Role of Oxidative Stress and Metal Toxicity in the Progression of Alzheimer’s Disease

Author(s): Hareram Birla, Tarun Minocha, Gaurav Kumar, Anamika Misra, Sandeep Kumar Singh*

Journal Name: Current Neuropharmacology

Volume 18 , Issue 7 , 2020

DOI : 10.2174/1570159X18666200122122512

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Graphical Abstract:


Abstract:

Alzheimer’s disease (AD) is one of the life-threatening neurodegenerative disorders in the elderly (>60 years) and incurable across the globe to date. AD is caused by the involvement of various genetic, environmental and lifestyle factors that affect neuronal cells to degenerate over the period of time. The oxidative stress is engaged in the pathogenesis of various disorders and its key role is also linked to the etiology of AD. AD is attributed by neuronal loss, abnormal accumulation of Amyloid-β (Aβ) and neurofibrillary tangles (NFTs) with severe memory impairments and other cognitive dysfunctions which lead to the loss of synapses and neuronal death and eventual demise of the individual. Increased production of reactive oxygen species (ROS), loss of mitochondrial function, altered metal homeostasis, aberrant accumulation of senile plaque and mitigated antioxidant defense mechanism all are indulged in the progression of AD. In spite of recent advances in biomedical research, the underlying mechanism of disruption of redox balance and the actual source of oxidative stress is still obscure. This review highlights the generation of ROS through different mechanisms, the role of some important metals in the progression of AD and free radical scavenging by endogenous molecule and supplementation of nutrients in AD.

Keywords: Alzheimer's disease (AD), oxidative stress, metal toxicity, mitochondrial dysfunction and neurodegeneration, Reactive Oxygen Species (ROS).

[1]
Hickman, R.A.; Faustin, A.; Wisniewski, T. Alzheimer disease and its growing epidemic: risk factors, biomarkers, and the urgent need for therapeutics. Neurol. Clin., 2016, 34(4), 941-953.
[http://dx.doi.org/10.1016/j.ncl.2016.06.009] [PMID: 27720002]
[2]
Martins, R.N.; Villemagne, V.; Sohrabi, H.R.; Chatterjee, P.; Shah, T.M.; Verdile, G.; Fraser, P.; Taddei, K.; Gupta, V.B.; Rainey-Smith, S.R.; Hone, E.; Pedrini, S.; Lim, W.L.; Martins, I.; Frost, S.; Gupta, S.; O’Bryant, S.; Rembach, A.; Ames, D.; Ellis, K.; Fuller, S.J.; Brown, B.; Gardener, S.L.; Fernando, B.; Bharadwaj, P.; Burnham, S.; Laws, S.M.; Barron, A.M.; Goozee, K.; Wahjoepramono, E.J.; Asih, P.R.; Doecke, J.D.; Salvado, O.; Bush, A.I.; Rowe, C.C.; Gandy, S.E.; Masters, C.L. Alzheimer’s Disease: a journey from amyloid peptides and oxidative stress, to biomarker technologies and disease prevention strategies-gains from aibl and dian cohort studies. J. Alzheimers Dis., 2018, 62(3), 965-992.
[http://dx.doi.org/10.3233/JAD-171145] [PMID: 29562546]
[3]
Chin-Chan, M.; Navarro-Yepes, J.; Quintanilla-Vega, B. Environmental pollutants as risk factors for neurodegenerative disorders: Alzheimer and Parkinson diseases. Front. Cell. Neurosci., 2015, 9, 124.
[http://dx.doi.org/10.3389/fncel.2015.00124] [PMID: 25914621]
[4]
Halliwell, B.; Gutteridge, J.M. Free radicals in biology and medicine; Oxford University Press: USA, 2015.
[http://dx.doi.org/10.1093/acprof:oso/9780198717478.001.0001]
[5]
Butterfield, D.A.; Boyd-Kimball, D. Oxidative stress, amyloid-β peptide, and altered key molecular pathways in the pathogenesis and progression of Alzheimer’s disease. J. Alzheimers Dis., 2018, 62(3), 1345-1367.
[http://dx.doi.org/10.3233/JAD-170543] [PMID: 29562527]
[6]
Halliwell, B. Oxidative stress and neurodegeneration: where are we now? J. Neurochem., 2006, 97(6), 1634-1658.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03907.x] [PMID: 16805774]
[7]
Di Domenico, F.; Pupo, G.; Giraldo, E.; Badìa, M-C.; Monllor, P.; Lloret, A.; Schininà, M.E.; Giorgi, A.; Cini, C.; Tramutola, A.; Butterfield, D.A.; Viña, J.; Perluigi, M. Oxidative signature of cerebrospinal fluid from mild cognitive impairment and Alzheimer disease patients. Free Radic. Biol. Med., 2016, 91, 1-9.
[http://dx.doi.org/10.1016/j.freeradbiomed.2015.12.004] [PMID: 26675344]
[8]
Di Domenico, F.; Tramutola, A.; Butterfield, D.A. Role of 4-hydroxy-2-nonenal (HNE) in the pathogenesis of alzheimer disease and other selected age-related neurodegenerative disorders. Free Radic. Biol. Med., 2017, 111, 253-261.
[http://dx.doi.org/10.1016/j.freeradbiomed.2016.10.490] [PMID: 27789292]
[9]
Lauderback, C.M.; Hackett, J.M.; Huang, F.F.; Keller, J.N.; Szweda, L.I.; Markesbery, W.R.; Butterfield, D.A. The glial glutamate transporter, GLT-1, is oxidatively modified by 4-hydroxy-2-nonenal in the Alzheimer’s disease brain: the role of Abeta1-42. J. Neurochem., 2001, 78(2), 413-416.
[http://dx.doi.org/10.1046/j.1471-4159.2001.00451.x] [PMID: 11461977]
[10]
Martins, R.N.; Harper, C.G.; Stokes, G.B.; Masters, C.L. Increased cerebral glucose-6-phosphate dehydrogenase activity in Alzheimer’s disease may reflect oxidative stress. J. Neurochem., 1986, 46(4), 1042-1045.
[http://dx.doi.org/10.1111/j.1471-4159.1986.tb00615.x] [PMID: 3950618]
[11]
Smith, M.A.; Richey Harris, P.L.; Sayre, L.M.; Beckman, J.S.; Perry, G. Widespread peroxynitrite-mediated damage in Alzheimer’s disease. J. Neurosci., 1997, 17(8), 2653-2657.
[http://dx.doi.org/10.1523/JNEUROSCI.17-08-02653.1997] [PMID: 9092586]
[12]
Hensley, K.; Hall, N.; Subramaniam, R.; Cole, P.; Harris, M.; Aksenov, M.; Aksenova, M.; Gabbita, S.P.; Wu, J.F.; Carney, J.M. Brain regional correspondence between Alzheimer’s disease histopathology and biomarkers of protein oxidation. J. Neurochem., 1995, 65(5), 2146-2156.
[http://dx.doi.org/10.1046/j.1471-4159.1995.65052146.x] [PMID: 7595501]
[13]
Poprac, P.; Jomova, K.; Simunkova, M.; Kollar, V.; Rhodes, C.J.; Valko, M. Targeting free radicals in oxidative stress-related human diseases. Trends Pharmacol. Sci., 2017, 38(7), 592-607.
[http://dx.doi.org/10.1016/j.tips.2017.04.005] [PMID: 28551354]
[14]
Chen, Z.; Zhong, C. Oxidative stress in Alzheimer’s disease. Neurosci. Bull., 2014, 30(2), 271-281.
[http://dx.doi.org/10.1007/s12264-013-1423-y] [PMID: 24664866]
[15]
Singh, S.K.; Castellani, R.; Perry, G. Oxidative stress and Alzheimer’s disease. Inflammation, Aging, and Oxidative Stress; Springer, 2016, pp. 189-198.
[http://dx.doi.org/10.1007/978-3-319-33486-8_10]
[16]
Gella, A.; Durany, N. Oxidative stress in Alzheimer disease. Cell Adhes. Migr., 2009, 3(1), 88-93.
[http://dx.doi.org/10.4161/cam.3.1.7402] [PMID: 19372765]
[17]
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]
[18]
Cicero, C.E.; Mostile, G.; Vasta, R.; Rapisarda, V.; Signorelli, S.S.; Ferrante, M.; Zappia, M.; Nicoletti, A. Metals and neurodegenerative diseases. A systematic review. Environ. Res., 2017, 159, 82-94.
[http://dx.doi.org/10.1016/j.envres.2017.07.048] [PMID: 28777965]
[19]
Walters, M.; Hackett, K.; Caesar, E.; Isaacson, R.; Mosconi, L. Role of nutrition to promote healthy brain aging and reduce risk of Alzheimer’s Disease. Curr. Nutr. Rep., 2017, 6(2), 63-71.
[http://dx.doi.org/10.1007/s13668-017-0199-5]
[20]
Kumar, A.; Singh, A.; Ekavali, A review on Alzheimer’s disease pathophysiology and its management: an update. Pharmacol. Rep., 2015, 67(2), 195-203.
[http://dx.doi.org/10.1016/j.pharep.2014.09.004] [PMID: 25712639]
[21]
Selkoe, D.J. The molecular pathology of Alzheimer’s disease. Neuron, 1991, 6(4), 487-498.
[http://dx.doi.org/10.1016/0896-6273(91)90052-2] [PMID: 1673054]
[22]
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]
[23]
Trojanowski, J.Q.; Mawal-Dewan, M.; Schmidt, M.L.; Martin, J.; Lee, V.M-Y. Localization of the mitogen activated protein kinase ERK2 in Alzheimer’s disease neurofibrillary tangles and senile plaque neurites. Brain Res., 1993, 618(2), 333-337.
[http://dx.doi.org/10.1016/0006-8993(93)91286-2] [PMID: 8374766]
[24]
Dickson, D.W.; Farlo, J.; Davies, P.; Crystal, H.; Fuld, P.; Yen, S-H. Alzheimer’s disease. A double-labeling immunohistochemical study of senile plaques. Am. J. Pathol., 1988, 132(1), 86-101.
[PMID: 2456021]
[25]
Pohanka, M. Oxidative stress in Alzheimer disease as a target for therapy. Bratisl. Lek Listy, 2018, 119(9), 535-543.
[http://dx.doi.org/10.4149/BLL_2018_097] [PMID: 30226062]
[26]
Burnham, S.C.; Bourgeat, P.; Doré, V.; Savage, G.; Brown, B.; Laws, S.; Maruff, P.; Salvado, O.; Ames, D.; Martins, R.N.; Masters, C.L.; Rowe, C.C.; Villemagne, V.L. AIBL Research Group Clinical and cognitive trajectories in cognitively healthy elderly individuals with suspected non-Alzheimer’s disease pathophysiology (SNAP) or Alzheimer’s disease pathology: a longitudinal study. Lancet Neurol., 2016, 15(10), 1044-1053.
[http://dx.doi.org/10.1016/S1474-4422(16)30125-9] [PMID: 27450471]
[27]
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]
[28]
Bélanger, M.; Allaman, I.; Magistretti, P.J. Brain energy metabolism: focus on astrocyte-neuron metabolic cooperation. Cell Metab., 2011, 14(6), 724-738.
[http://dx.doi.org/10.1016/j.cmet.2011.08.016] [PMID: 22152301]
[29]
Mecocci, P.; Boccardi, V.; Cecchetti, R.; Bastiani, P.; Scamosci, M.; Ruggiero, C.; Baroni, M. A long journey into aging, brain aging, and Alzheimer’s disease following the oxidative stress tracks. J. Alzheimers Dis., 2018, 62(3), 1319-1335.
[http://dx.doi.org/10.3233/JAD-170732] [PMID: 29562533]
[30]
Markesbery, W.R.; Carney, J.M. Oxidative alterations in Alzheimer’s disease. Brain Pathol., 1999, 9(1), 133-146.
[http://dx.doi.org/10.1111/j.1750-3639.1999.tb00215.x] [PMID: 9989456]
[31]
Islam, M.T. Oxidative stress and mitochondrial dysfunction-linked neurodegenerative disorders. Neurol. Res., 2017, 39(1), 73-82.
[http://dx.doi.org/10.1080/01616412.2016.1251711] [PMID: 27809706]
[32]
Ortiz, G.G.; Pacheco‐Moisés, F.P.; Torres‐Sánchez, E.D.; Sorto‐Gómez, T.E.; Mireles‐Ramírez, M.; León‐Gil, A.; González‐Usigli, H.; Flores‐Alvarado, L.J.; González‐Renovato, E.D.; Sánchez‐López, A.L. Multiple sclerosis and its relationship with oxidative stress, glutathione redox system, atpase system, and membrane fluidity. Trending Topics in Multiple Sclerosis; InTech, 2016.
[http://dx.doi.org/10.5772/64737]
[33]
Yang, W.S.; Kim, K.J.; Gaschler, M.M.; Patel, M.; Shchepinov, M.S.; Stockwell, B.R. Peroxidation of polyunsaturated fatty acids by lipoxygenases drives ferroptosis. Proc. Natl. Acad. Sci. USA, 2016, 113(34), E4966-E4975.
[http://dx.doi.org/10.1073/pnas.1603244113] [PMID: 27506793]
[34]
Shichiri, M. The role of lipid peroxidation in neurological disorders. J. Clin. Biochem. Nutr., 2014, 54(3), 151-160.
[http://dx.doi.org/10.3164/jcbn.14-10] [PMID: 24895477]
[35]
Ansari, M.A.; Scheff, S.W. Oxidative stress in the progression of Alzheimer disease in the frontal cortex. J. Neuropathol. Exp. Neurol., 2010, 69(2), 155-167.
[http://dx.doi.org/10.1097/NEN.0b013e3181cb5af4] [PMID: 20084018]
[36]
Miller, M.W.; Sadeh, N. Traumatic stress, oxidative stress and post-traumatic stress disorder: neurodegeneration and the accelerated-aging hypothesis. Mol. Psychiatry, 2014, 19(11), 1156-1162.
[http://dx.doi.org/10.1038/mp.2014.111] [PMID: 25245500]
[37]
Osafo, N.; Obiri, D.D.; Danquah, K.O.; Yeboah, O.K.; Antwi, A.O.; Oppong, M.B. Oxidative Stress and Neurodegeneration. Handbook of research on critical examinations of neurodegenerative disorders; IGI Global, 2019, pp. 24-47.
[http://dx.doi.org/10.4018/978-1-5225-5282-6.ch002]
[38]
Yaribeygi, H.; Panahi, Y.; Javadi, B.; Sahebkar, A. The underlying role of oxidative stress in neurodegeneration: a mechanistic review. CNS & Neurological Disorders-Drug Targets (Formerly Current Drug Targets-CNS & Neurological Disorders),, 2018, 17(3), 207-215.
[39]
Sas, K.; Szabó, E.; Vécsei, L. Mitochondria, oxidative stress and the kynurenine system, with a focus on ageing and neuroprotection. Molecules, 2018, 23(1), 191.
[http://dx.doi.org/10.3390/molecules23010191] [PMID: 29342113]
[40]
Eleutherio, E.; Brasil, A.A.; França, M.B.; de Almeida, D.S.G.; Rona, G.B.; Magalhães, R.S.S. Oxidative stress and aging: Learning from yeast lessons. Fungal Biol., 2018, 122(6), 514-525.
[http://dx.doi.org/10.1016/j.funbio.2017.12.003] [PMID: 29801796]
[41]
Perry, G.; Cash, A.D.; Smith, M.A. Alzheimer disease and oxidative stress. J. Biomed. Biotechnol., 2002, 2(3), 120-123.
[http://dx.doi.org/10.1155/S1110724302203010] [PMID: 12488575]
[42]
Chandra, K.; Salman, A.S.; Mohd, A.; Sweety, R.; Ali, K.N. Protection against FCA induced oxidative stress induced DNA damage as a model of arthritis and In vitro anti-arthritic potential of costus speciosus rhizome extract. Inter J Pharma Phyto Res, 2015, 7(2), 383-389.
[43]
Jadoon, S.; Malik, A. A Comprehensive review article on isoprostanes as biological markers. Biochem Pharmacol (Los Angel),, 2018, 7(246), 2167-0510.1000246
[http://dx.doi.org/10.4172/2167-0501.1000246]
[44]
Ortiz, G.G.; Moisés, F.P.P.; Mireles-Ramírez, M.; Flores-Alvarado, L.J.; González-Usigli, H.; Sanchez-Gonzalez, V.J.; Sanchez-Lopez, A.L.; Sánchez-Romero, L.; Díaz-Barba, E.I.; Santoscoy-Gutiérrez, J.F. Oxidative stress: Love and hate history in central nervous system. Advances in protein chemistry and structural biology; Elsevier, 2017, Vol. 108, pp. 1-31.
[45]
Perrotte, M.; Le Page, A.; Fournet, M.; Le Sayec, M.; Rassart, É.; Fulop, T.; Ramassamy, C. Blood-based redox-signature and their association to the cognitive scores in MCI and Alzheimer’s disease patients. Free Radic. Biol. Med., 2019, 130, 499-511.
[PMID: 30445127]
[46]
Singh, S. Oxidative stress and neurodegeneration. J. Cytol. Histol., 2017, 8(4)
[47]
Santos, R.X.; Correia, S.C.; Zhu, X.; Smith, M.A.; Moreira, P.I.; Castellani, R.J.; Nunomura, A.; Perry, G. Mitochondrial DNA oxidative damage and repair in aging and Alzheimer’s disease. Antioxid. Redox Signal., 2013, 18(18), 2444-2457.
[http://dx.doi.org/10.1089/ars.2012.5039] [PMID: 23216311]
[48]
Dalle-Donne, I.; Giustarini, D.; Colombo, R.; Rossi, R.; Milzani, A. Protein carbonylation in human diseases. Trends Mol. Med., 2003, 9(4), 169-176.
[http://dx.doi.org/10.1016/S1471-4914(03)00031-5] [PMID: 12727143]
[49]
Stadtman, E.R. Protein oxidation in aging and age-related diseases. Ann. N. Y. Acad. Sci., 2001, 928(1), 22-38.
[http://dx.doi.org/10.1111/j.1749-6632.2001.tb05632.x] [PMID: 11795513]
[50]
Butterfield, D.A.; Halliwell, B. Oxidative stress, dysfunctional glucose metabolism and Alzheimer disease. Nat. Rev. Neurosci., 2019, 20(3), 148-160.
[http://dx.doi.org/10.1038/s41583-019-0132-6] [PMID: 30737462]
[51]
Lin, M.T.; Beal, M.F. Glucose metabolism and Alzheimer’s disease. Ageing Res. Rev., 2006, 4(2), 240-257.
[52]
Schubert, D. Glucose metabolism and Alzheimer’s disease. Ageing Res. Rev., 2005, 4(2), 240-257.
[http://dx.doi.org/10.1016/j.arr.2005.02.003] [PMID: 15950548]
[53]
Mattson, M.P. Pathways towards and away from Alzheimer’s disease. Nature, 2004, 430(7000), 631-639.
[http://dx.doi.org/10.1038/nature02621] [PMID: 15295589]
[54]
Caspersen, C.; Wang, N.; Yao, J.; Sosunov, A.; Chen, X.; Lustbader, J.W.; Xu, H.W.; Stern, D.; McKhann, G.; Yan, S.D. Mitochondrial Abeta: a potential focal point for neuronal metabolic dysfunction in Alzheimer’s disease. FASEB J., 2005, 19(14), 2040-2041.
[http://dx.doi.org/10.1096/fj.05-3735fje] [PMID: 16210396]
[55]
Saqlain, M.; Parveen, A. Development of Antioxidant based therapeutics in unani system of medicine. Research and Reviews: A J. Unani. Siddha and Homeopathy, 2018, 5(3), 1-4.
[56]
Youssef, P.; Chami, B.; Lim, J.; Middleton, T.; Sutherland, G.T.; Witting, P.K. Evidence supporting oxidative stress in a moderately affected area of the brain in Alzheimer’s disease. Sci. Rep., 2018, 8(1), 11553.
[http://dx.doi.org/10.1038/s41598-018-29770-3] [PMID: 30068908]
[57]
Ramesh, S.; Govindarajulu, M.; Jones, E.; Suppiramaniam, V.; Moore, T.; Dhanasekaran, M. Mitochondrial dysfunction and the role of Mitophagy in Alzheimer’s Disease., 2018.
[58]
Duran-Aniotz, C.; Hetz, C. Glucose metabolism: a sweet relief of alzheimer’s disease. Curr. Biol., 2016, 26(17), R806-R809.
[http://dx.doi.org/10.1016/j.cub.2016.07.060] [PMID: 27623263]
[59]
Mutisya, E.M.; Bowling, A.C.; Beal, M.F. Cortical cytochrome oxidase activity is reduced in Alzheimer’s disease. J. Neurochem., 1994, 63(6), 2179-2184.
[http://dx.doi.org/10.1046/j.1471-4159.1994.63062179.x] [PMID: 7964738]
[60]
Wang, X.; Wang, W.; Li, L.; Perry, G.; Lee, H.G.; Zhu, X. Oxidative stress and mitochondrial dysfunction in Alzheimer’s disease. Biochim. Biophys. Acta, 2014, 1842(8), 1240-1247.
[http://dx.doi.org/10.1016/j.bbadis.2013.10.015] [PMID: 24189435]
[61]
La Penna, G.; Hureau, C.; Andreussi, O.; Faller, P. Identifying, by first-principles simulations, Cu[amyloid-β] species making Fenton-type reactions in Alzheimer’s disease. J. Phys. Chem. B, 2013, 117(51), 16455-16467.
[http://dx.doi.org/10.1021/jp410046w] [PMID: 24313818]
[62]
Zawia, N.H.; Lahiri, D.K.; Cardozo-Pelaez, F. Epigenetics, oxidative stress, and Alzheimer disease. Free Radic. Biol. Med., 2009, 46(9), 1241-1249.
[http://dx.doi.org/10.1016/j.freeradbiomed.2009.02.006] [PMID: 19245828]
[63]
Geng, L.; Wang, Z.; Cui, C.; Zhu, Y.; Shi, J.; Wang, J.; Chen, M. Rapid electrical stimulation increased cardiac apoptosis through disturbance of calcium homeostasis and mitochondrial dysfunction in human induced pluripotent stem cell-derived cardiomyocytes. Cell. Physiol. Biochem., 2018, 47(3), 1167-1180.
[http://dx.doi.org/10.1159/000490213] [PMID: 29913448]
[64]
Rygiel, K.A.; Picard, M.; Turnbull, D.M. The ageing neuromuscular system and sarcopenia: a mitochondrial perspective. J. Physiol., 2016, 594(16), 4499-4512.
[http://dx.doi.org/10.1113/JP271212] [PMID: 26921061]
[65]
Verkhratsky, A. Astroglial Calcium Signaling in Aging and Alzheimer’s Disease. Cold Spring Harb. Perspect. Biol., 2019, 11(7)a035188
[http://dx.doi.org/10.1101/cshperspect.a035188] [PMID: 31110130]
[66]
Vultur, A.; Gibhardt, C.S.; Stanisz, H.; Bogeski, I. The role of the mitochondrial calcium uniporter (MCU) complex in cancer. Pflugers Arch., 2018, 470(8), 1149-1163.
[http://dx.doi.org/10.1007/s00424-018-2162-8] [PMID: 29926229]
[67]
Anila, V.; Mahalaxmi, I.; Venkatesh, B.; Balachandar, V. Mitochondrial Calcium Uniporter as a potential therapeutic strategy for Alzheimer’s disease (AD). Acta Neuropsychiatr., 2019, 1-19.
[68]
Hussien, H.M.; Abd-Elmegied, A.; Ghareeb, D.A.; Hafez, H.S.; Ahmed, H.E.A.; El-Moneam, N.A. Neuroprotective effect of berberine against environmental heavy metals-induced neurotoxicity and Alzheimer’s-like disease in rats. Food Chem. Toxicol., 2018, 111, 432-444.
[http://dx.doi.org/10.1016/j.fct.2017.11.025] [PMID: 29170048]
[69]
Barai, P.; Raval, N.; Acharya, S.; Borisa, A.; Bhatt, H.; Acharya, N. Neuroprotective effects of bergenin in Alzheimer’s disease: Investigation through molecular docking, in vitro and in vivo studies. Behav. Brain Res., 2019, 356, 18-40.
[http://dx.doi.org/10.1016/j.bbr.2018.08.010] [PMID: 30118774]
[70]
Godoy, J.A.; Lindsay, C.B.; Quintanilla, R.A.; Carvajal, F.J.; Cerpa, W.; Inestrosa, N.C. Quercetin exerts differential neuroprotective effects against H 2 O 2 and Aβ aggregates in hippocampal neurons: the role of mitochondria. Mol. Neurobiol., 2017, 54(9), 7116-7128.
[http://dx.doi.org/10.1007/s12035-016-0203-x] [PMID: 27796749]
[71]
Zhang, X.; Wang, X.; Hu, X.; Chu, X.; Li, X.; Han, F. Neuroprotective effects of a Rhodiola crenulata extract on amyloid-β peptides (Aβ1-42) -induced cognitive deficits in rat models of Alzheimer’s disease. Phytomedicine, 2019, 57, 331-338.
[http://dx.doi.org/10.1016/j.phymed.2018.12.042] [PMID: 30807987]
[72]
Sureda, A.; Capó, X.; Tejada, S. Neuroprotective effects of flavonoid compounds on neuronal death associated to alzheimer’s disease. Curr. Med. Chem., 2019, 26(27), 5124-5136.
[http://dx.doi.org/10.2174/0929867325666171226103237] [PMID: 29278202]
[73]
Balez, R.; Steiner, N.; Engel, M.; Muñoz, S.S.; Lum, J.S.; Wu, Y.; Wang, D.; Vallotton, P.; Sachdev, P.; O’Connor, M.; Sidhu, K.; Münch, G.; Ooi, L. Neuroprotective effects of apigenin against inflammation, neuronal excitability and apoptosis in an induced pluripotent stem cell model of Alzheimer’s disease. Sci. Rep., 2016, 6, 31450.
[http://dx.doi.org/10.1038/srep31450] [PMID: 27514990]
[74]
Talarico, G.; Trebbastoni, A.; Bruno, G.; de Lena, C. Modulation of the cannabinoid system: a new perspective for the treatment of the alzheimer’s disease. Curr. Neuropharmacol., 2019, 17(2), 176-183.
[http://dx.doi.org/10.2174/1570159X16666180702144644] [PMID: 29962346]
[75]
Hatziagapiou, K.; Kakouri, E.; Lambrou, G.I.; Bethanis, K.; Tarantilis, P.A. Antioxidant properties of Crocus sativus L. and its constituents and relevance to neurodegenerative diseases; focus on Alzheimer’s and Parkinson’s disease. Curr. Neuropharmacol., 2019, 17(4), 377-402.
[http://dx.doi.org/10.2174/1570159X16666180321095705] [PMID: 29564976]
[76]
Aliev, G.; Ashraf, G.M.; Tarasov, V.V.; Chubarev, V.N.; Leszek, J.; Gasiorowski, K.; Makhmutovа, A.; Baeesa, S.S.; Avila-Rodriguez, M.; Ustyugov, A.A.; Bachurin, S.O. Alzheimer’s disease - future therapy based on dendrimers. Curr. Neuropharmacol., 2019, 17(3), 288-294.
[http://dx.doi.org/10.2174/1570159X16666180918164623] [PMID: 30227819]
[77]
Sadegh Malvajerd, S.; Izadi, Z.; Azadi, A.; Kurd, M.; Derakhshankhah, H.; Sharifzadeh, M.; Akbari Javar, H.; Hamidi, M. Neuroprotective potential of curcumin-loaded nanostructured lipid carrier in an animal model of alzheimer’s disease: behavioral and biochemical evidence. J. Alzheimers Dis., 2019, 69(3), 671-686.
[http://dx.doi.org/10.3233/JAD-190083] [PMID: 31156160]
[78]
Alvarez, C.C.; Bai, P.; Houtkooper, R.; Auwerx, J.; Mouchiroud, L. Methods of treating mitochondrial dysfunction; In Google Patents, 2017.
[79]
Onyango, I.G.; Dennis, J.; Khan, S.M. Mitochondrial dysfunction in Alzheimer’s disease and the rationale for bioenergetics based therapies. Aging Dis., 2016, 7(2), 201-214.
[http://dx.doi.org/10.14336/AD.2015.1007] [PMID: 27114851]
[80]
Safdar, A.; Little, J.P.; Stokl, A.J.; Hettinga, B.P.; Akhtar, M.; Tarnopolsky, M.A. Exercise increases mitochondrial PGC-1 α content and promotes nuclear-mitochondrial cross-talk to coordinate mitochondrial biogenesis. J. Biol. Chem., 2018, 293(13), 4953.
[http://dx.doi.org/10.1074/jbc.EC118.002682] [PMID: 29602880]
[81]
Jornayvaz, F.R.; Shulman, G.I.; Jornayvaz, F.R.; Shulman, G.I. Regulation of mitochondrial biogenesis. Essays Biochem., 2010, 47, 69-84.
[http://dx.doi.org/10.1042/bse0470069] [PMID: 20533901]
[82]
Shang, J.; Yamashita, T.; Tian, F.; Li, X.; Liu, X.; Shi, X.; Nakano, Y.; Tsunoda, K.; Nomura, E.; Sasaki, R.; Tadokoro, K.; Sato, K.; Takemoto, M.; Hishikawa, N.; Ohta, Y.; Abe, K. Chronic cerebral hypoperfusion alters amyloid-β transport related proteins in the cortical blood vessels of Alzheimer’s disease model mouse. Brain Res., 2019, 1723146379
[http://dx.doi.org/10.1016/j.brainres.2019.146379] [PMID: 31415766]
[83]
Zhu, X.; Smith, M.A.; Honda, K.; Aliev, G.; Moreira, P.I.; Nunomura, A.; Casadesus, G.; Harris, P.L.; Siedlak, S.L.; Perry, G. Vascular oxidative stress in Alzheimer disease. J. Neurol. Sci., 2007, 257(1-2), 240-246.
[http://dx.doi.org/10.1016/j.jns.2007.01.039] [PMID: 17337008]
[84]
Shi, X.; Ohta, Y.; Liu, X.; Shang, J.; Morihara, R.; Nakano, Y.; Feng, T.; Huang, Y.; Sato, K.; Takemoto, M.; Hishikawa, N.; Yamashita, T.; Abe, K. Chronic cerebral hypoperfusion activates the coagulation and complement cascades in Alzheimer’s disease mice. Neuroscience, 2019, 416, 126-136.
[http://dx.doi.org/10.1016/j.neuroscience.2019.07.050] [PMID: 31394196]
[85]
Takahashi, M.; Oda, Y.; Sato, K.; Shirayama, Y. Vascular risk factors and the relationships between cognitive impairment and hypoperfusion in late-onset Alzheimer’s disease. Acta Neuropsychiatr., 2018, 30(6), 350-358.
[http://dx.doi.org/10.1017/neu.2018.17] [PMID: 30132427]
[86]
Gorelick, P.B.; Counts, S.E.; Nyenhuis, D. Vascular cognitive impairment and dementia. Biochimica et Biophysica Acta, 2016, 1862(5), 860-868.
[http://dx.doi.org/10.1016/j.bbadis.2015.12.015]
[87]
Govaerts, K.; Lechat, B.; Struys, T.; Kremer, A.; Borghgraef, P.; Van Leuven, F.; Himmelreich, U.; Dresselaers, T. Longitudinal assessment of cerebral perfusion and vascular response to hypoventilation in a bigenic mouse model of Alzheimer’s disease with amyloid and tau pathology. NMR Biomed., 2019, 32(2)e4037
[http://dx.doi.org/10.1002/nbm.4037] [PMID: 30489666]
[88]
de la Torre, J.C. Critical threshold cerebral hypoperfusion causes Alzheimer’s disease? Acta Neuropathol., 1999, 98(1), 1-8.
[http://dx.doi.org/10.1007/s004010051044] [PMID: 10412794]
[89]
Gao, Z.; Cilento, E.M.; Stewart, T.; Zhang, J. Vascular dysfunction and neurodegenerative disease. Vessel Based Imaging Techniques; Springer, 2020, pp. 3-16.
[http://dx.doi.org/10.1007/978-3-030-25249-6_1]
[90]
Duncombe, J.; Kitamura, A.; Hase, Y.; Ihara, M.; Kalaria, R.N.; Horsburgh, K. Chronic cerebral hypoperfusion: a key mechanism leading to vascular cognitive impairment and dementia. Closing the translational gap between rodent models and human vascular cognitive impairment and dementia. Clin. Sci. (Lond.), 2017, 131(19), 2451-2468.
[http://dx.doi.org/10.1042/CS20160727] [PMID: 28963120]
[91]
Iqbal, S.; Hayman, E.G.; Hong, C.; Stokum, J.A.; Kurland, D.B.; Gerzanich, V.; Simard, J.M. Inducible nitric oxide synthase (NOS-2) in subarachnoid hemorrhage: Regulatory mechanisms and therapeutic implications. Brain Circ., 2016, 2(1), 8-19.
[http://dx.doi.org/10.4103/2394-8108.178541] [PMID: 27774520]
[92]
Wang, B.; Han, S. Inhibition of inducible nitric oxide synthase attenuates deficits in synaptic plasticity and brain functions following traumatic brain injury. Cerebellum, 2018, 17(4), 477-484.
[http://dx.doi.org/10.1007/s12311-018-0934-5] [PMID: 29556966]
[93]
Miners, J.S.; Schulz, I.; Love, S. Differing associations between Aβ accumulation, hypoperfusion, blood-brain barrier dysfunction and loss of PDGFRB pericyte marker in the precuneus and parietal white matter in Alzheimer’s disease. J. Cereb. Blood Flow Metab., 2018, 38(1), 103-115.
[http://dx.doi.org/10.1177/0271678X17690761] [PMID: 28151041]
[94]
Herrera, M.I.; Udovin, L.D.; Toro-Urrego, N.; Kusnier, C.F.; Luaces, J.P.; Otero-Losada, M.; Capani, F. Neuroprotection targeting protein misfolding on chronic cerebral hypoperfusion in the context of metabolic syndrome. Front. Neurosci., 2018, 12, 339.
[http://dx.doi.org/10.3389/fnins.2018.00339] [PMID: 29904335]
[95]
Yegambaram, M.; Manivannan, B.; Beach, T.G.; Halden, R.U. Role of environmental contaminants in the etiology of Alzheimer’s disease: a review. Curr. Alzheimer Res., 2015, 12(2), 116-146.
[http://dx.doi.org/10.2174/1567205012666150204121719] [PMID: 25654508]
[96]
Hock, C.; Drasch, G.; Golombowski, S.; Müller-Spahn, F.; Willershausen-Zönnchen, B.; Schwarz, P.; Hock, U.; Growdon, J.H.; Nitsch, R.M. Increased blood mercury levels in patients with Alzheimer’s disease. J. Neural Transm. (Vienna), 1998, 105(1), 59-68.
[http://dx.doi.org/10.1007/s007020050038] [PMID: 9588761]
[97]
Thompson, C.M.; Markesbery, W.R.; Ehmann, W.D.; Mao, Y.X.; Vance, D.E. Regional brain trace-element studies in Alzheimer’s disease. Neurotoxicology, 1988, 9(1), 1-7.
[PMID: 3393299]
[98]
Chakraborty, P. Mercury exposure and Alzheimer’s disease in India - An imminent threat? Sci. Total Environ., 2017, 589, 232-235.
[http://dx.doi.org/10.1016/j.scitotenv.2017.02.168] [PMID: 28262357]
[99]
Zahir, F.; Rizwi, S.J.; Haq, S.K.; Khan, R.H. Low dose mercury toxicity and human health. Environ. Toxicol. Pharmacol., 2005, 20(2), 351-360.
[http://dx.doi.org/10.1016/j.etap.2005.03.007] [PMID: 21783611]
[100]
Mutter, J.; Curth, A.; Naumann, J.; Deth, R.; Walach, H. Does inorganic mercury play a role in Alzheimer’s disease? A systematic review and an integrated molecular mechanism. J. Alzheimers Dis., 2010, 22(2), 357-374.
[http://dx.doi.org/10.3233/JAD-2010-100705] [PMID: 20847438]
[101]
Lee, H.J.; Park, M.K.; Seo, Y.R. Pathogenic mechanisms of heavy metal induced-Alzheimer’s disease. Toxicol. Environ.l Health Sci., 2018, 10(1), 1-10.
[http://dx.doi.org/10.1007/s13530-018-0340-x]
[102]
Mutter, J.; Naumann, J.; Sadaghiani, C.; Schneider, R.; Walach, H. Alzheimer disease: mercury as pathogenetic factor and apolipoprotein E as a moderator. Neuroendocrinol. Lett., 2004, 25(5), 331-339.
[PMID: 15580166]
[103]
Gochfeld, M. Cases of mercury exposure, bioavailability, and absorption. Ecotoxicol. Environ. Saf., 2003, 56(1), 174-179.
[http://dx.doi.org/10.1016/S0147-6513(03)00060-5] [PMID: 12915150]
[104]
Li, W.; Wang, W-X. In vivo oral bioavailability of fish mercury and comparison with in vitro bioaccessibility. Sci. Total Environ., 2019, 683, 648-658.
[http://dx.doi.org/10.1016/j.scitotenv.2019.05.290] [PMID: 31150885]
[105]
Min, J.Y.; Min, K.B. Blood cadmium levels and Alzheimer’s disease mortality risk in older US adults. Environ. Health, 2016, 15(1), 69.
[http://dx.doi.org/10.1186/s12940-016-0155-7] [PMID: 27301955]
[106]
Peng, Q.; Bakulski, K.M.; Nan, B.; Park, S.K. Cadmium and Alzheimer’s disease mortality in U.S. adults: Updated evidence with a urinary biomarker and extended follow-up time. Environ. Res., 2017, 157, 44-51.
[http://dx.doi.org/10.1016/j.envres.2017.05.011] [PMID: 28511080]
[107]
Panayi, A.E.; Spyrou, N.M.; Iversen, B.S.; White, M.A.; Part, P. Determination of cadmium and zinc in Alzheimer’s brain tissue using inductively coupled plasma mass spectrometry. J. Neurol. Sci., 2002, 195(1), 1-10.
[http://dx.doi.org/10.1016/S0022-510X(01)00672-4] [PMID: 11867068]
[108]
Hane, F.T.; Hayes, R.; Lee, B.Y.; Leonenko, Z. Effect of copper and zinc on the single molecule self-affinity of alzheimer’s amyloid-β peptides. PLoS One, 2016, 11(1), e0147488-e0147488.
[http://dx.doi.org/10.1371/journal.pone.0147488] [PMID: 26808970]
[109]
Hart, R.P.; Rose, C.S.; Hamer, R.M. Neuropsychological effects of occupational exposure to cadmium. J. Clin. Exp. Neuropsychol., 1989, 11(6), 933-943.
[http://dx.doi.org/10.1080/01688638908400946] [PMID: 2592532]
[110]
Li, X.; Lv, Y.; Yu, S.; Zhao, H.; Yao, L. The effect of cadmium on Aβ levels in APP/PS1 transgenic mice. Exp. Ther. Med., 2012, 4(1), 125-130.
[http://dx.doi.org/10.3892/etm.2012.562] [PMID: 23060935]
[111]
Endres, K.; Fahrenholz, F. The Role of the anti-amyloidogenic secretase ADAM10 in shedding the APP-like proteins. Curr. Alzheimer Res., 2012, 9(2), 157-164.
[http://dx.doi.org/10.2174/156720512799361664] [PMID: 21605036]
[112]
Del Pino, J.; Zeballos, G.; Anadón, M.J.; Moyano, P.; Díaz, M.J.; García, J.M.; Frejo, M.T. Cadmium-induced cell death of basal forebrain cholinergic neurons mediated by muscarinic M1 receptor blockade, increase in GSK-3β enzyme, β-amyloid and tau protein levels. Arch. Toxicol., 2016, 90(5), 1081-1092.
[http://dx.doi.org/10.1007/s00204-015-1540-7] [PMID: 26026611]
[113]
Jiang, L-F.; Yao, T-M.; Zhu, Z-L.; Wang, C.; Ji, L-N. Impacts of Cd(II) on the conformation and self-aggregation of Alzheimer’s tau fragment corresponding to the third repeat of microtubule-binding domain. Biochim. Biophys. Acta, 2007, 1774(11), 1414-1421.
[http://dx.doi.org/10.1016/j.bbapap.2007.08.014] [PMID: 17920001]
[114]
Mao, P.; Reddy, P.H. Aging and amyloid beta-induced oxidative DNA damage and mitochondrial dysfunction in Alzheimer’s disease: implications for early intervention and therapeutics. Biochim. Biophys. Acta, 2011, 1812(11), 1359-1370.
[http://dx.doi.org/10.1016/j.bbadis.2011.08.005] [PMID: 21871956]
[115]
Chen, C.; Qu, L.; Li, B.; Xing, L.; Jia, G.; Wang, T.; Gao, Y.; Zhang, P.; Li, M.; Chen, W.; Chai, Z. Increased oxidative DNA damage, as assessed by urinary 8-hydroxy-2′-deoxyguanosine concentrations, and serum redox status in persons exposed to mercury. Clin. Chem., 2005, 51(4), 759-767.
[http://dx.doi.org/10.1373/clinchem.2004.042093] [PMID: 15695327]
[116]
Katsila, T.; Patrinos, G.P.; Kardamakis, D. Searching for clinically relevant biomarkers in geriatric oncology. BioMed Res. Int., 2018, 2018, 3793154-3793154.
[http://dx.doi.org/10.1155/2018/3793154] [PMID: 29670897]
[117]
Hamilton, M.L.; Guo, Z.; Fuller, C.D.; Van Remmen, H.; Ward, W.F.; Austad, S.N.; Troyer, D.A.; Thompson, I.; Richardson, A. A reliable assessment of 8-oxo-2-deoxyguanosine levels in nuclear and mitochondrial DNA using the sodium iodide method to isolate DNA. Nucleic Acids Res., 2001, 29(10), 2117-2126.
[http://dx.doi.org/10.1093/nar/29.10.2117] [PMID: 11353081]
[118]
Sedelnikova, O.A.; Horikawa, I.; Zimonjic, D.B.; Popescu, N.C.; Bonner, W.M.; Barrett, J.C. Senescing human cells and ageing mice accumulate DNA lesions with unrepairable double-strand breaks. Nat. Cell Biol., 2004, 6(2), 168-170.
[http://dx.doi.org/10.1038/ncb1095] [PMID: 14755273]
[119]
von Figura, G.; Hartmann, D.; Song, Z.; Rudolph, K.L. Role of telomere dysfunction in aging and its detection by biomarkers. J. Mol. Med. (Berl.), 2009, 87(12), 1165-1171.
[http://dx.doi.org/10.1007/s00109-009-0509-5] [PMID: 19669107]
[120]
Bolin, C.M.; Basha, R.; Cox, D.; Zawia, N.H.; Maloney, B.; Lahiri, D.K.; Cardozo-Pelaez, F. Exposure to lead and the developmental origin of oxidative DNA damage in the aging brain. FASEB J., 2006, 20(6), 788-790.
[http://dx.doi.org/10.1096/fj.05-5091fje] [PMID: 16484331]
[121]
Basha, M.R.; Wei, W.; Bakheet, S.A.; Benitez, N.; Siddiqi, H.K.; Ge, Y.W.; Lahiri, D.K.; Zawia, N.H. The fetal basis of amyloidogenesis: exposure to lead and latent overexpression of amyloid precursor protein and beta-amyloid in the aging brain. J. Neurosci., 2005, 25(4), 823-829.
[http://dx.doi.org/10.1523/JNEUROSCI.4335-04.2005] [PMID: 15673661]
[122]
Meleleo, D.; Notarachille, G.; Mangini, V.; Arnesano, F. Concentration-dependent effects of mercury and lead on Aβ42: possible implications for Alzheimer’s disease. Eur. Biophys. J., 2019, 48(2), 173-187.
[http://dx.doi.org/10.1007/s00249-018-1344-9] [PMID: 30603762]
[123]
Bihaqi, S.W.; Zawia, N.H. Enhanced taupathy and AD-like pathology in aged primate brains decades after infantile exposure to lead (Pb). Neurotoxicology, 2013, 39, 95-101.
[http://dx.doi.org/10.1016/j.neuro.2013.07.010] [PMID: 23973560]
[124]
Koki, I.B.; Bayero, A.S.; Umar, A.; Yusuf, S. Health risk assessment of heavy metals in water, air, soil and fish. African J. Pure Applied Chem., 2015, 9(11), 204-210.
[125]
Feng, C.; Liu, S.; Zhou, F.; Gao, Y.; Li, Y.; Du, G.; Chen, Y.; Jiao, H.; Feng, J.; Zhang, Y.; Bo, D.; Li, Z.; Fan, G. Oxidative stress in the neurodegenerative brain following lifetime exposure to lead in rats: Changes in lifespan profiles. Toxicology, 2019, 411, 101-109.
[http://dx.doi.org/10.1016/j.tox.2018.11.003] [PMID: 30445054]
[126]
Basha, R.; Reddy, G.R. Developmental exposure to lead and late life abnormalities of nervous system. Indian J. Exp. Biol., 2010, 48(7), 636-641.
[127]
Du, M.; Wang, D. The neurotoxic effects of heavy metal exposure on GABAergic nervous system in nematode Caenorhabditis elegans. Environ. Toxicol. Pharmacol., 2009, 27(3), 314-320.
[http://dx.doi.org/10.1016/j.etap.2008.11.011] [PMID: 21783959]
[128]
Farooqui, Z.; Bakulski, K.M.; Power, M.C.; Weisskopf, M.G.; Sparrow, D.; Spiro, A., III; Vokonas, P.S.; Nie, L.H.; Hu, H.; Park, S.K. Associations of cumulative Pb exposure and longitudinal changes in Mini-Mental Status Exam scores, global cognition and domains of cognition: The VA Normative Aging Study. Environ. Res., 2017, 152, 102-108.
[http://dx.doi.org/110.1016/J.ENVRES.2016.10.007 PMID: 27770710]
[129]
Mocchegiani, E.; Bertoni-Freddari, C.; Marcellini, F.; Malavolta, M. Brain, aging and neurodegeneration: role of zinc ion availability. Prog. Neurobiol., 2005, 75(6), 367-390.
[http://dx.doi.org/10.1016/j.pneurobio.2005.04.005] [PMID: 15927345]
[130]
Maret, W. The Glutathione Redox State and Zinc Mobilization from metallothionein and other proteins with zinc–sulfur coordination sites. glutathione in the nervous system; routledge, 2018 pp, , 257-274.
[131]
Tian, Y.; Lu, W.; Deng, H.; Yang, F.; Guo, Y.; Gao, L.; Xu, Y. Phlorizin administration ameliorates cognitive deficits by reducing oxidative stress, tau hyper‐phosphorylation, and neuroinflammation in a rat model of Alzheimer’s disease. J. Food Biochem., 2018, e12644
[http://dx.doi.org/10.1111/jfbc.12644]
[132]
Christen, Y. Oxidative stress and Alzheimer disease Disciplinary Approaches to Aging: Biology of aging, 2002, 71-255.
[133]
Huat, T.J.; Camats-Perna, J.; Newcombe, E.A.; Valmas, N.; Kitazawa, M.; Medeiros, R. Metal toxicity links to Alzheimer’s disease and neuroinflammation. J. Mol. Biol., 2019, 431(9), 1843-1868.
[http://dx.doi.org/10.1016/j.jmb.2019.01.018] [PMID: 30664867]
[134]
Morris, D.R.; Levenson, C.W. Neurotoxicity of zinc. Neurotoxicity of Metals; Springer, 2017, pp. 303-312.
[http://dx.doi.org/10.1007/978-3-319-60189-2_15]
[135]
Kennard, M.L.; Feldman, H.; Yamada, T.; Jefferies, W.A. Serum levels of the iron binding protein p97 are elevated in Alzheimer’s disease. Nat. Med., 1996, 2(11), 1230-1235.
[http://dx.doi.org/10.1038/nm1196-1230] [PMID: 8898750]
[136]
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]
[137]
Gaier, E.D.; Eipper, B.A.; Mains, R.E. Copper signaling in the mammalian nervous system: synaptic effects. J. Neurosci. Res., 2013, 91(1), 2-19.
[PMID: 23115049]
[138]
Gao, Z.; Xu, H.; Huang, K. Effects of rutin supplementation on antioxidant status and iron, copper, and zinc contents in mouse liver and brain. Biol. Trace Elem. Res., 2002, 88(3), 271-279.
[http://dx.doi.org/10.1385/BTER:88:3:271] [PMID: 12350136]
[139]
Shaw, B.J.; Al-Bairuty, G.; Handy, R.D. Effects of waterborne copper nanoparticles and copper sulphate on rainbow trout, (Oncorhynchus mykiss): physiology and accumulation. Aquat. Toxicol., 2012, 116-117, 90-101.
[http://dx.doi.org/10.1016/j.aquatox.2012.02.032] [PMID: 22480992]
[140]
Huang, X.; Moir, R.D.; Tanzi, R.E.; Bush, A.I.; Rogers, J.T. Redox-active metals, oxidative stress, and Alzheimer’s disease pathology. Ann. N. Y. Acad. Sci., 2004, 1012(1), 153-163.
[http://dx.doi.org/10.1196/annals.1306.012] [PMID: 15105262]
[141]
Praticò, D. Oxidative stress hypothesis in Alzheimer’s disease: a reappraisal. Trends Pharmacol. Sci., 2008, 29(12), 609-615.
[http://dx.doi.org/10.1016/j.tips.2008.09.001] [PMID: 18838179]
[142]
Sadowska-Bartosz, I.; Bartosz, G. Redox nanoparticles: synthesis, properties and perspectives of use for treatment of neurodegenerative diseases. J. Nanobiotechnology, 2018, 16(1), 87.
[http://dx.doi.org/10.1186/s12951-018-0412-8] [PMID: 30390681]
[143]
Behl, C.; Moosmann, B. Antioxidant neuroprotection in Alzheimer’s disease as preventive and therapeutic approach. Free Radic. Biol. Med., 2002, 33(2), 182-191.
[http://dx.doi.org/10.1016/S0891-5849(02)00883-3] [PMID: 12106814]


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VOLUME: 18
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Year: 2020
Published on: 28 July, 2020
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DOI: 10.2174/1570159X18666200122122512
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