A behavioral and ultrastructural dissection of the interference of aluminum with aging

Journal of Alzheimer's Disease

Volumn 6, Issue 3, 2004, Pages 315-328

  Miu, Andrei C ^a   Olteanu, Adrian I ^b   Miclea, Mircea ^a  

^a BABE BOLYAI UNIVERSITY   (Romania)

^b IULIU HATIEGANU UNIVERSITY OF MEDICINE AND PHARMACY   (Romania)

Author keywords

Aging; Aluminum; Alzheimer's disease; Mitochondria; Myelin

Indexed keywords

ALUMINUM; AMYLOID; GLUCONIC ACID; LIPOFUSCIN; MYELIN; UNCLASSIFIED DRUG;

ADOLESCENT; AGED; AGING; ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BEHAVIOR; BRAIN MITOCHONDRION; CELL INCLUSION; DEMYELINATION; ELECTRON MICROSCOPY; EMOTIONALITY; FEMALE; GLUCONATE ALUMINUM; HIPPOCAMPUS; HIRANO BODY; INFLAMMATION; LIVER TOXICITY; MALE; MYELIN SHEATH; NERVE CELL DEGENERATION; NEUROPATHOLOGY; NEUROTOXICITY; NONHUMAN; PHYSICAL ACTIVITY; PRIORITY JOURNAL; RAT; ULTRASTRUCTURE;

EID: 3042539176     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2004-6312     Document Type: Article

References (94)

1. K. Abreo, J. Jangula, S.K. Jain and J. Glass, Aluminum uptake and toxicity in cultured mouse hepatocytes, The Journal of the American Society of Nephrology 1 (1991), 1299-1304.
2. D.C. Ackley and R.A. Yokel, Aluminum transport aout of the brain extracellular fluid is proton dependent and inhibited by mersalyl acid, suggesting mediation by the monocarboxylate transporter (MCT1), Toxicology 127 (1998), 59-67.
3. A.C. Alfrey, G.R. Le Gendre and W.D. Kaehny, The dyalisis encephalopathy syndrome. Possible aluminum intoxication, New England Journal of Medicine 294 (1976), 184-188.
4. E. Andrási, É. Farkas, Z. Molná and É/Bertalan, Analysis of aluminum in the human brain, Microchemical Journal 54 (1996), 210-217.
5. C.E. Andreescu, A.C. Miu, R. Vasiu and A.I. Olteanu, Morphopatological and haematological proofs for a hepatic mediation of the neurotoxicity of aluminum, Proceedings of the Annual Conference of the Iuliu Hatieganu University of Medicine and Pharmacy, Cluj-Napoca, 2001.
6. H. Atamna, D.W. Killilea, A.N. Killilea and B.N. Ames, Heme deficiency may be a factor in the mitochondrial and neuronal decay of aging, Proceedings of the National Academy of Sciences USA 99 (2002), 14807-14812.
7. R.L. Bertholf, M.M. Herman, J. Savory, R.M. Carpenter, B.C. Strugill, C.D. Katsetos, S.R. Vandenberg and M.R. Wills, A long-term intravenous model of aluminum maltol toxicity in rabbits: tissue distribution, hepatic, renal, and neuronal cytoskeletal changes associated with systemic exposure, Toxicology and Applied Pharmacology 98 (1989), 58-74.
8. A. Campbell, The potential role of aluminium in Alzheimer's disease, Nephrology Dialisis Transplantation 17 (2002), 17-20.
9. A. Campbell, M.A. Smith, L.M. Sayre, S.C. Bondy and G. Perry, Mechanisms by which metals promote events connected to neurodegenerative diseases, Brain Research Bulletin 55 (2001), 125-132.
10. W.O. Caster and M. Wang, Dietary aluminum and Alzheimer's disease - A review, The Science of the Total Environment 17 (1981), 31-36.
11. S. Chaves, M. Gil, S. Marques, L. Gano and M.A. Santos, Alkaryl-amino derivatives of 3-hydroxy-4-pyridinones as aluminium chelating agents with potential clinical application, Journal of Inorganic Biochemistry 97 (2003), 161-172.
12. M.T. Colomina, J.L. Roig, D.J. Sánchez and J.L. Domingo, Influence of age on aluminum-induced neurobehavioral effects and morphological changes in rat brain, NeuroToxicology 23 (2002), 775-781.
13. D.J. Connor, R.S. Jope and L.E. Harrell, Chronic, oral aluminum administration to rats: Cognition and cholinergic parameters, Pharmacology and Biochemistry of Behavior 31 (1988), 467-474.
14. D.J. Connor, L.E. Harrell and R.S. Jope, Reversal of an aluminum-induced behavioral deficit by administration of deferoxamine, Behavioral Neuroscience 103 (1989), 779-783.
15. R.R. Crichton, A. Florence and R.J. Ward, Aluminium and iron in the brain - prospects for chelation, Coordination Chemistry Reviews 228 (2002), 365-371.
16. L. Cunat, M.C. Lanhers, M. Joyeux and D. Burnel, Bioavailability and intestinal absorbtion of aluminum in rats: effects of aluminum compound and some dietary constituents, Biology of Trace Elements Research 76 (2000), 31-55.
17. R. Deloncle, F. Huguet, B. Fernandez, N. Quellard, P. Babin and O. Guillard, Ulrastructural study of rat hippocampus after chronic administration of aluminum L-glutamate: an acceleration of the aging process, Experimental Gerontology 36 (2001), 231-244.
18. M. Demircan, O. Ergun, C. Coker, F. Yilmaz, S. Avanoglu and G. Okuz, Aluminum in total parenteral nutrition solutions produces portal inflammation in rats, The Journal of Pediatric Gastroenterology and Nutrition 26 (1998), 274-278.
19. V.H. Denenberg, Open-field behavior in the rat: What does it mean? in: Experimental approaches to the study of emotional behavior, Annals of the New York Academy of Sciences, New York, 1969, pp. 852-859.
20. G.L. Eichorn, Aging, genetics, and the environment: Potential of errors introduced into genetic information transfer by metal ions, Mechanisms of Ageing and Development 9 (1979), 291-301.
21. C. Exley, A molecular mechanism of aluminium-induced Alzheimer's disease? Journal of Inorganic Biochemistry 76 (1999), 133-140.
22. M. Farina, F.S. Lara, R. Brandao, R. Jacques and J.B.T. Rocha, Effects of aluminum sulfate on erythropoiesis in rats, Toxicology Letters 132 (2002), 131-139.
23. M. Favarato, P. Zatta, M. Perazzolo, L. Fontana and M. Nicolini, Aluminum(III) influences the permeability of the blood-brain barrier to [14C] sucrose in rats, Brain Research 569 (1992), 330-335.
24. M. Fechheimer, R. Furukawa, A. Maselli and R.C. Davis, Hirano bodies in health and disease, Trends in Molecular Medicine 8 (2002), 590-591.
25. T.P. Flaten, Aluminium as a risk factor in Alzheimer's disease, with emphasis on drinking water, Brain research Bulletin 55 (2001), 187-196.
26. A.L. Florence, A. Gauthier, C. Ponsar, P. Van den Bosch de Aguilar and R.R. Crichton, An animal experimental model of aluminium overload, Neurodegeneration 3 (1994), 315-323.
27. J.F. Foncin, Alzheimer's disease and aluminium, Nature 326 (1987), 136.
28. B. Fulton and E.H. Jeffery, Heme oxygenase induction. A possible factor in aluminum-associated anemia, Biology of Trace Elements Research 40 (1994), 9-19.
29. G. Garbossa, A. Gutnisky and A. Nesse, Depressed erythroid progenitor cell activity in aluminum-overloaded mice, Mineral Electrolyte and Metabolism 22 (1996), 214-218.
30. M. Gearing, G.W. Rebeck, B.T. Hyman, J. Tigges and S.S. Mirra, Neuropathology and apolipoprotein E profile of aged chimpanzees: implications for Alzheimer disease, Proceedings of the National Academy of Sciences USA 91 (1994), 9382-9386.
31. O. Ghribi, M.M. Herman, M.S. Forbes, D.A. DeWitt and J. Savory, GDNF protects against aluminum-induced apoptosis in rabbits by upregulating Bcl-2 and Bcl-xL and inhibiting mitochondrial Bax translocation, Neurobiology of Disease 8 (2001), 764-773.
32. O. Ghribi, D.A. DeWitt, M.S. Forbes, M.M. Herman and J. Savory, Co-involvement of mitochondria and endoplasmic reticulum in regulation of apoptosis: changes in cytochrome c, Bcl-2 and Bax in the hippocampus of aluminum-treated rabbits, Brain Research 903 (2001), 66-73.
33. O. Ghribi, M.M. Herman and J. Savory, The endoplasmic reticulum is the main site for caspase-3 activation following aluminum-induced neurotoxicity in rabbit hippocampus, Neuroscience Letters 324 (2002), 217-221.
34. M.S. Golub and R.P. Tarara, Morphometric studies of myelination in the spinal cord of mice exposed developmentally to aluminum, Neurotoxicology 20 (1999), 953-999.
35. M. Gómez, D.J. Sánchez, J.M. Lobet, J. Corbella and J.L. Domingo, The effect of age on aluminum retention in rats, Toxicology 116 (1997), 1-8.
36. M. Gómez, D.J. Sánchez, J.M. Lobet, J. Corbella and J.L. Domingo, Concentrations of some essential elements in the brain of aluminum-exposed rats in relation to the age of exposure, Archives of Gerontology and Geriatrics 24 (1997), 287-294.
37. T. Gotow, J. Tanaka and M. Takeda, The organization of neurofilaments accumulated in perikaryon following aluminum administration: relationshi between structure and phosphorilation of neurofilaments, Neuroscience 64 (1995), 553-569.
38. W.R. Harris, G. Berthon, J.P. Day, C. Exley, T.P. Flaten, W.F. Forbes, T. Kiss, C. Orvig and P.F. Zatta, Speciation of aluminum in biological systems, Journal of Toxicology and Environmental Health 48 (1996), 543-568.
39. A. Hirano, Hirano bodies and related neuronal inclusions, Neuropathology and applied Neurobiology 20 (1994), 3-11.
40. A.Y. Jeantet, C. Ballan-Dufrancais, C. Petter and M. Truchet, Mechanisms of cellular detoxication, nuclear aluminum concentration and hepatocyte protection after experimental overload in rats, Comptes Rendus de l'Academie des Sciences III 315 (1992), 379-386.
41. D. Julka and K.D. Gill, Effect of aluminum on regional brain antioxidant defense status in Wistar rats, Research in Experimental Medicine 196 (1996), 187-194.
42. D. Julka and K.D. Gill, Altered calcium homeostasis: a possible mechanism of aluminium-induced neurotoxocity, Biochimica and Biophysica Acta 1315 (1996), 47-54.
43. B.L. Kagan, Y. Hirakura, R. Azimov, R. Azimova and M.-C. Lin, The channel hypothesis of Alzheimer's disease: current status, Peptides 23 (2002), 1311-1315.
44. K. Kanaya, N. Baba, M. Naka and H. Mori, The digital structural analysis of helical hirano bodies obtained by electron microscopy, Micron and Microscopica Acta 18 (1987), 131-146.
45. S.J. Karlik and G.L. Eichorn, Polynuclotide cross-linking by aluminium, Journal of Inorganic Biochemistry 37 (1989), 259-269.
46. I. Klatzo, H.M. Wisniewski and E. Streicher, Experimental production of neurofibrillary degeneration, Journal of Neuropathology and Experimental Neurology 24 (1965), 187-199.
47. G.L. Klein, T.C. Lee, P.A. Mann, N.L. Miller and A.C. Alfrey, Effects of aluminum on the liver following high-dose enteral administration to rats, The Journal of Pediatric Gastroenterology and Nutrition 9 (1989), 105-107.
48. B. Lal, A. Gupta, R. Murthy, M.A. Mohd and S. Chandra, Aluminum ingestion alters behavior and some neurochemicals in rats, Life Sciences 42 (1993), 863-875.
49. C.N. Martyn, The epidemiology of Alzheimer's disease in relation to aluminium, Ciba Foundation Symposiums 169 (1992), 79-86.
50. C.N. Martyn, D.J. Barker, C. Osmond, E.C. Harris, J.A. Edwardson and R.F. Lacey, Geographical relation between Alzheimer's disease and aluminum in drinking water, Lancet 1 (1989), 59-62.
51. D.R. McLachlan, A.J. Dalton, T.P. Kruck, M.Y. Bell, W.L. Smith, W. Kalow and D.F. Andrews, Intramuscular desferrioxamine in patients with Alzheimer's disease, The Lancet 337 (1991), 1304-1308.
52. D.R. McLachlan, C. Bergeron, J.E. Smith, D. Boomer and S.L. Rifat, Risk for neuropathologically confirmed Alzheimer's disease and residual aluminum in municipal drinking water employing weighted residential histories, Neurology 46 (1996), 401-405.
53. P. Mecocci, M.F. Beal, R. Cecchetti, M.C. Polidori, A. Cherubini, F. Chionne, L. Avellini, G. Romano and U. Senin, Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain, Molecular and Chemical Neuropathology 31 (1997), 53-64.
54. A.C. Miu, C.E. Andreescu, R. Vasiu and A.I. Olteanu, A behavioral and histological study of the effects of long-term exposure of adult rats to aluminum, International Journal of Neuroscience 113 (2003), 1197-1211.
55. A.C. Miu, R.I. Medrea, C.E. Andreescu, C.I. Stancu, N. Vlasie and A.I. Olteanu, Impaired recognition memory and emotional reactivity associated to loss of cortical integrity in rats after chronic exposure to aluminium, Cognition, Brain, Behavior 7 (2003), 219-234.
56. T.J. Neiva, D.M. Fries, H.P. Monteiro, E.A. D'Amico and D.A. Chamone, Aluminum induces lipid peroxidation and aggregation of human blood platelets, Brazilian Journal of Medical and Biological Research 30 (1997), 599-604.
57. P.E. Newman, Alzheimer's disease revisited, Medical Hypotheses 54 (2000), 774-776.
58. J. Nilsen and R.D. Brinton, Mechanisms of estrogen-mediated neuroprotection: Regulation of mitochondrial calcium and Bcl-2 expression, Proceedings of the National Academy of Science USA 100 (2003), 2842-2847.
59. C. Nordstedt, S.L. Gandy, I. Alafuzoff, G.L. Caporaso, K. Iverfeldt, J.A. Grebb, B. Windblad and P. Greengard, Alzheimer beta/A4 amyloid precursor protein in human brain: Aging-associated increases in holoprotein and in a proteolytic fragment, Proceedings of the National Academy of Sciences USA 88 (1991), 8910-8914.
60. B. Platt, G. Fiddler, G. Riedel and Z. Henderson, Aluminium toxicity in the rat brain: Histochemical and immunocytochemical evidence, Brain Research Bulletin 55 (2001), 257-267.
61. J.K. Rao, C.D. Katsetos, M.M. Herman and J. Savory, Experimental aluminum encephalomyelopathy. Relationship to human neurodegenerative disease, Clinical and Laboratory Medicine 18 (1998), 697-698.
62. E. Reusche, P. Pilz, G. Oberascher, B. Lindner, R. Egensperger, K. Gloeckner, E. Trinka and B. Iglseder, Subacute fatal aluminum encephalopathy after reconstructive otoneurosurgery: A case report, Human Pathology 32 (2001), 1136-1140.
63. M.A.M. Rogers and D.G. Simon, A preliminary study of dietary aluminium intake and risk of Alzheimer's disease, Age and Ageing 28 (1999), 205-209.
64. A.J. Roskams and J.R. Connor, Aluminum access to the brain: a role for tranferrin and its receptors, Proceedings of the National Academy of Sciences USA 87 (1990), 9024-9027.
65. J. Savory, C. Exley, W.F. Forbes, Y. Huang, J.G. Joshi, T. Kruck, D.R.C. McLachlan and I. Wakayama, Can the controversy of the role of aluminum in Alzheimer's disease be resolved? What are the suggested approaches to this controversy and methodological issues to be considered? Journal of Toxicology and Environmental Health 48 (1996), 615-636.
66. J. Savory and M.M. Herman, Advances in instrumental methods for the measurement and speciation of trace metals, Annals of Clinical and Laboratory Sciences 29 (1999), 118-126.
67. J. Savory, M.M. Herman and O. Ghribi, Intracellular mechanisms underlying aluminum-induced apoptosis in rabbit brain, Journal of Inorganic Chemistry 97 (2003), 151-154.
68. R.-W. Shin, T.P.A. Kruck, H. Murayama and T. Kitamoto, A novel trivalent cation chelator Feralex dissociates binding of aluminum and iron associated with hyperphosphorilated tau of Alzheimer's disease, Brain Research 961 (2003), 139-146.
69. D.E. Smith, J. Roberts, F.H. Gage and M.H. Tuszynski, Age-associated neuronal atrophy occurs in the primate brain and is reversible by growth factor gene therapy, Proceedings of the National Academy of Sciences USA 96 (1999), 10893-10898.
70. M.A. Smith and G. Perry, What are the facts and artifacts of the pathogenesis and etiology of Alzheimer disease? Journal of Chemical Neuroanatomy 16 (1998), 35-41.
71. A.J. Spencer, J.A. Wood, H.C. Saunders, M.S. Freeman and C.J. Lote, Aluminium deposition in liver and kidney following acute intravenous administration of aluminium chloride or citrate in conscius rats, Human and Experimental Toxicology 14 (1995), 787-794.
72. A. Strunecka and J. Patocka, Reassessment of the role of aluminum in the development of Alzheimer's disease, Ceska Fysiologia 48 (1999), 9-15.
73. C. Struys-Ponsar, A. Florence, A. Gauthier, R.R. Crichton and P. Van den Bosch de Aguilar, Ultrastructural changes in brain parenchyma during normal aging and in animal models of aging, Journal of Neural Transmission 44(Suppl) (1994), 111-132.
74. C. Struys-Ponsar, A. Kerkhofs, A. Gauthier, M. Soffié and P. Van den Bosch de Aguilar, Effects of aluminum exposure on behavioral parameters in the rat, Pharmacology and Biochemistry of Behavior 56 (1997), 643-648.
75. R.D. Terry and C. Paña, Experimental production of neurofibrillary degeneration, Journal of Neuropathology and Experimental Neurology 24 (1965), 200-210.
76. B.M. Thorne, A. Cook, T. Donhoe, S. Lyon, D.N. Medeiros and C. Moutzoukis, Aluminum toxicity and behavior in the weanling long-Evans rats, Bulletin of the Psychonomic Society 25 (1987), 129-132.
77. M. Toga and J.-F. Pellisier, Apects neuropathologiques du cerveau du troisième âge, in: Le Cerveau du Troisième Âge, J. Billé, ed., Dausse, Marseille, 1974, pp. 7-28.
78. R. Torp, E. Head, N.W. Milgram, F. Hahn, O.P. Ottersen and C.W. Cotman, Ultrastructural evidence of fibrillar beta-amyloid associated with neuronal membranes in behaviorally characterized aged dog brains, Neuroscience 96 (2000), 495-506.
79. G.B. van der Voet, A.E. Brandsma, E. Heijink and F.A. Wolff, Accumulation of aluminium in rat liver: association with constituents of the cytosol, Pharmacology and Toxicology 70 (1992), 173-176.
80. S.J. van Rensburg, M.E. Carstens, F.C. Potocnik, A.K. Aucamp, J.J. Taljaard and K.R. Koch, Membrane fluidity of platelets and erythrocytes in patients with Alzheimer's disease and the effect of small amounts of aluminium on platelet and erythrocyte membranes, Neurochemistry Research 17 (1992), 825-829.
81. P.P. Varma, R. Kumar, P.K. Prasher and N.D. Roy, Hypochromic anaemia in chronic renal failure - role of aluminium, The Journal of the Association of Physicians in India 48 (2000), 549-550.
82. J.A. Varner, W.J. Horvath, C.W. Huie, H.R. Naslund and R.L. Isaacson, Chronic aluminum fluoride administration: I. Behavioral observations, Behavioral and Neural Biology 61 (1994), 233-241.
83. J.A. Varner, K.F. Jensen, W. Horvath and R.L. Isaacson, Chronic administration of aluminum-fluoride or sodium-fluoride to rats in drinking water: Alterations in neuronal and cerebrovascular integrity, Brain Research 784 (1998), 284-298.
84. V.S. Verstraeten, M.S. Golub, C.L. Keen and P.I. Oteiza, Myelin is a preferential target of aluminum-mediated oxidative damage, Archives of Biochemistry and Biophysics 344 (1997), 289-294.
85. P.R. Walker, J. LeBlanc and M. Sikorska, Effects of aluminum and other cations on the structure of brain and liver chromatin, Biochemistry 28 (1989), 3911-3915.
86. R.J. Ward, Y. Zhang and R.R. Crichton, Aluminium toxicity and iron homeostasis, Journal of Inorganic Biochemistry 87 (2001), 9-14.
87. H.M. Wisniewski and R.D. Terry, Morphology of the aging brain, human and animal, in: Neurobiological aspects of maturation and aging, D.H. Ford, ed., Elsevier, Amsterdam, 1973, pp. 167-186.
88. R.A. Yokel, V. Lidums, P.J. McNamara and U. Ungerstedt, Aluminum distribution into brain and liver of rats and rabbits following intravenous aluminum lactate or citrate: a microdyalisis study, Toxicology and Applied Farmacology 107 (1991), 153-163.
89. R.A. Yokel and J.P. O'Callaghan, An aluminum-induced increase in GFAP is attenuated by some chelators, Neurotoxicology and Teratology 20 (1998), 55-60.
90. R.A. Yokel, D.D. Allen and D.C. Ackley, The distribution of aluminum into and out of the brain, Journal of Inorganic Biochemistry 76 (1999), 127-132.
91. R.A. Yokel, M. Wilson, W.R. Harris and A.P. Halestrap, Aluminum citrate uptake by immortalized brain endothelial cells: implications for its blood-brain barrier transport, Brain Research 930 (2002), 101-110.
92. S. Yumoto, H. Nagai, M. Imamura, H. Matsuzaki, K. Hayashi, A. Masuda, H. Kumazawa, H. Ohashi and K. Kobayashi, 26Al uptake and accumulation in the brain, Nuclear Instruments and Methods in Physics Research 123 (1997), 279-182.
93. S. Yumoto, H. Nagai, H. Matsuzaki, H. Matsumura, W. Tada, E. Nagatsuma and K. Kobayashi, Aluminium incorporation into the brain of rat fetuses and sucklings, Brain Research Bulletin 55 (2001), 229-234.
94. P. Zatta, R. Lucchini, S.J. van Rensburg and A. Taylor, The role of metals in neurodegenerative processes: aluminum, manganese, and zinc, Brain Research Bulletin 62 (2003), 15-28.