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Bisphenol A Induces a Distinct Transcriptome Profile in the Male Fish of the Marine Medaka Oryzias javanicus

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Abstract

While environmental concentration of bisphenol A (BPA) is ubiquitously detected in effluent and surface of freshwater, BPA has also been measured in coastal and marine ecosystems. To understand the effect of waterborne BPA on the transcriptome over time, male fish of the marine medaka Oryzias javanicus were exposed to 76 μg/L of BPA for 72 h. Time-course microarray study identified differentially expressed transcripts upon BPA exposure in the liver tissues in a time-dependent manner. The primary effect of BPA treatment appears to be significantly upregulated mRNA expression of lipid metabolism (e.g. fatty acid process, lipid/lipoprotein biosynthesis and transport, cholesterol regulation), while genes involved in diverse biochemical and physiological processes were downregulated. In particular, vertebrate immunity relevant genes showed strong downregulated patterns across time-courses. This study provides preliminary insights into the transcriptional response of marine medaka male fish to waterborne BPA exposure and suggests a basis for uncovering the mode of action particularly with respect to endocrine disrupting chemicals (EDCs) such as BPA.

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References

  1. Staples, C.A. et al. A review of the environmental fate, effects, and exposures of bisphenol A. Chemosphere 36, 2149–2173 (1998).

    Article  CAS  Google Scholar 

  2. Rochester, J.R. Bisphenol A and human health: a review of the literature. Reprod. Toxicol. 42, 132–155 (2013).

    Article  CAS  Google Scholar 

  3. Cousins, I.T., Staples, C.A., Klecka, G.M. & Mackay, D. A multimedia assessment of the environmental fate of bisphenol A. Hum. Ecol. Risk Assess. 8, 1107–1135 (2002).

    Article  Google Scholar 

  4. Oehlmann, J. et al. A critical analysis of the biological impacts of plasticizers on wildlife. Phil. Trans. R. Soc. B 364, 2047–2062 (2009).

    Article  CAS  Google Scholar 

  5. Peng, X. et al. Temporal trends of nonylphenol and bisphenol A contamination in the Pearl River Estuary and the adjacent South China Sea recorded by dated sedimentary cores. Sci. Total. Environ. 384, 393–400 (2007).

    Article  CAS  Google Scholar 

  6. David, A., Fenet, H. & Gomez, E. Alkylphenols in marine environments: distribution monitoring strategies and detection considerations. Mar. Pollut. Bull. 58, 953–960 (2009).

    Article  CAS  Google Scholar 

  7. Söffker, M. & Tyler, C.R. Endocrine disrupting chemicals and sexual behaviors in fish-a critical review on effects and possible consequences. Crit. Rev. Toxicol. 42, 653–668 (2012).

    Article  Google Scholar 

  8. Staples, C.A. et al. A weight of evidence approach to the aquatic hazard assessment of bisphenol A. Hum. Ecol. Risk Assess. 8, 1083–1105 (2002).

    Article  Google Scholar 

  9. Crane, M. et al. Review of aquatic in situ approaches for stressor and effect diagnosis. Integr. Environ. Assess. Manag. 3, 234–245 (2007).

    Article  Google Scholar 

  10. Kang, J.-H., Aasi, D. & Katayama, Y. Bisphenol A in the aquatic environment and its endocrine-disruptive effects on aquatic organisms. Crit. Rev. Toxicol. 37, 607–625 (2007).

    Article  CAS  Google Scholar 

  11. Bhandari, R.K. et al. Effects of the environmental estrogenic contaminants bisphenol A and 17a-ethinyl estradiol on sexual development and adult behaviors in aquatic wildlife species. Gen. Comp. Endocrinol. 214, 195–219 (2015).

    Article  CAS  Google Scholar 

  12. Hu, J. & Liu, J. 3D models of bisphenol A and its metabolite 4-methyl-2,4-bis (4-hydroxyphenyl)-pent-1-ene (MBP) antagonist binding to human progesterone receptor. Mol. Cell. Toxicol. 11, 145–152 (2015).

    Article  CAS  Google Scholar 

  13. Iwamatsu, T. The Integrated Book for the Biology of the Medaka. Japan: Daigaku Kyouiku Publishing (1998).

    Google Scholar 

  14. Bo, J. et al. The marine medaka Oryzias melastigma -a potential marine fish model for innate immune study. Mar. Pollut. Bull. 63, 267–276 (2011).

    Article  CAS  Google Scholar 

  15. Kim, B.-M. et al. Omics of the marine medaka (Oryzias melastigma) and its relevance to marine environmental research. Mar. Environ. Res. 113, 141–152 (2016).

    Article  CAS  Google Scholar 

  16. Inoue, K. & Takei, Y. Diverse adaptability in Oryzias species to high environmental salinity. Zool. Sci. 19, 727–734 (2002).

    Article  Google Scholar 

  17. Woo, S., Denis, V. & Yum, S. Transcriptional changes caused by bisphenol A in Oryzias javanicus, a fish species highly adaptable to environmental salinity. Mar. Drugs. 12, 983–998 (2014).

    Article  CAS  Google Scholar 

  18. Kashiwada, S. et al. Fish test for endocrine-disruption and estimation of water quality of Japanese rivers. Water Res. 36, 2161–2166 (2002).

    Article  CAS  Google Scholar 

  19. Rhee, Y.-J. & Rhee, J.-S. Bisphenol A causes mortality and reduced hatching success through increase of cell damage and dysfunction of antioxidant defense system in marine medaka embryo. Toxicol. Environ. Health. Sci. 8, 290–295 (2016).

    Article  Google Scholar 

  20. Brusle, J. & Anadon, G.G.I. The structure and function of fish liver, Fish Morphology: Horizon of New Research. Science Publisher Inc., New Hampshire (1996).

    Google Scholar 

  21. Marmugi, A. et al. Low doses of bisphenol A induce gene expression related to lipid synthesis and trigger triglyceride accumulation in adult mouse liver. Hepatology 55, 395–407 (2012).

    Article  CAS  Google Scholar 

  22. Masuno, H. et al. Bisphenol A accelerates terminal differentiation of 3T3-L1 cells into adipocytes through the phosphatidylinositol 3-kinase pathway. Toxicol. Sci. 84, 319–327 (2005).

    Article  CAS  Google Scholar 

  23. Phrakonkham, P. et al. Dietary xenoestrogens differentially impair 3T3-L1 preadipocyte differentiation and persistently affect leptin synthesis. J. Steroid Biochem. Mol. Biol. 110, 95–103 (2008).

    Article  CAS  Google Scholar 

  24. Somm, E. et al. Perinatal exposure to bisphenol A alters early adipogenesis in the rat. Environ. Health Perspect. 117, 1549–1555 (2009).

    Article  CAS  Google Scholar 

  25. Miyawaki, J. et al. Perinatal and postnatal exposure to bisphenol A increases adipose tissue mass and serum cholesterol level in mice. J. Atheroscler. Thromb. 14, 245–252 (2007).

    Article  CAS  Google Scholar 

  26. Sargis, R.M., Johnson, D.N., Choudhury, R.A. & Brady, M.J. Environmental endocrine disruptors promote adipogenesis in the 3T3-L1 cell line through glucocorticoid receptor activation. Obesity 18, 1283–1288 (2010).

    Article  CAS  Google Scholar 

  27. Riu, A. et al. Halogenated bisphenol-A analogs act as obesogens in zebrafish larvae (Danio rerio). Toxicol. Sci. 139, 48–58 (2014).

    Article  CAS  Google Scholar 

  28. Dimastrogiovanni, G. et al. Alteration of cellular lipids and lipid metabolism markers in RTL-W1 cells exposed to model endocrine disrupters. Aquat. Toxicol. 165, 277–285 (2015).

    Article  CAS  Google Scholar 

  29. Guan, Y. et al. Effects of bisphenol A on lipid metabolism in rare minnow Gobiocypris rarus. Comp. Biochem. Physiol. C 179, 144–149 (2016).

    CAS  Google Scholar 

  30. Dominiczak, M.H. & Caslake, M.J. Apolipoproteins: metabolic role and clinical biochemistry applications. Ann. Clin. Biochem. 48, 498–515 (2011).

    Article  CAS  Google Scholar 

  31. Carnevali, O. et al. Dietary administration of EDC mixtures: A focus on fish lipid metabolism. Aquat. Toxicol. 185, 95–104 (2017).

    Article  CAS  Google Scholar 

  32. Olivares-Rubio, H.F. & Vega-López, A. Fatty acid metabolism in fish species as a biomarker for environmental monitoring. Environ. Pollut. 218, 297–312 (2016).

    Article  CAS  Google Scholar 

  33. Milla, S., Depiereux, S. & Kestemont, P. The effects of estrogenic and androgenic endocrine disruptors on the immune system of fish: a review. Ecotoxicology 20, 305–319 (2011).

    Article  CAS  Google Scholar 

  34. Rogers, J.A., Metz, L. & Yong, V.W. Review: Endocrine disrupting chemicals and immune responses: a focus on bisphenol-A and its potential mechanisms. Mol. Immunol. 53, 421–430 (2013).

    Article  CAS  Google Scholar 

  35. Racanelli, V. & Rehermann, B. The liver as an immunological organ. Hepatology 43, 54–62 (2006).

    Article  Google Scholar 

  36. Qiu, W. et al. The potential immune modulatory effect of chronic bisphenol A exposure on gene regulation in male medaka (Oryzias latipes) liver. Ecotoxicol. Environ. Saf. 130, 146–154 (2016).

    Article  CAS  Google Scholar 

  37. Sumpter, J.P. & Jobling, S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health. Perspect. 103, 173–178 (1995).

    Article  CAS  Google Scholar 

  38. Sonnenschein, C. & Soto, A.M. An updated review of environmental estrogen and androgen mimics and antagonists. J. Steroid Biochem. Mol. Biol. 65, 143–150 (1998).

    Article  CAS  Google Scholar 

  39. Rhee, J.-S. et al. Endocrine disruptors modulate expression of hepatic choriogenin genes in the hermaphroditic fish, Kryptolebias marmoratus. Comp. Biochem. Physiol. C 150, 170–178 (2009).

    Google Scholar 

  40. Kang, I.J. et al. Effects of bisphenol A on the reproduction of Japanese medaka (Oryzias latipes). Environ. Toxicol. Chem. 21, 2394–2400 (2002).

    Article  CAS  Google Scholar 

  41. Hayashi, H., Nishimoto, A., Oshima, N. & Iwamuro, S. Expression of the estrogen receptor alpha gene in the anal fin of Japanese medaka, Oryzias latipes, by environmental concentrations of bisphenol A. J. Toxicol. Sci. 32, 91–96 (2007).

    Article  CAS  Google Scholar 

  42. Sun, L. et al. Toxic effects of bisphenol A on early life stages of Japanese medaka (Oryzias latipes). Bull. Environ. Contam. Toxicol. 93, 222–227 (2014).

    Article  CAS  Google Scholar 

  43. Yamaguchi, A., Ishibashi, H., Arizono, K. & Tominaga, N. In vivo and in silico analyses of estrogenic potential of bisphenol analogs in medaka (Oryzias latipes) and common carp (Cyprinus carpio). Ecotoxicol. Environ. Saf. 120, 198–205 (2015).

    Article  CAS  Google Scholar 

  44. Li, D. et al. The chronic effects of lignin-derived bisphenol and bisphenol A in Japanese medaka Oryzias latipes. Aquat. Toxicol. 170, 199–207 (2016).

    Article  CAS  Google Scholar 

  45. Lee, C., Na, J.G., Lee, K.C. & Park, K. Choriogenin mRNA induction in male medaka, Oryzias latipes as a biomarker of endocrine disruption. Aquat. Toxicol. 61, 233–241 (2002).

    Article  CAS  Google Scholar 

  46. Chen, X., Li, V.W., Yu, R.M. & Cheng, S.H. Choriogenin mRNA as a sensitive molecular biomarker for estrogenic chemicals in developing brackish medaka (Oryzias melastigma). Ecotoxicol. Environ. Saf. 71, 200–208 (2008).

    Article  Google Scholar 

  47. Yum, S., Jo, Y.J. & Woo, S. Metabolic changes in marine medaka fish (Oryzias javanicus) in response to acute 4-nonlyphenol toxicity. BioChip J. 9, 322–331 (2015).

    Article  CAS  Google Scholar 

  48. Kim, Y.-J. et al. Transcriptomic change as evidence for cadmium-induced endocrine disruption in marine fish model of medaka, Oryzias javanicus. Mol. Cell. Toxicol. 12, 409–420 (2016).

    Article  CAS  Google Scholar 

  49. Huang da, W., Sherman, B.T. & Lempicki, R.A. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44–57 (2009).

    Article  CAS  Google Scholar 

  50. Conesa, A. et al. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674–3676 (2005).

    Article  CAS  Google Scholar 

  51. Livak, K.J. & Schmittgen, T.D. Analysis of relative gene expression data using real time quantitative PCR and the 2-??Ct method. Methods 25, 402–408 (2001).

    Article  CAS  Google Scholar 

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Correspondence to Jae-Sung Rhee or Seungshic Yum.

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Kim, BM., Jo, Y.J., Lee, N. et al. Bisphenol A Induces a Distinct Transcriptome Profile in the Male Fish of the Marine Medaka Oryzias javanicus. BioChip J 12, 25–37 (2018). https://doi.org/10.1007/s13206-017-2104-0

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  • DOI: https://doi.org/10.1007/s13206-017-2104-0

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