Thyroid disrupting effects of halogenated and next generation chemicals on the swim bladder development of zebrafish

Godfrey, Amy; Hooser, Blair; Abdelmoneim, Ahmed; Horzmann, Katharine A.; Freeman, Jennifer L.; Sepúlveda, Marı́a S.

doi:10.1016/j.aquatox.2017.10.024

Cited by 78 publications

(42 citation statements)

References 33 publications

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“…This is exemplified through the physiological response of the swim bladder where males had no significant alterations, when the swim bladder did inflate, while females responded with either under (T 3 ) or over (MMI, TDCPP and PFOA) inflated swim bladders. In fish species, swim bladder development is under thyroid control, thus exposure to chemicals with thyroid disrupting effects might result in abnormal swim bladder development (Godfrey, Hooser, et al, ). Zebrafish larvae (6 dpf) exposed to the same set of halogenated compounds developed under‐inflated posterior swim bladders, representing a form of developmental impairment opposite to our observation in medaka (Godfrey, Hooser, et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…Medaka were exposed to sublethal concentrations based on the LC 50 values reported for zebrafish (Godfrey, Hooser, et al, ; TDCPP, 1.9 mg/L; PFOA, 473 mg/L; and PFBA, 13,795 mg/L) as no data were available for our model. However, before initiating exposures we compared the sensitivity of both fish species by exposing medaka to the zebrafish LC 50 values (Figure S1; see Supporting Information).…”

Section: Methodsmentioning

confidence: 99%

“…We also analyzed the expression of surfactant protein A ( sp‐a ) known as lectin mannose binding 2 ( lman2 ), surfactant protein B ( sp‐b ) known as prosaposin ( psap ), and surfactant protein C ( sp‐c ) known as tendomodulin ( tnmd ). These are proteins that prevent the swim bladder from deflating and are under thyroid control (Godfrey, Hooser, et al, ). We also analyzed the expression of estrogen receptors alpha and beta ( esrα , esrβ ) and vtg , which are important genes involved in the estrogen response.…”

Section: Methodsmentioning

confidence: 99%

“…A study conducted by Godfrey, Hooser, et al () showed zebrafish swim bladder developmental impairment after exposure to halogenated chemicals, while also showing that roughly 50% of exposed fish did not inflate a swim bladder. Assuming a 1:1 sex ratio, this suggests a possible sex‐specific response of the chemicals tested; however, sex could not be determined in these zebrafish larvae.…”

Section: Introductionmentioning

confidence: 99%

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Sex‐specific endocrine‐disrupting effects of three halogenated chemicals in Japanese medaka

Godfrey

Hooser

Abdelmoneim

et al. 2019

J of Applied Toxicology

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Several halogenated chemicals are found in an array of products that can cause endocrine disruption. Human studies have shown that endocrine responses are sex specific, with females more likely to develop hypothyroidism and males more likely to have reproductive impairment. The objective of this study was to assess sex differences on thyroid and estrogenic effects after exposure of Japanese medaka (Oryzias latipes, SK2MC) to halogenated compounds. This strain is an excellent model for these studies as sex can be determined non-destructively a few hours postfertilization. Medaka embryos were exposed to sublethal concentrations of Tris(1,3-dichloro-2-propyl) phosphate (TDCPP, 0.019 mg/L), perfluorooctanoic acid (PFOA, 4.7 mg/L) and its next generation alternative, perfluorobutyric acid (PFBA, 137 mg/L). Methimazole (inhibits thyroid hormone synthesis) and the thyroid hormone triiodothyronine served as reference controls. Fish were exposed throughout embryo development until 10 days postfertilization. Females displayed significantly larger swim bladders (which are under thyroid hormone control) after exposure to all chemicals with the exception of triiodothyronine, which caused the opposite effect. Females exposed to TDCPP and PFOA had increased expression of vitellogenin and exposure to PFOA upregulated expression of multiple thyroidrelated genes. Upregulation of estrogenic-regulated genes after exposure to TDCPP, PFOA and methimazole was only observed in males. Overall, our results suggest that females and males show an estrogenic response when exposed to these halogenated chemicals and that females appear more susceptible to thyroid-induced swim bladder dysfunction compared with males. These results further confirm the importance of considering sex effects when assessing the toxicity of endocrine-disrupting compounds.

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Sex‐specific endocrine‐disrupting effects of three halogenated chemicals in Japanese medaka

Godfrey

Hooser

Abdelmoneim

et al. 2019

J of Applied Toxicology

Self Cite

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“…In the zebrafish, swim bladder inflation is dependent on THs (Godfrey et al, 2017;Liu and Chan, 2002). The posterior chamber of the swim bladder inflates around 4.5dpf while the anterior chamber inflates by 21dpf (Winata et al, 2009).…”

Section: Discussionmentioning

confidence: 99%

Zebrafishduoxmutations provide a model for human congenital hypothyroidism

Chopra

Ishibashi

Amaya

2018

Preprint

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Thyroid dyshormonogenesis is a leading cause of congenital hypothyroidism, a highly prevalent but treatable condition. Thyroid hormone synthesis is dependent on the formation of reactive oxygen species (ROS). In humans, the primary sources for ROS production during thyroid hormone synthesis are the NADPH oxidase, DUOX1 and DUOX2. Indeed mutations in DUOX1 and DUOX2 have been linked with congenital hypothyroidism. Unlike humans, zebrafish has a single orthologue for DUOX1 and DUOX2. In this study, we investigated the phenotypes associated with two nonsense mutant alleles of the single duox gene in zebrafish, sa9892 and sa13017. Both alleles gave rise to readily observable phenotypes reminiscent of congenital hypothyroidism, from the larval stages through to adulthood. By using various methods to examine the external and internal phenotypes, we discovered a strong correlation between TH synthesis and duox function, beginning from the early larval stage, when T 4 levels are already noticeably absent in the mutants. Loss of T 4 production resulted in growth retardation, pigmentation defects, ragged fins, thyroid hyperplasia / external goiter, and infertility. Remarkably all of these defects associated with chronic congenital hypothyroidism could be rescued with T 4 treatment, even when initiated when the fish had already reached adulthood. Our work suggests that these zebrafish duox mutants may provide a powerful model to understand the aetiology of untreated and treated congenital hypothyroidism even in advance stages of development.

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Reversibility of Thyroid Hormone System–Disrupting Effects on Eye and Thyroid Follicle Development in Zebrafish (Danio rerio) Embryos

Pannetier

Poulsen

Gölz

et al. 2023

Enviro Toxic and Chemistry

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Early vertebrate development is partially regulated by thyroid hormones (THs). Environmental pollutants that interact with the TH system (TH system–disrupting chemicals [THSDCs]) can have massively disrupting effects on this essential phase. Eye development of fish is directly regulated by THs and can, therefore, be used as a thyroid‐related endpoint in endocrine disruptor testing. To evaluate the effects of THSDC‐induced eye malformations during early development, zebrafish (Danio rerio) embryos were exposed for 5 days postfertilization (dpf) to either propylthiouracil, a TH synthesis inhibitor, or tetrabromobisphenol A, which interacts with TH receptors. Subsequently, one half of the embryos were exposed further to the THSDCs until 8 dpf, while the other half of the embryos were raised in clean water for 3 days to check for reversibility of effects. Continued THSDC exposure altered eye size and pigmentation and induced changes in the cellular structure of the retina. This correlated with morphological alterations of thyroid follicles as revealed by use of a transgenic zebrafish line. Interestingly, effects were partly reversible after a recovery period as short as 3 days. Results are consistent with changes in TH levels measured in different tissues of the embryos, for example, in the eyes. The results show that eye development in zebrafish embryos is very sensitive to THSDC treatment but able to recover quickly from early exposure by effective repair mechanisms. Environ Toxicol Chem 2023;42:1276–1292. © 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

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Thyroid disrupting effects of halogenated and next generation chemicals on the swim bladder development of zebrafish

Cited by 78 publications

References 33 publications

Sex‐specific endocrine‐disrupting effects of three halogenated chemicals in Japanese medaka

Sex‐specific endocrine‐disrupting effects of three halogenated chemicals in Japanese medaka

Zebrafishduoxmutations provide a model for human congenital hypothyroidism

Reversibility of Thyroid Hormone System–Disrupting Effects on Eye and Thyroid Follicle Development in Zebrafish (Danio rerio) Embryos

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