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

Pauline Pannetier; Rikke Poulsen; Lisa Gölz; Sara Coordes; Hanna Stegeman; Johannes Koegst; Luisa Reger; Thomas Braunbeck; Martin Hansen; Lisa Baumann

doi:10.1002/etc.5608

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

Pauline Pannetier
, Rikke Poulsen
, Lisa Gölz
, Sara Coordes
, Hanna Stegeman
, Johannes Koegst
, Luisa Reger
, Thomas Braunbeck
, Martin Hansen
, Lisa Baumann^*

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

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.

Original language	English
Pages (from-to)	1276-1292
Number of pages	17
Journal	Environmental toxicology and chemistry
Volume	42
Issue number	6
Early online date	15 Mar 2023
DOIs	https://doi.org/10.1002/etc.5608
Publication status	Published - Jun 2023

Bibliographical note

Funding Information:
We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors’ view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et moléculaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF‐T‐2017‐FLS‐7‐4) and a Carlsberg Foundation Research Infrastructure grant (CF20‐0422). ©

Funding Information:
We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors’ view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et moléculaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide© for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF-T-2017-FLS-7-4) and a Carlsberg Foundation Research Infrastructure grant (CF20-0422).

Publisher Copyright:
© 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Funding

We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors’ view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et moléculaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF‐T‐2017‐FLS‐7‐4) and a Carlsberg Foundation Research Infrastructure grant (CF20‐0422). © We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors’ view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et moléculaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide© for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF-T-2017-FLS-7-4) and a Carlsberg Foundation Research Infrastructure grant (CF20-0422).

Funders	Funder number
Universität Heidelberg
Institut de Recherche Interdisciplinaire en Biologie Humaine et Moléculaire
European Commission
ERGO
Horizon 2020
Horizon 2020 Framework Programme	825753
Aarhus Universitets Forskningsfond	AUFF‐T‐2017‐FLS‐7‐4
Carlsbergfondet	CF20‐0422

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

SDG 14 Life Below Water

Keywords

Endocrine disruptors
Flame retardant
Histopathology
Propylthiouracil (PTU)
Tetrabromobisphenol A (TBBPA)
Transgenic line

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10.1002/etc.5608Licence: CC BY-NC-ND

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

abstract = "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.",

keywords = "Endocrine disruptors, Flame retardant, Histopathology, Propylthiouracil (PTU), Tetrabromobisphenol A (TBBPA), Transgenic line",

author = "Pauline Pannetier and Rikke Poulsen and Lisa G{\"o}lz and Sara Coordes and Hanna Stegeman and Johannes Koegst and Luisa Reger and Thomas Braunbeck and Martin Hansen and Lisa Baumann",

note = "Funding Information: We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors{\textquoteright} view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et mol{\'e}culaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF‐T‐2017‐FLS‐7‐4) and a Carlsberg Foundation Research Infrastructure grant (CF20‐0422). {\textcopyright} Funding Information: We acknowledge funding from the European Union's Horizon 2020 research and innovation program (grant 825753 [ERGO]). The present study reflects only the authors{\textquoteright} view, and the European Union cannot be held responsible for any use that may be made of the information contained therein. Thanks are due to the Costagliola laboratory at the Institut de Recherche interdisciplinaire en Biologie Humaine et mol{\'e}culaire (Brussels, Belgium) for providing the transgenic zebrafish line used in the present study, Biobide{\textcopyright} for providing the initial protocol for analyses of the transgenic zebrafish, and S. Rupp for final establishment of the protocol. We thank P. Matthiessen for critically reading the manuscript. Lisa Baumann is grateful to the “Olympia Morata Program” of the Office of Equal Opportunities, University of Heidelberg. Martin Hansen acknowledges a financial starting grant from Aarhus University Research Foundation (AUFF-T-2017-FLS-7-4) and a Carlsberg Foundation Research Infrastructure grant (CF20-0422). Publisher Copyright: {\textcopyright} 2023 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.",

year = "2023",

month = jun,

doi = "10.1002/etc.5608",

language = "English",

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AU - Gölz, Lisa

AU - Coordes, Sara

AU - Stegeman, Hanna

AU - Koegst, Johannes

AU - Reger, Luisa

AU - Braunbeck, Thomas

AU - Hansen, Martin

AU - Baumann, Lisa

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KW - Flame retardant

KW - Histopathology

KW - Propylthiouracil (PTU)

KW - Tetrabromobisphenol A (TBBPA)

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

Abstract

Bibliographical note

Funding

UN SDGs

Keywords

Access to Document

Persistent URL (handle)

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