Asian-Australasian Journal of Animal Sciences

Asian Australasian Association of Animal Production Societies (아세아태평양축산학회)
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Arsenic Toxicity on Duck Spermatozoa and the Ameliorating Effect of L-Ascorbic Acid

  • Lin, Chai-Ching (Department of Applied Animal Science, National Ilan Institute of Technology) ;
  • Huang, Chia-Cherng (Ilan Branch Institute, Taiwan Livestock Research Institute) ;
  • Chen, Ming-Cheng (Department of Applied Animal Science, National Ilan Institute of Technology) ;
  • Huang, Andrew Jeng-Fang (Ilan Branch Institute, Taiwan Livestock Research Institute) ;
  • Chiou, Hung-Yi (Department of Public Health, Taipei Medical University)
  • Received : 2001.06.19
  • Accepted : 2001.09.28
  • Published : 2002.01.01
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Abstract

The objectives of this study were to understand the possible mechanism of duck sperm toxicity induced by arsenic exposure in vivo, and to investigate the roles of the antioxidant L-ascorbic acid in ameliorating the arsenic-induced sperm impairment. To test the acute toxicity, the percentages of mortality of mature drakes treated with different concentrations of trivalent sodium arsenite, As (III), and pentavalent sodium arsenate, As (V) were measured. The LD50 value of As (III) for mature drakes was $4.89{\pm}1.49$ ppm. Although As (V) didn't cause any deaths even at a concentration of 40 ppm, the chronic toxicity of As (V) on sperm quality was shown by a decreased fertilization rate. When the concentrations of As (V) were above 0.4 ppm, fertilization rates were lower than those of 0.04 ppm and control. Drakes treated with 40 ppm of As (V) had the highest malondialdehyde (MDA) level in the testis tissue, $3.100{\pm}0.218{\mu}mole/g$ testis. This showed that 40 ppm of As (V) significantly induced lipid peroxidation in testis tissue. For the 1.2 ppm As (III) treatment, several significant effects were observed: (1) sperm motility was decreased most dramatically by $52.0{\pm}9.1$% after three days of incubation; (2) fertilization rate of artificially inseminated semen was the lowest, $26.4{\pm}15.4$; (3) the MDA concentration in testis tissue, $7.846{\pm}0.246{\mu}mole/g$ testis, was significantly higher than the others (p<0.05); (4) the sperm number, $1.17{\pm}0.40({\times}10^9)$, was significantly lower than with the 60 ppb and control treatments (p<0.05); (5) a black appearance and soft texture was observed in the testis tissue. The antioxidant L-ascorbic acid administered along with 1.2 ppm As (III) decreased the toxicity of arsenic. The ameliorating effects included: improved sperm motility, increased sperm number and fertilization rate, and decreased MDA concentration in the testis tissue. This study suggests that the toxicity of the trivalent arsenic on sperm quality is partly from free radicals generated by its metabolic pathway, and the antioxidant ascorbic acid ameliorates arsenic-caused sperm impairment.

Keywords

References

  1. Aitken, R. J., D. Buckinhham and D. Harkiss. 1993. Use of xanthine oxidase free radical generating system to investigate the cytotoxic effects of reactive oxygen species on human spermatozoa. J. Reprod. Fertil. 97:441-450. https://doi.org/10.1530/jrf.0.0970441
  2. Aitken, R. J. and J. S. Clarkson. 1987. Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81:459-469. https://doi.org/10.1530/jrf.0.0810459
  3. Alvarez, J. G., J. C. Touchstone, L. Blasco and B. T. Storey. 1987. Spontaneous lipid peroxidation and production of hydrogen peroxide and superoxide in human spermatozoa. Superoxide dismutase as major enzyme protectant against oxygen toxicity. J. Androl. 8:338-348. https://doi.org/10.1002/j.1939-4640.1987.tb00973.x
  4. Anke, M., G. Hoffmann, M. Grn, B. Groppel and E. Riedel. 1982. IAEA-TEC DOC 267:135-146.
  5. Baxley, M. N., R. D. Hood, G. C. Vedel, W. P. Harrison and G. M. Szczech. 1981. Bull. Environ. Contam. Toxicol. 26:749-756. https://doi.org/10.1007/BF01622166
  6. Beaudoin, A. R. 1974. Teratology 10:153-156. https://doi.org/10.1002/tera.1420100211
  7. Blair, P. C., M. B. Thompson, B. Bechtold, R. E. Wilson, M. P. Moorman and B. A. Fowler. 1990. Evidence for oxidative damage to red blood cells in mice induced by arsine gas. Toxicol. 63:25-24. https://doi.org/10.1016/0300-483X(90)90065-O
  8. Brown, K. G. and C. J. Chen. 1994. Observed dose-response for internal cancers and arsenic in drinking water in the blackfoot disease endemic region of Taiwan. In: Arsenic Exposure and Health (Ed. W. R. Chappell, C. O. Abernathy and C. R. Cothern). Science and Technology Letters. Northwood. pp. 153-170.
  9. Chang, W. C., S. H. Chen, H. L. Wu, G. Y. Shi, S. Murota and I. Morita. 1991. Cytoprotective effect of reduced glutathione in arsenic-induced endothelial cell injury. Toxicol. 69:101-110. https://doi.org/10.1016/0300-483X(91)90157-V
  10. Charbonneau, S. M., G. K. H. Tam, F. Bryce, Z. Zawidzka and E. Sandi. 1979. Toxicol. Lett. 3:107-113. https://doi.org/10.1016/0378-4274(79)90094-8
  11. Chen, C. J. 1980. Blackfoot disease. Lancet. 336:442. https://doi.org/10.1016/0140-6736(90)91990-R
  12. Chen, C. J., C. W. Chen, M. M. Wu and T. L. Kuo. 1992. Cancer potential in liver, lung, bladder and kidney due to ingested inorganic arsenic in drinking water. Br. J. Cancer 66:888-892. https://doi.org/10.1038/bjc.1992.380
  13. Chen, C. J. and L. J. Lin. 1994. Human carcinogenicity and atherogenicity induced by chronic exposure to inorganic arsenic. In: Advances in Environmental Science and Technology: Arsenic in Environment. Part II: Human health and ecosystem effects (Ed. J. O. Nriagu). John Wiley & Sons, Ins., New York. 27:109-131.
  14. Chen, C. J., T. L. Kuo and M. M. Wu. 1988. Arsenic and cancers. Lancet. 1:414-415. https://doi.org/10.1016/S0140-6736(88)91207-X
  15. Chen, C. J., Y. C. Chuang, T. M. Lin and H. Y. Wu. 1985. Malignant neoplasms among residents of a blackfoot diseaseendemic area in Taiwan: High arsenic artesian well water and cancers. Cancer Res. 45:5895-5899.
  16. Chen, C. J., Y. C. Chuang, S. L. You, T. M. Lin and H. Y. Wu. 1986. A retrospective study on malignant neoplasms of bladder, lung and liver in blackfoot disease-endemic area in Taiwan. Br. J. Cancer 53:399-405. https://doi.org/10.1038/bjc.1986.65
  17. Esterbauer, H., R. J. Schaur and H. Zollner. 1991. Chemistry and biochemistry of 4-hydroxynonenal, malondialdehyde and related aldehydes. Free Rad. Biol. Med. 11:81-128. https://doi.org/10.1016/0891-5849(91)90192-6
  18. Farmer, J. G. and L. R. Johnson. 1990. Assessment of occupational exposure to inorganic arsenic based on urinary concentrations and speciation of arsenic. Br. J. Ind. Med. 47:342-348.
  19. Ferm, V. H. and L. Kilham. 1977. Environ. Res. 14:483-486. https://doi.org/10.1016/0013-9351(77)90055-X
  20. Griveau, J. F., P. Renard and D. LeLannou. 1994. An in vitro promoting role for hydrogen peroxide in human sperm capacitation. Int. J. Androl. 17:300-307. https://doi.org/10.1111/j.1365-2605.1994.tb01260.x
  21. Guo, H. R., C. J. Chen and H. L. Greene. 1994. Arsenic in drinking water cancers: a brief descriptive review of Taiwan studies. In: Arsenic Exposure and Health (Ed. W. R. Chappell, C. O. Abernathy and C. R. Cothern) Science and Technology Letters. Northwood. pp. 129-138.
  22. Hollins, J. G., S. M. Charbonneau, F. Bryce, J. M. Ridgeway, G. K. H. Tam and R. F. Will. 1979. Toxicol. Lett. 4:7-13. https://doi.org/10.1016/0378-4274(79)90023-7
  23. Hood, R. D. and W. P. Harrison. 1982. Bull. Environ. Contam. Toxicol. 29:671-678. https://doi.org/10.1007/BF01606106
  24. Huang, H., C. F. Huang,, D. R. Wu, C. M. Jinn and K. Y. Jan. 1993. Glutathione as a cellular defense against arsenite toxicity in cultured Chinese hamster ovary cells. Toxicol. 79:195-204. https://doi.org/10.1016/0300-483X(93)90211-A
  25. IARC (International Agents for Research on Cancer) 1980. Carcinogenesis of arsenic and arsenic compounds. IARC Monogr. 23: 37-141.
  26. Ishinishi, N., K. Tsuchiya, M. Vahter and B. A. Fowler. 1986. Arsenic. In: Handbook on the Toxicology of Metals (Ed. L. Friberg, G. F. Nordberg and V. Vouk) Elsevier Science Publishers. Amsterdam. pp. 43-83.
  27. Iwasaki, A. and C. F. Gagnon. 1992. Formation of reactive oxygen species in spermatozoa of infertile patients. Fertil. Steril. 57(2):409-416. https://doi.org/10.1016/S0015-0282(16)54855-9
  28. Keyse, S. M. and R. M. Tyrrell. 1989. Heme oxygenase is the major 32-kDa stress protein induced in human skin fibroblasts by UVA radiation, hydrogen peroxide, and sodium arsenite. Proc. Natl. Acad. Sci. USA 86:99-103. https://doi.org/10.1073/pnas.86.1.99
  29. Lakso, J. and S. A. Peoples. 1975. Aric. Biol. Chem. 44:1993-1994.
  30. Lee, T. C. and I. C. Ho. 1994. Expression of heme oxygenase in arsenite-resistant human lung adenocarcinoma cells. Cancer Res. 54:1660-1664.
  31. Lee, T. C. and I. C. Ho. 1995. Modulation of cellular antioxidant defense activities by sodium arsenite in human fibroblasts. Arch. Toxicology 69:498-504. https://doi.org/10.1007/s002040050204
  32. Lee, T. C., M. Oshimura and J. C. Barrett. 1985. Comparison of arsenic-induced cell transformation, cytotoxicity, mutation and cytogenetic effects in Syrian hamster embryo cells in culture. Carcinogenesis 6:1421-1426. https://doi.org/10.1093/carcin/6.10.1421
  33. Lee, T. C., W. J. Wei, W. J. Chang,, I. C. Ho, J. F. Lo, K. Y. Jan and H. Huang. 1989. Elevation of glutathione levels and glutathione S-transferase activity in arsenic-resistant Chinese hamster ovary cells. In Vitro Cell Dev. Biol. 25:442-448. https://doi.org/10.1007/BF02624629
  34. Leonard, A. and R. R. Lauwerys. 1980. Carcinogenicity, teratogenicity and mutagenicity of arsenic. Mutat. Res. 75:49-62. https://doi.org/10.1016/0165-1110(80)90027-5
  35. Lindgren, A., B. R. G. Danielsson, L. Dencker and M. Vahter. 1984. Acta. Pharmacol. Toxicol. 54:311-320. https://doi.org/10.1111/j.1600-0773.1984.tb01936.x
  36. Marafante, E., J. Rade, R. Pietra, E. Sabbioni and F. Bertolero. 1980. In: Arseni. 3. Spurenelement-Symposium (Ed. M. Anke, H. J. Schneider and C. Bruckner). Wiss. Publ., Friedrich-Schiller-Univ., Jena, G.D.R. pp. 49-55.
  37. Nordenson, I. and L. Beckman. 1991. Is the genotoxic effect of arsenic mediated by oxygen free radicals? Hum. Hered. 41:71-73. https://doi.org/10.1159/000153979
  38. Odanaka, Y., O. Matano and S. Goto. 1980. Bull. Environ. Contam. Toxicol. 24:452-459. https://doi.org/10.1007/BF01608138
  39. Oehninger, S., P. Blackmore, M. Mahony and G. Hodgen. 1995. Effects of hydrogen peroxide on human spermatozoa. J. Assisted Reprod. Genetics 12(1):41-47. https://doi.org/10.1007/BF02214128
  40. Tseng, C. H., C. J. Chen, B. J. Lin and T. Y. Tai. 1994. Abnormal response of ankle pressure after exercise in seemingly normal subjects living in blackfoot disease-hyperendemic villages in Taiwan. Vascular Surg. 28:607-617. https://doi.org/10.1177/153857449402800906
  41. Tseng, W. P. 1977. Effects and dose-response relationships of skin cancer and blackfoot disease with arsenic. Environ. Health. Perspect. 19:109-119. https://doi.org/10.2307/3428460
  42. Tseng, W. P. 1989. Blackfoot disease in Taiwan: A 30 year followup. Angiology 40:547-558. https://doi.org/10.1177/000331978904000606
  43. Tseng, W. P., H. M. Chu and S. W. How. 1968. Prevalence of skin cancer in an endemic area of chronic arsenicism in Taiwan. J. Natl. Cancer. Inst. 40:453-463.
  44. Vahter, M. and J. Envall. 1983. Environ. Res. 32:14-24. https://doi.org/10.1016/0013-9351(83)90187-1
  45. Vodela, J. K., S. D. Lenz, J. A. Renden, W. H. Mcelhenney and Kemppainen. 1997. Drinking water contaminants (arsenic, cadmium, lead, benzene, and trichloroehtylene). 2. Effects on reproductive performance, egg quality, and embryo toxicity in broiler breeders. Poult. Sci. 76:1493-1500. https://doi.org/10.1093/ps/76.11.1493
  46. Wang, T. S. and H. Huang. 1994. Active oxygen species are involved in the induction of micronuclei by arsenic in XRS-5 cells. Mutagenesis 9:253-257. https://doi.org/10.1093/mutage/9.3.253
  47. Wu, M. M., T. L. Kuo, Y. H. Huang and C. J. Chen. 1989. Doseresponse relationship between arsenic concentration in well water and mortality from cancers and vascular disease. Am. J. Epidemiol. 130:1123-1132. https://doi.org/10.1093/oxfordjournals.aje.a115439
  48. Yamanaka, K., A. Hasegawa, R. Sawamura and S. Okada. 1991. Cellular response to oxidative damage in lung induced by the administration of dimethylarsinic acid, a major metabolite of inorganic arsenics, in mice. Toxicol. Appl. Pharmacol. 108:205-213. https://doi.org/10.1016/0041-008X(91)90111-Q
  49. Yamanaka, K., A. Hasegawa, R. Sawamura and S. Okada. 1989a. DNA Strand breaks in mammalian tissue induced by methylarsenics. Biol. Trace. Elem. Res. 21:413-417. https://doi.org/10.1007/BF02917283
  50. Yamanaka, K., A. Hasegawa, R. Sawamura and S. Okada. 1989b. Dimethylated arsenics induce DNA strand breaks in lung via the production of active oxygen in mice. Biochem. Biophys. Res. Commun. 165:43-50. https://doi.org/10.1016/0006-291X(89)91031-0
  51. Yamanaka, K., M. Hoshino, M. Okamoto, R. Sawamura, A. Hasegawa and S. Okada. 1990. Induction of DNA damage by dimethylarsine, a metabolite of inorganic arsenics, is for the major part likely due to its peroxyl radical. Biochem. Biophys. Res. Commun. 168:58-64. https://doi.org/10.1016/0006-291X(90)91674-H

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