DOI QR코드

DOI QR Code

Effects of nonylphenol and 3,3',4,4',5-pentachlorobiphenyl on in vitro oocyte steroidogenesis in redlip mullet, Chelon haematocheilus

  • Baek, Hea-Ja (Department of Marine Biology, Pukyong National University) ;
  • Hwang, In-Joon (Department of Marine Biology, Pukyong National University) ;
  • Lee, Young-Don (Marine and Environmental Research Institute, Cheju National University) ;
  • Kim, Hyung-Bae (Department of Marine Bio-resources, Gangwon Provincial University)
  • Received : 2010.12.28
  • Accepted : 2011.03.22
  • Published : 2011.09.30

Abstract

We investigated the in vitro effects of nonylphenol (NP) and 3,3',4,4',5-pentachlorobiphenyl (PCB126) on steroidogenesis in redlip mullet, Chelon haematocheilus, oocytes. In experiment 1, we investigated the effects of NP and PCB126 on steroid production from exogenous steroid precursors. Vitellogenic oocytes (0.75 mm in diameter) were incubated with 10 and 100 ng/ml NP or PCB126 with $[^3H]17{\alpha}$-hydroxyprogesterone as a precursor. The major metabolites produced were androstenedione, testosterone (T), estrone, and estradiol-$17{\beta}$ ($E_2$). Both NP and PCB126 increased T production and decreased $E_2$ production, except for 100 ng/ml PCB126. In experiment 2, oocytes (0.65-0.75 mm in diameter) were exposed to NP and PCB126 at different concentrations (0.01, 0.1, 1, 10, and 100 ng/mL). After the incubation, T and $E_2$ production was measured by radioimmunoassay. NP inhibited $E_2$ production at concentrations of 0.01 and 0.1 ng/ml in 0.75-mm-diameter oocytes. NP at 1 and 100 ng/mL stimulated T production, but had no observable effect on $E_2$ production. PCB126 treatment did not affect $E_2$ production at any of the concentrations tested. NP alone at 0.1 ng/mL resulted in a significant decrease in $E_2$ production in 0.65-mm-diameter oocytes. PCB126 did not show any significant effects on either T or $E_2$ production at all concentrations tested. These results suggest that NP acts like an antiestrogen at lower concentrations (0.01-0.1 ng/ml) in vitellogenic oocytes of redlip mullet.

Keywords

References

  1. Arcand-Hoy LD, Benson WH. 1998. Fish reproduction: an ecologically relevant indicator of endocrine disruption. Environ Toxicol Chem. 17:49-57. https://doi.org/10.1002/etc.5620170108
  2. Arukwe A, Goksøyr A. 2003. Eggshell and egg yolk proteins in fish: hepatic proteins for the next generation-oogenetic, population, and evolutionary implications of endocrine disruption. Comp Hepatol. 2:4. https://doi.org/10.1186/1476-5926-2-4
  3. Arukwe A, Knudsen FR, Goksoyr A. 1997. Fish zona radiata (eggshell) protein: a sensibile biomarker for enviromental estrogens. Environ Health Perspect. 105:418-422. https://doi.org/10.1289/ehp.97105418
  4. 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
  5. Arukwe A, Celius T,Walther BT, Goksoyr A. 2000. Effects of xenoestrogen treatment on zona radiata protein and vitellogenin expression in Atlantic salmon (Salmo salar). Aquat Toxicol. 49:159-170. https://doi.org/10.1016/S0166-445X(99)00083-1
  6. Astroff B, Safe S. 1990. 2,3,7,8-tetrachlorodibenzo-p-dioxin as an antiestrogen: effect on rat uterine peroxidase activity. Biochem Pharmacol. 39:485-488. https://doi.org/10.1016/0006-2952(90)90054-O
  7. 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.
  8. 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. https://doi.org/10.1023/B:FISH.0000030609.71170.f9
  9. Baek HJ, Hwang IJ, Park MH, Kim HB. 2009. Effects of nonylphenol and 2,2',4,6,6'-pentachlorobiphenyl on in vitro sex steroid production in maturing oocytes of the yellowfin goby, Acanthogobius flavimanus. Fish Aqua Sci. 12:293-298.
  10. Billsson K, Westerlund L, Tysklind M, Olsson P. 1998. Developmental disturbances caused by polychlorina-ted biphenyls in zebrafish (Brachydanio rerio). Mar Environ Res. 46:461-464. https://doi.org/10.1016/S0141-1136(97)00041-X
  11. Cionna C, Maradonna F, Olivotto I, Pizzonia G, Carnevali O. 2006. Effects of nonylphenol on juveniles and adults in the grey mullet, Liza aurata. Reprod Toxicol. 22:449-454. https://doi.org/10.1016/j.reprotox.2006.04.025
  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. Gregoraszczuk EL, Grochowalski A, Chrzaszcz R, Wegiel M 2003a. Congener-specific accumulation of polychlorinated biphenyls in ovarian follicular wall follows repeated exposure to PCB126 and PCB153. Comparison of tissue levels of PCB and biological changes. Chemosphere. 50:481-488. https://doi.org/10.1016/S0045-6535(02)00637-9
  14. Gregoraszczuk EL, Sowa M, Kajta M, Ptak A, Wojtowicz A 2003b. Effect of PCB 126 and PCB 153 on incidence of apoptosis in cultured theca and granulosa cells collected from small, medium and large preovulatory follicles. Reprod Toxicol. 17:465-471. https://doi.org/10.1016/S0890-6238(03)00042-X
  15. Gregoraszczuk EL, Rak A, Ludewig G, Gasin?ska A. 2008. Effects of estradiol, PCB3 and their hydroxylated metabolites on proliferation, cell cycle, and apoptosis of human breast cancer cells. Environ Toxicol Pharmacol. 25:227-233. https://doi.org/10.1016/j.etap.2007.10.004
  16. Hong L, Fujita T, Wada T, Amano H, Hiramatsu N, Zhang X, Todo T, Hara A. 2009. Choriogenin and vitellogenin in red lip mullet (Chelon haematocheilus): purification, haracterization, and evaluation as potential biomarkers for detecting estrogenic activity. Comp Biochem Physiol. 149C:9-17.
  17. 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.
  18. Jobling S, Reynolds T, White R, Parker MG, Sumpter JP. 1995. A variety of environmentally persistent chemicals, including some phthalate plasticizers, are weakly estrogenic. Environ Health Perspect. 103:582-587. https://doi.org/10.1289/ehp.95103582
  19. 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. https://doi.org/10.1002/etc.5620150218
  20. Jobling S, Casey D, Rodgers-Gray T, Oehlmann J, Pawlowski S, Baunbcck T, Turner AP, Tyler CR. 2003. Comparative responses of molluscs and fish to environmental oestrogens and an oestrogenic effluent. Aquat Toxicol. 65: 205-220. https://doi.org/10.1016/S0166-445X(03)00134-6
  21. Kime DE. 1998. Endocrine Disruption in Fish. Boston (MA): Kluwer Academic. p. 240-245.
  22. 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.
  23. 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
  24. Lind PM, Eriksen EF, Sahlin L, Edlund M, Orberg J. 1999. Effects of the antiestrogenic environmental pollutant 3,3$\prime$,4,4$\prime$,5-pentachlorobiphenyl (PCB126) in rat bone and uterus: diverging effects in ovariectomized and intact animals. Toxicol Appl Pharmacol. 154:236-244. https://doi.org/10.1006/taap.1998.8568
  25. Liu S, Abdelrahim M, Khan S, Ariazi E, Jordan VC, Safe S. 2006. Aryl hydrocarbon receptor agonists directly activate estrogen receptor alpha in MCF-7 breast cancer cells. Biol Chem. 387:1209-1213.
  26. Maguire RJ. 1999. Review of the persistence of nonylphenol and nonylphenol ethoxylates in aquatic environments. Water Qual Res J Can. 34:37-78.
  27. Mortensen AS, Arukwe A. 2008. Activation of estrogen receptor signaling by the dioxin-like aryl hydrocarbon receptor agonist, 3,3$\prime$,4,4V,5-Pentachlorobiphenyl (PCB 126) in salmon in vitro system. Toxicol Appl Pharmacol. 227:313-324. https://doi.org/10.1016/j.taap.2007.11.003
  28. Muto T, Wakui S, Imano N, Nakaaki K, Takahashi H, Hano H, Furusato M, Masaoka T. 2002. Mammary gland differentiation in female rats after prenatal exposure to 3,3',4,4',5-pentachlorobiphenyl. Toxicology. 177: 197-205. https://doi.org/10.1016/S0300-483X(02)00224-X
  29. Navas JM, Segner H. 2006. Vitellogenin synthesis in primary cultures of fish liver cells as endpoint for in vitro screening of the (anti)estrogenic activity of chemical substances. Aquat Toxicol. 80:1-22. https://doi.org/10.1016/j.aquatox.2006.07.013
  30. Safe S. 1994. Polychlorinated biphenyls PCBs: Environmental impact, biochemical and toxic responses, and implications for risk assessment. CRC Crit Rev Toxicol. 24:87. https://doi.org/10.3109/10408449409049308
  31. Scholz S, Mayer I. 2008. Molecular biomarkers of endocrine disruption in small model fish. Mol Cell Endocrinol. 293:57-70. https://doi.org/10.1016/j.mce.2008.06.008
  32. Segner H, Caroll K, Fenske M, Janssen CR, Maack G, Pascoe D, Schafers C, Vandenbergh GF, Watts M, Wenzel A. 2003. Identification of endocrine-disrupting effects in aquatic vertebrates and invertebrates: report from the European IDEA project. Ecotoxicol Environ Safe. 54:302-314. https://doi.org/10.1016/S0147-6513(02)00039-8
  33. 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.
  34. Sheahan DA, Brighty GC, Daniel M, Jobling S, Harries JE, Hurst MR, Kennedy J, Kirby SJ, Morris S, Routledge EJ, Sumpter JP, Waldock MJ. 2002. Reduction in the estrogenic activity of a treated sewage effluent discharge to an English river as a result of a decrease in the concentration of industrially-derived surfactants. Environ Toxicol Chem. 21:515-519. https://doi.org/10.1002/etc.5620210307
  35. Trant JM, 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://doi.org/10.1016/0016-6480(88)90259-6
  36. UNEP (United Nations Environmental Programme). 1997. Report of the meeting of experts to review the MEDPOL biomonitoring programme. Athens, Greece, Document UNEP-(OCA)/MED WG. 132/7. UNEP, Athens.
  37. Vaccaro E, Meucci V, Intorre L, Soldani G, Di Bello D, Longo V. 2005. Effects of 17beta-estradiol, 4-nonylphenol and PCB126 on the estrogenic activity and phase 1 and 2 biotransformation enzymes in male sea bass (Dicentrarchus labrax). Aquat Toxicol. 75:293-305. https://doi.org/10.1016/j.aquatox.2005.08.009
  38. Wojtowicz AK, Gregoraszczuk EL, Lyche JL, Ropstad E. 2000. Time dependent and cell-specific action of polychlorinated biphenyls (PCB153 and PCB126) on steroid secretion by porcine theca and granulosa cells in monoand co-culture. J Physiol Pharmacol. 51:555-568.
  39. 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
  40. Young G, Kagawa H, Nagahama Y. 1982. Oocyte maturation in the amago salmon (Oncorhynchus rhodurus): in vitro effects of salmon gonadotropin, steroids, and cyanoketon (an inhibitor of 3b-hydroxy steroid dehydrogenase). J Exp Zool. 224:265-275. https://doi.org/10.1002/jez.1402240217

Cited by

  1. 우리나라 숭어과 어류의 어명 및 자원 활용에 대한 고찰 vol.4, pp.2, 2019, https://doi.org/10.23005/ksmls.2019.4.2.96
  2. In Vitro Sex Steroid Metabolism in Red Spotted Grouper, Epinephelus akaara during Oocyte Maturation vol.25, pp.2, 2021, https://doi.org/10.12717/dr.2021.25.2.75