Deiodinase inhibition impairs the formation of the three posterior swim bladder tissue layers during early embryonic development in zebrafish

Aquatic Toxicology - Tập 261 - Trang 106632 - 2023
Imke Van Dingenen1, Lucia Vergauwen1, Ann-Cathrin Haigis1, Brett R. Blackwell2, Emma Stacy2, Daniel L. Villeneuve2, Dries Knapen1
1Zebrafishlab, Veterinary Physiology and Biochemistry, Department of Veterinary Sciences, University of Antwerp, Universiteitsplein 1, Wilrijk 2610, Belgium
2United States Environmental Protection Agency, Great Lakes Toxicology and Ecology Division, Duluth, MN 55804, United States

Tài liệu tham khảo

Alt, 2006, Analysis of origin and growth of the thyroid gland in zebrafish, Dev. Dyn., 235, 1872, 10.1002/dvdy.20831 Arrojo, 2013, Role of the type 2 iodothyronine deiodinase (D2) in the control of thyroid hormone signaling, Biochim. Biophys. Acta, 1830, 3956, 10.1016/j.bbagen.2012.08.019 Bagci, 2015, Deiodinase knockdown during early zebrafish development affects growth, development, energy metabolism, motility and phototransduction, PLoS One, 10, 10.1371/journal.pone.0123285 Baumann, 2016, Thyroid disruption in zebrafish (Danio rerio) larvae: different molecular response patterns lead to impaired eye development and visual functions, Aquat. Toxicol., 172, 44, 10.1016/j.aquatox.2015.12.015 Becker, 1997, The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles, Endocrinology, 138, 2989, 10.1210/endo.138.7.5272 Bianco, 2006, Deiodinases: implications of the local control of thyroid hormone action, J. Clin. Invest., 116, 2571, 10.1172/JCI29812 Blanton, 2007, The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction, Crit. Rev. Toxicol., 37, 97, 10.1080/10408440601123529 Bouzaffour, 2010, Implication of type 3 deiodinase induction in zebrafish fin regeneration, Gen. Comp. Endocrinol., 168, 88, 10.1016/j.ygcen.2010.04.006 Cai, 2004, Expression of type II iodothyronine deiodinase marks the time that a tissue responds to thyroid hormone-induced metamorphosis in Xenopus laevis, Dev. Biol., 266, 87, 10.1016/j.ydbio.2003.10.005 Campos-Barros, 2000, Type 2 iodothyronine deiodinase expression in the cochlea before the onset of hearing, Proc. Natl Acad. Sci., 97, 1287, 10.1073/pnas.97.3.1287 Cavallin, 2017, Impaired swim bladder inflation in early life stage fathead minnows exposed to a deiodinase inhibitor, iopanoic acid, Environ. Toxicol. Chem., 36, 2942, 10.1002/etc.3855 Chang, 2012, Changes in thyroid hormone levels during zebrafish development, Zool. Sci., 29, 181, 10.2108/zsj.29.181 Chu, 2009, New school in liver development: lessons from zebrafish, Hepatology, 50, 1656, 10.1002/hep.23157 Darras, 1999, Regulation of thyroid hormone metabolism during fetal development, Mol. Cell. Endocrinol., 151, 37, 10.1016/S0303-7207(99)00088-X de Escobar, 2004, Role of thyroid hormone during early brain development, Eur. J. Endocrinol., 151, U25, 10.1530/eje.0.151u025 Dentice, 2007, Sonic hedgehog-induced type 3 deiodinase blocks thyroid hormone action enhancing proliferation of normal and malignant keratinocytes, Proc. Natl Acad. Sci., 104, 14466, 10.1073/pnas.0706754104 Dentice, 2012, Beta-Catenin regulates deiodinase levels and thyroid hormone signaling in colon cancer cells, Gastroenterology, 143, 1037, 10.1053/j.gastro.2012.06.042 Desouza, 2011, Thyroid hormone regulates the expression of the sonic hedgehog signaling pathway in the embryonic and adult Mammalian brain, Endocrinology, 152, 1989, 10.1210/en.2010-1396 Dong, 2013, Using whole mount in situ hybridization to examine thyroid hormone deiodinase expression in embryonic and larval zebrafish: a tool for examining OH-BDE toxicity to early life stages, Aquat. Toxicol., 132-133, 190, 10.1016/j.aquatox.2013.02.008 Ely, 2018, Wnt signaling in thyroid homeostasis and carcinogenesis, Genes, 9, 10.3390/genes9040204 Fang, 2022, Tpo knockout in zebrafish partially recapitulates clinical manifestations of congenital hypothyroidism and reveals the involvement of TH in proper development of glucose homeostasis, Gen. Comp. Endocrinol., 323-324, 10.1016/j.ygcen.2022.114033 Finney, 2006, Structure and autonomic innervation of the swim bladder in the zebrafish (Danio rerio), J. Comp. Neurol., 495, 587, 10.1002/cne.20948 Gölz, 2022, AOP report: thyroperoxidase inhibition leading to altered visual function in fish via altered retinal layer structure, Environ. Toxicol. Chem., 41, 2632, 10.1002/etc.5452 Goolish, 1999, Lack of gas bladder inflation by the larvae of zebrafish in the absence of an air–water interface, J. Fish Biol., 55, 1054 Hagenaars, 2014, PFOS affects posterior swim bladder chamber inflation and swimming performance of zebrafish larvae, Aquat. Toxicol., 157, 225, 10.1016/j.aquatox.2014.10.017 Hasebe, 2008, Thyroid hormone-up-regulated hedgehog interacting protein is involved in larval-to-adult intestinal remodeling by regulating sonic hedgehog signaling pathway in Xenopus laevis, Dev. Dyn., 237, 3006, 10.1002/dvdy.21698 Haselman, 2022, Characterization of the mechanistic linkages between iodothyronine deiodinase inhibition and impaired thyroid-mediated growth and development in Xenopus laevis using iopanoic acid, Toxicol. Sci., 187, 139, 10.1093/toxsci/kfac014 Huang, 2001, Timing of metamorphosis and the onset of the negative feedback loop between the thyroid gland and the pituitary is controlled by type II iodothyronine deiodinase in Xenopus laevis, Proc. Natl Acad. Sci., 98, 7348, 10.1073/pnas.131198998 Huang, 2011, The thyroid hormone degrading type 3 deiodinase is the primary deiodinase active in murine epidermis, Thyroid, 21, 1263, 10.1089/thy.2011.0105 Ishizuya-Oka, 2001, Thyroid hormone-induced expression of Sonic hedgehog correlates with adult epithelial development during remodeling of the Xenopus stomach and intestine, Differentiation, 96, 27, 10.1046/j.1432-0436.2001.690103.x Jones, 2017, Negative feedback regulation of thyrotropin subunits and pituitary deiodinases in red drum, Sciaenops ocellatus, Gen. Comp. Endocrinol., 240, 19, 10.1016/j.ygcen.2016.09.003 Kaplan, 1980, Phenolic and tyrosyl ring deiodination of iodothyronines in rat brain homogenates, J. Clin. Invest., 66, 551, 10.1172/JCI109887 Knapen, 2020, Toward an AOP network-based tiered testing strategy for the assessment of thyroid hormone disruption, Environ. Sci. Technol., 54, 8491, 10.1021/acs.est.9b07205 Korzh, 2011, The interaction of epithelial Ihha and mesenchymal Fgf10 in zebrafish esophageal and swimbladder development, Dev. Biol., 359, 262, 10.1016/j.ydbio.2011.08.024 Li, 2012, Phenylthiourea specifically reduces zebrafish eye size, PLoS One, 7, e40132, 10.1371/journal.pone.0040132 Lindsey, 2010, From inflation to flotation: contribution of the swimbladder to whole-body density and swimming depth during development of the zebrafish (Danio rerio), Zebrafish, 7, 85, 10.1089/zeb.2009.0616 Liu, 2008, Serum thyroid hormone levels may not accurately reflect thyroid tissue levels and cardiac function in mild hypothyroidism, Am. J. Physiol. Heart Circ. Physiol., 294, 10.1152/ajpheart.01379.2007 Michiels, 2017, Evaluating complex mixtures in the zebrafish embryo by reconstituting field water samples: a metal pollution case study, Int. J. Mol. Sci., 18, 10.3390/ijms18030539 Muller, 2014, Tissue-specific alterations in thyroid hormone homeostasis in combined Mct10 and Mct8 deficiency, Endocrinology, 155, 315, 10.1210/en.2013-1800 Nelson, 2016, Impaired anterior swim bladder inflation following exposure to the thyroid peroxidase inhibitor 2-mercaptobenzothiazole part I: fathead minnow, Aquat. Toxicol., 173, 192, 10.1016/j.aquatox.2015.12.024 2013 Peeters, 2005, Tissue thyroid hormone levels in critical illness, J. Clin. Endocrinol. Metab., 90, 6498, 10.1210/jc.2005-1013 Reider, 2014, Effects of low-dose embryonic thyroid disruption and rearing temperature on the development of the eye and retina in zebrafish, Birth Defects Res. B Dev. Reprod. Toxicol., 101, 347, 10.1002/bdrb.21118 Renko, 2015, An improved nonradioactive screening method identifies genistein and xanthohumol as potent inhibitors of iodothyronine deiodinases, Thyroid, 25, 962, 10.1089/thy.2015.0058 Robertson, 2007, Development of the swimbladder and its innervation in the zebrafish, Danio rerio, J. Morphol., 268, 967, 10.1002/jmor.10558 Sharma, 2016, Effects of thyroid endocrine manipulation on sex-related gene expression and population sex ratios in zebrafish, Gen. Comp. Endocrinol., 235, 38, 10.1016/j.ygcen.2016.05.028 Skah, 2017, The thyroid hormone nuclear receptors and the Wnt/beta-catenin pathway: an intriguing liaison, Dev. Biol., 422, 71, 10.1016/j.ydbio.2017.01.003 Stinckens, 2016, Impaired anterior swim bladder inflation following exposure to the thyroid peroxidase inhibitor 2-mercaptobenzothiazole part II: Zebrafish, Aquat. Toxicol., 173, 204, 10.1016/j.aquatox.2015.12.023 Stinckens, 2018, An AOP-based alternative testing strategy to predict the impact of thyroid hormone disruption on swim bladder inflation in Zebrafish, Aquat. Toxicol., 200, 1, 10.1016/j.aquatox.2018.04.009 Stinckens, 2020, Effect of thyroperoxidase and deiodinase inhibition on anterior swim bladder inflation in the Zebrafish, Environ. Sci. Technol., 54, 6213, 10.1021/acs.est.9b07204 Tang, 2007, Validation of Zebrafish (Danio rerio) reference genes for quantitative real-time RT-PCR normalization, Acta Biochim. Biophys. Sin., 39, 384, 10.1111/j.1745-7270.2007.00283.x Tao, 2009, Liver development in Zebrafish (Danio rerio), J. Genet. Genomics, 36, 325, 10.1016/S1673-8527(08)60121-6 Umezawa, 2012, O2-filled swimbladder employs monocarboxylate transporters for the generation of O2 by lactate-induced root effect hemoglobin, PLoS One, 7, e34579, 10.1371/journal.pone.0034579 van der Spek, 2017, The classic pathways of thyroid hormone metabolism, Mol. Cell. Endocrinol., 458, 29, 10.1016/j.mce.2017.01.025 Vandesompele, 2002, Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes, Genome Biol., 3, 1, 10.1186/gb-2002-3-7-research0034 Vergauwen, 2018, Gene transcription ontogeny of hypothalamic-pituitary-thyroid axis development in early-life stage fathead minnow and Zebrafish, Gen. Comp. Endocrinol., 266, 87, 10.1016/j.ygcen.2018.05.001 Vergauwen, L., Stinckens, E., Villeneuve, D.L., Knapen, D. (2022a). Deiodinase 1 inhibition leading to increased mortality via reduced anterior swim bladder inflation, OECD Series on Adverse Outcome Pathways, No. 25, OECD Publishing, Paris. doi:10.1787/9f651c16-en. Vergauwen, L., Stinckens, E., Villeneuve, D.L., Knapen, D. (2022b). Deiodinase 1 inhibition leading to increased mortality via reduced posterior swim bladder inflation, OECD Series on Adverse Outcome Pathways, No. 24, OECD Publishing, Paris. doi:10.1787/9cb525e9-en. Vergauwen, L., Stinckens, E., Villeneuve, D.L., Knapen, D. (2022c). Deiodinase 2 inhibition leading to increased mortality via reduced anterior swim bladder inflation, OECD Series on Adverse Outcome Pathways, No. 23, OECD Publishing, Paris. doi:10.1787/b1bf0bea-en. Vergauwen, L., Stinckens, E., Villeneuve, D.L., Knapen, D. (2022d). Deiodinase 2 inhibition leading to increased mortality via reduced posterior swim bladder inflation, OECD Series on Adverse Outcome Pathways, No. 22, OECD Publishing, Paris. doi:10.1787/dc406014-en. Vergauwen, L., Stinckens, E., Villeneuve, D.L., Knapen, D. (2022e). Thyroperoxidase inhibition leading to increased mortality via reduced anterior swim bladder inflation, OECD Series on Adverse Outcome Pathways, No. 26, OECD Publishing, Paris. doi:10.1787/447c5cba-en. Villeneuve, 2014, Investigating alternatives to the fish early-life stage test: a strategy for discovering and annotating adverse outcome pathways for early fish development, Environ. Toxicol. Chem., 33, 158, 10.1002/etc.2403 Walpita, 2007, The effect of 3,5,3′-triiodothyronine supplementation on zebrafish (Danio rerio) embryonic development and expression of iodothyronine deiodinases and thyroid hormone receptors, Gen. Comp. Endocrinol., 152, 206, 10.1016/j.ygcen.2007.02.020 Walter, 2019, Effects of thyroid hormone disruption on the ontogenetic expression of thyroid hormone signaling genes in developing Zebrafish (Danio rerio), Gen. Comp. Endocrinol., 272, 20, 10.1016/j.ygcen.2018.11.007 Winata, 2009, Development of Zebrafish swimbladder: the requirement of Hedgehog signaling in specification and organization of the three tissue layers, Dev. Biol., 331, 222, 10.1016/j.ydbio.2009.04.035 Xing, 2014, Epiphyseal chondrocyte secondary ossification centers require thyroid hormone activation of Indian hedgehog and osterix signaling, J. Bone Miner. Res., 29, 2262, 10.1002/jbmr.2256 Yin, 2011, Wnt signaling is required for early development of Zebrafish swimbladder, PLoS One, 6, e18431, 10.1371/journal.pone.0018431 Yin, 2012, Perturbation of Zebrafish swimbladder development by enhancing Wnt signaling in Wif1 morphants, Biochim. Biophys. Acta, 1823, 236, 10.1016/j.bbamcr.2011.09.018 Zheng, 2011, Comparative transcriptome analyses indicate molecular homology of Zebrafish swimbladder and mammalian lung, PLoS One, 6, e24019, 10.1371/journal.pone.0024019