Waterborne exposure of zebrafish embryos to micromole concentrations of ioxynil and diethylstilbestrol disrupts thyrocyte development

Aquatic Toxicology

Volumn 140-141, Issue , 2013, Pages 279-287

  Campinho, M A ^a   Power, D M ^a  

^a UNIVERSITY OF ALGARVE   (Portugal)

Author keywords

Development; Diethylstilbestrol; Endocrine disruption; Ioxynil; Thyrocytes; Zebrafish

Indexed keywords

DIETHYLSTILBESTROL; HERBICIDE; IOXYNIL; MESSENGER RNA; MORPHOLINO OLIGONUCLEOTIDE; THYROGLOBULIN; THYROID HORMONE; TROPONIN I; UNCLASSIFIED DRUG;

CONCENTRATION (COMPOSITION); EMBRYO; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; FISH; GENE EXPRESSION; GROWTH RESPONSE; HERBICIDE; HORMONE; INHIBITOR; POLLUTION EXPOSURE; RNA;

ARTICLE; CELL MATURATION; CMLC2 GENE; CONTROLLED STUDY; EMBRYO; ENVIRONMENTAL EXPOSURE; ENZYME INHIBITION; GENE; GENE SEQUENCE; HEART DEVELOPMENT; HEART FUNCTION; HYPOTHALAMIC PITUITARY THYROID AXIS; HYPOTHALAMUS HYPOPHYSIS SYSTEM; NK2.1A GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; TG GENE; THYROID CELL; THYROID GLAND; WATER CONTAMINATION; ZEBRA FISH;

DEVELOPMENT; DIETHYLSTILBESTROL; ENDOCRINE DISRUPTION; IOXYNIL; THYROCYTES; ZEBRAFISH;

ANIMALS; DIETHYLSTILBESTROL; EMBRYO, NONMAMMALIAN; GENE EXPRESSION REGULATION; HEART; HYPOTHALAMUS; IODOBENZENES; NITRILES; NK CELL LECTIN-LIKE RECEPTOR SUBFAMILY A; THYROGLOBULIN; THYROID GLAND; WATER POLLUTANTS, CHEMICAL; ZEBRAFISH;

EID: 84880384234     PISSN: 0166445X     EISSN: 18791514     Source Type: Journal    
DOI: 10.1016/j.aquatox.2013.06.014     Document Type: Article

References (55)

1. Alt B., Elsalini O.A., Schrumpf P., Haufs N., Lawson N.D., Schwabe G.C., Mundlos S., Gruters A., Krude H., Rohr K.B. Arteries define the position of the thyroid gland during its developmental relocalisation. Development 2006, 133:3797-3804.
2. Alt B., Reibe S., Feitosa N.M., Elsalini O.A., Wendl T., Rohr K.B. Analysis of origin and growth of the thyroid gland in zebrafish. Develop. Dyn. 2006, 235:1872-1883.
3. Auman H.J., Coleman H., Riley H.E., Olale F., Tsai H.J., Yelon D. Functional modulation of cardiac form through regionally confined cell shape changes. PLoS Biol. 2007, 5:e53.
4. Auman H.J., Yelon D. Vertebrate organogenesis: getting the heart into shape. Curr. Biol. 2004, 14:R152-R153.
5. Bartman T., Hove J. Mechanics and function in heart morphogenesis. Develop. Dyn. 2005, 233:373-381.
6. Bianco A.C., Larsen P.R. Cellular and structural biology of the deiodinases. Thyroid 2005, 15:777-786.
7. Boas M., Feldt-Rasmussen U., Main K.M. Thyroid effects of endocrine disrupting chemicals. Mol. Cell. Endocrinol. 2012, 355:240-248.
8. Brar N.K., Waggoner C., Reyes J.A., Fairey R., Kelley K.M. Evidence for thyroid endocrine disruption in wild fish in San Francisco Bay, California, USA. Relationships to contaminant exposures. Aquat. Toxicol. 2009, 96:203-215.
9. Campinho M.A., Morgado I., Pinto P.I.S., Silva N., Power D.M. The goitrogenic efficiency of thioamides in a marine teleost, sea bream (Sparus auratus). General Comparative Endocrinol. 2012, 179:369-375.
10. Carr J.A., Patiño R. The hypothalamus-pituitary-thyroid axis in teleosts and amphibians: Endocrine disruption and its consequences to natural populations. General Comparative Endocrinol. 2011, 170:299-312.
11. Chen H.-C., Kuo H.-W., Ding W.-H. Determination of estrogenic compounds in wastewater using liquid chromatography-tandem mass spectrometry with electrospray and atmospheric pressure photoionization following desalting extraction. Chemosphere 2009, 74:508-514.
12. Davis F.B., Tang H.-Y., Shih A., Keating T., Lansing L., Hercbergs A., Fenstermaker R.A., Mousa A., Mousa S.A., Davis P.J., Lin H.-Y. Acting via a cell surface receptor, thyroid hormone is a growth factor for glioma cells. Cancer Res. 2006, 66:7270-7275.
13. Davis P.J., Davis F.B., Cody V. Membrane receptors mediating thyroid hormone action. Trends Endocrinol. Metab. 2005, 16:429-435.
14. de Jesus E.G., Hirano T., Inui Y. Changes in cortisol and thyroid hormone concentrations during early development and metamorphosis in the Japanese flounder, Paralichthys olivaceus. General Comparative Endocrinol. 1991, 82:369-376.
15. de Jesus E.G., Inui Y., Hirano T. Cortisol enhances the stimulating action of thyroid hormones on dorsal fin-ray resorption of flounder larvae in vitro. General Comparative Endocrinol. 1990, 79:167-173.
16. Denver R.J. Environmental stress as a developmental cue: corticotropin-releasing hormone is a proximate mediator of adaptive phenotypic plasticity in amphibian metamorphosis. Hormones Behav. 1997, 31:169-179.
17. Denver R.J., Boorse G.C., Glennemeier K.A. Endocrinology of complex life cycles: amphibians. Hormones, Brain and Behavior 2002, 469-513. Academic Press, Inc., San Diego. D. Pfaff (Ed.).
18. Dobrydneva Y., Williams R.L., Blackmore P.F. Diethylstilbestrol and other nonsteroidal estrogens: novel class of store-operated calcium channel modulators. J. Cardiovasc. Pharmacol. 2010, 55:522-530.
19. Dobrydneva Y., Williams R.L., Katzenellenbogen J.A., Ratz P.H., Blackmore P.F. Diethylstilbestrol and tetrahydrochrysenes are calcium channel blockers in human platelets: relationship to the stilbene pharmacophore. Thrombosis Res. 2003, 110:23-31.
20. Elsalini O., Rohr K. Phenylthiourea disrupts thyroid function in developing zebrafish. Develop. Genes Evol. 2003, 212:593-598.
21. Elsalini O.A., Gartzen J.v., Cramer M., Rohr K.B. Zebrafish hhex, nk2.1a, and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors. Develop. Biol. 2003, 263:67-80.
22. European-Comission Review Report for the Active Substance Ioxynil 2004, European Report Directorate.
23. Ferrante M.I., Kiff R.M., Goulding D.A., Stemple D.L. Troponin T is essential for sarcomere assembly in zebrafish skeletal muscle. J. Cell Sci. 2011, 124:565-577.
24. Helweg A. Threats to water quality from pesticides-case histories from Denmark. Pestic Outlook 1994, 5:12-18.
25. Henley D.V., Korach K.S. Physiological effects and mechanisms of action of endocrine disrupting chemicals that alter estrogen signaling. Hormones 2010, 9:191-205.
26. Holtzman N.G., Schoenebeck J.J., Tsai H.J., Yelon D. Endocardium is necessary for cardiomyocyte movement during heart tube assembly. Development 2007, 134:2379-2386.
27. Kimmel C.B., Ballard W.W., Kimmel S.R., Ullmann B., Schilling T.F. Stages of embryonic development of the zebrafish. Develop. Dyn. 1995, 203:253-310.
28. le Maire A., Bourguet W., Balaguer P. A structural view of nuclear hormone receptor: endocrine disruptor interactions. Cell. Mol. Life Sci. 2010, 67:1219-1237.
29. Leatherland J.F. Changes in thyroid hormone economy following consumption of environmentally contaminated Great Lakes fish. Toxicol. Ind. Health 1998, 14:41-57.
30. Leatherland J.F., Sonstegard R. Effect of dietary mirex or PCB (Arochlor 1254) on serum thyroxine (T4) and triiodothyronine (T3) levels in rainbow-trout. Acta Endocrinol. 1977, 85:234.
31. Leithe E., Kjenseth A., Bruun J., Sirnes S., Rivedal E. Inhibition of connexin43 gap junction channels by the endocrine disruptor ioxynil. Toxicol. Appl. Pharmacol. 2011, 247:10-17.
32. Linders J.B.H.J., Jansma J.W., Mensink B.J.W.G., Otermann K. Pesticides: benefaction or Pandora's box? A synopsis of the environmental aspects of 243 pesticides 1994, National Institute of Public Health and the Environment (RIVM), The Netherlands.
33. Ma L. Endocrine disruptors in female reproductive tract development and carcinogenesis. Trends Endocrinol. Metab. 2009, 20:357-363.
34. Morgado I., Campinho M.A., Costa R., Jacinto R., Power D.M. Disruption of the thyroid system by diethylstilbestrol and ioxynil in the sea bream (Sparus aurata). Aquat. Toxicol. 2009, 92:271-280.
35. Morgado I., Hamers T., Van der Ven L., Power D.M. Disruption of thyroid hormone binding to sea bream recombinant transthyretin by ioxinyl and polybrominated diphenyl ethers. Chemosphere 2007, 69:155-163.
36. Mukhi S., Patiño R. Effects of prolonged exposure to perchlorate on thyroid and reproductive function in zebrafish. Toxicol. Sci. 2007, 96:246-254.
37. Nesan D., Vijayan M.M. Embryo exposure to elevated cortisol level leads to cardiac performance dysfunction in zebrafish. Mol. Cell. Endocrinol. 2012, 363:85-91.
38. Opitz R., Maquet E., Huisken J., Antonica F., Trubiroha A., Pottier G.l., Janssens V.r., Costagliola S. Transgenic zebrafish illuminate the dynamics of thyroid morphogenesis and its relationship to cardiovascular development. Develop. Biol. 2012, 372:203-216.
39. Opitz R., Maquet E., Zoenen M., Dadhich R., Costagliola S. TSH receptor function is required for normal thyroid differentiation in zebrafish. Mol. Endocrinol. 2011, 25:1579-1599.
40. Raldúa D., André M., Babin P.J. Clofibrate and gemfibrozil induce an embryonic malabsorption syndrome in zebrafish. Toxicol. Appl. Pharmacol. 2008, 228:301-314.
41. Richardson S.J., Monk J.A., Shepherdley C.A., Ebbesson L.O., Sin F., Power D.M., Frappell P.B., Kohrle J., Renfree M.B. Developmentally regulated thyroid hormone distributor proteins in marsupials, a reptile, and fish. Am. J. Physiol. Regul. Integ. Comp. Physiol. 2005, 288:R1264-R1272.
42. Rohr K.B., Barth K.A., Varga Z.n.M., Wilson S.W. The nodal pathway acts upstream of hedgehog signaling to specify ventral telencephalic identity. Neuron 2001, 29:341-351.
43. Rohr K.B., Concha M.L. Expression of nk2.1a during early development of the thyroid gland in zebrafish. Mech. Develop. 2000, 95:267-270.
44. Saal F.S.V., Timms B.G., Montano M.M., Palanza P., Thayer K.A., Nagel S.C., Dhar M.D., Ganjam V.K., Parmigiani S., Welshons W.V. Prostate enlargement in mice due to fetal exposure to low doses of estradiol or diethylstilbestrol and opposite effects at high doses. Proc. Natl. Acad. Sci. 1997, 94:2056-2061.
45. Santos C.R.A., Anjos L., Power D.M. Transthyretin in fish: state of the art. Clin. Chem. Lab. Med. 2002, 40:1244-1249.
46. Schoenebeck J.J., Yelon D. Illuminating cardiac development: advances in imaging add new dimensions to the utility of zebrafish genetics. Semin. Cell. Develop. Biol. 2007, 18:27-35.
47. Sehnert A., Huq A., Weinstein B., Walker C., Fishman M., Stainier D. Cardiac troponin T is essential in sarcomere assembly and cardiac contractility. Nat. Genet. 2002, 31:106-110.
48. Thisse C., Thisse B. High-resolution in situ hybridization to whole-mount zebrafish embryos. Nat. Protocols 2008, 3:59-69.
49. Vandenberg L.N., Colborn T., Hayes T.B., Heindel J.J., Jacobs D.R., Lee D.-H., Shioda T., Soto A.M., vom Saal F.S., Welshons W.V., Zoeller R.T., Myers J.P. Hormones and endocrine-disrupting chemicals: low-dose effects and nonmonotonic dose responses. Endocr. Rev. 2012, 33:378-455.
50. Welshons W.V., Thayer K.A., Judy B.M., Taylor J.A., Curran E.M., vom Saal F.S. Large effects from small exposures. I. Mechanisms for endocrine-disrupting chemicals with estrogenic activity. Environ. Health Perspect. 2003, 111.
51. Wendl T., Lun K., Mione M., Favor J., Brand M., Wilson S.W., Rohr K.B. Pax2.1 is required for the development of thyroid follicles in zebrafish. Development 2002, 129:3751-3760.
52. Wendl T., Adzic D., Schoenebeck J.J., Scholpp S., Brand M., Yelon D., Rohr K.B. Early developmental specification of the thyroid gland depends on han-expressing surrounding tissue and on FGF signals. Development 2007, 134:2871-2879.
53. Witorsch R.J. Low-dose in utero effects of xenoestrogens in mice and their relevance to humans: an analytical review of the literature. Food Chem. Toxicol. 2002, 40:905-912.
54. 2+ fluxes and prolactin release in GH3/B6 pituitary tumor cells. Environ. Health Perspect. 2005, 113:431-439.
55. Yang L., Lin L., Weng S., Feng Z., Luan T. Sexually disrupting effects of nonylphenol and diethylstilbestrol on male silver carp (Carassius auratus) in aquatic microcosms. Ecotoxicol. Environmen. Saf. 2008, 71:400-411.