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Responses of growth, malformation, and thyroid hormone-dependent genes expression in Bufo gargarizans embryos following chronic exposure to Pb2+

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Abstract

The aim of this study was to examine the adverse effects of lead (Pb) exposure on Bufo gargarizans embryos. The 96 h-LC50 of Pb2+ for B. gargarizans embryos was determined to be 26.6 mg L−1 after an acute test. In the chronic test, B. gargarizans embryos at Gosner stage 3 were exposed to 10~2000 μg Pb2+ L−1 during embryogenesis. Total length, weight, developmental stage, and malformation were monitored. In addition, the transcript levels of type II and type III iodothyronine deiodinase (Dio2 and Dio3) and thyroid hormone receptors (TRα and TRβ) were determined to assess the thyroid-disrupting effects of Pb2+. Slightly increased growth and development of B. gargarizans embryos were observed at low concentrations of Pb2+ (10, 50, and 100 μg L−1), while retarded growth and development were found at high concentrations of Pb2+ (1000 and 2000 μg L−1). In addition, Pb2+ exposure induced morphological abnormalities, which were characterized by edema at tail, wavy fin, abdominal edema, stunted growth, hyperplasia, and axial flexures in B. gargarizans embryos. Furthermore, our results showed that exposure to 2000 μg Pb2+ L−1 decreased the transcript levels of Dio2, TRα, and TRβ, but it increased Dio3 mRNA level. In contrast, exposure to 50 μg Pb2+ L−1 increased TRα mRNA level and decreased Dio3 mRNA level. These results suggested that Pb2+ might have thyroid-disrupting effects, leading to the disruption of growth and development in B. gargarizans embryos.

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References

  • Aronzon CM, Sandoval MT, Herkovits J, Pérez-Coll CS (2011) Stage-dependent toxicity of 2,4-dichlorophenoxyacetic on the embryonic development of a South American toad, Rhinella arenarum. Environ Toxicol 26(4):373–381

    Article  CAS  Google Scholar 

  • Banker DE, Bigler J, Eisenman RN (1991) The thyroid hormone receptor gene (c-erbA alpha) is expressed in advance of thyroid gland maturation during the early embryonic development of Xenopus laevis. Mol Cell Biol 11(10):5079–5089

    Article  CAS  Google Scholar 

  • Berzins DW, Bundy KJ (2002) Bioaccumulation of lead in Xenopus laevis tadpoles from water and sediment. Environ Int 28(1–2):69–77

    Article  CAS  Google Scholar 

  • Bonett RM, Hoopfer ED, Denver RJ (2010) Molecular mechanisms of corticosteroid synergy with thyroid hormone during tadpole metamorphosis. Gen Comp Endocrinol 168(2):209–219

    Article  CAS  Google Scholar 

  • Boyd RS (2010) Heavy metal pollutants and chemical ecology: exploring new frontiers. J Chem Ecol 36:46–58

    Article  CAS  Google Scholar 

  • Brown DD, Cai L (2007) Amphibian metamorphosis. Dev Biol 306:20–33

    Article  CAS  Google Scholar 

  • Buchholz DR, Paul BD, Fu L, Shi YB (2006) Molecular and developmental analyses of thyroid hormone receptor function in Xenopus laevis, the African clawed frog. Gen Comp Endocrinol 145(1):1–19

    Article  CAS  Google Scholar 

  • Chai L, Dong S, Zhao H, Deng H, Wang H (2016a) Effects of fluoride on development and growth of Rana chensinensis embryos and larvae. Ecotoxicol Environ Saf 126:129–137

    Article  CAS  Google Scholar 

  • Chai L, Wang H, Zhao H, Deng H (2016b) Chronic effects of triclosan on embryonic development of Chinese toad, Bufo gargarizans. Ecotoxicology 25(8):1600–1608

    Article  CAS  Google Scholar 

  • Chai L, Wang H, Zhao H, Dong S (2017) Chronic effects of fluoride exposure on growth, metamorphosis, and skeleton development in Bufo gargarizans larvae. Bull Environ Contam Toxicol 98(4):496–501

    Article  CAS  Google Scholar 

  • Dou C, Zhang J (2011) Effects of lead on neurogenesis during zebrafish embryonic brain development. J Hazard Mater 194:277–282

    Article  CAS  Google Scholar 

  • Dundar B, Öktem F, Arslan MK, Delibas N, Baykal B, Arslan Ç, Gultepe M, Ilhan IE (2006) The effect of long-term low-dose lead exposure on thyroid function in adolescents. Environ Res 101:140–145

    Article  CAS  Google Scholar 

  • Duzgoren-Aydin NS (2007) Sources and characteristics of lead pollution in the urban environment of Guangzhou. Sci Total Environ 385:182–195

    Article  CAS  Google Scholar 

  • Fini JB, Le Mével S, Palmier K, Darras VM, Punzon I, Richardson SJ, Clerget-Froidevaux MS, Demeneix BA (2012) Thyroid hormone signaling in the Xenopus laevis embryo is functional and susceptible to endocrine disruption. Endocrinology 153(10):5068–5081

    Article  CAS  Google Scholar 

  • Fort DJ, Degitz S, Tietge J, Touart LW (2007) The hypothalamic-pituitary-thyroid (HPT) axis in frogs and its role in frog development and reproduction. Crit Rev Toxicol 37(1–2):117–161

    Article  CAS  Google Scholar 

  • Furlow JD, Yang HY, Hsu M, Lim W, Ermio DJ, Chiellini G, Scanlan TS (2004) Induction of larval tissue resorption in Xenopus laevis tadpoles by the thyroid hormone receptor agonist GC-1. J Biol Chem 279(25):26555–26562

    Article  CAS  Google Scholar 

  • Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 16:183–190

    Google Scholar 

  • Heijlen M, Houbrechts AM, Bagci E, Van Herck SL, Kersseboom S, Esguerra CV, Blust R, Visser TJ, Knapen D, Darras VM (2014) Knockdown of type 3 iodothyronine deiodinase severely perturbs both embryonic and early larval development in zebrafish. Endocrinology 155(4):1547–1559

    Article  Google Scholar 

  • Hu L, Zhu J, Rotchell JM, Wu L, Gao J, Shi H (2015) Use of the enhanced frog embryo teratogenesis assay-Xenopus (FETAX) to determine chemically-induced phenotypic effects. Sci Total Environ 508:258–265

    Article  CAS  Google Scholar 

  • Huang MY, Duan RY, Ji X (2014) Chronic effects of environmentally-relevant concentrations of lead in Pelophylax nigromaculata tadpoles: threshold dose and adverse effects. Ecotoxicol Environ Saf 104:310–316

    Article  CAS  Google Scholar 

  • Hutler Wolkowicz IR, Aronzon CM, Pérez Coll CS (2013) Lethal and sublethal toxicity of the industrial chemical epichlorohydrin on Rhinella arenarum (Anura, Bufonidae) embryos and larvae. J Hazard Mater 263(Pt 2):784–791

    Article  CAS  Google Scholar 

  • Ishizuya-Oka A (2011) Amphibian organ remodeling during metamorphosis: insight into thyroid hormone-induced apoptosis. Develop Growth Differ 53(2):202–212

    Article  CAS  Google Scholar 

  • James SM, Little EE (2003) The effects of chronic cadmium exposure on American toad (Bufo americanus) tadpoles. Environ Toxicol Chem 22(2):377–380

    Article  CAS  Google Scholar 

  • Jofré MB, Antón RI, Caviedes-Vidal E (2011) Lead and cadmium accumulation in anuran amphibians of a permanent water body in arid Midwestern Argentina. Environ Sci Pollut Res Int 19(7):2889–2897

    Article  Google Scholar 

  • Khargarot BS, Sehgal A, Bhasin MK (1985) “Man and the biosphere”—studies on the Sikkim Himalayas. Part 5: acute toxicity of selected heavy metals on the tadpoles of Rana hexadactyla. Acta Hydrochim et Hydrobiol 13:259–263

  • Leduc J, Echaubard P, Trudeau V, Lesbarrères D (2016) Copper and nickel effects on survival and growth of northern leopard frog (Lithobates pipiens) tadpoles in field-collected smelting effluent water. Environ Toxicol Chem 35(3):687–694

    Article  CAS  Google Scholar 

  • Ling Q, Hong F (2010) Antioxidative role of cerium against the toxicity of lead in the liver of silver crucian carp. Fish Physiol Biochem 36:367–376

    Article  CAS  Google Scholar 

  • Liu YW, Chan WK (2002) Thyroid hormones are important for embryonic to larval transitory phase in zebrafish. Differentiation 70(1):36–45

    Article  CAS  Google Scholar 

  • Lopez CM, Pineiro AE, Nunez N, Avagnina AM, Villaamil EC, Roses OE (2000) Thyroid hormone changes in males exposed to lead in the Buenos Aires area (Argentina). Pharmacol Res 42:599–602

    Article  CAS  Google Scholar 

  • Loumbourdis NS (2003) Nephrotoxic effects of lead nitrate in Rana ridibunda. Arch Toxicol 77(9):527–532

    Article  CAS  Google Scholar 

  • Maher SK, Wojnarowicz P, Ichu TA, Veldhoen N, Lu L, Lesperance M, Propper CR, Helbing CC (2016) Rethinking the biological relationships of the thyroid hormones, l-thyroxine and 3,5,3′-triiodothyronine. Comp Biochem Physiol Part D Genomics Proteomics 18:44–53

    Article  CAS  Google Scholar 

  • Miao W, Zhu B, Xiao X, Li Y, Dirbaba NB, Zhou B, Wu H (2015) Effects of titanium dioxide nanoparticles on lead bioconcentration and toxicity on thyroid endocrine system and neuronal development in zebrafish larvae. Aquat Toxicol 161:117–126

    Article  CAS  Google Scholar 

  • Morvan Dubois G, Sebillot A, Kuiper GG, Verhoelst CH, Darras VM, Visser TJ, Demeneix BA (2006) Deiodinase activity is present in Xenopus laevis during early embryogenesis. Endocrinology 147(10):4941–4949

    Article  CAS  Google Scholar 

  • Mouchet F, Cren S, Cunienq C, Deydier E, Guilet R, Gauthier L (2007) Assessment of lead ecotoxicity in water using the amphibian larvae (Xenopus laevis) and preliminary study of its immobilization in meat and bone meal combustion residues. Biometals 20(2):113–127

    Article  CAS  Google Scholar 

  • Mukhi S, Patiño R (2007) Effects of prolonged exposure to perchlorate on thyroid and reproductive function in zebrafish. Toxicol Sci 96(2):246–254

    Article  CAS  Google Scholar 

  • Nations S, Long M, Wages M, Maul JD, Theodorakis CW, Cobb GP (2015) Subchronic and chronic developmental effects of copper oxide (CuO) nanoparticles on Xenopus laevis. Chemosphere 135:166–174

    Article  CAS  Google Scholar 

  • Nations S, Wages M, Cañas JE, Maul J, Theodorakis C, Cobb GP (2011) Acute effects of Fe2O3, TiO2, ZnO and CuO nanomaterials on Xenopus laevis. Chemosphere 83(8):1053–1061

    Article  CAS  Google Scholar 

  • Oetting A, Yen PM (2007) New insights into thyroid hormone action. Best Pract Res Clin Endocrinol Metab 21(2):193–208

    Article  CAS  Google Scholar 

  • Pérez-Coll C, Herkovits J (1990) Stage dependent susceptibility to lead in Bufo arenarum embryos. Environ Pollut 63:239–245

    Article  Google Scholar 

  • Puzianowska-Kuznicka M, Damjanovski S, Shi YB (1997) Both thyroid hormone and 9-cis retinoic acid receptors are required to efficiently mediate the effects of thyroid hormone on embryonic development and specific gene regulation in Xenopus laevis. Mol Cell Biol 17(8):4738–4749

    Article  CAS  Google Scholar 

  • Rice C, Ghorai JK, Zalewski K, Weber DN (2011) Developmental lead exposure causes startle response deficits in zebrafish. Aquat Toxicol 105(3–4):600–608

    Article  CAS  Google Scholar 

  • Rowe CL, Kinney OM, Nagle RD, Congdon JD (1998) Elevated maintenance costs in an anuran (Rana catesbeiana) exposed to a mixture of trace elements during the embryonic and early larval periods. Physiol Zool 71:27–35

    Article  CAS  Google Scholar 

  • Singh B, Chandran V, Bandhu HK, Mittal BR, Bhattacharya A, Jindal SK, Varma S (2000) Impact of lead exposure on pituitary-thyroid axis in humans. Biometals 13:187–192

    Article  CAS  Google Scholar 

  • Sparling DW, Krest S, Ortiz-Santaliestra M (2006) Effects of lead-contaminated sediment on Rana sphenocephala tadpoles. Arch Environ Contam Toxicol 51(3):458–466

    Article  CAS  Google Scholar 

  • Tchernitchin NN, Clavero A, Mena MA, Unda C, Villagra R, Cumsille M, Tchernitchin AN (2003) Effect of chronic exposure to lead on estrogen action in the prepubertal rat uterus. Environ Toxicol 18:268–277

    Article  CAS  Google Scholar 

  • Tindall AJ, Morris ID, Pownall ME, Isaacs HV (2007) Expression of enzymes involved in thyroid hormone metabolism during the early development of Xenopus tropicalis. Biol Cell 99(3):151–163

    Article  CAS  Google Scholar 

  • Unrine JM, Jagoe CH, Hopkins WA, Brant HA (2004) Adverse effects of ecologically relevant dietary mercury exposure in southern leopard frog (Rana sphenocephala) larvae. Environ Toxicol Chem 23(12):2964–2970

    Article  Google Scholar 

  • Walpita CN, Crawford AD, Janssens ED, Van der Geyten S, Darras VM (2009) Type 2 deiodinase is essential for thyroid hormone-dependent embryonic development and pigmentation in zebrafish. Endocrinology 150(1):530–539

    Article  CAS  Google Scholar 

  • Wang M, Chai L, Zhao H, Wu M, Wang H (2015) Effects of nitrate on metamorphosis, thyroid and iodothyronine deiodinases expression in Bufo gargarizans larvae. Chemosphere 139:402–409

    Article  CAS  Google Scholar 

  • Wang MZ, Jia XY (2009) Low levels of lead exposure induce oxidative damage and DNA damage in the testes of the frog Rana nigromaculata. Ecotoxicology 18(1):94–99

    Article  Google Scholar 

  • Wang X, Lu X, Li C, Gao W, Gao M (2001) Toxicity of heavy metal irons to embryos and larvae of Rana nigromaculata. Sichuan journal of zoology 20:59–61

    Google Scholar 

  • Wu C, Zhang Y, Chai L, Wang H (2017b) Histological changes, lipid metabolism and oxidative stress in the liver of Bufo gargarizans exposed to cadmium concentrations. Chemosphere 179:337–346

    Article  CAS  Google Scholar 

  • Wu C, Zhang Y, Chai L, Wang H (2017a) Oxidative stress, endocrine disruption, and malformation of Bufo gargarizans embryo exposed to sub-lethal cadmium concentrations. Environ Toxicol Pharmacol 49:97–104

    Article  CAS  Google Scholar 

  • Xia K, Zhao H, Wu M, Wang H (2012) Chronic toxicity of copper on embryo development in Chinese toad, Bufo gargarizans. Chemosphere 87(11):1395–1402

    Article  CAS  Google Scholar 

  • Yin X, Jiang S, Yu J, Zhu G, Wu H, Mao C (2014) Effects of spirotetramat on the acute toxicity, oxidative stress, and lipid peroxidation in Chinese toad (Bufo bufo gargarizans) tadpoles. Environ Toxicol Pharmacol 37(3):1229–1235

    Article  CAS  Google Scholar 

  • Zhu B, Wang Q, Wang X, Zhou B (2014) Impact of co-exposure with lead and decabromodiphenyl ether (BDE-209) on thyroid function in zebrafish larvae. Aquat Toxicol 157:186–195

    Article  CAS  Google Scholar 

  • Zhuang P, Wang R, Shi X, Zhang L (2009) Acute toxicity and safety assessment of fluoride to larval Siberian sturgeon Acipenser baeri. Asian J Ecotoxicol 3:440–445

    Google Scholar 

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Funding

This study was funded by the National Natural Science Foundation of China (No. 41401570 and No. 31572222) and the Natural Science Foundation of Shaanxi Province, China (No. 2015JQ4098).

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Author notes

  1. Lihong Chai and Yanbin Li contributed equally to this work.

Authors and Affiliations

  1. School of Environmental Science and Engineering, Chang’an University, Xi’an, 710054, People’s Republic of China

    Lihong Chai, Yanbin Li, Zhihong Chen, Aixia Chen & Hongzhang Deng

  2. Key Laboratory of Subsurface Hydrology and Ecological Effect in Arid Region Ministry of Education, Xi’an, 710062, People’s Republic of China

    Lihong Chai, Yanbin Li, Zhihong Chen, Aixia Chen & Hongzhang Deng

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  1. Lihong Chai
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  2. Yanbin Li
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  3. Zhihong Chen
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  5. Hongzhang Deng
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Correspondence to Lihong Chai.

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Responsible editor: Philippe Garrigues

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Chai, L., Li, Y., Chen, Z. et al. Responses of growth, malformation, and thyroid hormone-dependent genes expression in Bufo gargarizans embryos following chronic exposure to Pb2+ . Environ Sci Pollut Res 24, 27953–27962 (2017). https://doi.org/10.1007/s11356-017-0413-4

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