Chronic effects of lead on metamorphosis, development of thyroid gland, and skeletal ossification in Bufo gargarizans

Yang, Hong-Chang; Liu, Rong; Liang, Zhijia; Zheng, Rui; Yang, Yijie; Chai, Lihong; Wang, Hongyuan

doi:10.1016/j.chemosphere.2019.06.221

Cited by 20 publications

(5 citation statements)

References 64 publications

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“…Some metals are anti-thyroidogenic and decrease metamorphic rate, thereby posing a threat to wild amphibians (Thambirajah et al, 2019). Sublethal concentrations of Pb has been shown to inhibit metamorphosis in Bufo arenarum (Pérez-Coll et al, 1988, L. pipiens (Northern leopard frog; Chen et al, 2006), Pelophylax nigromaculatus (Black spotted frog; Huang et al, 2014) and B. gargarizans (Yang et al, 2019). In B. gargarizans, Pb exposure at 1000 µg/L caused follicular cell hyperplasia and colloid depletion in thyroid glands, increased the transcript levels of dio2, trα, and trβ, while decreasing dio3 mRNA levels (Yang et al, 2019).…”

Section: Metalsmentioning

confidence: 99%

Agrochemicals disrupt multiple endocrine axes in amphibians

Trudeau

Thomson

Zhang

et al. 2020

Molecular and Cellular Endocrinology

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Section: Metalsmentioning

confidence: 99%

Agrochemicals disrupt multiple endocrine axes in amphibians

Trudeau

Thomson

Zhang

et al. 2020

Molecular and Cellular Endocrinology

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“…The timing of metamorphosis and the percentage of tadpoles that reached metamorphosis are significant factors affecting the number of amphibian juveniles recruited into terrestrial environments (Semlitsch and Gibbons 1988; Pechmann et al 1989), and they can be affected by multiple environmental stressors (Wang et al 2015; Chai et al 2016a; Yang et al 2019). In the present study, the Cr‐treated groups experienced developmental delay, and tadpoles exposed to 13 to 416 μg/L Cr (VI) reached metamorphic climax 1 to 3 d later than controls.…”

Section: Discussionmentioning

confidence: 99%

“…Histomorphological changes of the thyroid gland are used as a sensitive indicator for chemical‐induced thyrotoxicity (Grim et al 2009; Miyata and Ose 2012). Usually, histopathological changes were characterized by glandular atrophy, reduced colloid, and follicular cell hyperplasia (Zhao et al 2013; Ose et al 2019; Yang et al 2019). Several studies have shown that exposure to Cr (VI) affects thyroid gland histological characteristics in experimental organisms (Hassanin et al 2013; Mishra and Mohanty 2015).…”

Section: Discussionmentioning

confidence: 99%

“…Chinese toad (Bufo gargarizans) is one of the most common amphibian species and is widely distributed in eastern Asia. In previous studies, B. gargarizans has been used as a test organism in the assessment of the potential toxic effects of aquatic pollutants, including copper (Xia et al 2012;Wang et al 2016), Cr (VI) (Li et al 2018;Yao et al 2019;Yang et al 2020), triclosan (Chai et al 2016b(Chai et al , 2017a, lead (Chai et al 2017b;Yang et al 2019), cadmium (Wu et al 2017a(Wu et al , 2017b, fluoride (Bo et al 2018;Wu et al 2018;Wang et al 2019), nitrate (Wang et al 2015;Xie et al 2019), and spirotetramat (Yin et al 2014). Although the adverse effects of Cr (VI) on B. gargarizans have been explored in previous studies, they mainly focused on the embryonic stage (Li et al 2018), gut microbiota (Yao et al 2019), or liver (Yang et al 2020).…”

Section: Introductionmentioning

confidence: 99%

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Inhibition of Metamorphosis, Thyroid Gland, and Skeletal Ossification Induced by Hexavalent Chromium in Bufo gargarizans Larvae

Wang

Yang

Chen

et al. 2021

Enviro Toxic and Chemistry

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Hexavalent chromium (Cr [VI]) is one of the major detrimental heavy metal pollutants. In the present study, Bufo gargarizans were exposed to 0, 52, 104, 208, and 416 μg/L Cr (VI) from Gosner stage 2 until metamorphosis; and growth, development, and histological characteristics of the thyroid gland and skeletal ossification were examined. The results demonstrated that the survival rate of larvae exposed to Cr (VI) was not different from that measured in animals from the control group. However, high levels of Cr (VI) (104, 208, and 416 μg/L) were associated with significantly delayed growth and development. The suppression of skeletal ossification was observed at high Cr (VI) levels. Besides, histological alterations of the thyroid gland, such as follicular cell hyperplasia, colloid depletion, and peripheral colloid vacuolation, were found in 52 to 416 μg/L Cr (VI) treatments. The results of the present study highlight reductions in growth and development as well as percent metamorphosis and skeletal ossification due to histological alteration of the thyroid gland during exposure to Cr (VI) in B. gargarizans larvae. The present investigation could provide a basis for understanding the detrimental effects of Cr (VI) in amphibian larvae. Environ Toxicol Chem 2021;40:2474–2483. © 2021 SETAC

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“…Cadmium has also been shown to depress the cardiac function of Lithobates catesbeianus (Shaw, 1802) tadpoles as low as 1 µg/L (Dal- Medico et al, 2014). Similarly, chronic Pb exposure resulted in embryonic malformations and reduced metamorphosis rate in B. gargarizans (Chai et al, 2017;Yang et al, 2019). A study by Kaczor-Kamin ´ska et al (2020) found that Cd or Pb exposure affected the levels of compounds related to sulfur metabolism in various frog tissues.…”

Section: Introductionmentioning

confidence: 99%

Effects of Separate and Combined Exposure of Cadmium and Lead on the Endochondral Ossification in Bufo gargarizans

Chen

Deng

Song

et al. 2022

Enviro Toxic and Chemistry

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Cadmium (Cd) and lead (Pb) are ubiquitous in aquatic environments and most studies have examined the potential effects of Cd or Pb alone on aquatic organisms. In the present study, chronic effects of Cd and Pb, alone and in combination, on Bufo gargarizans were investigated by exposing embryos to these contaminants throughout metamorphosis. Significant reductions in body mass and snout-to-vent length were observed in B. gargarizans at Gosner stage 42 (Gs 42) and Gs 46 exposed to a Cd/Pb mixture. Single and combined exposure with Cd and Pb induced histological alterations of the thyroid gland characterized by reduced colloid area and thickness of epithelial cells. There was a significant decrease in the maximum jump distance of froglets exposed to Cd alone and the Cd/Pb mixture, and the jumping capacity showed a positive correlation with hind limb length and tibia/fibula. Moreover, single metals and their mixture induced reduction of endochondral bone formation in B. gargarizans. Transcriptomic and real-time quantitative polymerase chain reaction results showed that genes involved in skeletal ossification (TRα, TRβ, Dio2, Dio3, MMP9, MMP13, Runx1, Runx2, and Runx3) were transcriptionally dysregulated by Cd and Pb exposure alone or in combination. Our results suggested that despite the low concentration tested, the Cd/Pb mixture induced more severe impacts on B. gargarizans. In addition, the Cd/Pb mixture might reduce chances of survival for B. gargarizans froglets by decreasing size at metamorphosis, impaired skeletal ossification, and reduction in jumping ability, which might result from dysregulation of genes involved in thyroid hormone action and endochondral ossification. The findings obtained could add a new dimension to understanding of the mechanisms underpinning skeletal ossification response to heavy metals in amphibians.

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Chronic effects of lead on metamorphosis, development of thyroid gland, and skeletal ossification in Bufo gargarizans

Cited by 20 publications

References 64 publications

Agrochemicals disrupt multiple endocrine axes in amphibians

Agrochemicals disrupt multiple endocrine axes in amphibians

Inhibition of Metamorphosis, Thyroid Gland, and Skeletal Ossification Induced by Hexavalent Chromium in Bufo gargarizans Larvae

Effects of Separate and Combined Exposure of Cadmium and Lead on the Endochondral Ossification in Bufo gargarizans

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