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Histological and Histometrical Study of the Protective Role of α-Tocopherol against Sodium Arsenite Toxicity in Rat Ovaries

Published online by Cambridge University Press:  15 April 2014

Maryam Ghandi Zadeh Dezfouli*
Affiliation:
Department of Biology, Faculty of Basic Science, Arak University, Shahid Beheshti Street, Arak, Markazi Province, 3945-5-38138Iran
Samira Eissazadeh
Affiliation:
Department of Cellular and Molecular Biology, Faculty of Biotechnology and Biomolecular Science, Serding, Selangor, Darul Ehsan, 43400Malaysia
Sayed Mohammad Ali Shariat Zade
Affiliation:
Department of Biology, Faculty of Basic Science, Arak University, Shahid Beheshti Street, Arak, Markazi Province, 3945-5-38138Iran
*
*Corresponding author. [email protected]
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Abstract

This study examines histometrical changes induced by sodium arsenite (SA), as an environmental pollutant, and investigates the protective effect of α-tocopherol on ovaries of SA-treated rats during the prenatal stage until sexual maturity. Rats were classified into groups: control, SA (8 ppm/day), α-tocopherol (100 ppm/day), and SA+α-tocopherol. Treatment was performed from pregnancy until maturation when the rats and ovaries were weighed. The Cavalieri method was used to estimate volume of the ovaries, cortex, medulla, and corpus luteum. The mean diameter of oocytes, granulosa cells, and nuclei were measured and volume was estimated using the Nucleator method. The number of oocytes and thickness of the zona pellucida (ZP) were determined using an optical dissector and orthogonal intercept method, respectively. SA reduced the body and ovary weight, the number of secondary, antral and Graafian oocytes, volume of the ovaries, cortex, medulla and corpus luteum, mean diameter and volume of oocytes in primordial and primary follicles, mean diameter and volume of oocyte nuclei in all types of follicles, and mean thickness of the ZP in secondary and antral follicles. Also, the mean diameter and volume of granulosa cells and their nuclei in antral and Graafian follicles decreased significantly. Vacuolization and vascular congestion in the corpus luteum and an increase in the number of atretic oocytes were seen in the SA group. Most of these parameters were unchanged from the control level in the SA+α-tocopherol group. It was concluded that α-tocopherol supplementation reduced the toxic effects of SA exposure on ovarian tissue in rats.

Type
Biological Applications
Copyright
© Microscopy Society of America 2014 

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References

Adashi, E.Y., Resnick, C.E., D’Ercole, A.J., Svoboda, M.E. & Van Wyk, J.J. (1985). Insulin-like growth factors as intraovarian regulators of granulosa cell growth and function. Endocr Rev 6(3), 400420.Google Scholar
Akram, Z., Jalali, S., Shami, S.A., Ahmad, L., Batool, S. & Kalsoom, O. (2009). Genotoxicity of sodium arsenite and DNA fragmentation in ovarian cells of rat. Toxicol Lett 190, 8185.Google Scholar
Banerjee, M., Banerjee, N., Bhattacharjee, P., Mondal, D., Lythgoe, R.P., Martínez, M., Pan, J., Polya, A.D. & Giri, K.A. (2013). High arsenic in rice is associated with elevated genotoxic effects in humans. Sci Rep 3, 2195.Google Scholar
Bera, K., Rana, T., Das, S., Bhattacharya, D., Bandyopadhyay, S., Pan, D., De, S., Samanta, S., Chowdhury, A.N., Mondal, T.K. & Das, S.K. (2010). Ground water arsenic contamination in West Bengal, India: A risk of sub-clinical toxicity in cattle as evident by correlation between arsenic exposure, excretion and deposition. Toxicol Ind Health 26, 709716.Google Scholar
Blaner, W.S. (2013 a). The fat-soluble vitamins 100 years later: Where are we now? J Lipid Res 54(7), 17161718.Google Scholar
Blaner, W.S. (2013 b). Vitamin E: The enigmatic one! J Lipid Res 54(9), 22932294.Google Scholar
Bose, R. & De, A. (2013). Arsenic contamination: Unavoidable natural phenomenon or an anthropogenic crisis. Proc Nat Acad Sci, India A Phys Sci 83, 181185.Google Scholar
Britt, K.L., Kerr, J., O’Donnell, L., Jones, M.E.E., Drummond, A.E., Davis, S.R., Simpson Evan, R. & Findlay, J.K. (2002). Estrogen regulates development of the somatic cell phenotype in the eutherian ovary. FASEB J 16, 13891397.Google Scholar
Calado, A.M., Rocha, E., Colaco, A. & Sousa, M. (2001). Stereologic characterization of bovine (Bos taurus) cumulus-oocyte complexes aspirated from small antral follicles during the diestrous phase. Biol Reprod 65, 13831391.Google Scholar
Cassano, E., Tosto, L., Balestrieri, M., Zicarelli, L. & Abrescia, P. (1999). Antioxidant defense in the follicular fluid of water buffalo. Cell Physiol Biochem 9, 106116.Google Scholar
Chang, S.I., Jin, B., Youn, P., Park, C., Park, J.D. & Ryu, D.Y. (2007). Arsenic-induced toxicity and the protective role of ascorbic acid in mouse testis. Toxicol Appl Pharmacol 218(2), 196203.Google Scholar
Chatterjee, A. & Chatterji, U. (2010). Arsenic abrogates the estrogen-signaling pathway in the rat uterus. Reprod Biol Endocrinol 8, 80.Google Scholar
Chattopadhyay, S., Ghosh, S., Chaki, S., Debnath, J. & Ghosh, D. (1999). Effect of sodium arsenite on plasma levels of gonadotrophins and ovarian steroidogenesis in mature albino rats: Duration-dependent response. J Toxicol Sci 24(5), 425431.CrossRefGoogle ScholarPubMed
Chattopadhyay, S., Ghosh, S., Debnath, J. & Ghosh, D. (2001). Protection of sodium arsenite-induced ovarian toxicity by coadministration of L-ascorbate (Vitamin C) in mature Wistar strain rat. Arch Environ Contam Toxicol 41, 8389.Google Scholar
Chattopadhyay, S., Sampa, P., Ghosh, D. & Debnath, J. (2003). Effect of dietary co-administration of sodium selenite on sodium arsenite-induced ovarian and uterine disorders in mature albino rats. Toxicol Sci 75, 412422.Google Scholar
Chaudhuri, S. & Maiti, B.R. (1998). Effects of gonadotropins and prolactin on ovarian activity of a wild avian species, the tree pie Dendrocitta vagabunda. Indian J Exp Biol 36(8), 790795.Google Scholar
Christian, J.J. (1964). Actions of ACTH in intact and coticoid-maintained adrenalectomized female mice with emphasis on the reproductive tract. Endocrinology 75, 655657.Google Scholar
Cruz-Orive, L.M., Ramos-Herrera, M.L. & Artacho-Pérula, E. (2010). Stereology of isolated objects with the invariator. J Microsc 240, 94110.Google Scholar
EPA. (2009). Organic arsenicals; product cancellation order and amendments to terminate uses, EPA–HQ– OPP–2009–0191; FRL–8437–7. Washington, DC: EPA.Google Scholar
Erickson, G.F., Wang, C. & Hsueh, A.J.W. (1979). FSH induction of functional LH receptors in granulosa cells cultured in a chemically defined medium. Nature 279, 336338.Google Scholar
Ferrando, R.E., Nyengaard, J.R., Hays, S.R., Fahy, J.V. & Woodruff, P.G. (2003). Applying stereology to measure thickness of the basement membrane zone in bronchial biopsy specimens. J Allergy Clin Immunol 112, 12431245.Google Scholar
Ghosh, D., Chattopadhyay, S. & Debnath, J. (1999). Effect of sodium arsenite on adrenocortical activity in immature female rats: Evidence of dose dependent response. J Environ Sci 11, 419422.Google Scholar
Golub, M.S., Macintosh, M.S. & Baumrind, N. (1998). Developmental and reproductive toxicity of inorganic arsenic: Animal studies and human concerns. J Toxicol Environ Health B Crit Rev 1(3), 199241.Google Scholar
Griffin, J., Emery, B.R., Huang, I., Peterson, C.M. & Carrell, D.T. (2006). Comparative analysis of follicle morphology and oocyte diameter in four mammalian species (mouse, hamster, pig, and human). J Exp Clin Assist Reprod 3, 2.Google Scholar
Gupta, S.K., Kalai Selvan, V., Agrawal, S.S. & Saxena, R. (2009). Advances in pharmacological strategies for the prevention of cataract development. Indian J Ophthalmol 57(3), 175183.Google Scholar
Gutteridge, J.M. (1995). Lipid peroxidation and antioxidants as biomarkers of tissue damage. Clin Chem 41, 18191828.Google Scholar
Gutteridge, J.M. & Halliwell, B. (1990). The measurement and mechanism of lipid peroxidation in biological systems. Trends Biochem Sci 15, 129135.CrossRefGoogle ScholarPubMed
Hegele-Hartung, C, Siebel, P, Peters, O., Kosemund, D., Muller, G., Hillisch, A., Walter, A., Kraetzschmar, J. & Fritzemeier, K.-H. (2003). Impact of isotypeselective estrogen receptor agonists on ovarian function. Proc Nat Acad Sci 101(14), 51295134.Google Scholar
Hemalatha, P., Reddy, A.G., Reddy, Y.R. & Shivakumar, P. (2013). Evaluation of protective effect of N-acetyl cysteine on arsenic-induced hepatotoxicity. J Nat Sci Biol Med 4(2), 393395.Google Scholar
Hernáandez, J., Syed, S., Weiss, G., Fernandes, G., von Merveldt, D., Troyer, D.A., Basler, J.W. & Thompson, I.M. Jr. (2005). The modulation of prostate cancer risk with alpha-tocopherol: a pilot randomized, controlled clinical trial. J Urol 174, 519522.Google Scholar
Hinshelwood, M.M., Demter-Arlotto, M., Means, G.D. & Simpson, E.R. (1994). Expression of genes encoding steroidogenic enzymes in the ovary. In Molecular Biology of the Female Reproductive System , Findlay, J.D. (Ed.), pp. 129145. San Diego, USA: Academic Press.Google Scholar
Hochstein, P. & Atallah, A.S. (1988). The nature of oxidants and antioxidant systems in the inhibition of mutation and cancer. Mutat Res 202(2), 363375.Google Scholar
Hong, I.-S., Cheung, A.P. & Leung, P.C.K. (2008). Gonadotropin-releasing hormones I and II induce apoptosis in human granulosa cells. J Clin Endocrinol Metab 93(8), 31793185.Google Scholar
Howard, C. & Reed, M. (1998). Unbiased Stereology: Three-Dimentional Measurement in Microscopy. UK: Bios Scientific Publishers.Google Scholar
Hughes, M.F., Beck, B.D., Chen, Y., Lewis, A.S. & Thomas, D.J. (2011). Arsenic exposure and toxicology: A historical perspective. Toxicol Sci 123(2), 305332.Google Scholar
Hyde, D.M., Tyler, N.K. & Plopper, C.G. (2007). Morphometry of the respiratory tract: Avoiding the sampling, size, orientation, and reference traps. Toxicol Pathol 35, 4148.Google Scholar
Jhala, D.D., Chinoy, N.J., Rao, M.V. (2008). Mitigating effects of some antidotes on fluoride and arsenic induced free radical toxicity in mice ovary. Food Chem Toxicol 46(3), 11381142.Google Scholar
Jhala, D.D., Nair, S.B. & Chinoy, N.J. (2004). Reversible toxicity of fluoride and arsenic in ovary of mice. Fluoride 37, 7179.Google Scholar
Jiang, J.-Q., Ashekuzzaman, S.M., Jiang, A., Sharifuzzaman, S.M. & Chowdhury, S.R. (2013). Arsenic contaminated groundwater and its treatment options in Bangladesh. Int J Environ Res Public Health 10, 1846.Google Scholar
Jones, R.E. (2005). Effects of mammalian gonadotropins on the ovaries and oviducts of the lizard, Lygosoma laterale. J Exp Zoology 171, 217221.Google Scholar
Kamel, F.A. & Kubajak, C.L. (1987). Modulation of gonadotropin secretion by corticosterone interaction with gonadal steroids and mechanism of action. Endocrinology 121, 561565.Google Scholar
Karbalay-Doustaied, S. & Noorafshan, A. (2012). Stereological estimation of ovarian oocyte volume, surface area and number: application on mice treated with nandrolone decanoate. Folia Histochem Cytobiol 50, 275279.Google Scholar
Lan, C.W., Chen, M.J., Jan, P.S., Chen, H.F. & Ho, H.N. (2013). Differentiation of human embryonic stem cells into functional ovarian granulosa-like cells. J Clin Endocrinol Metab 98(9), 37133723.Google Scholar
Lantz, R.C. & Hays, A.M. (2006). Role of oxidative stress in arsenic-induced toxicity. Drug Metab Rev 38(4), 791804.CrossRefGoogle ScholarPubMed
Litwin, I., Bocer, T., Dziadkowiec, D. & Wysocki, R. (2013). Oxidative stress and replication-independent DNA breakage induced by arsenic in Saccharomyces cerevisiae. PLoS Genet 9(7), e1003640.Google Scholar
Mahan, D.C. (1994). Effects of dietary vitamin E on sow reproductive performance over a five-parity. J Anim Sci 72, 28702879.Google Scholar
Mazumder, D.N.G. (2008). Chronic arsenic toxicity & human health. Indian J Med Res 128, 436447.Google Scholar
Menschik, Z. (1947). The influence of vitamin E on ovarian structure in mice. Q J Exp Physiol Cogn Med Sci 34(2), 97113.Google Scholar
Milton, A.H., Smith, W., Rahman, B., Hasan, Z., Kulsum, U., Dear, K., Rakibuddin, M. & Ali, A. (2005). Chronic arsenic exposure and adverse pregnancy outcomes in Bangladesh. Epidemiology 16, 8286.CrossRefGoogle ScholarPubMed
Mittal, M. & Flora, S.J. (2007). Vitamin E supplementation protects oxidative stress during arsenic and fluoride antagonism in male mice. Drug Chem Toxicol 30(3), 263281.Google Scholar
Morakinyo, A.O., Achema, P.U. & Adegoke, O.A. (2010). Effect of Zingiber officinale (Ginger) on sodium arsenite-induced reproductive toxicity in male rats. Afr J Biomed Res 13, 3945.Google Scholar
Mouton, P.R. (2002). Principles and Practices of Unbiased Stereology: An Introduction for Bioscientists. Baltimore and London: The Johns Hopkins University Press.Google Scholar
Mühlfeld, C., Nyengaard, J.R., Mayhew, T.M. (2010). A review of state-of-the-art stereology for better quantitative 3D morphology in cardiac research. Cardiovasc Pathol 19, 6582.Google Scholar
Myers, M., Britt, K.L., Wreford, N.G., Ebling, F.J., Kerr, J.B. (2004). Methods for quantifying follicular numbers within the mouse ovary. Reproduction 127, 569580.CrossRefGoogle ScholarPubMed
Nagao, T., Wada, K., Marumo, H., Yoshimura, S. & Ono, H. (2001). Reproductive effects of nonylphenol in rats after gavage administration: A two-generation study. Reprod Toxicol 15(3), 293315.Google Scholar
Nagaraja, T.N. & Desiraju, T. (1993). Regional alterations in the levels of brain biogenic amines, glutamate, GABA, and GAD activity due to chronic consumption of inorganic arsenic in developing and adult rats. Bull Environ Contam Toxicol 50, 100107.Google Scholar
Nasrabadi, T. & Bidabadi, N.S. (2013). Evaluating the spatial distribution of quantitative risk and hazard level of arsenic exposure in groundwater, case study of Qorveh County, Kurdistan Iran. Iranian J Environ Health Sci Eng 10(1), 30.Google Scholar
Nemec, M.D., Holson, J.F., Farr, C.H. & Hood, R.D. (1998). Developmental toxicity assessment of arsenic acid in mice and rabbits. Reprod Toxicol 12, 647658.Google Scholar
Niki, E. & Traber, M.G. (2012). A history of vitamin E. Ann Nutr Metab 61, 207212.Google Scholar
Noor, M., Joshi, D.V., Patel, B.J., Kher, A.C., Urvit, P.P. & Ghasura, R.S. (2012). Dimethoate induced haematological alterations and its amelioration with vitamin E in Wistar rats (Rattus norvegicus). Wayamba J Anim S 4, P413P419.Google Scholar
Noorafshan, A., Ahmadi, M., Mesbah, S.-F. & Karbalay-Doust, S. (2013). Stereological study of the effects of letrozole and estradiol valerate treatment on the ovary of rats. Clin Exp Reprod Med 40(3), 115121.Google Scholar
Omara, E.A., Nada, S.A., El-Toumy, S.A., Abdel-Salam, O. & Esmail, R.S. (2013). Ameliorative potential effect of grape seeds extract on testicular damage induced by sodium arsenite in rat. Planta Med 79, PA28.Google Scholar
Pal, S. & Chatterjee, A.K. (2006). Possible beneficial effects of melatonin supplementation on arsenic-induced oxidative stress in Wistar rats. Drug Chem Toxicol 29, 423433.Google Scholar
Parillo, F., Dall’Aglio, C., Verini Supplizi, A., Ceccarelli, P. & Gargiulo, A.M. (2003). Immunogold study on lectin binding in the porcine zona pellucida and granulosa cells. Eur J Histochem 47, 353358.Google Scholar
Pasternak, K., Sztanke, M. & Borzecki, A. (2004). Magnesium concentration in rat tissues receiving sex hormones and vitamin E. Ann Univ Mariae Curie Sklodowska Med 59(2), 114118.Google Scholar
Paszkowski, T., Traub, A.I., Robinson, S.Y. & McMaster, D. (1995). Selenium dependent glutathione peroxidase activity in human follicular fluid. Clin Chem Acta 236, 173180.Google Scholar
Pathania, V., Syal, N., Pathak, C.M. & Khanduja, K.L. (1999). Vitamin E suppresses the induction of reactive oxygen species release by lipopolysaccharide, interleukin-1beta and tumor necrosis factor-alpha in rat alveolar macrophages. J Nutr Sci Vitaminol (Tokyo) 45(6), 675686.Google Scholar
Patlolla, A.K. & Tchounwou, P.B. (2005). Serum acetyl cholinesterase as a biomarker of arsenic induced neurotoxicity in sprague-dawley rats. Int J Environ Res Public Health 2(1), 8083.Google Scholar
Portier, K.M. (2001). Statistical issues in assessing anthropogenic background for arsenic. Environ Forensic 2, 155160.Google Scholar
Rahman, A., Persson, L.A., Nermell, B.E.l., Arifeen, S., Ekström, E.C., Smith, A.H. & Vahter, M. (2010). Arsenic exposure and risk of spontaneous abortion, stillbirth, and infant mortality. Epidemiology 21(6), 797804.Google Scholar
Rao, M.V., Chawla, S.L. & Sharma, S.R. (2009). Protective role of vitamin E on nickel and/or chromium induced oxidative stress in the mouse ovary. Food Chem Toxicol 47, 13681371 .Google Scholar
Reilly, M.P., Saca, J.C., Hamilton, A., Solano, R.F., Rivera, J.R., Whitehouse-Innis, W., Parsons, J.G. & Dearth, R.K. (2013). Prepubertal exposure to arsenic(III) suppresses circulating insulin-like growth factor-1 (IGF-1) delaying sexual maturation in female rats. Reprod Toxicol S0890–6238(13), 0035100351.Google Scholar
Ricciarelli, R., Zingg, J.M. & Azzi, A. (2000). Vitamin E reduces the uptake of oxidized LDL by inhibiting CD36 scavenger receptor expression in cultured aortic smooth muscle cells. Circulation 102(1), 8287.Google Scholar
Ricciarelli, R., Zingg, J.M. & Azzi, A. (2001). Vitamin E: Protective role of a Janus molecule. FASEB J 15(13), 23142325.Google Scholar
Roy, P. & Saha, A. (2002). Metabolism and toxicity of arsenic: A human carcinogen. Curr Sci 82(1), 3845.Google Scholar
Sahinturk, V., Guclu, C. & Baycu, C. (2007). Protective effects of vitamin E on ethane dimethane sulfonate-induced testicular toxicity in rats. Asian J Androl 9, 117124.Google Scholar
Sengupta, S.R., Das, N.K. & Datta, P.K. (2008). Pathogenesis, clinical features and pathology of chronic arsenicosis. Indian J Dermatol Venereol Leprol 74, 559570.Google Scholar
Shahryari, T., Sharifzadah, G.h.R., Miry, M.R., Khosravi, R. & Barikbin, B. (2012). Check of arsenic in drinking water sources in the cities of South Khorasan in the year 2011. Eur J Exp Biol 2(5), 15031508.Google Scholar
Sharifi, Z. & Safari, A.A.S. (2013). Assessment of arsenic, nitrate and phosphorus pollutions in shallow groundwater of the rural area in Kurdistan province (Iran). Iranian J Environ Health Sci Eng 10, 30.Google Scholar
Shubin, M.V., Poglazov, A.F., Skotselias, I.u.G. & Vladimirov, I.u.A. (1975). [Letter: Effect of lipid peroxidation on the permeability of liposome membranes for Ca2+ ions]. Biofizika 20(1), 161163.Google Scholar
Shugo, S., Arnold, L.L. & Takamasa, O. (2008). Effects of inorganic arsenic on the rat and mouse urinary bladder. Toxicol Sci 106(2), 350363.Google Scholar
Shukla, J.P. & Pandey, K. (1984). Impaired ovarian functions in arsenic-treated freshwater fish, Colisa fasciatus (BL. and SCH.). Toxicol Lett 20, 13.Google Scholar
Sokka, T.A. & Huhtaniem, I.T. (1995). Functional maturation of the pituitary-gonadal axis in the neonatal female rat. Biol Reprod 52, 14041409.Google Scholar
Soleimani Mehranjani, M., Noorafshan, A., Momeni, H.R., Abnosi, M.H., Mahmoodi, M., Anvari, M. & Hoseini, S.M. (2009). Stereological study of the effects of vitamin E on testis structure in rats treated with para-nonylphenol. Asian J Androl 11, 508516.Google Scholar
Stilwell, D.E. & Gorny, K.D. (1997). Contamination of soil with copper, chromium, and arsenic under decks built from pressure treated wood. Bull Environ Contam Toxicol 58, 2229.Google Scholar
Styblo, M., Del Razo, L.M., Vega, L., Germolec, D.R., LeCluyse, E.L., Hamilton, G.A., Reed, W., Wang, C., Cullen, W.R. & Thomas, D.J. (2000). Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenical in rat and human cells. Arch Toxicol 74, 289299.Google Scholar
Sun, Y. (1990). Free radicals, antioxidant enzymes, and carcinogenesis. Free Radic Biol Med 8(6), 583599.Google Scholar
Susa, N., Ueno, S., Furukawa, Y. & Sugiyama, M. (1996). Protective effect of vitamin E on chromium (VI)-induced cytotoxicity and lipid peroxidation in primary cultures of rat hepatocytes. Arch Toxicol 71(1–2), 2024.Google Scholar
Tanaka, M., Takahashi, Y. & Yamaguchi, N. (2013). A study on adsorption mechanism of organoarsenic compounds on ferrihydrite by XAFS. J Phys Conf Ser 430, . doi: 10.1088/1742-6596/430/1/012100.Google Scholar
Umeda, F., Kato, K., Muta, K. & Ibayashi, H. (1982). Effect of vitamin E on function of pituitary-gonadal axis in male rats and human subjects. Endocrinol Jpn 29(3), 287292.Google Scholar
Waalkes, M.P., Ward, J.M. & Diwan, B.A. (2004). Induction of tumors of the liver, lung, ovary and adrenal in adult mice after brief maternal gestational exposure to inorganic arsenic: Promotional effects of postnatal phorbol ester exposure on hepatic and pulmonary, but not dermal cancers. Carcinogenesis 25, 133141.Google Scholar
Wang, X., Goldberg, J.M., Falcone, T., Agarwal, A., Attaran, M. & Sharma, R.K. (2002). Vitamin C and vitamin E supplementation reduce oxidative stress-induced embryo toxicity and improve the blastocyst development rate. Fertil Steril 78, 12721277.Google Scholar
Wang, Y., Newton, H., Spaliviero, J.A., Allan, C.M., Marshan, B., Handelsman, D.J. & Illingworth, P.J. (2005). Gonadotropin control of inhibin secretion and the relationship to follicle type and number in the hpg mouse. Biol Reprod 73(4), 610618.Google Scholar
Wassarman, P.M. (2008). Zona pellucida glycoproteins. J Biol Chem 283, 2428524289.Google Scholar
Welch, A.H., Westjohn, D.B., Helsel, D.R. & Wanty, R.B. (2005). Arsenic in ground water of the United States: Occurrence and geochemistry. Groundwater 38, 589604.CrossRefGoogle Scholar
Wolf, G. (2005). The discovery of the antioxidant function of vitamin E: The contribution of Henry A. Mattill. Am Soc Nutr Sci 135, 363366.Google Scholar
Wong-Ekkabut, J., Xu, Z.H., Triampo, W., Tang, I.-M., Tieleman, D.P. & Monticelli, L. (2007). Effect of lipid peroxidation on the properties of lipid bilayers: A molecular dynamics study. Biophys J 93(12), 42254236.Google Scholar
Yang, C.Y., Chang, C.C., Tsai, S.S., Chuang, H.Y., Ho, C.K. & Wu, T.N. (2003). Arsenic in drinking water and adverse pregnancy outcome in an arseniasisendemic area in northeastern Taiwan. Environ Res 91(1), 2934.Google Scholar
Yu, Y., Li, W., Han, Z., Luo, M., Chang, Z. & Tan, J. (2003). The effect of follicle-stimulating hormone on follicular development, granulosa cell apoptosis and steroidogenesis and its mediation by insulin-like growth factor-I in the goat ovary. Theriogenology 60(9), 16911704.Google Scholar
Zadorozhnaja, T.D., Little, R.E., Miller, R.K., Mendel, N.A., Taylor, R.J., Presley, B.J. & Gladen, B.C. (2000). Concentrations of arsenic, cadmium, copper, lead, mercury, and zinc in human placentas from two cities in Ukraine. J Toxicol Environ Health A 61(4), 255263.Google Scholar
Zhang, H., Long, D.M., Zhan, L. & Wu, D.S. (2006). Effects of nonylphenol on testis tissue development and apoptosis of F1 generation male SD rats in weaning. Sichuan Da Xue Xue Bao Yi Xue Ban 37(3), 421423.Google Scholar
Zheng, Y., Stute, M., van Geen, A., Gavrieli, I., Simpson, H.J., Schlosser, P., Ahmed, K.M. & Dhar, R. (2004). Redox control of arsenic mobilization in Bangladesh groundwater. Appl Geochem 19, 201214.Google Scholar