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Silicon Reverses Lipid Peroxidation but not Acetylcholinesterase Activity Induced by Long-Term Exposure to Low Aluminum Levels in Rat Brain Regions

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Abstract

Aluminum (Al) is the most widely distributed metal in the environment and is extensively used in daily life leading to easy exposure to human beings. Besides not having a recognized physiological role, Al may produce adverse effects through the interaction with the cholinergic system contributing to oxidative stress. The present study evaluated, in similar conditions of parenteral nutrition, whether the reaction of silicon (SiO2) with Al3+ to form hydroxyaluminosilicates (HAS) reduces its bioavailability and toxicity through intraperitoneal administrations of 0.5 mg Al/kg/day and/or 2 mg Si/kg/day in Wistar rats. Al and Si concentrations were determined in rat brain tissue and serum. Acetylcholinesterase (AChE) activity and lipid peroxidation (LPO) were analyzed in the cerebellum, cortex, hippocampus, striatum, hypothalamus, and blood. An increase in the Al concentration was verified in the Al + Si group in the brain. All the groups demonstrated enhanced Si compared to the control animals. Al3+ increased LPO measured by thiobarbituric acid reactive substances (TBARS) in cerebellum and hippocampus, whereas SiO2 reduced it when compared with the control group. An increase of AChE activity was observed in the Al-treated group in the cerebellum whereas a decrease of this enzyme activity was observed in the cortex and hippocampus in the Al and Al + Si groups. Al and Si concentrations increased in rat serum; however, no effect was observed in blood TBARS levels and AChE activity. SiO2 showed a protective effect in the hippocampus and cerebellum against cellular damage caused by Al3+-induced lipid peroxidation. Thus, SiO2 may be considered an important protector in LPO induced by Al3+.

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References

  1. Verstraeten SV, Aimo L, Oteiza PI (2008) Aluminium and lead: molecular mechanisms of brain toxicity. Arch Toxicol 82:789–802

    Article  PubMed  CAS  Google Scholar 

  2. de Oliveira SMR, Bertagnolli D, Bohrer D, et al (2005) Nível Sérico de Alumínio: Influência da Água e de Alimentos Ingeridos Por Pacientes Com Insuficiência Renal Crônica Mantidos em Hemodiálise. J Bras Nefrol 27:101–109

    Google Scholar 

  3. Priest ND, Talbot RJ, Newton D, et al (1998) Uptake by man of aluminium in a public water supply. Hum Exp Toxicol 17:296–301

    Article  PubMed  CAS  Google Scholar 

  4. Alvarez L, Rebollido M, Fernandez-Lorenzo JR, et al (2007) Electrothermal atomic absorption spectrometry determination of aluminium in parenteral nutrition and its components. J Trace Elem Med Biol 21(Suppl 1):29–30

    Article  PubMed  CAS  Google Scholar 

  5. Bohrer D, do Nascimento PC, Binotto R, et al (2002) Contribution of the raw material to the aluminum contamination in parenterals. JPEN J Parenter Enteral Nutr 26:382–388

    Article  PubMed  CAS  Google Scholar 

  6. Llopis LS, Díez FB (2002) Revisión de los estudios sobre exposición al aluminio y enfermedad de Alzheimer. Rev Esp Salud Pública 76:645–658

    Article  Google Scholar 

  7. Alvarez EM, Otero RS, Ameijeiras AH, et al (2001) Effects of aluminum and zinc on the oxidative stress caused by 6-hydroxydopamine autoxidation: relevance for the pathogenesis of Parkinson’s disease. Biochim Biophys Acta 1586:155–168

    Article  Google Scholar 

  8. Golub MS, Han B, Keen CL (1996) Developmental patterns of aluminum and five essential mineral elements in the central nervous system of the fetal and infant Guinea pig. Biol Trace Elem Res 55:241–251

    Article  PubMed  CAS  Google Scholar 

  9. Savory J, Huang Y, Herman MM, Wills MR (1996) Quantitative image analysis of temporal changes in tau and neurofilament proteins during the course of acute experimental neurofibrillary degeneration; non-phosphorylated epitopes precede phosphorylation. Brain Res 707:272–281

    Article  PubMed  CAS  Google Scholar 

  10. Kaizer RR, Correa MC, Spanevello RM, et al (2005) Acetylcholinesterase activation and enhanced lipid peroxidation after long-term exposure to low levels of aluminum on different mouse brain regions. J Inorg Biochem 99:1865–1870

    Article  PubMed  CAS  Google Scholar 

  11. Sharma D, Sethi P, Hussain E, Singh R (2009) 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. Biogerontology 10:489–502

    Article  PubMed  CAS  Google Scholar 

  12. Moro MA, Almeida A, Bolanos JP, Lizasoain I (2005) Mitochondrial respiratory chain and free radical generation in stroke. Free Radic Biol Med 39:1291–1304

    Article  PubMed  CAS  Google Scholar 

  13. Mesulam MM, Guillozet A, Shaw P, et al (2002) Acetylcholinesterase knockouts establish central cholinergic pathways and can use butyrylcholinesterase to hydrolyze acetylcholine. Neuroscience 110:627–639

    Article  PubMed  CAS  Google Scholar 

  14. Appleyard ME (1992) Secreted acetylcholinesterase: non-classical aspects of a classical enzyme. Trends Neurosci 15:485–490

    Article  PubMed  CAS  Google Scholar 

  15. Soreq H, Seidman S (2001) Acetylcholinesterase-new roles for an old actor. Nat Rev Neurosci 2:294–302

    Article  PubMed  CAS  Google Scholar 

  16. Worek F, Reiter G, Eyer P, Szinicz L (2002) Reactivation kinetics of acetylcholinesterase from different species inhibited by highly toxic organophosphates. Arch Toxicol 76:523–529

    Article  PubMed  CAS  Google Scholar 

  17. Pailler FM, Bequet D, Corbé H, Giudicelli CP (1995) Aluminum, hypothetic cause of Alzheimer disease. Presse Med 24:489–490

    PubMed  CAS  Google Scholar 

  18. Bilkei-Gorzo A (1993) Neurotoxic effect of enteral aluminium. Food Chem Toxicol 31:357–361

    Article  PubMed  CAS  Google Scholar 

  19. Platt B, Fiddler G, Riedel G, Henderson Z (2001) Aluminium toxicity in the rat brain: histochemical and immunocytochemical evidence. Brain Res Bull 55:257–267

    Article  PubMed  CAS  Google Scholar 

  20. Calabrese V, Bates TE, Stella AM (2000) NO synthase and NO-dependent signal pathways in brain aging and neurodegenerative disorders: the role of oxidant/antioxidant balance. Neurochem Res 25:1315–1341

    Article  PubMed  CAS  Google Scholar 

  21. Exley C (2004) The pro-oxidant activity of aluminum. Free Radic Biol Med 36:380–387

    Article  PubMed  CAS  Google Scholar 

  22. Wu ZH, Du YM, Xue H, et al (2012) Aluminum induces neurodegeneration and its toxicity arises from increased iron accumulation and reactive oxygen species (ROS) production. Neurobiol Aging 33:199.e1–199.e12

    Article  CAS  Google Scholar 

  23. Chumlea WC (2007) Silica, a mineral of unknown but emerging health importance. J Nutr Health Aging 11:93

    PubMed  Google Scholar 

  24. Perez-Granados AM, Vaquero MP (2002) Silicon, aluminium, arsenic and lithium: essentiality and human health implications. J Nutr Health Aging 6:154–162

    PubMed  CAS  Google Scholar 

  25. Pérez JCR, Mancilla CLA (2012) El Papel del Silicio en los Organismos y Ecosistemas. Conciencia Tecnológica 43:42–46

    Google Scholar 

  26. Bohrer D, do Nascimento PC, Binotto R, Becker E (2003) Influence of the glass packing on the contamination of pharmaceutical products by aluminium. Part III: interaction container-chemicals during the heating for sterilisation. J Trace Elem Med Biol 17:107–115

    Article  PubMed  CAS  Google Scholar 

  27. Bohrer D, Bortoluzzi F, Nascimento PC, et al (2008) Silicate release from glass for pharmaceutical preparations. Int J Pharm 355:174–183

    Article  PubMed  CAS  Google Scholar 

  28. Bohrer D, do Nascimento PC, Martins P, Binotto R (2002) Availability of aluminum from glass and an Al form ion exchanger in the presence of complexing agents and amino acids. Anal Chim Acta 459:267–27635

    Article  CAS  Google Scholar 

  29. Swaddle TW (2001) Silicate complexes of aluminum(III) in aqueous systems. Coord Chem Rev 219:665–686

    Article  Google Scholar 

  30. Reffitt DM, Jugdaohsingh R, Thompson RPH, Powell JJ (1999) Silicic acid: its gastrointestinal uptake and urinary excretion in man and effects on aluminium excretion. J Inorg Biochem 76:141–147

    Article  PubMed  CAS  Google Scholar 

  31. Rondeau V, Commenges D, Jacqmin-Gadda H, Dartigues JF (2000) Relation between aluminum concentrations in drinking water and Alzheimer’s disease: an 8-year follow-up study. Am J Epidemiol 152:59–66

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  32. Jacqmin-Gadda H, Commenges D, Letenneur L, et al (1996) Silica and aluminium in drinking water and cognitive impairment in the elderly. Epidemiology 7:281–285

    Article  PubMed  CAS  Google Scholar 

  33. Gillette-Guyonnet S, Andrieu S, Vellas B (2007) The potential influence of silica presents in drinking water on Alzheimer’s disease and associated disorders. J Nutr Health Aging 11:119–124

    PubMed  CAS  Google Scholar 

  34. Desouky M, Jugdaohsingh R, Catherine R, et al (2002) Aluminum-dependent regulation of intracellular silicon in the aquatic invertebrate Lymnaea stagnalis. Proc Natl Acad Sci 99:3394–3399

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  35. White KN, Ejim AI, Walton RC, et al (2008) Avoidance of aluminum toxicity in freshwater snails involves intracellular silicon-aluminum biointeraction. Environ. Sci Technol 42:2189–2194

    Article  PubMed  CAS  Google Scholar 

  36. Gura KM, Pharm D (2010) Aluminum contamination in products used in parenteral nutrition: has anything changed? Nutrition 26:585–594

    Article  PubMed  CAS  Google Scholar 

  37. Klein CJ, Nielsen FH, Moser-Veillon PB (2008) Trace element loss in urine and effluent following traumatic injury. J Parenteral Enteral Nutr 32:129–139

    Article  CAS  Google Scholar 

  38. Noremberg S, Veiga M, Bohrer D, et al (2015) Determination of aluminum and silicon in bovine liver by graphite furnace atomic absorption spectrometry after dissolution with tetramethylammonium hydroxide. Anal Methods 7:500–506

    Article  CAS  Google Scholar 

  39. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95

    Article  PubMed  CAS  Google Scholar 

  40. Rocha JBT, Emanuelli T, Pereira ME (1993) Effects of early undernutrition on kinetic parameters of brain acetylcholinesterase from adult rats. Acta Neurobiol Exp 53:431–437

    CAS  Google Scholar 

  41. Worek F, Mast U, Kiderlen D, et al (1999) Improved determination of acetylcholinesterase activity in human whole blood. Clin Chim Acta 288:73–90

    Article  PubMed  CAS  Google Scholar 

  42. Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  PubMed  CAS  Google Scholar 

  43. Rossato JI, Zeni G, Mello CF, et al (2002) Ebselen blocks the quinolinic acid-induced production of thiobarbituric acid reactive species but does not prevent the behavioral alterations produced by intra-striatal quinolinic acid administration in the rat. Neurosci Lett 318:137–140

    Article  PubMed  CAS  Google Scholar 

  44. Jentzsch AM, Bachmann H, Furst P, Biesalski HK (1996) Improved analysis of malondialdehyde in human body fluids. Free Radic Biol Med 20:251–256

    Article  PubMed  CAS  Google Scholar 

  45. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  46. Birchall JD, Chappell JS (1989) Aluminium, water chemistry, and Alzheimer’s disease. Lancet 29:953

    Article  Google Scholar 

  47. Gonzalez-Munoz MJ, Meseguer I, Sanchez-Reus MI, et al (2008) Beer consumption reduces cerebral oxidation caused by aluminum toxicity by normalizing gene expression of tumor necrotic factor alpha and several antioxidant enzymes. Food Chem Toxicol 46:1111–1118

    Article  PubMed  CAS  Google Scholar 

  48. Srivastava RAK, Jain JC (2002) Scavenger receptor class B type I expression and elemental analysis in cerebellum and parietal cortex regions of the Alzheimer’s disease brain. J Neurol Sci 196:45–52

    Article  PubMed  CAS  Google Scholar 

  49. Bronner F (2008) Metals in bone: aluminum, boron, cadmium, chromium, silicon, and strontium lead. In: Bilezikian JP, Raisz LG, Martin TJ (eds) Principles of bone biology, 3rd edn. Academic Press, San Diego, pp. 515–531

    Chapter  Google Scholar 

  50. Amador FC, Santos MS, Oliveira CR (2001) Lipid peroxidation and aluminium effects on the cholinergic system in nerve terminals. Neurotox Res 3:223–233

    Article  PubMed  CAS  Google Scholar 

  51. Dua R, Gill KD (2001) Aluminium phosphide exposure: implications on rat brain lipid peroxidation and antioxidant defence system. Pharmacol Toxicol 89:315–319

    Article  PubMed  CAS  Google Scholar 

  52. Yousef MI (2004) Aluminium-induced changes in hemato-biochemical parameters, lipid peroxidation and enzyme activities of male rabbits: protective role of ascorbic acid. Toxicology 199:47–57

    Article  PubMed  CAS  Google Scholar 

  53. Bondy SC, Cambell A (2001) Oxidative and inflammatory properties of aluminium possible relevance in Alzheimer’s disease. In: Exley C (ed) Aluminium and Alzheimer’s disease, 1st edn. Elsevier Science, Amsterdam, pp. 311–321

    Chapter  Google Scholar 

  54. Stohs SJ, Bagchi D (1995) Oxidative mechanisms in the toxicity of metal ions. Free Radic Biol Med 18:321–336

    Article  PubMed  CAS  Google Scholar 

  55. Abubakar MG, Taylor A, Ferns GA (2004) Regional accumulation of aluminium in the rat brain is affected by dietary vitamin E. J Trace Elem Med Biol 18:53–59

    Article  PubMed  CAS  Google Scholar 

  56. Kaur J, Singh S, Sharma D, Singh R (2003) Aluminium-induced enhancement of ageing-related biochemical and electrophysiological parameters in rat brain regions. Indian J Biochem Biophys 40:330–339

    PubMed  CAS  Google Scholar 

  57. Pratico D, Delanty N (2000) Oxidative injury in diseases of the central nervous system: focus on Alzheimer’s disease. Am J Med 109:577–585

    Article  PubMed  CAS  Google Scholar 

  58. Campbell A, Prasad KN, Bondy SC (1999) Aluminum-induced oxidative events in cell lines: glioma are more responsive than neuroblastoma. Free Radic Biol Med 26:1166–1171

    Article  PubMed  CAS  Google Scholar 

  59. Yokel RA (2000) The toxicology of aluminum in the brain: a review. Neurotoxicology 21:813–828

    PubMed  CAS  Google Scholar 

  60. da Silva AC, Rocha JB, Morsch AL, et al (2007) Oxidative stress and delta-ALA-D activity in chronic renal failure patients. Biomed Pharmacother 61:180–185

    Article  PubMed  CAS  Google Scholar 

  61. Gomez M, Esparza JL, Nogues MR, et al. (2005) Pro-oxidant activity of aluminum in the rat hippocampus: gene expression of antioxidant enzymes after melatonin administration. Free Radic Biol Med 38:104–111

    Article  PubMed  CAS  Google Scholar 

  62. Bhadauria M (2012) Combined treatment of HEDTA and propolis prevents aluminum induced toxicity in rats. Food Chem Toxicol 50:2487–2495

    Article  PubMed  CAS  Google Scholar 

  63. Flora SJ, Mehta A, Satsangi K, et al (2003) Aluminum-induced oxidative stress in rat brain: response to combined administration of citric acid and HEDTA. Comp Biochem Physiol C Toxicol Pharmacol 134:319–328

    Article  PubMed  CAS  Google Scholar 

  64. Oddo S, LaFerla FM (2006) The role of nicotinic acetylcholine receptors in Alzheimer’s disease. J Physiol Paris 99:172–179

    Article  PubMed  CAS  Google Scholar 

  65. Perry EK, Perry RH (1980) In: Roberts PJ (ed) Biochemistry of dementia. John Wiley & Sons, Chichester, pp. 135–183

    Google Scholar 

  66. Olney JW, Collins RC, Sloviter RS (1986) Excitotoxic mechanisms of epileptic brain damage. Adv Neurol 44:857–877

    PubMed  CAS  Google Scholar 

  67. Ecobichon DJ (1996) Toxic effects of pesticides. In: Klaassen CD, Doull J (eds) Casarett and Doull’s toxicology: the basic science of poisons, 5th edn. McGraw-Hill, New York, pp. 643–689

    Google Scholar 

  68. Exley C, Birchall JD (1992) The cellular toxicity of aluminium. J Theor Biol 159:83–98

    Article  PubMed  CAS  Google Scholar 

  69. Caccamo A, Oddo S, Sugarman MC, et al (2005) Age- and region-dependent alterations in Abeta-degrading enzymes: implications for Abeta-induced disorders. Neurobiol Aging 26:645–654

    Article  PubMed  CAS  Google Scholar 

  70. Arendt T, Bigl V, Tennstedt A, Arendt A (1984) Correlation between cortical plaque count and neuronal loss in the nucleus basalis in Alzheimer’s disease. Neurosci Lett 48:81–85

    Article  PubMed  CAS  Google Scholar 

  71. Kumar S (1999) Aluminium-induced biphasic effect. Med Hypotheses 52:557–559

    Article  PubMed  CAS  Google Scholar 

  72. Dave KR, Syal AR, Katyare SS (2002) Effect of long-term aluminum feeding on kinetics attributes of tissue cholinesterases. Brain Res Bull 58:225–233

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was supported by CNPq (grant 477258/2010–7) and the Federal University of Santa Maria, RS, Brazil.

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The authors declare that they have no conflict of interest.

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Noremberg, S., Bohrer, D., Schetinger, M.R.C. et al. Silicon Reverses Lipid Peroxidation but not Acetylcholinesterase Activity Induced by Long-Term Exposure to Low Aluminum Levels in Rat Brain Regions. Biol Trace Elem Res 169, 77–85 (2016). https://doi.org/10.1007/s12011-015-0392-6

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