Abstract
The differentially expressed genes in the liver tissue of the marine medaka fish, Oryzias javanicus, were profiled using an oligo-microarray (EnviHaz Fish Array ver. 01) after the fish were exposed to 20 µg/L 4-nonylphenol (4-NP) for 12, 24, 48, or 72 h to determine the metabolic and physiological changes with exposure time. The transcriptomic changes were highly dynamic in the 4-NP-exposed fish in that among the 216 differentially expressed genes identified in all four exposed fish groups, 106 genes (49.1%) appeared after a specific exposure time. The differentially expressed genes were used to predict the changes that occurred in the metabolic pathways and processes in response to 4-NP exposure. Many physiological and metabolic changes were detected in the early phase of exposure. Significant vitellogenin expression and an estrogenic stimulus response were observed in the fish exposed to 4-NP for 48 h. These results extend our understanding of the biological responses to environmental chemicals at the molecular level and will allow the toxic effects of environmental chemicals, especially endocrine-disrupting chemicals, to be evaluated.
Similar content being viewed by others
References
Jobling, S. et al. in State of the science of endocrine disrupting chemicals 2012 (eds. Berggren, Å., Heindel, J.J., Jobling, S., Kidd, K.A. & Zoeller, R.T.) 260 pp. (United Nations Environmental Programme and the World Health Organization, 2013).
Zhang, L. et al. Effect of bisphenol A exposure during early development on glucose metabolism and adipokine expression in adolescent female rats. Mol. Cell. Toxicol. 9, 385–391 (2013).
Lee, H.A. et al. Longitudinal changes in offspring body weight, fat mass and sex hormone levels according to maternal bisphenol A exposure during gestation and lactation. Mol. Cell. Toxicol. 9, 285–293 (2013).
Sager, D.B., Shih-Schroeder, W. & Girard, D. Effect of early postnatal exposure to polychlorinated biphenyls (PCBs) on fertility in male rats. Bull. Environ. Contam. Toxicol. 38, 946–953 (1987).
Jensen, A.A. & Leffers, H. Emerging endocrine disrupters: perfluoroalkylated substances. Int. J. Androl. 31, 161–169 (2008).
Schreiber, T. et al. Polybrominated diphenyl ethers induce developmental neurotoxicity in a human in vitro model: evidence for endocrine disruption. Environ. Health. Perspect. 118, 572–578 (2010).
Santodonato, J. Review of the estrogenic and antiestrogenic activity of polycyclic aromatic hydrocarbons: relationship to carcinogenicity. Chemosphere 34, 835–848 (1997).
Raut, S.A. & Angus, R.A. Triclosan has endocrine-disrupting effects in male western Mosquitofish, Gambusia Affinis. Environ. Toxicol. Chem. 29, 1287–1291 (2010).
Rubin, B.S. Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J. Steroid Biochem. Mol. Biol. 127, 27–34 (2011).
Jeong, S.W. et al. Genomic expression responses toward bisphenol-A toxicity in Daphnia magna in terms of reproductive activity. Mol. Cell. Toxicol. 9, 149–158 (2013).
McCormick, S.D. et al. Endocrine disruption of parrsmolt transformation and seawater tolerance of Atlantic salmon by 4-nonylphenol and 17beta-estradiol. Gen. Comp. Endocrinol. 142, 280–288 (2005).
Lagadic, L., Coutellec, M.A. & Caquet, T. Endocrine disruption in aquatic pulmonate molluscs: few evidences, many challenges. Ecotoxicology 16, 45–59 (2007).
Leung, K.M.Y., Wheeler, J.R., Morritt, D. & Crane, M. Endocrine Disruption in Fishes and Invertebrates: Issues for Saltwater Ecological Risk Assessment. In: Coastal and Esturarine Risk Assessment (eds. Newman, M.C., Roberts, M.H.J. & Hale, R.C.) 189–215 (CRC Press, New York, 2001).
Mills, L.J. & Chichester, C. Review of evidence: are endocrine-disrupting chemicals in the aquatic environment impacting fish populations? Sci. Total. Environ. 343, 1–34 (2005).
Inoue, K. & Takei, Y. Diverse adaptability in Oryzias species to high environmental salinity. Zoolog. Sci. 19, 727–734 (2002).
Inoue, K. & Takei, Y. Asian medaka fishes offer new models for studying mechanisms of seawater adaptation. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 136, 635–645 (2003).
Ekelund, R., Bergman, A., Granmo, A. & Berggren, M. Bioaccumulation of 4-nonylphenol in marine animals—a re-evaluation. Environ. Pollut. 64, 107–120 (1990).
Spehar, R.L., Brooke, L.T., Markee, T.P. & Kahl, M.D. Comparative toxicity and bioconcentration of nonylphenol in freshwater organisms. Environ. Toxicol. Chem. 29, 2104–2111 (2010).
Vetillard, A. & Bailhache, T. Effects of 4-n-nonylphenol and tamoxifen on salmon gonadotropin-releasing hormone, estrogen receptor, and vitellogenin gene expression in juvenile rainbow trout. Toxicol. Sci. 92, 537–544 (2006).
Xie, L. et al. Evaluation of estrogenic activities of aquatic herbicides and surfactants using an rainbow trout vitellogenin assay. Toxicol. Sci. 87, 391–398 (2005).
Huang da, W., Sherman, B.T. & Lempicki, R.A. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1–13 (2009).
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).
Cho, H.-H., Song, M. & Ryu, J.C. Gene expression profile of endometrial carcinoma cells exposed to di-(2-ethylhexyl) phthalate. Mol. Cell. Toxicol. 9, 113–120 (2013).
Guenther, K. et al. Endocrine disrupting nonylphenols are ubiquitous in food. Environ. Sci. Technol. 36, 1676–1680 (2002).
Lussier, S.M. et al. Acute toxicity of para-nonylphenol to saltwater animals. Environ. Toxicol. Chem. 19, 617–621 (2000).
Lee, A. et al. Changes in gene expression profile due to acute toxicity of toxaphene in the marine medaka. Mol. Cell. Toxicol. 9, 121–128 (2013).
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).
Won, H., Woo, S. & Yum, S. Acute 4-nonylphenol toxicity changes the genomic expression profile of marine medaka fish, Oryzias javanicus. Mol. Cell. Toxicol. 10, 181–195 (2014).
Yoshimura, K. Biodegradation and fish toxicity of nonionic surfactants. J. Am. Oil. Chem. Soc. 63, 1590–1596 (1986).
Woo, S. et al. Effects of heavy metals on antioxidants and stress-responsive gene expression in Javanese medaka (Oryzias javanicus). Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 289–299 (2009).
Woo, S., Yum, S., Kim, D.W. & Park, H.S. Transcripts level responses in a marine medaka (Oryzias javanicus) exposed to organophosphorus pesticide. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 149, 427–432 (2009).
Dong, Y. et al. Bisphenol A impairs mitochondrial function in spleens of mice via oxidative stress. Mol. Cell. Toxicol. 9, 401–406 (2013).
Mahley, R.W. & Rall, S.C., Jr. Apolipoprotein E: far more than a lipid transport protein. Annu. Rev. Genomics Hum. Genet. 1, 507–537 (2000).
Stan, S. et al. Apo A-IV: an update on regulation and physiologic functions. Biochim. Biophys. Acta. 1631, 177–187 (2003).
Spicer, L.J. & Aad, P.Y. Insulin-like growth factor (IGF) 2 stimulates steroidogenesis and mitosis of bovine granulosa cells through the IGF1 receptor: role of follicle-stimulating hormone and IGF2 receptor. Biol. Reprod. 77, 18–27 (2007).
Pepys, M.B. & Hirschfield, G.M. C-reactive protein: a critical update. J. Clin. Invest. 111, 1805–1812 (2003).
Kishore, U. et al. Structural and functional anatomy of the globular domain of complement protein C1q. Immunol. Lett. 95, 113–128 (2004).
Gulick, T. et al. The peroxisome proliferator-activated receptor regulates mitochondrial fatty acid oxidative enzyme gene expression. Proc. Natl. Acad. Sci. U S A 91, 11012–11016 (1994).
Evans, R.M., Barish, G.D. & Wang, Y.X. PPARs and the complex journey to obesity. Nat. Med. 10, 355–361 (2004).
Hendershot, L.M. et al. Localization of the gene encoding human BiP/GRP78, the endoplasmic reticulum cognate of the HSP70 family, to chromosome 9q34. Genomics 20, 281–284 (1994).
Patel, Y.C. Somatostatin and its receptor family. Front. Neuroendocrinol. 20, 157–198 (1999).
Sumpter, J.P. & Jobling, S. Vitellogenesis as a biomarker for estrogenic contamination of the aquatic environment. Environ. Health Perspect. 103(Suppl 7), 173–178 (1995).
Delanghe, J.R. & Langlois, M.R. Hemopexin: a review of biological aspects and the role in laboratory medicine. Clin. Chim. Acta. 312, 13–23 (2001).
Kashiwada, S. et al. Fish test for endocrine-disruption and estimation of water quality of Japanese rivers. Water Res. 36, 2161–2166 (2002).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
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). https://doi.org/10.1007/s13206-015-9408-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13206-015-9408-8