Biogerontology

, Volume 10, Issue 4, pp 489–502 | Cite as

Curcumin counteracts the aluminium-induced ageing-related alterations in oxidative stress, Na+, K+ ATPase and protein kinase C in adult and old rat brain regions

  • Deepak Sharma
  • Pallavi Sethi
  • Ezaj Hussain
  • Rameshwar Singh
Research Article

Abstract

This study investigated the effect of curcumin on aluminium-induced alterations in ageing-related parameters: lipid peroxidation, superoxide dismutase (SOD), glutathione peroxidase (GPx), glutathione-s-transferase (GST), protein kinase C (PKC), Na+, K+-adenosine triphosphatase (Na+, K+-ATPase) and acetylcholinesterase (AChE) in the cerebral cortex and hippocampus of the brain of 10- and 24-month-old rats. Measurements taken from aluminium-fed rats were compared with those from rats in which curcumin and aluminium were co-administered. In aluminium-treated rats the levels of lipid peroxidation, PKC and AChE were enhanced while the activities of SOD, GPx, GST and Na+, K+-ATPase were significantly decreased in both the brain regions of both age-groups. In animals co-administered with curcumin and aluminium, the levels of lipid peroxidation, activities of PKC and AChE were significantly lowered while the activities of SOD, GPx, GST and Na+, K+-ATPase were significantly enhanced in the two brain regions studied indicating curcumin’s protective effects against aluminium toxicity. Though the magnitudes of curcumin-induced alterations varied in young and old animals, the results of the present study also demonstrated that curcumin exerts a protective effect against aluminium-induced elevation of ageing-related changes by modulating the extent of oxidative stress (by upregulating the activities of antioxidant enzymes) and by regulating the activities of Na+, K+ ATPase, PKC and AChE. Therefore, it is suggested that curcumin counters aluminium-induced enhancement in ageing-related processes.

Keywords

Anti-ageing effects Antioxidant enzymes Curcumin Na+ K+-ATPase Protein kinase C Aluminium-induced neurotoxicity Glutathione-s-transferase Superoxide dismutase Glutathione peroxidase Lipid peroxidation Oxidative stress 

References

  1. Aggarwal BB, Harikumar KB (2008) Potential therapeutic effects of curcumin, the anti-inflammatory agent, against neuro-degenerative, cardiovascular, pulmonary, metabolic, autoimmune and neoplastic diseases. Int J Biochem Cell Biol. doi:10.1016/j.biocel.2008.06.010 PubMedGoogle Scholar
  2. Aggarwal BB, Bhatt ID, Ichikawa H, Ahn KS, Sethi G, Sandur SK et al (2006) Curcumin-biological and medicinal properties. Turmeric: the genus curcumin. Taylor & Francis, London, pp 279–368Google Scholar
  3. Anane R, Bonini M, Grafeille J-M, Creppy EE (1995) Bioaccumulation of water soluble aluminium chloride in the hippocampus after transdermal uptake in mice. Arch Toxicol 69:568–571. doi:10.1007/s002040050214 PubMedGoogle Scholar
  4. Awasthi S, Pandya U, Singhal SS, Lin JT, Thiviyanathan V, Seifert WE Jr, Awasthi YC, Ansari GAS (2000) Curcumin-glutathione interactions and the role of human glutathione s-tranferase P1-1. Chem Biol Interact 128:19–38. doi:10.1016/S0009-2797(00)00185-X PubMedGoogle Scholar
  5. Bala K, Tripathy BC, Sharma D (2006) Neuroprotective and anti-ageing effects of curcumin in aged rat brain regions. Biogerontology 7:81–89. doi:10.1007/s10522-006-6495-x PubMedGoogle Scholar
  6. Barcley LR, Vinqvist MR, Mukai K, Goto H, Hashimoto Y, Tokunaga A, Uno H (2000) On the antioxidant mechanism of curcumin: classical methods are needed to determine antioxidant mechanism and activity. Org Lett 7:2841–2843. doi:10.1021/ol000173t Google Scholar
  7. Bastianetto S, Brouillette J, Quirion R (2007) Neuroprotective effects of natural products: interaction with intracellular kinases, amyloid peptides and a possible role for transthyretin. Neurochem Res 32:1720–1725. doi:10.1007/s11064-007-9333-x PubMedGoogle Scholar
  8. Battaini F, Pascale A (2005) Protein kinase C signal transduction regulation in physiological and pathological aging. Ann N Y Acad Sci 1057:177–192. doi:10.1196/annals.1356.011 PubMedGoogle Scholar
  9. Bolla KL, Briefil G, Spector D, Schwartz BS, Wieler L, Herron J, Gimnez L (1992) Neurocognitive effect of aluminium. Arch Neurol 49:1021–1026PubMedGoogle Scholar
  10. Brichall JD, Chappell JS (1988) Aluminium, chemical physiology and Alzheimer’s disease. Lancet 2:1008–1010. doi:10.1016/S0140-6736(88)90754-4 Google Scholar
  11. Byus CV, Lundak RL, Fletcher RM, Adey WR (1984) Alterations in protein kinase activity following exposure of cultured human lymphocytes to modulate microwave fields. Bioelectromagnetics 5:341–351. doi:10.1002/bem.2250050307 PubMedGoogle Scholar
  12. Calabrese V, Butterfield DA, Stella AM (2003) Nutritional antioxidants and the heme oxygenase pathway of stress tolerance: novel targets for neuroprotection in Alzheimer’s disease. Ital J Biochem 52:177–181PubMedGoogle Scholar
  13. Chainy GBN, Sahoo A, Swain C (1993) Effect of aluminium on lipid proxidation of cerebral hemisphere of chick. Bull Environ Contam Toxicol 50:85–91. doi:10.1007/BF00196545 PubMedGoogle Scholar
  14. Chakravarty AK, Yasmin H (2008) Free radical scavenging and nitric oxide synthase activation in murine lymphocytes and Erhlrich carcinoma cells treated with ethanolic extract of turmeric. Proc Nat Acad Sci India (Sec B) 78 Pt I:37–44Google Scholar
  15. Crambert G, Fuzesi M, Garty H, Karlish S, Greeing K (2002) Phospholemman (FXYDI) associate with Na+, K+-ATPase and regulate its transport properties. Proc Natl Acad Sci USA 99:11476–11481. doi:10.1073/pnas.182267299 PubMedGoogle Scholar
  16. de Roberties E, de Lores arnaiz GR, Salganicoff L (1963) Isolation of synaptic vesicles and structural organization of acetylcholine system within brain nerve endings. J Neurochem 10:225–235. doi:10.1111/j.1471-4159.1963.tb05038.x Google Scholar
  17. Deloncle R, Guillard O, Clanet F, Courois P, Piriou A (1990) Aluminium transfer as glutamate complex through blood brain barrier. Possible implication in dialysis encephalopathy. Biol Trace Elem Res 25:39–45PubMedGoogle Scholar
  18. Deloncle R, Guillard O, Huguet F, Clanet F (1995) Modification of the blood brain barrier through chronic intoxication by aluminium glutamate: possible role. Biol Trace Elem Res 47:227–233. doi:10.1007/BF02790121 PubMedGoogle Scholar
  19. Deloncle R, Huguet F, Fernandez B, Quellard N, Babin PH, Guillard O (2001) Ultrastructural study of rat hippocampus after chronic administration of aluminium l-glutamate: an acceleration of the ageing process. Exp Gerontol 36:231–244. doi:10.1016/S0531-5565(00)00214-X PubMedGoogle Scholar
  20. Deodhar SD, Sethi R, Srimal RC (1980) Preliminary study on antirheumatic activity of curcumin (diferuloylmethane). Indian J Med Res 71:601–608Google Scholar
  21. Disterhoft JF, Oh MM (2006) Pharmacological and molecular enhancement of learning in aging and Alzheimer’s disease. J Physiol (Paris) 99:180–192. doi:10.1016/j.jphysparis.2005.12.079 Google Scholar
  22. Ellman GL, Courtney KD, Andres V Jr, Feather-Stone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95. doi:10.1016/0006-2952(61)90145-9 PubMedGoogle Scholar
  23. Feschenko MS, Donnet C, Wetzel RK, Asinovski NK, Jones LR, Sweadner KJ (2003) Phospholemman, a single-span membrane protein, is an accessory protein of Na+, K+-ATPase in cerebellum and choroid plexus. J Neurosci 23:2161–2169PubMedGoogle Scholar
  24. Flohe L, Gunzler WA (1984) Assays of glutathione peroxidase. Methods of Enzymology. Academic Press, New York, pp 114–121Google Scholar
  25. Florence AL, Gauthier A, Ward RJ, Crichton RR (1995) Influence of hydroxypyridones and desferrioxamine on the mobilization of aluminium from tissues of aluminium-loaded rats. Neurodegeneration 4:449–455. doi:10.1006/neur.1995.0054 PubMedGoogle Scholar
  26. Florrence AL, Gauthier A, Ponsar C, Van den Bosch de Aguilar P, Crichton RR (1994) An experimental animal model of aluminium overload. Neurodegeneration 3:315–323Google Scholar
  27. Fordycee DE, Wehner JM (1993) Effects of aging on spatial learning and hippocampal protein kinase C in mice. Neurobiol Aging 14:309–317. doi:10.1016/0197-4580(93)90116-S Google Scholar
  28. Frautschy SA, Hu W, Kim P, Miller SA, Chu T, Herris-White ME, Cole GM (2001) Phenolic anti-inflammatory antioxidant reversal of a beta-induced cognitive deficits and neuropathology. Neurobiol Aging 22:993–1005. doi:10.1016/S0197-4580(01)00300-1 PubMedGoogle Scholar
  29. 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. doi:10.1111/j.1471-4159.1989.tb10915.x PubMedGoogle Scholar
  30. Goel A, Kunnumakkara AB, Aggarwal BB (2008) Curcumin as “Cure cumin”: from kitchen to clinic. Biochem Pharmacol 75:787–809. doi:10.1016/j.bcp.2007.08.016 PubMedGoogle Scholar
  31. Gomez M, Sanchez DJ, Llobet JM, Corbella J, Domingo JL (1997) Concentration of some essential elements in the brain of aluminium-exposed rats in relation to the age of exposure. Arch Gerontol Geriatr 24:287–294. doi:10.1016/S0167-4943(96)00766-2 PubMedGoogle Scholar
  32. Gong G-H, Wu Q, Huang X-N, Sun A-S, Shi J-S (2005) Protective effects og Ginko biloba leaf extract on aluminium-induced brain dysfunction in rats. Life Sci 77:140–148. doi:10.1016/j.lfs.2004.10.067 PubMedGoogle Scholar
  33. Gulya K, Rakonczay P, Kasa J (1990) Cholinotoxic effects of aluminium in rat brain. J Neurochem 54:1020–1026. doi:10.1111/j.1471-4159.1990.tb02352.x PubMedGoogle Scholar
  34. Habig WH, Pabst MJ, Jakoby WB (1974) Glutathione s-transferases. J Biol Chem 249:7130–7139PubMedGoogle Scholar
  35. Hetherington A, Trewavas A (1982) Calcium-dependent protein kinase in pea shoot membranes. FEBS Lett 145:67–71. doi:10.1016/0014-5793(82)81208-8 Google Scholar
  36. Igwe OJ, Filla MB (1995) Regulation of phosphatidylinositide transduction system in the rat spinal cord during aging. Neuroscience 69:1239–1251. doi:10.1016/0306-4522(95)00298-W PubMedGoogle Scholar
  37. Jacqmin H, Commenges D, Latenneur L, Barberger-Gateau JF (1994) Component of drinking water and risk of cognitive impairment in the elderly. Am J Epidemiol 139:48–57PubMedGoogle Scholar
  38. Jovanovic SV, Boone CW, Steenken S, Trinoga M, Kaskey RB (2001) How curcumin works preferentially with water soluble antioxidants. J Am Chem Soc 123:3064–3068. doi:10.1021/ja003823x PubMedGoogle Scholar
  39. Julka D, Gill KD (1996) Altered calcium homeostasis: possible mechanisms of aluminium-induced neurotoxicity. Biochim Biophys Acta 17:47–54Google Scholar
  40. Kabir N, Schaefer AW, Nakhost A, Sossin WS, Forscher P (2001) Protein kinase C activation promotes microtubule advance in neural growth cones by increasing average microtubule growth lifetimes. J Cell Biol 152:1033–1043. doi:10.1083/jcb.152.5.1033 PubMedGoogle Scholar
  41. Kaizer RR, Correa MC, Spanevello RM, Morsch VM, Mazzanti CM, Goncalves JF, Schetinger MRC (2005) Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminium on different mouse brain regions. J Inorg Biochem 99:1865–1870. doi:10.1016/j.jinorgbio.2005.06.015 PubMedGoogle Scholar
  42. Kalpana C, Menon VP (2004) Modulatory effect of curcumin on lipid peroxidation and antioxidant status during nicotine-induced toxicity. Pol J Pharmacol 56:581–586PubMedGoogle Scholar
  43. Katsuyama H, Saijoh K, Inoue Y, Sumino K (1989) The interaction of aluminium with soluble protein kinase C from mouse brain. Arch Toxicol 63:474–478. doi:10.1007/BF00316451 PubMedGoogle Scholar
  44. Kaul S, Krishnakanth TP (1994) Effect of retinal deficiency and curcumin or turmeric feeding on brain Na+, K+-ATPase adenosine triphosphate activity. Mol Cell Biochem 137:101–107. doi:10.1007/BF00944071 PubMedGoogle Scholar
  45. Kaur J, Sharma D, Singh R (1998) Regional effects of ageing on Na+,K(+)- ATPase activity in rat brain and correlation with multiple unit action potentials and lipid peroxidation. Indian J Biochem Biophys 35(6):364–371PubMedGoogle Scholar
  46. Kaur J, Sharma D, Singh R (2001) Acetyl-l-cranitine enhances Na+, K+ ATPase, glutathione-s-transferase and multiple unit activity and reduces lipid peroxidation and lipofuscin concentration in aged rat brain regions. Neurosci Lett 301:1–4. doi:10.1016/S0304-3940(01)01576-2 PubMedGoogle Scholar
  47. Kaur J, Singh S, Sharma D, Singh R (2003a) Aluminium-induced enhancement of ageing-related parameters in rat brain regions. Indian J Biochem Biophys 40:330–339Google Scholar
  48. Kaur J, Singh S, Sharma D, Singh R (2003b) Neurostimualtory and antioxidative effects of l-deprenyl in aged rat brain regions. Biogerontology 4:105–111. doi:10.1023/A:1023351904840 PubMedGoogle Scholar
  49. Khare CP (2007) Indian medicinal plants—an illustrated dictionary. Springer, New Delhi, pp 286–287Google Scholar
  50. Kubo T, Hagiwara Y (2005) Posterior hypothalamus cholinergic stimulation-induced activation of anterior hypothalamic area neurons is enhanced in spontaneously hypersensitive rats. Brain Res 1061:36–41. doi:10.1016/j.brainres.2005.08.054 PubMedGoogle Scholar
  51. Lal B, Gupta A, Murthy RC, Ali MM, Chanda SV (1993) Aluminum ingestion alters behavior and some neurochemicals in rats. Indian J Exp Biol 31:30–35PubMedGoogle Scholar
  52. Laterra J, Bressler JP, Indurti RR, Belloni-Olivi L, Goldstein GW (1992) Inhibition of astroglia-induced endothelial differentiation by inorganic lead: a role for protein kinase C. Proc Natl Acad Sci USA 89:10748–10752. doi:10.1073/pnas.89.22.10748 PubMedGoogle Scholar
  53. Logan-Smith MJ, Lockyer PJ, East JM, Lee AG (2001) Curcumin a molecule that inhibits the Ca2+-ATPase of sarcoplasmic reticulum but increases the rate of accumulation of Ca2+. J Biol Chem 276:46905–469011. doi:10.1074/jbc.M108778200 PubMedGoogle Scholar
  54. Lowry OH, Rosenborough NJ, Farr AL (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275PubMedGoogle Scholar
  55. Markesbery WR, Ehmann WD, Alauddin M, Hossain TI (1984) Brain trace element concentrations in ageing. Neurobiol Aging 5:19–28. doi:10.1016/0197-4580(84)90081-2 PubMedGoogle Scholar
  56. Marklund S, Marklund G (1974) Involvement of the super oxide anion radical in the autooxidation of pyrogallol and convenient assay for super oxide dismutase. Eur J Biochem 47:469–474. doi:10.1111/j.1432-1033.1974.tb03714.x PubMedGoogle Scholar
  57. Markovac J, Goldstein GW (1988) Picomolar concentration of lead stimulate brain protein kinase C. Nature 334:71–73PubMedGoogle Scholar
  58. Martin-Aragno S, Benedi JM, Villar AM (1997) Modification of antioxidant capacity and lipid peroxidation in mice under fraxetin treatment. J Pharm Pharmacol 49:49–52Google Scholar
  59. Mattson MP (1998) Modification of ion homeostasis by lipid peroxidation: role of neuronal degeneration and adaptive plasticity. Trends Neurosci 21:53–57. doi:10.1016/S0166-2236(97)01188-0 PubMedGoogle Scholar
  60. Mc Dermott JR, Smith AI, Iqbal K, Wisniewski HM (1979) Brain aluminium in ageing and Alzheimer’s disease. Neurology 29:809–814Google Scholar
  61. Mclaughlin AGI, Kazantis G, King E, Teare D, Porter RJ, Owen P (1962) Pulmonary fibrosis and encephalopathy associated with the inhalation of aluminium dust. Br J Ind Med 19:253–263PubMedGoogle Scholar
  62. Mukhopadhyay A, Basu N, Ghatak N, Gujral PK (1982) Anti-inflammatory and irritant activities of curcumin analogues in rats. Agents Actions 12:508–515. doi:10.1007/BF01965935 PubMedGoogle Scholar
  63. Nakamura S, Ishihara T (1989) Region selective increase in activities of CNS cholinergic marker enzymes during learning of memory task in aged rats. Pharmacol Biochem Behav 34:805–810. doi:10.1016/0091-3057(89)90278-5 PubMedGoogle Scholar
  64. Nehru B, Bhalla P (2006) Reversal of an aluminium-induced alteration in redox status in different regions of rat brain by administration of centrophenoxine. Mol Cell Biochem 290:185–191. doi:10.1007/s11010-006-9186-7 PubMedGoogle Scholar
  65. Nishizuka Y (1986) Studies and perspectives of protein kinase C. Science 233:305–312. doi:10.1126/science.3014651 PubMedGoogle Scholar
  66. Okhawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxide in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358. doi:10.1016/0003-2697(79)90738-3 Google Scholar
  67. Osawa T, Kato Y (2005) Protective role of antioxidative food factors in oxidative stress caused by hyperglycemia. Ann N Y Acad Sci 1043:440–451. doi:10.1196/annals.1333.050 PubMedGoogle Scholar
  68. Pascale A, Amadio M, Govoni S, Battaini F (2007) The aging brain, a key for the future: the protein kinase C involvement. Pharmacol Res 55:560–569. doi:10.1016/j.phrs.2007.04.013 PubMedGoogle Scholar
  69. Patil TN, Srinivasan M (1971) Hypocholesteremic effect of curcumin in induced-hypercholesteremic rats. Indian J Exp Biol 9:167–169PubMedGoogle Scholar
  70. Paulraj R, Behari J (2004) Radio frequency radiation effects on protein kinase C activity in rats’ brain. Mutat Res 545:127–130. doi:10.1016/S0027-5107(03)00113-1 PubMedGoogle Scholar
  71. Piper JT, Singhal SS, Salameh MS, Torman RT, Awasthi YC, Awasthi S (1998) Mechanism of anticarcinogenic properties of curcumin: the effect of curcumin on glutathione linked detoxification enzyme in rat liver. Int J Biochem Cell Biol 30:445–456. doi:10.1016/S1357-2725(98)00015-6 PubMedGoogle Scholar
  72. Proven SD, Yokel RA (1992) Aluminium inhibits glutamate release from transverse rat hippocampal slices: role of G protein, Ca channels and protein kinase C. Neurotoxicology 13:1313–1420Google Scholar
  73. Rajakumar DV, Rao MN (1994) Antioxidant properties of dehydrozingerone and curcumin in rat brain homogenates. Mol Cell Biochem 140:73–79. doi:10.1007/BF00928368 PubMedGoogle Scholar
  74. Rajkrishnan V, Vishwanathan P, Rajasekharan KN, Menon VP (1999) Neuroprotective role of curcumin from curcuma longa on ethanol—induced brain damage. Phytother Res 13:571–574. doi :10.1002/(SICI)1099-1573(199911)13:7<571::AID-PTR494>3.0.CO;2-7Google Scholar
  75. Reddy S, Aggarwal BB (1994) Curcumin is a non-compititive and selective inhibitor of phosphorylase kinase. FEBS Lett 341:19–22. doi:10.1016/0014-5793(94)80232-7 PubMedGoogle Scholar
  76. Reddy A Ch and Lokesh BR (1994) Studies on the inhibitory effects of curcumin and eugenol on the formation of reactive oxygen species and oxidation of ferrous ions. Mol Cell Biochem 137:1–8. doi:10.1007/BF00926033
  77. ReddyA Ch and Lokesh BR (1996) Effect of turmeric (Curcuma longa) on iron—induced lipid per oxidation in the rat liver. Food Chem Toxicol 32:279–283. doi:10.1016/0278-6915(94)90201-1 Google Scholar
  78. Redhead K, Quinlan GJ, Das RG, Gutteridge JM (1992) Aluminium-adjuvanted vaccines transiently increase aluminium levels in murine brain tissue. Pharmacol Toxicol 70:278–280PubMedCrossRefGoogle Scholar
  79. Rifat AL, Eastwood MR, Crapper-Mclachlan DR (1990) Effect of exposure of minors to aluminium powder. Lancet 336:1162–1165. doi:10.1016/0140-6736(90)92775-D PubMedGoogle Scholar
  80. Rodella L, Rezzani R, Lanzi R, Bianchi R (2001) Chronic exposure to aluminium decreases NADPH-diaphorase positive neurons in the rat cerebral cortex. Brain Res 889:229–233. doi:10.1016/S0006-8993(00)03044-4 PubMedGoogle Scholar
  81. Roskans AJ, Cinnor JR (1990) Aluminium access to the brain: a role for transferrine and its receptors. Proc Natl Acad Sci USA 87:9024–9027. doi:10.1073/pnas.87.22.9024 Google Scholar
  82. Runyan JD, Moore AN, Dash PK (2005) A role of prefrontal calcium-sensitive protein phoaphatase and kinase activity in working memory. Learn Mem 12:103–110. doi:10.1101/lm.89405 PubMedGoogle Scholar
  83. Sarin S, Julka D, Gill KD (1997) Regional alteration in calcium homeostasis in the primate brain following chronic aluminium exposure. Mol Cell Biochem 168:95–100. doi:10.1023/A:1006891125762 PubMedGoogle Scholar
  84. Sethi P, Jyoti A, Singh R, Hussain E, Sharma D (2008) Aluminium-induced electrophysiological, biochemical and cognitive modifications in the hippocampus of aging rats. Neurotoxicology. doi:10.1016/j.neuro.2008.08.005 PubMedGoogle Scholar
  85. Sharma D, Singh R (1995) Centrophenoxine activates acetylcholinesterase activity in hippocampus of aged rats. Indian J Exp Biol 33:365–368PubMedGoogle Scholar
  86. Sharma D, Maurya AK, Singh R (1993) Age-related decline in the multiple unit action potentials of CA3 neurons of rat hippocampus: correlation with lipid peroxidation and lipofuscin concentration and the effect of centrophenoxine. Neurobiol Aging 14:319–330. doi:10.1016/0197-4580(93)90117-T PubMedGoogle Scholar
  87. Shishodia S, Singh T, Chaturvedi MM (2007) Modulation of transcription factors by curcumin. Adv Exp Med Biol 595:127–148. doi:10.1007/978-0-387-46401-5_4 PubMedGoogle Scholar
  88. Sirvio J, Pitkanen A, Paakkonen A (1989) Brain cholinergic enzymes and cortical EEG activity in young and old rats. Comp Biochem Physiol 94:277–283Google Scholar
  89. Sossin WS (2007) Isoform specificity of protein kinase Cs in synaptic plasticity. Learn Mem 14:236–246. doi:10.1101/lm.469707 PubMedGoogle Scholar
  90. Srimal RC, Dhawan BN (1973) Pharmacology of diferuloyl methane (curcumin), a non-steroidal anti-inflammatory agent. J Pharm Pharmacol 25:447–452PubMedGoogle Scholar
  91. Srinivasan M (1972) Effect of curcumin on blood sugar as seen in diabetic subject. Indian J Med Sci 26:269–270PubMedGoogle Scholar
  92. Suarez-Fernandez MB, Soldado AB, Sanz-Medal A, Vega JA, Novelli A, Fernandez-Sanchez MT (1999) Aluminium- induced degeneration of astrocytes occur via apoptosis and results in neuronal death. Brain Res 835:125–136. doi:10.1016/S0006-8993(99)01536-X PubMedGoogle Scholar
  93. Sun YM, Zhang HY, Chen DZ, Liu CB (2002) Theoretical elucidation on the antioxidant mechanism of curcumin: a DFT study. Org Lett 4:2909–29011. doi:10.1021/ol0262789 PubMedGoogle Scholar
  94. Surh YJ (1999) Molecular mechanisms of chemopreventive effects of selected dietary and medicinal phenolic substances. Mutat Res 428:305–327. doi:10.1016/S1383-5742(99)00057-5 PubMedGoogle Scholar
  95. Tanaka Y, Ando S (1990) Synaptic ageing as revealed by changes in membrane potential and decreased activity of Na+, K+-ATPase. Brain Res 43:425–434Google Scholar
  96. Ure JA, Perassolo M (2000) Update on the pathophysiology of the epilepsy. J Neurol Sci 177:1–17. doi:10.1016/S0022-510X(00)00356-7 PubMedGoogle Scholar
  97. Van der Zee EA, Palm IF, O’Connor M, Maizels ET, Hunzicket-Dunn M, Disterhoft JF (2004) Aging-related alterations in the distribution of Ca(2+)-dependent PKC isoforms in rabbit hippocampus. Hippocampus 14:849–860. doi:10.1002/hipo.20000 PubMedGoogle Scholar
  98. Van Rensberg SJ, Carstens ME, Potocnik FC, Van der Walt BJ, Taljaard JJ (1995) Transferrin C2 and Alzheimer’s disease: another piece of puzzle found? Med Hypotheses 44:268–272. doi:10.1016/0306-9877(95)90178-7 Google Scholar
  99. Van Rensberg SJ, Daniel WM, Potocnik FC, van Zyl JM, Taljaard JJ, Emsley RA (1997) A new model for the pathophysiology of Alzheimer’s disease. Aluminium toxicity is exacerbated by hydrogen peroxide and attenuated by an amyloid protein fragment and melatonin. S Afr Med J 87:1111–1115Google Scholar
  100. Varner JA, Jensen KF, Harweth W, Issacson RL (1998) Chronic administration of aluminium-fluoride or sodium fluoride to rats in drinking water: alterations in neuronal and cerebrovascular integrity. Brain Res 784:284–298. doi:10.1016/S0006-8993(97)01336-X PubMedGoogle Scholar
  101. Walton JR (2006) Aluminium in hippcampal neurons from human with Alzheimer’s disease. Neurotoxicology 27:385–394. doi:10.1016/j.neuro.2005.11.007 PubMedGoogle Scholar
  102. Walton JR (2007) An aluminium-based rat model for Alzheimer’s disease exhibits oxidative damage, inhibition of PP2A activity, hyperphosphorylated tau, and granulovacuolar degeneration. J Inorg Chem 101:1275–1284Google Scholar
  103. Watanabe S, Fukui T (2000) Suppressive effect of curcumin on trichloroethane-induced oxidative stress. J Nutr Sci Vitaminaol Tokyo 46:230–234Google Scholar
  104. Wu A, Ying Z, Gomez-Pinilla F (2006) Dietary curcumin counteracts the outcome of traumatic brain injury on oxidative stress, synaptic plasticity, and cognition. Exp Neurol 197:309–317. doi:10.1016/j.expneurol.2005.09.004 PubMedGoogle Scholar
  105. Xu N, Majid V, Markesbery WR, Ehman WD (1992) Brain aluminium in Alzheimer’s disease using an improved GFAAS method. Neurotoxicology 13:735–744PubMedGoogle Scholar
  106. Yang X, Thomas DP, Zhang X, Culver BW, Alexander BM, Murdoch WJ, Rao MN, Tulis DA, Ren J, Sreejayan N (2006) Curcumin inhibits platelet-derived growth factor-stimulated vascular smooth muscle cell function and injury-induced neointima formation. Arterioscler Thromb Vasc Biol 26:85–90. doi:10.1161/01.ATV.0000191635.00744.b6 PubMedGoogle Scholar
  107. Zatta P, Favarato M, Nicolini M (1993) Deposition of aluminium in brain tissues of rats exposed to inhalation of aluminium acetylacetonate. Neuroreport 4:1119–1122. doi:10.1097/00001756-199308000-00015 PubMedGoogle Scholar
  108. Zatta P, Zambenedetti P, Bruna V, Filippi B (1994) Activation of acetylcholinesterase by aluminium (III): the relevance of the metal species. Neuroreport 5(14):1777–1780PubMedCrossRefGoogle Scholar
  109. Zhao Q, Slavkovich V, Zheng W (1998) Lead exposure promotes translocation of protein kinase C in rat choroids plexus in vitro, but not in vivo. Toxicol Appl Pharmacol 149:99–106. doi:10.1006/taap.1997.8352 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Deepak Sharma
    • 1
  • Pallavi Sethi
    • 1
  • Ezaj Hussain
    • 2
  • Rameshwar Singh
    • 1
  1. 1.School of Life SciencesJawaharlal Nehru UniversityNew DelhiIndia
  2. 2.School of BiosciencesJamia Millia Islamia UniversityNew DelhiIndia

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