The Role of Oxidative Stress in Metals Toxicity; Mitochondrial Dysfunction as a Key Player
AbstractMetals can cause oxidative stress by increasing the formation of reactive oxygen species (ROS), which make antioxidants incapable of defiance against growing amounts of free radicals. Metal toxicity is related to their oxidative state and reactivity with other compounds. However, several reports about metals have been published in the recent years. Mitochondria, as a site of cellular oxygen consumption and energy production, can be a target for metals toxicity. Dysfunction of Mitochondrial oxidative phosphorylation led to the production of some metals toxicities metals through alteration in the activities of I, II, III, IV and V complexes and disruption of mitochondrial membrane. Reductions of adenosine triphosphate (ATP) synthesis or induction of its hydrolysis can impair the cellular energy production. In the present review study, the researchers have criticized reviews and some evidence about the oxidative stress as a mechanism of toxicity of metals. The metals disrupt cellular and antioxidant defense, reactive oxygen species (ROS) generation, and promote oxidative damage. The oxidative injuries induced by metals can be restored by use of antioxidants such as chelators, vitamin E and C, herbal medicine, and through increasing the antioxidants level. However, to elucidate many aspect of mechanism toxicity of metals, further studies are yet to be carried out.
1. Halliwell B. Biochemistry of oxidative stress. Biochemical Society Transactions. 2007;35(Pt 5):1147.
Ranjbar A, Khorami S, Safarabadi M, Shahmoradi A, Malekirad AA, Vakilian K, et al. Antioxidant activity of Iranian Echium amoenum Fisch & CA Mey flower decoction in humans: a cross-sectional before/after clinical trial. Evidence-based Complementary and Alternative Medicine. 2006;3(4):469-73.
Guo T, Cui L, Shen J, Wang R, Zhu W, Xu Y, et al. A dual-emission and large Stokes shift fluorescence probe for real-time discrimination of ROS/RNS and imaging in live cells. Chemical Communications. 2013;49(18):1862-4.
Dröge W. Free radicals in the physiological control of cell function. Physiological reviews. 2002;82(1):47-95.
Halliwell B, Gutteridge J, Cross C. Free radicals, antioxidants, and human disease: where are we now? The Journal of laboratory and clinical medicine. 1992;119(6):598.
Mittler R. Oxidative stress, antioxidants and stress tolerance. Trends in plant science. 2002;7(9):405-10.
Valko M, Rhodes C, Moncol J, Izakovic M, Mazur M. Free radicals, metals and antioxidants in oxidative stress-induced cancer. Chemico-biological interactions. 2006;160(1):1-40.
Ranjbar A, Khani-Jazani R, Sedighi A, Jalali-Mashayekhi F, Ghazi-Khansari M, Abdollahi M. Alteration of body total antioxidant capacity and thiol molecules in human chronic exposure to aluminum. Toxicological & Environmental Chemistry. 2008;90(4):707-13.
Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radical Biology and Medicine. 2000;29(3):222-30.
Ott M, Gogvadze V, Orrenius S, Zhivotovsky B. Mitochondria, oxidative stress and cell death. Apoptosis. 2007;12(5):913-22.
Orrenius S, Gogvadze V, Zhivotovsky B. Mitochondrial oxidative stress: implications for cell death. Annu Rev Pharmacol Toxicol. 2007;47:143-83.
Golden T-R, Melov S. Mitochondrial DNA mutations, oxidative stress, and aging. Mechanisms of ageing and development. 2001;122(14):1577-89.
Lin MT, Beal MF. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. nature. 2006;443(7113):787-95.
Krumschnabel G, Manzl C, Berger C, Hofer B. Oxidative stress, mitochondrial permeability transition, and cell death in Cu-exposed trout hepatocytes. Toxicology and applied pharmacology. 2005;209(1):62-73.
Huang X, Moir RD, Tanzi RE, Bush AI, Rogers JT. Redox‐Active Metals, Oxidative Stress, and Alzheimer's Disease Pathology. Annals of the New York Academy of Sciences. 2004;1012(1):153-63.
Valko M, Morris H, Cronin M. Metals, toxicity and oxidative stress. Current medicinal chemistry. 2005;12(10):1161-208.
Ercal N, Gurer-Orhan H, Aykin-Burns N. Toxic metals and oxidative stress part I: mechanisms involved in metal-induced oxidative damage. Current topics in medicinal chemistry. 2001;1(6):529-39.
Jomova K, Valko M. Advances in metal-induced oxidative stress and human disease. Toxicology. 2011;283(2):65-87.
Hansford RG, Hogue BA, Mildaziene V. Dependence of H2O2 formation by rat heart mitochondria on substrate availability and donor age. Journal of bioenergetics and biomembranes. 1997;29(1):89-95.
Requejo R, Chouchani ET, Hurd TR, Menger KE, Hampton MB, Murphy MP. Measuring mitochondrial protein thiol redox state. Methods in enzymology. 2010;474:123-47.
Brand MD. The sites and topology of mitochondrial superoxide production. Experimental gerontology. 2010;45(7):466-72.
Ranjbar A, Ghahremani MH, Sharifzadeh M, Golestani A, Ghazi-Khansari M, Baeeri M, et al. Protection by pentoxifylline of malathion-induced toxic stress and mitochondrial damage in rat brain. Human & experimental toxicology. 2010;29(10):851-64.
Brand M. Uncoupling to survive? The role of mitochondrial inefficiency in ageing. Experimental gerontology. 2000;35(6):811-20.
Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, et al. Mitochondrial α-ketoglutarate dehydrogenase complex generates reactive oxygen species. The Journal of neuroscience. 2004;24(36):7779-88.
Jang YC, Lustgarten MS, Liu Y, Muller FL, Bhattacharya A, Liang H, et al. Increased superoxide in vivo accelerates age-associated muscle atrophy through mitochondrial dysfunction and neuromuscular junction degeneration. The FASEB Journal. 2010;24(5):1376-90.
Weisiger RA, Fridovich I. Mitochondrial superoxide dismutase site of synthesis and intramitochondrial localization. Journal of Biological Chemistry. 1973;248(13):4793-6.
Liang L, Ho Y, Patel M. Mitochondrial superoxide production in kainate-induced hippocampal damage. Neuroscience. 2000;101(3):563-70.
Sies H, Cadenas E. Oxidative stress: damage to intact cells and organs. Philos Trans R Soc Lond B Biol Sci. 1985;311(1152):617-31.
Abdollahi M, Ranjbar A, Shadnia S, Nikfar S, Rezaie A. Pesticides and oxidative stress: a review. Medical science monitor: international medical journal of experimental and clinical research. 2004;10(6):RA141-7.
Young I, Woodside J. Antioxidants in health and disease. Journal of clinical pathology. 2001;54(3):176-86.
Yon J-M, Baek I-J, Lee S-R, Jin Y, Kim M-R, Nahm S-S, et al. The spatio-temporal expression pattern of cytoplasmic Cu/Zn superoxide dismutase (SOD1) mRNA during mouse embryogenesis. Journal of molecular histology. 2008;39(1):95-103.
Fantel AG, Mackler B, Stamps LD, Tran TT, Person RE. Reactive oxygen species and DNA oxidation in fetal rat tissues. Free Radical Biology and Medicine. 1998;25(1):95-103.
Flohé L. Glutathione peroxidase. Oxygen Radicals in Biology and Medicine: Springer; 1988. p. 663-8.
Flohé L. Glutathione Peroxidases. Selenoproteins and Mimics: Springer; 2012. p. 1-25.
Webb AJ, Patel N, Loukogeorgakis S, Okorie M, Aboud Z, Misra S, et al. Nitric Oxide, Oxidative Stress. 2008.
Stohs SJ, Bagchi D, Hassoun E, Bagchi M. Oxidative mechanisms in the toxicity of chromium and cadmium ions. Journal of environmental pathology, toxicology and oncology: official organ of the International Society for Environmental Toxicology and Cancer. 1999;19(3):201-13.
Barnhart J. Occurrences, uses, and properties of chromium. Regulatory toxicology and pharmacology. 1997;26(1):S3-S7.
Vincent J. The nutritional biochemistry of chromium (III): Access Online via Elsevier; 2011.
Bagchi D, Bagchi M, Stohs SJ. Chromium (VI)-induced oxidative stress, apoptotic cell death and modulation of p53 tumor suppressor gene. Molecular Mechanisms of Metal Toxicity and Carcinogenesis: Springer; 2001. p. 149-58.
Mertz W. Chromium occurrence and function in biological systems. Physiol Rev;(United States). 1969;49(2).
Anderson RA. Chromium metabolism and its role in disease processes in man. Clinical physiology and biochemistry. 1985;4(1):31-41.
Wedeen RP, Qian L. Chromium-induced kidney disease. Environmental health perspectives. 1991;92:71.
Hummel M, Standl E, Schnell O. Chromium in metabolic and cardiovascular disease. Hormone and metabolic research. 2007;39(10):743-51.
Wang ZQ, Cefalu WT. Current concepts about chromium supplementation in type 2 diabetes and insulin resistance. Current diabetes reports. 2010;10(2):145-51.
Gambelunghe A, Piccinini R, Ambrogi M, Villarini M, Moretti M, Marchetti C, et al. Primary DNA damage in chrome-plating workers. Toxicology. 2003;188(2):187-95.
Newbold R, Amos J, Connell J. The cytotoxic, mutagenic and clastogenic effects of chromium-containing compounds on mammalian cells in culture. Mutation Research/Genetic Toxicology. 1979;67(1):55-63.
Levis A, Bianchi V, Tamino G, Pegoraro B. Cytotoxic effects of hexavalent and trivalent chromium on mammalian cells in vitro. British journal of cancer. 1978;37(3):386.
Vasylkiv OY, Kubrak OI, Storey KB, Lushchak VI. Cytotoxicity of chromium ions may be connected with induction of oxidative stress. Chemosphere. 2010;80(9):1044-9.
Rossi SC, Gorman N, Wetterhahn KE. Mitochondrial reduction of the carcinogen chromate: formation of chromium (V). Chemical Research in Toxicology. 1988;1(2):101-7.
Khan FH, Ambreen K, Fatima G, Kumar S. Assessment of health risks with reference to oxidative stress and DNA damage in chromium exposed population. Science of the Total Environment. 2012;430:68-74.
Bagchi D, Stohs SJ, Downs BW, Bagchi M, Preuss HG. Cytotoxicity and oxidative mechanisms of different forms of chromium. Toxicology. 2002;180(1):5-22.
Peterson-Roth E, Reynolds M, Quievryn G, Zhitkovich A. Mismatch repair proteins are activators of toxic responses to chromium-DNA damage. Molecular and cellular biology. 2005;25(9):3596-607.
Sugden KD, Stearns DM. The role of chromium (V) in the mechanism of chromate-induced oxidative DNA damage and cancer. Journal of environmental pathology, toxicology and oncology: official organ of the International Society for Environmental Toxicology and Cancer. 2000;19(3):215.
Arakawa H, Weng M-w, Chen W-c, Tang M-s. Chromium (VI) induces both bulky DNA adducts and oxidative DNA damage at adenines and guanines in the p53 gene of human lung cells. Carcinogenesis. 2012;33(10):1993-2000.
Chiu A, Shi X, Lee W, Hill R, Wakeman T, Katz A, et al. Review of chromium (VI) apoptosis, cell-cycle-arrest, and carcinogenesis. Journal of Environmental Science and Health, Part C. 2010;28(3):188-230.
Aiyar J, Borges KM, Floyd RA, Wetterhahn KE. Role of chromium (V), glutathione thiyl radical and hydroxyl radical intermediates in Chromium (VI)‐induced DNA Damage. Toxicological & Environmental Chemistry. 1989;22(1-4):135-48.
Sahin K, Sahin N, Kucuk O. Effects of chromium, and ascorbic acid supplementation on growth, carcass traits, serum metabolites, and antioxidant status of broiler chickens reared at a high ambient temperature (32 C). Nutrition Research. 2003;23(2):225-38.
Guha G, Rajkumar V, Kumar RA, Mathew L. Antioxidant activity of Lawsonia inermis extracts inhibits chromium (VI)-induced cellular and DNA toxicity. Evidence-based Complementary and Alternative Medicine. 2011;2011.
Friberg L, Piscator M, Nordberg GF, Kjellström T. Cadmium in the environment1974.
Kasuya M. Recent epidemiological studies on itai-itai disease as a chronic cadmiumpoisoning in Japan. Water Science & Technology. 2000;42(7-8):147-54.
Murata I, Hirono T, Saeki Y, Nakagawa S. Cadmium enteropathy, renal osteomalacia (" Itai Itai" disease in Japan). Bulletin de la Société internationale de chirurgie. 1970;29(1):34.
Oskarsson A, Widell A, Olsson M, Grawé KP. Cadmium in food chain and health effects in sensitive population groups. Biometals. 2004;17(5):531-4.
Satarug S, Garrett SH, Sens MA, Sens DA. Cadmium, environmental exposure, and health outcomes. Ciência & Saúde Coletiva. 2011;16(5):2587-602.
Shim J, Son Y, Park JM, Kim MK. Effect of Chlorella intake on Cadmium metabolism in rats. Nutrition research and practice. 2009;3(1):15-22.
Shaikh ZA, Vu TT, Zaman K. Oxidative stress as a mechanism of chronic cadmium-induced hepatotoxicity and renal toxicity and protection by antioxidants. Toxicology and applied pharmacology. 1999;154(3):256-63.
Prozialeck WC, Edwards JR, Vaidya VS, Bonventre JV. Preclinical evaluation of novel urinary biomarkers of cadmium nephrotoxicity. Toxicology and applied pharmacology. 2009;238(3):301-5.
A Shaikh Z, Tang W. Protection against chronic cadmium toxicity by glycine. Toxicology. 1999;132(2):139-46.
Zhang X, Li D, Dong S, Zhang J. Study on the relationship between cadmium immunotoxicity and corticotropin-releasing factor]. Wei sheng yan jiu= Journal of hygiene research. 2000;29(4):193.
Waalkes MP. Cadmium carcinogenesis. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 2003;533(1):107-20.
Cuypers A, Plusquin M, Remans T, Jozefczak M, Keunen E, Gielen H, et al. Cadmium stress: an oxidative challenge. Biometals. 2010;23(5):927-40.
Liu J, Qu W, Kadiiska MB. Role of oxidative stress in cadmium toxicity and carcinogenesis. Toxicology and applied pharmacology. 2009;238(3):209-14.
Rikans LE, Yamano T. Mechanisms of cadmium‐mediated acute hepatotoxicity. Journal of biochemical and molecular toxicology. 2000;14(2):110-7.
Al-Nasser IA, Al-Nasser I. Cadmium hepatotoxicity and alterations of the mitochondrial function. Clinical Toxicology. 2000;38(4):407-13.
Li M, Xia T, Jiang C-S, Li L-J, Fu J-L, Zhou Z-C. Cadmium directly induced the opening of membrane permeability pore of mitochondria which possibly involved in cadmium-triggered apoptosis. Toxicology. 2003;194(1):19-33.
Wang Y, Fang J, Leonard SS, Krishna Rao KM. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radical Biology and Medicine. 2004;36(11):1434-43.
Heyno E, Klose C, Krieger‐Liszkay A. Origin of cadmium‐induced reactive oxygen species production: mitochondrial electron transfer versus plasma membrane NADPH oxidase. New Phytologist. 2008;179(3):687-99.
Azzouzi BE, Tsangaris GT, Pellegrini O, Manuel Y, Benveniste J, Thomas Y. Cadmium induced apoptosis in a human T cell line. Toxicology. 1994;88(1):127-39.
Kondoh M, Araragi S, Sato K, Higashimoto M, Takiguchi M, Sato M. Cadmium induces apoptosis partly via caspase-9 activation in HL-60 cells. Toxicology. 2002;170(1):111-7.
Wang C, Ma W, Su Y. NF-κB Pathway Contributes to Cadmium-Induced Apoptosis of Porcine Granulosa Cells. Biological trace element research. 2013:1-8.
Zhang C, Mao W, Kong X, Yue L, Gao Y, Yin Z. Inhibition of cadmium-induced apoptosis by Glutathione S-transferase P1 via mitogen-activated protein kinases (MAPKs) and mitochondria. 2010.
Fujiki K, Inamura H, Matsuoka M. Phosphorylation of FOXO3a by PI3K/Akt pathway in HK-2 renal proximal tubular epithelial cells exposed to cadmium. Archives of toxicology. 2013:1-9.
Nguyen KC, Willmore WG, Tayabali AF. Cadmium telluride quantum dots cause oxidative stress leading to extrinsic and intrinsic apoptosis in hepatocellular carcinoma HepG2 cells. Toxicology. 2013.
Yang Z, Yang S, Qian SY, Hong J-S, Kadiiska MB, Tennant RW, et al. Cadmium-induced toxicity in rat primary mid-brain neuroglia cultures: role of oxidative stress from microglia. Toxicological sciences. 2007;98(2):488-94.
Brama M, Politi L, Santini P, Migliaccio S, Scandurra R. Cadmium-induced apoptosis and necrosis in human osteoblasts: role of caspases and mitogen-activated protein kinases pathways. Journal of endocrinological investigation. 2012;35(2):198.
Patrick L. Lead toxicity, a review of the literature. Part I: exposure, evaluation, and treatment. Alternative Medicine Review. 2006;11(1):2-22.
Gidlow D. Lead toxicity. Occupational Medicine. 2004;54(2):76-81.
Humphreys D. Effects of exposure to excessive quantities of lead on animals. British Veterinary Journal. 1991;147(1):18-30.
Sanders T, Liu Y, Buchner V, Tchounwou PB. Neurotoxic effects and biomarkers of lead exposure: a review. Reviews on environmental health. 2009;24(1):15-46.
Patra R, Swarup D, Dwivedi S. Antioxidant effects of α tocopherol, ascorbic acid and L-methionine on lead induced oxidative stress to the liver, kidney and brain in rats. Toxicology. 2001;162(2):81-8.
Sandhir R, Gill K. Effect of lead on lipid peroxidation in liver of rats. Biological trace element research. 1995;48(1):91-7.
Wang L, Li J, Li J, Liu Z. Effects of lead and/or cadmium on the oxidative damage of rat kidney cortex mitochondria. Biological trace element research. 2010;137(1):69-78.
Prasanthi R, Devi CB, Basha DC, Reddy NS, Reddy GR. Calcium and zinc supplementation protects lead (Pb)-induced perturbations in antioxidant enzymes and lipid peroxidation in developing mouse brain. International Journal of Developmental Neuroscience. 2010;28(2):161-7.
Villeda-Hernandez J, Barroso-Moguel R, Mendez-Armenta M, Nava-Ruız C, Huerta-Romero R, Rıos C. Enhanced brain regional lipid peroxidation in developing rats exposed to low level lead acetate. Brain research bulletin. 2001;55(2):247-51.
Buettner GR. The pecking order of free radicals and antioxidants: lipid peroxidation, α-tocopherol, and ascorbate. Archives of Biochemistry and Biophysics. 1993;300(2):535-43.
Daniel EE. Ameliorative Effect of Vitamin C on Serum Liver Enzymes in Lead-Induced Toxicity in Wistar Rats. Journal of Science. 2013;3(1):188-912.
Bokara KK, Brown E, McCormick R, Yallapragada PR, Rajanna S, Bettaiya R. Lead-induced increase in antioxidant enzymes and lipid peroxidation products in developing rat brain. Biometals. 2008;21(1):9-16.
Sugawara E, Nakamura K, Miyake T, Fukumura A, Seki Y. Lipid peroxidation and concentration of glutathione in erythrocytes from workers exposed to lead. British journal of industrial medicine. 1991;48(4):239-42.
Goyer RA, Clarkson TW. Toxic effects of metals. Casarett & Doull’s Toxicology The Basic Science of Poisons, Fifth Edition, Klaassen, CD [Ed] McGraw-Hill Health Professions Division, ISBN. 1996;71054766.
Ullah N, Khan MF, Mukhtiar M, Khan H, Rehman AU. Metabolic modulation of glutathione in whole blood components against lead-induced toxicity. African Journal of Biotechnology. 2011;10(77):17853-8.
Campana O, Sarasquete C, Blasco J. Effect of lead on ALA-D activity, metallothionein levels, and lipid peroxidation in blood, kidney, and liver of the toadfish< i> Halobatrachus didactylus. Ecotoxicology and Environmental Safety. 2003;55(1):116-25.
Jiun YS, Hsien LT. Lipid peroxidation in workers exposed to lead. Archives of Environmental Health: An International Journal. 1994;49(4):256-9.
Gurer-Orhan H, Sabır HU, Özgüneş H. Correlation between clinical indicators of lead poisoning and oxidative stress parameters in controls and lead-exposed workers. Toxicology. 2004;195(2):147-54.
Rocha JB, Pereira ME, Emanuelli T, Christofari RS, Souz DO. Effect of treatment with mercury chloride and lead acetate during the second stage of rapid postnatal brain growth on δ-aminolevulinic acid dehydratase (ALA-D) activity in brain, liver, kidney and blood of suckling rats. Toxicology. 1995;100(1):27-37.
Rodriguez BL, Curb JD, Davis J, Shintani T, Perez MH, Apau‐Ludlum N, et al. Use of the Dietary Supplement 5‐Aminiolevulinic Acid (5‐ALA) and Its Relationship with Glucose Levels and Hemoglobin A1C among Individuals with Prediabetes. Clinical and Translational Science. 2012;5(4):314-20.
Ahamed M, Siddiqui M. Low level lead exposure and oxidative stress: current opinions. Clinica Chimica Acta. 2007;383(1):57-64.
Young KW, Piñon LG, Bampton ET, Nicotera P. Different pathways lead to mitochondrial fragmentation during apoptotic and excitotoxic cell death in primary neurons. Journal of biochemical and molecular toxicology. 2010;24(5):335-41.
He L, Poblenz AT, Medrano CJ, Fox DA. Lead and calcium produce rod photoreceptor cell apoptosis by opening the mitochondrial permeability transition pore. Journal of Biological Chemistry. 2000;275(16):12175-84.
Liu Z, Li D, Zhao W, Zheng X, Wang J, Wang E. A potent lead induces apoptosis in pancreatic cancer cells. PloS one. 2012;7(6):e37841.
Hsu P-C, Guo YL. Antioxidant nutrients and lead toxicity. Toxicology. 2002;180(1):33-44.
Gargouri M, Magné C, Dauvergne X, Ksouri R, El Feki A, Metges M-AG, et al. Cytoprotective and antioxidant effects of the edible halophyte< i> Sarcocornia perennis L.(swampfire) against lead-induced toxicity in renal cells. Ecotoxicology and Environmental Safety. 2013.
Berlyne G, Ben Ari J, Knopf E, Yagil R, Weinberger G, Danovitch G. Aluminium toxicity in rats. The Lancet. 1972;299(7750):564-8.
Boscolo PR, Menossi M, Jorge RA. Aluminum-induced oxidative stress in maize. Phytochemistry. 2003;62(2):181-9.
Xie CX, Mattson MP, Lovell MA, Yokel RA. Intraneuronal aluminum potentiates iron-induced oxidative stress in cultured rat hippocampal neurons. Brain research. 1996;743(1):271-7.
Sood PK, Nahar U, Nehru B. Curcumin attenuates aluminum-induced oxidative stress and mitochondrial dysfunction in rat brain. Neurotoxicity research. 2011;20(4):351-61.
Flora SJ, Mehta A, Satsangi K, Kannan GM, Gupta M. Aluminum-induced oxidative stress in rat brain: Response to combined administration of citric acid and HEDTA. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology. 2003;134(3):319-28.
Mahieu ST, Gionotti M, Millen N, Elías MM. Effect of chronic accumulation of aluminum on renal function, cortical renal oxidative stress and cortical renal organic anion transport in rats. Archives of toxicology. 2003;77(11):605-12.
Wang H, Liang W, Huang J. Putrescine Mediates Aluminum Tolerance in Red Kidney Bean by Modulating Aluminum-Induced Oxidative Stress. Crop Science. 2013.
Federico A, Cardaioli E, Da Pozzo P, Formichi P, Gallus GN, Radi E. Mitochondria, oxidative stress and neurodegeneration. Journal of the neurological sciences. 2012;322(1):254-62.
Niemi NM, MacKeigan JP. Mitochondrial Phosphorylation in Apoptosis: Flipping the Death Switch. Antioxidants & redox signaling. 2012.
Li Z, Xing D. Mechanistic study of mitochondria-dependent programmed cell death induced by aluminium phytotoxicity using fluorescence techniques. Journal of experimental botany. 2011;62(1):331-43.
Kumar V, Bal A, Gill KD. Impairment of mitochondrial energy metabolism in different regions of rat brain following chronic exposure to aluminium. Brain research. 2008;1232:94-103.
Bharathi VP, Govindaraju M, Palanisamy A, Sambamurti K, Rao K. Molecular toxicity of aluminium in relation to neurodegeneration. Indian J Med Res. 2008;128(4):545-56.
Schildknecht PH, Vidal BC. Aluminium triggers necrosis and apoptosis in V79 cells. Toxicological & Environmental Chemistry. 2004;86(1):63-72.
Gupta VB, Anitha S, Hegde M, Zecca L, Garruto R, Ravid R, et al. Aluminium in Alzheimer’s disease: are we still at a crossroad? Cellular and Molecular Life Sciences CMLS. 2005;62(2):143-58.
El-Demerdash FM. Antioxidant effect of vitamin E and selenium on lipid peroxidation, enzyme activities and biochemical parameters in rats exposed to aluminium. Journal of Trace Elements in Medicine and Biology. 2004;18(1):113-21.
Silva S, Pinto G, Correia B, Pinto-Carnide O, Santos C. Rye oxidative stress under long term Al exposure. Journal of plant physiology. 2013.
Rottkamp CA, Nunomura A, Raina AK, Sayre LM, Perry G, Smith MA. Oxidative stress, antioxidants, and Alzheimer disease. Alzheimer Disease & Associated Disorders. 2000;14(1):S62-S6.
Zorov DB, Juhaszova M, Sollott SJ. Mitochondrial ROS-induced ROS release: an update and review. Biochimica et Biophysica Acta (BBA)-Bioenergetics. 2006;1757(5):509-17.
Blokhina O, Virolainen E, Fagerstedt KV. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Annals of botany. 2003;91(2):179-94.
Klaunig JE, Kamendulis LM, Hocevar BA. Oxidative stress and oxidative damage in carcinogenesis. Toxicologic pathology. 2010;38(1):96-109.
Halliwell B, Gutteridge J. Free radicals in biology and medicine. Pergamon; 1985.
Costa M. Dioxygenases as Targets of Metals, Hypoxia and Oxidative Stress during Carcinogenesis. Journal of Molecular and Genetic Medicine. 2013.
Bahavar M, Tarbali N, Einolahi N, Dashti N. Evaluation of trace metal (cd, cr, cu)–induced oxidative stress in presence of H2O2 on purified DNA strands break from nonpathogenic Escherichia coli. KAUMS Journal (FEYZ). 2013;16(7):633-4.
Belyaeva EA, Sokolova TV, Emelyanova LV, Zakharova
IO. Mitochondrial electron transport chain in heavy metal-induced neurotoxicity: effects of cadmium, mercury, and copper. The Scientific World Journal. 2012;2012.
Pulido MD, Parrish AR. Metal-induced apoptosis: mechanisms. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis. 2003;533(1):227-41.
Granchi D, Cenni E, Ciapetti G, Savarino L, Stea S, Gamberini S, et al. Cell death induced by metal ions: necrosis or apoptosis? Journal of materials science: materials in medicine. 1998;9(1):31-7.
Shi H, Hudson LG, Liu KJ. Oxidative stress and apoptosis in metal ion-induced carcinogenesis. Free Radical Biology and Medicine. 2004;37(5):582-93.
Kasprzak KS. Possible role of oxidative damage in metal-induced carcinogenesis. Cancer investigation. 1995;13(4):411-30.
Martinez-Zamudio R, Ha HC. Environmental epigenetics in metal exposure. Epigenetics. 2011;6(7):820-7.
Patrick L. Toxic metals and antioxidants: Part II. The role of antioxidants in arsenic and cadmium toxicity. Alternative Medicine Review. 2003;8(2):106-28.
Kostova I, Balkansky S. Metal Complexes of Biologically Active Ligands as Potential Antioxidants. Current medicinal chemistry. 2013.
Gaurav D, Preet S, Dua K. Chronic cadmium toxicity in rats: Treatment with combined administration of vitamins, amino acids, antioxidants and essential metals. Journal of Food and Drug Analysis. 2010;18(6):464-70.
Pham-Huy LA, He H, Pham-Huy C. Free radicals, antioxidants in disease and health. International journal of biomedical science: IJBS. 2008;4(2):89.
Tavakol HS, Akram R, Azam S, Nahid Z. Protective effects of green tea on antioxidative biomarkers in chemical laboratory workers. Toxicology and Industrial Health. 2013.
Authors who publish with this journal agree to the following terms:
- Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution 4.0 International License that allows others to share the work with an acknowledgment of the work's authorship and initial publication in this journal.
- Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgment of its initial publication in this journal.
- Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work (See The Effect of Open Access).