Aluminum induces neurodegeneration and its toxicity arises from increased iron accumulation and reactive oxygen species (ROS) production

Neurobiology of Aging

Volumn 33, Issue 1, 2012, Pages 199.e1-199.e12

  Wu, Zhihao ^a   Du, Yumei ^a   Xue, Hua ^a   Wu, Yongsheng ^a   Zhou, Bing ^a  

^a TSINGHUA UNIVERSITY   (China)

Author keywords

AD (Alzheimer's disease); Al; Iron dyshomeostasis; ROS

Indexed keywords

ACETYLCYSTEINE; ALPHA TOCOPHEROL; ALUMINUM; AMYLOID BETA PROTEIN; BATHOPHENANTHROLINEDISULFONIC ACID; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; FERRITIN; FRATAXIN; IRON; IRON CHELATING AGENT; MANGANESE SUPEROXIDE DISMUTASE; NORPHENAZONE; REACTIVE OXYGEN METABOLITE; TAU PROTEIN; UNCLASSIFIED DRUG;

ALUMINUM OVERLOAD; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DROSOPHILA; DRUG EFFECT; ENZYME ACTIVITY; FRIEDREICH ATAXIA; GENE EXPRESSION; GENE OVEREXPRESSION; GENE THERAPY; IRON CHELATION; IRON STORAGE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; TAUOPATHY;

EID: 81355123407     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2010.06.018     Document Type: Article

References (46)

1. Anderson P.R., Kirby K., Hilliker A.J., Phillips J.P. RNAi-mediated suppression of the mitochondrial iron chaperone, frataxin, in Drosophila. Hum. Mol. Genet 2005, 14:3397-3405.
2. Anderson P.R., Kirby K., Orr W.C., Hilliker A.J., Phillips J.P. Hydrogen peroxide scavenging rescues frataxin deficiency in a Drosophila model of Friedreich's ataxia. Proc. Natl. Acad. Sci. U S A 2008, 105:611-616.
3. Bertholf R.L., Herman M.M., Savory J., Carpenter R.M., Sturgill B.C., Katsetos C.D., Vandenberg S.R., Wills M.R. A long-term intravenous model of aluminum maltol toxicity in rabbits: tissue distribution, hepatic, renal, and neuronal cytoskeletal changes associated with systemic exposure. Toxicol. Appl. Pharmacol 1989, 98:58-74.
4. Bilen J., Bonini N.M. Drosophila as a model for human neurodegenerative disease. Annu. Rev. Genet 2005, 39:153-171.
5. Bondy S.C., Kirstein S. The promotion of iron-induced generation of reactive oxygen species in nerve tissue by aluminum. Mol. Chem. Neuropathol 1996, 27:185-194.
6. Cathcart R., Schwiers E., Ames B.N. Detection of picomole levels of hydroperoxides using a fluorescent dichlorofluorescein assay. Anal. Biochem 1983, 134:111-116.
7. Culotta V.C., Klomp L.W., Strain J., Casareno R.L., Krems B., Gitlin J.D. The copper chaperone for superoxide dismutase. J. Biol. Chem 1997, 272:23469-23472.
8. Dobson C.B., Day J.P., King S.J., Itzhaki R.F. Location of aluminum and gallium in human neuroblastoma cells treated with metal-chelating agent complexes. Toxicol. Appl. Pharmacol 1998, 152:145-152.
9. Drago D., Cavaliere A., Mascetra N., Ciavardelli D., di Ilio C., Zatta P., Sensi S.L. 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. 2008, 11:861-871.
10. Dua R., Gill K.D. Effect of aluminum phosphide exposure on kinetic properties of cytochrome oxidase and mitochondrial energy metabolism in rat brain. Biochim. Biophys. Acta 2004, 1674:4-11.
11. Hayflick S.J. Neurodegeneration with brain iron accumulation: from genes to pathogenesis. Semin. Pediatr. Neurol 2006, 13:182-185.
12. Henson C.P., Cleland W.W. Purification and kinetic studies of beef liver cytoplasmic aconitase. J. Biol. Chem 1967, 242:3833-3838.
13. Iijima K., Chiang H.C., Hearn S.A., Hakker I., Gatt A., Shenton C., Granger L., Leung A., Iijima-Ando K., Zhong Y. Abeta42 mutants with different aggregation profiles induce distinct pathologies in Drosophila. PLoS ONE 2008, 3:e1703.
14. Iijima K., Liu H.P., Chiang A.S., Hearn S.A., Konsolaki M., Zhong Y. Dissecting the pathological effects of human. Abeta 40 and Abeta42 in Drosophila: a potential model for Alzheimer's disease. Proc Natl Acad Sci U S A 2004, 101(17):6. 623-628.
15. Karlik S.J., Eichhorn G.L., Lewis P.N., Crapper D.R. Interaction of aluminum species with deoxyribonucleic acid. Biochemistry 1980, 19:5991-5998.
16. Khanna P., Nehru B. Antioxidant enzymatic system in neuronal and glial cells enriched fractions of rat brain after aluminum exposure. Cell. Mol. Neurobiol 2007, 27:959-969.
17. Kihira T., Yoshida S., Kondo T., Yase Y., Ono S. ALS-like skin changes in mice on a chronic low-Ca/Mg high-Al diet. J. Neurol. Sci 2004, 219:7-14.
18. Kim Y., Olivi L., Cheong J.H., Maertens A., Bressler J.P. Aluminum stimulates uptake of non-transferrin bound iron and transferrin bound iron in human glial cells. Toxicol. Appl. Pharmacol 2007, 220:349-356.
19. Klatzo I., Wisniewski H., Streicher E. Experimental Production of Neurofibrillary Degeneration. I. Light Microscopic Observations. J. Neuropathol. Exp. Neurol 1965, 24:187-199.
20. Kondapalli K.C., Kok N.M., Dancis A., Stemmler T.L. Drosophila frataxin: an iron chaperone during cellular Fe-S cluster bioassembly. Biochemistry 2008, 47:6917-6927.
21. Kumar V., Bal A., Gill K.D. Impairment of mitochondrial energy metabolism in different regions of rat brain following chronic exposure to aluminum. Brain Res. 2008, 1232:94-103.
22. Kumar V., Bal A., Gill K.D. Susceptibility of mitochondrial superoxide dismutase to aluminum induced oxidative damage. Toxicology 2009, 255:117-123.
23. Lankoff A., Banasik A., Duma A., Ochniak E., Lisowska H., Kuszewski T., Gozdz S., Wojcik A. A comet assay study reveals that aluminum induces DNA damage and inhibits the repair of radiation-induced lesions in human peripheral blood lymphocytes. Toxicol. Lett 2006, 161:27-36.
24. Llorens J.V., Navarro J.A., Martinez-Sebastian M.J., Baylies M.K., Schneuwly S., Botella J.A., Molto M.D. Causative role of oxidative stress in a Drosophila model of Friedreich ataxia. FASEB J. 2007, 21:333-344.
25. Massie H.R., Williams T.R., Aiello V.R. Excess dietary aluminum increases Drosophila's rate of aging. Gerontology 1985, 31:309-314.
26. Middaugh J., Hamel R., Jean-Baptiste G., Beriault R., Chenier D., Appanna V.D. Aluminum triggers decreased aconitase activity via Fe-S cluster disruption and the overexpression of isocitrate dehydrogenase and isocitrate lyase: a metabolic network mediating cellular survival. J. Biol. Chem 2005, 280:3159-3165.
27. Missirlis F., Kosmidis S., Brody T., Mavrakis M., Holmberg S., Odenwald W.F., Skoulakis E.M., Rouault T.A. Homeostatic mechanisms for iron storage revealed by genetic manipulations and live imaging of Drosophila ferritin. Genetics 2007, 177:89-100.
28. Miu A.C., Benga O. Aluminum and Alzheimer's disease: a new look. J. Alzheimers Dis 2006, 10:179-201.
29. Miwa S., St-Pierre J., Partridge L., Brand M.D. Superoxide and hydrogen peroxide production by Drosophila mitochondria. Free Radic. Biol. Med 2003, 35:938-948.
30. Mizoroki T., Meshitsuka S., Maeda S., Murayama M., Sahara N., Takashima A. Aluminum induces tau aggregation in vitro but not in vivo. J. Alzheimers Dis 2007, 11:419-427.
31. Oyanagi K. The nature of the parkinsonism-dementia complex and amyotrophic lateral sclerosis of Guam and magnesium deficiency. Parkinsonism Relat. Disord. 2005, 11(suppl 1):S17-S23.
32. Savory J., Ghribi O. Can studies of aluminum toxicity in vivo and in vitro provide relevant information on the pathogenesis and etiology of Alzheimer's disease?. J. Alzheimers Dis. 2007, 11:429-430. [Discussion, 31-32].
33. Savory J., Herman M.M., Ghribi O. Mechanisms of aluminum-induced neurodegeneration in animals: Implications for Alzheimer's disease. J. Alzheimers Dis 2006, 10:135-144.
34. Savory J., Rao J.K., Huang Y., Letada P.R., Herman M.M. Age-related hippocampal changes in Bcl-2: Bax ratio, oxidative stress, redox-active iron and apoptosis associated with aluminum-induced neurodegeneration: increased susceptibility with aging. Neurotoxicology 1999, 20:805-817.
35. Tanimura T., Isono K., Yamamoto M.T. Taste Sensitivity to Trehalose and Its Alteration by Gene Dosage in Drosophila Melanogaster. Genetics 1988, 119:399-406.
36. Tully T., Quinn W.G. Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A 1985, 157(2):263-277.
37. Vasudevaraju P., Govindaraju M., Palanisamy A.P., Sambamurti K., Rao K.S. Molecular toxicity of aluminum in relation to neurodegeneration. Indian J. Med. Res 2008, 128:545-556.
38. Waghray M., Cui Z., Horowitz J.C., Subramanian I.M., Martinez F.J., Toews G.B., Thannickal V.J. Hydrogen peroxide is a diffusible paracrine signal for the induction of epithelial cell death by activated myofibroblasts. FASEB J. 2005, 19:854-856.
39. Walton J.R. An aluminum-based rat model for Alzheimer's disease exhibits oxidative damage, inhibition of PP2A activity, hyperphosphorylated tau, and granulovacuolar degeneration. J. Inorg. Biochem 2007, 101:1275-1284.
40. Ward R.J., Zhang Y., Crichton R.R. Aluminum toxicity and iron homeostasis. J. Inorg. Biochem 2001, 87:9-14.
41. Wittmann C.W., Wszolek M.F., Shulman J.M., Salvaterra P.M., Lewis J., Hutton M., Feany M.B. Tauopathy in Drosophila: neurodegeneration without neurofibrillary tangles. Science 2001, 293:711-714.
42. Wong A., Yang J., Cavadini P., Gellera C., Lonnerdal B., Taroni F., Cortopassi G. The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum. Mol. Genet 1999, 8:425-430.
43. Wu Z., Li C. S. Lv In Zhou, B. Pantothenate kinase-associated neurodegeneration: insights from a Drosophila model. Hum Mol Genet 2009, 18(19):3. 659-672.
44. Yamanaka K., Minato N., Iwai K. Stabilization of iron regulatory protein 2, IRP2, by aluminum. FEBS Lett. 1999, 462:216-220.
45. Yokel R.A. Aluminum produces age related behavioral toxicity in the rabbit. Neurotoxicol. Teratol 1989, 11:237-242.
46. Yokel R.A. Blood-brain barrier flux of aluminum, manganese, iron and other metals suspected to contribute to metal-induced neurodegeneration. J. Alzheimers Dis 2006, 10:223-253.