Skip to main content

Alterations in lipid composition and neuronal injury in primates following chronic aluminium exposure

Abstract

The effect of chronic aluminium exposure (25 mg/kg b.wt.) was studied on the lipid composition and various membrane-bound enzymes in different regions of monkey brain. Aluminium (Al) administration caused a significant decrease in the total lipid, glycolipid, and phospholipid content of primate brain. Cholesterol levels and the phospholipid to cholesterol ratio were, however, markedly increased as a consequence of Al administration, thereby indicating a loss of membrane integrity. This was further confirmed when Al treatment was found to have a significant effect on the various membrane-bound enzymes in terms of decreased activities of Na+ K+ ATPase and acetylcholinesterase along with a decrease in the activity of the myelin-specific enzyme, 2′ 3′-cyclic nucleotide phosphohydrolase.

This is a preview of subscription content, access via your institution.

References

  1. D. Julka, R. Sandhir, and K. D. Gill, Altered cholinergic metabolism in rat CNS following aluminium exposure: implications on learning performance,J. Neuwchem. 65, 2157–2167 (1995).

    CAS  Article  Google Scholar 

  2. S. S. Krishnan, D. R. Mclachlan, A. J. Dalton, B. Krishnan, S. A. Stanley, J. E. Harrison, and T. Kruck, Aluminium toxicity in humans, inEssential and Toxic Trace Elements in Health and Disease. Alan R. Liss, pp. 645–659 (1988).

  3. J. M. Candy, A. E. Dakley, and J. Klinowski, Alumino-Silicates and senile plaque formation in Alzheimer’s disease,Lancet ii, 354–357 (1986).

    Article  Google Scholar 

  4. A. Bizzi and P. Gambetti, Phosphorylation of neurofilaments is altered in aluminium intoxication,Acta Neuropathol. 71, 154–158 (1986).

    PubMed  Article  CAS  Google Scholar 

  5. T. B. Shea, J. E. Clarke, T. R. Wheelock, P. A. Paskevich, and R. A. Nixon, Aluminium salts induce the accumulation of neurofilaments in perikarya of NB2a/dl neuroblastoma,Brain Res. 492, 53–64 (1989).

    PubMed  Article  CAS  Google Scholar 

  6. A. C. Alfrey, G. R. Le Gendre, and W. D. Kachny, The dialysis encephalopathy syndrome: possible aluminium intoxication,N. Eng. J. Med. 294, 184–188.

  7. R. M. Strong, R. M. Garruto, J. G. Joshi, W. R. Mundy, and T. J. Shafer, Can the mechanism of aluminium neurotoxicity be integrated into a unified scheme?J. Toxicol. Environ. Health 48, 599–614 (1996).

    PubMed  Article  CAS  Google Scholar 

  8. C. G. Fraga, P. I. Oteiza, M. S. Golub, M. E. Gershwin, and C. L. Keen, Effects of aluminium on brain lipid peroxidation,Toxicol. Lett. 51, 213–219 (1990).

    PubMed  Article  CAS  Google Scholar 

  9. H. Zumkley, H. P. Bertram, A. Lison, O. Knoll, and H. Loose, Al, Zn and Cu concentrations in plasma chronic renal insufficiency,Clin. Nephrol. 12, 18–21 (1979).

    PubMed  CAS  Google Scholar 

  10. J. Folch, M. Lees, and G. H. S. Stanley, A simple method for the isolation and purification of total lipid from animal tissues,J. Biol. Chem. 226, 497–509 (1957).

    PubMed  CAS  Google Scholar 

  11. E. Levin and C. Head, Quantitative analysis of tissue neutral lipids,Anal. Biochem. 10, 23–31 (1965).

    PubMed  Article  CAS  Google Scholar 

  12. G. R. Bartlett, Phosphorus assay in column chromatography,J. Biol. Chem. 234, 466–468 (1959).

    PubMed  CAS  Google Scholar 

  13. M. Dubois, K. A. Gilles, J. K. Hamilton, P. A. Rebbers, and F. Smith, Colorimetric method for determination of sugars and related substances.Anal. Chem. 28, 350–356 (1956).

    Article  CAS  Google Scholar 

  14. A. Zlatkis, B. Zak, and A. J. Boyle, A new method for the direct determination of cholesterol,J. Lab. Clin. Med. 41, 486–492 (1953).

    PubMed  CAS  Google Scholar 

  15. L. Warren, The thiobarbituric acid assay of sialic acids,J. Biol. Chem. 234, 1971–1975 (1959).

    PubMed  CAS  Google Scholar 

  16. E. D. Wills, Mechanisms of lipid peroxide formation in animal tissues,Biochem. J. 99, 667–676 (1966).

    PubMed  CAS  Google Scholar 

  17. P. D. Swanson, H. F. Bradford, and H. Mcllwain, Stimulation and stabilization of the sodium ion activated adenosine triphosphate of cerebral microsomes by surface active, especially polyoxyethylene ethers: actions of phospholipases and neuraminidase,Biochem. J. 92, 235–247 (1964).

    PubMed  CAS  Google Scholar 

  18. J. B. Martin and D. M. Dotty, Determination of inorganic phosphate: modification of isobutyl alcohol procedures,Anal. Chem. 21, 965–968, (1949).

    Article  CAS  Google Scholar 

  19. G. L. Ellman, K. D. Courtney, V., Jr. Anders, and R. M. Featherstone, A new and repid colorimetric determination of acetylcholinesterase activity,Biochem. Pharmacol. 7, 88–95 (1961).

    PubMed  Article  CAS  Google Scholar 

  20. J. R. Prohaska, D. A. Clark, and W. W. Wells, Improved rapidity and precision in the determination of Brain 2′,3′cyclic nucleotide 3′phosphohydrolase,Anal. Biochem. 56, 275–282 (1973).

    PubMed  Article  CAS  Google Scholar 

  21. O. H. Lowry, N. J. Rosebrough, A. L. Farr, and R. J. Randall, (1951) Protein measurement with Folin-Phenol reagent,J. Biol. Chem. 193, 265–275 (1951).

    PubMed  CAS  Google Scholar 

  22. F. Islam, K. Tayabba, and M. Hasan, Organophosphate metasystox induced increment of lipase activity and lipid peroxidation in cerebral hemispheres: diminution of lipids in discrete areas of rat brain,Acta Phramacol. Toxicol. 53, 121–124 (1983).

    CAS  Google Scholar 

  23. J. P. Kehrer, Free radicals as mediators of tissue injury and disease,Crit. Rev. Toxicol. 23, 21–48 (1993).

    PubMed  Article  CAS  Google Scholar 

  24. D. Julka and K. D. Gill, Altered calcium homeostasis: possible mechanism of aluminium induced neurotoxicity,Biochim. Biophys. Acta 1315, 47–54 (1996).

    PubMed  Google Scholar 

  25. M. L. Koenig and R. S. Jope, Aluminium inhibits fast phase of voltage-dependent calcium influx into synaptosomes,J. Neurochem. 49, 316–320 (1987).

    PubMed  Article  CAS  Google Scholar 

  26. S. Sarin, D. Julka, and K. D. Gill, Regional alterations in calcium homeostasis in the primate brain following chronic aluminium exposure,Mol Cell. Biochem. 168, 95–100 (1997).

    PubMed  Article  CAS  Google Scholar 

  27. M. Deleers, Cationic atmosphere and cation competition binding at negatively charged membranes: pathological implications of aluminium,Res. Commun. Chem. Pathol. Pharmacol. 49, 277–294 (1985).

    PubMed  CAS  Google Scholar 

  28. M. Deleers, J. P. Servais, and E. Wulfert, Neurotoxic cations induce membrane rigidification and membrane fusion at micromolar concentrations,Biochem. Biophys. Acta 855, 271–276 (1986).

    PubMed  Article  CAS  Google Scholar 

  29. M. Cochran, D. C. Elliott, P. Brennan, and V. Chawtur, Inhibition of protein kinase C activation by low concentration of aluminium,Clin. Chim. Acta 194, 167–172 (1990).

    PubMed  Article  CAS  Google Scholar 

  30. P. E. Godiei and F. R. Landesberger,13C nuclear magnetic resonance study of the dynamic structure of lecithin: cholesterol membranes and the position of stearic acid spin labels,Biochemistry 14, 3927–3933 (1975).

    Article  Google Scholar 

  31. S. Ando, Gangliosides in the nervous system,Int. Rev. Neurochem. 5, 507–537 (1983).

    Article  CAS  Google Scholar 

  32. I. Kracun, H. Rosner, C. Cosovic, and A. Savlgenic, Topographical atlas of the ganliosides of the adult human brain,J. Neurochem. 43, 979–989 (1984).

    PubMed  Article  CAS  Google Scholar 

  33. H. Rahman, Functional indication of gangliosides in uraemic rats treated with 24R, 25-Dihydroxy vitamin D3,Neuropathol. Appl. Neurobiol. 15, 55–62 (1983).

    Google Scholar 

  34. G. J. Quinlan, B. Halliwell, C. P. Moorhouse, and J. M. C. Gutteridge, Action of lead (II) and aluminium (III) ions on iron stimulated lipid peroxidation in liposomes, erythrocytes and rat liver microsomal fraction,Biochim. Biophys. Acta 962, 196–200 (1988).

    PubMed  CAS  Google Scholar 

  35. P. Oteiza, Aluminium has both oxidant and antioxidant effects in mouse brain membranes,Arch. Biochem. Biophys. 300, 517–521 (1993).

    PubMed  Article  CAS  Google Scholar 

  36. P. Ott, Membrane acetylcholinesterase: purification, molecular properties and interactions with amphiphilic environments,Biochim. Biophys. Acta. 822, 375–392 (1985).

    PubMed  CAS  Google Scholar 

  37. J. C. K. Lai, J. F. Guest, T. K. C. Leung, L. Lim, and A. N. Davison, The effect of cadmium, manganese and aluminium on Na+ K+ activated and magnesium activated adenosine triphosphatase activity and choline uptake in rat brain synaptosomes,Biochem. Pharmacol. 29, 141–146 (1980).

    PubMed  Article  CAS  Google Scholar 

  38. B. Roelofson, The specificity in the lipid requirement of calcium and (sodium plus potassium) transporting adenosine triphosphatase,Life Sci. 29, 2235–2247 (1981).

    Article  Google Scholar 

  39. A. G. Garcia, and S. M. Kirpekar, Inhibition of Na+K+ATPase and release of neurotransmitters,Nature 257, 722 (1975).

    PubMed  Article  CAS  Google Scholar 

  40. G. L. Schimdt, Development of biochemical activities associated with myelination in chick brain reaggregate cultures,Brain Res. 87, 110–113 (1975).

    Article  Google Scholar 

  41. K. A. Funk, C. H. Liu, B. W. Wilson, and R. J. Higgings, Avian embryonic brain reaggregate culture system, I: characterization for organophosphorus compound toxicity studies,Toxicol. Appl. Pharmacol. 124, 149–158 (1994).

    PubMed  Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Sarin, S., Gupta, V. & Gill, K.D. Alterations in lipid composition and neuronal injury in primates following chronic aluminium exposure. Biol Trace Elem Res 59, 133–143 (1997). https://doi.org/10.1007/BF02783238

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02783238

Index Entries

  • Aluminium
  • brain
  • lipids
  • membrane
  • monkey