Effects of low concentrations of triphenyltin on neurobehavior and the thyroid endocrine system in zebrafish

https://doi.org/10.1016/j.ecoenv.2019.109776Get rights and content

Highlights

  • Exposure to TPT induced neurobehavioral toxicity in zebrafish larvae.

  • The contents of neurotransmitters were decreased in fish brain exposed to TPT.

  • The abnormal non-reproductive behavior were observed in fish after exposure to TPT.

  • Thyroid hormone system were disturbed in zebrafish larvae.

Abstract

In the present study, to evaluate neurobehavioral toxicity and the thyroid-disrupting effects of environmental levels of triphenyltin (TPT), the zebrafish larvae were exposed to 1, 10 and 100 ng/l TPT. In the neurobehavioral assay, increased levels of dopamine and serotonin, decreased content of nitric oxide, inhibited activities of acetylcholinesterase and monoamine oxidase were observed in the whole body of zebrafish larvae after TPT treatment, as well as the serious abnormal non-reproductive behavior. Moreover, the whole-body the T4 levels were markedly decreased significantly, whereas T3 levels were not significantly changed under TPT stress. In addition, TPT exposure significantly changed the expression levels of genes related to thyroid system, including corticotropin-releasing hormone gene crh, thyroid-stimulating hormone gene tshβ, thyroglobulin gene tg, sodium/iodide symporter gene nis, thyroid hormone nuclear receptor trα, isoform trβ, types I deiodinase gene dio1and types II deiodinase gene dio2. The regulated responsiveness of thyroid hormone and related genes expression levels suggested that TPT could induce the thyroid disrupting effects in zebrafish larvae. Therefore, our results provide new aspects of TPT as an endocrine disrupting chemical.

Graphical abstract

IBR of all parameters measured in zebrafish larvae exposed to different concentrations of TPT.

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Introduction

Due to their biocidal properties, organotin compounds are commonly used as chemicals throughout the world (Hoch, 2001). Triphenyltin (TPT), which has been used for antifouling coating since the 1960s (Fent, 1996; Oliveira and Santelli, 2010), is considered to be a worldwide contaminant. Due to the adverse health effects caused by organotin compounds, many countries have banned the use of TPT for antifouling coating. However, due to its usage in biocides or fungicides, high concentrations of TPT are still found in aquatic environments (Antes et al., 2011). In rivers, TPT concentrations generally range from the limit of detection to hundreds of ng/L. Furthermore, organotin compounds accumulate in sediments and their concentrations decrease very slowly (Gao et al., 2017). Recent surveys show that TPT has been one of the most serious environmental contaminants in some areas of China, including Hong Kong (Ho et al., 2016).

Several adverse effects of TPT on fish or other aquatic organisms have been reported. These adverse effects include disrupting the biosynthesis of endogenous estrogens in rainbow trout (Hinfray et al., 2006), decreasing the spawning frequency in the Japanese medaka (Zhang et al., 2008), influencing the hypothalamus-pituitary-gonadal axis in rockfish (Sun et al., 2011), and altering the mating behaviors in male guppies (Zhang et al., 2019). The thyroid hormone system plays a key role in the reproduction, development, and energy metabolism of vertebrates (Schnitzler et al., 2012). THs may play an important role during embryonic development since high concentrations of maternal THs have been detected in embryos (Cheng et al., 2017; Shi et al., 2019). However, there are no reports about the effects of TPT on the disruption of the thyroid hormone system in fish (Spaan et al., 2019).

Under conditions of environmental stress, fish exhibit abnormal behavioral responses; these findings could provide a link between the fish and their surroundings (Weis and Candelmo, 2012). Although behavioral data from fish populations have been widely used to assess the potential risks associated with environmental pollutants, the molecular mechanisms underlying the effects of these pollutants are still not clear (Robinson, 2009). Compared with other endocrine-disrupting endpoints, only some studies report the influences of organotin on fish behavioral responses (Yu et al., 2013; Li and Li, 2015; Xiao et al., 2018). According to the available data, there is still an information gap regarding the effects of TPT on non-reproductive behavior in fish. Determining how TPT affects behavioral responses is important for fully understanding its mechanisms of toxicity.

The aim of this study was to assess the thyroid-disrupting effects of TBT as well as the neurobehavioral responses of fish exposed to environmental levels of this chemical. Zebrafish were used as the vertebrate model because of previous biological and genetic discoveries using this model. At 7 days after hatching, zebrafish larvae were exposed to different levels of TPT for a period of 14 days. The levels of THs and the expression of genes related to the hypothalamus-pituitary-thyroid (HPT) axis were measured. Also, the levels of neurotransmitters and non-reproductive behavior were examined after exposure to TPT.

Section snippets

Chemicals and test fish

TPT chloride (98%; CAS:1124-19-2) and other chemicals were purchased from Sigma–Aldrich Chemical Co. (USA). The chemical solution was prepared using the same method as that used in our previous study (Li and Li, 2015). Briefly, a suitable amount of this compound was directly weighed into a brown volume vessel and dissolved in 50 mL of 95% ethanol to form a stock solution with a stable concentration. This stock solution was sealed and stored at 4 °C until use. The working standard solution

Effect of TPT on fish non-reproductive behavior

While there were no obvious behavioral changes observed in the control group, abnormal behavior was observed in all the exposed groups. Larvae exposed to higher concentrations of TPT exhibited more serious signs of disordered behavior such as dyspnea, decreased activity, and slower response time lags (Table 2).

This is the first study to investigate the effects of TPT exposure on non-reproductive behaviors in zebrafish. These behavioral responses could provide useful information regarding the

Conclusion

The toxicity of TPT was evaluated by examining neurobehavioral responses and TH levels in zebrafish larvae. Significant alterations in neurobiological parameters and non-reproductive behavior were observed in fish following exposure to TPT. Additionally, the environmental levels of TPT caused dysregulation of the HTP axis, which is reflected by altered levels of THs and expression of related genes. Our study provides useful information regarding the effects of TPT on the non-reproductive

Disclaimer

The authors have no conflict of interest to declare.

Acknowledgments

This work was financially supported by the National Natural Science Foundation of China (No. 31570511, 21407181), Hubei Provincial Natural Science Funds for Distinguished Young Scholar, China (No. 2017CFA071), Wuhan Sci-Tech Chenguang Funds for Youth scientists, China (No. 2017050304010273), Key Technologies Research and Development Program of China (2018YFD0900902, 2018YFD0900905), and Natural Science Foundation of Shandong Province, China (No.ZR2019MC011).

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