Developmental toxicity of the PBDE metabolite 6-OH-BDE-47 in zebrafish and the potential role of thyroid receptor β

Aquatic Toxicology

Volumn 168, Issue , 2015, Pages 38-47

  Macaulay, Laura J ^a   Chen, Albert ^a   Rock, Kylie D ^a   Dishaw, Laura V ^a   Dong, Wu ^a   Hinton, David E ^a   Stapleton, Heather M ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Development; Metabolite; OH BDE; PBDE; Thyroid receptor; Zebrafish

Indexed keywords

6 HYDROXY 2,2',4,4' TETRABROMODIPHENYL ETHER; IOPANOIC ACID; LIOTHYRONINE; MESSENGER RNA; POLYBROMINATED DIPHENYL ETHER; PROPYLTHIOURACIL; RECEPTOR; THYROID HORMONE; THYROID RECEPTOR BETA; UNCLASSIFIED DRUG; 6-OH-BDE-47; POLYBROMINATED BIPHENYL; THYROID HORMONE RECEPTOR BETA; WATER POLLUTANT;

CHEMICAL POLLUTANT; CYPRINID; EMBRYO; FERTILIZATION (REPRODUCTION); HORMONE; METABOLITE; PBDE; TOXICITY;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY HEIGHT; CELL CYCLE; CONTROLLED STUDY; CRANIOFACIAL MALFORMATION; DEVELOPMENTAL TOXICITY; DOWN REGULATION; EMBRYO; HORMONAL REGULATION; IN VIVO STUDY; JAW MALFORMATION; LARVA; NONHUMAN; PIGMENTATION; PRIORITY JOURNAL; ZEBRA FISH; ANIMAL; DRUG EFFECTS; METABOLISM; NONMAMMALIAN EMBRYO; PHYSIOLOGY; THYROID GLAND; TOXICITY; WATER POLLUTANT;

DANIO RERIO;

ANIMALS; EMBRYO, NONMAMMALIAN; POLYBROMINATED BIPHENYLS; THYROID GLAND; THYROID HORMONE RECEPTORS BETA; THYROID HORMONES; TRIIODOTHYRONINE; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84943155561     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2015.09.007     Document Type: Article

References (69)

1. Abdelouahab N., Langlois M.-F., Lavoie L., Corbin F., Pasquier J.-C., Takser L. Maternal and cord-blood thyroid hormone levels and exposure to polybrominated diphenyl ethers and polychlorinated biphenyls during early pregnancy. Am. J. Epidemiol. 2013, 178:701-713. 10.1093/aje/kwt141.
2. Bohnsack B.L., Kahana A. Thyroid hormone and retinoic acid interact to regulate zebrafish craniofacial neural crest development. Dev. Biol. 2013, 373:300-309. 10.1016/j.ydbio.2012.11.005.
3. Bouzaffour M., Rampon C., Ramaugé M., Courtin F., Vriz S. Implication of type 3 deiodinase induction in zebrafish fin regeneration. Gen. Comp. Endocrinol. 2010, 168:88-94. 10.1016/j.ygcen.2010.04.006.
4. Brown D.D. The role of thyroid hormone in zebrafish and axolotl development. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:13011-13016.
5. Butt C., Stapleton H.M. Inhibition of thyroid hormone sulfotransferase activity by brominated flame retardants and halogenated phenolics. Chem. Res. Toxicol. 2013, 26(11):1692-1702. 10.1021/tx400342k.
6. Butt C.M., Wang D., Stapleton H.M. Halogenated phenolic contaminants inhibit the in vitro activity of the thyroid-regulating deiodinases in human liver. Toxicol. Sci. 2011, 124(2):339-347. 10.1093/toxsci/kfr117.
7. Chen A., Park J.-S., Linderholm L., Rhee A., Petreas M., DeFranco E.A., Dietrich K.N., Ho S.-M. Hydroxylated polybrominated diphenyl ethers in paired maternal and cord sera. Environ. Sci. Technol. 2013, 47:3902-3908. 10.1021/es3046839.
8. Chevrier J., Harley K.G., Bradman A., Sjödin A., Eskenazi B. Prenatal exposure to polybrominated diphenyl ether flame retardants and neonatal thyroid-stimulating hormone levels in the CHAMACOS study. Am. J. Epidemiol. 2011, 174:1166-1174. 10.1093/aje/kwr223.
9. Darras V.M., Houbrechts A.M., Van Herck S.L.J. Intracellular thyroid hormone metabolism as a local regulator of nuclear thyroid hormone receptor-mediated impact on vertebrate development. Biochim. Biophys. Acta 2014, 1849:130-141. 10.1016/j.bbagrm.2014.05.004.
10. Darras V.M., Van Herck S.L.J., Heijlen M., De Groef B. Thyroid hormone receptors in two model species for vertebrate embryonic development: chicken and zebrafish. J. Thyroid Res. 2011, 2011:402320. 10.4061/2011/402320.
11. Dingemans M.M.L., de Groot A., van Kleef R.G.D.M., Bergman A., van den Berg M., Vijverberg H.P.M., Westerink R.H.S. Hydroxylation increases the neurotoxic potential of BDE-47 to affect exocytosis and calcium homeostasis in PC12 cells. Environ. Health Perspect. 2008, 116:637-643. 10.1289/ehp.11059.
12. Dingemans M.M.L., van den Berg M., Bergman A., Westerink R.H.S. Calcium-related processes involved in the inhibition of depolarization-evoked calcium increase by hydroxylated PBDEs in PC12 cells. Toxicol. Sci. 2010, 114:302-309. 10.1093/toxsci/kfp310.
13. Dingemans M.M.L., van den Berg M., Westerink R.H.S. Neurotoxicity of brominated flame retardants: (in) direct effects of parent and hydroxylated polybrominated diphenyl ethers on the (developing) nervous system. Environ. Health Perspect. 2011, 119:900-907. 10.1289/ehp.1003035.
14. Dong W., Macaulay L.J., Ferguson P.L.L., Hinton D.E., Stapleton H.M., Kwok K.W., Hinton D.E., Ferguson P.L.L., Stapleton H.M. The PBDE metabolite 6-OH-BDE 47 affects melanin pigmentation and THRβ MRNA expression in the eye of zebrafish embryos. Disruptors 2014, e969072. (in press). 10.4161/23273739.2014.969072.
15. Dong W., Macaulay L.J., Kwok K.W.H., Hinton D.E., Stapleton H.M. 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. 2013, 132-133:190-199. 10.1016/j.aquatox.2013.02.008.
16. Erratico C.A., Moffatt S.C., Bandiera S.M. Comparative oxidative metabolism of BDE-47 and BDE-99 by rat hepatic microsomes. Toxicol. Sci. 2011, 123:37-47. 10.1093/toxsci/kfr155.
17. Essner J.J., Breuer J.J., Essner R.D., Fahrenkrug S.C., Hackett P.B. The zebrafish thyroid hormone receptor alpha 1 is expressed during early embryogenesis and can function in transcriptional repression. Differentiation 1997, 62:107-117. 10.1046/j.1432-0436.1997.6230107.x.
18. Feo M.L., Gross M.S., McGarrigle B.P., Eljarrat E., Barceló D., Aga D.S., Olson J.R. Biotransformation of BDE-47 to potentially toxic metabolites is predominantly mediated by human CYP2B6. Environ. Health Perspect. 2013, 121:440-446. 10.1289/ehp.1205446.
19. Hamers T., Kamstra J.H., Sonneveld E., Murk A.J., Visser T.J., Van Velzen M.J.M., Brouwer A., Bergman A. Biotransformation of brominated flame retardants into potentially endocrine-disrupting metabolites, with special attention to 2,2,4,4'-tetrabromodiphenyl ether (BDE-47). Mol. Nutr. Food Res. 2008, 52:284-298. 10.1002/mnfr.200700104.
20. Heijlen M., Houbrechts A.M., Bagci E., Van Herck S.L.J., Kersseboom S., Esguerra C.V., Blust R., Visser T.J., Knapen D., Darras V.M. Knockdown of type 3 iodothyronine deiodinase severely perturbs both embryonic and early larval development in zebrafish. Endocrinology 2014, 155:1547-1559. 10.1210/en.2013-1660.
21. Howdeshell K.L. A model of the development of the brain as a construct of the thyroid system. Environ. Health Perspect. 2002, 110:337-348.
22. Ibhazehiebo K., Iwasaki T., Kimura-Kuroda J., Miyazaki W., Shimokawa N., Koibuchi N. Disruption of thyroid hormone receptor-mediated transcription and thyroid hormone-induced Purkinje cell dendrite arborization by polybrominated diphenyl. Environ. Health Perspect. 2011, 119:168-175.
23. Jegstrup I.M., Rosenkilde P. Regulation of post-larval development in the European eel: thyroid hormone level, progress of pigmentation and changes in behaviour. J. Fish Biol. 2003, 63:168-175. 10.1046/j.1095-8649.2003.00138.x.
24. Kelly B.C., Blair J.D., Gobas F.A.P.C., Ikonomou M.G. Hydroxylated and methoxylated polybrominated diphenyl ethers in a Canadian Arctic marine food web. Environ. Sci. Technol. 2008, 42:7069-7077.
25. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Dev. Dyn. 1995, 203:253-310. 10.1002/aja.1002030302.
26. Kitamura S., Shinohara S., Iwase E., Sugihara K., Uramaru N., Shigematsu H., Fujimoto N., Ohta S. Affinity for thyroid hormone and estrogen receptors of hydroxylated polybrominated diphenyl ethers. J. Health Sci. 2008, 54:607-614.
27. Kojima H., Takeuchi S., Uramaru N., Sugihara K., Yoshida T., Kitamura S. Nuclear hormone receptor activity of polybrominated diphenyl ethers and their hydroxylated and methoxylated metabolites in transactivation assays using Chinese hamster ovary cells. Environ. Health Perspect. 2009, 117:1210-1218. 10.1289/ehp.0900753.
28. Legradi J., Dahlberg A.-K., Cenijn P., Marsh G., Asplund L., Bergman A., Legler J. Disruption of oxidative phosphorylation (OXPHOS) by hydroxylated polybrominated diphenyl ethers (OH-PBDEs) present in the marine environment. Environ. Sci. Technol. 2014, 48:14703-14711. 10.1021/es5039744.
29. Lema S.C., Dickey J.T., Schultz I.R., Swanson P. Dietary exposure to 2,2,4,4'-tetrabromodiphenyl ether (PBDE-47) alters thyroid status and thyroid hormone-regulated gene transcription in the pituitary and brain. Environ. Health Perspect. 2008, 116:1694-1699. 10.1289/ehp.11570.
30. Li F., Xie Q., Li X., Li N., Chi P., Chen J., Wang Z., Hao C. Hormone activity of hydroxylated polybrominated diphenyl ethers on human thyroid receptor-beta: in vitro and in silico investigations. Environ. Health Perspect. 2010, 118:602-606. 10.1289/ehp.0901457.
31. Li, T., Wang, W., Pan, Y.-W., Xu, L., Xia, Z., 2013. A hydroxylated metabolite of flame-retardant PBDE-47 decreases the survival, proliferation, and neuronal differentiation of primary cultured adult neural stem cells and interferes with signaling of ERK5 MAP kinase and neurotrophin 3. Toxicol. Sci. 134, 111-24, . http://10.1093/toxsci/kft083.
32. Liu H., Tang S., Zheng X., Zhu Y., Ma Z., Liu C., Hecker M.M., Saunders D.M.V., Giesy J.P., Zhang X., Yu H. Bioaccumulation, biotransformation and toxicity of BDE-47, 6-OH-BDE-47 and 6-MeO-BDE-47 in early life-stages of zebrafish (Danio rerio). Environ. Sci. Technol. 2015, 49:1823-1833. 10.1021/es503833q.
33. Liu Y.-W., Chan W.-K. Thyroid hormones are important for embryonic to larval transitory phase in zebrafish. Differentiation 2002, 70:36-45. 10.1046/j.1432-0436.2002.700104.x.
34. Liu Y.W., Lo L.J., Chan W.K. Temporal expression and T3 induction of thyroid hormone receptors alpha1 and beta1 during early embryonic and larval development in zebrafish, Danio rerio. Mol. Cell. Endocrinol. 2000, 159:187-195.
35. McMenamin S.K., Parichy D.M. Metamorphosis in teleosts. Curr. Top. Dev. Biol. 2013, 103:127-165. 10.1016/B978-0-12-385979-25-8.
36. Meerts I.A., Letcher R.J., Hoving S., Marsh G., Bergman A., Lemmen J.G., van der Burg B., Brouwer A. In vitro estrogenicity of polybrominated diphenyl ethers, hydroxylated PDBEs, and polybrominated bisphenol A compounds. Environ. Health Perspect. 2001, 109:399-407.
37. Meerts I.A., van Zanden J.J., Luijks E.A., van Leeuwen-Bol I., Marsh G., Jakobsson E., Bergman A., Brouwer A. Potent competitive interactions of some brominated flame retardants and related compounds with human transthyretin in vitro. Toxicol. Sci. 2000, 56:95-104.
38. Miwa S., Tagawa M., Inui Y., Hirano T. Thyroxine surge in metamorphosing flounder larvae. Gen. Comp. Endocrinol. 1988, 70:158-163. 10.1016/0016-6480(88)90105-0.
39. Morvan-Dubois G., Fini J.B., Demeneix B.A. Is thyroid hormone signaling relevant for vertebrate embryogenesis?. Curr. Top. Dev. Biol. 2013, 103:365-396. 10.1016/B978-0-12-385979-213-7.
40. Mukhi S., Patiño R. Effects of prolonged exposure to perchlorate on thyroid and reproductive function in zebrafish. Toxicol. Sci. 2007, 96:246-254. 10.1093/toxsci/kfm001.
41. Nelson E.R., Habibi H.R. Thyroid receptor subtypes: structure and function in fish. Gen. Comp. Endocrinol. 2009, 161:90-96. 10.1016/j.ygcen.2008.09.006.
42. Nomiyama K., Eguchi A., Mizukawa H., Ochiai M., Murata S., Someya M., Isobe T., Yamada T.K., Tanabe S. Anthropogenic and naturally occurring polybrominated phenolic compounds in the blood of cetaceans stranded along Japanese coastal waters. Environ. Pollut. 2011, 159:3364-3373. 10.1016/j.envpol.2011.08.035.
43. Orozco A., Linser P., Valverde-R C. Kinetic characterization of outer-ring deiodinase activity (ORD) in the liver, gill and retina of the killifish Fundulus heteroclitus. Comp. Biochem. Physiol. Part B Biochem. Mol. Biol. 2000, 126:283-290. 10.1016/s0305-0491(00)186-3.
44. Porazzi P., Calebiro D., Benato F., Tiso N., Persani L. Thyroid gland development and function in the zebrafish model. Mol. Cell. Endocrinol. 2009, 312:14-23. 10.1016/j.mce.2009.05.011.
45. Power D.M., Llewellyn L., Faustino M., Nowell M.A., Björnsson B.T., Einarsdottir I.E., Canario A.V., Sweeney G.E. Thyroid hormones in growth and development of fish. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 2001, 130:447-459.
46. Ren X.-M., Guo L.-H. Molecular toxicology of polybrominated diphenyl ethers: nuclear hormone receptor mediated pathways. Environ. Sci. Process. Impacts 2013, 15:702-708. 10.1039/c3em00023k.
47. Ren X.-M., Guo L.-H., Gao Y., Zhang B.-T., Wan B. Hydroxylated polybrominated diphenyl ethers exhibit different activities on thyroid hormone receptors depending on their degree of bromination. Toxicol. Appl. Pharmacol. 2013, 268:256-263. 10.1016/j.taap.2013.01.026.
48. Sanders J.P., Van der Geyten S., Kaptein E., Darras V.M., Kühn E.R., Leonard J.L., Visser T.J. Characterization of a propylthiouracil-insensitive type I iodothyronine deiodinase. Endocrinology 1997, 138:5153-5160. 10.1210/endo.138.12.5581.
49. Schmidt F., Braunbeck T. Alterations along the hypothalamic-pituitary-thyroid axis of the zebrafish (Danio rerio) after exposure to propylthiouracil. J. Thyroid Res. 2011, 3:1-17. 10.4061/2011/376243.
50. Schriks M., Roessig J.M., Murk A.J., Furlow J.D. Thyroid hormone receptor isoform selectivity of thyroid hormone disrupting compounds quantified with an in vitro reporter gene assay. Environ. Toxicol. Pharmacol. 2007, 23:302-307. 10.1016/j.etap.2006.11.007.
51. Stapleton H.M., Eagle S., Anthopolos R., Wolkin A., Miranda M.L. Associations between polybrominated diphenyl ether (PBDE) flame retardants, phenolic metabolites, and thyroid hormones during pregnancy. Environ. Health Perspect. 2011, 119:1454-1459. 10.1289/ehp.1003235.
52. Stoker T.E., Laws S.C., Crofton K.M., Hedge J.M., Ferrell J.M., Cooper R.L. Assessment of DE-71, a commercial polybrominated diphenyl ether (PBDE) mixture, in the EDSP male and female pubertal protocols. Toxicol. Sci. 2004, 78:144-155. 10.1093/toxsci/kfh029.
53. Strecker R., Weigt S., Braunbeck T. Cartilage and bone malformations in the head of zebrafish (Danio rerio) embryos following exposure to disulfiram and acetic acid hydrazide. Toxicol. Appl. Pharmacol. 2013, 268:221-231. 10.1016/j.taap.2013.01.023.
54. Sun J., Liu J., Liu Q., Ruan T., Yu M., Wang Y., Wang T., Jiang G. Hydroxylated polybrominated diphenyl ethers (OH-PBDEs) in biosolids from municipal wastewater treatment plants in China. Chemosphere 2013, 90:2388-2395. 10.1016/j.chemosphere.2012.10.034.
55. Szabo D.T., Richardson V.M., Ross D.G., Diliberto J.J., Kodavanti P.R.S., Birnbaum L.S. Effects of perinatal PBDE exposure on hepatic phase I, phase II, phase III, and deiodinase 1 gene expression involved in thyroid hormone metabolism in male rat pups. Toxicol. Sci. 2009, 107:27-39. 10.1093/toxsci/kfn230.
56. Tata J.R. Amphibian metamorphosis as a model for the developmental actions of thyroid hormone. Mol. Cell. Endocrinol. 2006, 246:10-20. 10.1016/j.mce.2005.11.024.
57. Usenko C.Y., Hopkins D.C., Trumble S.J., Bruce E.D. Hydroxylated PBDEs induce developmental arrest in zebrafish. Toxicol. Appl. Pharmacol. 2012, 262:43-51. 10.1016/j.taap.2012.04.017.
58. Van Boxtel A.L., Kamstra J.H., Cenijn P.H., Pieterse B., Wagner J.M., Antink M., Krab K., van der Burg B., Marsh G., Brouwer A., Legler J. Microarray analysis reveals a mechanism of phenolic polybrominated diphenylether toxicity in zebrafish. Environ. Sci. Technol. 2008, 42:1773-1779.
59. Visser T.J., Kaplan M.M., Leonard J.L., Larsen P.R. Evidence for two pathways of iodothyronine 5'-deiodination in rat pituitary that differ in kinetics, propylthiouracil sensitivity, and response to hypothyroidism. J. Clin. Invest. 1983, 71:992-1002.
60. Walker M.B., Kimmel C.B. A two-color acid-free cartilage and bone stain for zebrafish larvae. Biotech. Histochem. 2007, 82:23-28. 10.1080/10520290701333558.
61. Walpita C.N., Crawford A.D., Darras V.M. Combined antisense knockdown of type 1 and type 2 iodothyronine deiodinases disrupts embryonic development in zebrafish (Danio rerio). Gen. Comp. Endocrinol. 2010, 166:134-141. 10.1016/j.ygcen.2009.09.011.
62. Walpita C.N., Crawford A.D., Janssens E.D.R., Van der Geyten S., Darras V.M. Type 2 iodothyronine deiodinase is essential for thyroid hormone-dependent embryonic development and pigmentation in zebrafish. Endocrinology 2009, 150:530-539. 10.1210/en.2008-0457.
63. Walpita C.N., Van der Geyten S., Rurangwa E., Darras V.M. 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. 2007, 152:206-214. 10.1016/j.ygcen.2007.02.020.
64. Wan Y., Wiseman S., Chang H., Zhang X., Jones P.D., Hecker M., Kannan K., Tanabe S., Hu J., Lam M.H.W., Giesy J.P. Origin of hydroxylated brominated diphenyl ethers: natural compounds or man-made flame retardants?. Environ. Sci. Technol. 2009, 43:7536-7542.
65. Zhang Y.-F., Xu W., Lou Q.-Q., Li Y.-Y., Zhao Y.-X., Wei W.-J., Qin Z.-F., Wang H.-L., Li J.-Z. Tetrabromobisphenol A disrupts vertebrate development via thyroid hormone signaling pathway in a developmental stage-dependent manner. Environ. Sci. Technol. 2014, 48:8227-8234. 10.1021/es502366g.
66. Zhao Y., Ruan X., Li Y., Yan M., Qin Z. Polybrominated diphenyl ethers (PBDEs) in aborted human fetuses and placental transfer during the first trimester of pregnancy. Environ. Sci. Technol. 2013, 47:5939-5946. 10.1021/es305349x.
67. Zheng X., Zhu Y., Liu C., Liu H., Giesy J.P., Hecker M., Lam M.H.W., Yu H. Accumulation and biotransformation of BDE-47 by zebrafish larvae and teratogenicity and expression of genes along the hypothalamus-pituitary-thyroid axis. Environ. Sci. Technol. 2012, 46:12943-12951. 10.1021/es303289n.
68. Zhou T., Taylor M.M., DeVito M.M.J., Crofton K.K.M.A. Developmental exposure to brominated diphenyl ethers results in thyroid hormone disruption. Toxicol. Sci. 2002, 66:105-116.
69. Zota A.R., Park J.-S., Wang Y., Petreas M., Zoeller R.T., Woodruff T.J. Polybrominated diphenyl ethers, hydroxylated polybrominated diphenyl ethers, and measures of thyroid function in second trimester pregnant women in California. Environ. Sci. Technol. 2011, 45:7896-7905. 10.1021/es200422b.