A screening assay for thyroid hormone signaling disruption based on thyroid hormone-response gene expression analysis in the frog Pelophylax nigromaculatus

Journal of Environmental Sciences (China)

Volumn 34, Issue , 2015, Pages 143-154

  Zhang, Yinfeng ^a   Li, Yuanyuan ^a   Qin, Zhanfen ^a   Wang, Huili ^a   Li, Jianzhong ^a  

^a RESEARCH CENTER FOR ECO ENVIRONMENTAL SCIENCES   (China)

Author keywords

Pelophylax nigromaculatus; Screening assay; Tetrabromobisphenol A; TH response gene expression; Thyroid hormone signaling disruptor

Indexed keywords

GENE EXPRESSION; HORMONES; SIGNALING;

AMPHIBIAN METAMORPHOSIS; EFFECTIVE CONCENTRATION; ENVIRONMENTAL CHEMICALS; GENE EXPRESSION ANALYSIS; PELOPHYLAX NIGROMACULATUS; SCREENING ASSAYS; TETRABROMOBISPHENOL A; THYROID HORMONES;

SIGNAL DETECTION;

CONCENTRATION (COMPOSITION); ENDOCRINE SYSTEM; FROG; GENE EXPRESSION; HORMONE;

AMPHIBIA; ANURA; PELOPHYLAX; XENOPUS LAEVIS;

ENDOCRINE DISRUPTOR; FLAME RETARDANT; POLYBROMINATED BIPHENYL; TETRABROMOBISPHENOL A; THYROID HORMONE; WATER POLLUTANT;

ANIMAL; DRUG EFFECTS; ENVIRONMENTAL MONITORING; GENE EXPRESSION REGULATION; GROWTH, DEVELOPMENT AND AGING; INTESTINE; LARVA; METABOLISM; METAMORPHOSIS; PROCEDURES; RANIDAE; SIGNAL TRANSDUCTION; TOXICITY; WATER POLLUTANT;

ANIMALS; ENDOCRINE DISRUPTORS; ENVIRONMENTAL MONITORING; FLAME RETARDANTS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; INTESTINES; LARVA; METAMORPHOSIS, BIOLOGICAL; POLYBROMINATED BIPHENYLS; RANIDAE; SIGNAL TRANSDUCTION; THYROID HORMONES; WATER POLLUTANTS, CHEMICAL;

EID: 84938604608     PISSN: 10010742     EISSN: 18787320     Source Type: Journal    
DOI: 10.1016/j.jes.2015.01.028     Document Type: Article

References (69)

1. Astapova I., Hollenberg A.N. The in vivo role of nuclear receptor corepressors in thyroid hormone action. Biochim. Biophys. Acta 2013, 1830(7):3876-3881.
2. Beausoleil C., Ormsby J.-N., Gies A., Hass U., Heindel J.J., Holmer M.L., et al. Low dose effects and non-monotonic dose responses for endocrine active chemicals: Science to practice workshop: workshop summary. Chemosphere 2013, 93(6):847-856.
3. Boas M., Feldt-Rasmussen U., Main K.M. Thyroid effects of endocrine disrupting chemicals. Mol. Cell. Endocrinol. 2012, 355(2):240-248.
4. Coady K., Marino T., Thomas J., Currie R., Hancock G., Crofoot J., et al. Evaluation of the amphibian metamorphosis assay: exposure to the goitrogen methimazole and the endogenous thyroid hormone l-thyroxine. Environ. Toxicol. Chem. 2010, 29(4):869-880.
5. Crump D., Werry K., Veldhoen N., Van Aggelen G., Helbing C.C. Exposure to the herbicide acetochlor alters thyroid hormone-dependent gene expression and metamorphosis in Xenopus laevis. Environ. Health Perspect. 2002, 110(12):1199-1205.
6. Dai J.H., Ma J.Y., Xu L.L., Wei Y.Q., Gu Y.F., Zhou K.Y. Declines of farm land and pond frogs in thirteen provinces in China. J. Nanjing Normal Univ. 2011, 34(1):80-85.
7. Davey J.C., Nomikos A.P., Wungjiranirun M., Sherman J.R., Ingram L., Batki C., et al. Arsenic as an endocrine disruptor: arsenic disrupts retinoic acid receptor- and thyroid hormone receptor-mediated gene regulation and thyroid hormone-mediated amphibian tail metamorphosis. Environ. Health Perspect. 2008, 116(2):165-172.
8. Fini J.B., Le Mevel S., Turque N., Palmier K., Zalko D., Cravedi J.P., et al. An in vivo multiwell-based fluorescent screen for monitoring vertebrate thyroid hormone disruption. Environ. Sci. Technol. 2007, 41(16):5908-5914.
9. Fini J.B., Le Mevel S., Palmier K., Darras V.M., Punzon I., Richardson S.J., et al. Thyroid hormone signaling in the Xenopus laevis embryo is functional and susceptible to endocrine disruption. Endocrinology 2012, 153(10):5068-5081.
10. Fini J.B., Riu A., Debrauwer L., Hillenweck A., Le Mevel S., Chevolleau S., et al. Parallel biotransformation of tetrabromobisphenol A in Xenopus laevis and mammals: Xenopus as a model for endocrine perturbation studies. Toxicol. Sci. 2012, 125(2):359-367.
11. Freitas J., Cano P., Craig-Veit C., Goodson M.L., Furlow J.D., Murk A.J. Detection of thyroid hormone receptor disruptors by a novel stable in vitro reporter gene assay. Toxicol. in Vitro 2011, 25(1):257-266.
12. Freitas J., Miller N., Mengeling B.J., Xia M., Huang R., Houck K., et al. Identification of thyroid hormone receptor active compounds using a quantitative high-throughput screening platform. Curr. Chem. Genomics Transl. Med. 2014, 7(8):36-46.
13. Freytag R.E., Hullinghorst R.L., Hunter G.W., Ritchie L.S. Comparison of Xenopus Laevis and Rana nigromaculata as test animals for the determination of pregnancy. J. Lab. Clin. Med. 1953, 42(4):646-654.
14. Furlow J.D., Yang H.Y., Hsu M., Lim W., Ermio D.J., Chiellini G., et al. Induction of larval tissue resorption in Xenopus laevis tadpoles by the thyroid hormone receptor agonist GC-1. J. Biol. Chem. 2004, 279(25):26555-26562.
15. Ge Y.N., Li Y.Y., Zhang Y.F., Lou Q.Q., Zhao Y.X., Qin Z.F. The development and thyroid hormone levels of thyroid gland during Rana nigromaculata metamorphosis. Acta Hydrobiol. Sin. 2014, 38(4):714-719.
16. Gosner K.L. A simplified table for staging anuran embryos and larvae with notes on identification. Herpetologica 1960, 16(3):183-190.
17. Hammond S.A., Veldhoen N., Kobylarz M., Webber N.R., Jordan J., Rehaume V., et al. Characterization of gene expression endpoints during postembryonic development of the northern green frog (Rana clamitans melanota). Zool. Sci. 2013, 30(5):392-401.
18. Hasebe T., Buchholz D.R., Shi Y.B., Ishizuya-Oka A. Epithelial-connective tissue interactions induced by thyroid hormone receptor are essential for adult stem cell development in the Xenopus laevis intestine. Stem Cells 2011, 29(1):154-161.
19. He M.J., Luo X.J., Yu L.H., Wu J.P., Chen S.J., Mai B.X. Diasteroisomer and enantiomer-specific profiles of hexabromocyclododecane and tetrabromobisphenol A in an aquatic environment in a highly industrialized area, South China: vertical profile, phase partition, and bioaccumulation. Environ. Pollut. 2013, 179:105-110.
20. Heimeier R.A., Das B., Buchholz D.R., Shi Y.B. The xenoestrogen bisphenol A inhibits postembryonic vertebrate development by antagonizing gene regulation by thyroid hormone. Endocrinology 2009, 150(6):2964-2973.
21. Heimeier R.A., Das B., Buchholz D.R., Fiorentino M., Shi Y.B. Studies on Xenopus laevis intestine reveal biological pathways underlying vertebrate gut adaptation from embryo to adult. Genome Biol. 2010, 11(5):R55. 10.1186/gb-2010-11-5-r55.
22. Helbing C.C., Ovaska K., Ji L. Evaluation of the effect of acetochlor on thyroid hormone receptor gene expression in the brain and behavior of Rana catesbeiana tadpoles. Aquat. Toxicol. 2006, 80(1):42-51.
23. Hinther A., Domanski D., Vawda S., Helbing C.C. C-fin: a cultured frog tadpole tail fin biopsy approach for detection of thyroid hormone-disrupting chemicals. Environ. Toxicol. Chem. 2010, 29(2):380-388.
24. Hofmann P.J., Schomburg L., Köhrle J. Interference of endocrine disrupters with thyroid hormone receptor-dependent transactivation. Toxicol. Sci. 2009, 110(1):125-137.
25. Hogan N.S., Crump K.L., Duarte P., Lean D.R.S., Trudeau V.L. Hormone cross-regulation in the tadpole brain: developmental expression profiles and effect of T3 exposure on thyroid hormone- and estrogen-responsive genes in Rana pipiens. Gen. Comp. Endocrinol. 2007, 154(1-3):5-15.
26. Hoopfer E.D., Huang L.Y., Denver R.J. Basic transcription element binding protein is a thyroid hormone-regulated transcription factor expressed during metamorphosis in Xenopus laevis. Develop. Growth Differ. 2002, 44(5):365-381.
27. Hu X.X., Shi W., Zhang F.X., Cao F., Hu G.J., Hao Y.Q., et al. In vitro assessment of thyroid hormone disrupting activities in drinking water sources along the Yangtze River. Environ. Pollut. 2013, 173:210-215.
28. Huang M.-Y., Duan R.-Y., Ji X. Chronic effects of environmentally-relevant concentrations of lead in Pelophylax nigromaculata tadpoles: threshold dose and adverse effects. Ecotoxicol. Environ. Saf. 2014, 104:310-316.
29. Ishihara A., Makita Y., Yamauchi K. Gene expression profiling to examine the thyroid hormone-disrupting activity of hydroxylated polychlorinated biphenyls in metamorphosing amphibian tadpole. J. Biochem. Mol. Toxicol. 2011, 25(5):303-311.
30. Jagnytsch O., Opitz R., Lutz I., Kloas W. Effects of tetrabromobisphenol A on larval development and thyroid hormone-regulated biomarkers of the amphibian Xenopus laevis. Environ. Res. 2006, 101(3):340-348.
31. Jia X.Y., Cai C.C., Wang J., Gao N.N., Zhang H.J. Endocrine-disrupting effects and reproductive toxicity of low dose MCLR on male frogs (Rana nigromaculata) in vivo. Aquat. Toxicol. 2014, 155:24-31.
32. Jugan M.L., Lévy-Bimbot M., Pomérance M., Tamisier-Karolak S., Blondeau J.P., Lévi Y. A new bioluminescent cellular assay to measure the transcriptional effects of chemicals that modulate the alpha-1 thyroid hormone receptor. Toxicol. in Vitro 2007, 21(6):1197-1205.
33. Kitamura S., Kato T., Iida M., Jinno N., Suzuki T., Ohta S., et al. Anti-thyroid hormonal activity of tetrabromobisphenol A, a flame retardant, and related compounds: affinity to the mammalian thyroid hormone receptor, and effect on tadpole metamorphosis. Life Sci. 2005, 76(14):1589-1601.
34. Kudo Y., Yamauchi K., Fukazawa H., Terao Y. In vitro and in vivo analysis of the thyroid system-disrupting activities of brominated phenolic and phenol compounds in Xenopus laevis. Toxicol. Sci. 2006, 92(1):87-95.
35. Labadie P., Tlili K., Alliot F., Bourges C., Desportes A., Chevreuil M. Development of analytical procedures for trace-level determination of polybrominated diphenyl ethers and tetrabromobisphenol A in river water and sediment. Anal. Bioanal. Chem. 2010, 396(2):865-875.
36. Laudet V. The origins and evolution of vertebrate metamorphosis. Curr. Biol. 2011, 21(18):R726-R737.
37. Li J., Ma M., Wang Z.J. A two-hybrid yeast assay to quantify the effects of xenobiotics on thyroid hormone-mediated gene expression. Environ. Toxicol. Chem. 2008, 27(1):159-167.
38. Li J., Ren S.J., Han S.L., Li N. A yeast bioassay for direct measurement of thyroid hormone disrupting effects in water without sample extraction, concentration, or sterilization. Chemosphere 2014, 100:139-145.
39. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)). Method. 2001, 25(4):402-408.
40. Lou Q.Q., Zhang Y.F., Ren D.K., Xu H.M., Zhao Y.X., Qin Z.F., et al. Molecular characterization and developmental expression patterns of thyroid hormone receptors (TRs) and their responsiveness to TR agonist and antagonist in Rana nigromaculata. J. Environ. Sci. 2014, 26(10):2084-2094.
41. Lou Q.Q., Cao S., Xu W., Zhang Y.F., Qin Z.F., Wei W.J. Molecular characterization and mRNA expression of ribosomal protein L8 in Rana nigromaculata during development and under exposure to hormones. J. Environ. Sci. 2014, 26(11):2331-2339.
42. Matsubara K., Sanoh S., Ohta S., Kitamura S., Sugihara K., Fujimoto N. An improved thyroid hormone reporter assay to determine the thyroid hormone-like activity of amiodarone, bithionol, closantel and rafoxanide. Toxicol. Lett. 2012, 208(1):30-35.
43. Mullur R., Liu Y.-Y., Brent G.A. Thyroid hormone regulation of metabolism. Physiol. Rev. 2014, 94(2):355-382.
44. Nakajima K., Fujimoto K., Yaoita Y. Regulation of thyroid hormone sensitivity by differential expression of the thyroid hormone receptor during Xenopus metamorphosis. Genes Cells 2012, 17(8):645-659.
45. Oka T., Mitsui-Watanabe N., Tatarazako N., Onishi Y., Katsu Y., Miyagawa S., et al. Establishment of transactivation assay systems using fish, amphibian, reptilian and human thyroid hormone receptors. J. Appl. Toxicol. 2012, 33(9):991-1000.
46. Opitz R., Braunbeck T., Bogi C., Pickford D.B., Nentwig G., Oehlmann J., et al. Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds. Environ. Toxicol. Chem. 2005, 24(3):653-664.
47. Remaud S., Gothié J.-D., Morvan-Dubois G., Demeneix B.A. Thyroid hormone signaling and adult neurogenesis in mammals. Front. Endocrinol.(Lausanne) 2014, 5:62. 10.3389/fendo.2014.00062.
48. 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(3):256-263.
49. Ren X.M., Zhang Y.F., Guo L.H., Qin Z.F., Lü Q.Y., Zhang L.Y. Structure-activity relations in binding of perfluoroalkyl compounds to human thyroid hormone T3 receptor. Arch. Toxicol. 2015, 89(2):233-242. 10.1007/s00204-014-1258-y.
50. Searcy B.T., Beckstrom-Sternberg S.M., Beckstrom-Sternberg J.S., Stafford P., Schwendiman A.L., Soto-Pena J., et al. Thyroid hormone-dependent development in Xenopus laevis: a sensitive screen of thyroid hormone signaling disruption by municipal wastewater treatment plant effluent. Gen. Comp. Endocrinol. 2012, 176(3):481-492.
51. Shi Y.B. Dual functions of thyroid hormone receptors in vertebrate development: the roles of histone-modifying cofactor complexes. Thyroid 2009, 19(9):987-999.
52. Shiizaki K., Asai S., Ebata S., Kawanishi M., Yagi T. Establishment of yeast reporter assay systems to detect ligands of thyroid hormone receptors α and β. Toxicol. in Vitro 2010, 24(2):638-644.
53. State Science and Technology Commission in China Regulation for the Administration of Affairs Concerning Experimental Animals 1988, The Ministry of Science and Technology of the People's Republic of China, Beijing.
54. Stolow M.A., Shi Y.B. Xenopus sonic hedgehog as a potential morphogen during embryogenesis and thyroid hormone-dependent metamorphosis. Nucleic Acids Res. 1995, 23(13):2555-2562.
55. Sun H., Shen O.X., Wang X.R., Zhou L., Zhen S.Q., Chen X.D. Anti-thyroid hormone activity of bisphenol A, tetrabromobisphenol A and tetrachlorobisphenol A in an improved reporter gene assay. Toxicol. in Vitro 2009, 23(5):950-954.
56. Tata J.R. Gene expression during metamorphosis: an ideal model for post-embryonic development. BioEssays 1993, 15(4):239-248.
57. Terasaki M., Kosaka K., Kunikane S., Makino M., Shiraishi F. Assessment of thyroid hormone activity of halogenated bisphenol A using a yeast two-hybrid assay. Chemosphere 2011, 84(10):1527-1530.
58. The IUCN Red List of Threatened Species Pelophylax nigromaculatus (Black-spotted Pond Frog, Dark-spotted Frog). International Union for Conservation of Nature 2014, (Available at: http://www.iucnredlist.org/details/58679/0)).
59. Turque N., Palmier K., Le Mével S., Alliot C., Demeneix B.A. A rapid, physiologic protocol for testing transcriptional effects of thyroid-disrupting agents in premetamorphic Xenopus tadpoles. Environ. Health Perspect. 2005, 113(11):1588-1593.
60. Vandenberg L.N. Non-monotonic dose responses in studies of endocrine disrupting chemicals: bisphenol A as a case study. Dose-Response 2014, 12(2):259-276.
61. Veldhoen N., Boggs A., Walzak K., Helbing C.C. Exposure to tetrabromobisphenol-A alters TH-associated gene expression and tadpole metamorphosis in the Pacific tree frog Pseudacris regilla. Aquat. Toxicol. 2006, 78(3):292-302.
62. Veldhoen N., Propper C.R., Helbing C.C. Enabling comparative gene expression studies of thyroid hormone action through the development of a flexible real-time quantitative PCR assay for use across multiple anuran indicator and sentinel species. Aquat. Toxicol. 2014, 148:162-173.
63. Veldhoen N., Skirrow R.C., Brown L.L., van Aggelen G., Helbing C.C. Effects of acute exposure to the non-steroidal anti-inflammatory drug ibuprofen on the developing North American bullfrog (Rana catesbeiana) tadpole. Environ. Sci. Technol. 2014, 48(17):10439-10447.
64. Wang X.D., Matsuda H., Shi Y.B. Developmental regulation and function of thyroid hormone receptors and 9-cis retinoic acid receptors during Xenopus tropicalis metamorphosis. Endocrinology 2008, 149(11):5610-5618.
65. Yang S.W., Wang S.R., Liu H.L., Yan Z.G. Tetrabromobisphenol A: tissue distribution in fish, and seasonal variation in water and sediment of Lake Chaohu, China. Environ. Sci. Pollut. Res. 2012, 19(9):4090-4096.
66. Yen P.M. Physiological and molecular basis of thyroid hormone action. Physiol. Rev. 2001, 81(3):1097-1142.
67. Zhang J., Lazar M.A. The mechanism of action of thyroid hormones. Annu. Rev. Physiol. 2000, 62(1):439-466.
68. Zhang Y.F., Xu W., Lou Q.Q., Li Y.Y., Zhao Y.X., Wei W.J., et al. Tetrabromobisphenol A disrupts vertebrate development via thyroid hormone signaling pathway in a developmental stage-dependent manner. Environ. Sci. Technol. 2014, 48(14):8227-8234.
69. Zoeller R.T., Tyl R.W., Tan S.W. Current and potential rodent screens and tests for thyroid toxicants. Crit. Rev. Toxicol. 2007, 37(1-2):55-95.