Evidence for participation of aluminum in neurofibrillary tangle formation and growth in Alzheimer's disease

Journal of Alzheimer's Disease

Volumn 22, Issue 1, 2010, Pages 65-72

  Walton, J R ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Aluminum; Alzheimer's disease; hyperphosphorylated tau; neurofibrillary tangles

Indexed keywords

ALUMINUM; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ARTICLE; BRAIN CELL; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; FEMALE; HIPPOCAMPAL CA1 REGION; HUMAN; HUMAN CELL; MALE; NEUROFIBRILLARY TANGLE; NEUROFILAMENT; PRIORITY JOURNAL;

EID: 78650643641     PISSN: 13872877     EISSN: None     Source Type: Journal    
DOI: 10.3233/JAD-2010-100486     Document Type: Article

References (70)

1. Alzheimer A (1907) Ueber eine eigenartige Erkrankung der Hirnrinde. Zentralbl Nervenheit Psychiatr 30, 177-179.
2. Alzheimer's Disease International. World Alzheimer Report Eds. Price M, Jackson J. http://www.alz.co.uk/research/files/World%20Alzheimer%20Report.pdf, Accessed on 14 April 2010.
3. Henderson AS (1986) The epidemiology of Alzheimer's disease. Br Med Bull 42, 3-10.
4. Raiha I, Kaprio J, Koskenvuo M, Rajala T, Sourander L (1996) Alzheimer's disease in Finnish twins. Lancet 347, 573-578.
5. Savva GM, Wharton SB, Ince PG, Forster G, Matthews FE, Brayne C (2009) Age, neuropathology, and dementia. New Engl J Med 360, 2302-2309.
6. Alzheimer A (1911) Uber eigenartige Krankheitsfalle des spateren Alters. Z Neurol Psychiatr 4, 356-385.
7. Bancher C, Brunner C, Lassmann H, Budka H, Jellinger K, Seitelberger F, Grundke-Iqbal I, Iqbal K, Wisniewski HM (1989) Accumulation of abnormally phosphorylated tau precedes the formation of neurofibrillary tangles in Alzheimer's disease. Brain Res 477, 90-99.
8. Bancher C, Grundke-Iqbal I, Iqbal K, Fried VA, Smith HT, Wisniewski HM (1991) Abnormal phosphorylation of tau precedes ubiquitination in neurofibrillary pathology of Alzheimer disease. Brain Res 539, 11-18.
9. Wischik CM, Novak M, Edwards PC, Klug A, Tichelaar W, Crowther RA (1988) Structural characterization of the core of the paired helical filament of Alzheimer's disease. Proc Natl Acad Sci USA 85, 4506-4510.
10. Wischik CM, Crowther RA, Stewart M, Roth M (1985) Sub-unit structure of paired helical filaments in Alzheimer's disease. J Cell Biol 100, 1905-1912.
11. Miyasaka T, Watanabe A, Saito Y, Murayama S, Mann DM, Yamazaki M, Ravid R, Morishima-Kawashima M, Nagashima K, Ihara Y (2005) Visualization of newly deposited tau in neurofibrillary tangles and neuropil threads. J Neuropathol Exp Neurol 64, 665-674.
12. Walton JR (2006) Aluminum accumulation in hippocampal neurons from Alzheimer cases and aged controls. Neurotoxi-cology 27, 385-394.
13. Murayama H, Shin R-W, Higuchi J, Shibuya S, Muramoto T, Kitamoto T (1999) Interaction of aluminum with PHFT in Alzheimer's disease neurofibrillary degeneration evidenced by desferrioxamine-assisted chelating autoclave method. Am J Pathol 155, 877-885.
14. Solomon B (2001) Calmodulin, aluminium and Alzheimer's disease. In Aluminium and Alzheimer's Disease: The Science that Describes the Link, Exley C, ed. Elsevier Science BV, Amsterdam, pp. 393-409.
15. Perl DP, Brody AR (1980) Alzheimer's disease: X-ray spec-trometric evidence of aluminum accumulation in neurofibril-lary tangle-bearing neurons. Science 208, 297-299.
16. Good PF, Perl DP, Bierer LM, Schmeidler J (1992) Selective accumulation of aluminum and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study. Ann Neurol 31, 286-292.
17. Mirra SS, Heyman A, McKeel D, Sumi SM, Crain BJ, Brown-lee LM, Vogel FS, Hughes JP, van Belle G, Berg L (1991) The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology 41, 479-486.
18. Walton JR (2007) An aluminum-based rat model for Alzheimer's disease exhibits oxidative damage, inhibition of PP2A activity, hyperphosphorylated tau, and granulovacuolar degeneration. J Inorg Biochem 101, 1275-1284.
19. Walton JR (2004) A bright field/fluorescent stain for aluminum: its specificity, validation, and staining characteristics. Biotech Histochem 79, 169-176.
20. Walton JR (2009) Functional impairment in aged rats chronically exposed to human range dietary aluminum equivalents. Neurotoxicology 30, 182-193.
21. Walton JR (2009) Brain lesions comprised of aluminum-rich cells that lack microtubules may be associated with the cognitive deficit of Alzheimer's disease. Neurotoxicology 30, 10591069.
22. Lapham LW, Johnstone MA, Brundjar KH (1964) A new paraffin method for the combined staining of myelin and glial fibers. J Neuropathol Exp Neurol 23, 156-160.
23. Verstraeten SV, Golub MS, Keen CL, Oteiza PI (1997) Myelin is a preferential target of aluminum-mediated oxidative damage. Arch Biochem Biophys 344, 289-294.
24. Itoh M, Suzuki Y, Sugai K, Ozuka N, Ohsawa M, Otsuki T, Goto Y (2008) Progressive leukoencephalopathy associated with aluminum deposits in myelin sheath. J Child Neurol 23, 938-943.
25. Golub MS, Tarara RP (1999) Morphometric studies of myeli-nation in the spinal cord of mice exposed developmentally to aluminum. Neurotoxicology 20, 953-959.
26. Deloncle R, Huguet F, Fernandez B, Quellard N, Babin P, Guillard O (2001) Ultrastructural study of rat hippocampus after chronic administration of aluminum L-glutamate: an acceleration of the aging process. Exp Gerontol 36, 231-244.
27. Greger JL, Sutherland JE (1997) Aluminum exposure and metabolism. Crit Rev Clin Lab Sci 34, 439-474.
28. Yokel RA (2000) The toxicology of aluminum in the brain: a review. Neurotoxicology 21, 813-828.
29. McDermott JR, Smith AI, Iqbal K, Wisniewski HM (1979) Brain aluminum in aging and Alzheimer disease. Neurology 29, 809-814.
30. Markesbery WR, Ehmann WD, Alauddin M, Goodin DT (1984) Brain trace element concentrations in aging. Neurobiol Aging 5, 19-28.
31. Shimizu H, Mori T, Koama M, Sekiya M, Ooami H (1994) A correlative study of the aluminum content and aging changes of the brain in non-demented elderly subjects. Nippon Ronen Igakkai Zasshi - Jap J Geriatr (Tokyo) 31, 950-960.
32. Krishnan SS, McLachlan DR, Krishnan B, Fenton SSA, Harrison JE (1988) Aluminum toxicity to the brain. Sci Total Environ 71, 59-64.
33. McLachlan DRC (1995) Aluminium and the risk for Alzheimer's disease. Environmetrics 6, 233-275.
34. Bondy SC (2010) The neurotoxicity of environmental aluminum is still an issue. Neurotoxicology 31, 575-581.
35. Edwardson JA, Candy JM, Ince PG, McArthur FK, Morris CM, Oakley AE, Taylor GA, Bjertness E (1992) Aluminium accumulation, β-amyloid deposition and neurofibrillary changes in the central nervous system. In Aluminium in Biology and Medicine. Wiley, Chichester. CIBA Found Symp 169, 165-185.
36. Morris CM, Candy JM, Oakley AE, Taylor GA, Mountfort S, Bishop H, Ward MK, Bloxham CA, Edwardson JA (1989) Comparison of the regional distribution of transferrin receptors and aluminium in the forebrain of chronic renal dialysis patients. J Neurol Sci 94, 295-306. (Pubitemid 20019465)
37. Harrington CR, Wischik CM, McArthur FK, Taylor GA, Edwardson JA, Candy JM (1994) Alzheimer's-disease-like changes in tau protein processing: association with aluminium accumulation in brains of renal dialysis patients. Lancet 343, 993-997.
38. Kowall NW, Pendlebury WW, Kessler JB, Perl DP, Beal MF (1989) Aluminum-induced neurofibrillary degeneration affects a subset of neurons in rabbit cerebral cortex, basal fore-brain and upper brainstem. Neuroscience 29, 329-337.
39. Gong C-X, Shaikh S, Wang JZ, Zaidi T, Grundke-Iqbal I, Iqbal K (1995) Phosphatase activity toward abnormally phosphory-lated T : decrease in Alzheimer disease brain. J Neurochem 65, 732-738.
40. Goedert M, Jakes R, Qi Z, Wang JH, Cohen P (1995) Protein phosphatase 2A is the major enzyme in brain that dephospho-rylates T protein phosphorylated by proline-directed protein kinases or cyclic AMP-dependent protein kinase. J Neurochem 65, 2804-2807.
41. Gong C-X, Lidsky T, Wegiel J, Zuck L, Grundke-Iqbal I, Iqbal K (2000) Phosphorylation of microtubule-associated protein tau is regulated by protein phosphatase 2A in mammalian brain. Implications for neurofibrillary degeneration in Alzheimer's disease. J Biol Chem 275, 5535-5544.
42. Vogelsberg-RagagliaV, SchuckT, Trojanowski JQ, Lee VM-Y (2001) PP2A mRNA expression is quantitatively decreased in Alzheimer's disease hippocampus. Exp Neurol 168, 402-412.
43. Sontag E, Luangpirom A, Hladik C, Mudrak I, Ogris E, Spe-ciale S, White CL 3rd (2004) Altered expression levels of the protein phosphatase 2A ABalphaC enzyme are associated with Alzheimer disease pathology. J Neuropathol Exp Neurol 63, 287-301.
44. Shin R-W, Iwaki T, Kitamoto T, Sato Y, Tateishi J (1992) Massive accumulation ofmodified tau and severe depletion of normal tau characterize the cerebral cortex and white matter of Alzheimer's disease. Am J Pathol 140, 937-945.
45. Liu F, Liang Z, Gong CX (2006) Hyperphosphorylation oftau and protein phosphatases in Alzheimer disease. Panminerva Med 48, 97-108.
46. Yamamoto H, Saitoh Y, Yasugawa S, Miyamoto E (1990) Dephosphorylation of tau factor by protein phosphatase 2A in synaptosomal cytosol fractions, and inhibition by aluminum. J Neurochem 55, 683-690.
47. Walton JR (2007) A longitudinal study of rats chronically exposed to aluminum at human dietary levels. Neurosci Lett 412, 29-33.
48. Jones KR, Oorschot DE (1998) Do aluminium and/or gluta-mate induce Alz-50 reactivity? A light microscopic immuno-histochemical study. JNeurocytol 27, 57-57.
49. Mesco ER, Kachen C, Timiras PS (1991) Effects of aluminum on tau proteins in neuroblastoma cells. Mol Chem Neuropathol 14, 199-212.
50. Guillozet-Bongaarts AL, Garcia-Sierra F, Reynolds MR, Horowitz PM, Fu Y, Wang T, Cahill ME, Bigio EH, Berry RW, Binder LI (2005) Tau truncation during neurofibrillary tangle evolution in Alzheimer's disease. Neurobiol Aging 26, 1015-1022.
51. Yang S-J, Lee JE, Lee KW, Huh J-W, Choi SY, Cho S-W (2004) Opposed regulation ofaluminum-induced apoptosis by glial cell line-derived neurotrophic factor and brain-derived neurotrophic factor in rat brains. Mol Brain Res 127, 146-149.
52. Ghribi O, Herman MM, Forbes MS, DeWitt DA, Savory J (2001) GDNF protects against aluminum-induced apoptosis in rabbits by upregulating Bcl-2 and Bcl-XL and inhibiting mitochondrial Bax translocation. Neurobiol Dis 8, 764-773.
53. Savory J, Herman MM, Ghribi O (2003) Intracellular mechanisms underlying aluminum-induced apoptosis in rabbit brain. J Inorg Biochem 97, 151-154.
54. Johnson VJ, Sang-Hyun Kim S-H, Sharma RP (2005) Aluminum-maltolate induces apoptosis and necrosis in Neuro-2a Cells: Potential role for p53 signaling. Toxicol Sci 83, 329-339.
55. de Calignon A, Fox LM, Pitstick R, Carlson GA, Bacskai BJ, Spires-Jones TL, Hyman BT (2010) Caspase activation precedes and leads to tangles. Nature 464, 1201-1203.
56. Mena R, Edwards PC, Harrington CR, Mukaetova-Ladinska EB, Wischik CM (1996) Staging the pathological assembly of truncated tau protein into paired helical filaments in Alzheimer's disease. Acta Neuropathol 91, 633-641.
57. Birchall JD, Chappell JS (1988) Aluminium, chemical physiology, and Alzheimer's disease. Lancet 332, 1008-1010.
58. Haug A, Vitorello V (1996) Aluminum coordination to calmodulin: thermodynamic and kinetic aspects. Coord Chem Rev 140, 113-124.
59. Shin RW, Lee VM, Trojanowski JQ (1994) Aluminum modifies the properties of Alzheimer's disease PHF tau proteins in vivo and in vitro. J Neurosci 14, 7221-7233.
60. Madhav TR, Vatsala S, Ramakrishna T, Ramesh J, Easwaran KRK (1996) Preservation of native conformation during aluminium-induced aggregation of tau protein. NeuroReport 7, 1072-1076.
61. Savory J, Huang Y, Wills MR, Herman MM (1998) Reversal by desferrioxamine of tau protein aggregates following two days of treatment in aluminum-induced neurofibrillary degeneration in rabbit: implications for clinical trials in Alzheimer's disease. Neurotoxicology 19, 209-214.
62. Nixon RA, Clarke JF, Logvinenko KB, Tan MK, Hoult M, Grynspan F (1990) Aluminum inhibits calpain-mediated pro-teolysis and induces human neurofilament proteins to form protease-resistant high molecular weight complexes. J Neu-rochem 55, 1950-1959.
63. Leterrier JF, Langui D, Probst A, Ulrich J (1992) A molecular mechanism for the induction of neurofilament bundling by aluminum ions. J Neurochem 58, 2060-2070.
64. Shea TB (1995) Calcium modulates aluminum neurotoxicity and interaction with neurofilaments. Mol Chem Neuropathol 24, 151-163.
65. Strong MJ, Garruto RM (1991) Chronic aluminum-induced motor neuron degeneration: clinical, neuropathological and molecular biological aspects. Can J Neurol Sci 18(Suppl 3), 428-431.
66. Lee H-G, Perry G, Moreira PI, Garrett MR, Liu Q, Zhu X, Takeda A, Nunomura A, Smith MA (2005) Tau phosphoryla-tion in Alzheimer's diseaes: pathogen or protector? TrendsMol Med 11,164-169.
67. Iqbal K, Alonso A del C, Grundke-Iqbal, I (2008) Cytoso-lic abnormally hyperphosphorylated tau but not paired heli-cal filaments sequester normal MAPs and inhibit microtubule assembly. J Alzheimers Dis 14, 365-370.
68. Exley C (2004) The pro-oxidant activity of aluminum. Free RadicBiolMed36, 380-387.
69. Karlik SJ, Eichhorn GL, Lewis PN, Crapper DR (1980) Interaction of aluminum species with deoxyribonucleic acid. Biochem 19, 5991-5998.
70. Crapper McLachlan DR, Lukiw WJ, Kruck TPA (1989) New evidence for an active role of aluminum in Alzheimer's disease. Can J Neurol Sci 16, 490-497.