Inhibition of di(2-ethylhexyl) phthalate (DEHP)-induced endocrine disruption by co-treatment of vitamins C and E and their mechanism of action

References

• Akingbemi, B. T., R. Ge, G. R. Klinefelter, B. R. Zirkin, and M. P. Hardy. 2004. Phthalate-induced Leydig cell hyperplasia is associated with multiple endocrine disturbances. Proceedings of the National Academy of Sciences 101:775–80. doi:10.1073/pnas.0305977101.
   PubMed Web of Science ®Google Scholar
• Akingbemi, B. T., R. T. Youker, C. M. Sottas, R. Ge, E. Katz, G. R. Klinefelter, B. R. Zirkin, and M. P. Hardy. 2001. Modulation of rat Leydig cell steroidogenic function by di(2-ethylhexyl)phthalate. Biology of Reproduction 65:1252–59. doi:10.1095/biolreprod65.4.1252.
   PubMed Web of Science ®Google Scholar
• Amaral, S., K. Redmann, V. Sanchez, C. Mallidis, J. Ramalho-Santos, and S. Schlatt. 2013. UVB irradiation as a tool to assess ROS-induced damage in human spermatozoa. Andrology 1:707–14. doi:10.1111/j.2047-2927.2013.00098.x.
   PubMed Web of Science ®Google Scholar
• Barakat, R., P. P. Lin, S. Rattan, E. Brehm, I. F. Canisso, M. E. Abosalum, J. A. Flaws, R. Hess, and C. Ko. 2017. Prenatal exposure to DEHP induces premature reproductive senescence in male mice. Toxicological Sciences 156:96–108. doi:10.1093/toxsci/kfw248.
   PubMed Web of Science ®Google Scholar
• Bedwal, R. S., and A. Bahuguna. 1994. Zinc, copper and selenium in reproduction. Experientia 50:626–40. doi:10.1007/BF01952862.
   PubMedGoogle Scholar
• Blazak, W. F., K. A. Treinen, and P. C. Juniewicz. 1993. Male reproductive toxicology. In Methods in Toxicology, ed R. E. Chapin and J. J. Heindel, 86–94. New York: Academic Press.
   Google Scholar
• Blom, A., E. Ekman, A. Johannisson, L. Norrgren, and M. Pesonen. 1998. Effects of xenoestrogenic environmental pollutants on the proliferation of a human breast cancer cell line (MCF-7). Archives of Environmental Contamination and Toxicology 34:306–10. doi:10.1007/s002449900322.
   PubMed Web of Science ®Google Scholar
• Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72:248–54. doi:10.1016/0003-2697(76)90527-3.
   PubMed Web of Science ®Google Scholar
• Caxico Vieira, C. A. S., J. S. Vieira, M. S. Bastos, V. Zancanela, L. T. Barbosa, E. Gasparino, and A. P. Del Vesco. 2018. Expression of genes related to antioxidant activity in Nile tilapia kept under salinity stress and fed diets containing different levels of vitamin C. Journal of Toxicology and Environmental Health, Part A 81:20–30. doi:10.1080/15287394.2017.1401968.
   PubMed Web of Science ®Google Scholar
• Cho, D. H., J. T. Hong, K. Chin, T. S. Cho, and B. M. Lee. 1993. Organotropic formation and disappearance of 8-hydroxydeoxyguanosine in the kidney of Sprague-Dawley rats exposed to adriamycin and KBrO3. Cancer Letters 74:141–45. doi:10.1016/0304-3835(93)90235-2.
   PubMed Web of Science ®Google Scholar
• Choi, S. M., S. D. Yoo, and B. M. Lee. 2004. Toxicological characteristics of endocrine-disrupting chemicals: Developmental toxicity, carcinogenicity, and mutagenicity. Journal of Toxicology and Environmental Health, Part B 7:1–24. doi:10.1080/10937400490253229.
   PubMed Web of Science ®Google Scholar
• Eagon, P. K., N. Chandar, M. J. Epley, M. S. Elm, E. P. Brady, and K. N. Rao. 1994. Di(2-ethylhexyl)phthalate-induced changes in liver estrogen metabolism and hyperplasia. International Journal of Cancer 58:736–43. doi:10.1002/ijc.2910580519.
   PubMed Web of Science ®Google Scholar
• Erkekoglu, P., B. Giray, W. Rachidi, I. Hininger-Favier, A. M. Roussel, A. Favier, and F. Hincal. 2014. Effects of di(2-ethylhexyl)phthalate on testicular oxidant/antioxidant status in selenium-deficient and selenium-supplemented rats. Environmental Toxicology 29:98–107. doi:10.1002/tox.20776.
   PubMed Web of Science ®Google Scholar
• Fagundes, G. E., A. P. Damiani, G. D. Borges, K. O. Teixeira, M. M. Jesus, F. Daumann, F. Ramlov, T. Carvalho, D. D. Leffa, P. Rohr, and V. Moraes. 2017. Effect of green juice and their bioactive compounds on genotoxicity induced by alkylating agents in mice. Journal of Toxicology and Environmental Health, Part A 80:756–66. doi:10.1080/15287394.2017.1357307.
   PubMed Web of Science ®Google Scholar
• Fromme, H., L. Gruber, M. Schlummer, G. Wolz, S. Böhmer, J. Angerer, R. Mayer, B. Liebl, and G. Bolte. 2007. Intake of phthalates and di(2-ethylhexyl)adipate: Results of the integrated exposure assessment survey based on duplicate diet samples and biomonitoring data. Environment International 33:1012–20. doi:10.1016/j.envint.2007.05.006.
   PubMed Web of Science ®Google Scholar
• Gardner, S. T., A. T. Wood, R. Lester, P. E. Onkst, N. Burnham, D. H. Perygin, and J. Rayburn. 2016. Assessing differences in toxicity and teratogenicity of three phthalates, Diethyl phthalate, di-n-propyl phthalate, and di-n-butyl phthalate, using Xenopus laevis embryos. Journal of Toxicology and Environmental Health, Part A 79:71–82. doi:10.1080/15287394.2015.1106994.
   PubMed Web of Science ®Google Scholar
• Garratt, M., R. Bathgate, S. P. De Graaf, and R. C. Brooks. 2013. Copper-zinc superoxide dismutase deficiency impairs sperm motility and in vivo fertility. Reproduction 146:297–304. doi:10.1530/REP-13-0229.
   PubMed Web of Science ®Google Scholar
• Ha, M., X. Guan, L. Wei, P. Li, M. Yang, and C. Liu. 2016. Di-(2-ethylhexyl) phthalate inhibits testosterone level through disturbed hypothalamic-pituitary-testis axis and ERK-mediated 5α-reductase 2. Science of the Total Environment 563-564:566–75. doi:10.1016/j.scitotenv.2016.04.145.
   PubMed Web of Science ®Google Scholar
• Hamdi, S. A., O. I. Nassif, and M. S. Ardawi. 1997. Effect of marginal or severe dietary zinc deficiency on testicular development and functions of the rat. Archives of Andrology 38:243–53. doi:10.3109/01485019708994883.
   PubMed Web of Science ®Google Scholar
• He, F., Y. Tian, Z. Xu, L. Luo, J. Yang, H. Wang, Y. Sun, Q. Du, and Y. Shen. 2018. Development of an immunochromatographic assay as a screen for detection of total phthalate acid esters in cooking oil. Journal of Toxicology and Environmental Health, Part A 81:80–88. doi:10.1080/15287394.2017.1414023.
   PubMed Web of Science ®Google Scholar
• Herreros, M. A., T. Encinas, L. Torres-Rovira, R. A. Garcia-Fernandez, J. M. Flores, J. M. Ros, and A. Gonzalez-Bulnes. 2013. Exposure to the endocrine disruptor di(2-ethylhexyl)phthalate affects female reproductive features by altering pulsatile LH secretion. Environmental Toxicology and Pharmacology 36:1141–49. doi:10.1016/j.etap.2013.09.020.
   PubMed Web of Science ®Google Scholar
• Hess, R. A., D. Bunick, K. H. Lee, J. Bahr, J. A. Taylor, K. S. Korach, and D. B. Lubahn. 1997. A role for oestrogens in the male reproductive system. Nature 390:509–12. doi:10.1038/37352.
   PubMed Web of Science ®Google Scholar
• Hong, S. H., J. E. Lee, S. M. An, Y. Y. Shin, D. Y. Hwang, S. Y. Yang, S. K. Cho, and A. B. An. 2017. Effect of vitamin D3 on biosynthesis of estrogen in porcine granulosa cells via modulation of steroidogenic enzymes. Toxicogical Research 33:49–54. doi:10.5487/TR.2017.33.1.049.
   PubMed Web of Science ®Google Scholar
• Huang, L. P., C. C. Lee, J. P. Fan, P. H. Kuo, T. S. Shih, and P. C. Hsu. 2014. Urinary metabolites of di(2-ethylhexyl) phthalate relation to sperm motility, reactive oxygen species generation, and apoptosis in polyvinyl chloride workers. International Archives of Occupational and Environmental Health 87:635–46. doi:10.1007/s00420-013-0905-6.
   PubMed Web of Science ®Google Scholar
• Husain, K., and S. M. Somani. 1997. Interaction of exercise training and chronic ethanol ingestion on hepatic and plasma antioxidant system in rat. Journal of Applied Toxicology 17:189–94. doi:10.1002/(SICI)1099-1263(199705)17:3<189::AID-JAT431>3.0.CO;2-7.
   PubMed Web of Science ®Google Scholar
• Inoue, K., H. Okumura, T. Higuchi, H. Oka, Y. Yoshimura, and H. Nakazawa. 2002. Characterization of estrogenic compounds in medical polyvinyl chloride tubing by gas chromatography-mass spectrometry and estrogen receptor binding assay. Clinica Chimica Acta 325:157–63. doi:10.1016/S0009-8981(02)00291-7.
   PubMed Web of Science ®Google Scholar
• Ishihara, M., M. Itoh, K. Miyamoto, S. Suna, Y. Takeuchi, I. Takenaka, and F. Jitsunari. 2000. Spermatogenic disturbance induced by di-(2-ethylhexyl) phthalate is significantly prevented by treatment with antioxidant vitamins in the rat. International Journal of Andrology 23:85–94. doi:10.1046/j.1365-2605.2000.00212.x.
   PubMedGoogle Scholar
• Janszen, F. H., B. A. Cooke, M. J. Van Driel, and H. J. Van Der Molen. 1976. The effect of calcium ions on testosterone production in Leydig cells from rat testis. The Biochemical Journal 160:433–37. doi:10.1042/bj1600433.
   PubMed Web of Science ®Google Scholar
• Jones, D. P., V. E. Kagan, S. D. Aust, D. J. Reed, and S. T. Omaye. 1995. Impact of nutrients on cellular lipid peroxidation and antioxidant defense system. Fundamental and Applied Toxicology 26:1–7. doi:10.1093/toxsci/26.1.1.
   PubMedGoogle Scholar
• Kim, H. S., K. Saito, M. Ishizuka, A. Kazusaka, and S. Fujita. 2003. Short period exposure to di-(2-ethylhexyl) phthalate regulates testosterone metabolism in testis of prepubertal rats. Archives of Toxicology 77:446–51. doi:10.1007/s00204-003-0466-7.
   PubMed Web of Science ®Google Scholar
• Kim, J. N., and B. M. Lee. 2018. Risk management of free radicals involved in air travel syndromes by antioxidants. Journal of Toxicology and Environmental Health, Part B 21:47–60. doi:10.1080/10937404.
   PubMed Web of Science ®Google Scholar
• Lee, B. M., and R. M. Santella. 1988. Quantitation of protein adducts as a marker of genotoxic exposure: Immunologic detection of benzo[a]pyrene–Globin adducts in mice. Carcinogenesis 9:1773–77. doi:10.1093/carcin/9.10.1773.
   PubMed Web of Science ®Google Scholar
• Lee, H. K., T. S. Kim, C. Y. Kim, I. H. Kang, M. G. Kim, K. K. Jung, H. S. Kim, S. Y. Han, H. J. Yoon, and G. S. Rhee. 2012. Evaluation of in vitro screening system for estrogenicity: Comparison of stably transfected human estrogen receptor-α transcriptional activation (OECD TG455) assay and estrogen receptor (ER) binding assay. The Journal of Toxicological Sciences 37:431–37. doi:10.2131/jts.37.431.
   PubMed Web of Science ®Google Scholar
• Lee, Y. 2018. Cancer chemopreventive potential of procyanidin. Toxicogical Research 33:273–82. doi:10.5487/TR.2017.33.4.273.
   Web of Science ®Google Scholar
• Lephart, E. D., and E. R. Simpson. 1991. Assay of aromatase activity. Meth Enzymol 206:477–83. doi:10.1016/0076-6879(91)06116-K.
   PubMed Web of Science ®Google Scholar
• Lim, D. S., S. K. Lim, M. K. Kim, Y. C. Kwon, T. H. Roh, S. M. Choi, S. Yoon, H. S. Kim, and B. M. Lee. 2018. Formation and inhibition of N-nitrosodiethanolamine in cosmetics under pH, temperature, and fluorescent, ultraviolet, and visual light. Journal of Toxicology and Environmental Health, Part A 81:241–53. doi:10.1080/15287394.2018.1440172.
   PubMed Web of Science ®Google Scholar
• Lovekamp-Swan, T., and B. J. Davis. 2003. Mechanisms of phthalate ester toxicity in the female reproductive system. Environmental Health Perspectives 111:139–45. doi:10.1289/ehp.5658.
   PubMed Web of Science ®Google Scholar
• Madkour, N. K. 2014. Beneficial role of celery oil in lowering the di(2-ethylhexyl) phthalate-induced testicular damage. Toxicology and Industrial Health 30:861–72. doi:10.1177/0748233712464808.
   PubMed Web of Science ®Google Scholar
• Magdouli, S., R. Daghrir, S. K. Brar, P. Drogui, and R. D. Tyagi. 2013. Di 2-ethylhexylphtalate in the aquatic and terrestrial environment: A critical review. Journal of Environmental Management 127:36–49. doi:10.1016/j.jenvman.2013.04.013.
   PubMed Web of Science ®Google Scholar
• Moore, R. W., T. A. Rudy, T. M. Lin, K. Ko, and R. E. Peterson. 2001. Abnormalities of sexual development in male rats with in utero and lactational exposure to the antiandrogenic plasticizer di(2-ethylhexyl) phthalate. Environmental Health Perspectives 109:229–37. doi:10.2307/3434690.
   PubMed Web of Science ®Google Scholar
• Park, J. D., S. S. Habeebu, and C. D. Klaassen. 2002. Testicular toxicity of di-(2-ethylhexyl)phthalate in young Sprague-Dawley rats. Toxicology 171:105–15. doi:10.1016/S0300-483X(01)00567-4.
   PubMed Web of Science ®Google Scholar
• Roh, T., U. De, S. K. Lim, M. K. Kim, S. M. Choi, D. S. Lim, S. Yoon, S. Kacew, H. S. Kim, and B. M. Lee. 2018. Detoxifying effect of pyridoxine on acetaminophen-induced hepatotoxicity via suppressing oxidative stress injury. Food and Chemical Toxicology 114:11–22. doi:10.1016/j.fct.2018.02.017.
   PubMed Web of Science ®Google Scholar
• Rosenfeld, C. S., N. D. Denslow, E. F. Orlando, J. M. Gutierrez-Villagomez, and V. L. Trudeau. 2017. Neuroendocrine disruption of organizational and activational hormone programming in poikilothermic vertebrates. Journal of Toxicology and Environmental Health, Part B 20:276–304. doi:10.1080/10937404.2017.1370083.
   PubMed Web of Science ®Google Scholar
• Sato, M., and I. Bremner. 1993. Oxygen free radicals and metallothionein. Free Radical Biology and Medicine 14:325–37. doi:10.1016/0891-5849(93)90029-T.
   PubMed Web of Science ®Google Scholar
• Suna, S., F. Yamaguchi, S. Kimura, M. Tokuda, and F. Jitsunari. 2007. Preventive effect of D-psicose, one of rare ketohexoses, on di-(2-ethylhexyl) phthalate (DEHP)-induced testicular injury in rat. Toxicology Letters 173:107–17. doi:10.1016/j.toxlet.2007.06.015.
   PubMed Web of Science ®Google Scholar
• Wang, X., and P. J. Quinn. 1999. Vitamin E and its function in membranes. Progress in Lipid Research 38:309–36. doi:10.1016/S0163-7827(99)00008-9.
   PubMed Web of Science ®Google Scholar
• Wang, Y., B. Chen, T. Lin, S. Wu, and G. Wei. 2017a. Protective effects of vitamin E against reproductive toxicity induced by di(2-ethylhexyl) phthalate via PPAR-dependent mechanisms. Toxicology Mechanisms and Methods 27:551–59. doi:10.1080/15376516.2017.1333556.
   PubMed Web of Science ®Google Scholar
• Wang, Y., F. Chen, L. Ye, B. Zirkin, and H. Chen. 2017b. Steroidogenesis in Leydig cells: Effects of aging and environmental factors. Reproduction 154:R111–R122. doi:10.1530/REP-17-0064.
   PubMed Web of Science ®Google Scholar
• Yoon, K., S. J. Kwack, H. S. Kim, and B. M. Lee. 2014. Estrogenic endocrine-disrupting chemicals: Molecular mechanisms of actions on putative human diseases. Journal of Toxicology and Environmental Health, Part B 17:127–74. doi:10.1080/10937404.
   PubMed Web of Science ®Google Scholar
• Zawatski, W., and M. M. Lee. 2013. Male pubertal development: Are endocrine-disrupting compounds shifting the norms? Journal of Endocrinology 218:R1–R12. doi:10.1530/JOE-12-0449.
   PubMed Web of Science ®Google Scholar