A new insight on Al-maltolate-treated aged rabbit as Alzheimer's animal model

Brain Research Reviews

Volumn 52, Issue 2, 2006, Pages 275-292

  Bharathi, ^a   Shamasundar, N M ^b   Sathyanarayana Rao, T S ^b   Dhanunjaya Naidu, M ^c   Ravid, R ^d   Rao, K S J ^a  

^a CENTRAL FOOD TECHNOLOGICAL RESEARCH INSTITUTE   (India)

^b JSS MEDICAL COLLEGE   (India)

^c SRI VENKATESWARA UNIVERSITY   (India)

^d NETHERLANDS BRAIN BANK   (Netherlands)

Author keywords

A deposition; Aged rabbit; Al maltolate; Alzheimer's disease; Apoptosis; Neurofibrillary tangle; Oxidative stress

Indexed keywords

ALUMINUM MALTOL; AMYLOID BETA PROTEIN; DEXTRO ASPARTIC ACID; IRON; N ACETYLASPARTIC ACID; N ACETYLASPARTYLGLUTAMIC ACID; TAU PROTEIN;

AGING; ALZHEIMER DISEASE; APOPTOSIS; BEHAVIOR CHANGE; BIOCHEMISTRY; COMPARATIVE STUDY; DEGENERATIVE DISEASE; DISEASE PREDISPOSITION; ENDOPLASMIC RETICULUM; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MITOCHONDRION; NERVE DEGENERATION; NEUROANATOMY; NEUROCHEMISTRY; NEUROFILAMENT; NEUROPATHOLOGY; NONHUMAN; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PATHOLOGY; PRIORITY JOURNAL; RABBIT; REVIEW;

AGE FACTORS; AGING; ALZHEIMER DISEASE; ANIMALS; BRAIN; DISEASE MODELS, ANIMAL; FEMALE; HUMANS; NERVE DEGENERATION; NEUROFIBRILLARY TANGLES; NEURONS; NEUROTOXINS; ORGANOMETALLIC COMPOUNDS; OXIDATIVE STRESS; PYRONES; RABBITS; SENILE PLAQUES;

EID: 33748696860     PISSN: 01650173     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresrev.2006.04.003     Document Type: Review

References (168)

1. Aarsland D., Cummings J.L., and Larsen J.P. Neuropsychiatric differences between Parkinson's disease with dementia and Alzheimer's disease. Int. J. Geriatr. Psychiatry 16 (2001) 184-191
2. Adams J.M., and Cory S. The Bcl-2 protein family arbiters of cell survival. Science 281 (1998) 1322-1326
3. Anitha S., Rao K.S.J., Latha K.S., and Viswamitra M.A. First evidence to show the topological change of DNA from B-DNA to Z-DNA conformation in the hippocampus of Alzheimer's brain. Neuromol. Med. 2 (2002) 289-297
4. Baddeley A.D., Bressi S., Sala S.D., Logie R., and Spinnler H. The decline of working memory in Alzheimer's disease. A longitudinal study. Brain 6 (1991) 2521-2542
5. Bartus R.T. On neurodegenerative diseases, models and treatment strategies: lessons learned and lessons forgotten a generation following the cholinergic hypothesis. Exp. Neurol. 163 (2000) 495-529
6. Beal M.F., Mazurek M.F., Ellison D.W., Kowall N.W., Solomon P.R., and Pendlebury W.W. Neurochemical characteristics of aluminum-induced neurofibrillary degeneration in rabbits. Neuroscience 29 (1989) 339-346
7. Bertholf R.L., Nicholson J.R.P., Wills M.R., and Savory J. Measurement of lipid peroxidation products in rabbit brain and organs (response to aluminium exposure). Ann. Clin. Lab. Sci. 17 (1987) 418-423
8. Binder L.I., Frankfurter A., and Rebhun L.I. The distribution of tau in the mammalian central nervous system. J. Cell Biol. 101 (1985) 1371-1378
9. Bishop G.M., and Robinson S.R. β-Amyloid helps to protect neurons against oxidative stress. Neurobiol. Aging Suppl. 21 (2000) S226
10. Brining S.K., Jones C.R., and Chang M.C. Effects of chronic beta-amyloid treatment on fatty acid incorporation into rat brain. Neurobiol. Aging 17 (1996) 301-310
11. Campbell A., Yang E.Y., Tsai-Turton M., and Bondy S.C. Pro-inflammatory effects of aluminum in human glioblastoma cells. Brain Res. 933 (2002) 60-65
12. Carpenter A.F., Carpenter P.W., and Markesberry W.R. Morphometric analyses of microglia in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 52 (1993) 601-608
13. Chafi A.H., Hauw J.-J., Rancurel G., Berry J.P., and Galle C. Absence of aluminium in Alzheimer's disease brain tissue: electron microprobe and ion microprobe studies. Neurosci. Lett. 123 (1991) 61-64
14. 1H] Propionyl-Neuropeptide Y (NPY) binding in rabbit aortic membranes: comparisons with binding in rat brain and biological responses in rat vas deferens. Biochem. Biophys. Res. Commun. 151 (1998) 1213-1219
15. Clark R.E., and Squire L.R. Classical conditioning and brain systems: the role of awareness. Science 280 (1998) 77-81
16. Colangelo V., Schurr J., Ball M.J., Pelaez R.P., Bazan N.G., and Lukiw W.J. Gene expression profiling of 12633 genes in Alzheimer hippocampal CA1: transcription and neurotrophic factor down-regulation and upregulation of apoptotic and pro-inflammatory signaling. J. Neurosci. Res. 70 (2002) 462-473
17. Coleman, and Greenberg. Animal model for Alzheimer's disease. Neurobiol. Aging 17 (1996) 1-2
18. Corain B., Abdiqqfrar Osman A., Bertani R., Tapparo A., Zatta P.F., and Bombi G.G. The aqueous solution state of α-hydroxocarboxylate complexes of aluminium (III): an IR and NMR approach. Life Sci. Report. 11 (1994) 103-109
19. Crapper D.R., and Dalton A.J. Alterations in short-term retention, conditioned avoidance response acquisition and motivation following aluminium induced neurofibrillary degeneration. Physiol. Behav. 10 (1973) 925-933
20. Crapper D.R., Krishnan S.S., and Dalton A.J. Brain aluminium distribution in Alzheimer's disease and experimental neurofibrillary degeneration. Science 180 (1973) 511-513
21. Cummings J.L. Cognitive and behavioral heterogeneity in Alzheimer's disease, seeking the neurobiological basis. Neurobiol. Aging 21 (2000) 345-361
22. Dai J., Buijs R.M., Kamphorst W., and Swaab D.F. Impaired axonal transport of cortical neurons in Alzheimer's disease is associated with neuropathological changes. Brain Res. 948 (2002) 138-144
23. Dale G.E., Leigh P.N., Luthert P., Anderton B.H., and Roberts G.W. Neurofibrillary tangles in dementia pugilistica are ubiquitinated. J. Neurol., Neurosurg. Psychiatry 54 (1991) 116-118
24. Demircan M., Ergun O., Coker C., Avanoglu S., and Ozok G. Aluminium in total parenteral nutrition solutions produces portal inflammation in rats. J. Pediatr. Gastroenterol. Nutr. 26 (1998) 274-278
25. D'mello S.R., Anelli R., and Calissano P. Induction of apoptosis in immature granule cells but promotes survival of mature neurons. Exp. Cell Res. 211 (1994) 232-238
26. Doll R. Alzheimer's disease and environmental aluminium. Age Ageing 22 (1993) 138-153
27. Dollken V. Uber die Wirkung des Aluminium mit besbonderer Berucksichtigung der durch das Aluminium verusachten lasionen im Zentralnervensystem. Arch. Exp. Pathol. (1897) 98-120
28. Eichenbaum H. Conscious awareness, memory and the hippocampus. Nat. Neurosci. 2 (1999) 775-776
29. 2+ ions. J. Cell Biol. 143 (1998) 217-224
30. Finneagan M.M., Rettig S., and Orvig C.A. A neutral water soluble aluminium complex of neurological interest. J. Am. Chem. Soc. 108 (1986) 5033-5035
31. Fontana L., Perazzolo M., Stella M.P., Tapparo A., Corain B., Favarato M., and Zatta P. A long term toxicological investigation on the effect of tris(maltolate) aluminium (III) in rabbits. Biol. Trace Elem. Res. 2 (1991) 183-191
32. Games D., Adams R., Alesandrini R., Barbour R., Berthelette P., Blackwell C., Carr T., Clemens J., Donaldson T., and Gillespie F. Alzheimer's-type neuropathology in transgenic mice overexpressing V71F beta amyloid precursor protein. Nature 373 (1995) 523-527
33. Garruto R.M. Pacific paradigms of environmentally-induced neurological disorders: clinical, epidemiological and molecular perspectives. Neurotoxicology 12 (1991) 347-377
34. Garruto R.M., Fukatsu R., Yanagihara R., Gajdusek D.C., Hook G., and Fiori C.E. Imaging of calcium and aluminium in neurofibrillary tangle-bearing neurons in parkinsonism dementia of Guam. Proc. Natl. Acad. Sci. U. S. A. 81 (1984) 1875-1879
35. Garruto R.M., Yanagihara R., Shankar S.K., Wolff A., Salazar A.M., and Amyx H.L. Experimental models of metal-induced neurofibrillary degeneration. In: Tsubaki T., and Yase Y. (Eds). Amyotrophic Lateral Sclerosis (1988), Elsevier, Amsterdam 41-50
36. Gerald C., Walker M.W., and Cyisolone L. A receptor subtype involved in neuropeptide Y-induced food Intake. Nature 382 (1996) 162-171
37. Germano C., and Kinsella G.J. Working memory and learning in early Alzheimer's disease. Neuropsychol. Rev. 15 (2005) 1-10
38. Geula C., Wu C.K., Saroff D., Lorenzo A., Yuan M., and Yankner B.A. Aging renders the brain vulnerable to amyloid β-protein neurotoxicity. Nat. Med. 4 (1998) 827-831
39. Ghribi O., Herman M.M., Forbes M.S., DeWitt D.A., and Savory J. GDNF protects against aluminum-induced apoptosis in rabbits by upregulating Bcl-2 and Bcl-XL and inhibiting mitochondrial Bax translocation. Neurobiol. Dis. 5 (2001) 764-773
40. Ghribi O., Dewitt D.A., Forbes M.S., Herman M.M., and Savory J. Co-involvement of mitochondria and endoplasmic reticulum in regulation of apoptosis: changes in cytochrome-c, Bcl-2 and Bax in the hippocampus of aluminium treated rabbits. Brain Res. 8 (2001) 66-73
41. Ghribi O., Dewitt D.A., Forbes M.S., Arad A., Herman M.M., and Savory J. Cyclosporin A inhibits Al-induced cytochrome c release from mitochondria in aged rabbits. J. Alzheimer's Dis. 3 (2001) 387-391
42. Ghribi O., Herman M.M., Dewitt D.A., Forbes M.S., and Savory J. Abeta (1-42) and aluminium induce stress in the endoplasmic reticulum in rabbit hippocampus, involving nuclear translocation of gadd 153 and NF-kappa B. Brain Res. Mol. Brain Res. 96 (2001) 30-38
43. Ghribi O., Herman M.M., and Savory J. The endoplasmic reticulum is the main site for caspase activation following aluminium-induced neurotoxicity in rabbit hippocampus. Neurosci. Lett. 324 (2002) 217-221
44. Ghribi O., Herman M.M., Spaulding N.K., and Savory J. Lithium inhibits aluminium induced apoptosis in rabbit hippocampus, by preventing cytochrome c translocation, Bcl-2 decrease, Bax elevation and caspase-3 activation. J. Neurochem. 82 (2002) 137-145
45. Ghribi O., Herman M.M., and Savory J. Lithium inhibits abeta-induced stress in endoplasmic reticulum of rabbit hippocampus but does not prevent oxidative damage and tau phosphorylation. J. Neurosci. Res. 71 (2003) 853-862
46. Gibson G.E., and Peterson C. Aging decreases oxidative metabolism and the release and synthesis of acetylcholine. J. Neurochem. 37 (1981) 978-984
47. Gomez-Isla T., Hollister R., West H., Mui S., Growdon J.H., Petersen R.C., Parisi J.E., and Hyman B.T. Neuronal loss correlates with but exceeds neurofibrillary tangles in Alzheimer's disease. Ann. Neurol. 41 (1997) 17-24
48. Gong Q., Wu H., Q., Huang X.N., Sun A.S., and Shi J.S. Protective effects of Ginkgo biloba leaf extract on aluminium-induced brain dysfunction in rats. Life Sci. 77 (2005) 140-148
49. Good P.F., and Perl D.P. Aluminium in Alzheimer's?. Nature 362 (1993) 418
50. Good P.F., Perl D.P., Bierer L.M., and Schmeidler J. Selective accumulation of aluminium and iron in the neurofibrillary tangles of Alzheimer's disease: a laser microprobe (LAMMA) study. Ann. Neurol. 31 (1992) 286-292
51. Good P.F., Werner P., Hsu A., Olanow C.W., and Perl D.P. Evidence for neuronal oxidative damage in Alzheimer's disease. Am. J. Pathol. 140 (1996) 621-628
52. Gormezano I. Classical conditioning. In: Sidowski J.B. (Ed). Experimental Methods and Instrumentation in Psychology (1996), McGraw Hill, New York 385-420
53. Graur D., Duret L., and Gouy M. Phylogenetic position of the order Lagomorpha (rabbits, hares, allies). Nature 379 (1996) 333-335
54. Griffioen K.J., Ghribi O., Fox N., Savory J., and Dewitt D.A. Aluminium-maltolate induced toxicity in NT2 cells occurs through apoptosis and includes cytochrome c release. Neurotoxicology 25 (2004) 859-867
55. Gron G., Kirstein M., Thielscher A., Riepe M.W., and Spitzer M. Cholinergic enhancement of episodic memory in healthy young adults. Pyschopharmacology (Berl) 182 (2005) 170-179
56. Grundke-Iqbal I., Wang G.P., Iqbal K., and Wisniewski H.M. Alzheimer paired helical filaments: identification of polypeptides with monoclonal antibodies. Acta Neuropathol. 68 (1985) 279-283
57. Hardy J.A., and Higgins G.A. Alzheimer's disease: the amyloid cascade hypothesis. Science 256 (1992) 184-185
58. Hardy J.A., and Selkoe D.J. The amyloid hypothesis of Alzheimer's disease: progress and problems on the road to therapeutics. Science 297 (2002) 353-356
59. Harkness J.E., and Wagner J.E. The Biology and Medicine of Rabbits and Rodents. 3rd ed. (1989), Lea and Febiger, Philadelphia 49
60. He B.P., and Strong M.J. Motor neuronal death in sporadic amyotrophic lateral sclerosis (ALS) is not apoptotic. A comparative study of ALS and chronic aluminium chloride neurotoxicity. Neuropathol. Appl. Neurobiol. 2 (2000) 150-160
61. Hegde M.L., Anitha S., Latha K.S., Mushtak M.S., Stein R., Ravid R., and Rao K.S.J. First evidence for helical transitions in supercoiled DNA by Aβ peptide(1-42) and aluminium. J. Mol. Neurosci. 22 (2004) 67-79
62. Hewitt C.D., Herman M.M., Lopes M.B., Savory J., and Wills M.R. Aluminium maltol-induced neurocytoskeletal changes in fetal midbrain in matrix culture. Neuropathol. Appl. Neurobiol. 17 (1991) 47-60
63. Hodges J.R., Salmon D.P., and Butters N. Differential impairment of semantic and episodic memory in Alzheimer's and Huntington's diseases: a controlled prospective study. J. Neurol., Neurosurg. Psychiatry 53 (1990) 1089-1095
64. Hof P.R., Bouras C., Buee L., Delacourte A., Perl D.P., and Morrison J.H. Differential distribution of neurofibrillary tangles in the cerebral cortex of dementia pugilistica and Alzheimer's disease cases. Acta Neuropathol. (Berl.) 85 (1992) 23-30
65. Hofstetter J.R., Vincent I., Buigiani O., Ghetti B., and Richter J.A. Aluminium-induced decreases in choline acetyltransferase, tyrosine hydroxylase, and glutamate decarboxylase in selected regions of rabbit brain. Neurochem. Pathol. 6 (1987) 177-193
66. Huang Y., Herman M.M., Katsetos C.D., Wills M.R., and Savory J. Neurofibrillary lesions in experimental aluminium-induced encephalopathy and Alzheimer's disease share immunoreactivity for amyloid, Ab, a1-antichymotrypsin and ubiquitin-protein conjugates. Brain Res. 771 (1997) 213-220
67. Iqbal K., Zaidi T., Bancher C., and Grundke-Iqbal I. Alzheimer paired helical filaments. Restoration of the biological activity by dephosphorylation. FEBS Lett. 349 (1994) 104-108
68. Jaarsma D., Veenma-van der Duin L., and Korf J. N-Acetyl aspartate and acetyl aspartyl glutamate levels in Alzheimer's disease post-mortem brain tissue. J. Neuro Sci. 127 (1994) 230-233
69. Janson E.T. Aluminium exposure and Alzheimer's disease. J. Alzheimer's Dis. 3 (2001) 541-549
70. Kadioglu E., Sardas S., Aslan S., Isik E., and Karakaya A.E. Detection of oxidative damage in lymphocytes of patients with Alzheimer's disease. Biomarkers 9 (2004) 203-209
71. Katsetos C.D., Savory J., Herman M.M., Carpenter R.M., Frankfurter A., Hewitt C.D., and Wills M.R. Neuronal cytoskeletal lesions induced in the CNS by intraventricular and intravenous aluminum maltol in rabbits. Neuropathol. Appl. Neurobiol. 16 (1990) 511-528
72. Kihira T., Yoshida S., Wakayama I., and Yase Y. Aluminium induced mode of motor neuron degeneration: subperineurial injection of aluminum in rabbits. Neurotoxicology 16 (1995) 413-424
73. Kitamura Y., Shimohama S., Kamoshima W., Ota T., Matsuoka Y., Nomura Y., Smith M.A., Perry G., Whitehouse P.I., and Taniguchi T. Alteration of proteins regulating apoptosis, Bcl-2, Bcl-x, Bax, Bak, Bad, ICH-1 and CPP32, in Alzheimer's-disease. Brain Res. 780 (1998) 260-269
74. Klatzo I., Wisniewski H.M., and Streicher E. Experimental production of neurofibrillary degeneration: I. Light microscopic observations. J. Neuropathol. Exp. Neurol. 24 (1965) 187-199
75. Klatzo I., Wisniewski H.M., and Streicher E. Experimental production of Al-induced neurofibrillary degeneration in rabbits with those of Alzheimer's disease using probes for tau, APP, β/A4, α1-antichymotrypsin, and ubiquitin (abstracts). Soc. Neurosci. 22 (1996) 974
76. Kosik K.S., Joachim C.L., and Selkoe D.J. Microtubule-associated protein tau is a major antigenic component of paired helical filaments in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 83 (1986) 4044-4048
77. Kowall N.W., Pendlebury W.W., Kesler J.B., Perl D.P., and Beal M.F. Aluminium-induced neurofibrillary degeneration affects a subset of neurons in rabbit cerebral cortex, basal forebrain and upper brainstem. Neuroscience 29 (1989) 329-377
78. Lai J.C.K., Guest J.F., Leung T.K.C., Lim L., and Davison A.N. The effects of cadmium, manganese and aluminium on sodium-potassium-activated and magnesium-activated adenosine triphosphatase activity and choline uptake in rat brain synaptosomes. Biochem. Pharmacol. 29 (1980) 141-146
79. Landsberg I.P., McDonald B., and Watt F. Absence of aluminium in neuritic plaque cores in Alzheimer's disease. Nature 360 (1992) 65-67
80. Langlais P.J., Thal L., Hansen L., Galasko D., Alford M., and Masliah E. Neurotransmitters in basal ganglia and cortex of Alzheimer's disease with and without Lewy bodies. Neurology 43 (1993) 1927-1934
81. Latha K.S., Anitha S., Rao K.S.J., Bali G., and Easwaran K.R.K. Aluminium induced racemization of aspartate and glutamate in the hippocampal region of rabbit brain: relevance to Alzheimer's disease. Alzheimer's Rep. 4 (2001) 197-204
82. Lavond D.G., Kim J.J., and Thompson R.F. Mammalian brain substrates of aversive classical conditioning. Annu. Rev. Psychol. 44 (1993) 317-342
83. Liwincz B.H., Kristensson K., Wisniewski H.M., Shelanski M.L., and Terry R.D. Observations on axoplasmic transport in rabbits with aluminium-induced neurofibrillary tangles. Brain Res. 80 (1974) 413-420
84. Lovell M.A., Ehmann W.D., and Markesberry W.R. Laser microprobe analysis of brain aluminium in Alzheimer's disease. Ann. Neurol. 33 (1993) 36-42
85. Lovestone S., and Reynolds C.H. The phosphorylation of tau: a critical stage in neurodevelopmental and neurodegenerative process. Neuroscience 78 (1997) 309-324
86. Lukiw W.J., Percy M.E., and Kruck T.P. Nanomolar aluminium induces pro-inflammatory and pro-apoptotic gene expression in human brain cells in primary culture. J. Inorg. Biochem. 99 (2005) 1895-1898
87. Lyras L., Cairns N.J., Jenner A., Jenner P., and Halliwell B. An assessment of oxidative damage to proteins, lipids, and DNA in brain from patients with Alzheimer's disease. J. Neurochem. 68 (1997) 2061-2069
88. Maccioni R.B., and Cambiazo V. Role of microtubule-associated proteins in the control of microtubule assembly. Physiol. Rev. 75 (1995) 835-864
89. Markesberry W.R. Oxidative stress hypothesis in Alzheimer's disease. Free Radical Biol. Med. 23 (1994) 134-147
90. Martin R.B. Aluminium in chemistry, biology and medicine. Clin. Chem. 32 (1986) 1797-1806
91. Matsuo E.S., Shin R.W., Billingsley M.L., Van de Voorde A., O' Connor M., Trojanowski J.Q., and Lee V.M. Biopsy derived adult human brain tau is phosphorylated at many of the same sites as Alzheimer's disease paired helical filament tau. Neuron 13 (1994) 989-1002
92. McGeer P.L., and McGeer E.G. Inflammation of the brain in Alzheimer's disease: implications for therapy. J. Leukocyte Biol. 65 (1999) 409-415
93. Mclachlan D.R.C., Dalton A.J., Kruck T.P., Bell M.Y., Smith W.L., Kalow W., and Andrews D.F. Intramuscular desferrioxamine in patients with Alzheimer's disease. Lancet 337 (1991) 1304-1308
94. McLaughlin A.I.G., Kazantis G., King E., Teare D., Porter R.J., and Owen R. Pulmonary fibrosis and encephalopathy associated with the inhalation of aluminium dust. Br. J. Ind. Med. 19 (1962) 253-263
95. Mecocci P., MacGarvey U., and Beal M.F. Oxidative damage to mitochondrial DNA is increased in Alzheimer's disease. Ann. Neurol. 36 (1994) 747-751
96. Mecocci P., Beal M.F., Cecchetti R., Polidori M.C., Cherubini A., Chionne F., Avellini L., Ronano G., and Senin U. Mitochondrial membrane fluidity and oxidative damage to mitochondrial DNA in aged and AD human brain. Mol. Chem. Neuropathol. 31 (1997) 53-56
97. Muma N.A., and Singer S.M. Aluminium-induced neuropathology: transient changes in micro-tubule associated proteins. Neurotoxicol. Teratol. 18 (1996) 679-690
98. Nicholls D.M., Speares G.M., Miller A.C., Math J., and Del Bianco G. Brain protein synthesis in rabbits following low level aluminium exposure. Int. J. Biochem. 8 (1991) 737-741
99. Nordahl C.W., Ranganath C., Yonelinas A.P., DeCarli C., Reed B.R., and Jagust W.J. Different mechanisms of episodic memory failure in mild cognitive impairment. Neuropsychologia 43 (2005) 1688-1697
100. Nordberg A. Biological markers and the cholinergic hypothesis in Alzheimer's disease. Acta Neurol. Scand., Suppl. 139 (1992) 54-58
101. Passani L.A., Vonsattel J.P., and Coyle J.T. Distribution of N-acetylaspartyl glutamate immunoreactivity in human brain and its alterations in neurodegenerative disease. Brain Res. 772 (1997) 9-22
102. Perl D.P., and Brondy A.R. Alzheimer's disease: X-ray spectrometric evidence of aluminium accumulation in neurofibrillary tangle-bearing neurons. Science 208 (1980) 297-299
103. Perry E.K., and Perry R.H. New insights into the nature of senile (Alzheimer type) plaques. Trends Neurosci. 8 (1985) 301-303
104. Petit T.L., Biederman G.B., and McMullen P.A. Neurofibrillary degeneration, dendritic dying back and learning memory deficits after aluminium administration: implications for brain aging. Exp. Neurol. 67 (1980) 152-162
105. Petit T.L., Biederman G.B., Jonas P., and Leboutiller J.C. Neurobehavioral development of following aluminium administration in infant rabbits. Exp. Neurol. (1985) 640-651
106. Priest N.D. The biological behaviour and bioavailability of aluminium in man, with special reference to studies employing aluminium-26 as a tracer: review and study update. J. Environ. Monit. 5 (2004) 375-403
107. Rabe A., Moon H.L., Shek J., and Wisniewski H.M. Learning deficit in immature rabbits with aluminium induced neurofibrillary changes. Exp. Neurol. 76 (1982) 441-446
108. Ramesh J., Rao K.S.J., and Easwaran K.R.K. The effect of an acidic neurotransmitter, N-acetyl-l-aspartyl-l-glutamate and its precursor N-acetyl-l-aspartate. Alzheimer's Rep. 4 (2001) 87-92
109. Rao K.S.J., Katsetos C.D., Herman M.M., and Savory J. Experimental aluminium encephalopathy. Clin. Lab. Med. 18 (1998) 687-697
110. Rao K.S.J., Ramesh J., and Easwaran K.R.K. Neuropeptide Y structure is modulated by aluminium in the hypothalamus. Alzheimer's Rep. 2 (1999) 99-103
111. Rao K.S.J., Anitha S., and Latha K.S. Aluminium induced neurodegeneration in hippocampus of aged rabbits mimics Alzheimer's disease. Alzheimer's Rep. 3 (2000) 83-88
112. Savory J., and Garruto R.M. Aluminium, tau protein and Alzheimer's disease: an important link?. Nutrition 3 (1998) 313-314
113. Savory J., Herman M.M., Hundley J.C., Seward R.L., Griggs C.M., Katsetos C.D., and Wills M.R. Quantitative studies on aluminium deposition and its effects on neurofilament protein expression and phosphorylation, following the intraventricular administration of aluminium maltolate to adult rabbits. Neurotoxicology 14 (1993) 9-12
114. Savory J., Herman M.M., Erasmus R.T., Boyd J.C., and Wills M.R. Partial reversal of aluminium-induced neurofibrillary degeneration by desferrioxamine in adult male rabbits. Neuropathol. Appl. Neurobiol. 20 (1994) 31-37
115. Savory J., Huang Y., Herman M.M., Reyes M.R., and Wills M.R. Tau immuno reactivity associated with aluminium maltolate-induced neurofibrillary degeneration in rabbits. Brain Res. 669 (1995) 325-329
116. Savory J., Huang Y., Herman M.M., and Wills M.R. Quantitative image analysis of temporal changes in tau and neurofilament proteins during the course of acute experimental neurofibrillary degeneration; nonphosphorylated epitopes precede phosphorylation. Brain Res. 707 (1996) 272-281
117. Savory J., Exley C., Forbes W.F., Huang Y., Joshi J.G., Kruck T., Mclachlan D.R., and Wakayama I. Can the controversy of the role of aluminium in Alzheimer's disease be resolved? What are the suggested approaches to this controversy and methodological issues to be considered?. J. Toxicol. Environ. Health 48 (1996) 615-635
118. Savory J., Rao K.S.J., and Huang Y. Age related hippocampal changes in Bcl-2: Bax ratio, oxidative stress, redox-active iron and apoptosis associated with aluminium-induced neurodegeneration: increased susceptibility with aging. Neurotoxicology 20 (1999) 805-815
119. Savory J., Ghribi O., Forbes M.S., and Herman M.M. Aluminium and neuronal cell injury: inter-relationships between neurofilamentous arrays and apoptosis. J. Inorg. Biochem. 87 (2001) 15-19
120. Savory J., Herman M.M., and Ghribi O. Intracellular mechanisms underlying aluminium-induced apoptosis in rabbit brian. J. Inorg. Biochem. 97 (2003) 154-157
121. Scahill V.L., Hodges J.R., and Graham K.S. Can episodic memory tasks differentiate semantic dementia from Alzheimer's disease. Neurocase 11 (2005) 441-451
122. Selkoe D.J. Biochemistry of altered brain proteins in Alzheimer's disease. Annu. Rev. Neurosci. 12 (1989) 463-490
123. Selkoe D.J. The molecular pathology of Alzheimer's disease. Neuron 6 (1991) 487-498
124. Singer S.M., Chambers C.B., Newfry G.A., Norhund M.A., and Muma N.A. Tau in aluminium-induced neurofibrillary tangles. Neurotoxicology 18 (1997) 63-76
125. Slotkin T.A., Seidler F.J., Crain B.J., Bell J.M., Bissette G., and Nemeroff C.B. Regulatory changes in pre-synaptic cholinergic function assessed in rapid autopsy material from patients with Alzheimer's disease: implications for etiology and therapy. Proc. Natl. Acad. Sci. U. S. A. 87 (1990) 2452-2455
126. Smith M.A., and Perry G. The pathogenesis of Alzheimer disease: an alternative to the amyloid hypothesis. J. Neuropathol. Exp. Neurol. 56 (1997) 217-222
127. Smith M.A., Kutty R.K., Richey P.L., Yan S.D., and Stern D. Hemeoxygenase-I is associated with the neurofibrillary pathology of Alzheimer's disease. Am. J. Pathol. 145 (1994) 42-47
128. Smith M.A., Sayre L.M., Monnier V.M., and Perry G. Radical ageing in Alzheimer's disease. Trends Neuosci. 18 (1995) 172-176
129. Smith M.A., Perry G., and Richey P.L. Oxidative damage in Alzheimer's. Nature 382 (1996) 120-121
130. Smith M.A., Siedlak S.L., Richey P.L., Nagaraj R.H., Elhammer A., and Perry G. Quantitative solubilization and analysis of insoluble paired helical filaments from Alzheimer's disease. Brain Res. 717 (1996) 99-108
131. Smith M.A., Nunomura A., Lee H.G., Zhu X., Moreira P.I., Avila J., and Perry G. Chronological primary of oxidative stress in Alzheimer's disease. Neurobiol. Aging 5 (2005) 579-580
132. Spafforth J. Case of aluminium poisoning. Lancet (1921) 1301
133. Starr J.M., Loeffler B., Abousleiman Y., Simonotto E., Marshall I., Goddard N., and Wardlaw J.M. Episodic and semantic memory tasks activate different brain regions in Alzheimer's disease. Neurology 65 (2005) 266-269
134. Strong M.J., and Garruto R.M. Chronic aluminium induced motor neuron degeneration: clinical, neuropathological and molecular biological aspects. Can. J. Neurol. Sci. 18 (1991) 428-431
135. Strong M.J., Wolff A.V., Wakayama I., and Garruto R.M. Aluminum induced chronic myelopathy in rabbits. Neurotoxicology 12 (1991) 9-21
136. Su J.H., Anderson A.J., and Cummings B.J. Immunohistochemical evidence for apoptosis in Alzheimer's disease. NeuroReport 5 (1994) 2529-2533
137. Su J.H., Cummings B.J., and Cotman C.W. Plaque biogenesis in brain aging and Alzheimer's disease: I. Progressive changes in phosphorylation states of paired helical filaments and neurofilaments. Brain Res. 739 (1996) 79-87
138. Sugaya K., Reeves M., and McKinney M. Topographic association between DNA fragmentation and Alzheimer's disease neuropathology in the hippocampus. Neurochem. Int. 31 (1997) 275-281
139. Sun Y.X., Minthon L., Wallmark A., Warkentin S., Blennow K., and Janciauskiene S. Inflammatory markers in matched plasma and cerebrospinal fluid from patients with Alzheimer's disease. Dementia Geriatr. Cognit. Disord. 16 (2003) 136-144
140. Terry A.V., and Buccafusco J.J. The cholinergic hypothesis of age and Alzheimer's disease related cognitive deficits: recent challenges and their implications for novel drug development. J. Pharmacol. Exp. Ther. 3 (2003) 821-827
141. Terry R.D., and Peña C. Experimental production of neurofibrillary degeneration. 2. Electron microscopy, phosphatase histochemistry and electron probe analysis. J. Neuropathol. Exp. Neurol. 24 (1986) 200-210
142. Tomlinson B.E. Aging and the dementias. In: Adams J.H., and Duchen L.W. (Eds). Greenfield's Neuropathology. 5th ed. (1992), Edward Arnold, London 1284-1411
143. Tsunoda M., and Sharma R.P. Modulation of tumor necrosis factor alpha expression in mouse brain after exposure to aluminium in drinking water. Arch. Toxicol. 73 (1999) 419-426
144. Uemura E. Intranuclear aluminium accumulation in chronic animals with experimental neurofibrillary changes. Exp. Neurol. 85 (1984) 10-18
145. Uno H., Aslum P.B., and Dong S. Cerebral amyloid angiopathy and plaques, and visceral amyloidosis in aged macaques. Neurobiol. Aging 17 (1999) 275-282
146. Van Ginkel M.F., Heijink E., Dekker P.B., Miralem T., Vander Voet G.B., and de Wolff F.A. Effect of aluminium chloride, -citrate and -maltol on the calcium mediated degradation of neurofilament proteins. Neurotoxicology 14 (1993) 13-18
147. Vyas S.B., and Duffy L.K. Stabilization of secondary structure of Alzheimer's beta protein by Al (III) ions and d-Asp sustitution. Biochem. Biophys. Res. Commun. 206 (1995) 718-723
148. Wakayama I., Nerunkar V.R., and Garruto R.M. Immunohistochemical and ultrastructural evidence of dendritic degeneration in motor neurons of Al-intoxicated rabbits. Acta Neuropathol. 85 (1993) 122-128
149. Walton J.R. Aluminium in hippocampal neurons from humans with Alzheimer's disease. Neurotoxicology 3 (2006) 385-394
150. Walton J., Tuniz C., Fink D., Jacobsen G., and Wilcox D. Uptake of trace amounts of aluminium into the brain from drinking water. Neurotoxicology 16 (1995) 187
151. Wen G.Y., and Wisniewski H.M. Histochemical localization of aluminium in the rabbit CNS. Acta Neuropathol. (Berl.) 3 (1985) 175-184
152. Wills M.R., and Savory J. Aluminium poisoning: dialysis encephalopathy, osteomalacia and anaemia. Lancet 11 (1983) 29
153. Wisniewski H.M., and Sofer D. Neuro-fibrillary pathology: current status and research perspectives. Mech. Aging Dev. 1 (1979) 119-142
154. Wisniewski H.M., Narkiewicz O., and Wisniewski K. Topography and dynamics of neurofibrillary degeneration in aluminium encephalopathy. Acta Neuropathol. (Berl.) 9 (1967) 127-133
155. Wisniewski H.M., Sturman J.A., and Shek J.W. Aluminium chloride induced neurofibrillary changes developing rabbits by metallic aluminium. Ann. Neurol. 8 (1980) 479-490
156. Wisniewski H.M., Shek J.W., Gruca S., and Sturman J.A. Chronic model of neurofibrillary changes induced by metallic aluminium. Neurobiol. Aging 3 (1982) 11-22
157. Wisniewski H.M., Shek J.W., Gruca S., and Sturman J.A. Aluminium induced neurofibrillary changes in axons and dendrites. Acta Neuropthol. (Berlin) 3 (1984) 190-197
158. Woodruff-Pak D.S., and Li Y.-T. Nefiracetam. Effect on eye blink classical conditioning in rabbits. Psychopharmacology (Berlin) 114 (1994) 200-208
159. Woodruff-Pak D.S., and Papka M. Alzheimer's disease and eye blink conditioning: 750 ms trace vs 400 ms delay paradigm. Neurobiol. Aging 3 (1996) 397-404
160. Woodruff-Pak D.S., and Trojanowski J.Q. The older rabbit as an animal model: implications for Alzheimer's disease. Neurobiol. Aging 17 (1996) 283-290
161. Yankner B.A. New clues to Alzheimer's disease: unraveling the roles of amyloid and tau. Nat. Med. 2 (1996) 850-852
162. Yokel R.A. Aluminium produces age related behavioral toxicity in the rabbit. Neurotoxicol. Teratol. 11 (1989) 237-242
163. Yokel R.A., and O'Callaghan J.P. An aluminum-induced increase in GFAP is attenuated by some chelators. Neurotoxicol. Teratol. 20 (1998) 55-60
164. Yokel R.A., Allen D.D., and Meyer J.J. Studies of aluminum neurobehavioral toxicity in the intact mammal. Cell. Mol. Neurobiol. 14 (1994) 791-808
165. Yumoto S., Nagai H., Matsuzaki H., Matsumura H., Tada W., Nagatsuma E., and Kobayashi K. Aluminium-26 incorporation into the brain of rat fetuses and sucklings. Brain Res. Bull. 55 (2001) 229-234
166. Zatta P., Zambenedetti P., and Milanese M. Activation of monoamine oxidase type-B by aluminum in rat brain homogenate. NeuroReport 10 (1999) 3645-3648
167. Zatta P., Ibn-Lkhayat-Idrissi M., Zambenedetti P., Kilyen M., and Kiss T. In vivo and in vitro effects of aluminium on the activity of mouse brain acetylcholinesterase. Brain Res. Bull. 59 (2002) 41-45
168. Zhao M., Cribbs D.H., Anderson A.J., Cummings B.J., Su J.H., Wasserman A.J., and Cotman C.W. The induction of the TNF alpha death domain signaling pathway in Alzheimer's disease brain. Neurochem. Res. 28 (2003) 307-318