Skip to main content
Log in

Alteration of trace element distribution and testis ACE activity in mice with high peritoneal aluminum

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

The present investigation was conducted to assess the effects of subacute aluminum (Al) exposure on testicular zinc (Zn), copper (Cu), and iron (Fe) distribution in mice. Animals were intraperitoneally exposed to 0, 13, or 35 mg Al/kg body weight/d for a period of 14 d. Al concentrations in serum and testis in Al-treated animals were significantly higher than those of controls. The serum concentrations of Fe were lower, whereas serum Zn and Cu showed a pattern comparable to that of controls. The accumulation of testicular Fe and Cu remarkably increased in Al-exposed groups, whereas the Zn concentration in testis was significantly reduced only at the highest dose of Al exposure. The values of testicular thiobarbituric acid reactive substances (TBARS) were also increased after Al administration, indicating increased lipid peroxidation and oxidative stress. In addition, when the testicular Al was increased, the testis-specific angiotensin-converting enzyme (testis ACE) was noted. The results of this study indicated that part of the effect of Al intoxication on testis might contribute to abnormal metabolism of other minerals, such as Fe, Zn, and/or Cu. It was also suggested that reduced testis ACE activity presumably plays an important role in oxidative damage of Al-induced testicular toxicity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. E. Reusche, B. Lindner, and H. Arnholdt, Widespread aluminum deposition in extracerebral organ systems of patients with dialysis-associated encephalopathy, Virchows Arch. 424, 105–112 (1994).

    Article  PubMed  CAS  Google Scholar 

  2. E. B. Dawson, D. R. Evans, W. A. Harris, and L. C. Powell, Seminal plasma trace metal levels in industrial workers, Biol. Trace Element Res. 74, 97–105 (2000).

    Article  CAS  Google Scholar 

  3. E. B. Dawson, S. Ritter, W. A. Harris, D. R. Evans, and L. C. Powell, Comparison of sperm viability with seminal plasma metal levels, Biol. Trace Element Res. 64, 215–219 (1998).

    CAS  Google Scholar 

  4. O. Hovatta, E. R. Venäläinen, L. Kuusimäki, J. Heikkilä, T. Hirvi, and I. Reima, Aluminum, lead and cadmium concentrations in seminal plasma and spermatozoa, and semen quality in Finnish men, Hum. Reprod. 13, 115–119 (1998).

    Article  PubMed  CAS  Google Scholar 

  5. B. Sjögren, I. Lundberg, and V. Lidums, Aluminum in the blood and urine of industrially exposed workers, Br. J. Ind. Med. 40, 301–304 (1983).

    PubMed  Google Scholar 

  6. C. G. Elinder, L. Ahrengart, V. Lidums, E. Pettersson, and B. Sjögren, Evidence of aluminum accumulation in aluminum welders, Br. J. Ind. Med. 48, 735–738 (1991).

    PubMed  CAS  Google Scholar 

  7. A. K. Roy, G. Talukder, and A. Sharma, Similar effects in vivo of two aluminum salts on the liver, kidney, bone, and brain of Rattus norvegicus, Bull. Environ. Contam. Toxicol. 47, 288–295 (1991).

    Article  PubMed  CAS  Google Scholar 

  8. J. M. Llobet, M. T. Colomina, J. J. Sirvent, J. L. Domingo, and J. Corbella, Reproductive toxicology of aluminum in male mice, Fundam. Appl. Toxicol. 25, 45–51 (1995).

    Article  PubMed  CAS  Google Scholar 

  9. H. Bataineh, M. H. Al-Hamood, and A. M. Elbetieha, Assessment of aggression, sexual behavior and fertility in adult male rat following long-term ingestion of four industrial metals salts, Human Exp. Toxicol. 17, 570–576 (1998).

    Article  CAS  Google Scholar 

  10. C. H. Guo, C. J. Huang, S. T. Chen, and G-S. W. Hsu, Serum and testicular testosterone and nitric oxide products in aluminum-treated mice, Environ. Toxicol. Pharmacol. 10, 53–60 (2001).

    Article  CAS  PubMed  Google Scholar 

  11. J-P. Stéphan, C. Guillemois, B. Jégou, and F. Bauché, Nitric oxide production by Sertoli cells in response to cytokines and lipopolysaccharide, Biochim. Biophys. Res. Commun. 213, 218–224 (1995).

    Article  Google Scholar 

  12. J. L. Greger, E. N. Bula, and E. T. Gum, Mineral metabolism of rats fed moderate levels of various aluminum compounds for short periods of time, J. Nutr. 115, 1708–1716 (1985).

    PubMed  CAS  Google Scholar 

  13. M. S. Yang, H. F. Wong, and K. L. Yung, Determination of endogenous trace metal contents in various mouse brain regions after prolonged oral administration of aluminum chloride, J. Toxicol. Environ. Health 55, 445–453 (1998).

    Article  CAS  Google Scholar 

  14. S. A. Hamdi, O. I. Nassif, and M. S. M. Ardawi, Effect of marginal or severe dietary zinc deficiency on testicular development and functions of the rat, Arch. Androl. 38, 243–253 (1997).

    PubMed  CAS  Google Scholar 

  15. K. M. Hambidge, Mild zinc deficiency in human subjects, in Zinc in Human Biology, C. F. Mills, ed., Springer-Verlag, London, pp. 281–296 (1989).

    Google Scholar 

  16. A. E. Favier, The role of zinc in reproduction. Hormonal mechanisms, Biol. Trace Element Res. 32, 363–382 (1992).

    CAS  Google Scholar 

  17. F. E. Van Niekerk and C. H. Van Niekerk, The influence of experimentally induced copper deficiency on the fertility of rams. II. Macro- and microscopic changes in the testes, J. S. Afr. Vet. Assoc. 60, 32–35 (1989).

    PubMed  Google Scholar 

  18. K. P. Skandhan, Review on copper in male reproduction and contraception, Rev. Fr. Gynecol. Obstet. 87, 594–598 (1992).

    PubMed  CAS  Google Scholar 

  19. J. Huggenvik, S. R. Sylvester, and M. D. Griswold, Control of transferrin mRNA synthesis in Sertoli cells, Ann. NY Acad. Sci. 438, 1–7 (1984).

    Article  PubMed  CAS  Google Scholar 

  20. M. P. Cuajungco, L. E. Goldstein, A. Nunomura, M. A. Smith, J. T. Lim, C. S. Atwood, et al., Evidence that the beta-amyloid plaques of Alzheimer’s disease represent the redox-silencing and entombment of abeta by zinc, Toxicology 137, 1447S-1454S (1999).

    Google Scholar 

  21. S. R. Powell, The antioxidation properties of zinc, J. Nutr. 130, 1447S-1454S (2000).

    PubMed  CAS  Google Scholar 

  22. S. C. Bondy, D. Liu, and S. Guo-Ross, Aluminum treatment induces nitric oxide synthase in the rat brain, Neurochem. Int. 33, 51 (1995).

    Article  Google Scholar 

  23. M. J. Richard, B. Portal, J. Meo, C. Coudray, A. Hadjian, and A. Favier, Malondialdehyde kit evaluated for determining plasma and lipoprotein fractions that react with thiobarbituric acid, Clin. Chem. 38, 704–709 (1992).

    PubMed  CAS  Google Scholar 

  24. D. W. Cushman and H. S. Cheung, Concentrations of angiotensin-converting enzyme in tissues of the rat, Biochim. Biophys. Acta 250, 261–265 (1971).

    PubMed  CAS  Google Scholar 

  25. H. Schunkert, V. J. Dzau, S. S. Tng, A. T. Hirsch, C. S. Apstein, and B. H. Lorell, Increased rat cardiac angiotensin converting enzyme activity and mRNA expression in pressure overload left ventricular hypertrophy. J. Clin. Invest. 86, 1913–19210 (1990).

    Article  PubMed  CAS  Google Scholar 

  26. J. Chmielnicka and M. Nasiadek, Tissue distribution and urinary excretion of essential elements in rats orally exposed to aluminum chloride, Biol. Trace Element Res. 31, 131–138 (1991).

    CAS  Google Scholar 

  27. Z. Deng, C. Coudray, L. Gouzoux, A. Mazur, Y. Rayssiguier, and D. Pépin, Effects of acute and chronic coingestion of AlCl3 with citrate or polyphenolic acids on tissue retention and distribution of aluminum in rats, Biol. Trace Element Res. 76, 245–278 (2000).

    Article  CAS  Google Scholar 

  28. K. Rajasekaran, Effects of combined exposure to aluminium and ethanol on food intake, motor behaviour and a few biochemical parameters in pubertal rats, Environ. Toxicol. Pharmacol. 9, 25–30 (2000).

    Article  CAS  PubMed  Google Scholar 

  29. J. Chamielnicka, M. Nasiadek, R. Pinkowski, and M. Paradowski, Disturbances of morphological parameters in blood of rats orally exposed to aluminum chloride, Biol. Trace Element Res. 42, 191–199 (1994).

    Google Scholar 

  30. J. Chamielnicka, M. Nasiadek, E. Lewandowska-Źyndul, and R. Pinkowski, Effect of aluminum on hematopoiesis after intraperitoneal exposure in rats, Ecotoxicol. Environ. Safety 33, 201–206 (1996).

    Article  Google Scholar 

  31. D. Julka, R. K. Vasishta, and K. D. Gill, Distribution of aluminum in different brain regions and body organs of rat, Biol. Trace Element Res. 52, 181–192 (1996).

    CAS  Google Scholar 

  32. R. A. Yokel, K. A. Meurer, T. L. Skinner, and A. M. Fredenburg, The 3-hydroxypyridin-4-ones more effectively chelate aluminum in a a rabbit model of aluminum intoxication than does desferrioxamine, Drug Metab. Dispos. 24, 105–111 (1996).

    PubMed  CAS  Google Scholar 

  33. D. J. Sánchez, M. Gómez, J. M. Llobet, J. Corbella, and J. L. Domingo, Effects of aluminum on the mineral metabolism of rats in relation to age, Pharmacol. Toxicol. 80, 11–17 (1997).

    PubMed  Google Scholar 

  34. A. S. Prasad, C. S. Mantzoros, F. W. J. Beck, J. W. Hess, and G. J. Brewer, Zinc status and serum testosterone levels of healthy adults, Nutrition 12, 344–348 (1996).

    Article  PubMed  CAS  Google Scholar 

  35. C. Sugawara, N. Sugawara, N. Ikeda, H. Okawa, T. Okazaki, J. Otaki, et al., Effects of ingested 4000 ppm aluminum on the essential metals, especially zinc, in intact and ethanol treated mice, Drug Chem. Toxicol. 10, 195–207 (1987).

    PubMed  CAS  Google Scholar 

  36. G. Müller, D. Burnel, A. Gery, and P. R. Lehr, Elements variations in pregnant and non pregnant female rats orally intoxicated by aluminum lactate, Biol. Trace Element Res. 39, 211–219 (1993).

    Google Scholar 

  37. M. Dlugaszek, M. A. Fiejka, A. Graczyk, J. C. Alksandrowicz, and M. Slowikowska, Effects of various aluminum compounds given orally to mice on Al tissue distribution and tissue concentrations of essential elements, Pharmacol. Toxicol. 86, 135–139 (2000).

    Article  PubMed  CAS  Google Scholar 

  38. E. H. Jeffery, H. T. Jansen, and J. A. Dellinger, In vivo interactions of aluminum with hepatic cytochrome P-450 and metallothionein, Fundane. Appl. Toxicol. 8, 541–548 (1987).

    Article  CAS  Google Scholar 

  39. R. S. Bedwal and A. Bahuguna, Zinc, copper and selenium in reproduction, Experientia 50, 626–640 (1994).

    Article  PubMed  CAS  Google Scholar 

  40. C. E. Thomas, L. A. Moorehouse, and S. D. Aust, Ferritin and superoxide-dependent lipid peroxidation, J. Biol. Chem. 260, 3275–3280 (1985).

    PubMed  CAS  Google Scholar 

  41. G. M. Ehrenfeld, J. B. Shipley, D. C. Heimbrook, H. Sugiyama, E. C. Long, J. H. van Bloom, et al., Copper-dependent clearage of DNA by bleomycin, Biochemistry 26, 931–942 (1987).

    Article  PubMed  CAS  Google Scholar 

  42. I. Sternlieb, Copper and the liver, Gastoenterology 78, 1615–1628 (1980).

    CAS  Google Scholar 

  43. S. Zidenberg-Chen, K. L. Olin, J. Villanueva, A. Tang, S. D. Phinney, C. H. Halsted, et al., Ethanol-induced changes in hepatic free radical defense-mechanisms and fatty acid composition in the miniature pig, Hepatology 13, 1185–1192 (1991).

    Google Scholar 

  44. T. K. Brown and R. Schwartz, Aluminum accumulation in serum, liver and spleen of Fe-depleted and Fe-adequate rats, Biol. Trace Element Res. 34, 1–10 (1992).

    CAS  Google Scholar 

  45. R. Jones and T. Mann, Lipid peroxidation in spermatozoa, Proc. R. Soc. Lond. B 184, 103–107 (1973).

    Article  PubMed  CAS  Google Scholar 

  46. R. Jones, T. Mann, and R. Sherins, Peroxidative breakdown of phospholipids in human spermatozoa, spermicidal properties of fatty acid peroxides, and protective action of seminal plasma, Fertil. Steril. 31, 531–537 (1979).

    PubMed  CAS  Google Scholar 

  47. R. J. Aitken, J. S. Clarkson, and S. Fishel, Generation of reactive oxygen species, lipid peroxidation and human sperm function, Biol. Reprod. 40, 183–197 (1989).

    Article  Google Scholar 

  48. A. A. A. El-Fattah, H. M. Al-Yousef, A. M. Al-Bekaira, and H. A. Al-Sawaf, Vitamin E protects the brain against oxidative injury stimulated by excessive aluminum intake, Biochem. Mol. Biol. Int. 46, 1175–1180 (1998).

    CAS  Google Scholar 

  49. S. Toda and Y. Yase, Effect of aluminum on iron-induced lipid peroxidation and protein oxidative modification of mouse brain homogenate, Biol. Trace Element Res. 61, 207–217 (1998).

    CAS  Google Scholar 

  50. M. Ohtawa, M. Seko, and F. Takayama, Effect of aluminum ingestion on lipid peroxidation in rats, Chem. Pharm. Bull. 31, 1415–1418 (1983).

    PubMed  CAS  Google Scholar 

  51. C. G. Fragga, P. I. Oteiza, M. S. Golub, M. E. Gershin, and C. L. Keen, Effects of aluminum on brain lipid peroxidation, Toxicol. Lett. 23, 213–219 (1990).

    Article  Google Scholar 

  52. G. B. N. Chainy, A. Sahoo, and C. Swain, Effect of aluminum on lipid peroxidation of cerebral hemisphere of chick, Bull. Environ. Contam. Toxicol. 50, 85–91 (1993).

    Article  PubMed  CAS  Google Scholar 

  53. M. G. Davies, G. J. Fulton, and P. O. Hagen, Clinical biology of nitric oxide, Br. J. Surg. 82, 1598–1610 (1995).

    Article  PubMed  CAS  Google Scholar 

  54. R. P. Erickson, S. P. Kessler, H. Kremling, and G. C. Sen, Species variation in the testicular angiotensin-converting enzyme promoter studied in transgenic mice. Mol. Reprod. Dev. 44, 324–331 (1996).

    Article  PubMed  CAS  Google Scholar 

  55. J. R. Hagaman, J. S. Moyer, E. S. Bachman, M. Sibony, P. L. Magyar, J. E. Welch, et al., Angiotensin-converting enzyme and male fertility, Proc. Natl. Acad. Sci. USA 95, 2552–2557 (1998).

    Article  PubMed  CAS  Google Scholar 

  56. S. M. Strittmatter and S. H. Snyder, Angiotensin-converting enzyme in the male rat reproductive system: autoradiographic visualization with [3H] captopril, Endocrinology 115, 2332–2341 (1984).

    Article  PubMed  CAS  Google Scholar 

  57. P. G. Reeves and K. L. Rossow, Zinc deficiency affects the activity and protein concentration of angiotensin-converting enzyme in rat testes, Proc. Soc. Exp. Biol. Med. 203, 336–342 (1993).

    PubMed  CAS  Google Scholar 

  58. C. R. Esther, D. Semeniuk, E. M. Marino, Y. Zhou, P. A. Overbeek, and K. E. Bernstein, Expression of testis angiotensin-converting enzyme is mediated by a cyclic AMP responsive element, Lab. Invest. 77, 483–488 (1997).

    PubMed  CAS  Google Scholar 

  59. A. Ackermann, M. S. Fernández-Alfonso, R. Sánchez de Rojas, T. Ortega, M. Paul, and C. Gonzálezx, Modulation of angiotensin-converting enzyme by nitric oxide, Br. J. Pharmacol. 124, 291–298 (1998).

    Article  PubMed  CAS  Google Scholar 

  60. E. M. V. De Cavanagh, I. Felipe, F. León, and G. F. César, Enalapril and captopril enhance glutathione-dependent antioxidant defenses in mouse tissues, Am. J. Physiol. Regul. Integrat. Comp. Physiol. 278, R572-R577 (2000).

    Google Scholar 

  61. P. G. Reeves and B. L. O’Dell, An experimental study of the effect of zinc on the activity of angiotensin converting enzyme in serum, Clin. Chem. 31, 581–584 (1985).

    PubMed  CAS  Google Scholar 

  62. E. G. Udupa and N. M. Rao, Effect of chloride and diamide on angiotensin converting enzyme from sheep testis and epididymis, Indian J. Exp. Biol. 36, 43–45 (1998).

    PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Guo, CH., Huang, CJ., Chiou, YL. et al. Alteration of trace element distribution and testis ACE activity in mice with high peritoneal aluminum. Biol Trace Elem Res 86, 145–157 (2002). https://doi.org/10.1385/BTER:86:2:145

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1385/BTER:86:2:145

Index Entries

Navigation