Neurotoxicity of Aluminum pp 173-191 | Cite as
Cross Talk Between Aluminum and Genetic Susceptibility and Epigenetic Modification in Alzheimer’s Disease
Abstract
This chapter primarily focuses on two key aspects related to aluminum neurotoxicity and its mechanism in Alzheimer’s disease (AD), which are genetic susceptibility and epigenetic modification. The toxicity of aluminum has been confirmed from plant experiments, animal experiments, in vitro experiments, and epidemiological studies. However, the mechanisms underlying this phenomenon have largely remained elusive. Furthermore, there are more and more genetic factors that have been found to be strongly implicated for causing or increasing the risk of AD development and have been proved to be associated with the neurotoxicity of Al and play a significant role in the initiation and progression of AD. Epigenetics provide a bridge between genes and environment to improve our understanding on the etiology of AD. Al can modify the epigenetic status by DNA methylation, histone modifications, and noncoding RNAs and might thereby contribute to the pathophysiology of AD. However, very little is known about exact epigenetic patterns in AD.
Keywords
Aluminum Alzheimer’s disease Genetic susceptibility Epigenetic modificationReferences
- 1.Akinola OB, Biliaminu SA, Adediran RA, Adeniye KA, Abdulquadir FC (2015) Characterization of prefrontal cortex microstructure and antioxidant status in a rat model of neurodegeneration induced by aluminium chloride and multiple low-dose streptozotocin. Metab Brain Dis 30:1531PubMedCrossRefGoogle Scholar
- 2.Anderson KW, Chen J, Wang M, Mast N, Pikuleva IA, Turko IV (2015) Quantification of histone deacetylase isoforms in human frontal cortex, human retina, and mouse brain. PLoS One 10:e0126592PubMedPubMedCentralCrossRefGoogle Scholar
- 3.Aubry S, Shin W, Crary JF, Lefort R, Qureshi YH, Lefebvre C, Califano A, Shelanski ML (2015) Assembly and interrogation of Alzheimer’s disease genetic networks reveal novel regulators of progression. PLoS One 10:e0120352PubMedPubMedCentralCrossRefGoogle Scholar
- 4.Bagyinszky E, Youn YC, An SSA, Kim SY (1994) The genetics of Alzheimer’s disease. Clin Interv Aging 3:217–240Google Scholar
- 5.Bednarek PT, Orłowska R, Niedziela A (2017) A relative quantitative Methylation-Sensitive Amplified Polymorphism (MSAP) method for the analysis of abiotic stress. BMC Plant Biol 17:79PubMedPubMedCentralCrossRefGoogle Scholar
- 6.Bharathi S, Sathyanarayana NM, Rao TS, Dhanunjaya NM, Ravid R, Rao KS (2006) A new insight on Al-maltolate-treated aged rabbit as Alzheimer’s animal model. Brain Res Rev 52:275–292PubMedCrossRefPubMedCentralGoogle Scholar
- 7.Bird A (1992) The essentials of DNA methylation. Cell 70:5–8PubMedCrossRefPubMedCentralGoogle Scholar
- 8.Bird A (2002) DNA methylation patterns and epigenetic memory. Genes Dev 16:6–21CrossRefPubMedGoogle Scholar
- 9.Bollati V, Galimberti D, Pergoli L, Valle ED, Barretta F, Cortini F, Scarpini E, Bertazzi PA, Baccarelli A (2011) DNA methylation in repetitive elements and Alzheimer disease. Brain Behav Immun 25:1078–1083PubMedPubMedCentralCrossRefGoogle Scholar
- 10.Bondy SC (2014) Prolonged exposure to low levels of aluminum leads to changes associated with brain aging and neurodegeneration. Toxicology 315:1–7PubMedCrossRefPubMedCentralGoogle Scholar
- 11.Bondy SC (2016) Low levels of aluminum can lead to behavioral and morphological changes associated with Alzheimer’s disease and age-related neurodegeneration. Neurotoxicology 52:222–229PubMedCrossRefPubMedCentralGoogle Scholar
- 12.Bowman GD, Poirier MG (2016) Post-translational modifications of histones that influence nucleosome dynamics. Chem Rev 115:2274–2295CrossRefGoogle Scholar
- 13.Burklew CE, Ashlock J, Winfrey WB, Zhang B (2012) Effects of aluminum oxide nanoparticles on the growth, development, and microRNA expression of tobacco (Nicotiana tabacum). PLoS One 7:e34783PubMedPubMedCentralCrossRefGoogle Scholar
- 14.Cacabelos R, Torrellas C (2015) Epigenetics of aging and Alzheimer’s disease: implications for pharmacogenomics and drug response. Int J Mol Sci 16:30483–30543PubMedPubMedCentralCrossRefGoogle Scholar
- 15.Cai Z, Zhao B, Ratka A (2011) Oxidative stress and β-amyloid protein in Alzheimer’s disease. Neuromol Med 13:223–250CrossRefGoogle Scholar
- 16.Cannon JR, Greenamyre JT (2011) The role of environmental exposures in neurodegeneration and neurodegenerative diseases. Toxicol Sci 124:225PubMedPubMedCentralCrossRefGoogle Scholar
- 17.Castorina A, Tiralongo A, Giunta S, Carnazza ML, Scapagnini G, D’Agata V (2010) Early effects of aluminum chloride on beta-secretase mRNA expression in a neuronal model of ß-amyloid toxicity. Cell Biol Toxicol 26:367–377PubMedCrossRefPubMedCentralGoogle Scholar
- 18.Chen SM, Fan CC, Chiue MS, Chi C, Chen JH, Hseu RS (2013) Hemodynamic and neuropathological analysis in rats with aluminum trichloride-induced Alzheimer’s disease. PLoS One 8:e82561PubMedPubMedCentralCrossRefGoogle Scholar
- 19.Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, Strome R, Zuker N, Loukides J, French J (2001) Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 276:21562–21570PubMedCrossRefPubMedCentralGoogle Scholar
- 20.Colomina MT, Peris-Sampedro F (2017) Aluminum and Alzheimer’s disease. Adv Neurobiol 18:183PubMedCrossRefPubMedCentralGoogle Scholar
- 21.Crapper DR, Krishnan SS, Dalton AJ (1973) Brain aluminum distribution in Alzheimer’s disease and experimental neurofibrillary degeneration. Science 180:511–513PubMedCrossRefPubMedCentralGoogle Scholar
- 22.Di PC, Reverte I, Colomina MT, Domingo JL, Gomez M (2014) Chronic exposure to aluminum and melatonin through the diet: neurobehavioral effects in a transgenic mouse model of Alzheimer disease. Food Chem Toxicol 69:320–329CrossRefGoogle Scholar
- 23.Drago D, Cavaliere A, Mascetra N, Ciavardelli D, DI IC, Zatta P, Sensi SL (2008b) Aluminum modulates effects of beta amyloid (1-42) on neuronal calcium homeostasis and mitochondria functioning and is altered in a triple transgenic mouse model of Alzheimer’s disease. Rejuvenation Res 11:861–871PubMedCrossRefPubMedCentralGoogle Scholar
- 24.Elinder CG, Ahrengart L, Lidums V, Pettersson E, Sj Gren B (1991) Evidence of aluminium accumulation in aluminium welders. Br J Ind Med 48:735–738PubMedPubMedCentralGoogle Scholar
- 25.Erazi H, Sansar W, Ahboucha S, Gamrani H (2010) Aluminum affects glial system and behavior of rats. C R Biol 333:23PubMedCrossRefPubMedCentralGoogle Scholar
- 26.Ertekin-Taner N (2007) Genetics of Alzheimer’s disease: a centennial review. Neurol Clin 25:611–667PubMedPubMedCentralCrossRefGoogle Scholar
- 27.Exley C (2003) A biogeochemical cycle for aluminium? J Inorg Biochem 97:1–7PubMedCrossRefPubMedCentralGoogle Scholar
- 28.Exley C (2013) Human exposure to aluminium. Environ Sci Process Impacts 15:1807–1816PubMedCrossRefGoogle Scholar
- 29.Exley C (2014a) What is the risk of aluminium as a neurotoxin? Expert Rev Neurother 14:589–591PubMedCrossRefGoogle Scholar
- 30.Exley C (2014b) Why industry propaganda and political interference cannot disguise the inevitable role played by human exposure to aluminum in neurodegenerative diseases, including Alzheimer’s disease. Front Neurol 5:212PubMedPubMedCentralCrossRefGoogle Scholar
- 31.Ezaki B, Higashi A, Nanba N, Nishiuchi T (2016) An S-adenosyl Methionine Synthetase (SAMS) gene from Andropogon virginicus L. confers aluminum stress tolerance and facilitates epigenetic gene regulation in Arabidopsis thaliana. Front Plant Sci 7:1627PubMedPubMedCentralCrossRefGoogle Scholar
- 32.Ferreira PC, Piai KA, Takayanagui AM, Seguramu OZ SI (2008) Aluminum as a risk factor for Alzheimer’s disease. Rev Lat Am Enfermagem 16:151PubMedCrossRefGoogle Scholar
- 33.Flaten TP (2001) Aluminium as a risk factor in Alzheimer’s disease, with emphasis on drinking water. Brain Res Bull 55:187–196PubMedCrossRefGoogle Scholar
- 34.Frisardi V, Solfrizzi V, Capurso C, Kehoe PG, Imbimbo BP, Santamato A, Dellegrazie F, Seripa D, Pilotto A, Capurso A (2010) Aluminum in the diet and Alzheimer’s disease: from current epidemiology to possible disease-modifying treatment. J Alzheimers Dis Jad 20:17–30PubMedCrossRefGoogle Scholar
- 35.Fulgenzi A, Vietti D, Ferrero ME (2014) Aluminium involvement in neurotoxicity. Biomed Res Int 2014:758323PubMedPubMedCentralGoogle Scholar
- 36.Fuso A, Seminara L, Cavallaro RA, D’Anselmi F, Scarpa S (2005) S-adenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Mol Cell Neurosci 28:195–204PubMedCrossRefGoogle Scholar
- 37.Gatz M, Reynolds CA, Fratiglioni L, Johansson B, Mortimer JA, Berg S, Fiske A, Pedersen NL (2006) Role of genes and environments for explaining Alzheimer disease. Arch Gen Psychiatry 63:168–174PubMedCrossRefGoogle Scholar
- 38.Goldberg AD, Allis CD, Bernstein E (2007) Epigenetics: a landscape takes shape. Cell 128:635CrossRefPubMedGoogle Scholar
- 39.Graff J, Kim D, Dobbin MM, Tsai LH (2011) Epigenetic regulation of gene expression in physiological and pathological brain processes. Physiol Rev 91:603PubMedCrossRefGoogle Scholar
- 40.Graff J, Rei D, Guan JS, Wang WY, Seo J, Hennig KM, Nieland TJ, Fass DM, Kao PF, Kahn M (2012) An epigenetic blockade of cognitive functions in the neurodegenerating brain. Nature 483:222PubMedPubMedCentralCrossRefGoogle Scholar
- 41.Grimm MO, Mett J, Hartmann T (2016) The impact of vitamin E and other fat-soluble vitamins on Alzheimer’s disease. Int J Mol Sci 17:1785PubMedCentralCrossRefPubMedGoogle Scholar
- 42.Haggarty P (2015) Genetic and metabolic determinants of human epigenetic variation. Curr Opin Clin Nutr Metab Care 18:334PubMedCrossRefGoogle Scholar
- 43.Hantson P, Mahieu P, Gersdorff M, Sindic C, Lauwerys R (1995) Fatal encephalopathy after otoneurosurgery procedure with an aluminum-containing biomaterial. Clin Toxicol 33:645–648Google Scholar
- 44.Hara N, Kikuchi M, Miyashita A, Hatsuta H, Saito Y, Kasuga K, Murayama S, Ikeuchi T, Kuwano R (2017) Serum microRNA miR-501-3p as a potential biomarker related to the progression of Alzheimer’s disease. Acta Neuropathol Commun 5:10PubMedPubMedCentralCrossRefGoogle Scholar
- 45.Hardy JA, Higgins GA (1992) Alzheimer’s disease: the amyloid cascade hypothesis. Science 256:184PubMedCrossRefGoogle Scholar
- 46.Hinterberger M, Fischer P (2013) Folate and Alzheimer: when time matters. J Neural Transm 120:211–224PubMedCrossRefPubMedCentralGoogle Scholar
- 47.Jakovcevski M, Akbarian S (2012) Epigenetic mechanisms in neurological disease. Nat Med 18:1194–1204PubMedPubMedCentralCrossRefGoogle Scholar
- 48.Javed H, Khan MM, Khan A, Vaibhav K, Ahmad A, Khuwaja G, Ahmed ME, Raza SS, Ashafaq M, Tabassum R (2011) S-allyl cysteine attenuates oxidative stress associated cognitive impairment and neurodegeneration in mouse model of streptozotocin-induced experimental dementia of Alzheimer’s type. Brain Res 1389:133PubMedCrossRefPubMedCentralGoogle Scholar
- 49.Jonesrhoades MW, Bartel DP, Bartel B (2006) MicroRNAs and their regulatory roles in plants. Annu Rev Plant Biol 57:19CrossRefGoogle Scholar
- 50.Kumar V, Gill KD (2014) Oxidative stress and mitochondrial dysfunction in aluminium neurotoxicity and its amelioration: a review. Neurotoxicology 41:154PubMedCrossRefPubMedCentralGoogle Scholar
- 51.Kwon MJ, Kim S, Han MH, Lee SB (2016) Epigenetic changes in neurodegenerative diseases. Mol Cell 39:783–789CrossRefGoogle Scholar
- 52.Lahiri DK, Maloney B (2010) The “LEARn” (latent early–life associated regulation) model integrates environmental risk factors and the developmental basis of Alzheimer’s disease, and proposes remedial steps. Exp Gerontol 45:291–296PubMedPubMedCentralCrossRefGoogle Scholar
- 53.Lahiri DK, Maloney B, Basha MR, Ge YW, Zawia NH (2007) How and when environmental agents and dietary factors affect the course of Alzheimer’s disease: the “LEARn” model (latent early-life associated regulation) may explain the triggering of AD. Curr Alzheimer Res 4:219–228PubMedCrossRefPubMedCentralGoogle Scholar
- 54.Lardenoije R, Hove DLAVD, Havermans M, Casteren AV, Le KX, Palmour R, Lemere CA, Rutten BPF (2018) Age-related epigenetic changes in hippocampal subregions of four animal models of Alzheimer’s disease. Mol Cell Neurosci 86:1–15PubMedCrossRefPubMedCentralGoogle Scholar
- 55.Liaquat L, Ahmad S, Sadir S, Batool Z, Khaliq S, Tabassum S, Emad S, Madiha S, Shahzad S, Haider S (2017) Development of AD like symptoms following co-administration of AlCl3 and D-gal in rats: a neurochemical, biochemical and behavioural study. Pak J Pharm Sci 30:647–653PubMedPubMedCentralGoogle Scholar
- 56.Liddell MB, Lovestone S, Owen MJ (2001) Genetic risk of Alzheimer’s disease: advising relatives. Br J Psychiatry J Ment Sci 178:7CrossRefGoogle Scholar
- 57.Lima JC, Arenhart RA, Margis-Pinheiro M, Margis R (2011) Aluminum triggers broad changes in microRNA expression in rice roots. Genet Mol Res 10:2817PubMedCrossRefPubMedCentralGoogle Scholar
- 58.Lin WT, Chen RC, Lu WW, Liu SH, Yang FY (2015) Protective effects of low-intensity pulsed ultrasound on aluminum-induced cerebral damage in Alzheimer’s disease rat model. Sci Rep 5:9671PubMedPubMedCentralCrossRefGoogle Scholar
- 59.Lu X, Deng Y, Yu D, Cao H, Wang L, Li L, Yu C, Zhang Y, Guo X, Yu G (2014) Histone acetyltransferase p300 mediates histone acetylation of PS1 and BACE1 in a cellular model of Alzheimer’s disease. PLoS One 9:e103067PubMedPubMedCentralCrossRefGoogle Scholar
- 60.Lunnon K, Mill J (2013) Epigenetic studies in Alzheimer’s disease: current findings, caveats, and considerations for future studies. Am J Med Genet B Neuropsychiatr Genet 162B:789–799PubMedCrossRefPubMedCentralGoogle Scholar
- 61.Ma J, Yang Q, Wei Y (2016) Effect of the PGD2-DP signaling pathway on primary cultured rat hippocampal neuron injury caused by aluminum overload. Sci Rep 6:24646PubMedPubMedCentralCrossRefGoogle Scholar
- 62.Manivannan Y, Manivannan B, Beach TG, Halden RU (2015) Role of environmental contaminants in the etiology of Alzheimer’s disease: a review. Curr Alzheimer Res 12:116–146PubMedPubMedCentralCrossRefGoogle Scholar
- 63.Maoz R, Garfinkel BP, Soreq H (2017) Alzheimer’s disease and ncRNAs. Springer International Publishing, ChamCrossRefGoogle Scholar
- 64.Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J (2010) Epigenetic changes in Alzheimer’s disease: decrements in DNA methylation. Neurobiol Aging 31:2025PubMedCrossRefPubMedCentralGoogle Scholar
- 65.Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J (2011a) Epigenetic mechanisms in Alzheimer’s disease. Curr Med Chem 18:1751–1756CrossRefGoogle Scholar
- 66.Mastroeni D, Grover A, Delvaux E, Whiteside C, Coleman PD, Rogers J (2011c) Epigenetics mechanisms in Alzheimer’s disease. Neurobiol Aging 4:1161–1180CrossRefGoogle Scholar
- 67.Migliore L, Copped F (2009) Genetics, environmental factors and the emerging role of epigenetics in neurodegenerative diseases. Mutat Res 667:82–97PubMedCrossRefPubMedCentralGoogle Scholar
- 68.Mirza A, King A, Troakes C, Exley C (2017) Aluminium in brain tissue in familial Alzheimer’s disease. J Trace Elements Med Biol 40:30CrossRefGoogle Scholar
- 69.Morris G, Puri BK, Frye RE (2017) The putative role of environmental aluminium in the development of chronic neuropathology in adults and children. How strong is the evidence and what could be the mechanisms involved? Metab Brain Dis 32:1335PubMedPubMedCentralCrossRefGoogle Scholar
- 70.Nee LE, Eldridge R, Sunderland T, Thomas CB, Katz D, Thompson KE, Weingartner H, Weiss H, Julian C, Cohen R (1987) Dementia of the Alzheimer type: clinical and family study of 22 twin pairs. Neurology 37:359–363PubMedCrossRefPubMedCentralGoogle Scholar
- 71.Oshima E, Ishihara T, Yokota O, Nakashima-Yasuda H, Nagao S, Ikeda C, Naohara J, Terada S, Uchitomi Y (2013) Accelerated tau aggregation, apoptosis and neurological dysfunction caused by chronic oral administration of aluminum in a mouse model of tauopathies. Brain Pathol 23:633–644PubMedCrossRefPubMedCentralGoogle Scholar
- 72.Pedersen NL (2010) Reaching the limits of genome-wide significance in Alzheimer disease: back to the environment. JAMA 303:1864–1865PubMedCrossRefPubMedCentralGoogle Scholar
- 73.Pratic D, Uryu K, Sung S, Tang S, Trojanowski JQ, Lee VM (2002) Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. FASEB J 16:1138CrossRefGoogle Scholar
- 74.Prema A, Justin TA, Manivasagam T, Mohamed EM, Guillemin GJ (2017) Fenugreek seed powder attenuated aluminum chloride-induced tau pathology, oxidative stress, and inflammation in a rat model of Alzheimer’s disease. J Alzheimers Dis 60:S209–S220PubMedCrossRefPubMedCentralGoogle Scholar
- 75.Qazi TJ, Quan Z, Mir A, Hong Q (2017) Epigenetics in Alzheimer’s disease: perspective of DNA methylation. Mol Neurobiol 55:1026–1044PubMedCrossRefPubMedCentralGoogle Scholar
- 76.Raiha I, Kaprio J, Koskenvuo M, Rajala T, Sourander L (1996) Alzheimer’s disease in Finnish twins. Lancet 347:573PubMedCrossRefGoogle Scholar
- 77.Raiha I, Kaprio J, Koskenvuo M, Rajala T, Sourander L (1998) Environmental differences in twin pairs discordant for Alzheimer’s disease. J Neurol Neurosurg Psychiatry 65:785–787PubMedPubMedCentralCrossRefGoogle Scholar
- 78.Rao JS, Keleshian VL, Klein S, Rapoport SI (2012) Epigenetic modifications in frontal cortex from Alzheimer’s disease and bipolar disorder patients. Transl Psychiatry 2:e132PubMedPubMedCentralCrossRefGoogle Scholar
- 79.Reitz C, Mayeux R (2014) Alzheimer disease: epidemiology, diagnostic criteria, risk factors and biomarkers. Biochem Pharmacol 88:640–651PubMedPubMedCentralCrossRefGoogle Scholar
- 80.Ribes D, Colomina MT, Vicens P, Domingo JL (2010) Impaired spatial learning and unaltered neurogenesis in a transgenic model of Alzheimer’s disease after oral aluminum exposure. Curr Alzheimer Res 7:401–408PubMedCrossRefPubMedCentralGoogle Scholar
- 81.Richmond TJ, Davey CA (2003) The structure of DNA in the nucleosome core. Nature 423:145PubMedCrossRefPubMedCentralGoogle Scholar
- 82.Ridge PG, Ebbert MTW, Kauwe JSK (1982) Genetics of Alzheimer’s disease. Arch Med Res 284:622–631Google Scholar
- 83.Rivera DS, Inestrosa NC, Bozinovic F (2016) On cognitive ecology and the environmental factors that promote Alzheimer disease: lessons from Octodon degus (Rodentia: Octodontidae). Biol Res 49:1–10CrossRefGoogle Scholar
- 84.Robinson M, Lee BY, Hane FT (2017) Recent progress in Alzheimer’s disease research, part 2: genetics and epidemiology. J Alzheimers Dis 57:317PubMedPubMedCentralCrossRefGoogle Scholar
- 85.Rondeau V, Jacqmingadda H, Commenges D, Helmer C, Dartigues JF (2009) Aluminum and silica in drinking water and the risk of Alzheimer’s disease or cognitive decline: findings from 15-year follow-up of the PAQUID cohort. Am J Epidemiol 169:489–496PubMedCrossRefPubMedCentralGoogle Scholar
- 86.Russ TC, Gatz M, Pedersen NL, Hannah J, Wyper G, Batty GD, Deary IJ, Starr JM (2015) Geographical variation in dementia: examining the role of environmental factors in Sweden and Scotland. Epidemiology 26:263–270PubMedPubMedCentralCrossRefGoogle Scholar
- 87.Said MM, Rabo MM (2017) Neuroprotective effects of eugenol against aluminium induced toxicity in the rat brain. Arch Ind Hyg Toxicol 68:27Google Scholar
- 88.Sanchez-Guerra M, Zheng Y, Osorio-Yanez C, Zhong J, Chervona Y, Wang S, Chang D, Mccracken JP, Diaz A, Bertazzi PA (2015) Effects of particulate matter exposure on blood 5-hydroxymethylation: results from the Beijing truck driver air pollution study. Epigenetics 10:633–642PubMedPubMedCentralCrossRefGoogle Scholar
- 89.Sanchez-Mut JV, Gräff J (2015) Epigenetic alterations in Alzheimer’s disease. Front Behav Neurosci 9:347PubMedPubMedCentralCrossRefGoogle Scholar
- 90.Sanchezmut JV, Heyn H, Vidal E, Moran S, Sayols S, Delgadomorales R, Schultz MD, Ansoleaga B, Garciaesparcia P, Ponsespinal M (2016) Human DNA methylomes of neurodegenerative diseases show common epigenomic patterns. Transl Psychiatry 6:e718CrossRefGoogle Scholar
- 91.Serretti A, Olgiati P, De RD (2007) Genetics of Alzheimer’s disease. A rapidly evolving field. J Alzheimers Dis 12:73PubMedCrossRefPubMedCentralGoogle Scholar
- 92.Shu L, Sun W, Li L, Xu Z, Li L, Pei X, Hui S, Huang L, Qi X, Peng J (2016) Genome-wide alteration of 5-hydroxymenthylcytosine in a mouse model of Alzheimer’s disease. BMC Genomics 17:381PubMedPubMedCentralCrossRefGoogle Scholar
- 93.Singla N, Dhawan DK (2016) Zinc improves cognitive and neuronal dysfunction during aluminium-induced neurodegeneration. Mol Neurobiol:1–17Google Scholar
- 94.Slooter AJ, Cruts M, Kalmijn S, Hofman A, Breteler MM, Van Broeckhoven C, Van Duijn CM (1998) Risk estimates of dementia by apolipoprotein E genotypes from a population-based incidence study: the Rotterdam study. Arch Neurol 55:964–968PubMedCrossRefPubMedCentralGoogle Scholar
- 95.Sun C, Lu L, Yu Y, Liu L, Hu Y, Ye Y, Jin C, Lin X (2016) Decreasing methylation of pectin caused by nitric oxide leads to higher aluminium binding in cell walls and greater aluminium sensitivity of wheat roots. J Exp Bot 67:979–989PubMedCrossRefPubMedCentralGoogle Scholar
- 96.Sweatt JD (2010) Mechanisms of memory, 2nd edn. Elsevier, AmsterdamGoogle Scholar
- 97.Sweatt JD (2013) The emerging field of neuroepigenetics. Neuron 80:624PubMedCrossRefPubMedCentralGoogle Scholar
- 98.Tacik P, Sanchezcontreras M, Rademakers R, Dickson DW, Wszolek ZK (2015) Genetic disorders with tau pathology: a review of the literature and report of two patients with tauopathy and positive family histories. Neurodegener Dis 16:12–21PubMedPubMedCentralCrossRefGoogle Scholar
- 99.Tomljenovic L (2011) Aluminum and Alzheimer’s disease: after a century of controversy, is there a plausible link? J Alzheimers Dis 23:567PubMedCrossRefGoogle Scholar
- 100.Urdinguio RG, Sanchez-MUT JV, Esteller M (2009) Epigenetic mechanisms in neurological diseases: genes, syndromes, and therapies. Lancet Neurol 8:1056PubMedCrossRefPubMedCentralGoogle Scholar
- 101.Virk SA, Eslick GD (2015) Aluminum levels in brain, serum, and cerebrospinal fluid are higher in Alzheimer’s disease cases than in controls: a series of meta-analyses. J Alzheimers Dis 47:629–638PubMedCrossRefPubMedCentralGoogle Scholar
- 102.Walton JR (2009) Functional impairment in aged rats chronically exposed to human range dietary aluminum equivalents. Neurotoxicology 30:182–193PubMedCrossRefPubMedCentralGoogle Scholar
- 103.Walton JR (2013) Aluminum’s involvement in the progression of Alzheimer’s disease. J Alzheimers Dis 35:7–43PubMedCrossRefPubMedCentralGoogle Scholar
- 104.Walton JR (2014) Chronic aluminum intake causes Alzheimer’s disease: applying Sir Austin Bradford Hill’s causality criteria. J Alzheimers Dis 40:765PubMedCrossRefPubMedCentralGoogle Scholar
- 105.Walton JR, Wang MX (2009) APP expression, distribution and accumulation are altered by aluminum in a rodent model for Alzheimer’s disease. J Inorg Biochem 103:1548–1554PubMedCrossRefPubMedCentralGoogle Scholar
- 106.Waly M, Olteanu H, Banerjee R, Choi SW, Mason JB, Parker BS, Sukumar S, Shim S, Sharma A, Benzecry JM (2004) Activation of methionine synthase by insulin-like growth factor-1 and dopamine: a target for neurodevelopmental toxins and thimerosal. Mol Psychiatry 9:358PubMedCrossRefPubMedCentralGoogle Scholar
- 107.Wang SC, Oelze B, Schumacher A (2008) Age-specific epigenetic drift in late-onset Alzheimer’s disease. PLoS One 3:e2698PubMedPubMedCentralCrossRefGoogle Scholar
- 108.Wang J, Yu JT, Tan MS, Jiang T, Tan L (2013) Epigenetic mechanisms in Alzheimer’s disease: implications for pathogenesis and therapy. Ageing Res Rev 12:1024–1041PubMedCrossRefPubMedCentralGoogle Scholar
- 109.Wang L, Hu J, Zhao Y, Lu X, Zhang Q, Niu Q (2014) Effects of aluminium on β-amyloid (1–42) and secretases (APP-cleaving enzymes) in rat brain. Neurochem Res 39:1338–1345PubMedCrossRefPubMedCentralGoogle Scholar
- 110.Watson CT, Roussos P, Garg P, Ho DJ, Azam N, Katsel PL, Haroutunian V, Sharp AJ (2016) Genome-wide12 DNA methylation profiling in the superior temporal gyrus reveals epigenetic signatures associated with Alzheimer’s disease. Genome Med 8:1–14CrossRefGoogle Scholar
- 111.Wen K, Mili J, Elkhodor B, Dhana K, Nano J, Pulido T, Kraja B, Zaciragic A, Bramer WM, Troup J (2016) The role of DNA methylation and histone modifications in neurodegenerative diseases: a systematic review. PLoS One 11:e0167201PubMedPubMedCentralCrossRefGoogle Scholar
- 112.Whitehead MW, Farrar G, Christie GL, Blair JA, Thompson RP, Powell JJ (1997) Mechanisms of aluminum absorption in rats. Am J Clin Nutr 65:1446PubMedCrossRefGoogle Scholar
- 113.Whyte LS, Lau AA, Hemsley KM, Hopwood JJ, Sargeant TJ (2017) Endo-lysosomal and autophagic dysfunction: a driving factor in Alzheimer’s disease? J Neurochem 140:703PubMedCrossRefGoogle Scholar
- 114.Xi L, Li W, Yu C, Yu D, Gang Y (2015) Histone acetylation modifiers in the pathogenesis of Alzheimer’s disease. Front Cell Neurosci 9:226Google Scholar
- 115.Xing Y, Tang Y, Jia J (2015) Sex differences in neuropsychiatric symptoms of Alzheimer’s disease: the modifying effect of apolipoprotein Eε4 status. Behav Neurol 2015:1–6CrossRefGoogle Scholar
- 116.Yang WN, Hu XD, Han H, Shi LL, Feng GF, Liu Y, Qian YH (2014) The effects of valsartan on cognitive deficits induced by aluminum trichloride and d-galactose in mice. Neurol Res 36:651PubMedCrossRefGoogle Scholar
- 117.Yang X, Yuan Y, Lu X, Yang J, Wang L, Song J, Nie J, Zhang Q, Niu Q (2015) The relationship between cognitive impairment and global DNA methylation decrease among aluminum Potroom workers. J Occup Environ Med 57:713–717PubMedPubMedCentralCrossRefGoogle Scholar
- 118.Yang X, Yuan Y, Niu Q (2016a) Effects of aluminium chloride on the methylation of app in hippocampal of rats. J Hyg Res 45:345Google Scholar
- 119.Yang XJ, Yuan YZ, Niu Q (2016b) Association between serum aluminium level and methylation of amyloid precursor protein gene in workers engaged in aluminium electrolysis. Chin J Ind Hyg Occup Dis 34:255Google Scholar
- 120.Yegambaram M, Manivannan B, Beach TG, Halden RU (2015) Role of environmental contaminants in the etiology of Alzheimer’s disease: a review. Curr Alzheimer Res 12:116PubMedCrossRefGoogle Scholar
- 121.Yuan Y, Yang X, Ren P, Kang P, Li Z, Niu Q (2015) Research of aluminum to the cognitive ability and genome-wide methylation in rats. J Hyg Res 44:359–363Google Scholar
- 122.Zaky A, Mohammad B, Moftah M, Kandeel KM, Bassiouny AR (2013) Apurinic/apyrimidinic endonuclease 1 is a key modulator of aluminum-induced neuroinflammation. BMC Neurosci 14:26PubMedPubMedCentralCrossRefGoogle Scholar
- 123.Zawilla NH, Taha FM, Kishk NA, Farahat SA, Farghaly M, Hussein M (2014) Occupational exposure to aluminum and its amyloidogenic link with cognitive functions. J Inorg Biochem 139:57PubMedPubMedCentralCrossRefGoogle Scholar
- 124.Zhang QL, Jia L, Jiao X, Guo WL, Ji JW, Yang HL, Niu Q (2012) APP/PS1 transgenic mice treated with aluminum: an update of Alzheimer’s disease model. Int J Immunopathol Pharmacol 25:49PubMedCrossRefPubMedCentralGoogle Scholar
- 125.Zhang L, Jin C, Liu Q, Lu X, Wu S, Yang J, Du Y, Zheng L, Cai Y (2013) Effects of subchronic aluminum exposure on spatial memory, ultrastructure and L-LTP of hippocampus in rats. J Toxicol Sci 38:255PubMedCrossRefPubMedCentralGoogle Scholar
- 126.Zhang L, Jin C, Lu X, Yang J, Wu S, Liu Q, Chen R, Bai C, Zhang D, Zheng L (2014) Aluminium chloride impairs long-term memory and downregulates cAMP-PKA-CREB signalling in rats. Toxicology 323:95–108PubMedCrossRefPubMedCentralGoogle Scholar
- 127.Zhangyu Zou, Lui C, Chunhui Che, Huapin Huang (2014) Clinical genetics of Alzheimer’s disease. Biomed Res Int 2014:291862PubMedPubMedCentralGoogle Scholar
- 128.Zovkic IB, Guzmankarlsson MC, Sweatt JD (2013) Epigenetic regulation of memory formation and maintenance. Learn Mem 20:61–74PubMedPubMedCentralCrossRefGoogle Scholar