Animal cells and systems

The Korean Society for Integrative Biology (한국통합생물학회)
권호 표지

Induction of In Vitro Vitellogenin Synthesis by Bisphenol, Nonylphenol and Octylphenol in Chinese Minnow(Phoxinus oxycephalus) Hepatocytes

  • Park, Chang-Beom (Marine and Environmental Research Institute, Cheju National University) ;
  • Kim, Byung-Ho (Marine and Environmental Research Institute, Cheju National University) ;
  • Na, Oh-Soo (Marine and Environmental Research Institute, Cheju National University) ;
  • Choi, Young-Chan (Marine and Environmental Research Institute, Cheju National University) ;
  • Lee, Young-Don (Marine and Environmental Research Institute, Cheju National University) ;
  • Baek, Hae-Ja (Conbined Department of Fisheries Marine Life Science, Pukyong National University) ;
  • Kim, Hyung-Bae (Department of Marine Biotechnology, Kangwon Provincial University) ;
  • Akihiro Takemura (Sesoko Station, Tropical Biosphere Research Center, University of the Ryukyus)
  • Published : 2003.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Bisphenol A (BPA), nonylphenol (NP), and 4-tert-octylphenol (OP) are known endocrine disrupting chemicals (EDCs) with estrogenic activity in fish. This study compared the effects of BPA, NP and OP on in vitro vitellogenin (VTG) synthesis in primary cultures of hepatocytes of the Chinese minnow Phoxinus oxycephalus. The VTG secreted into the culture medium was measured using enzyme-linked immunosorbent assay (ELISA), which we developed in this study using an antibody prepared from homogenates of Chinese minnow egg. VTG synthesis was induced by estradiol-17$\beta$ ($E_2$) and phenols (BPA, NP and OP) treatment. $E_2$ at concentrations of 10$^{-6}$ M or higher increased VTG levels significantly (P < 0.05). Exposure to 10^5\;M\;BPA\;or\;10^-4$M NP and OPinduced in vitro VTG synthesis (P < 0.01). However, $10^-3$ M BPA, NP or OP did not induce VTG synthesis. These results suggest that SPA has the highest estrogenic potential in Chinese minnow hepatocytes. Tamoxifen, an anti-estrogen, drastically blocked the production of VTG by phenols (BPA, NP and OP) suggesting that phenols (BPA, NP and OP) may act via binding to estrogen receptor (ER) in Chinese minnow hepatocytes.

Keywords

References

  1. Arukwe A, Knudsen FR, and Goksoyr A (1997) Fish zona radiata (eggshell) protein: a sensitive biomarker for environmental estrogens. Environ Health Perspect 105: 418-422 https://doi.org/10.2307/3433339
  2. Ashby J (2000) Validation of in vitro and in vivo methods for assessing endocrine disrupting chemicals. Toxicol Pathol 28: 432-437 https://doi.org/10.1177/019262330002800312
  3. Bond CE (1979) Biology of Fishes. W.B. Saunders Company, Philadelphia
  4. Cao YA, Blair JB, and Ostrander GK (1996) The initial report of the establishment of primary liver cell cultures from medaka (Oryzias latipes). Fish Biol J Medaka 8: 47-56
  5. Celius T, Haugen TB, Grotmol T, and Walther BT (1999) A sensitive zonagenetic assay for rapid in vitro assessment of estrogenic potency of xenobiotics and mycotoxins. Environ Health Perspect 107: 63-68 https://doi.org/10.2307/3434290
  6. Christiansen T, Korsgaard B, and Jespersen A (1998) Effects of nonylphenol and 17${\beta}$-oestradiol on vitellogenin synthesis, testicular structure and cytology in male eelpout Zoarces viviparus. J Exp Biol 201: 172-192
  7. Colborn T (1995) Environmental estrogens: health implications for humans and wildlife. Environ Health Perspect 103: 135-136 https://doi.org/10.2307/3432522
  8. Colborn T and Clement C (1992) Chemically-induced Alterations in Sexual and Functional Development. The Wildlife/Human Connection. Princeton Scientific Publications, Princeton
  9. Flouriot G, Pakdel F, and Valotaire Y (1995) Influence of xenobiotics on rainbow trout liver estrogen receptor and vitellogenin gene expression. J Mol Endocrinol 15: 143-151 https://doi.org/10.1677/jme.0.0150143
  10. Gray MA and Metcalfe CD (1997) Induction of testis-ova in Japanese medaka (Oryzias latipes) exposed to p-nonylpheol. Environ Toxicol Chemm 16: 1082-1086 https://doi.org/10.1897/1551-5028(1997)016<1082:IOTOIJ>2.3.CO;2
  11. Gray JLE, Ostby J, Wolf C, Lambright C, and Kelce W (1998) The value of mechanistic studies in laboratory animals for the prediction of reproductive effects in wildlife: endocrine effects on mammalian sexual differentiation. Environ Toxicol Soc 17: 109-118 https://doi.org/10.1897/1551-5028(1998)017<0109:TVOMSI>2.3.CO;2
  12. Hara A, Matsubara T, Saneyoshi M, and Takano K (1984) Vitellogenin and its derivatives in egg yolk proteins of white-spotted charr (Salvelinus leucomaenis). Bull Fac Fish Hokkaido Univ 35: 144-153
  13. Harries JE, Sheahan DA, Jolbing S, Mattthiessen P, Neall P, Routledge EJ, Rycroft R, Sumpter JP, and Tylor T (1996) A survey of estrogenic activity in United Kinngdim inland waters. Environ Toxicol Chem 15: 1993-2002 https://doi.org/10.1897/1551-5028(1996)015<1993:ASOEAI>2.3.CO;2
  14. Harries JE, Sheahan DA, Jolbing S, Mattthiessen P, Neall P, Sumpter JP, Tylor T, and Zaman N (1997) Estrogenic activity in five United Kingdom rivers detected by measurement of vitellogenesis in caged male trout. Environ Toxicol Chem 16: 534-542 https://doi.org/10.1897/1551-5028(1997)016<0534:EAIFUK>2.3.CO;2
  15. Islinger M, Pawlowski S, Hollert H, Volkl A, and Braunbeck T (1999) Measurement of vitellogenin-mRNA expression in primary cultures of rainbow trout hepatocytes in a mom-radioactive dot blot/RNAase protection-assay. Sci Total Environ 233: 109-122 https://doi.org/10.1016/S0048-9697(99)00218-1
  16. Jobling S, Sheahan D, Osborne JA, Methiessen P, and Sumpter JP (1996) Inhibition of testicular growth in rainbow trout (Oncorhynchus mykiss) exposed to estrogenic alkylphenolic chemicals. Environ Toxicol Chem 15: 194-202 https://doi.org/10.1897/1551-5028(1996)015<0194:IOTGIR>2.3.CO;2
  17. Jobling S and Sumpter JP (1993) Detergent components in sewage effluent are weakly oestrogenic to fish: an in vitro study using rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat Toxicol 27: 361-372 https://doi.org/10.1016/0166-445X(93)90064-8
  18. Jobling S, Nolan M, Tyler CR, Brighty G, and Sumpter JP (1998) Widespread sexual distruption in wild fish. Environ Sci Technol 32: 2498-2506 https://doi.org/10.1021/es9710870
  19. Johnsen HK, Tveiten H, Willassen NP, and Arnesen AM (1999) Arctic charr (Salvelinus alpinus) vitellogenin: development and validation of an enzyme-linked immunosorbent assay. Comp Biochem Physiol 124A: 355-362 https://doi.org/10.1016/S0305-0491(99)00132-7
  20. Kim BH, Takemura A, and Nakamura M (2002) Comparison of in vitro vitellogenin synthesis among different nonylphenol products using primary cultures of tilapia hepatocytes. Fish Sci 68: 838-842 https://doi.org/10.1046/j.1444-2906.2002.00500.x
  21. Kinnberg K, Korsgaard B, Bjerregaard P, and Jespersen A (2000) Effects of nonylphenol and $17{\beta}-estradiol$ on vitellogenin synthesis and testis morphology in male platyfish Xiphophorus maculatus. J Exp Biol 203: 171-181
  22. Korsgaard B and Pedersen KL (1998) Vitellogenin in Zoarces viviparus: purification, quantification and induction by estradiol-17${\beta}$ and 4-nonylphenol. Comp Biochem Physiol 120A: 159-166
  23. Kristine H, Pedersen SN, Pedersen KL, Korsgarrd B, and Bjerregarrd P (2003) Estrogenic effect of dietary 4-tert-octylphenol in rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 62: 295-303 https://doi.org/10.1016/S0166-445X(02)00107-8
  24. Kwon HC and Mugiya Y (1994) Involvement of growth hormone and prolactin in the induction of vitellogenin synthesis in primary hepatocyte culture in the eel, Anguilla japonica. Gen Comp Endocrinol 93: 51 -60 https://doi.org/10.1006/gcen.1994.1007
  25. Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685 https://doi.org/10.1038/227680a0
  26. Lazier CB, Langley S, Ramsey NB, and Wright JM (1996) Androgen inhibition of vitellogenin gene expression in tilapia (Oreochromis niloticus). Gen Comp Endcrinol 104: 321-329 https://doi.org/10.1006/gcen.1996.0177
  27. Lye CM, Frid CLJ, Gill ME, and McComick D (1997) Abnormalites in the reproductive health of flounder Platichthys flesus exposed to effluent from a sewage treatment works. Mar Pollut Bull 34: 34-41 https://doi.org/10.1016/S0025-326X(96)00061-6
  28. Maitre J, Valotaire Y, and Guguen-Guillouzo C (1986) Estradiol-17${\beta}$ stimulation of vitellogenin synthesis in primary culture of male rainbow trout hepatocytes. In Vitro Cell Dev Biol 22: 337-343 https://doi.org/10.1007/BF02623408
  29. Matthiessen P and Sumpter JP (1998) Effects of estrogenic substances in the aquatic environment. In: Braunbeck T, Streit B, and Hinton DE (eds), Fish Ecotoxicology, Birkhauser, Basel, pp 319-336
  30. Mommsen TP and Walsh PJ (1988) Vitellogenesis and oocyte assembly. In: Hoar WS and Randall DJ (eds), Fish Physiology, Academic Press, New York, pp 347-406
  31. Monteverdi GH and Di Giulio RT (1999) An enzyme-linked immunosorbent assay for estrogenicity using primary hepatocytes cultures from the channel catfish (Octalurus punctatus). Arch Environ Contam Toxicol 37: 355-375 https://doi.org/10.1007/s002449900490
  32. Mori T, Matsumoto H, and Yokota H (1998) Androgen induced vitellogenin gene expression in primary cultures of rainbow trout hepatocytes. J Steroid Biochem Mol Biol 67: 133-141 https://doi.org/10.1016/S0960-0760(98)00099-5
  33. Nishi K, Chikae M, Hatano Y, Mizukami H, Yamashita M, Sakakibara R, and Tamiya E (2002) Development and application of a monoclonal antibody-based sandwich ELISA for quantification of Japanese medaka (Oryzias latipes) vitellogenin. Comp Biochem Physiol 132A: 161-169 https://doi.org/10.1016/S1532-0456(02)00058-3
  34. Ouchterlony O (1953) Antigen-antibody reaction in gels. IV. Types of reactions in coordinated systems of diffusion. Acta Pathol Microbiol Scand 32: 231-240 https://doi.org/10.1111/j.1699-0463.1953.tb00247.x
  35. Peyon P, Baloche S, and Berzawa-Gerard E (1997) Investigation into the possible role of androgens in the induction of hepatic vitellogenesis in the European eel: in vivo and in vitro studies. Fish Physiol Biochem 16: 107-118 https://doi.org/10.1007/BF00004668
  36. Peyon P, Calvayrac R, Baloche S, and Berzawa-Gerard E (1998) Metabolic studies on eel (Anguilla anguilla L.) hepatocytes in primary culture: effect of 17${\beta}$-estradiol and growth hormone. Comp Biochem Physiol 121 A: 35-44
  37. Roubal WT, Lomax DP, Willisn ML, and Johnson L (1997) Purification and pautial characterization of English sole (Pleuronectes vetulus) vitellogenin. Comp Biochem Physiol 118B: 613-622
  38. Segner H, Navas JM, Schafers C, and Wenzel A (2003) Potencies of estrogenic compounds in in vitro screening assays and in life cycle tests with zebrafish in vivo. Ecotoxicol Environ Safety 54: 315-322 https://doi.org/10.1016/S0147-6513(02)00040-4
  39. Smeets JMW, Rankouhi TR, Nichols KM, Komen H, Kaminski NE, Giesy JP, and Van den Berg M (1999) in vitro vitellogeninn production by carp (Cyprinus caprio) hepatocytes as a screening method for determinig (anti)estrogen activity of xenobiotics. Toxicol Appl Phamacol 157: 68-76 https://doi.org/10.1006/taap.1999.8663
  40. Specker JL and Sullivan G (1994) Vitellogenin in fish: status and perspectives. In: Davey KG, Peter RE, and Tobe SS (eds), National Research Council of Canada, Ottawa, pp 304-315
  41. Sumpter JP and Jobling S (1995) Vitellogenesis as a biomarker for estrogenic contamination of aquatic environment. Environ Health Perspect 107: 173-178 https://doi.org/10.2307/3432529
  42. Sumpter JP and Tyler CR (1996) Estrogenic substances in the aquatic environment and their potential impact in animals, particularly fish. Soc Exp Biol Sem Ser pp 57
  43. Takemura A, Hara A, and Takano K (1991) Immunochemical identification and partial characterization of female-specific serum proteins in white-edged rockfish, Sebastes taczanowskii. Envion Biol Fish 30: 49-56 https://doi.org/10.1007/BF02296876
  44. Takemura A and Kim BH (2001) Effects of estradiol-17{\beta}$ treatment on in vitro and in vivo synthesis of two distinct vitellogenin in tilapia. Comp Biochem Physiol 129A: 641-651
  45. Takemura A and Teruya K (1997) Purification and partial characterization of the vitellogenin of coral trout, Plectropomus leopardus. Bull Mar Sci 61: 791-800
  46. Tyler CR, Jobling S, and Sumpter JP (1998) Endocrine disruption in wildlife: a critical review of evidence. Crit Rev Toxicol 28: 319-361 https://doi.org/10.1080/10408449891344236
  47. Wallace RA (1985) Vitellogenin and oocyte growth in non-mammalian vertebrates. In: Browder L (ed), Developmental Biology. Plenum, New York, pp 127-177
  48. Wallace RA and Selman K (1981) Cellular and dynamics aspects of oocytes growth in teleosts. Am Zool 21: 325-343 https://doi.org/10.1093/icb/21.2.325
  49. White R, Jobling S, Hoare SA, Sumpter JP, and Parker MG (1994) Environmentally persistent alkylphenolic compounds are estrogenic. Endocrinology 135: 175-182 https://doi.org/10.1210/en.135.1.175
  50. Zacharewski T (1997) In vitro bioassays for assessing estrogenic substances. Environ Sci Technol 31: 613-623 https://doi.org/10.1021/es960530o