Skip to main content

Advertisement

Log in

Early life exposure of zebrafish (Danio rerio) to synthetic pyrethroids and their metabolites: a comparison of phenotypic and behavioral indicators and gene expression involved in the HPT axis and innate immune system

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Ecotoxicological studies have revealed the association between synthetic pyrethroid (SP) exposure and aquatic toxicity in fish; however, research on the toxic effects of SP metabolites is still limited. In this study, the toxicity of two SPs (permethrin (PM) and β-cypermethrin (β-CP)) and their three metabolites (3-phenoxybenzoic alcohol (PBCOH), 3-phenoxybenzaldehyde (PBCHO), and 3-phenoxybenzoic acid (PBCOOH)) towards zebrafish embryos and larvae was evaluated. Both SPs and their metabolites exhibited significant developmental toxicities, caused abnormal vascular development, and changed locomotor activities in larvae. The alteration of gene expression involved in the thyroid system and the innate immune system indicated that SPs and their three metabolites have the potency to induce thyroid disruption and trigger an immune response. The results from the present study suggest that SP metabolites could induce multiple toxic responses similar to parent compounds, and their toxicity should be considered for improving the understanding of environmental risks of SPs.

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

Access this article

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Ahmed SR (2000) The immune system as a potential target for environmental estrogens (endocrine disrupters): a new emerging field. Toxicology 150:191–206

    Article  CAS  Google Scholar 

  • Alexander S, Bernasconi J, Schneider WR, Orbach R (1981) Excitation dynamics in random one-dimensional systems. Rev Mod Phys 53:175–198

    Article  Google Scholar 

  • Berkowitz RJ (2003) Causes, treatment and prevention of early childhood caries: a microbiologic perspective. J Can Dent Assoc 69:304–307

    Google Scholar 

  • Blanton ML, Specker JL (2007) The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction. Crit Rev Toxicol 37:97–115

    Article  CAS  Google Scholar 

  • Bradberry SM, Cage SA, Proudfoot AT, Vale JA (2005) Poisoning due to pyrethroids. Toxicol Rev 24(2):93–106

    Article  CAS  Google Scholar 

  • Chen Q, Yu L, Yang L, Zhou B (2012) Bioconcentration and metabolism of decabromodiphenyl ether (BDE-209) result in thyroid endocrine disruption in zebrafish larvae. Aquat Toxicol 110-111:141–148

    Article  CAS  Google Scholar 

  • Corcellas C, Eljarrat E, Barcelo D (2015) First report of pyrethroid bioaccumulation in wild river fish: a case study in Iberian river basins (Spain). Environ Int 75:110–116

    Article  CAS  Google Scholar 

  • Couillard CM (2002) A microscale test to measure petroleum oil toxicity to mummichog embryos. Environ Toxicol 17:195–202

    Article  CAS  Google Scholar 

  • DeMicco A, Cooper KR, Richardson JR, White LA (2010) Developmental neurotoxicity of pyrethroid insecticides in zebrafish embryos. Toxicol Sci 113:177–186

    Article  CAS  Google Scholar 

  • Eder KJ, Clifford MA, Hedrick RP, Kohler HR, Werner I (2008) Expression of immune-regulatory genes in juvenile Chinook salmon following exposure to pesticides and infectious hematopoietic necrosis virus (IHNV). Fish Shellfish Immun 25:508–516

    Article  CAS  Google Scholar 

  • Escher BI, Hermens JL (2002) Modes of action in ecotoxicology: their role in body burdens, species sensitivity, QSARs, and mixture effects. Environmental Science & Technology 36(20):4201–4217

    Article  CAS  Google Scholar 

  • Feo ML, Ginebreda A, Eljarrat E, Barceló D (2010) Presence of pyrethroid pesticides in water and sediments of Ebro River Delta. J Hydrol 393:156–162

    Article  CAS  Google Scholar 

  • Fraysse B, Mons R, Garric J (2006) Development of a zebrafish 4-day embryo-larval bioassay to assess toxicity of chemicals. Ecotoxicol Environ Saf 63:253–267

    Article  CAS  Google Scholar 

  • Ge J, Cong J, Sun Y, Li GX, Zhou ZQ, Qian CF, Liu FM (2010) Determination of endocrine disrupting chemicals in surface water and industrial wastewater from Beijing, China. Bull Environ Contam Toxicol 84:401–405

    Article  CAS  Google Scholar 

  • Gianoukakis AG, Khadavi N, Smith TJ (2008) Cytokines, Graves' disease, and thyroid-associated ophthalmopathy. Thyroid 18(9):953–958

    Article  CAS  Google Scholar 

  • Irons TD, MacPhail RC, Hunter DL, Padilla S (2010) Acute neuroactive drug exposures alter locomotor activity in larval zebrafish. Neurotoxicol Teratol 32:84–90

    Article  CAS  Google Scholar 

  • Jeffries KM, Komoroske LM, Truong J, Werner I, Hasenbein M, Hasenbein S, Fangue NA, Connon RE (2015) The transcriptome-wide effects of exposure to a pyrethroid pesticide on the critically endangered delta smelt Hypomesus transpacificus. Endanger Species Res 28:43–60

    Article  Google Scholar 

  • Jiang JH, Wu SG, Wang YH, An XH, Cai LM, Zhao XP, Wu CX (2015) Carbendazim has the potential to induce oxidative stress, apoptosis, immunotoxicity and endocrine disruption during zebrafish larvae development. Toxicol in Vitro 29:1473–1481

    Article  CAS  Google Scholar 

  • Jin MQ, Zhang XF, Wang LJ, Huang CJ, Zhang Y, Zhao MR (2009) Developmental toxicity of bifenthrin in embryo-larval stages of zebrafish. Aquat Toxicol 95:347–354

    Article  CAS  Google Scholar 

  • Jin MQ, Li L, Xu C, Wen YZ, Zhao MR (2010b) Estrogenic activities of two synthetic pyrethroids and their metabolites. J Environ Sci-China 22:290–296

    Article  CAS  Google Scholar 

  • Jin YX, Chen R, Liu W, Fu Z (2010a) Effect of endocrine disrupting chemicals on the transcription of genes related to the innate immune system in the early developmental stage of zebrafish (Danio rerio). Fish Shellfish Immunol 28:854–861

    Article  CAS  Google Scholar 

  • Jin YX, Pan X, Cao L, Ma B, Fu Z (2013) Embryonic exposure to cis-bifenthrin enantioselectively induces the transcription of genes related to oxidative stress, apoptosis and immunotoxicity in zebrafish (Danio rerio). Fish Shellfish Immunol 34:717–723

    Article  CAS  Google Scholar 

  • Jin YX, Liu ZZ, Liu F, Yang Y, Peng T, Fu ZW (2015a) Embryonic exposure to cadmium (II) and chromium (VI) induce behavioral alterations, oxidative stress and immunotoxicity in zebrafish (Danio rerio). Neurotoxicol Teratol 48:9–17

    Article  CAS  Google Scholar 

  • Jin YX, Liu ZZ, Peng T, Fu ZW (2015b) The toxicity of chlorpyrifos on the early life stage of zebrafish: a survey on the endpoints at development, locomotor behavior, oxidative stress and immunotoxicity. Fish & Shellfish Immunol 43:405–414

    Article  CAS  Google Scholar 

  • Kim S, Jung J, Lee I, Jung D, Youn H, Choi K (2015) Thyroid disruption by triphenyl phosphate, an organophosphate flame retardant, in zebrafish (Danio rerio) embryos/larvae, and in GH3 and FRTL-5 cell lines. Aquat Toxicol 160:188–196

    Article  CAS  Google Scholar 

  • Klein JR (2006) The immune system as a regulator of thyroid hormone activity. Experimetal Biology and Medicine 231(3):229–236

    Article  CAS  Google Scholar 

  • Knobel M, Busser FJM, Rico-Rico A, Kramer NI, Hermens JLM, Hafner C, Tanneberger K, Schirmer K, Scholz S (2012) Predicting adult fish acute lethality with the zebrafish embryo: relevance of test duration, endpoints, compound properties, and exposure concentration analysis. Environ Sci Technol 46:9690–9700

    Article  CAS  Google Scholar 

  • Lema SC, Dickey JT, Schultz IR, Swanson P (2008) Dietary exposure to 2,2′,4,4′-tetrabromodiphenyl ether (PBDE-47) alters thyroid status and thyroid hormone-regulated gene transcription in the pituitary and brain. Environ Health Persp 116:1694–1699

    Article  CAS  Google Scholar 

  • Li W, Zha J, Spear PA, Li Z, Yang L, Wang Z (2009) Changes of thyroid hormone levels and related gene expression in Chinese rare minnow (Gobiocypris rarus) during 3-amino-1,2,4-triazole exposure and recovery. Aquat Toxicol 92:50–57

    Article  CAS  Google Scholar 

  • Liu YW, Lo LJ, Chan WK (2000) Temporal expression and T3 induction of thyroid hormone receptors alpha 1 and beta 1 during early embryonic and larval development in zebrafish, Danio rerio. Mol Cell Endocrinol 159:187–195

    Article  CAS  Google Scholar 

  • Liu Z, Tang R, Li D, Hu Q, Wang Y (2015) Subacute microcystin-LR exposure alters the metabolism of thyroid hormones in juvenile zebrafish (Danio rerio). Toxins (Basel) 7:337–352

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(T) (−delta delta C) method. Methods 25:402–408

    Article  CAS  Google Scholar 

  • Lu CS, Barr DB, Pearson M, Bartell S, Bravo R (2006) A longitudinal approach to assessing urban and suburban children's exposure to pyrethroid pesticides. Environ Health Persp 114:1419–1423

    Article  CAS  Google Scholar 

  • Lv X, Pan LM, Wang JY, Lu LP, Yan WL, Zhu YY, Xu YW, Guo M, Zhuang SL (2017) Effects of triazole fungicides on androgenic disruption and CYP3A4 enzyme activity. Environ Pollut 222:504–512

    Article  CAS  Google Scholar 

  • MacPhail RC, Brooks J, Hunter DL, Padnos B, Irons TD, Padilla S (2009) Locomotion in larval zebrafish: influence of time of day, lighting and ethanol. Neurotoxicology 30:52–58

    Article  CAS  Google Scholar 

  • Mehler WT, Li HZ, Lydy MJ, You J (2011) Identifying the causes of sediment-associated toxicity in urban waterways of the Pearl River Delta, China. Environ Sci Technol 45:1812–1819

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Morgan K (2007) The learning region: institutions, innovation and regional renewal. Reg Stud 41:S147–S159

    Article  Google Scholar 

  • Oliveri AN, Bailey JM, Levin ED (2015) Developmental exposure to organophosphate flame retardants causes behavioral effects in larval and adult zebrafish. Neurotoxicol Teratol 52:220–227

    Article  CAS  Google Scholar 

  • Orozco A, Valverde RC (2005) Thyroid hormone deiodination in fish. Thyroid 15:799–813

    Article  CAS  Google Scholar 

  • Power DM, Llewellyn L, Faustino M, Nowell MA, Bjornsson BT, Einarsdottir IE, Canario AVM, Sweeney GE (2001) Thyroid hormones in growth and development of fish. Comp Biochem Physiol C Toxicol Pharmacol 130(4):447–459

    Article  CAS  Google Scholar 

  • Renick VC, Anderson TW, Morgan SG, Cherr GN (2015) Interactive effects of pesticide exposure and habitat structure on behavior and predation of a marine larval fish. Ecotoxicology 24:391–400

    Article  CAS  Google Scholar 

  • Riar N, Crago J, Jiang WY, Maryoung LA, Gan J, Schlenk D (2013) Effects of salinity acclimation on the endocrine disruption and acute toxicity of bifenthrin in freshwater and euryhaline strains of oncorhynchus mykiss. Environ Toxicol Chem 32:2779–2785

    Article  CAS  Google Scholar 

  • Richards J, Lu Z, Fu Q, Schlenk D, Gan J (2017) Conversion of pyrethroid insecticides to 3-phenoxybenzoic acid on urban hard surfaces. Environmental Science & Technology Letters 4:546–550. https://doi.org/10.1021/acs.estlett.7b00466

    Article  CAS  Google Scholar 

  • Roh YS, Cho A, Islam MR, Cho S, Kim J, Kim JH, Lee JW, Lim CW, Kim B (2011) 3,3′-Diindolylmethane induces immunotoxicity via splenocyte apoptosis in neonatal mice. Toxicol Lett 206:218–228

    Article  CAS  Google Scholar 

  • Sereda B, Bouwman H, Kylin H (2009) Comparing water, bovine milk, and indoor residual spraying as possible sources of DDT and pyrethroid residues in breast milk. J Toxicol Environ Health A 72(13):842–851

    Article  CAS  Google Scholar 

  • Shi XJ, Liu CS, Wu GQ, Zhou BS (2009) Waterborne exposure to PFOS causes disruption of the hypothalamus-pituitary-thyroid axis in zebrafish larvae. Chemosphere 77:1010–1018

    Article  CAS  Google Scholar 

  • Soderlund DM, Clark JM, Sheets LP, Mulin LS, Piccirillo VJ, Sargent D, Stevens JT, Weiner MY (2002) Mechanisms of pyrethroid neurotoxicity: implications for cumulative risk assessment. Toxicology 171:3–59

    Article  CAS  Google Scholar 

  • Trede NS, Langenau DM, Traver D, Look AT, Zon LI (2004) The use of zebrafish to understand immunity. Immunity 20:367–379

    Article  CAS  Google Scholar 

  • Tu WQ, Lu B, Niu LL, Xu C, Lin CM, Liu WP (2014) Dynamics of uptake and elimination of pyrethroid insecticides in zebrafish (Danio rerio) eleutheroembryos. Ecotoxicol Environ Saf 107:186–191

    Article  CAS  Google Scholar 

  • Tu WQ, Niu LL, Liu WP, Xu C (2013) Embryonic exposure to butachlor in zebrafish (Danio rerio): endocrine disruption, developmental toxicity and immunotoxicity. Ecotox Environ Safe 89:189–195

    Article  CAS  Google Scholar 

  • Tu WQ, Xu C, Jin YX, Lu B, Lin CM, Wu YM, Liu WP (2016a) Permethrin is a potential thyroid-disrupting chemical: in vivo and in silico envidence. Aquat Toxicol 175:39–46

    Article  CAS  Google Scholar 

  • Tu WQ, Xu C, Lu B, Lin CM, Wu YM, Liu WP (2016b) Acute exposure to synthetic pyrethroids causes bioconcentration and disruption of the hypothalamus-pituitary-thyroid axis in zebrafish embryos. Sci Total Environ 542:876–885

    Article  CAS  Google Scholar 

  • Tyler CR, Beresford N, Woning MVD, Sumpter JP, Thorpe K (2000) Metabolism and environmental degradation of pyrethroid insecticides produce compounds with endocrine activities. Environ Toxicol Chem 19:801–809

    Article  CAS  Google Scholar 

  • Weis JS (2014) Delayed behavioral effects of early life toxicant exposures in aquatic biota. Toxics 2(2):165–187

    Article  CAS  Google Scholar 

  • Whyatt RM, Camann DE, Kinney PL, Reyes A, Ramirez J, Dietrich J, Diaz D, Holmes D, Perera FP (2002) Residential pesticide use during pregnancy among a cohort of urban minority women. Environ Health Persp 110:507–514

    Article  CAS  Google Scholar 

  • Xu C, Wang JJ, Liu WP, Sheng GD, Tu YJ, Ma Y (2008a) Separation and aquatic toxicity of enantiomers of the pyrethroid insecticide lambda-cyhalothrin. Environ Toxicol Chem 27:174–181

    Article  CAS  Google Scholar 

  • Xu C, Tu W, Deng M, Jin Y, Lu B, Zhang C, Lin C, Wu Y, Liu W (2016) Stereoselective induction of developmental toxicity and immunotoxicity by acetochlor in the early life stage of zebrafish. Chemosphere 164:618–626

    Article  CAS  Google Scholar 

  • Xu C, Zhao MR, Liu WP, Chen SW, Gan JY (2008b) Enantioselectivity in zebrafish embryo toxicity of the insecticide acetofenate. Chem Res Toxicol 21:1050–1055

    Article  CAS  Google Scholar 

  • Zhao DD, Liu XY, Shi WR, Liu RF (2011) Determination of cypermethrin residues in crucian carp tissues by MSPD/GC-ECD. Chromatographia 73:1021–1025

    Article  CAS  Google Scholar 

  • Zheng XM, Zhu YT, Liu CS, Liu HL, Giesy JP, Hecker M, Yu HX (2012) Accumulation and biotransformation of BDE-47 by zebrafish larvae and teratogenicity and expression of genes along the hypothalamus-pituitary-thyroid axis. Environ Sci Technol 46:12943–12951

    Article  CAS  Google Scholar 

  • Zhang Y, Zhao M, Jin M, Xu C, Wang C, Liu W (2010) Immunotoxicity of pyrethroid metabolites in an in vitro model. Environ Toxicol Chem 29:2505–2510

    Article  CAS  Google Scholar 

  • Zhuang SL, Lv X, Pan LM, Lu LP, Ge ZW, Wang JY, Wang JP, Liu JS, Liu WP, Zhang CL (2017) Benzotriazole UV 328 and UV-P showed distinct antiandrogenic activity upon human CYP3A4-mediated biotransformation. Environ Pollut 220, Part A:616-624

  • Zhuang S, Zhang Z, Zhang W, Bao L, Xu C, Zhang H (2015) Enantioselective developmental toxicity and immunotoxicity of pyraclofos toward zebrafish (Danio rerio). Aquat Toxicol 159:119–126

    Article  CAS  Google Scholar 

Download references

Funding

This work was supported by the National Natural Science Foundation of China (Nos. 21277126 and 21320102007) and the Zhejiang Provincial Natural Science Foundation of China (No. LY15B070007).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Chao Xu or Lili Niu.

Additional information

Responsible editor: Markus Hecker

Electronic supplementary material

ESM 1

(DOCX 20 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xu, C., Li, X., Jin, M. et al. Early life exposure of zebrafish (Danio rerio) to synthetic pyrethroids and their metabolites: a comparison of phenotypic and behavioral indicators and gene expression involved in the HPT axis and innate immune system. Environ Sci Pollut Res 25, 12992–13003 (2018). https://doi.org/10.1007/s11356-018-1542-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-018-1542-0

Keywords

Navigation