Skip to main content
Log in

An evaluation of the combined effects of phenolic endocrine disruptors on vitellogenin induction in goldfish Carassius auratus

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Phenolic compounds are widely distributed in the natural environment, typically existing as a mixture at the nanogram or microgram per liter level. Among the phenolic compounds, 4-nonylphenol, 4-t-octylphenol, bisphenol A and 2,4-dichlorophenol attract the most concern due to their abundance and risks within the natural environment. The former three chemicals are known as endocrine disruptors causing feminization in various organisms, whereas the latter one requires further clarification concerning its feminization effect. This study aims to evaluate the combined effects of these chemicals using vitellogenin protein induction in male juvenile goldfish Carassius auratus as an endpoint after 15 days of exposure. The results showed that all these chemicals can induce vitellogenin with a relative potency of 4-t-octylphenol > bisphenol A > 4-nonylphenol ≫ 2,4-dichlorophenol. 2,4-dichlorophenol showed a very weak estrogenic effect with an induction of vitellogenin concentration of <1 % of positive control, and it is therefore omitted in further tests to evaluate their combined effect. The other three chemicals were mixed in two ways, at an equipotent ratio and at an equal environmental level ratio, and their combined effects were evaluated with both the toxicity units method and concentration addition model. The resulting effect of exposure to both mixtures showed that these chemicals generally exhibited an additive effect. The ecological risk of phenolic chemicals may therefore be underestimated if based on the presence of single chemicals whereas their combined effects warrant further consideration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Explore related subjects

Discover the latest articles and news from researchers in related subjects, suggested using machine learning.

References

  • Blackburn MA, Waldock MJ (1995) Concentrations of alkylphenols in rivers and estuaries in England and Wales. Water Res 29:1623–1629

    Article  CAS  Google Scholar 

  • Blair RM, Fang H, Branham WS et al (2000) The estrogen receptor relative binding affinities of 188 natural and xenochemicals: structural diversity of ligands. Toxicol Sci 54:138–153

    Article  CAS  Google Scholar 

  • Borgert CJ, Mihaich EM, Quill TF et al (2011) Evaluation of EPA’s tier 1 endocrine screening battery and recommendations for improving the interpretation of screening results. Regul Toxicol Pharmacol 59:397–411

    Article  CAS  Google Scholar 

  • Cionna C, Maradonna F, Olivotto I et al (2006) Effects of nonylphenol on juveniles and adults in the grey mullet, Liza aurata. Reprod Toxicol 22:449–454

    Article  CAS  Google Scholar 

  • Connolly L, Ropstad E, Verhaegen S (2011) In vitro bioassays for the study of endocrine-disrupting food additives and contaminants. Trend Anal Chem 30:227–238

    Article  CAS  Google Scholar 

  • Duan Z, Zhu L, Zhu L et al (2008) Individual and joint toxic effects of pentachlorophenol and bisphenol A on the development of zebrafish (Danio rerio) embryo. Ecotox Environ Safe 71:774–780

    Article  CAS  Google Scholar 

  • Fent K, Escher C, Caminada D (2006) Estrogenic activity of pharmaceuticals and pharmaceutical mixtures in a yeast reporter gene system. Reprod Toxicol 22:175–185

    Article  CAS  Google Scholar 

  • Fu M, Li Z, Gao H (2007) Distribution characteristics of nonylphenol in Jiaozhou Bay of Qingdao and its adjacent rivers. Chemosphere 69:1009–1016

    Article  CAS  Google Scholar 

  • Giesy JP, Hilscherova K, Jones PD et al (2002) Cell bioassays for detection of aryl hydrocarbon (AhR) and estrogen receptor (ER) mediated activity in environmental samples. Mar Pollut Bull 45:3–16

    Article  CAS  Google Scholar 

  • Gültekin I, Ince NH (2007) Synthetic endocrine disruptors in the environment and water remediation by advanced oxidation processes. J Environ Manage 85:816–832

    Article  Google Scholar 

  • Gutendorf B, Westendorf J (2001) Comparison of an array of in vitro assays for the assessment of the estrogenic potential of natural and synthetic estrogens, phytoestrogens and xenoestrogens. Toxicology 166:79–89

    Article  CAS  Google Scholar 

  • Hashimoto Y, Moriguchi Y, Oshima H et al (2000) Estrogenic activity of chemicals for dental and similar use in vitro. J Mater Sci Mater Med 11:465–468

    Article  CAS  Google Scholar 

  • Huang YQ, Wong CKC, Zheng JS et al (2012) Bisphenol A (BPA) in China: a review of sources, environmental levels, and potential human health impacts. Environ Int 42:91–99

    Article  CAS  Google Scholar 

  • Isidori M, Cangiano M, Palermo FA et al (2010) E-screen and vitellogenin assay for the detection of the estrogenic activity of alkylphenols and trace elements. Comp Biochem Physiol C: Toxicol Pharmacol 152:51–56

    Article  Google Scholar 

  • Jayne VB, Catherine AH, Martin S et al (2005) Accurate prediction of the response of freshwater fish to a mixture of estrogenic chemicals. Environ Health Perspect 113:721–728

    Article  Google Scholar 

  • Jones PA, Baker VA, Irwin AKE et al (1998) Interpretation of the in vitro proliferation response of MCF-7 cells to potential oestrogens and non-estrogenic substances. Toxicol In Vitro 12:373–382

    Article  CAS  Google Scholar 

  • Knudsen JG, Holbech H, Madsen SS et al (2011) Uptake of 17β-estradiol and biomarker responses in brown trout (Salmo trutta) exposed to pulses. Environ Pollut 159:3374–3380

    Article  CAS  Google Scholar 

  • Kortenkamp A, Altenburger R (1999) Approaches to assessing combination effects of oestrogenic environmental pollutants. Sci Total Environ 233:131–140

    Article  CAS  Google Scholar 

  • Laws SC, Carey SA, Ferrell JM et al (2000) Estrogenic activity of octylphenol, nonylphenol, bisphenol A and methoxychlor in rats. Toxicol Sci 54:154–167

    Article  CAS  Google Scholar 

  • Li Z, Li D, Oh J-R et al (2004) Seasonal and spatial distribution of nonylphenol in Shihwa Lake, Korea. Chemosphere 56:611–618

    Article  CAS  Google Scholar 

  • Li J, Ma M, Wang Z (2010) In vitro profiling of endocrine disrupting effects of phenols. Toxicol In Vitro 24:201–207

    Article  CAS  Google Scholar 

  • Maekawa S, Nishizuka M, Heitaku S et al (2004) Development of a competitive enzyme immunoassay for detection of capacity of chemicals to bind quail estrogen receptor α and β. J Health Sci 50:25–32

    Article  CAS  Google Scholar 

  • Matozzo V, Gagné F, Marin M et al (2008) Vitellogenin as a biomarker of exposure to estrogenic compounds in aquatic invertebrates: a review. Environ Int 34:531–545

    Article  CAS  Google Scholar 

  • Pedersen SN, Christiansen LB, Pedersen KL et al (1999) In vivo estrogenic activity of branched and linear alkylphenols in rainbow trout (Oncorhynchus mykiss). Sci Total Environ 223:89–96

    Article  Google Scholar 

  • Pillon A, Servant N, Vignon F et al (2005) In vivo bioluminescence imaging to evaluate estrogenic activities of endocrine disrupters. Anal Biochem 340:295–302

    Article  CAS  Google Scholar 

  • Pomatto V, Palermo F, Mosconi G et al (2011) Xenoestrogens elicit a modulation of endocannabinoid system and estrogen receptors in 4-NP treated goldfish, Carassius auratus. Gen Comp Endocrinol 174:30–35

    Article  CAS  Google Scholar 

  • Richter CA, Birnbaum LS, Farabollini F et al (2007) In vivo effects of bisphenol A in laboratory rodent studies. Reprod Toxicol 24:199–224

    Article  CAS  Google Scholar 

  • Rubin BS (2011) Bisphenol A: an endocrine disruptor with widespread exposure and multiple effects. J Steroid Biochem Mol Biol 127:27–34

    Article  CAS  Google Scholar 

  • Silva E, Rajapakse N, Kortenkamp A (2002) Something from “nothing”—eight weak estrogenic chemicals combined at concentrations below NOECs produce significant mixture effects. Environ Sci Technol 36:1751–1756

    Article  CAS  Google Scholar 

  • Staples CA, Hall AT, Friederich U et al (2011) Early life-stage and multigeneration toxicity study with bisphenol A and fathead minnows (Pimephales promelas). Ecotoxicol Environ Saf 74:1548–1557

    Article  CAS  Google Scholar 

  • Sun L, Zha J, Wang Z (2009) Interactions between estrogenic chemicals in binary mixtures investigated using vitellogenin induction and factorial analysis. Chemosphere 75:410–415

    Article  CAS  Google Scholar 

  • Tan BL, Kassim NM, Mohd MA (2003) Assessment of pubertal development in juvenile male rats after sub-acute exposure to bisphenol A and nonylphenol. Toxicol Lett 143:261–270

    Article  CAS  Google Scholar 

  • Toyoizumi T, Deguchi Y, Masuda S et al (2008) Genotoxicity and estrogenic activity of 3,3′-dinitrobisphenol A in goldfish. Biosci Biotechnol Biochem 72:2118–2123

    Article  CAS  Google Scholar 

  • Tubau I, Vázquez-Suñé E, Carrera J et al (2010) Occurrence and fate of alkylphenol polyethoxylate degradation products and linear alkylbenzene sulfonate surfactants in urban ground water: Barcelona case study. J Hydrol 383:102–110

    Article  CAS  Google Scholar 

  • Uchiyama T, Makino M, Saito H et al (2008) Syntheses and estrogenic activity of 4-nonylphenol isomers. Chemosphere 73:60–65

    Article  Google Scholar 

  • Vanparys C, Depiereux S, Nadzialek S et al (2010) Performance of the flow cytometric E-screen assay in screening estrogenicity of pure compounds and environmental samples. Sci Total Environ 408:4451–4460

    Article  CAS  Google Scholar 

  • Writer JH, Barber LB, Brown GK et al (2010) Anthropogenic tracers, endocrine disrupting chemicals, and endocrine disruption in Minnesota lakes. Sci Total Environ 409:100–111

    Article  CAS  Google Scholar 

  • Zhang X, Zha J, Li W et al (2008) Effects of 2,4-dichlorophenol on the expression of vitellogenin and estrogen receptor genes and physiology impairments in Chinese rare minnow (Gobiocypris rarus). Environ Toxicol 23:694–701

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was funded by Ocean Public Service Foundation (No. 201005012-2) and National Science and Technology Foundation of China (No. 2009ZX07528-006-03).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Zhengyan Li.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Li, Z., Zhang, H., Gibson, M. et al. An evaluation of the combined effects of phenolic endocrine disruptors on vitellogenin induction in goldfish Carassius auratus . Ecotoxicology 21, 1919–1927 (2012). https://doi.org/10.1007/s10646-012-0925-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-012-0925-0

Keywords