Aluminum disruption of calcium homeostasis and signal transduction resembles change that occurs in aging and alzheimer's disease

Journal of Alzheimer's Disease

Volumn 29, Issue 2, 2012, Pages 255-273

  Walton, J R ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Aluminum; Alzheimer's disease; calcium; calmodulin; G proteins; magnesium; neurotoxicant; oxidative damage; protein kinase C; signal transduction

Indexed keywords

ALUMINUM; CALCIUM; DRINKING WATER; FOOD ADDITIVE; IRON; MAGNESIUM; SUNSCREEN;

AGING; ALZHEIMER DISEASE; BIOACCUMULATION; BLOOD BRAIN BARRIER; BRAIN CORTEX; BRAIN REGION; CALCIUM HOMEOSTASIS; CALCIUM METABOLISM; CALCIUM SIGNALING; CALCIUM TRANSPORT; CIRCULATION; HIPPOCAMPUS; HUMAN; INDUSTRIALIZATION; INTERNEURON; OXIDATIVE STRESS; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; REVIEW;

EID: 84859406975     PISSN: 13872877     EISSN: 18758908     Source Type: Journal    
DOI: 10.3233/JAD-2011-111712     Document Type: Review

References (209)

1. Berridge MJ (1993) Inositol triphosphate and calcium signaling. Nature 361, 315-325.
2. +-dependent processes as mediators of neurotoxicity. Neurotoxicology 13, 139-138.
3. Orrenius S, Nicotera P (1994) The calcium ion and cell death. J Neural Trans Suppl 3, 1-11. (Pubitemid 24362355)
4. Freissmuth M, Casey PJ, Gilman AG (1989) G proteins control diverse pathways of transmembrane signaling. FASEB J 3, 2125-2131.
5. Khachaturian ZS (1987) Hypothesis on the regulation of cytosol calcium concentration and the aging brain. Neuro-biol Aging 8, 345-346.
6. Walton JR (2012) Evidence that ingested aluminum additives containedinprocessed foods and alum-treated drinking water are a major risk factor for Alzheimer's disease. Curr Inorg Chem 2, 19-39.
7. Markesbery WR, Ehmann WD, Hossain TI, Alauddin M, Goodin DT (1981) Instrumental neutron activation analysis of brain aluminum in Alzheimer disease and aging. Ann Neurol 10, 511-516. (Pubitemid 12242177)
8. McDermott JR, Smith AI, Iqbal K, Wisniewski HM (1979) Brain aluminum in aging and Alzheimer disease. Neurology 29, 809-813.
9. Shimizu H, Mori T, Koama M, Sekiya M, Ooami H (1994) A correlative study ofthe aluminum content and aging changes of the brain in non-demented elderly subjects. Nihon Ronen Igakkai Zasshi 31, 950-960.
10. Walton JR (2009) Functional impairmentinaged ratschroni-cally exposedto human range dietary aluminum equivalents. Neurotoxicology 30, 182-193.
11. 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 forebrain and upper brainstem. Neuroscience 29, 329-337. (Pubitemid 19113424)
12. Edwardson JA, Ferrier IN, McArthur FK, McKeith IG, McLaughlin I, Morris CM, Mountfort SA, Oakley AE, Taylor GA, Ward MK, Candy JM (1986) Alzheimer's disease and the aluminium hypothesis. In: Aluminium in Chemistry Biology and Medicine Raven Press, New York, 1, pp. 85-96
13. Walton JR (2006) Aluminum in hippocampal neurons from humans with Alzheimer's disease. Neurotoxicology 27, 385-394.
14. Martin RB (1986) The chemistry of aluminum as related to biology and medicine. Clin Chem 32, 1797-1806. (Pubitemid 17018049)
15. Macdonald TL, Humphreys WG, Martin RB (1987) Promotion of tubulin assembly by aluminum ion in vitro. Science 236, 183-186. (Pubitemid 17061035)
16. Ganrot PO (1986) Metabolism and possible health effects of aluminum. Environ Health Perspect 65, 363-441. (Pubitemid 16117505)
17. Cowan JA, Ed (1995) The Biological Chemistry of Magnesium, VCH Publishers, New York, pp. 1-254.
18. Cowan JA (2002) Structural and catalytic chemistry of magnesium-dependent enzymes. Bio Metals 15, 225-235. (Pubitemid 34816207)
19. Seamon KB (1980) Calcium-and magnesium-dependent conformational states of calmodulin as determined by nuclear magnetic resonance. Biochemistry 19, 207-215.
20. 2+-ATPase of human red cell membranes. Biochim Biophys Acta 596, 487-489. (Pubitemid 10119504)
21. 2+-induced conformational changes in porcine calmodulin by H/D exchange and ESI-MS: Effect of cations and ionic strength. Biochemistry 42, 15388-15397. (Pubitemid 38035156)
22. Permyakov EA, Kretsinger RH (2009) Cell signaling, beyond cytosolic calcium in eukaryotes. J Inorg Biochem 103, 77-86.
23. Trapp GA (1986) Interactions of aluminium with cofactors, enzymes and other proteins. Kidney Int 29, S12-S16.
24. Miller JL, Hubbard CM, Litman BJ, Macdonald TL (1989) Inhibition of transducin activation and guanosine triphosphatase activity by aluminum ion. J Biol Chem 264, 243-250. (Pubitemid 19027597)
25. Exley C, Birchall JD (1992) The cellular toxicity of aluminum. J Theor Biol 159, 83-98.
26. Cox PA (2000) Inorganic Chemistry, Springer-Verlag New York Inc., New York, p. 115.
27. Exley C (2004) The pro-oxidant activity of aluminum. Free Radic Biol Med 36, 380-387. (Pubitemid 38130236)
28. Bondy SC, Guo-Ross SX, Pien J (1998) Mechanisms underlying the aluminum-induced potentiation of the pro-oxidant properties of transition metals. Neurotoxicology 19, 65-71.
29. 3+, neomycin, polyamines, and melittin. J Lipid Med Cell Signal 11, 81-91.
30. Kumar S (1999) Aluminium-induced biphasic effect. Med Hypothesis 52, 557-559. (Pubitemid 29322576)
31. Chen L, Liu C-J, Tang M, Li A, Hu X-W, Du Y-M, Shen J-J, Lu Y-L, Heschler J (2005) Action of aluminum on high voltage-dependent calcium current and its modulation by ginkgolide B. Acta Pharmacol Sinica 26, 539-545. (Pubitemid 40676162)
32. Gilman AG (1987) G proteins: Transducers of receptor-generated signals. Rev Biochem 56, 615-649.
33. Shi B, Chou K, Haug A (1993) Aluminium impacts elements of the phosphoinositide signalling pathway in neuroblastoma cells. Mol Cell Biochem 121, 109-118. (Pubitemid 23138036)
34. Gibson GE, Peterson C (1987) Calcium and the aging nervous system. Neurobiol Aging 8, 329-344.
35. Martinez A, Vitorica J, Satrustegui J (1988) Cytosolic free calcium levels increase with age in rat brain synaptosomes. Neurosci Lett 88, 336-342.
36. Reynolds JN, Carlen PL (1987) Diminished calcium currents in aged hippocampal dentate gyrus granule neurons. Brain Res 410, 137-153.
37. Kirischuk S, Pronchuk N, Verkhratsky A (1992) Measurements of intracellular calcium in sensory neurons of adult and old rats. Neuroscience 50, 947-951.
38. Kirischuk S, Voitenko N, Kostyuk P, Verkhratsky A (1996) Age-associated changes of cytoplasmic calcium homeostasis in cerebellar granule neurons in situ: Investigation on thin cerebellar slices. Exp Gerontol 31, 475-487. (Pubitemid 26234903)
39. Verkhratsky A, Shmigol A, Kirischus S, Pronchuk N, Kostyuk P (1994) Age-dependent changes in calcium currents and calcium homeostasis in mammalian neurons. Ann NY Acad Sci 747, 365-381.
40. Kirischuk S, Verkhratsky A (1996) Calcium homeostasis in aged neurones. Life Sci 59, 451-459. (Pubitemid 26246900)
41. Das N, Ghosh S (1996) The effect of age on calcium dynamics in rat brain in vivo. Mech Ageing Dev 88, 17-24. (Pubitemid 26184062)
42. Raza M, Deshpande LS, Blair RE, Carter DS, Sombati S, DeLorenzo RJ (2007) Aging is associated with elevated intracellular calcium levels and altered calcium homeostatic mechanisms in hippocampal neurons. Neurosci Lett 418, 77-81. (Pubitemid 46602700)
43. Toescu EC, Verkhratsky A (2007) The importance of being subtle: Small changes in calcium homeostasis control cognitive decline in normal aging. Aging Cell 6, 267-273. (Pubitemid 46785132)
44. Eckert A, Forstl H, Zerfass R, Oster M, Hennerici M, Müller WE (1998) Changes of intracellular calcium regulation in Alzheimer's disease and vascular dementia. J Neural Transm Suppl 54, 201-210. (Pubitemid 28539357)
45. Green KN, LaFerla FM (2008) Linking calcium to Afj and Alzheimer's disease. Neuron 59, 190-194. (Pubitemid 352033693)
46. McLachlan DRC (2006) Aluminium and the risk for Alzheimer's disease. Environmetrics 6, 233-275.
47. Guo-Ross S, Yang E, Bondy SC (1998) Elevation of cerebral proteases after systemic administration of aluminum. Neurochem Int 33, 277-282. (Pubitemid 28418299)
48. Kaur A, Gill KD (2005) Disruption of neuronal calcium homeostasis after chronic aluminium toxicity in rats. Basic Clin Pharmacol Toxicol 96, 118-122. (Pubitemid 40320615)
49. Yase Y (1980) The role of aluminum in CNS degeneration with interaction of calcium. In: L. Liss (Ed.), Aluminum Neurotoxicity Pathotox Publ., Park Forest South, IL, USA, pp. 101-109. (Pubitemid 11217736)
50. Yasui M, Yase Y, Ota K, Garruto RM (1991) Evaluation of magnesium, calcium and aluminum metabolism in rats and monkeys maintained on calcium-deficient diets. Neurotoxi-cology 12, 603-613.
51. Julka D, Gill KD (1996) Altered calcium homeostasis: A possible mechanisms of aluminium-induced neurotoxicity. Biochim Biophys Acta 1315, 47-54. (Pubitemid 26047213)
52. Sarin S, Julka D, Gill KD (1997) Regional alterations in calcium homeostasis in the primate brain following chronic aluminium exposure. Mol Cell Biochem 168, 95-100. (Pubitemid 27091060)
53. Anghileri LJ (1992) Effects of complexed iron and aluminum on brain calcium. Neurotoxicology 13, 475-478.
54. Farnell BJ, Crapper McLachlan DR, Baimbridge K, DeBoni U, Wong L, Wood PL (1985) Calcium metabolism in aluminum encephalopathy. Exp Neurol 88, 68-83. (Pubitemid 15114485)
55. Mundy WR, Freudenrich TM, Kodavanti PRS (1997) Aluminum potentiates glutamate-induced calcium accumulation and iron-induced oxygen free radical formation in primary neuronal cultures. Mol Chem Neuropathol 32, 41-57.
56. Guo G-W, Liang Y-X (2001) Aluminum-induced apoptosis in cultured astrocytes and its effect on calcium homeostasis. Brain Res 888, 221-226. (Pubitemid 32058786)
57. Shi B, Haug A (1992) Aluminium interferes with signal transduction in neuroblastoma cells. Pharmacol Toxicol 71, 308-313.
58. Garruto RM, Fukatsu R, Yanagihara R, Gajdusek DC, Hook G, Fiori CE (1984) Imaging of calcium and aluminum in neurofibrillary tangle-bearing neurons in parkinsonism-dementia of Guam. Proc Natl Acad Sci USA 81, 1875-1879. (Pubitemid 14149568)
59. Siesjo BK (1990) Calcium in the brain under physiological and pathological conditions. Eur Neurol 30 (Suppl 2), 3-9. (Pubitemid 20074952)
60. Wenk GL, Barnes CA (2000) Regional changes in the hip-pocampal density of AMPA and NMDA receptors across the lifespan of the rat. Brain Res 885, 1-5.
61. Bonhaus DW, Perry WB, McNamara JO (1990) Decreased density, but not number of N-methyl-D-aspartate, glycine and phencyclidine binding sites in hippocampus of senescent rats. Brain Res 532, 82-86. (Pubitemid 20384643)
62. 3H]TCP) binding in human frontal cortex: Decreases in Alzheimer-type dementia. J Neurochem 54, 526-532.
63. Penney JB, Maragos WF, Greenamyre JT, Debowey DL, Hollingsworth Z, Young AB (1990) Excitatory amino acid binding sites in the hippocampal region of Alzheimer's disease and other dementias. J Neurol Neurosurg Psychiatry 53, 313-320.
64. Ulas J, Brunner LC, Geddes JW, Choe W, Cotman CW (1992) N-methyl-D-aspartate receptor complex in the hippocampus of elderly, normal individuals and those with Alzheimer's disease. Neuroscience 49, 45-61.
65. Campbell LW, Hao SY, Thibault O, Blalock EM, Land-field PW (1996) Aging changes in voltage-gated calcium currents in hippocampal CA1 neurons. J Neuroscience 16, 6286-6295. (Pubitemid 26314001)
66. Reynolds JN, Carlen PL (1987) Diminished calcium currents in aged hippocampal dentate gyrus granule neurons. Brain Res 410, 137-153.
67. 2+ changes in rat cortical synapto-somes. J Neurochem 53, 392-398. (Pubitemid 19186071)
68. Peterson C, Gibson GE (1983) Aging and 3, 4-diaminiopyridine alter synaptosomal calcium uptake. J Biol Chem 258, 11382-11386.
69. Power JM, Wu WW, Sametsky E, Oh MM, Disterhoft JF (2002) Age-related enhancement of the slow outward calcium-activated current in hippocampal CA1 pyramidal neurons in vitro. J Neurosci 22, 7234-7243. (Pubitemid 35379177)
70. Moyer JR Jr, Thompson LT, Black JP, Disterhoft JF (1992) Nimodipine increases excitability of rabbit CA1 pyramidal neurons in an age-and concentration-dependent manner. J Neurophysiol 68, 2100-2109. (Pubitemid 23015511)
71. Nachshen DA (1985) Regulation of cytosolic calcium concentrations in presynaptic nerve endings isolated from rat brain. J Physiol 363, 87-101. (Pubitemid 15000294)
72. Platt B, Haas H, Busselberg D (1994) Aluminium reduces glutamate-activated currents of rat hippocampal neurones. Neuroreport 5, 2329-2332. (Pubitemid 24374866)
73. Busselberg D (1995) Calcium channels as target sites of heavy metals. Toxicol Lett 82, 255-261. (Pubitemid 26054711)
74. + concentration and expression of phospholipase C and NMDA receptor a genes in hippocampus of weaning rats as well as their neural behavior through subchronic exposure. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi (Chin J Ind Hyg Occup Dis), 28, 648-651.
75. Koss DJ, Hindley KP, Riedel G, Platt B (2007) Modulation of hippocampal calcium signalling and plasticity by serine/threonine protein phosphatases. J Neurochem 102, 1009-1023. (Pubitemid 47174215)
76. Amador FC, Henriques AG, da Cruz e Silva OAB, da Cruz e Silva EF (2004) Monitoring protein phosphatase 1 isoform levels as a marker for cellular stress. Neurotox Teratol 26, 387-395. (Pubitemid 38534471)
77. 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. (Pubitemid 120021646)
78. Walton JR (2007) An aluminum-based rat model for Alzheimer's disease exhibits oxidative damage, inhibition of PP2A activity, hyperphosphorylated tau, and gran-ulovacuolar degeneration. J Inorg Biochem 101, 1275-1284. (Pubitemid 47313520)
79. 2+ modulatory action on GABA transport in brain cortex nerve terminals. J Inorg Biochem 97, 132-132.
80. Koenig ML, Jope RS (1987) Aluminum inhibits the fast phase of voltage-dependent calcium influx into synapto-somes. J Neurochem 49, 316-320. (Pubitemid 17108266)
81. Platt B, Busselberg D (1994) Actions of aluminum on voltage-activated calcium channel currents. Cell Mol Neu-robiol 13, 819-829.
82. Provan SD, Yokel RA (1992) Aluminum inhibits glutamate release from transverse rat hippocampal slices: Role of G proteins, Ca channels and protein kinase C. Neurotoxicology 13, 413-420.
83. 3+. Brain Res 622, 163-168. (Pubitemid 23264961)
84. Lai JCK, Blass JP (1984) Inhibition of brain glycolysis by aluminum. J Neurochem 42, 438-446. (Pubitemid 14180778)
85. Fukuyama R, Wadhwani KC, Galdzicki Z, Rapoport SI, Ehrenstein G (1994) fj-Amyloid polypeptide increases calcium-uptake in PC12 cells: A possible mechanism for its cellular toxicity in Alzheimer's disease. Brain Res 667, 269-272.
86. Arispe N, Rojas E, Pollard HB (1993) Alzheimer disease amyloid beta protein forms calcium channels in bilayer membranes: Blockade by tromethamine and aluminum. Proc Natl Acad Sci USA 90, 567-571. (Pubitemid 23028904)
87. Chandler LJ, Crews FT (1990) Calcium-versus G protein-mediated phosphoinositide hydrolysis in rat cerebral cortical synaptoneurosomes. J Neurochem 55, 1022-1030.
88. Surichamorn W, Abdallah AM, El-Fakahany EE (1989) Aging does not alter brain muscarinic receptor-mediated phosphoinositide hydrolysis and its inhibition by phorbol esters, tetrodotoxin and receptor desensitization. J Pharmacol Exp Ther 25, 543-549. (Pubitemid 20005597)
89. Nalepa L, Pintor A, Fortuna S, Vetulani J, Michaelik H (1989) Increased responsiveness of the cerebral cortical phosphatidylinositol system to noradrenaline and carbachol in senescent rats. Neurosci Lett 107, 195-199.
90. Pietrzak ER, Wilce PA, Shanley BC (1990) Effects of chronic ethanol treatment and aging on brain phophoinosi-tide turnover and adenylate cyclase activity. Neurochem Int 17, 593-598. (Pubitemid 20366569)
91. Burnett DM, Bowyer JF, Masserano JM, Zahniser NR (1990) Effect of aging on alpha-1 adrenergic stimulation of phosphoinositide hydrolysis in various regions of rat brain. J Pharmacol Exp Ther 255, 1265-1270.
92. Mundy W, Tandon P, Ali S, Tilson H (1991) Age-related changes in receptor-mediated phosphoinositide hydrolysis in various regions of rat brain. Life Sci 49, PL97-PL102.
93. Gonzales RA, Brown LM, Jones TW, Trent RD, Westbrook SL, Leslie SW (1991) N-methyl-D-aspartate mediated responses decrease with age in Fischer 344 rat brain. Neu-robiol Aging 19, 219-225.
94. Ayyagari PV, Gerber M, Joseph JA, Crewes FT (1998) Uncoupling of muscarinic cholinergic phosphoinositide signals in senescent cerebral cortical and hippocampal membranes. Neurochem Int 32, 107-115. (Pubitemid 28020244)
95. Nicolle MM, Colombo PJ, Gallagher M, McKinney M (1999) Metabotropic glutamate receptor-mediated hippocampal phosphoinositide turnover is blunted in spatial learning-impaired aged rats. J Neurosci 19, 9604-9610. (Pubitemid 30228111)
96. Pintor A, Potenza RL, Domenici MR, Tburzi F, Reggio R, Pezzola A, Popoli P (2000) Age-related decline in the functional response of striatal group 1 mGlu receptors. Neu-roreport 11, 3033-3038.
97. Domenici MR, Pintor A, Potenza RL, Gaudi S, Gro MC, Passarelli F, Reggio R, Galluzzo M, Massotti M, Papoli P (2003) Metabotropic glutamate receptor 5 (mGluR5)-mediated phosphoinositide hydrolysis and NMDA-potentiating effects are blunted in the striatum of aged rats: A possible additional mechanism in striatal senescence. Eur J Neurosci 17, 2047-2055. (Pubitemid 36713966)
98. Crews FT, Kurian P, Freund (1994) Cholinergic and serotonergic stimulation of phosphoinositide hydrolysis is decreased in Alzheimer's disease. Life Sci 55, 1993-2002.
99. Jope RS, Song L, Li X, Powers R (1994) Impaired phospho-inositide hydrolysis in Alzheimer's disease brain. Neurobiol Aging 15, 221-226. (Pubitemid 24120830)
100. Greenwood AF, Powers RE, Jope RS (1995) Phosphoinosi-tide hydrolysis, G alpha q, phospholipase C, and protein kinase C in post mortem human brain: Effects of post mortem interval, subject age, and Alzheimer's disease. Neuroscience 69, 125-138.
101. 3H]-PIP2 hydrolysis in Alzheimer's disease. Life Sci 53, PL439-PL444.
102. Jope RS (1999) Modulation of phosphoinositide hydrolysis by NaF and aluminum in rat cortical slices. J Alzheimers Dis 1, 231-247.
103. Mundy WR, Shafer TJ (2001) Aluminium-induced alteration of phosphoinositide and calcium signalling. In: Aluminium and Alzheimer's Disease: The Science that Describes the Link. Exley C, Ed., Elsevier Science BV Amsterdam, pp. 340-360.
104. Johnson GV, Jope RS (1986) Aluminum impairs glucose utilization and cholinergic activity in rat brain in vitro. Toxicology 40, 93-102. (Pubitemid 16079879)
105. Kanaho A, Moss J, Vaughan M (1985) Mechanism of inhibition of transducin GTPase activity by fluoride and aluminum. J Biol Chem 260, 11393-11397.
106. McDonald LJ, Mamrack MD (1988) Aluminum affects phosphoinositide hydrolysis by phosphoinositidase C. Biochem Biophys Res Comm 155, 203-208.
107. Nostrandt AC, Shafer TJ, Mundy WR, Padilla S (1996) Inhibition of rat brain phosphatidylinositol-specific phospholipase C by aluminum: Regional differences, interactions with aluminum salts, and mechanisms. Toxicol Appl Pharmacol 136, 118-125. (Pubitemid 26049717)
108. Roychowdhury S, Rasenick MM (1994) Tubulin-G protein association stabilizes GTP binding and activates GTPase: Cytoskeletal participation in neuronal signal transduction. Biochemistry 33, 9800-9805. (Pubitemid 24272942)
109. 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, 1059-1069.
110. Jope RS, Song L, Powers RE (1997) Cholinergic activation of phosphoinositide signaling is impaired in Alzheimer's disease brain. Neurobiol Aging 18, 111-120. (Pubitemid 27062193)
111. 3 inhibition of agonist-stimulated inositol phosphate accumulation. Role of calcium, G-proteins, phospholipase C and protein kinase C. Biochem Pharmacol 47, 1317-1325.
112. Shafer TJ, Mundy WR, Tilson HA (1993) Aluminum decreases muscarinic, adrenergic, and metabotropic receptor-stimulated phosphoinositide hydrolysis in hip-pocampal and cortical slices from rat brain. Brain Res 629, 133-140. (Pubitemid 23328796)
113. Mundy WR, Freudenrich T, Shafer TJ, Nostrandt AC (1995) In vitro aluminum inhibition of brain phosphoinositide metabolism: Comparison of neonatal and adult rats. Neu-rotoxicology 16, 35-44.
114. Wood PC, Wojcikiewicz RJH, Burgess J, Castleden CM, Nahorski SR (1994) Aluminum inhibits muscarinic agonist-induced inositol 1, 4, 5-triphosphate production and calcium mobilization in permeabilized SH-SY5Y human neuroblastoma cells. JNeurochem 62, 2219-2223.
115. 3+-mediated changes in membrane physical properties participate in the inhibition of polyphosphoinositide hydrolysis. Arch Biochem Biophys 408, 263-271. (Pubitemid 36027048)
116. 3+-mediated changes on membrane fluidity affects the activity of PI-PLC but not of PLC. Chem Phys Lipids 122, 159-163. (Pubitemid 36207521)
117. Jones DL, Kochian LV (1995) Aluminum inhibition of the inositol 1, 4, 5-triphosphate signal transduction pathway in wheat roots: A role in aluminium toxicity? Plant Cell 7, 1913-1922. (Pubitemid 3019807)
118. McCullar JS, Malencik DA, Vogel WK, Crofoot KM, Anderson SR, Filtz TM (2007) Calmodulin potentiates Gfjy activation of phospholipase C-fj3. Biochem Pharmacol 73, 270-278. (Pubitemid 44855731)
119. Johnson GVW, Cogdill KW, Jope RS (1990) Oral aluminum alters in vitro protein phosphorylation and kinase activities in rat brain. Neurobiol Aging 11, 209-216. (Pubitemid 20181898)
120. Friedman E, Wang HY (1989) Effect of age on brain cortical protein kinase C and its mediation of 5-hydroxytryptamine release. J Neurochem 52, 187-192. (Pubitemid 19023367)
121. Battaini F, Del Vesco R, Govoni S, Trabucchi M (1990) Regulation of phorbol ester binding and protein kinase C activity in aged rat brain. Neurobiol Aging 11, 563-566. (Pubitemid 20297150)
122. Magnoni MS, Govoni S, Battaini F, Trabucchi M (1991) The ageing brain: Protein phosphorylation as a target of changes in neuronal function. Life Sci 48, 373-385.
123. Cole G, Dobkins KR, Hansen LA, Terry RD, Saitoh T (1988) Decreased levels of protein kinase C in Alzheimer disease. Brain Res 452, 165-174.
124. Wang H-Y, Pisano MR, Friedman E (1994) Attenuated protein kinase C activity and translocation in Alzheimer's disease brain. Neurobiol Aging 15, 293-298. (Pubitemid 24194869)
125. Cochran M, Elliott DC, Brennan P, Chawtur V (1990) Inhibition of protein kinase C activation by low concentrations of aluminium. Clin Chim Acta 194, 167-172.
126. Katsuyama H, Saijoh K, Inoue Y, Sumino K (1998) The interaction of aluminium with soluble protein kinase C from mouse brain. Arch Toxicol 63, 474-478.
127. Dobransky T, Davis WL, Rylett RJ (2001) Functional characterization of phosphorylation of 69-kDa human choline acetyltransferase at serine 440 by protein kinase C. J Biol Chem 276, 22244-22250.
128. Silva VS, Nunes MA, Cordeiro JM, Calejo AI, Santos S, Neves P, Sykes A, Morgado F, Dunant Y, Goncalves PP (2007) Comparative effects of aluminum and ouabain on synaptosomal choline uptake, acetylcholine release and (Na+/K+) ATPase. Toxicology 236, 58-77.
129. Szutowicz A, Tomaszewicz M, Jankowska A, Madziar B, Bielarczyk H (2000) Acetyl-CoA metabolism in cholinergic neurons and their susceptibility to neurotoxic inputs. Metab Brain Dis 15, 29-44. (Pubitemid 30422087)
130. Hansen LA, DeTeresa R, Davies P, Terry RD (1988) Neocortical morphometry, lesion counts, and choline acetyl-transferase levels in the age spectrum of Alzheimer's disease. Neurology 38, 48-54. (Pubitemid 18028091)
131. Gandy S, Greengard P (1994) Regulated cleavage of the Alzheimer amyloid precursor protein: Molecular and cellular basis. Biochimie 76, 300-303. (Pubitemid 24295549)
132. Hung AY, Haass C, Nitsch RM, Qui WWQ, Citron M, Wurtman RJ, Growdon JH, Selkoe DJ (1993) Activation of protein kinase C inhibits cellular production of the amyloid fj-protein. J Biol Chem 268, 22959-22962. (Pubitemid 23327996)
133. 2+/calmodulin-dependent protein kinase II. Proc Natl Acad Sci USA 85, 6218-6221.
134. Caporaso GL, Gandy SE, Buxbaum JD, Ramabhadran TV, Greengard P (1992) Protein phosphorylation regulates secretion of Alzheimer fj/A4 amyloid precursor protein. Proc Natl Acad Sci USA 89, 3055-3059.
135. Nitsch RM, Growdon RJ (1994) Role of neurotransmission in the regulation of amyloid beta-protein precursor processing. Biochem Pharm 47, 1275-1284. (Pubitemid 24130919)
136. Drago D, Cavaliere A, Mascetra N, Ciavardelli D, di Ilio C, Zatta P, Sensi SL (2008) 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. Rejuv Res 11, 861-871.
137. Kawahara M, Muramoto K, Kobayashi K, Mori H, Kuroda Y (1994) Aluminum promotes the aggregation of Alzheimer's amyloid beta-protein in vitro. Biochem Biophys Res Com-mun 198, 531-535. (Pubitemid 24178401)
138. Pratico D, Uryu K, Sung S, Tang S, Trojanowski JW, Lee VM-Y (2002) Aluminum modulates brain amyloidosis through oxidative stress in APP transgenic mice. FASEB J16, 1138-1131.
139. Banks WA, Niehoff ML, Drago D, Zatta P (2006) Aluminum complexing enhances amyloid beta protein penetration of blood brain barrier. Brain Res 1116, 115-221.
140. Martini A, Battaini F, Govoni S, Volpe P (1994) Inositol 1, 4, 5-trisphosphate receptor and ryanodine receptor in the aging brain of Wistar rats. Neurobiol Aging 15, 203-206. (Pubitemid 24120827)
141. 3H]inositol 1, 4, 5-triphosphate binding in Alzheimer's disease. Neurosci Lett 94, 198-202.
142. 3H]inositol (1, 3, 4, 5) P4 binding in Alzheimer's disease brain. Brain Res 681, 160-166.
143. Haug LS, Øestvold AD, Cowburn RF, Garlind A, Winblad B, Bogdanovich N, Walaas SJ (1996) Decreased inositol (1, 4, 5)-triphosphate receptor levels in Alzheimer's disease cerebral cortex: Selectivity of changes and possible correlation to pathological severity. Neurodegeneration 5, 169-176.
144. Johnson GV, Watson AL Jr, Lartius R, Uemura E, Jope RS (1992) Dietary aluminum selectively decreases MAP-2 in brains of developing and adult rats. Neurotoxicology 13, 463-474.
145. 2+ mobilization. FEBS Lett 267, 301-304. (Pubitemid 20216713)
146. Kawahara M, Muramoto K, Kobayashi K, Mori H, Kuroda Y (1992) Aluminum promotes the aggregation of Alzheimer's amyloid ß-protein in vitro. Biochem Biophys Res Commun 189, 1317-1322.
147. Kuroda Y, Kobayashi K, Ichikawa M, Kawahara M, Muramoto K (1995) Application of long-term cultured neurons in aging and neurological research: Aluminum neurotoxicity, synaptic degeneration and Alzheimer's disease. Gerontology 41 (Suppl 1), 2-6.
148. Schofl C, Sanchez-Bueno A, Dixon CJ, Woods NM, Lee JA, Cuthbertson KS, Cobbold PH, Birchall JD (1990) Aluminium perturbs oscillatory phosphoinositide-mediated calcium signalling in hormone-stimulated hepatocytes. Biochem J 269, 547-550. (Pubitemid 20236054)
149. 2+ oscillations. Science 179, 227-230. (Pubitemid 28103880)
150. Hoskins B, Scott JM (1984) Changes in activities of calmodulin-mediated enzymes in rat brain during aging. Mech Aging Dev 26, 231-239. (Pubitemid 14033329)
151. Teolato S, Calderini G, Bonetti AC, Toffano G (1983) Calmodulin content in different brain areas of aging rats. Neurosci Lett 38, 57-60. (Pubitemid 13029103)
152. Levine AS, Gosnell BA, Morley JE (1986) Alterations in calmodulin levels in tissues from aged animals. J Gerontol 41, 20-23. (Pubitemid 16161240)
153. McLachlan DR, Wong L, Bergeron C, Baimbridge KG (1987) Calmodulin and calbindin D28K in Alzheimer disease. Alzheimer Dis Assoc Disord 1, 171-179.
154. Gao J, Yin D, Yao Y, Williams TD, Squier TC (1998) Progressive decline in the ability of calmodulin isolated from aged brain to activate the plasma membrane Ca-ATPase. Biochemistry 37, 9536-9548. (Pubitemid 28307710)
155. Yamamoto M, Gotz ME, Ozawa H, Luckhaus C, Saito T, Rosler M, Riederer P (2000) Hippocampal level of neural specific adenylyl cyclase type I is decreased in Alzheimer's disease. Biochim Biophys Acta 1535, 60-68.
156. Yao Y, Yin D, Jas GS, Kuczer K, Williams TD, Schon-eich C, Squier TC (1996) Oxidative modification of a carboxyl-terminal vicinal methionine in calmodulin by hydrogen peroxide inhibits calmodulin-dependent activation of the plasma membrane Ca-ATPase. Biochemistry 35, 2767-2787. (Pubitemid 26098775)
157. Solomon B, Koppel R, Jossiphov J (2001) Immunostaining of calmodulin and aluminium in Alzheimer's disease-affected brains. Brain Res Bull 55, 253-256. (Pubitemid 32722167)
158. O'Day D, Myre MA (2004) Calmodulin-binding domains in Alzheimer's disease proteins: Extending the calcium hypothesis. Biochem Biophys Res Commun 320, 1051-1054. (Pubitemid 38916649)
159. 3+ effect ontarget bindingof calmodulin. Biochem Biophys Res Commun 333, 1060-1065. (Pubitemid 40910111)
160. 2+ ion binding to methionine and tyrosine spin-labeled bovine brain calmod-ulin. J Inorg Biochem 41, 283-291.
161. Siegel N, Coughlin R, Haug A (1983) Athermodynamic and electron paramagnetic resonance studyofstructural changes in calmodulin induced by aluminium binding. Biochem Bio-phys Res Commun 115, 512-517.
162. Wolf T, Solomon B, Ivnitski D, Rishpon J, Fleminger G (1998) Interactions of calmodulin with metal ions and with its target proteins revealed by conformation-sensitive monoclonal antibodies. J Mol Recogn 11, 13-19.
163. Siegel N, Haug A (1983) Aluminum interaction with calmodulin. Evidencefor altered structure and function from optical and enzymatic studies. Biochim Biophys Acta 744, 36-45. (Pubitemid 13101040)
164. Weis C, Haug A (1987) Aluminum-induced conformational changes in calmodulin alter the dynamics ofinteraction with melittin. Arch Biochem Biophys 254, 304-312. (Pubitemid 17068822)
165. Suhayda CG, Haug A (1984) Organic acids prevent aluminium-induced conformational changes in calmodulin. Biochem Biophys Res Comm 119, 376-381.
166. Julka D, Gill KD (1996) Involvement of altered cytoskeletal protein phosphorylation in aluminium-induced CNS dysfunction. J Biochem Toxicol 11, 227-233. (Pubitemid 126803510)
167. Richardt G, Federolf G, Habermann E (1985) The interaction of aluminum and other metal ions with calcium-calmodulin-dependent phosphodiesterase. Arch Toxicol 57, 257-259. (Pubitemid 16253427)
168. Julka D, Gill KD (1996) Altered calcium homeostasis: A possible mechanism of aluminium-induced neurotoxicity. Biochim Biophys Acta 1315, 47-54. (Pubitemid 26047213)
169. Vig PJ, Nath R, Desaiah D (1989) Metal inhibition of calmodulin activity in monkey brain. J Appl Toxicol 9, 313-316. (Pubitemid 19230509)
170. Ali M, Bullock S, Rose PR (1988) Phosphorylationofsynap-tic proteins in chick forebrain: Changes with development and passive avoidance training.J Neurochem50, 1579-1587.
171. Johnson GV, Li XH, Jope RS (1989) Aluminum increases agonist-stimulated cyclic AMP production in rat cerebral cortical slices. J Neurochem 53, 258-263. (Pubitemid 19158137)
172. Johnson GVW, Jope RS (1987) Aluminum alters cyclic AMP and cyclic GMP levels but not presynaptic cholinergic markers in rat brain in vivo. Brain Res 403, 1-6. (Pubitemid 17009733)
173. Robison AJ, Winder DG, Colbran RJ, Bartlett RK (2007) Oxidation of calmodulin alters activation and regulation of CAMKII. Biochem Biophys Res Commun 356, 97-101. (Pubitemid 46413134)
174. Hof PR, Rosenthal RE, Fiskum G (1996) Distribution of neurofilament protein and calcium-binding proteins parval-bumin, calbindin, and calretinin in the canine hippocampus. J Chem Neuroanat 11, 1-12. (Pubitemid 26248748)
175. Blaustein MP (1988) Calcium transport and buffering in neurons. Trends Neurosci 11, 438-443.
176. Kirischuk S, Pronchuk N, Verkhratsky A (1992) Measurements of intracellular calcium in sensory neurons of adults and old rats. Neuroscience 50, 947-951.
177. Iaocopino AM, Christakos S (1990) Specific reduction of calcium-binding protein (28-kilodalton calbindin-D) gene expression in aging and neurodegenerative diseases. Proc Natl Acad Sci USA 87, 4078-4082.
178. 2+ binding proteins during rat brain ageing: Loss of calbindin and calretinin in the hippocam pus, with no change in the cerebellum. Eur J Neurosci 6, 1391-1399.
179. Krzywkowski P, De Bilbao F, Senut MC, Lamour Y (1995) Age-related changes in parvalbumin-and GABA-immunoreactive cells in the rat septum. Neurobiol Aging 16, 29-40.
180. Kishimoto J, Tsuchiya T, Cox H, Emson PC, Nakayama Y (1998) Age-related changes of calbindin-D28k, calretinin, and parvalbumin mRNAs in the hamster brain. Neurobiol Aging 19, 77-82. (Pubitemid 28167799)
181. Geula C, Nagykery N, Wu C-K, Bu Jing (2003) Loss of calbindin-D28K from aging human cholinergic basal fore-brain: Relation to plaques and tangles. J Neuropathol Exp Neurol 62, 605-616. (Pubitemid 36682633)
182. Choi JH, Hwang IK, Yoo KY, Yi SS, Park OK, Lee CH, Yoon YS, Won MH (2009) Reduction of calbindin D-28k-immunoreactive neurons in the dog dentate gyrus. J Vet Med Sci 71, 1125-1128.
183. Mundy WR, Kodavanti PR, Dulchinos VF, Tilson HA (1994) Aluminum alters calcium transport in plasma membrane and endoplasmic reticulum from rat brain. J Biochem Toxicol 9, 17-23.
184. Zaidi A, Gao J, Squier TC, Michaelis ML (1998) Age-related decrease in brain synaptic membrane Ca-ATPase in F344/BNF1 rats. Neurobiol Aging 19, 487-495. (Pubitemid 29065498)
185. Peterson C, Nicholls DG, Gibson GE (1985) Sub-synaptosomal calcium distribution during aging and 3, 4-diaminopyridine treatment. Neurobiol Aging 6, 297-304. (Pubitemid 16207682)
186. Michaelis ML, Bigelow DJ, Schöneich C, Williams TD, Ramonda L, Yin D, Hühmer AF, Yao Y, Gao J, Squier TC (1996) Decreased plasma membrane calcium transport activity in aging brain. Life Sci 59, 405-412. (Pubitemid 26246895)
187. Martinez A, Vitorica J, Bogonez E, Satrustegui J (1987) Differential effects of age on the pathways of calcium influx into nerve terminals. J Brain Res 435, 249-257. (Pubitemid 18009794)
188. 2+-ATPase in human brain affected by Alzheimer's disease. FASEB J 23, 1826-1834.
189. Jencks WP, Yang T, Peisach D, Myung J (1993) Calcium ATPase of sarcoplasmic reticulum has four binding sites for calcium. Biochemistry 32, 7030-7034. (Pubitemid 23221638)
190. Zafar TA (1999) Effect of aluminum on intestinal calbindin-D9K in rats. Agricult 15, 227-230.
191. Cox KA, Dunn MA (2001) Aluminum toxicity alters the regulationof calbindin-D28k protein and mRNA expression in chick intestine. J Nutr 131, 2007-2013. (Pubitemid 32661072)
192. Orihuelo D, Meichtry V, Pizarro M (2005) Aluminium-induced impairment of transcellular calcium absorption in the small intestine: Calcium uptake and glutathione influence. J Inorg Biochem 99, 1879-1886. (Pubitemid 41253777)
193. Kodavanti PRS, Mundy WR, Tilson HA, Harry GJ (1993) Effects of selected neuroactive chemicals on calcium transporting systems in rat cerebellum and on survival of cerebellar granule cells. Fund Appl Toxicol 21, 308-316. (Pubitemid 23316233)
194. Gandolfi L, Stella MP, Zambenedetti P, Zatta P (1998) Aluminum alters intracellular calcium homeostasis in vitro. Biochim Biophys Acta 1306, 315-320. (Pubitemid 28269315)
195. 2+ flux modulation as an indicator ofheavy metal toxicity. Ind J Exp Biol 48, 737-743.
196. Mundy WR, Kodavanti PR, Dulchinos VF, Tilson HA (1994) Aluminum alters calcium transport in plasma membrane and endoplasmic reticulum from rat brain. J Biochem Toxicol 9, 17-23.
197. 2+ homeostasis and cell viability. J Neurochem 102, 454-465. (Pubitemid 47000602)
198. Deleers M (1985) Cationic atmosphere and cation competition binding at negatively charged membranes: Pathological implications of aluminum. Res Comm Chem Pathol Pharmacol 49, 277-294. (Pubitemid 15007377)
199. Green KN, Demuro A, Akbari Y, Hitt BD, Smith IF, Parker I, LaFerla FM (2008) SERCA pump activity is physiologically regulated by presenilin and regulates amyloid fj production. J Cell Biol 181, 1107-1116. (Pubitemid 351915486)
200. + leak function of presenilin. J Clin Invest 117, 1230-1239. (Pubitemid 46718411)
201. Sato N, Hori O, Yamaguchi A, Lambert J-C, Chartier-Harlin M-C, Robinson PA, Delacourte A, Schmidt AM, Furuyama T, Imaizumi K, Tohyama M, Takagi T (1999) A novel presenilin-2 splice variant in human Alzheimer's disease brain tissue. J Neurochem 72, 2498-2505. (Pubitemid 29242201)
202. Sato N, Imaizumi K, Manabe T, Taniguchi M, Hitomi J, Katayama T, Yoneda T, Morihara T, Yasuda Y, Takagi T, Kudo T, Tsuda T, Itoyama Y, Makifuchi T, Fraser PE, St George-Hyslop P, Tohyama M (2001) Increased production of fj-amyloid and vulnerability to endoplasmic reticulum stress by an aberrant spliced form of presenilin 2. J Biol Chem 276, 2108-2113.
203. Matsuzaki S, Manabe T, Katayama T, Nishikawa A, Yanagita T, Okuda H, Yasuda Y, Miyata S, Meshitsuka S, Tohyama M (2004) Metals accelerate production of the aberrant splicing isoform of the presenilin-2. J Neurochem 88, 1345-1351. (Pubitemid 38366909)
204. Ghribi O, Herman MM, DeWitt DA, Forbes MS, Savory J (2001) Abeta (1-42) and aluminum induce stress in the endoplasmic reticulum in rabbit hippocampus, involving nuclear translocation of gadd 153 and NF-kappaB. Brain Res Mol Brain Res 96, 30-38. (Pubitemid 33145361)
205. Savory J, Herman MM, Ghribi O (2003) Intracellular mechanisms underlying aluminium-induced apoptosis in rabbit brain. J Inorg Biochem 97, 151-154. (Pubitemid 37152421)
206. Walton JR (2010) Evidence for participation of aluminum in neurofibrillary tangle formation and growth in Alzheimer's disease. J Alzheimers Dis 22, 65-72.
207. Hempen B, Brion J-P (1996) Reduction of acetylated a-tubulin immunoreactivities in neurofibrillary tangle-bearing neurons in Alzheimer's disease. J Neuropathol Exp Neurol 55, 964-972. (Pubitemid 126449410)
208. Walton JR (2007) A longitudinal study of rats chronically exposed to aluminum at human dietary levels. Neurosci Lett 412, 29-33. (Pubitemid 46038549)
209. Flood DG (1993) Critical issues in the analysis of dendritic extent in aging humans, primates, and rodents. Neurobiol Aging 14, 649-634.