Role of early life exposure and environment on neurodegeneration: implications on brain disorders

Translational Neurodegeneration

Akshay Anand¹  Vijay L Sharma²  Debomoy K Lahiri³  Shweta Modgil² 

[1] Department of Neurology, Neuroscience Research Lab, Post Graduate Institute of Medical Education and Research, #3036, Research Block-B, 160012 Chandigarh, India;Department of Zoology, Panjab University, Chandigarh, India;Department of Psychiatry, Institute of Psychiatric Research, Indiana University Medical Center Indianapolis, Indianapolis, USA

关键词: Pesticides;    Methylation;    LEARn;    Epigenetics;    Metals;    Aging;   

Others  :  834659
DOI  :  10.1186/2047-9158-3-9

 received in 2014-01-12, accepted in 2014-04-17,  发布年份 2014

【 摘 要 】

Neurodegenerative diseases such as Alzheimer’s disease (AD), Parkinson’s disease (PD), Amyotrophic lateral sclerosis (ALS) and retinal degeneration have been studied extensively and varying molecular mechanisms have been proposed for onset of such diseases. Although genetic analysis of these diseases has also been described, yet the mechanisms governing the extent of vulnerability to such diseases remains unresolved. Recent studies have, therefore, focused on the role of environmental exposure in progression of such diseases especially in the context of prenatal and postnatal life, explaining how molecular mechanisms mediate epigenetic changes leading to degenerative diseases. This review summarizes both the animal and human studies describing various environmental stimuli to which an individual or an animal is exposed during in-utero and postnatal period and mechanisms that promote neurodegeneration. The SNPs mediating gene environment interaction are also described. Further, preventive and therapeutic strategies are suggested for effective intervention.

【 授权许可】

   
2014 Modgil et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】

• [1]Lahiri DK, Maloney B: 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 2010, 45:291-296.
• [2]Charleta L, Chapronb Y, Faller P, Kirscha R, Stoned AT, Baveyee PC: Neurodegenerative diseases and exposure to the environmental metals Mn, Pb, and Hg. Coord Chem Rev 2012, 256:2147-2163.
• [3]Oteiza PI, Mackenzie GG, Verstraeten SV: Metals in neurodegeneration: involvement of oxidants and oxidant-sensitive transcription factors. Mol Aspects Med 2004, 25:103-115.
• [4]Parron T, Requena M, Hernández AF, Alarcon R: Association between environmental exposure to pesticides and neurodegenerative diseases. Toxicol Appl Pharmacol 2011, 256:379-385.
• [5]Caldwell KA, Tucci ML, Armagost J, Hodges TW, Chen J, Memon SB, Blalock JE, Deleon SM, Findlay RH, Ruan Q, Webber PJ, Standaert DG, Olson JB, Caldwell GA: Investigating bacterial sources of toxicity as an environmental contributor to dopaminergic neurodegeneration. PLoS One 2009, 4:e7227. doi:10.1371/journal.pone.0007227
• [6]Ali SF, Binienda ZK, Imam SZ: Molecular aspects of dopaminergic neurodegeneration: gene-environment interaction in parkin dysfunction. Int J Environ Res Public Health 2011, 8:4702-4713.
• [7]Gordon PH: Amyotrophic lateral sclerosis: an update for 2013 clinical features, pathophysiology, management and therapeutic trials. Aging Dis 2013, 4:295-310.
• [8]Baldi I, Lebailly P, Mohammed-Brahim B, Letenneur L, Dartigues JF, Brochard P: Neurodegenerative diseases and exposure to pesticides in the elderly. Am J Epidemiol 2002, 157:409-414.
• [9]Li N, Yu ZL, Wang L, Zheng YT, Jia JX, Wang Q, Zhu MJ, Liu XL, Xia X, Li WJ: Increased tau phosphorylation and beta amyloid in the hippocampus of mouse pups by early life lead exposure. Acta Biol Hung 2010, 61:123-134.
• [10]Claus- Henn B, Schnaas L, Ettinger AS, Schwartz J, Lamadrid-Figueroa H, Hernandez-Avila M, Amarasiriwardena C, Hu H, Bellinger DC, Wright RO, Tellez-Rojo MM: Associations of early childhood manganese and lead coexposure with neurodevelopment. Environ Health Perspect 2012, 120:126-131.
• [11]Karagas MR, Choi AL, Oken E, Horvat M, Schoeny R, Kamai E, Cowell W, Grandien P, Korrick S: Evidence on the human health effects of Low-level methylmercury exposure. Environ Health Perspect 2012, 120:799-806.
• [12]Anderson OS, Sant KE, Dolinoy DC: Nutrition and epigenetics: an interplay of dietary methyl donors, one-carbon metabolism and DNA methylation. J Nutr Biochem 2012, 23:853-859.
• [13]Erikson KM, Syversen T, Aschner JL, Aschner M: Interactions between excessive manganese exposures and dietary iron-deficiency in neurodegeneration. Environ Toxicol Pharmacol 2005, 19:415-421.
• [14]Rauh VA, Perera FP, Horton MK, Whyatt RM, Bansal R, Hao X, Liu J, Barr DB, Slotkin TA, Peterson BS: Brain anomalies in children exposed prenatally to a common organophosphate pesticide. Proc Natl Acad Sci U S A 2012, 109:7871-7876.
• [15]Hatcher JM, Richardson JR, Guillot TS, McCormack AL, Di Monte DA, Jones DP, Penell KD, Miller GW: Dieldrin exposure induces oxidative damage in the mouse nigrostriatal dopamine system. Exp Neurol 2007, 204:619-630.
• [16]Xiong N, Long X, Xiong J, Jia M, Chen C, Huang J, Ghoorah D, Kong X, Lin Z, Wang T: Mitochondrial complex I inhibitor rotenone-induced toxicity and its potential mechanisms in Parkinson’s disease models. Crit Rev Toxicol 2012, 42:613-632.
• [17]Pienaar IS, Kellaway LA, Russell VA, Smith AD, Stein DJ, Zigmond MJ, Daniel WMU: Maternal separation exaggerates the toxic effects of 6-hydroxydopamine in rats: Implications for neurodegenerative disorders. Stress 2008, 11:448-456.
• [18]Samuelsson A, Jennische E, Hansson H, Holmang A: Prenatal exposure to interleukin-6 results in inflammatory neurodegeneration in hippocampus with NMDA/GABAA dysregulation and impaired spatial learning. Am J Physiol Regul Integr Comp Physiol 2006, 290:R1345-R1356.
• [19]Gluckman PD, Hanson MA: Maternal constraint of fetal growth and its consequences. Semin Fetal Neonatal Med 2004, 9:419-425.
• [20]Gluckman PD, Hanson MA, Cooper C, Thornberg KL: Effect of in utero and early life conditions on adult health and disease. N Engl J Med 2008, 359:61-73.
• [21]Charalambous M, da Rosa ST, Ferguson-Smith AC: Genomic imprinting, growth control and the allocation of nutritional resources: consequences for postnatal life. Curr Opin Endocrinol Diabetes Obes 2007, 14:3-12.
• [22]Morales P, Fiedler JL, Andres S, Berrios C, Huaiquin P, Bustamante D, Cardenas S, Parra E, Herrera-Marschitz M: Plasticity of hippocampus following perinatal asphyxia: effects on postnatal apoptosis and neurogenesis. J Neurosci Res 2008, 86:2650-2662.
• [23]Kiss P, Szogyi D, Reglodi D, Horvath G, Farkas J, Lubics A, Tamas A, Atlasz T, Szabadfi K, Babai N, Gabriel R, Koppan M: Effects of perinatal asphyxia on the neurobehavioral and retinal development of newborn rats. Brain Res 2009, 1255:42-50.
• [24]Kapoor A, Petropoulos S, Mathews SG: Fetal programming of hypothalamic–pituitary–adrenal (HPA) axis function and behavior by synthetic glucocorticoids. Brain Res Rev 2008, 57:586-595.
• [25]Piscopo P, Bernardo A, Calamandrei G, Venerosi A, Valanzano A, Bianchi D, Confaloni A, Minghetti L: Altered expression of cyclooxygenase-2, presenilins and oxygen radical scavenging enzymes in a rat model of global perinatal asphyxia. Exp Neurol 2008, 209:192-198.
• [26]van Vliet E, Eixarch E, Illa M, Arbat-Plana A, Gonzalez-Tendero A, Hogberg HT, Zhao L, Hartung T, Gratacos E: Metabolomics reveals metabolic alterations by intrauterine growth restriction in the fetal rabbit brain. PLoS One 2013, 8:e64545. doi:10.1371/journal.pone.0064545
• [27]Johnston MV, Nakajima W, Hagberg H: Mechanisms of Hypoxic Neurodegeneration in the Developing Brain. Neuroscientist 2002, 8:212-220.
• [28]Ling J, Gayle DA, Ma SY, Lipton JW, Tong CW, Hong JS, Carvey PM: In utero bacterial endotoxin exposure causes loss of tyrosine hydroxylase neurons in the postnatal rat midbrain. Mov Disord 2002, 17:116-124.
• [29]Erikson KM, Dormann DC, Fitsanakis V, Lash LH, Ashner M: Alteration of oxidative stress markers due to in utero and neonatal exposures of airborne manganese. Biol Trace Elem Res 2006, 111:199-215.
• [30]Ahlbom E, Gogvadze V, Chen M, Celsi G, Ceccatelli S: Prenatal exposure to high levels of glucocorticoids increases the susceptibility of cerebellar granule cells to oxidative stress-induced cell death. Proc Natl Acad Sci U S A 2000, 97:14726-14730.
• [31]Barker DJ, Gluckman PD, Godfrey KM, Harding JE, Owens JA, Robinson JS: Fetal nutrition and cardiovasculardisease in adult life. Lancet 1993, 341:938-941.
• [32]Lovblad K, Ramelli G, Remonda L, Nirkko AC, Ozdoba C, Schroth G: Retardation of myelination due to dietary vitamin B12 deficiency: cranial MRI findings. Pediatr Radiol 1997, 27:155-158.
• [33]Roy S, Sable P, Khaire A, Randhir K, Kale A, Joshi S: Effect of maternal micronutrients (folic acid and vitamin B12) and omega 3 fatty acids on indices of brain oxidative stress in the offspring. Brain Dev 2014, 36:219-227.
• [34]White CL, Pistell PJ, Purpera MN, Gupta S, Feranandez-Kim SO, Hise TL, Keller JN, Ingram DK, Morrison CD, Bruce-Keller AJ: Effects of high fat diet on Morris maze performance, oxidative stress, and inflammation in rats: Contributions of maternal diet. Neurobiol Dis 2009, 35:3-13.
• [35]Langie SA, Achterfeldt S, Gorniak JP, Halley-Hogg KJA, Oxley D, Schooten FJ, Godschalk RW, McKay JA, Mathers JC: Maternal folate depletion and high-fat feeding from weaning affects DNA methylation and DNA repair in brain of adult offspring. FASEB J 2013, 27:3323-3334. doi:10.1096/fj.12-224121
• [36]Koza ST, Gouwyb NT, Demirc N, Nedzvetskyd VS, Eteme E, Baydasf G: Effects of maternal hyperhomocysteinemia induced by methionine intake on oxidative stress and apoptosis in pup rat brain. Int J Dev Neurosci 2010, 28:325-329.
• [37]Kaur D, Peng J, Chinta SJ, Rajagopalan S, Di Monteb DA, Cherny RA, Andersen JK: Increased murine neonatal iron intake results in Parkinson-like neurodegeneration with age. Neurobiol Aging 2007, 28:907-913.
• [38]Tuzun F, Kumral A, Dilek M, Ozbal S, Ergur B, Yesilirmark DC, Duman N, Yilmaz O, Ozkan H: Maternal omega-3 fatty acid supplementation protects against lipopolysaccharide-induced white matter injury in the neonatal rat brain. J Matern Fetal Neonatal Med 2012, 25:849-854.
• [39]Zhang W, Aschner M, Ghersi-igea J: Brain barrier systems: a new frontier in metal neurotoxilogical research. Toxicol Appl Pharmacol 2003, 192:1-11.
• [40]McLachlan DR, Bergeron C, Smith JE, Boomer D, Rifat SL: Risk for neuropathologically confirmed Alzheimer’s disease and residual aluminum in municipal drinking water employing weighted residential histories. Neurology 1996, 46:401-405.
• [41]Martyn CN, Coggon DN, Inskip H, Lacey RF, Young WF: Aluminum concentrations in drinking water and risk of Alzheimer’s disease. Epidemiology 1997, 8:281-286.
• [42]Gauthier E, Fortier I, Courchesna F, Pepsin P, Mortimer J, Gauvreau D: Aluminium forms in drinking water and risk of Alzheimer’s disease. Environ Res 2000, 84:234-246.
• [43]Kozlowski H, Luczkowski M, Remelli M, Valensin D: Copper, zinc and iron in neurodegenerative diseases (Alzheimer’s, Parkinson’s and prion diseases). Coord Chem Rev 2012, 256:2129-2141.
• [44]Hood DC, Cideciyan AV, Halevy DA, Jacobson SG: Sites of disease action in a retinal dystrophy with supernormal and delayed rod electroretinogram b-waves. Vision Res 1996, 36:889-901.
• [45]Luo L, Xu Y, Du Z, Sun X, Ma Z, Hu Y: Manganese-enhanced MRI optic nerve tracking: effect of intravitreal manganese dose on retinal toxicity. NMR Biomed 2012, 25:1360-1368.
• [46]Mela M, Grotzner SR, Legeay A, Mesmer-Dudons N, Massabuau J, Ventura DF, de Oliveira Ribeiro CA: Morphological evidence of neurotoxicity in retina after methylmercury exposure. Neurotoxicology 2012, 33:407-415.
• [47]Rothenberg SJ, Schnaas L, Salgado-Valladares M, Casanueva E, Geller AM, Hudnell HK, Fox DA: Increased ERG a- and b-wave amplitudes in 7- to 10-Year-old children resulting from prenatal lead exposure. Invest Ophthalmol Vis Sci 2002, 43:2036-2044.
• [48]Ethier A, Muckle G, Bastien C, Dewailly E, Ayotte P, Arfken C, Jacobson SW, Jacobson JL, Saint-Amour D: Effects of environmental contaminant exposure on visual brain development: A prospective electrophysiological study in school-aged children. Neurotoxicology 2012, 33:1075-1085.
• [49]Lisman J, Yasuda R, Raghavachari S: Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 2012, 13:169-182.
• [50]Gilbert ME, Lasley SM: Developmental lead (Pb) exposure reduces the ability of the NMDA antagonist MK-801 to suppress long-term potentiation (LTP) in the rat dentate gyrus, in vivo. Neurotoxicol Teratol 2007, 29:385-393.
• [51]Luscher C, Malenka RC: NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect Biol 2012., 4doi:10.1101/cshperspect.a005710
• [52]Chen J, Wang D, Ruan D, She J: Early chronic aluminium exposure impairs long-term potentiation and depression to the rat dentate gyrus in vivo. Neuroscience 2002, 112:879-887.
• [53]Viggiano A, Seru R, Damiano S, Luca B, Santillo M, Mondola P: Inhibition of long-term potentiation by CuZn superoxide dismutase injection in rat dentate gyrus: involvement of muscarinic M1 receptor. J Cell Physiol 2012, 227:3111-3115.
• [54]Gilbert ME, Mack CM, Lasley SM: The influence of developmental period of lead exposure on long-term potentiation in the adult rat dentate gyrus in vivo. Neurotoxicology 1999, 20:57-69.
• [55]Rai A, Maurya SK, Khare P, Srivastava A, Bandopadhyay S: Characterization of Developmental Neurotoxicity of As, Cd, and Pb Mixture: synergistic action of metal mixture in glial and neuronal functions. Toxicol Sci 2010, 118:586-601.
• [56]Moreira EG, Vassilieff I, Vassilieff VS: Developmental lead exposure: behavioral alterations in the short and long term. Neurotoxicol Teratol 2001, 23:489-495.
• [57]Basha MR, Wei W, Bakheet SA, Benitez N, Siddiqi HK, Ge YW, Lahiri DK, Zawia NH: 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, 25:823-829.
• [58]Wu J, Basha MR, Brock B, Cox DP, Cardozo-Pelaez F, McPherson CA, Harry J, Rice DC, Maloney B, Chen D, Lahiri DK, Zawia NH: Alzheimer’s disease (AD)-like pathology in aged monkeys after infantile exposure to environmental metal lead (Pb): evidence for a developmental origin and environmental link for AD. J Neurosci 2008, 28:3-9.
• [59]Jaga K, Dharmani C: Ocular toxicity from pesticide exposure: a recent review. Environ Health Prev Med 2006, 11:102-107.
• [60]Hernandez A, Parron T, Tsatsakis AM, Requena M, Alarcon R, Lopez-Guarnido O: Toxic effects of pesticide mixtures at a molecular level: their relevance to human health. Toxicology 2013, 307:136-145.
• [61]Bradberry SM, Proudfoot AT, Vale JA: Glyphosate poisoning. Toxicol Rev 2004, 23:159-167.
• [62]Budai P, Varnagy L, Somlyay IM, Linczmayer K, Pongracz A: Irritative effects of some pesticides and a technical component on tissue structure of the chorioallantoic membrane. Commun Agric Appl Biol Sci 2004, 69:807-809.
• [63]Naeher LP, Tulve NS, Egeghy PP, Barr DB, Adetona O, Fortmann RC, Needham LA, Bozeman E, Hilliard A, Sheldon LS: Organophosphorus and pyrethroid insecticide urinary metabolite concentrations in young children living in a southeastern United States city. Sci Total Environ 2010, 408:1145-1153.
• [64]Relton CL, Davey Smith G: Epigenetic epidemiology of common complex disease:prospects for prediction, prevention, and treatment. PLoS Med 2010, 7:e1000356. doi:10.1371/journal.pmed.1000356
• [65]Richardson JR, Caudle WM, Wang M, Dean ED, Pennell KD, Miller GW: Developmental exposure to the pesticide dieldrin alters the dopamine system and increases neurotoxicity in an animal model of Parkinson’s disease. FASEB J 2006, 20:1695-1697.
• [66]Thiruchelvam M, Brockel BJ, Richfield EK, Baggs RB, Cory-Slechta DA: Potentiated and preferential effects of combined paraquat and maneb on nigrostriatal dopamine systems: environmental risk factors for Parkinson’s disease? Brain Res 2000, 873:225-234.
• [67]Carloni M, Nasuti C, Fedeli D, Montani M, Amici A, Vadhana MS, Gabbianelli R: The impact of early life permethrin exposure on development of neurodegeneration in adulthood. Exp Gerontol 2012, 47:60-66.
• [68]Hillman CH, Erickson KI, Kramer AF: Be smart, exercise your heart: exercise effects on brain and cognition. Nat Rev Neurosci 2008, 9:58-65.
• [69]Costa J, Lunet N, Santos C, Santos J, Vaz-Carneiro A: Caffeine exposure and the risk of Parkinson’s disease: a systematic reviewand meta-analysis of observational studies. J Alzheimers Dis 2010, 20:S221-S238.
• [70]de Zeeuw P, Zwart F, Schrama R, van Engeland H, Durston S: Prenatal exposure to cigarette smoke or alcohol and cerebellum volume in attention-deficit/hyperactivity disorder and typical development. Transl Psychiatry 2012, 2:e84. doi:10.1038/tp
• [71]Qin L, Crews FT: NADPH oxidase and reactive oxygen species contribute to alcohol-induced microglial activation and neurodegeneration. J Neuroinflammation 2012, 9:5. doi:10.1186/1742-2094-9-5 BioMed Central Full Text
• [72]Anand A, Sharma NK, Gupta A, Prabhakar S, Sharma SK, Singh R, Gupta PK: Single nucleotide polymorphisms in mcp-1 and its receptor are associated with the risk of age related macular degeneration. PLoS One 2012, 7:e49905. doi:10.1371/journal.pone.0049905
• [73]Kim H, Lee SH, Kim SS, Yoo JH, Kim CJ: The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci 2007, 25:243-249.
• [74]Gomes da Silva S, Unsain N, Masco DH, Toscano- Silva M, de Amorim HA, Silva-Araujo BH: Early exercise promotes positive hippocampal plasticity and improves spatial memory in the adult life of rats. Hippocampus 2012, 22:347-358.
• [75]Perfeito R, Cunha-Oliveira T, Rego AC: Revisiting oxidative stress and mitochondrial dysfunction in the pathogenesis of Parkinson disease—resemblance to the effect of amphetamine drugs of abuse. Free Radic Biol Med 2012, 53:1791-1806.
• [76]Melo P, Zanon-Moreno V, Alves CJ, Magalhaes A, Tavares MA, Pinazo-Duran MD, Moradas- Ferreira P: Oxidative stress response in the adult rat retina and plasma after repeated administration of methamphetamine. Neurochem Int 2010, 56:431-436.
• [77]Melo P, Zanon-Moreno V, Vazquez SP, Pinazo-Duran MD, Tavares MA: Myelination changes in the rat optic nerve after prenatal exposure to methamphetamine. Brain Res 2006, 1106:21-29.
• [78]Melo P, Pinazo-Duran MD, Salgado-Borges J, Tavares MA: Correlation of axon size and myelin occupancy in rat prenatally exposed to methamphetamine. Brain Res 2008, 1222:61-68.
• [79]Dursun I, Jakubowska-Dogru E, van der List D, Liets LC, Coombs JL, Berman RF: Effects of early postnatal exposure to ethanol on retinal ganglion cell morphology and numbers of neurons in the Dorsolateral geniculate in mice. Alcohol Clin Exp Res 2011, 35:2063-2074.
• [80]Nassar SA, Emam NMM, Eid FA, Mohammed WT: Effects of non-ionizing radiation on the ultrastructure of the retina of albino mice. J Am Sci 2011, 7:1196-1208.
• [81]El-Sayyad HI, Sakr SA, Badawy GM, Afify HS: Hazardous effects of fried potato chips on the development of retina in albino rats. Asian Pac J Trop Biomed 2011, 1:253-260.
• [82]Perkins GA, Scott R, Perez A, Ellisman MH, Johnson JE, Fox DA: Bcl-xL-mediated remodeling of rod and cone synaptic mitochondria after postnatal lead exposure: Electron microscopy, tomography and oxygen consumption. Mol Vis 2012, 18:3029-3048.
• [83]Esteve-Rudd J, Fernandez-Sanchez L, Lax P, De Juan E, Martin-Nieto J, Cuenca N: Rotenone induces degeneration of photoreceptors and impairs the dopaminergic system in the rat retina. Neurobiol Dis 2011, 44:102-115.
• [84]Kisby GE, Fry RC, Lasarev MR, Bammler TK, Beyer RP, Churchwell M, Doerge DR, Meira LB, Palmer VS, Ramos- Crawford AL, Ren X, Sullivan RC, Kavanagh TJ, Samson LD, Zarbl H, Spencer PS: The cycad genotoxin MAM modulates brain cellular pathways involved in neurodegenerative disease and cancer in a DNA damage-linked manner. PLoS One 2011, 6:e20911. doi:10.1371/journal.pone.0020911
• [85]Gatto NM, Cockburn M, Bronstein J, Manthripragada AD, Ritz B: Well-water consumption and Parkinson’s disease in rural California. Environ Health Perspect 2009, 117:1912-1918.
• [86]Muthian G, Mackey V, King J, Charlton CG: Modeling a sensitization stage and a precipitation stage for parkinson’s disease using prenatal and postnatal 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine administration. Neuroscience 2010, 169:1085-1093.
• [87]Siegela JA, Craytora MJ, Rabera J: Long-term effects of methamphetamine exposure on cognitive function and muscarinic acetylcholine receptor levels in mice. Behav Pharmacol 2010, 21:602-614.
• [88]Singh AK, Tiwari MN, Upadhyay G, Patel DK, Singh D, Prakash O, Singh MP: Long term exposure to cypermethrin induces nigrostriatal dopaminergic neurodegeneration in adult rats: postnatal exposure enhances the susceptibility during adulthood. Neurobiol Aging 2012, 33:404-415.
• [89]Abu-Taweel GM, Ajarem JS, Ahmad M: Neurobehavioral toxic effects of perinatal oral exposure to aluminum on the developmental motor reflexes, learning, memory and brain neurotransmitters of mice offspring. Pharmacol Biochem Behav 2012, 101:49-56.
• [90]Mukhopadhyay P, Horn KH, Greene RM, Michele-Pisano M: Prenatal exposure to environmental tobacco smoke alters gene expression in the developing murine hippocampus. Reprod Toxicol 2010, 29:164-175.
• [91]Tsankova N, Renthal W, Kumar A, Nestler EJ: Epigenetic regulation in psychiatric disorders. Nat Rev Neurosci 2007, 8:355-367.
• [92]Mehler MF: Epigenetic principles and mechanisms underlying nervous system functions in health and disease. Prog Neurobiol 2008, 86:305-341.
• [93]Feil R: Environmental and nutritional effects on the epigenetic regulation of genes. Mutat Res 2006, 600:46-57.
• [94]Lahiri DK, Maloney B, Zawia NH: The LEARn model: an epigenetic explanation for idiopathic neurobiological diseases. Mol Psychiatry 2009, 14:992-1003.
• [95]Martin GM: Epigenetic drift in aging identical twins. Proc Natl Acad Sci U S A 2005, 102:10413-10414.
• [96]Fraga MF, Ballestar E, Paz MF, Ropero S, Setien F, Ballestar ML, Heine-Suner D, Ciqudosa JC, Urioste M, Benitez J, Boix-Chornet M, Sanchez-Aquilera A, Ling C, Carlsson E, Poulsen P, Vaag A, Stephan Z, Spector TD, Wu YZ, Plass C, Esteller M: Epigenetic differences arise during the lifetime of monozygotic twins. Proc Natl Acad Sci U S A 2005, 102:10604-10609.
• [97]Mastroeni D, McKee A, Grover A, Rogers J, Coleman PD: Epigenetic differences in cortical neurons from a pair of monozygotic twins discordant for Alzheimer’s disease. PLoS One 2009, 4:e6617. doi:10.1371/journal.pone.0006617
• [98]Rodenhiser D, Mann M: Epigenetics and human disease: translating basic biology into clinical applications. CMAJ 2006, 174:341-348.
• [99]Fuso A, Seminara L, Cavallaro RA, Danselmi F, Scarpa S: S- adenosylmethionine/homocysteine cycle alterations modify DNA methylation status with consequent deregulation of PS1 and BACE and beta-amyloid production. Mol Cell Neurosci 2005, 28:195-204.
• [100]Lahiri DK, Maloney B: The “LEARn” (latent early-life associated regulation) Model: an epigenetic pathway linking metabolic and cognitive disorders. J Alzheimers Dis 2012, 30:S15-S30.
• [101]Babenko O, Kovalchuk I, Metz GA: Epigenetic programming of neurodegenerative diseases by an adverse environment. Brain Res 2012, 1444:96-111.
• [102]Gluckman PD, Hanson MA, Spencer HG: Predictive adaptive responses and human evolution. Trends Ecol Evol 2005, 20:527-533.
• [103]Lee TM, Spears N, Tuthill CR, Zucker I: Maternal melatonin treatment influences rates of neonatal development of meadow vole pups. Biol Reprod 1989, 40:495-502.
• [104]Sambamurti K, Granholm AC, Kindy MS, Bhat NR, Greig NH, Lahiri DK, Mintzer JE: Cholesterol and Alzheimer’s disease: clinical and experimental models suggest interactions of different genetic, dietary and environmental risk factors. Curr Drug Targets 2004, 5:517-528.
• [105]Mortimer JA, van Duijn CM, Chandra V, Fratiglioni L, Graves AB, Heyman A, Kokmen E, Kondo K, Rocca WA, Shalat SL, Soininen H: Head trauma as a risk factor for Alzheimer’s disease: a collaborative re-analysis of case control studies. EURODEM Risk Factors Research Group. Int J Epidemiol 1991, 20:S28-S35.
• [106]Bolin CM, Basha R, Cox D, Zawia NH, Maloney B, Lahiri DK, Cardozo- Pelaez F: Exposure to lead and the developmental origin of oxidativeDNAdamage in the aging brain. FASEB J 2006, 20:788-790.
• [107]Friedland RP, Fritsch T, Smyth KA, Koss E, Lerner AJ, Chen CH, Petot GJ, Debanne SM: Patients with Alzheimer’s disease have reduced activities in midlife compared with healthy control-group members. Proc Natl Acad Sci U S A 2001, 98:3440-3445.
• [108]Signore AP, Zhang F, Weng Z, Gao Y, Chen J: Leptin neuroprotection in CNS: mechanism and therapeutic potentials. J Neurochem 2008, 106:1977-1990.
• [109]Kakuma T, Wang ZW, Pan W, Unger RH, Zhou YT: Role of leptin in peroxisome proliferator-activated receptor gamma coactivator-1 expression. Endocrinology 2000, 141:4576-4582.
• [110]Niculescue MD, Ziesel SH: Diet, Methyl donor and DNA methylation: interactions between dietary folate, methionine and choline. J Nutr 2002, 132:2333S-2335S.
• [111]Chan A, Shea TB: Supplementation with apple juice attenuates presenilin-1 overexpression during dietary and genetically induced oxidative stress. J Alzheimers Dis 2006, 10:353-358.
• [112]Lahiri DK: Where the actions of environment (nutrition), gene and protein meet: beneficial role of fruit and vegetable juices in potentially delaying the onset of Alzheimer’s disease. J Alzheimer Dis 2006, 10:359-361.
• [113]Bousquet M, Saint-Pierre M, Julien C, Salem N, Cicchetti F, Calon F: Beneficial effects of dietary omega-3 polyunsaturated fatty acid on toxin-induced neuronal degeneration in an animal model of Parkinson’s disease. FASEB J 2008, 22:1213-1225.
• [114]Green KN, Martinez-Coria H, Khashwji H, Hall EB, Yurko-Mauro KA, Ellis L, LaFerla FM: Dietary docosahexaenoic acid and docosapentaenoic acid ameliorate amyloid and tau pathology via a mechanism involving presenilin 1 levels. J Neurosci 2007, 27:4385-4395.
• [115]Ireland Z, Castillo-Melendez M, Dickinson H, Snow R, Walker DW: A maternal diet supplemented with creatine from mid-pregnancy protects the newborn spiny mouse brain from birth hypoxia. Neuroscience 2011, 194:372-379.
• [116]Babai N, Atlasz T, Tamas A, Reglodi D, Toth G, Kiss P, Gabriel R: Search for the optimal monosodium glutamate treatment schedule to study the neuroprotective effects of PACAP in the retina. Ann N Y Acad Sci 2006, 1070:149-155.
• [117]Szabadfi K, Atlasz T, Horvath G, Kiss P, Hamza L, Farkas J, Tamas A, Lubics A, Gabriel R, Reglodi D: Early postnatal enriched environment decreases retinal degeneration induced by monosodium glutamate treatment in rats. Brain Res 2009, 1259:107-112.
• [118]Elsner VR, Lovatel GA, Moyses F, Bertoldi K, Spindler C, Cechinel LR, Muotri AR, Siqueira IR: Exercise induces age-dependent changes on epigenetic parameters in rat hippocampus: A preliminary study. Exp Gerontol 2013, 48:136-139.
• [119]Elsner VR, Lovatel GA, Moyses F, Vanzella C, Santos M, Spindler C, Almeida EF, Nardin P, Siqueira IR: Effect of different exercise protocols on histone acetyltransferases and histone deacetylases activities in rat hippocampus. Neuroscience 2011, 192:580-587.
• [120]Scopel D, Fochesatto C, Cimarosti H, Rabbo M, Belló-Klein A, Salbego C, Netto CA, Siqueira IR: Exercise intensity influences cell injury in rat hippocampal slices exposed to oxygen and glucose deprivation. Brain Res Bull 2006, 71:155-159.
• [121]Dosunmu R, Alashwal H, Zawia NH: Genome-wide expression and methylation profiling in the agedrodent brain due to early-life Pb exposure and its relevance toaging. Mech Ageing Dev 2012, 133:435-443.
• [122]Rahman A, Brew BJ, Guillemin GJ: Lead dysregulates serine/threonine protein phosphatases in human neurons. Neurochem Res 2011, 36:195-204.
• [123]Vinish M, Anand A, Prabhakar S: Altered oxidative stress levels in Indian Parkinson’s diseasepatients with PARK2 mutations. Acta Biochim Pol 2011, 58:165-169.
• [124]Zawia NH, Cardozo-Pelaez F: An Epigenetic Model for Susceptibility to Oxidative DNA Damage in the Aging Brain and Alzheimer’s Disease in Ageing and age related disorders. In Aging and Age related disorders. Edited by Bondy S, Maiese K. Humana Press; 2010:439-453.
• [125]Barnham KJ, Bush AI: Metals in Alzheimer’s and Parkinson’s Diseases. Curr Opin Chem Biol 2008, 12:222-228.
• [126]Osfor MM, Ibrahim HS, Mohamed YA, Ahmed SM, El Azeem AS, Hegazy AM: Effect of Alpha Lipoic Acid and Vitamin E on Heavy Metals Intoxication in Male Albino Rats. J Am Sci 2010, 6:56-63.
• [127]Ozawa Y, Sasaki M, Takahashi N, Kamoshita M, Miyake S, Tsubota K: Neuroprotective Effects of Lutein in the Retina. Curr Pharm Des 2012, 18:51-56.
• [128]Jaiswal N, Kumar D, Rizvi SI: Red onion extract (Allium cepa L.) supplementation improves redox balance in oxidatively stressed rats. Food Sci Hum Wellness 2013, 2:99-104.
• [129]Cordova FM, Aguiar AS, Peres TV, Lopes MW, Goncalves FM, Remor AP, Lopes SC, Pilati C, Latini AS, Prediger RD, Erikson KM, Aschner M, Leal RB: In vivo manganese exposure modulates erk, akt and darpp-32 in the striatum of developing rats, and impairs their motor function. PLoS One 2012, 7:e33057. doi:10.1371/journal.pone.0033057
• [130]May JM, Qu ZC, Nazarewicz R, Di Kalov S: Ascorbic acid efficiency enhances neuronal synthesis of nor-epinephrine from dopamine. Brain Res Bull 2013, 90:35-42.
• [131]Li XM, Xu CL, Deng JM, Li LF, Ma SP, Qu R: Protective effect of Zhen-Wu-Tang (ZWT) through keeping DA stable and VMAT 2/DAT mRNA in balance in rats with striatal lesions induced by MPTP. J Ethnopharmacol 2011, 134:768-774.
• [132]Erbas O, Oltulub F, Taskiran D: Amelioration of rotenone-induced dopaminergic cell death in the striatum by oxytocin treatment. Peptides 2012, 38:312-317.
• [133]Zheng B, Liao Z, Locascio JJ, Lesniak KA, Roderick SS, Watt ML, Eklund AC, Zhang-James Y, Kim PD, Hauser MA, Grunblatt E, Moran LB, Mandel SA, Riederer P, Miller RM, Federoff HJ, Wüllner U, Papapetropoulos S, Youdim MB, Cantuti-Castelvetri I, Young AB, Vance JM, Davis RL, Hedreen JC, Adler CH, Beach TG, Graeber MB, Middleton FA, Rochet JC, Scherzer CR, et al.: PGC-1α, A Potential Therapeutic Target for Early Intervention in Parkinson’s disease. Sci Transl Med 2010, 2:52ra73. doi:10.1126/scitranslmed.3001059
• [134]Guilarte TR, McGlothan JL, Nihei MK: Hippocampal expression of Nmethyl- D-aspartate receptor (NMDAR1) subunit splice variant mRNA is altered by developmental exposure to Pb (2+). Brain Res Mol Brain Res 2000, 76:299-305.
• [135]Busselberg D, Michael D, Platt B: Pb2+ reduces voltage- and N-methyl- D-aspartate (NMDA)-activated calcium channel currents. Cell Mol Neurobiol 1994, 14:711-722.
• [136]Guilarte TR, McGlothan JL: Selective decrease in NR1 subunit splice variant mRNA in the hippocampus of Pb2 + -exposed rats: implications for synaptic targeting and cell surface expression of NMDAR complexes. Brain Res Mol Brain Res 2003, 113:37-43.
• [137]Froger N, Cadetti L, Lorach H, Martins J, Bemelmans AP, Dubus E, Degardin J, Pain D, Forster V, Chicaud L, Ivkovic I, Simonutti M, Fouquet S, Jammoul F, Léveillard T, Benosman R, Sahel JA, Picaud S: Taurine Provides Neuroprotection against Retinal Ganglion Cell Degeneration. PLoS One 2012, 7:e42017. doi:10.1371/journal.pone.0042017
• [138]Romero-Granados R, Fontan-Lozano A, Aguilar-Montilla FJ, Carrion AM: Postnatal proteasome inhibition induces neurodegeneration and cognitive deficiencies in adult mice: a new model of neurodevelopment syndrome. PLoS One 2011, 6:e28927. doi:10.1371/journal.pone.0028927
• [139]Chuang D, Leng Y, Marinova Z, Kim H, Chiu C: Multiple roles of HDAC inhibition in neurodegenerative conditions. Trends Neurosci 2009, 32:591-601.
• [140]Wu X, Li S, Wu Q, Peng Y, Yu D, Wang H, Chui D, Zhao J: Histone deacetylase inhibition leads to neuroprotection through regulation on glial function. Mol Neurodegen 2013, 8(Suppl 1):49. BioMed Central Full Text
• [141]Morahan JM, Yu B, Trent RJ, Pamphlett R: Genetic susceptibility to environmental toxicants in ALS. Am J Med Genet B Neuropsychiatr Genet 2007, 144:885-890.
• [142]Menegon A, Board PG, Blackburn AC, Mellick GD, Le Couteur DG: Parkinson’s disease, pesticides, and glutathione transferase polymorphisms. Lancet 1998, 352:1344-1346.
• [143]Goodrich JM, Basu N: Variants of glutathione s-transferase pi 1 exhibit differential enzymatic activity and inhibition by heavy metals. Toxicol In Vitro 2012, 26:630-635.
• [144]Sharma E, Mustafa M, Pathak R, Guleria K, Ahmed RS, Vaid NB, Banerjee BD: A case control study of gene environmental interaction in fetal growth restriction with special reference to organochlorine pesticides. Eur J Obstet Gynecol Reprod Biol 2012, 161:163-169.
• [145]Agusa T, Iwata H, Fujihara J, Kunito T, Takeshita H, Minh TB, Trang PT, Viet PH, Tanabe S: Genetic polymorphisms in glutathione S-transferase (GST) superfamily and arsenic metabolism in residents of the Red River Delta, Vietnam. Toxicol Appl Pharmacol 2010, 242:352-362.
• [146]Engel SM, Wetmur J, Chen J, Zhu C, Barr DB, Canfield RL, Wolff MS: Prenatal Exposure to Organophosphates, Paraoxonase 1, and Cognitive Development in Childhood. Environ Health Perspect 2011, 119:1182-1188.
• [147]Singh S, Kumar V, Singh P, Banerjee BD, Rautela RS, Grover SS, Rawat DS, Pasha ST, Jain SK, Rai A: Influence of CYP2C9, GSTM1, GSTT1 and NAT2 genetic polymorphisms on DNA damage in workers occupationally exposed to organophosphate pesticides. Mutat Res 2012, 741:101-108.
• [148]Tekin D, Kayaalt Z, Aliyev V, Soylemezoglu T: The effects of metallothionein 2A polymorphism on placental cadmium accumulation: is metallothionein a modifiying factor in transfer of micronutrients to the fetus? J Appl Toxicol 2012, 32:270-275.
• [149]Poggi C, Giusti B, Vestri A, Pasquini E, Abbate R, Dani C: Genetic polymorphisms of antioxidant enzymes in preterm infants. J Matern Fetal Neonatal Med 2012, 25:131-134.