Keerikkattil P. JOY, Geeta J. GAUTAM, Radha CHAUBE

In Vitro Effects of 4-Nonylphenol on Oocyte Maturation and Ovarian Steroid Hormone Dynamics in the Catfish Heteropneustes fossilis

Alkylphenols are known endocrine-disrupting chemicals present in water bodies ascontaminants, affecting aquatic life adversely. In this study, post vitellogenic follicles of thecatfish Heteropneustes fossilis were in vitro exposed to 4-nonylphenol (4-NP) atconcentrations of 0.1, 0.5, 1, 10, 100 and 200 ng/mL for 12 and 24 h. Germinal vesiclebreakdown (GVBD), an indicator of final oocyte maturation (FOM), and the mortality ofovarian follicles were monitored. Levels of estradiol-17β (E2), testosterone (T), progestins;progesterone (P4), 17α-hydroxyprogesterone (17-P), 17α, 20β-dihydroxy-4-pregnen-3-one(17, 20β-DP), and cortisol (F) were measured by ELISA or HPLC. The exposure to lowerconcentrations of 4-NP (0.1, 0.5, 1 and 10 ng/mL) induced GVBD time dependently and thehighest rate of induction was up to 25% in 0.5 ng/mL group. The higher concentrationsdecreased GVBD. 4-NP significantly increased the mortality rate of follicles in a dosedependentmanner. Concentrations ≥10 ng/mL produced more than 60% mortality. 4-NPelicited biphasic effects on all hormones measured, except in the level of 17-P. The levels ofT, E2, P4, 17, 20β-DP and F increased at the lower concentrations and maximum increase wasat 0.1 ng/mL dose for E2, P4 and 17, 20β-DP, at 0.5 ng/mL dose for F and at 1 ng/mL dose forT. Then, they were declined with increasing 4-NP concentration. In contrast, 17-P levelexhibited a continuous decline in a dose-dependent manner. From the results, it is inferredthat the low concentrations of 4-NP stimulated GVBD. Increase in E2level might havelowered the rate of GVBD, despite the high level of 17,20β-DP, maturation-inducing steroid,and F. The cytotoxicity infused by 4-NP at higher concentrations adversely affected GVBDand steroid secretion, causing follicle mortality.

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Arukwe, A., Goksoyr, A., Thibaut, R., &Cravedi, J.P. (2000). Metabolism and organ distribution of nonylphenol in Atlantic salmon (Salmo salar). Mar. Environ. Res.50, 141- 45.https://dx.doi.org/10.1016/s0141-1136(00)00081-7
Arukwe, A., Knudsen, F.R.,&Goksøyr, A.(1997).Fish zona radiata (eggshell) protein: A sensitive biomarker for environmental estrogens. Environ. Health. Perspect. 105, 418-22.https://dx.doi.org/10.1289/ehp.97105418
Arukwe, A.(2005). Modulation of brain steroidogenesis by affecting transcriptional changes of steroidogenic acute regulatory (StAR) protein and cholesterol side chain cleavage (P450scc) in Juvenile Atlantic salmon (Salmosalar) is a novel aspect of nonylphenol toxicity. Env. Sci. Technol. 39, 9791-9798. https://dx.doi.org/10.1021/es0509937
Babin, P.J., Carnevali, O., Lubzens, E., &Schneider, W.J.(2007). Molecular aspects of oocyte vitellogenesis in fish. In: Babin, P.J., Cerdà, J., Lubzens, E. (Eds.), The Fish Oocyte: from Basic Studies to Biotechnological Applications. Springer, The Netherlands. ISBN: 978-1-4020-6234-6. 39, 6234-6236. https://dx.doi.org/10.1007/978-1-4020-6235-3_2
Baek, H.J., Park, M.H., Lee, Y.D., &Kim, H.B.(2003). Effect of in vitro xenoestrogens on steroidogenesis in mature female fish, Chasmichthysdolichognathus. Fish Physiol. Biochem. 28, 413–414. https://dx.doi.org/10.1023/b:fish.0000030609.71170.f9
Bennie, D.T.(1999). Review of the environmental occurrence of alkylphenols and alkylphenol ethoxylates. Wat. Qual. Res. J. Can. 34, 79-122.
Chaube, R., Gautam, G.J., &Joy, K.P.(2013). Teratogenic effects of 4-nonylphenol on early embryonic and larval development of the catfish Heteropneustes fossilis. Arch. Environ. Contam. Toxicol. 64, 554-561. https://dx.doi.org/10.1007/s00244-012-9851-7
Chester Jones, I., Mosley, W., Henderson, I. W., &Garland, H. O.(1980). The interregnal gland in pisces. In General, Comparative and Clinical Endocrinology of the adrenal cortex. (I. Chester Jones and I. W. Henderson eds) London: Academic Press.) vol. III: 396–523. https://dx.doi.org/10.1016/b978-0-12-171502-1.50004-6
Chitra, K. C., Latchoumycandane, C., &Mathur, P.P.(2002). Effect of nonylphenol on the antioxidant system in epididymal sperm of rats. Arch. Toxicol. 76, 545– 551.https://dx.doi.org/10.1007/s00204-002-0372-4
Chitra, K. C., Latchoumycandane, C., &Mathur, P.P. (2003). Induction of oxidative stress by bisphenol A in the epididymal sperm of rats. Toxicology 185, 119- 127.https://dx.doi.org/10.1016/s0300-483x(02)00597-8
Chourasia, T., &Joy, K.P.(2012). In vitro effects of 2- hydroxyestradiol-17 on steroid production by postvitellogenic ovary in the catfish Heteropneustes fossilis: identification of the receptor and signaling mechanisms. Gen. Comp. Endocrinol. 175(3), 500- 513.https://dx.doi.org/10.1016/j.ygcen.2011.12.007
Denslow, N. D., &Sepulveda, M. S.(2007). Ecotoxicological effects of endocrine disrupting compounds on fish reproduction. In The Fish Oocyte: From Basic Studies to Biotechnological Applications (Babin, P. J., Cerda, J., Lubzens, E., eds), pp. 255– 322. The Netherlands: Springer Publishing Co, Dordrecht. https://dx.doi.org/10.1007/978-1-4020-6235-3_10
Ferreira, M., Moradas-Ferreira, P.,& Reis-Henriques, M. A.(2005). Oxidative stress biomarkers in two resident species, mullet (Mugil cephalus) and flounder (Platichthys flesus), from a polluted site in River Douro Estuary, Portugal. Aquat. Toxicol. 71, 39-48 https://dx.doi.org/10.1016/j.aquatox.2004.10.009
Folmar, L.C., Denslow, N.D., Rao, V., Chow, M., Crain, D.A., Enblom, J., Marcino, J., &Guillette, L.J. Jr, (1996). Vitellogenin induction and reduced serum testosterone concentrations in feral male carp (Cyprinus carpio) captured near a major metropolitan sewage treatment plant. Environ. Health Perspect. 104, 1096–1101. https://dx.doi.org/10.1289/ehp.961041096
Ghosh, S., &Thomas, P.(1995). Antagonistic effects of xenobiotics on steroid-induced final maturation of Atlantic croaker oocytes in vitro. Mar. Environ. Res. 39, 159-163. https://dx.doi.org/10.1016/0141-1136(94)00036-o
Giesy, J.P., Pierens, S.L., Synder, E.M., Miles-Richardson, S., Kramer, V.J., Snyder, S.A., Nichols, K.M., &Villeneuve, D.A.(2000). Effects of 4-nonylphenol on fecundity and biomarkers of estrogenicity in fathead minnows Pimephales promelas. Environ. Toxicol. Chem. 19, 1368- 1377. https://dx.doi.org/10.1897/1551- 5028(2000)019<1368:eonofa>2.3.co;2
Goetz, F. W.(1983). Hormonal control of oocyte maturation and ovulation in fishes. In Fish Physiology, Vol. IXA (eds W. S. Hoar, D. J. Randall & E. M. Donaldson), Academic Press, New York, 117-170 https://dx.doi.org/10.1016/s1546-5098(08)60303-9
Goswami, S. V., &Sundararaj, B. I.(1971). In vitro maturation and ovulation of oocytes of the catfish, Heteropneustes fossilis (Bloch): Effects of mammalian hypophyseal hormones, catfish pituitary homogenate, steroid precursors and metabolites, and gonadal and adrenocortical steroids. J. Exp. Zool. 467-478. https://dx.doi.org/10.1002/jez.1401780405
Gray, M.A., &Metcalfe, C.D. (1997). Induction of testis-ova in Japanese medaka (Oryzias latipes) exposed to pnonylphenol. Environ. Toxicol. Chem. 16, 1082-86. https://dx.doi.org/10.1897/1551- 5028(1997)016<1082:iotoij>2.3.co;2
Hill, R.L., &Jr Janz, D.M.(2003). Developmental estrogenic exposure in zebrafish (Danio rerio). I. Effects on sex ratio and breeding success. Aquat. Toxicol. 63, 417- 29.https://dx.doi.org/10.1016/s0166-445x(02)00207-2
Hwang, I.J., Kima, H.W., Kima, J.K., Leeb, Y.D., &Baeka, H. J.(2010). Estrogenicity of 4-nonylphenol and diethylstilbestrol on in vitro oocyte maturation of the dusky tripletooth goby. Ani. Cells Sys. 14(3), 161- 167.https://dx.doi.org/10.1080/19768354.2010.504339
Hwang, I.J., Lee, Y.D., Kim, H.B., &Baek, H.J. (2008). Estrogenic activity of nonylphenol in marine fish, Hexagrammos otakii, during oocyte development by evaluating sexsteroid levels. Cybium 32(2), 251-252.
Ishibashi H, Hirano M, Matsumura N, Watanabe N, Takao Y, &Arizono K.(2006). Reproductive effects and bioconcentration of 4-nonylphenol in medaka fish (Oryzias latipes). Chemosphere 65, 1019–1026. https://dx.doi.org/10.1016/j.chemosphere.2006.03.034
Jalabert, B., Fostier, A., Breton, Β., &Weil, C.(1991). Oocyte maturation in vertebrates; In Vertebrate. endocrinology: Fundamentals and biomedical implications(eds) Peter Κ Τ Pang and Μ Ρ Schreibman (New York; Academic Press) Vol. 4 part A, 23-90
Jobling, S.,& Tyler, C.R.(2003).Endocrine disruption in wild freshwater fish.Pure Appl. Chem., 75(11–12), 2219-2234. https://dx.doi.org/10.1351/pac200375112219
Khim, J.S., Lee, K.T., Kannan, K., Villeneuve, D.L., Giesy, J.P., &Koh, C.H.(2001). Trace organic contaminants in sediment and water from Ulsan Bay and its vicinity, Korea. Arch. Environ. Contam. Toxicol. 40, 141- 150.https://dx.doi.org/10.1007/s002440010157
Kinnberg, K., Korsgaard, B., Bjerregaard, P., &Jespersen, A.(2000). Effects of nonylphenol and 17ß-estradiol on vitellogenin synthesis and testis morphology in male platyfish, Xiphophorus maculates. J. Exp. Biol. 203, 171- 181.
Kortner, T. M., &Arukwe, A.(2007). The xenoestrogen, 4- nonylphenol, impaired steroidogenesis in previtellogenic oocyte culture of Atlantic cod (Gadus morhua) by targeting the StAR protein and P450scc expressions. Gen. Comp. Endocrinol. 150 ,419–429. https://dx.doi.org/10.1016/j.ygcen.2006.10.008
Labadie, P., &Budzinski, H.(2006). Alteration of steroid hormone profile in juvenile turbot (Psetta maxima) as a consequence of short-term exposure to17aethynylestradiol. Chemosphere 64, 1274–1286. https://dx.doi.org/10.1016/j.chemosphere.2005.12.065
Lahnsteiner, F., Berger, B., Grubinger, F., &Weismann, T.(2005). The effect of 4-nonylphenol on semen quality, viability of gametes, fertilization success, and embryo and larvae survival in rainbow trout (Oncorhynchus mykiss). Aquat. Toxicol.71, 297-306. https://dx.doi.org/10.1016/j.aquatox.2004.11.007
Mishra, A. & Joy, K.P.(2006). Involvement of mitogen-activated protein kinase in 2-hydroxyestradiol-17β-induced oocyte maturation in the catfish Heteropneustes fossilisand a note on possible interaction with protein phosphatases. Gen. Comp. Endocrinol. 147(3):329-335 https://dx.doi.org/10.1016/j.ygcen.2006.02.002
Nagahama, Y. &Yamashita, M.(2008). Regulation of oocyte maturation in fish. Develop. Growth Differ. 50, S195- S219. https://dx.doi.org/10.1111/j.1440-169x.2008.01019.x
Nagahama, Y.(1997). 17 α,20 β-Dihydroxy-4-Pregnen-3-One, a Maturation-Inducing Hormone in Fish Oocytes: Mechanisms of Synthesis and Action.Steroids 62, 190– 196. https://dx.doi.org/10.1016/s0039-128x(96)00180-8
Nagahama, Y., Yoshikuni, M., Yamashita, M., Tokumoto, T.,& Katsu, Y.(1995). Regulation of oocytegrowth and maturation in fish. Curr. Top. Dev. Biol. 30.https://dx.doi.org/10.1016/s0070-2153(08)60565-7
Nimrod, A.C.,& Benson, W.H.(1996). Environmental Estrogenic Effects of Alkylphenol Ethoxylates.Cri. Rev. Toxicol. 26(3), 335-364. https://dx.doi.org/10.3109/10408449609012527
Pang, Y., &Thomas, P.(2009). Involvement of estradiol-17 beta and its membrane receptor, G protein coupled receptor 30 (GPR30) in regulation of oocyte maturation in zebrafish, Danio rerio. Gen. Comp. Endocrinol. 161, 58– 61. https://dx.doi.org/10.1016/j.ygcen.2008.10.003
Pankhurst, N.W., &Riple, G.(2000). Characterization of parameters for in vitro culture of isolated ovarian follicles of greenback flounder Rhombosolea tapirina. Comp. Biochem. Physiol. A. 127, 177- 189.https://dx.doi.org/10.1016/s1095-6433(00)00251-8
Petrovic, M., Sole, M., de Alda, M.J.L., &Barcelo, D., (2002). Endocrine disruptors in sewage treatment plants, receiving river waters, and sediments: integration of chemical analysis and biological effects on feral carp. Environ. Toxicol. Chem. 21, 2146-56. https://dx.doi.org/10.1897/1551- 5028(2002)021<2146:edistp>2.0.co;2
Pocar, P., Brevini, T.A., Fischer, B.,& Gandolfi, F., (2003). The impact of endocrine disruptors on oocyte competence. Reproduction 125, 313–325. https://dx.doi.org/10.1530/rep.0.1250313
Rocha, M.J., &Reis-Henriques, M.A.(1998). Steroid metabolism by ovarian follicles of the tilapia Oreochromis mossambicus (Teleostei, Cichlidae). Comp. Biochem. Physiol. B. 121, 85- 90.https://dx.doi.org/10.1016/s0305-0491(98)10130-x
Scholz, S., &Gutzeit, H.O.(2000). 17-a-Ethinylestradiol affects reproduction, sexual differentiation and aromatase gene expression of the medaka (Oryzias latipes). Aquat. Toxicol. 50, 363– 373. https://dx.doi.org/10.1016/s0166-445x(00)00090-4
Servos, M.R.(1999). Review of the aquatic toxicity, estrogenic responses and bioaccumulation of alkylphenols and alkylphenol polyethoxylates. Water Qual. Res. J Can. 34, 123-177.
Soares, A., Guieysse, B., Jefferson, B., Cartmell, E., &Lester, J.N.(2008). Nonylphenol in the environment: a critical review on occurrence, fate, toxicity and treatment in wastewaters. Environ. Int. 34, 1033–1049. https://dx.doi.org/10.1016/j.envint.2008.01.004
Sohoni, P., Tyler, C.R., Hurd, K., Caunter, J., Hetheridge, M., Williams, T., Woods, C., Evans, M., Toy, R., Gargas, M., &Sumpter J.P.(2001). Reproductive effects of long-term exposure to Bisphenol A in 40 the fathead minnow (Pimephales promelas). Environ. Sci. Technol.35(14), 2917-2925. https://dx.doi.org/10.1021/es000198n
Sundararaj, B.I.&Goswami, S.V.(1977). Hormonal regulation of in vivo and in vitro oocyte maturation in the catfish, Heteropneustes fossilis (Bloch). Gen. Comp. Endocrinol. 32, 17-28. https://dx.doi.org/10.1016/0016-6480(77)90079-x
Thomas, P.(1999). Nontraditional sites of endocrine disruption by chemicals on the hypothalamus-pituitary-gonadal axis: Interactions with steroid membrane receptors, monoaminergic pathways and signal transduction systems. In R. K. Naz (ed.). Endocrine disruptors: Effects on male and female reproductive systems. CRC Press, Boca Raton, Florida. 3-38.
Tokumoto, T., Tokumoto, M., Horiguchi, R., Ishikawa., K.,&Nagahama., Y.(2004). Diethylstilbestrol induces fish oocyte maturation, Proc. Natl. Acad.Sci. USA. 101, 3686- 3690 https://dx.doi.org/10.1073/pnas.0400072101 T okumoto, T., Tokumoto, M., & Nagahama, Y.(2005). Induction and inhibition of oocyte maturation by EDCs in zebrafish. Reprod. Biol. Endocrinol. 3, 69. https://dx.doi.org/10.1186/1477-7827-3-69
Tokumoto, T., Tokumoto, M., & Thomas, P.(2007). Interactions of diethylstilbestrol (DES) and DES analogs with membrane progestin receptor-alpha and the correlation with their nongenomic progestin activities. Endocrinology 148, 3459-3467. https://dx.doi.org/10.1210/en.2006-1694
Trant, J.M., & Thomas, P.(1988). Structure-activity relationships of steroids in inducing germinal vesicle breakdown of Atlantic croaker oocyte in vitro. Gen. Comp. Endocrinol. 71, 307–317. https://dx.doi.org/10.1016/0016-6480(88)90259-6
Vetillard, A., & Bailhache, T. (2006). Effects of 4-n-Nonylphenol and Tamoxifen on Salmon Gonadotropin-Releasing Hormone, Estrogen Receptor, and Vitellogenin Gene Expression in Juvenile Rainbow Trout. Tox. Sci. 92 (2), 537-544https://dx.doi.org/10.1093/toxsci/kfl015
White. R., Jobling, S., Hoare, S.A., Sumpter, J.P., &Parker, M.G. (1994). Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology135,175-82. https://dx.doi.org/10.1210/endo.135.1.8013351
Ying, G.G., & Kookana, R.S.(2002). Endocrine disruption: an Australian Perspective. AWA. J. Water,29(no. 6):53-57. Identifier: procite:5bf92e7f-2f14-441f-9150- fe0f43381560
Ying, G.G., Williams, B., & Kookana, R.(2002). Environmental fate of alkylphenols and alkylphenol ethoxylates-a review. Environ. Int. 28, 215-226. https://dx.doi.org/10.1016/s0160-4120(02)00017-x
Zhong, X., Xu, Y., Liang, Y., Liao, T., &Wang, J.(2005).The Chinese rare minnow (Gobiocypris rarus) as an invivo model for endocrine disruption in freshwater teleosts: a full life-cycle test with diethylstilbestrol. Aquat. Toxicol. 71, 85-95 https://dx.doi.org/10.1016/j.aquatox.2004.10.014