Toxicological Research

Korean Society of Toxicology & Korea Environmental Mutagen Society (한국독성학회)
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Evaluation of Some Biochemical Parameters and Brain Oxidative Stress in Experimental Rats Exposed Chronically to Silver Nitrate and the Protective Role of Vitamin E and Selenium

  • Gueroui, Mouna (Laboratory of Applied Biochemistry and Microbiology, Department of Biochemistry, Science faculty, Badji Mokhtar University) ;
  • Kechrid, Zine (Laboratory of Applied Biochemistry and Microbiology, Department of Biochemistry, Science faculty, Badji Mokhtar University)
  • Received : 2016.03.28
  • Accepted : 2016.08.18
  • Published : 2016.10.15
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Abstract

Due to undesirable hazardous interactions with biological systems, this investigation was undertaken to evaluate the effect of chronic exposure to silver on certain biochemical and some oxidative stress parameters with histopathological examination of brain, as well as the possible protective role of selenium and/or vitamin E as nutritional supplements. Thirty six male rats were divided into six groups of six each: the first group used as a control group. Group II given both vitamin E (400 mg/kg) of diet and selenium (Se) (1 mg/L) in their drinking water. Group III given silver as silver nitrate ($AgNO_3$) (20 mg/L). Group IV given vitamin E and $AgNO_3$. Group V given both $AgNO_3$ and selenium. Group VI given $AgNO_3$, vitamin E and Se. The animals were in the same exposure conditions for 3 months. According to the results which have been obtained; there was an increase in serum lactate dehydrogenase (LDH), lipase activities and cholesterol level, a decrease in serum total protein, calcium and alkaline phosphatase (ALP) activity in Ag-intoxicated rats. Moreover, the findings showed that $Ag^+$ ions affected antioxidant defense system by decreasing superoxide dismutase (SOD) activity and increasing vitamin E concentration with a high level of malondialdehyde (MDA) in brain tissue. The histological examination also exhibited some nervous tissue alterations including hemorrhage and cytoplasm vacuolization. However, the co-administration of selenium and/or vitamin E ameliorated the biochemical parameters and restored the histological alterations. In conclusion, this study indicated that silver could cause harmful effects in animal body and these effects can be more toxic in high concentrations or prolonged time exposure to this metal. However, selenium and vitamin E act as powerful antioxidants which may exercise adverse effect against the toxicity of this metal.

Keywords

References

  1. Powers, C.M., Wrench, N., Ryde, I.T., Smith, A.M., Seidler, F.J. and Slotkin, T.A. (2010) Silver impairs neurodevelopment: studies in PC12 cells. Environ. Health Perspect., 118, 73-79.
  2. Lee, Y., Choi, J., Kim, P., Choi, K., Kim, S., Shon, W. and Park, K. (2012) A transfer of silver nanoparticles from pregnant rat to offspring. Toxicol. Res., 28, 139-141. https://doi.org/10.5487/TR.2012.28.3.139
  3. Roh, J.Y., Eom, H.J. and Choi, J. (2012) Involvement of caenohabditis elegans MAPK signaling pathways in oxidative stress response induced by silver nanoparticles exposure. Toxicol. Res., 28, 19-24. https://doi.org/10.5487/TR.2012.28.1.019
  4. Kwon, J.T., Minai-Tehrani, A., Hwang, S.K., Kim, J.E., Shin J.Y., Yu, K.N., Chang, S.H., Kim, D.S., Kwon, Y.T., Choi, I.J., Cheong, Y.H., Kim, J.S. and Cho, M.H. (2012) Acute pulmonary toxicity and body distribution of inhaled metallic silver nanoparticles. Toxicol. Res., 28, 25-31. https://doi.org/10.5487/TR.2012.28.1.025
  5. WHO (1996) Silver in drinking-water in Guidelines for drinking-water quality (2nd edition, Volume 2), World Health Organization, Geneva, pp. 338-343.
  6. Holler, J.S., Fawler, B.A. and Nordberg, G.R. (2015) Handbook on the toxicology of metals: Silver (4th edition), Elsevier, pp. 1209-1216.
  7. Ohbo, Y., Fukuzako, H., Takeuchi, K. and Takigawa, M. (1996) Argyria and convulsive seizures caused by ingestion of silver in a patient with schizophrenia. Psychiatry Clin. Neurosci., 50, 89-90. https://doi.org/10.1111/j.1440-1819.1996.tb01669.x
  8. Landas, S., Fischer, J., Wilkin, L.D., Mitchell, L.D., Johnson, A.K., Turner, J.W., Theriac, M. and Moore, K.C. (1985) Demonstration of regional blood-brain barrier permeability in human brain. Neurosci. Lett., 57, 251-256. https://doi.org/10.1016/0304-3940(85)90500-2
  9. Rungby, J. and Danscher, G. (1984) Hypoactivity in silver exposed mice. Acta Pharmacol. Toxicol. (Copenh.), 55, 398-401.
  10. Rungby, J., Slomianka, L., Danscher, G., Andersen, A.H. and West, M.J. (1987) A quantitative evaluation of the neurotoxic effect of silver on the volumes of the components of the developing rat hippocampus. Toxicology, 43, 261-268. https://doi.org/10.1016/0300-483X(87)90085-0
  11. Serafín Munoz, A.H., Wrobel, K., Gutierrez Corona, J.F. and Wrobel, K. (2007) The protective effect of selenium inorganic forms against cadmium and silver toxicity in mycelia of Pleurotus ostreatus. Mycol. Res., 111, 626-632. https://doi.org/10.1016/j.mycres.2007.03.002
  12. Letavayova, L., Vlasakova, D., Spallholz, J.E., Brozmanova, J. and Chovanec, M. (2008) Toxicity and mutagenicity of selenium compounds in Saccharomyces cerevisiae. Mutat. Res., 638, 1-10. https://doi.org/10.1016/j.mrfmmm.2007.08.009
  13. Ben Amara, I., Soudani, N., Hakim, A., Troudi, A., Zeghal, K.M., Boudawara, T. and Zeghal, N. (2011) Selenium and vitamin E, natural antioxidants, protect rat cerebral cortex against dimethoate-induced neurotoxicity. Pestic. Biochem. Physiol., 101, 165-174. https://doi.org/10.1016/j.pestbp.2011.08.012
  14. Peterson, R.P. and Jensen, L.S. (1972) Poult. Sci., 51, 1849.
  15. Kabay, S.C., Ozden, H., Guven, G., Ustuner, M.C., Degirmenci, I., Olgun, E.G. and Unal, N. (2009) Protective effects of vitamin E on central nervous system in streptozotocin-induced diabetic rats. Clin. Invest. Med., 32, E314-E321. https://doi.org/10.25011/cim.v32i5.6918
  16. Chow, C.K. (1990) Effects of dietary vitamin E and selenium on rats: pyruvate kinase, glutathione peroxidase and oxidative damage. Nutr. Res., 10, 183-194. https://doi.org/10.1016/S0271-5317(05)80606-2
  17. Chow, C.K. (1988) Interrelation ship of antioxidant defense systems in Cellular Antioxidant Defense Mechanisms, Vol. 2 (Chow, C.K. Ed.). CRC Press Inc., Boca Raton, pp. 217-237.
  18. US Environmental Protection Agency (1980) Ambient water quality criteria for silver, Washington (EPA 440/5-80-071).
  19. Kim, K.R., Kim, J.K. and Rhee, S.J. (2001) Effects of vitamin E on arachidonic acid cascade in platelets and aorta of acute cadmium-poisoned rats. Nutr. Res., 21, 657-665. https://doi.org/10.1016/S0271-5317(01)00265-2
  20. Wu, Q., Huang, K. and Xu, H. (2003) Effects of long-term selenium deficiency on glutathione peroxidase and thioredoxin reductase activities and expressions in rat aorta. J. Inorg. Biochem., 94, 301-306. https://doi.org/10.1016/S0162-0134(03)00058-8
  21. Esterbauer, H. and Cheeseman, K. (1990) Determination of aldehydic lipid peroxidation products: malonaldehyde and 4-hydroxynonenal. Meth. Enzymol., 186, 407-421. https://doi.org/10.1016/0076-6879(90)86134-H
  22. Misra, H.P. and Fridovich, I. (1977) Superoxide dismutase: "positive" spectrophotometric assays. Anal. Biochem., 79, 553-560. https://doi.org/10.1016/0003-2697(77)90429-8
  23. Flohe, L. and Gunzler, W.A. (1984) Analysis of glutathione peroxidase. Meth. Enzymol., 105, 114-121. https://doi.org/10.1016/S0076-6879(84)05015-1
  24. Habig, W.H., Pabst, M.J. and Jakoby, W.B. (1974) Glutathione S-transferase. The first enzymatic step in mercapturic acid formation. J. Biol. Chem., 249, 7130-7139.
  25. Goldberg, D.M. and Spooner, R.J. (1983) Methods of enzymatic analysis (Bergmeyen, H.V. Ed.). VerlogChemie, Deerfield Beach, pp. 258-265.
  26. Sinha, A.K. (1972) Colorimetric assay of catalase. Anal. Biochem., 47, 389-394. https://doi.org/10.1016/0003-2697(72)90132-7
  27. Ellman, G.L. (1959) Tissue sulfhydryl groups. Arch. Biochem. Biophys., 82, 70-77. https://doi.org/10.1016/0003-9861(59)90090-6
  28. Desai, I.D. (1984) Vitamin E analysis method for animal tissue. Methods Enzymol., 105, 138-147. https://doi.org/10.1016/S0076-6879(84)05019-9
  29. Bradford, M.M. (1976) A rapid and sensitive method for the quantities of microgram quantities of protein utilizing the principle of protein binding. Anal. Biochem., 72, 248-254. https://doi.org/10.1016/0003-2697(76)90527-3
  30. Hould, R. (1984) Techniques d'histopathologie et de cytopathologie. Ed Maloine., 19-21, 225-227.
  31. Kim, Y.S., Song, M.Y., Park, J.D., Song, K.S., Ryu, H.R., Chung, Y.H., Chang, H.K., Lee, J.H., Oh, K.H., Kelman, B.J., Hwang, I.K. and Yu, I.J. (2010) Subchronic oral toxicity of silver nanoparticles. Part. Fibre Toxicol., 7, 20. https://doi.org/10.1186/1743-8977-7-20
  32. Burtis, C.A. and Ashwood, E.R. (1999) Tietz textbook of clinical chemistry (3rd edition), Saunders, Philadelphia.
  33. Evans, G.O., O'Brien, P.J. and Watterson, C.L. (2009) Animal clinical chemistry, Taylor & Francis Group, Boca Raton.
  34. Kim, Y.S., Kim, J.S., Cho, H.S., Rha, D.S., Kim, J.M., Park, J.D., Choi, B.S., Lim, R., Chang, H.K., Chung, Y.H., Kwon, I.H., Jeong, J., Han, B.S. and Yu, I.J. (2008) Twenty-eight-day oral toxicity, genotoxicity, and gender related tissue distribution of silver nanoparticles in Sprague Dawley rats. Inhal. Toxicol., 20, 575-583. https://doi.org/10.1080/08958370701874663
  35. Sung, J.H., Ji, J.H., Park, J.D., Yoon, J.U., Kim, D.S., Jeon, K.S., Song, M.Y., Jeong, J., Han, B.S., Han, J.H., Chung, Y.H., Chang, H.K., Lee, J.H., Cho, M.H., Kelman, B.J. and Yu, I.J. (2009) Subchronic inhalation toxicity of silver nanoparticles. Toxicol. Sci., 108, 452-61. https://doi.org/10.1093/toxsci/kfn246
  36. Das, K.K. and Dasgupta, S. (2000) Effect of nickel on testicular nucleic acid concentrations of rats on protein restriction. Biol. Trace Elem. Res., 73, 175-180. https://doi.org/10.1385/BTER:73:2:175
  37. Clarck, W.L., Balinski, E.L., Maie, S.S. and Zak, B. (1975) Spectrometric study of a direct determination of Serum Calcium. Microchem. J., 20, 22-32. https://doi.org/10.1016/0026-265X(75)90108-3
  38. Olcott, C.T. (1950) Experimental argyrosis; hypertrophy of the left ventricle of the heart in rats ingesting silver salts. AMA Arch. Pathol., 49, 138-149.
  39. Fung, M.C. and Bowen, D.L. (1996) Silver products for medical indications: risk-benefit assessment. J. Toxicol. Clin. Toxicol., 34, 119-126. https://doi.org/10.3109/15563659609020246
  40. Chow, C.K. (1985) Vitamin E and blood. World Rev. Nutr. Diet., 45, 133-166.
  41. Gueroui, M. and Kechrid, Z. (2015) Effect of the joint supplementation of vitamin E and selenium on chronic silver induced liver injury in male (wistar) albino rats. Int. J. Pharm. Sci. Rev. Res., 34, 176-182.
  42. Hadrup, N., Loeschner, K., Mortensen, A., Sharma, A.K., Qvortrup, K., Larsen, E.H. and Lam, H.R. (2012) The similar neurotoxic effects of nanoparticulate and ionic silver in vivo and in vitro. Neurotoxicology, 33, 416-423. https://doi.org/10.1016/j.neuro.2012.04.008
  43. Makar, T.K., Nedergaard, M., Preuss, A., Gelbard, A.S., Perumal, A.S. and Cooper, A.J. (1994) Vitamin E, ascorbate, glutathione, glutathione disulfide, and enzymes of glutathione metabolism in cultures of chick astrocytes and neurons: evidence that astrocytes play an important role in antioxidative processes in the brain. J. Neurochem., 62, 45-53.
  44. Devi, S.A. and Kiran, T.R. (2004) Regional responses in antioxidant system to exercise training and dietary Vitamin E in aging rat brain. Neurobiol. Aging, 25, 501-508. https://doi.org/10.1016/S0197-4580(03)00112-X
  45. Ilhan, A., Gurel, A., Armutcu, F., Kamisli, S., Iraz, M., Akyol, O. and Ozen, S. (2004) Ginkgo biloba prevents mobile phone-induced oxidative stress in rat brain. Clin. Chim. Acta, 340, 153-162. https://doi.org/10.1016/j.cccn.2003.10.012
  46. Lee, J. (2010) Use of antioxidants to prevent cyclosporine a toxicity. Toxicol. Res., 26, 163-170. https://doi.org/10.5487/TR.2010.26.3.163
  47. Nirwane, A., Sridhar, V. and Majumdar, A. (2016) Neurobehavioural changes and brain oxidative stress induced by acute exposure to GSM900 mobile phone radiations in Zebrafish (Danio rerio). Toxicol. Res., 32, 123-132. https://doi.org/10.5487/TR.2016.32.2.123
  48. Lee, J.G., Noh, W.J., Kim, H. and Lee M.Y. (2011) Generation of reactive oxygen species contributes to the development of carbon black cytotoxicity to vascular cells. Toxicol. Res., 27, 161-166. https://doi.org/10.5487/TR.2011.27.3.161
  49. Bourre, J.M., Dumonta, O., Cleament, M., Dinha, L., Droy- Lefaix, M.T. and Christen, Y. (2000) Vitamin E deficiency has different effects on brain and liver phospholipid hydroperoxide glutathione peroxidase activities in the rat. Neurosci. Lett., 286, 87-90. https://doi.org/10.1016/S0304-3940(00)01095-8
  50. Otitoju, O., Onwurah, I.N.E., Otitoju, G.T.O. and Ugwu, C.E. (2008) Oxidative stress and superoxide dismutase activity in brain of rats fed with diet containing permethrin. Biokemistri, 20, 93-98.
  51. Park, H.J., Kim, J.Y., Ki, J., Lee, J.H., Hahn, J.S., Gu, M.B. and Yoon, J. (2009) Silver-ion-mediated reactive species generation affecting bactericidal activity. Water Res., 43, 1027-1032. https://doi.org/10.1016/j.watres.2008.12.002
  52. Cortese-Krott, M.M., Munchow, M., Pirev, E., Hebner, F., Bozkurt, A., Uciechowski, P., Pallua, N., Kroncke, K.D. and Suschek, C.V. (2009) Silver ions induce oxidative stress and intracellular zinc release in human skin fibroblasts. Free Radic. Biol. Med., 47, 1570-1577. https://doi.org/10.1016/j.freeradbiomed.2009.08.023
  53. Almofti, M.R., Ichikawa, T., Yamashita, K., Terada, H. and Shinohara, Y. (2003) Silver ion induces a cyclosporine a-insensitive permeability transition in rat liver mitochondria and release of apoptogenic cytochrome C. J. Biochem., 134, 43-49. https://doi.org/10.1093/jb/mvg111
  54. Ognjanovic, B.I., Pavlovic, S.Z., Maletic, S.D., Zikic, R.V., Stajn, A.S., Radojicic, R.M., Saicic, Z.S. and Petrovic, V.M. (2003) tective influence of vitamin E on antioxidant defense system in the blood of rats treated with cadmium. Physiol. Res., 52, 563-570.
  55. van der Zande, M., Vanderbriel, R.J., Van Doren, E., Kramer, E., Herrera Rivera, Z., Serrano-Rojero, C.S., Gremmer, E.R., Mast, J., Peters, R.J., Hollman, P.C., Hendriksen, P.J., Marvin, H.J., Peijnenburg, A.A. and Bouwmeester, H. (2012) Distribution, elimination, and toxicity of silver nanoparticles and silver ions in rats after 28-day oral exposure. ACS Nano, 6, 7427-7442. https://doi.org/10.1021/nn302649p
  56. Liu, F., Mahmood, M., Xu, Y., Watanabe, F., Biris, A.S., Hansen, D.K., Inselman, A., Casciano, D., Patterson, T.A., Paule, M.G., Slikker, W. Jr. and Wang, C. (2015) ffects of silver nanoparticles on human and rat embryonic neural stem cells. Front. Neurosci., 9, 115.
  57. Yin, N., Yao, X., Zhou, Q., Faiola, F. and Jiang G. (2015) Vitamin E attenuates silver nanoparticle-induced effects on body weight and neurotoxicity in rats. Biochem. Biophys. Res. Commun., 458, 405-410. https://doi.org/10.1016/j.bbrc.2015.01.130

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