DOI QR코드

DOI QR Code

Estrogenicity of 4-nonylphenol and diethylstilbestrol on in vitro oocyte maturation of the dusky tripletooth goby, Tridentiger obscurus

  • Hwang, In-Joon (Department of Marine Biology, Pukyong National University) ;
  • Kim, Hyun-Woo (Department of Marine Biology, Pukyong National University) ;
  • Kim, Jin-Koo (Department of Marine Biology, Pukyong National University) ;
  • Lee, Young-Don (Marine and Environmental Research Institute, Cheju National University) ;
  • Baek, Hea-Ja (Department of Marine Biology, Pukyong National University)
  • Received : 2010.05.13
  • Accepted : 2010.06.22
  • Published : 2010.09.30

Abstract

This study investigated the estrogenicity of 4-nonylphenol (NP) and diethylstilbestrol (DES) in vitro during oocyte maturation in the marine fish, Tridentiger obscurus, using steroid hormone assays and GVBD assay. Vitellogenic (0.53mm diameter) and fully vitellogenic (0.75mm diameter) oocytes were in vitro exposed to NP (0.045 453.82 nM and DES (0.037 372.62 nM). In vitellogenic oocytes, 45.38 and 453.82nM NP and 3.73 372.62nM DES increas the estradiol-$17{\beta}$ (E2)/testosterone (T) ratio. In fully vitellogenic oocytes, 0.45, 45.38 and 453.82nM NP and 3.73nM DES increased E2/T. In the GVBD assay, 0.45 and 4.54nM NP and 0.037, 3.73 and 37.26nM DES inhibited GVBD. These results suggest that NP and DES have estrogen-agonistic effects in oocyte maturation in T. obscurus. In addition, NP and DES have different sensitivity according to the oocyte developmental stage, and the estrogenagonistic effects of DES were greater than were those of NP.

Keywords

References

  1. Arukwe A, Celius T, Walther BT, Goksoyr A. 1998. Plasma levels of vitellogenin and eggshell zona radiate proteins in 4-nonylphenol and o,p'-DDT treated juvenile atlantic salmon (Salmo salar). Mar Environ Res. 46:133-136. https://doi.org/10.1016/S0141-1136(98)00002-6
  2. Ashfield LA, Pottinger TG, Sumpter JP. 1998. Exposure of female juvenile rainbow trout to alkylphenolic compounds results in modifications to growth and ovosomatic index. Environ Toxicol Chem. 3:679-686.
  3. Baek HJ, Park MH, Lee YD, Kim HB. 2003. Effect of in vitro xenoestrogens on steroidogenesis in mature female fish, Chasmichthys dolichognathus. Fish Physiol Biochem. 28:413-414.
  4. Baek HJ, Hwang IJ, Kim KS, Lee YD, Kim HB, Yoo MS. 2007. Effects of BPA and DES on longchin goby (Chasmichthys dolichognathus) in vitro during the oocyte maturation. Mar Environ Res. 64:79-86. https://doi.org/10.1016/j.marenvres.2007.01.006
  5. Bevans HE, Goodbred SL, Miesner JF, Watkins SA, Gross TS, Denslow ND, Schoeb T. 1996. Synthetic organic compounds and carp endocrinology and histology in Las Vegas Wash and Las Vegas and Callville Bays of Lake Mead, Nevada 1992 and 1995. Water Resources Investigations Report 96-4266, US Department of the Interior- US Geological Survey, Carson City, NV, USA 12.
  6. Colborn T, Dunmanski D, Myers JP. 1996. Our stolen future. New York: Penguin Books. p. 1-306.
  7. Das S, Thomas P. 1999. Pesticides interfere with nongenomic action of a progestogen on meiotic maturation by binding to its plasma membrane receptor on fish oocytes. Endocrinol. 140:1953-1956. https://doi.org/10.1210/en.140.4.1953
  8. Folmar LC, Denslow ND, Rao V, Chow M, Crain DA, Enblom J, Marcino J, Guillette LJ. 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://doi.org/10.1289/ehp.961041096
  9. Folmar LC, Hemmer M, Hemmer R, Bowman C, Kroll K, Denslow ND. 2000. Comparative estrogenicity of estradiol, ethynyl estradiol and diethylstilbestrol in an in vivo, male sheepshead minnow (Caprinodon variegatus), vitellogenin bioassay. Aquat Toxicol. 49:77-88. https://doi.org/10.1016/S0166-445X(99)00076-4
  10. 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://doi.org/10.1016/0141-1136(94)00036-O
  11. Giesy JP, Pierens SL, Snyder EM, Miles-Richardson S, Kramer VJ, Snyder SA, Nichols KM, Villeneuve DL. 2000. Effects of 4-nonylphenol on fecundity and biomarkers of estrogenecity in fathead minnows (Pimephales promelas). Environ Toxicol Chem. 19:1368-1377. https://doi.org/10.1897/1551-5028(2000)019<1368:EONOFA>2.3.CO;2
  12. Gray MA, Metcalfe CD. 1997. Induction of testis-ova in Japanese medaka (Oryzias latipes) exposed to p-nonylphenol. Environ Toxicol Chem. 16:1082-1086.
  13. Heppell SA, Denslow ND, Folmar LC, Sullivan CV. 1995. Universal assay of vitellogenin as a biomarker for environmental estrogens. Environ Health Perspect. 103:9-15.
  14. Hwang IJ, Lee YD, Kim HB, Baek HJ. 2008. Estrogenic activity of nonylphenol in marine fish, Hexagrammos otakii, during oocyte development by evaluating sex steroid levels. Cybium 32(2):251-252.
  15. Jin YS, Park CB, Kim HJ, Lee CH, Song YB, Kim BH, Lee YD. 2006. Reproductive cycle of dusky tripletooth goby, Tridentiger obscurus in Jeju Island, Korea. Korean J Ichthyol. 18:184-192 (in Korean).
  16. Jobling S, Sheahan D, Osborne JA, Matthiessen P, Sumpter JP. 1996. Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic chemicals. Environ Toxicol Chem. 15:194-202.
  17. Kaneko T, Hanyu I. 1985. Annual reproductive cycle of the chichibu goby, Tridentiger obscurus. Bull Jap Soc Sci Fish. 51(10):1645-1650. https://doi.org/10.2331/suisan.51.1645
  18. Kilp H, Verloop J, van Gool JD, Koster ME, Burger CW, van Leeuwen FE. 2002. Hypospadias in sons of women exposed to diethylstilbestrol in utero: a cohort study. Lancet. 359:1102-1107. https://doi.org/10.1016/S0140-6736(02)08152-7
  19. Kim IS, Choi Y, Lee CL, Lee YJ, Kim BJ, Kim JH. 2005. Illustrated book of Korean fishes. Kyo-Hak Publishing.
  20. Kinnberg K, Korsgaard B, Bjerregaard P, Jespersen A. 2000. Effects of nonylphenol and 17$\beta$-estradiol on vitellogenin synthesis and testis morphology in male platyfish, Xiphophorus maculates. J Exp Biol. 203:171-181.
  21. Kobayashi M, Aida K, Sakai H, Kaneko T, Asahina K, Hanyu I, Ishii S. 1987. Radioimmunoassay for salmon gonadotropin. Nippon Suisan Gakk. 53:995-1003. https://doi.org/10.2331/suisan.53.995
  22. Maguire RJ. 1999. Review of the persistence of nonylphenol and nonylphenol ethoxylates in aquatic environments. Water Qual Res J Can. 34:37-78.
  23. Pankhurst NW, 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://doi.org/10.1016/S1095-6433(00)00251-8
  24. Patino R, Sullivan CV. 2002. Ovarian follicle growth, maturation, and ovulation in teleost fish. Fish Physiol Biochem. 26:57-70. https://doi.org/10.1023/A:1023311613987
  25. Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS. 2001. Estrogen imprinting of the developing prostate gland is mediated through stromal estrogen receptor a: Studies with aERKO and $\beta$ERKO mice. Cancer Res. 61:6089-6097.
  26. Rocha MJ, Reis-Henriques MA. 1998. Steroid metabolism by ovarian follicles of the tilapia Oreochromis mossambicus (Teleostei, Cichlidae). Comp Biochem Physiol B. 121:85- 90. https://doi.org/10.1016/S0305-0491(98)10130-X
  27. Rocha MJ, Reis-Henriques MA. 2000. Steroid metabolism by ovarian follicles of the sea bass Dicentrarchus labrax. Comp Biochem Physiol C. 125:85-91. https://doi.org/10.1016/S1095-6433(99)00156-7
  28. Servos MR. 1999. Review of the aquatic toxicity, estrogenic responses and bioaccumulation of alkylphenols and alkylphenol polyethoxylates. Water Qual Res J Can. 34:123-177.
  29. Sumpter JP, Jobling S. 1995. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ Health Perspect. 103:173-179.
  30. Talmage SS. 1994. Environmental and human safety of major surfactants: alcohol ethoxylates and alkylphenol ethoxylates. Boca Raton (FL): Lewis. p. 35-50.
  31. Tokumoto T, Tokumoto M, Horiguchi R, Ishikawa K, Nagahama Y. 2004. Diethylstilbestrol induces fish oocyte maturation. Proc Natl Acad Sci USA. 101:3686-3890. https://doi.org/10.1073/pnas.0400072101
  32. Tokumoto T, Tokumoto M, Nagahama Y. 2005. Induction and inhibition of oocyte maturation by EDCs in zebrafish. Reprod Biol Endocrinol. 3:69. https://doi.org/10.1186/1477-7827-3-69
  33. 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. Endocrinol. 148:3459-3467. https://doi.org/10.1210/en.2006-1694
  34. Yang L, Lin L, Weng S, Feng Z, Luan T. 2008. Sexually disrupting effects of nonylphenol and diethylstilbestrol on male silver carp (Carassius auratus) in aquatic microcosms. Ecotoxicol Environ Safety. 71:400-411.
  35. Ying GG, Williams B, Kookana R. 2002. Environmental fate of alkylphenols and alkylphenol ethoxylates-a review. Environ Int. 28:215-226. https://doi.org/10.1016/S0160-4120(02)00017-X
  36. Zhong XP, Xu Y, Liang Y, Liao T,Wang J. 2005. The Chinese rare minnow (Gobiocypris rarus) as an in vivo model for endocrine disruption in freshwater teleosts: a full lifecycle test with diethylstilbestrol. Aquat Toxicol. 71:85-95. https://doi.org/10.1016/j.aquatox.2004.10.014

Cited by

  1. Toxic Impact of Alkylphenols on the Fish Reproduction and Endocrine Disruption vol.74, pp.4, 2010, https://doi.org/10.1007/s12595-021-00416-z