sci., 1997, 147(2), 171-175.
[http://dx.doi.org/10.1016/S0022-510X(96)05334-8] [PMID: 9106124]
[74]
Barros, A.N.A.B.; Dourado, M.E.T., Jr; Pedrosa, L.F.C.; Leite-Lais, L. Association of copper status with lipid profile and functional status in patients with amyotrophic lateral sclerosis. J. Nutr. Metab., 2018, 2018, 1-7.
[http://dx.doi.org/10.1155/2018/5678698] [PMID: 30116640]
[75]
Kreuzer, M. Stamenković S.; Chen, S.; Andjus, P.; Dučić T. Lipids status and copper in a single astrocyte of the rat model for amyotrophic lateral sclerosis: Correlative synchrotron‐based X‐ray and infrared imaging. J. Biophotonics, 2020, 13(10), e202000069.
[http://dx.doi.org/10.1002/jbio.202000069] [PMID: 32463554]
[76]
Abati, E.; Bresolin, N.; Comi, G.; Corti, S. Silence superoxide dismutase 1 (SOD1): a promising therapeutic target for amyotrophic lateral sclerosis (ALS). Expert Opin. Ther. Targets, 2020, 24(4), 295-310.
[http://dx.doi.org/10.1080/14728222.2020.1738390] [PMID: 32125907]
[77]
Hilton, J.B.; White, A.R.; Crouch, P.J. Metal-deficient SOD1 in amyotrophic lateral sclerosis. J. Mol. Med. (Berl.), 2015, 93(5), 481-487.
[http://dx.doi.org/10.1007/s00109-015-1273-3] [PMID: 25754173]
[78]
Enge, T.G.; Ecroyd, H.; Jolley, D.F.; Yerbury, J.J.; Kalmar, B.; Dosseto, A. Assessment of metal concentrations in the SOD1G93A mouse model of amyotrophic lateral sclerosis and its potential role in muscular denervation, with particular focus on muscle tissue. Mol. Cell. Neurosci., 2018, 88, 319-329.
[http://dx.doi.org/10.1016/j.mcn.2018.03.001] [PMID: 29524628]
[79]
Tokuda, E.; Nomura, T.; Ohara, S.; Watanabe, S.; Yamanaka, K.; Morisaki, Y.; Misawa, H.; Furukawa, Y. A copper-deficient form of mutant Cu/Zn-superoxide dismutase as an early pathological species in amyotrophic lateral sclerosis. Biochim. Biophys. Acta Mol. Basis Dis., 2018, 1864(6), 2119-2130.
[http://dx.doi.org/10.1016/j.bbadis.2018.03.015] [PMID: 29551730]
[80]
Sirangelo, I.; Iannuzzi, C. The role of metal binding in the amyotrophic lateral sclerosis-related aggregation of copper-zinc superoxide dismutase. Molecules, 2017, 22(9), 1429.
[http://dx.doi.org/10.3390/molecules22091429] [PMID: 28850080]
[81]
Sauzéat, L.; Bernard, E.; Perret-Liaudet, A.; Quadrio, I.; Vighetto, A.; Krolak-Salmon, P.; Broussolle, E.; Leblanc, P.; Balter, V. Isotopic evidence for disrupted copper metabolism in amyotrophic lateral sclerosis. iScience, 2018, 6, 264-271.
[http://dx.doi.org/10.1016/j.isci.2018.07.023] [PMID: 30240616]
[82]
Tarnacka, B.; Jopowicz, A. Maślińska, M. Copper, iron, and manganese toxicity in neuropsychiatric conditions. Int. J. Mol. Sci., 2021, 22(15), 7820.
[http://dx.doi.org/10.3390/ijms22157820] [PMID: 34360586]
[83]
Kurlander, H.M.; Patten, B.M. Metals in spinal cord tissue of patients dying of motor neuron disease. Ann. Neurol., 1979, 6(1), 21-24.
[http://dx.doi.org/10.1002/ana.410060105] [PMID: 507754]
[84]
Katzeff, J.S.; Bright, F.; Phan, K.; Kril, J.J.; Ittner, L.M.; Kassiou, M.; Hodges, J.R.; Piguet, O.; Kiernan, M.C.; Halliday, G.M.; Kim, W.S. Biomarker discovery and development for frontotemporal dementia and amyotrophic lateral sclerosis. Brain, 2022, 145(5), 1598-1609.
[http://dx.doi.org/10.1093/brain/awac077] [PMID: 35202463]
[85]
Tokuda, E.; Ono, S.; Ishige, K.; Watanabe, S.; Okawa, E.; Ito, Y.; Suzuki, T. Ammonium tetrathiomolybdate delays onset, prolongs survival, and slows progression of disease in a mouse model for amyotrophic lateral sclerosis. Exp. Neurol., 2008, 213(1), 122-128.
[http://dx.doi.org/10.1016/j.expneurol.2008.05.011] [PMID: 18617166]
[86]
Bandmann, O.; Weiss, K.H.; Kaler, S.G. Wilson’s disease and other neurological copper disorders. Lancet Neurol., 2015, 14(1), 103-113.
[http://dx.doi.org/10.1016/S1474-4422(14)70190-5] [PMID: 25496901]
[87]
Lalioti, V.; Sandoval, I.; Cassio, D.; Duclos-Vallée, J.C. Molecular pathology of Wilson’s disease: A brief. J. Hepatol., 2010, 53(6), 1151-1153.
[http://dx.doi.org/10.1016/j.jhep.2010.07.008] [PMID: 20832891]
[88]
Xu, R.; Jiang, Y.; Zhang, Y.; Yang, X. The optimal threshold of serum ceruloplasmin in the diagnosis of Wilson’s disease: A large hospital-based study. PLoS One, 2018, 13(1), e0190887.
[http://dx.doi.org/10.1371/journal.pone.0190887] [PMID: 29324775]
[89]
Yang, Y.; Hao, W.; Wei, T.; Tang, L.; Qian, N.; Yang, Y.; Xi, H.; Zhang, S.; Yang, W. Role of serum ceruloplasmin in the diagnosis of Wilson’s disease: A large Chinese study. Front. Neurol., 2022, 13, 1058642.
[http://dx.doi.org/10.3389/fneur.2022.1058642] [PMID: 36570465]
[90]
Ala, A.; Walker, A.P.; Ashkan, K.; Dooley, J.S.; Schilsky, M.L. Wilson’s disease. Lancet, 2007, 369(9559), 397-408.
[http://dx.doi.org/10.1016/S0140-6736(07)60196-2] [PMID: 17276780]
[91]
Lutsenko, S. Atp7b −/− mice as a model for studies of Wilson’s disease. Biochem. Soc. Trans., 2008, 36(6), 1233-1238.
[http://dx.doi.org/10.1042/BST0361233] [PMID: 19021531]
[92]
Wooton-Kee, C.R.; Jain, A.K.; Wagner, M.; Grusak, M.A.; Finegold, M.J.; Lutsenko, S.; Moore, D.D. Elevated copper impairs hepatic nuclear receptor function in Wilson’s disease. J. Clin. Invest., 2015, 125(9), 3449-3460.
[http://dx.doi.org/10.1172/JCI78991] [PMID: 26241054]
[93]
Shribman, S.; Poujois, A.; Bandmann, O.; Czlonkowska, A.; Warner, T.T. Wilson’s disease: update on pathogenesis, biomarkers and treatments. J. Neurol. Neurosurg. Psychiatry, 2021, 92(10), 1053-1061.
[http://dx.doi.org/10.1136/jnnp-2021-326123] [PMID: 34341141]
[94]
Zischka, H.; Lichtmannegger, J. Pathological mitochondrial copper overload in livers of Wilson’s disease patients and related animal models. Ann. N. Y. Acad. Sci., 2014, 1315(1), 6-15.
[http://dx.doi.org/10.1111/nyas.12347] [PMID: 24517326]
[95]
Litwin, T.; Gromadzka, G.; Szpak, G.M. Jabłonka-Salach, K.; Bulska, E.; Członkowska, A. Brain metal accumulation in Wilson’s disease. J. Neurol. Sci., 2013, 329(1-2), 55-58.
[http://dx.doi.org/10.1016/j.jns.2013.03.021] [PMID: 23597670]
[96]
Lech, T.; Hydzik, P.; Kosowski, B. Significance of copper determination in late onset of Wilson’s disease. Clin. Toxicol. (Phila.), 2007, 45(6), 688-694.
[http://dx.doi.org/10.1080/15563650701502535] [PMID: 17849244]
[97]
Sokol, R.J.; Twedt, D.; McKim, J.M., Jr; Devereaux, M.W.; Karrer, F.M.; Kam, I.; Von Steigman, G.; Narkewicz, M.R.; Bacon, B.R.; Britton, R.S.; Neuschwander-Tetri, B.A. Oxidant injury to hepatic mitochondria in patients with Wilson’s disease and Bedlington terriers with copper toxicosis. Gastroenterology, 1994, 107(6), 1788-1798.
[http://dx.doi.org/10.1016/0016-5085(94)90822-2] [PMID: 7958693]
[98]
Brewer, G.J.; Askari, F.; Dick, R.B.; Sitterly, J.; Fink, J.K.; Carlson, M.; Kluin, K.J.; Lorincz, M.T. Treatment of Wilson’s disease with tetrathiomolybdate: V. control of free copper by tetrathiomolybdate and a comparison with trientine. Transl. Res., 2009, 154(2), 70-77.
[http://dx.doi.org/10.1016/j.trsl.2009.05.002] [PMID: 19595438]
[99]
Tümer, Z. An overview and update of ATP7A mutations leading to Menkes disease and occipital horn syndrome. Hum. Mutat., 2013, 34(3), 417-429.
[http://dx.doi.org/10.1002/humu.22266] [PMID: 23281160]
[100]
Donsante, A.; Yi, L.; Zerfas, P.M.; Brinster, L.R.; Sullivan, P.; Goldstein, D.S.; Prohaska, J.; Centeno, J.A.; Rushing, E.; Kaler, S.G. ATP7A gene addition to the choroid plexus results in long-term rescue of the lethal copper transport defect in a Menkes disease mouse model. Mol. Ther., 2011, 19(12), 2114-2123.
[http://dx.doi.org/10.1038/mt.2011.143] [PMID: 21878905]
[101]
Bertini, I.; Rosato, A. Menkes disease. Cell. Mol. Life Sci., 2008, 65(1), 89-91.
[http://dx.doi.org/10.1007/s00018-007-7439-6] [PMID: 17989919]
[102]
Lenartowicz, M.; Krzeptowski, W. Lipiński, P.; Grzmil, P.; Starzyński, R.; Pierzchała, O.; Møller, L.B. Mottled mice and non-mammalian models of Menkes disease. Front. Mol. Neurosci., 2015, 8, 72.
[http://dx.doi.org/10.3389/fnmol.2015.00072] [PMID: 26732058]
[103]
Giampietro, R.; Spinelli, F.; Contino, M.; Colabufo, N.A. The pivotal role of copper in neurodegeneration: A new strategy for the therapy of neurodegenerative disorders. Mol. Pharm., 2018, 15(3), 808-820.
[http://dx.doi.org/10.1021/acs.molpharmaceut.7b00841] [PMID: 29323501]
[104]
Horn, N.; Wittung-Stafshede, P. ATP7A-regulated enzyme metalation and trafficking in the Menkes disease puzzle. Biomedicines, 2021, 9(4), 391.
[http://dx.doi.org/10.3390/biomedicines9040391] [PMID: 33917579]
[105]
Guo, Y.; Xia, W.; Peng, X.; Shao, J. Almost misdiagnosed Menkes disease: A case report. Heliyon, 2022, 8(4), e09268.
[http://dx.doi.org/10.1016/j.heliyon.2022.e09268] [PMID: 35464712]
[106]
Aguzzi, A.; Zhu, C. Microglia in prion diseases. J. Clin. Invest., 2017, 127(9), 3230-3239.
[http://dx.doi.org/10.1172/JCI90605] [PMID: 28714865]
[107]
Choi, C.J.; Kanthasamy, A.; Anantharam, V.; Kanthasamy, A.G. Interaction of metals with prion protein: Possible role of divalent cations in the pathogenesis of prion diseases. Neurotoxicology, 2006, 27(5), 777-787.
[http://dx.doi.org/10.1016/j.neuro.2006.06.004] [PMID: 16860868]
[108]
Johnson, R.T. Prion diseases. Lancet Neurol., 2005, 4(10), 635-642.
[http://dx.doi.org/10.1016/S1474-4422(05)70192-7] [PMID: 16168932]
[109]
Unterberger, U.; Voigtländer, T.; Budka, H. Pathogenesis of prion diseases. Acta Neuropathol., 2005, 109(1), 32-48.
[http://dx.doi.org/10.1007/s00401-004-0953-9] [PMID: 15645262]
[110]
Kawahara, M.; Kato-Negishi, M.; Tanaka, K. Neurometals in the pathogenesis of Prion diseases. Int. J. Mol. Sci., 2021, 22(3), 1267.
[http://dx.doi.org/10.3390/ijms22031267] [PMID: 33525334]
[111]
Kretzschmar, H.A. Molecular pathogenesis of prion diseases. Eur. Arch. Psychiatry Clin. Neurosci., 1999, 249(S3)(Suppl. 3), S56-S63.
[http://dx.doi.org/10.1007/PL00014175] [PMID: 10654101]
[112]
Aguzzi, A.; Nuvolone, M.; Zhu, C. The immunobiology of prion diseases. Nat. Rev. Immunol., 2013, 13(12), 888-902.
[http://dx.doi.org/10.1038/nri3553] [PMID: 24189576]
[113]
Soto, C.; Satani, N. The intricate mechanisms of neurodegeneration in prion diseases. Trends Mol. Med., 2011, 17(1), 14-24.
[http://dx.doi.org/10.1016/j.molmed.2010.09.001] [PMID: 20889378]
[114]
Aguzzi, A.; Heikenwalder, M. Pathogenesis of prion diseases: current status and future outlook. Nat. Rev. Microbiol., 2006, 4(10), 765-775.
[http://dx.doi.org/10.1038/nrmicro1492] [PMID: 16980938]
[115]
Wong, B.S.; Chen, S.G.; Colucci, M.; Xie, Z.; Pan, T.; Liu, T.; Li, R.; Gambetti, P.; Sy, M.S.; Brown, D.R. Aberrant metal binding by prion protein in human prion disease. J. Neurochem., 2001, 78(6), 1400-1408.
[http://dx.doi.org/10.1046/j.1471-4159.2001.00522.x] [PMID: 11579148]
[116]
Leach, S.P.; Salman, M.D.; Hamar, D. Trace elements and prion diseases: a review of the interactions of copper, manganese and zinc with the prion protein. Anim. Health Res. Rev., 2006, 7(1-2), 97-105.
[http://dx.doi.org/10.1017/S1466252307001181] [PMID: 17389057]
[117]
Meneghetti, E.; Gasperini, L.; Virgilio, T.; Moda, F.; Tagliavini, F.; Benetti, F.; Legname, G. Prions strongly reduce NMDA receptor s-nitrosylation levels at pre-symptomatic and terminal stages of Prion diseases. Mol. Neurobiol., 2019, 56(9), 6035-6045.
[http://dx.doi.org/10.1007/s12035-019-1505-6] [PMID: 30710214]
[118]
Emwas, A.H.M.; Al-Talla, Z.A.; Guo, X.; Al-Ghamdi, S.; Al-Masri, H.T. Utilizing NMR and EPR spectroscopy to probe the role of copper in prion diseases. Magn. Reson. Chem., 2013, 51(5), 255-268.
[http://dx.doi.org/10.1002/mrc.3936] [PMID: 23436479]
[119]
Varela-Nallar, L.; González, A.; Inestrosa, N. Role of copper in prion diseases: deleterious or beneficial? Curr. Pharm. Des., 2006, 12(20), 2587-2595.
[http://dx.doi.org/10.2174/138161206777698873] [PMID: 16842180]
[120]
Lehmann, S. Metal ions and prion diseases. Curr. Opin. Chem. Biol., 2002, 6(2), 187-192.
[http://dx.doi.org/10.1016/S1367-5931(02)00295-8] [PMID: 12039003]
[121]
Alsiary, R.A.; Alghrably, M.; Saoudi, A.; Al-Ghamdi, S.; Jaremko, L.; Jaremko, M.; Emwas, A.H. Using NMR spectroscopy to investigate the role played by copper in prion diseases. Neurol. Sci., 2020, 41(9), 2389-2406.
[http://dx.doi.org/10.1007/s10072-020-04321-9] [PMID: 32328835]
[122]
Bounias, M.; Purdey, M. Transmissible spongiform encephalopathies: a family of etiologically complex diseases—a review. Sci. Total Environ., 2002, 297(1-3), 1-19.
[http://dx.doi.org/10.1016/S0048-9697(02)00140-7] [PMID: 12389776]
[123]
Bar-Or, A.; Li, R. Cellular immunology of relapsing multiple sclerosis: interactions, checks, and balances. Lancet Neurol., 2021, 20(6), 470-483.
[http://dx.doi.org/10.1016/S1474-4422(21)00063-6] [PMID: 33930317]
[124]
Bierhansl, L.; Hartung, H.P.; Aktas, O.; Ruck, T.; Roden, M.; Meuth, S.G. Thinking outside the box: non-canonical targets in multiple sclerosis. Nat. Rev. Drug Discov., 2022, 21(8), 578-600.
[http://dx.doi.org/10.1038/s41573-022-00477-5] [PMID: 35668103]
[125]
Colombo, E.; Triolo, D.; Bassani, C.; Bedogni, F.; Di Dario, M.; Dina, G.; Fredrickx, E.; Fermo, I.; Martinelli, V.; Newcombe, J.; Taveggia, C.; Quattrini, A.; Comi, G.; Farina, C. Dysregulated copper transport in multiple sclerosis may cause demyelination via astrocytes. Proc. Natl. Acad. Sci. USA, 2021, 118(27), e2025804118.
[http://dx.doi.org/10.1073/pnas.2025804118] [PMID: 34183414]
[126]
Malosio, M.L.; Tecchio, F.; Squitti, R. Molecular mechanisms underlying copper function and toxicity in neurons and their possible therapeutic exploitation for Alzheimer’s disease. Aging Clin. Exp. Res., 2021, 33(7), 2027-2030.
[http://dx.doi.org/10.1007/s40520-019-01463-5] [PMID: 31965480]
[127]
Burk, K.; Pasterkamp, R.J. Disrupted neuronal trafficking in amyotrophic lateral sclerosis. Acta Neuropathol., 2019, 137(6), 859-877.
[http://dx.doi.org/10.1007/s00401-019-01964-7] [PMID: 30721407]
[128]
Fasae, K.D.; Abolaji, A.O.; Faloye, T.R.; Odunsi, A.Y.; Oyetayo, B.O.; Enya, J.I.; Rotimi, J.A.; Akinyemi, R.O.; Whitworth, A.J.; Aschner, M. Metallobiology and therapeutic chelation of biometals (copper, zinc and iron) in Alzheimer’s disease: Limitations, and current and future perspectives. J. Trace Elem. Med. Biol., 2021, 67, 126779.
[http://dx.doi.org/10.1016/j.jtemb.2021.126779] [PMID: 34034029]
[129]
Barnham, K.J.; Bush, A.I. Biological metals and metal-targeting compounds in major neurodegenerative diseases. Chem. Soc. Rev., 2014, 43(19), 6727-6749.
[http://dx.doi.org/10.1039/C4CS00138A] [PMID: 25099276]
[130]
Das, N.; Raymick, J.; Sarkar, S. Role of metals in Alzheimer’s disease. Metab. Brain Dis., 2021, 36(7), 1627-1639.
[http://dx.doi.org/10.1007/s11011-021-00765-w] [PMID: 34313926]
[131]
Davies, K.M.; Mercer, J.F.B.; Chen, N.; Double, K.L. Copper dyshomoeostasis in Parkinson’s disease: implications for pathogenesis and indications for novel therapeutics. Clin. Sci. (Lond.), 2016, 130(8), 565-574.
[http://dx.doi.org/10.1042/CS20150153] [PMID: 26957644]
[132]
Safety, tolerability, and efficacy of PBT2 in Huntington’s disease: a phase 2, randomised, double-blind, placebo-controlled trial. Lancet Neurol., 2015, 14(1), 39-47.
[http://dx.doi.org/10.1016/S1474-4422(14)70262-5] [PMID: 25467848]
[133]
Choi, B.Y.; Jang, B.G.; Kim, J.H.; Seo, J.N.; Wu, G.; Sohn, M.; Chung, T.N.; Suh, S.W. Copper/zinc chelation by clioquinol reduces spinal cord white matter damage and behavioral deficits in a murine MOG-induced multiple sclerosis model. Neurobiol. Dis., 2013, 54, 382-391.
[http://dx.doi.org/10.1016/j.nbd.2013.01.012] [PMID: 23360710]
[134]
Hung, Y.H.; Bush, A.I.; Cherny, R.A. Copper in the brain and Alzheimer’s disease. J. Biol. Inorg. Chem., 2010, 15(1), 61-76.
[http://dx.doi.org/10.1007/s00775-009-0600-y] [PMID: 19862561]
[135]
Squitti, R.; Rossini, P.M.; Cassetta, E.; Moffa, F.; Pasqualetti, P.; Cortesi, M.; Colloca, A.; Rossi, L.; Finazzi-Agró, A. d-penicillamine reduces serum oxidative stress in Alzheimer’s disease patients. Eur. J. Clin. Invest., 2002, 32(1), 51-59.
[http://dx.doi.org/10.1046/j.1365-2362.2002.00933.x] [PMID: 11851727]
[136]
Brewer, G.J.; Askari, F.K. Wilson's disease: Clinical management and therapy. J Hepatol., 2005, 42(Suppl(1)), S13-S21.
[http://dx.doi.org/10.1016/j.jhep.2004.11.013] [PMID: 15777568]
[137]
Nomura, S.; Nozaki, S.; Hamazaki, T.; Takeda, T.; Ninomiya, E.; Kudo, S.; Hayashinaka, E.; Wada, Y.; Hiroki, T.; Fujisawa, C.; Kodama, H.; Shintaku, H.; Watanabe, Y. PET imaging analysis with 64Cu in disulfiram treatment for aberrant copper biodistribution in Menkes disease mouse model. J. Nucl. Med., 2014, 55(5), 845-851.
[http://dx.doi.org/10.2967/jnumed.113.131797] [PMID: 24627433]
[138]
Zhao, J.; Shi, Q.; Tian, H.; Li, Y.; Liu, Y.; Xu, Z.; Robert, A.; Liu, Q.; Meunier, B. TDMQ20, a specific copper chelator, reduces memory impairments in Alzheimer’s disease mouse models. ACS Chem. Neurosci., 2021, 12(1), 140-149.
[http://dx.doi.org/10.1021/acschemneuro.0c00621] [PMID: 33322892]
[139]
Tümer, Z.; Møller, L.B. Menkes disease. Eur. J. Hum. Genet., 2010, 18(5), 511-518.
[http://dx.doi.org/10.1038/ejhg.2009.187] [PMID: 19888294]
[140]
Squitti, R.; Siotto, M.; Arciello, M.; Rossi, L. Non-ceruloplasmin bound copper and ATP7B gene variants in Alzheimer’s disease. Metallomics, 2016, 8(9), 863-873.
[http://dx.doi.org/10.1039/C6MT00101G] [PMID: 27499330]
[141]
Lalioti, V.; Tsubota, A.; Sandoval, I. Disorders in hepatic copper secretion: Wilson’s disease and pleomorphic syndromes. Semin. Liver Dis., 2017, 37(2), 175-188.
[http://dx.doi.org/10.1055/s-0037-1602764] [PMID: 28564725]
[142]
Mathys, Z.K.; White, A.R. Copper and Alzheimer’s disease. Adv. Neurobiol., 2017, 18, 199-216.
[http://dx.doi.org/10.1007/978-3-319-60189-2_10] [PMID: 28889269]
[143]
Ellett, L.J.; Hung, L.W.; Munckton, R.; Sherratt, N.A.; Culvenor, J.; Grubman, A.; Furness, J.B.; White, A.R.; Finkelstein, D.I.; Barnham, K.J.; Lawson, V.A. Restoration of intestinal function in an MPTP model of Parkinson’s Disease. Sci. Rep., 2016, 6(1), 30269.
[http://dx.doi.org/10.1038/srep30269] [PMID: 27471168]
[144]
Abbaoui, A.; Chatoui, H.; El Hiba, O.; Gamrani, H. Neuroprotective effect of curcumin-I in copper-induced dopaminergic neurotoxicity in rats: A possible link with Parkinson’s disease. Neurosci. Lett., 2017, 660, 103-108.
[http://dx.doi.org/10.1016/j.neulet.2017.09.032] [PMID: 28919537]
[145]
Roberts, B.R.; Lim, N.K.H.; McAllum, E.J.; Donnelly, P.S.; Hare, D.J.; Doble, P.A.; Turner, B.J.; Price, K.A.; Chun Lim, S.; Paterson, B.M.; Hickey, J.L.; Rhoads, T.W.; Williams, J.R.; Kanninen, K.M.; Hung, L.W.; Liddell, J.R.; Grubman, A.; Monty, J.F.; Llanos, R.M.; Kramer, D.R.; Mercer, J.F.B.; Bush, A.I.; Masters, C.L.; Duce, J.A.; Li, Q.X.; Beckman, J.S.; Barnham, K.J.; White, A.R.; Crouch, P.J. Oral treatment with Cu(II)(atsm) increases mutant SOD1 in vivo but protects motor neurons and improves the phenotype of a transgenic mouse model of amyotrophic lateral sclerosis. J. Neurosci., 2014, 34(23), 8021-8031.
[http://dx.doi.org/10.1523/JNEUROSCI.4196-13.2014] [PMID: 24899723]
[146]
Tokuda, E.; Furukawa, Y. Copper homeostasis as a therapeutic target in amyotrophic lateral sclerosis with sod1 mutations. Int. J. Mol. Sci., 2016, 17(5), 636.
[http://dx.doi.org/10.3390/ijms17050636] [PMID: 27136532]
[147]
Guthrie, L.M.; Soma, S.; Yuan, S.; Silva, A.; Zulkifli, M.; Snavely, T.C.; Greene, H.F.; Nunez, E.; Lynch, B.; De Ville, C.; Shanbhag, V.; Lopez, F.R.; Acharya, A.; Petris, M.J.; Kim, B.E.; Gohil, V.M.; Sacchettini, J.C. Elesclomol alleviates Menkes pathology and mortality by escorting Cu to cuproenzymes in mice. Science, 2020, 368(6491), 620-625.
[http://dx.doi.org/10.1126/science.aaz8899] [PMID: 32381719]
[148]
Kempuraj, D.; Thangavel, R.; Kempuraj, D.D.; Ahmed, M.E.; Selvakumar, G.P.; Raikwar, S.P.; Zaheer, S.A.; Iyer, S.S.; Govindarajan, R.; Chandrasekaran, P.N.; Zaheer, A. Neuroprotective effects of flavone luteolin in neuroinflammation and neurotrauma. Biofactors, 2021, 47(2), 190-197.
[http://dx.doi.org/10.1002/biof.1687] [PMID: 33098588]
[149]
Liu, Q.S.; Jiang, H.L.; Wang, Y.; Wang, L.L.; Zhang, J.X.; He, C.H.; Shao, S.; Zhang, T.T.; Xing, J.G.; Liu, R. Total flavonoid extract from Dracoephalum moldavica L. attenuates β-amyloid-induced toxicity through anti-amyloidogenesic and neurotrophic pathways. Life Sci., 2018, 193, 214-225.
[http://dx.doi.org/10.1016/j.lfs.2017.10.041] [PMID: 29100755]
[150]
Liu, R.; Meng, F.; Zhang, L.; Liu, A.; Qin, H.; Lan, X.; Li, L.; Du, G. Luteolin isolated from the medicinal plant Elsholtzia rugulosa (Labiatae) prevents copper-mediated toxicity in β-amyloid precursor protein Swedish mutation overexpressing SH-SY5Y cells. Molecules, 2011, 16(3), 2084-2096.
[http://dx.doi.org/10.3390/molecules16032084] [PMID: 21368720]
[151]
Xu, Y.; Yang, J.; Lu, Y.; Qian, L.L.; Yang, Z.Y.; Han, R.M.; Zhang, J.P.; Skibsted, L.H. Copper(II) coordination and translocation in luteolin and effect on radical scavenging. J. Phys. Chem. B, 2020, 124(2), 380-388.
[http://dx.doi.org/10.1021/acs.jpcb.9b10531] [PMID: 31845805]
[152]
Zhao, L.; Wang, J.L.; Liu, R.; Li, X.X.; Li, J.F.; Zhang, L. Neuroprotective, anti-amyloidogenic and neurotrophic effects of apigenin in an Alzheimer’s disease mouse model. Molecules, 2013, 18(8), 9949-9965.
[http://dx.doi.org/10.3390/molecules18089949] [PMID: 23966081]
[153]
Zhao, L.; Wang, J.; Wang, Y.; Fa, X. Apigenin attenuates copper-mediated β-amyloid neurotoxicity through antioxidation, mitochondrion protection and MAPK signal inactivation in an AD cell model. Brain Res., 2013, 1492, 33-45.
[http://dx.doi.org/10.1016/j.brainres.2012.11.019] [PMID: 23178511]
[154]
Peng, H.; Xing, Y.; Gao, L.; Zhang, L.; Zhang, G. Simultaneous separation of apigenin, luteolin and rosmarinic acid from the aerial parts of the copper-tolerant plant Elsholtzia splendens. Environ. Sci. Pollut. Res. Int., 2014, 21(13), 8124-8132.
[http://dx.doi.org/10.1007/s11356-014-2747-5] [PMID: 24671394]
[155]
Wang, Q.; Jiang, H.; Wang, L.; Yi, H.; Li, Z.; Liu, R. Vitegnoside mitigates neuronal injury, mitochondrial apoptosis, and inflammation in an Alzheimer’s disease cell model via the p38 MAPK/JNK Pathway. J. Alzheimers Dis., 2019, 72(1), 199-214.
[http://dx.doi.org/10.3233/JAD-190640] [PMID: 31561371]
[156]
Lin, M.C.; Liu, C.C.; Liao, C.S.; Ro, J.H. Neuroprotective effect of quercetin during cerebral ischemic injury involves regulation of essential elements, transition metals, cu/zn ratio, and antioxidant activity. Molecules, 2021, 26(20), 6128.
[http://dx.doi.org/10.3390/molecules26206128] [PMID: 34684707]
[157]
Yang, D.; Wang, T.; Long, M.; Li, P. Quercetin: its main pharmacological activity and potential application in clinical medicine. Oxid. Med. Cell. Longev., 2020, 2020, 1-13.
[http://dx.doi.org/10.1155/2020/8825387] [PMID: 33488935]
[158]
Du, G.; Zhao, Z.; Chen, Y.; Li, Z.; Tian, Y.; Liu, Z.; Liu, B.; Song, J. Quercetin protects rat cortical neurons against traumatic brain injury. Mol. Med. Rep., 2018, 17(6), 7859-7865.
[http://dx.doi.org/10.3892/mmr.2018.8801] [PMID: 29620218]
[159]
Jomova, K.; Lawson, M.; Drostinova, L.; Lauro, P.; Poprac, P.; Brezova, V.; Michalik, M.; Lukes, V.; Valko, M. Protective role of quercetin against copper(II)-induced oxidative stress: A spectroscopic, theoretical and DNA damage study. Food Chem. Toxicol., 2017, 110, 340-350.
[http://dx.doi.org/10.1016/j.fct.2017.10.042] [PMID: 29107026]
[160]
Chakraborty, J.; Pakrashi, S.; Sarbajna, A.; Dutta, M.; Bandyopadhyay, J. Quercetin attenuates copper-induced apoptotic cell death and endoplasmic reticulum stress in SH-SY5Y cells by autophagic modulation. Biol. Trace Elem. Res., 2022, 200(12), 5022-5041.
[http://dx.doi.org/10.1007/s12011-022-03093-x] [PMID: 35149956]
[161]
Zubčić K.; Radovanović V.; Vlainić J.; Hof, P.R.; Oršolić N.; Šimić G.; Jazvinšćak Jembrek, M. PI3K/Akt and ERK1/2 signalling are involved in quercetin-mediated neuroprotection against copper-induced injury. Oxid. Med. Cell. Longev., 2020, 2020, 1-14.
[http://dx.doi.org/10.1155/2020/9834742] [PMID: 32733640]
[162]
Kuo, S.M.; Huang, C.T.; Blum, P.; Chang, C. Quercetin cumulatively enhances copper induction of metallothionein in intestinal cells. Biol. Trace Elem. Res., 2001, 84(1-3), 001-010.
[http://dx.doi.org/10.1385/BTER:84:1-3:001] [PMID: 11817679]
[163]
Gan, R.Y.; Li, H.B.; Sui, Z.Q.; Corke, H. Absorption, metabolism, anti-cancer effect and molecular targets of epigallocatechin gallate (EGCG): An updated review. Crit. Rev. Food Sci. Nutr., 2018, 58(6), 924-941.
[http://dx.doi.org/10.1080/10408398.2016.1231168] [PMID: 27645804]
[164]
Steinmann, J.; Buer, J.; Pietschmann, T.; Steinmann, E. Anti-infective properties of epigallocatechin-3-gallate (EGCG), a component of green tea. Br. J. Pharmacol., 2013, 168(5), 1059-1073.
[http://dx.doi.org/10.1111/bph.12009] [PMID: 23072320]
[165]
Koh, S.H.; Lee, S.M.; Kim, H.Y.; Lee, K.Y.; Lee, Y.J.; Kim, H.T.; Kim, J.; Kim, M.H.; Hwang, M.S.; Song, C.; Yang, K.W.; Lee, K.W.; Kim, S.H.; Kim, O.H. The effect of epigallocatechin gallate on suppressing disease progression of ALS model mice. Neurosci. Lett., 2006, 395(2), 103-107.
[http://dx.doi.org/10.1016/j.neulet.2005.10.056] [PMID: 16356650]
[166]
Teng, Y.; Zhao, J.; Ding, L.; Ding, Y.; Zhou, P. Complex of EGCG with Cu(II) suppresses amyloid aggregation and Cu(II)-induced cytotoxicity of alpha-synuclein. Molecules, 2019, 24(16), 2940.
[http://dx.doi.org/10.3390/molecules24162940] [PMID: 31416122]
[167]
Li, J.; Xiang, H.; Huang, C.; Lu, J. Pharmacological actions of myricetin in the nervous system: a comprehensive review of preclinical studies in animals and cell models. Front. Pharmacol., 2021, 12, 797298.
[http://dx.doi.org/10.3389/fphar.2021.797298] [PMID: 34975495]
[168]
Zhang, X.H.; Ma, Z.G.; Rowlands, D.K.; Gou, Y.L.; Fok, K.L.; Wong, H.Y.; Yu, M.K.; Tsang, L.L.; Mu, L.; Chen, L.; Yung, W.H.; Chung, Y.W.; Zhang, B.L.; Zhao, H.; Chan, H.C. Flavonoid myricetin modulates GABA(A) receptor activity through activation of Ca(2+) channels and CaMK-II pathway. Evid. Based Complement. Alternat. Med., 2012, 2012, 1-10.
[http://dx.doi.org/10.1155/2012/758097] [PMID: 23258999]
[169]
Ding, P.; Liao, X.; Shi, B. Adsorption chromatography separation of the flavonols kaempferol, quercetin and myricetin using cross-linked collagen fibre as the stationary phase. J. Sci. Food Agric., 2013, 93(7), 1575-1583.
[http://dx.doi.org/10.1002/jsfa.5924] [PMID: 23152137]
[170]
DeToma, A.S.; Choi, J.S.; Braymer, J.J.; Lim, M.H. Myricetin: a naturally occurring regulator of metal-induced amyloid-β aggregation and neurotoxicity. ChemBioChem, 2011, 12(8), 1198-1201.
[http://dx.doi.org/10.1002/cbic.201000790] [PMID: 21538759]
[171]
Xiang, B.; Li, D.; Chen, Y.; Li, M.; Zhang, Y.; Sun, T.; Tang, S. Curcumin ameliorates copper-induced neurotoxicity through inhibiting oxidative stress and mitochondrial apoptosis in SH-SY5Y cells. Neurochem. Res., 2021, 46(2), 367-378.
[http://dx.doi.org/10.1007/s11064-020-03173-1] [PMID: 33201401]
[172]
Abolaji, A.O.; Fasae, K.D.; Iwezor, C.E.; Aschner, M.; Farombi, E.O. Curcumin attenuates copper-induced oxidative stress and neurotoxicity in Drosophila melanogaster. Toxicol. Rep., 2020, 7, 261-268.
[http://dx.doi.org/10.1016/j.toxrep.2020.01.015] [PMID: 32025502]
[173]
RA Mans, D. Djotaroeno, M.; Friperson, P.; Pawirodihardjo, J. Phytochemical and pharmacological support for the traditional uses of Zingiberacea species in suriname - a review of the literature. Pharmacogn. J., 2019, 11(6s), 1511-1525.
[http://dx.doi.org/10.5530/pj.2019.11.232]
[174]
Abbaoui, A.; Gamrani, H. Obvious anxiogenic-like effects of subchronic copper intoxication in rats, outcomes on spatial learning and memory and neuromodulatory potential of curcumin. J. Chem. Neuroanat., 2019, 96, 86-93.
[http://dx.doi.org/10.1016/j.jchemneu.2019.01.001] [PMID: 30611899]
[175]
Ho, W.I.; Hu, Y.; Cheng, C.W.; Wei, R.; Yang, J.; Li, N.; Au, K.W.; Tse, Y.L.; Wang, Q.; Ng, K.M.; Esteban, M.A.; Tse, H.F. Liposome-encapsulated curcumin attenuates HMGB1-mediated hepatic inflammation and fibrosis in a murine model of Wilson’s disease. Biomed. Pharmacother., 2022, 152, 113197.
[http://dx.doi.org/10.1016/j.biopha.2022.113197] [PMID: 35687913]
[176]
Motavaf, M.; Sadeghizadeh, M.; Babashah, S.; Zare, L.; Javan, M. Protective effects of a nano-formulation of curcumin against cuprizone-induced demyelination in the mouse corpus callosum. Iran. J. Pharm. Res., 2020, 19(3), 310-320.
[PMID: 33680032]
[177]
Huang, H.C.; Lin, C.J.; Liu, W.J.; Jiang, R.R.; Jiang, Z.F. Dual effects of curcumin on neuronal oxidative stress in the presence of Cu(II). Food Chem. Toxicol., 2011, 49(7), 1578-1583.
[http://dx.doi.org/10.1016/j.fct.2011.04.004] [PMID: 21501647]
[178]
Sarawi, W.S.; Alhusaini, A.M.; Fadda, L.M.; Alomar, H.A.; Albaker, A.B.; Aljrboa, A.S.; Alotaibi, A.M.; Hasan, I.H.; Mahmoud, A.M. Curcumin and Nano-curcumin mitigate copper neurotoxicity by modulating oxidative stress, inflammation, and Akt/GSK-3beta signaling. Molecules, 2021, 26(18), 5591.
[http://dx.doi.org/10.3390/molecules26185591] [PMID: 34577062]
[179]
Abbaoui, A.; Gamrani, H. Neuronal, astroglial and locomotor injuries in subchronic copper intoxicated rats are repaired by curcumin: A possible link with Parkinson’s disease. Acta Histochem., 2018, 120(6), 542-550.
[http://dx.doi.org/10.1016/j.acthis.2018.06.005] [PMID: 29954586]
[180]
Lin, R.; Chen, X.; Li, W.; Han, Y.; Liu, P.; Pi, R. Exposure to metal ions regulates mRNA levels of APP and BACE1 in PC12 cells: Blockage by curcumin. Neurosci. Lett., 2008, 440(3), 344-347.
[http://dx.doi.org/10.1016/j.neulet.2008.05.070] [PMID: 18583042]
[181]
Enogieru, A.B.; Haylett, W.; Hiss, D.C.; Bardien, S.; Ekpo, O.E. Rutin as a Potent antioxidant: implications for neurodegenerative disorders. Oxid. Med. Cell. Longev., 2018, 2018, 1-17.
[http://dx.doi.org/10.1155/2018/6241017] [PMID: 30050657]
[182]
Arowoogun, J.; Akanni, O.O.; Adefisan, A.O.; Owumi, S.E.; Tijani, A.S.; Adaramoye, O.A. Rutin ameliorates copper sulfate‐induced brain damage via antioxidative and anti‐inflammatory activities in rats. J. Biochem. Mol. Toxicol., 2021, 35(1), e22623.
[http://dx.doi.org/10.1002/jbt.22623] [PMID: 32881150]
[183]
Lin, M.C.; Liu, C.C.; Lin, Y.C.; Liao, C.S. Resveratrol protects against cerebral ischemic injury via restraining lipid peroxidation, transition elements, and toxic metal levels, but enhancing anti-oxidant activity. Antioxidants, 2021, 10(10), 1515.
[http://dx.doi.org/10.3390/antiox10101515] [PMID: 34679650]
[184]
Tian, C.; Zhang, R.; Ye, X.; Zhang, C.; Jin, X.; Yamori, Y.; Hao, L.; Sun, X.; Ying, C. Resveratrol ameliorates high-glucose-induced hyperpermeability mediated by caveolae via VEGF/KDR pathway. Genes Nutr., 2013, 8(2), 231-239.
[http://dx.doi.org/10.1007/s12263-012-0319-1] [PMID: 22983702]
[185]
Majewski, M.; Ognik, K.; Thoene, M.; Rawicka, A. Juśkiewicz, J. Resveratrol modulates the blood plasma levels of Cu and Zn, the antioxidant status and the vascular response of thoracic arteries in copper deficient Wistar rats. Toxicol. Appl. Pharmacol., 2020, 390, 114877.
[http://dx.doi.org/10.1016/j.taap.2020.114877] [PMID: 31917326]
[186]
Matos, L.; Gouveia, A.M.; Almeida, H. Resveratrol attenuates copper-induced senescence by improving cellular proteostasis. Oxid. Med. Cell. Longev., 2017, 2017, 3793817.
[PMID: 28280523]
[187]
Asadi, S.; Moradi, M.N.; Khyripour, N.; Goodarzi, M.T.; Mahmoodi, M. Resveratrol attenuates copper and zinc homeostasis and ameliorates oxidative stress in Type 2 diabetic rats. Biol. Trace Elem. Res., 2017, 177(1), 132-138.
[http://dx.doi.org/10.1007/s12011-016-0861-6] [PMID: 27744600]
[188]
Muselin, F.; Gârban, Z.; Cristina, R.T.; Doma, A.O.; Dumitrescu, E. Vițălaru, A.B.; Bănățean-Dunea, I. Homeostatic changes of some trace elements in geriatric rats in the condition of oxidative stress induced by aluminum and the beneficial role of resveratrol. J. Trace Elem. Med. Biol., 2019, 55, 136-142.
[http://dx.doi.org/10.1016/j.jtemb.2019.06.013] [PMID: 31345351]
[189]
Majewski, M.; Ognik, K. Juśkiewicz, J. The interaction between resveratrol and two forms of copper as carbonate and nanoparticles on antioxidant mechanisms and vascular function in Wistar rats. Pharmacol. Rep., 2019, 71(5), 862-869.
[http://dx.doi.org/10.1016/j.pharep.2019.03.011] [PMID: 31408785]
[190]
Khalid, S.; Afzal, N.; Khan, J.A.; Hussain, Z.; Qureshi, A.S.; Anwar, H.; Jamil, Y. Antioxidant resveratrol protects against copper oxide nanoparticle toxicity in vivo. Naunyn Schmiedebergs Arch. Pharmacol., 2018, 391(10), 1053-1062.
[http://dx.doi.org/10.1007/s00210-018-1526-0] [PMID: 29936585]
[191]
Summers, K.L.; Roseman, G.P.; Sopasis, G.J.; Millhauser, G.L.; Harris, H.H.; Pickering, I.J.; George, G.N. Copper(II) binding to pbt2 differs from that of other 8-hydroxyquinoline chelators: implications for the treatment of neurodegenerative protein misfolding diseases. Inorg. Chem., 2020, 59(23), 17519-17534.
[http://dx.doi.org/10.1021/acs.inorgchem.0c02754] [PMID: 33226796]
[192]
Dzieżyc, K.; Karliński, M.; Litwin, T.; Członkowska, A. Compliant treatment with anti-copper agents prevents clinically overt Wilson’s disease in pre-symptomatic patients. Eur. J. Neurol., 2014, 21(2), 332-337.
[http://dx.doi.org/10.1111/ene.12320] [PMID: 24313946]
[193]
Kaler, S.G.; Holmes, C.S.; Goldstein, D.S.; Tang, J.; Godwin, S.C.; Donsante, A.; Liew, C.J.; Sato, S.; Patronas, N. Neonatal diagnosis and treatment of Menkes disease. N. Engl. J. Med., 2008, 358(6), 605-614.
[http://dx.doi.org/10.1056/NEJMoa070613] [PMID: 18256395]
[194]
Tosato, M.; Di Marco, V. Metal chelation therapy and Parkinson’s disease: a critical review on the thermodynamics of complex formation between relevant metal ions and promising or established drugs. Biomolecules, 2019, 9(7), 269.
[http://dx.doi.org/10.3390/biom9070269] [PMID: 31324037]
[195]
Gou, D.H.; Huang, T.T.; Li, W.; Gao, X.D.; Haikal, C.; Wang, X.H.; Song, D.Y.; Liang, X.; Zhu, L.; Tang, Y.; Ding, C.; Li, J.Y. Inhibition of copper transporter 1 prevents α-synuclein pathology and alleviates nigrostriatal degeneration in AAV-based mouse model of Parkinson’s disease. Redox Biol., 2021, 38, 101795.
[http://dx.doi.org/10.1016/j.redox.2020.101795] [PMID: 33232911]
[196]
Chen, L.; Min, J.; Wang, F. Copper homeostasis and cuproptosis in health and disease. Signal Transduct. Target. Ther., 2022, 7(1), 378.
[http://dx.doi.org/10.1038/s41392-022-01229-y] [PMID: 36414625]
[197]
Arnal, N.; Morel, G.R.; de Alaniz, M.J.T.; Castillo, O.; Marra, C.A. Role of copper and cholesterol association in the neurodegenerative process. Int. J. Alzheimers Dis., 2013, 2013, 1-15.
[http://dx.doi.org/10.1155/2013/414817] [PMID: 24288650]
[198]
Murillo, O.; Collantes, M.; Gazquez, C.; Moreno, D.; Hernandez-Alcoceba, R.; Barberia, M.; Ecay, M.; Tamarit, B.; Douar, A.; Ferrer, V.; Combal, J.P.; Peñuelas, I.; Bénichou, B.; Gonzalez-Aseguinolaza, G. High value of 64Cu as a tool to evaluate the restoration of physiological copper excretion after gene therapy in Wilson’s disease. Mol. Ther. Methods Clin. Dev., 2022, 26, 98-106.
[http://dx.doi.org/10.1016/j.omtm.2022.06.001] [PMID: 35795774]
[199]
Cai, H.; Cheng, X.; Wang, X.P. ATP7B gene therapy of autologous reprogrammed hepatocytes alleviates copper accumulation in a mouse model of Wilson’s disease. Hepatology, 2022, 76(4), 1046-1057.
[http://dx.doi.org/10.1002/hep.32484] [PMID: 35340061]
[200]
Du, A.; Cai, R.; Shi, J.; Wu, Q. Protective effects of icariin on traumatic brain injury. Curr. Neurovasc. Res., 2021, 18(5), 508-514.
[http://dx.doi.org/10.2174/1567202619666211223125628] [PMID: 34951380]
[201]
Abbaoui, A.; Hiba, O.E.; Gamrani, H. Neuroprotective potential of Aloe arborescens against copper induced neurobehavioral features of Parkinson’s disease in rat. Acta Histochem., 2017, 119(5), 592-601.
[http://dx.doi.org/10.1016/j.acthis.2017.06.003] [PMID: 28619286]
[202]
Pan, C.; Liu, N.; Zhang, P.; Wu, Q.; Deng, H.; Xu, F.; Lian, L.; Liang, Q.; Hu, Y.; Zhu, S.; Tang, Z. EGb761 ameliorates neuronal apoptosis and promotes angiogenesis in experimental intracerebral hemorrhage via RSK1/GSK3beta pathway. Mol. Neurobiol., 2018, 55(2), 1556-1567.
[http://dx.doi.org/10.1007/s12035-016-0363-8] [PMID: 28185127]
[203]
Rojas, P.; Montes, S.; Serrano-García, N.; Rojas-Castañeda, J. Effect of EGb761 supplementation on the content of copper in mouse brain in an animal model of Parkinson’s disease. Nutrition, 2009, 25(4), 482-485.
[http://dx.doi.org/10.1016/j.nut.2008.10.013] [PMID: 19091511]
[204]
Cao, J.; Li, C.; Ma, P.; Ding, Y.; Gao, J.; Jia, Q.; Zhu, J.; Zhang, T. Effect of kaempferol on IgE-mediated anaphylaxis in C57BL/6 mice and LAD2 cells. Phytomedicine, 2020, 79, 153346.
[http://dx.doi.org/10.1016/j.phymed.2020.153346] [PMID: 33002828]
[205]
Simunkova, M.; Barbierikova, Z.; Jomova, K.; Hudecova, L.; Lauro, P.; Alwasel, S.H.; Alhazza, I.; Rhodes, C.J.; Valko, M. Antioxidant vs. Prooxidant properties of the flavonoid, kaempferol, in the presence of Cu(II) ions: a ros-scavenging activity, fenton reaction and dna damage study. Int. J. Mol. Sci., 2021, 22(4), 1619.
[http://dx.doi.org/10.3390/ijms22041619] [PMID: 33562744]
[206]
Fachel, F.N.S.; Schuh, R.S.; Veras, K.S.; Bassani, V.L.; Koester, L.S.; Henriques, A.T.; Braganhol, E.; Teixeira, H.F. An overview of the neuroprotective potential of rosmarinic acid and its association with nanotechnology-based delivery systems: A novel approach to treating neurodegenerative disorders. Neurochem. Int., 2019, 122, 47-58.
[http://dx.doi.org/10.1016/j.neuint.2018.11.003] [PMID: 30439384]
[207]
Kola, A.; Hecel, A.; Lamponi, S.; Valensin, D. Novel perspective on Alzheimer’s disease treatment: rosmarinic acid molecular interplay with Copper(II) and amyloid beta. Life (Basel), 2020, 10(7), 118.
[http://dx.doi.org/10.3390/life10070118] [PMID: 32698429]
[208]
Costa, I.M.; Lima, F.O.V.; Fernandes, L.C.B.; Norrara, B.; Neta, F.I.; Alves, R.D.; Cavalcanti, J.R.L.P.; Lucena, E.E.S.; Cavalcante, J.S.; Rego, A.C.M.; Filho, I.A.; Queiroz, D.B.; Freire, M.A.M.; Guzen, F.P. Astragaloside IV supplementation promotes a neuroprotective effect in experimental models of neurological disorders: a systematic review. Curr. Neuropharmacol., 2019, 17(7), 648-665.
[http://dx.doi.org/10.2174/1570159X16666180911123341] [PMID: 30207235]
[209]
Ma, M.; Qiu, B.; Jin, J.; Wang, J.; Nie, Y.; Liang, Y.; Yu, Z.; Teng, C.B. Establishment of a specific in vivo Cu(Ⅰ) reporting system based on metallothionein screening. Metallomics, 2021, 13(7), mfab035.
[http://dx.doi.org/10.1093/mtomcs/mfab035] [PMID: 34114637]
[210]
Memariani, Z.; Abbas, S.Q. ul Hassan, S.S.; Ahmadi, A.; Chabra, A. Naringin and naringenin as anticancer agents and adjuvants in cancer combination therapy: Efficacy and molecular mechanisms of action, a comprehensive narrative review. Pharmacol. Res., 2021, 171, 105264.
[http://dx.doi.org/10.1016/j.phrs.2020.105264] [PMID: 33166734]
[211]
Yuan, J.; Wei, F.; Luo, X.; Zhang, M.; Qiao, R.; Zhong, M.; Chen, H.; Yang, W. Multi-component comparative pharmacokinetics in rats after oral administration of Fructus aurantii extract, naringin, neohesperidin, and naringin-neohesperidin. Front. Pharmacol., 2020, 11, 933.
[http://dx.doi.org/10.3389/fphar.2020.00933] [PMID: 32636752]
[212]
Chen, K.Y.; Lin, K.C.; Chen, Y.S.; Yao, C.H. A novel porous gelatin composite containing naringin for bone repair. Evid. Based Complement. Alternat. Med., 2013, 2013, 1-10.
[http://dx.doi.org/10.1155/2013/283941] [PMID: 23431335]
[213]
Guo, L.X. Sun, B. N′-1,10-Bis(Naringin) Triethylenetetraamine, synthesis and as a Cu(II) chelator for Alzheimer’s disease therapy. Biol. Pharm. Bull., 2021, 44(1), 51-56.
[http://dx.doi.org/10.1248/bpb.b20-00574] [PMID: 33162492]
[214]
Saini, R.K.; Shuaib, S.; Goyal, D.; Goyal, B. Insights into the inhibitory mechanism of a resveratrol and clioquinol hybrid against Aβ42 aggregation and protofibril destabilization: A molecular dynamics simulation study. J. Biomol. Struct. Dyn., 2019, 37(12), 3183-3197.
[http://dx.doi.org/10.1080/07391102.2018.1511475] [PMID: 30582723]
[215]
Mao, F.; Yan, J.; Li, J.; Jia, X.; Miao, H.; Sun, Y.; Huang, L.; Li, X. New multi-target-directed small molecules against Alzheimer’s disease: a combination of resveratrol and clioquinol. Org. Biomol. Chem., 2014, 12(31), 5936-5944.
[http://dx.doi.org/10.1039/C4OB00998C] [PMID: 24986600]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy