Table of Contents Author Guidelines Submit a Manuscript
Journal of Thyroid Research
Volume 2011 (2011), Article ID 376243, 17 pages
http://dx.doi.org/10.4061/2011/376243
Research Article

Alterations along the Hypothalamic-Pituitary-Thyroid Axis of the Zebrafish (Danio rerio) after Exposure to Propylthiouracil

Aquatic Ecology and Toxicology Group, Centre for Organismal Studies, University of Heidelberg, Im Neuenheimer Feld 230, 69120 Heidelberg, Germany

Received 12 January 2011; Revised 17 April 2011; Accepted 11 May 2011

Academic Editor: Jack R. Wall

Copyright © 2011 Florian Schmidt and Thomas Braunbeck. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. Bernanke and H. R. Köhler, “The impact of environmental chemicals on wildlife vertebrates,” Reviews of Environmental Contamination and Toxicology, vol. 198, pp. 1–47, 2009. View at Publisher · View at Google Scholar · View at Scopus
  2. M. L. Blanton and J. L. Specker, “The hypothalamic-pituitary-thyroid (HPT) axis in fish and its role in fish development and reproduction,” Critical Reviews in Toxicology, vol. 37, no. 1-2, pp. 97–115, 2007. View at Publisher · View at Google Scholar · View at Scopus
  3. T. M. Crisp, E. D. Clegg, R. L. Cooper et al., “Environmental endocrine disruption: an effects assessment and analysis,” Environmental Health Perspectives, vol. 106, supplement 1, pp. 11–56, 1998. View at Google Scholar
  4. A. K. Hotchkiss, C. V. Rider, C. R. Blystone et al., “Fifteen years after “wingspread”—environmental endocrine disrupters and human and wildlife health: where we are today and where we need to go,” Toxicological Sciences, vol. 105, no. 2, pp. 235–259, 2008. View at Publisher · View at Google Scholar
  5. W. Kloas, R. Urbatzka, R. Opitz et al., “Endocrine disruption in aquatic vertebrates,” Annals of the New York Academy of Sciences, vol. 1163, pp. 187–200, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. P. Matthiessen, “Historical perspective on endocrine disruption in wildlife,” Pure and Applied Chemistry, vol. 75, no. 11-12, pp. 2197–2206, 2003. View at Google Scholar · View at Scopus
  7. S. Scholz, S. Fischer, U. Gündel, E. Küster, T. Luckenbach, and D. Voelker, “The zebrafish embryo model in environmental risk assessment—applications beyond acute toxicity testing,” Environmental Science and Pollution Research, vol. 15, no. 5, pp. 394–404, 2008. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Scholz and I. Mayer, “Molecular biomarkers of endocrine disruption in small model fish,” Molecular and Cellular Endocrinology, vol. 293, no. 1-2, pp. 57–70, 2008. View at Publisher · View at Google Scholar · View at Scopus
  9. J. G. Vos, E. Dybing, H. A. Greim et al., “Health effects of endocrine-disrupting chemicals on wildlife, with special reference to the European situation,” Critical Reviews in Toxicology, vol. 30, no. 1, pp. 71–133, 2000. View at Google Scholar · View at Scopus
  10. L. E. Gray Jr., J. Ostby, V. Wilson et al., “Xenoendocrine disrupters-tiered screening and testing: filling key data gaps,” Toxicology, vol. 181-182, pp. 371–382, 2002. View at Publisher · View at Google Scholar · View at Scopus
  11. S. Jobling, “Review of suggested testing methods for endocrine-disrupting chemicals,” Pure and Applied Chemistry, vol. 70, no. 9, pp. 1805–1827, 1998. View at Google Scholar · View at Scopus
  12. C. R. Tyler, S. Jobling, and J. P. Sumpter, “Endocrine disruption in wildlife: a critical review of the evidence,” Critical Reviews in Toxicology, vol. 28, no. 4, pp. 319–361, 1998. View at Google Scholar · View at Scopus
  13. N. K. Brar, C. Waggoner, J. A. Reyes, R. Fairey, and K. M. Kelley, “Evidence for thyroid endocrine disruption in wild fish in San Francisco Bay, California, USA. Relationships to contaminant exposures,” Aquatic Toxicology, vol. 96, no. 3, pp. 203–215, 2010. View at Publisher · View at Google Scholar · View at Scopus
  14. F. Brucker-Davis, “Effects of environmental synthetic chemicals on thyroid function,” Thyroid, vol. 8, no. 9, pp. 827–856, 1998. View at Google Scholar · View at Scopus
  15. D. Raldúa and P. J. Babin, “Simple, rapid zebrafish larva bioassay for assessing the potential of chemical pollutants and drugs to disrupt thyroid gland function,” Environmental Science and Technology, vol. 43, no. 17, pp. 6844–6850, 2009. View at Publisher · View at Google Scholar · View at Scopus
  16. R. M. Rolland, “A review of chemically-induced alterations in thyroid and vitamin A status from field studies of wildlife and fish,” Journal of Wildlife Diseases, vol. 36, no. 4, pp. 615–635, 2000. View at Google Scholar · View at Scopus
  17. X. Shi, C. Liu, G. Wu, and B. Zhou, “Waterborne exposure to PFOS causes disruption of the hypothalamus-pituitary-thyroid axis in zebrafish larvae,” Chemosphere, vol. 77, no. 7, pp. 1010–1018, 2009. View at Publisher · View at Google Scholar · View at Scopus
  18. R. T. Zoeller, “Challenges confronting risk analysis of potential thyroid toxicants,” Risk Analysis, vol. 23, no. 1, pp. 143–162, 2003. View at Publisher · View at Google Scholar · View at Scopus
  19. S. J. Degitz, G. W. Holcombe, K. M. Flynn, P. A. Kosian, J. J. Korte, and J. E. Tietge, “Progress towards development of an amphibian-based thyroid screening assay using Xenopus laevis. Organismal and thyroidal responses to the model compounds 6-propylthiouracil, methimazole, and thyroxine,” Toxicological Sciences, vol. 87, no. 2, pp. 353–364, 2005. View at Publisher · View at Google Scholar · View at Scopus
  20. W. Kloas, “Amphibians as a model for the study of endocrine disruptors,” International Review of Cytology, vol. 216, pp. 1–57, 2002. View at Publisher · View at Google Scholar · View at Scopus
  21. R. Opitz, T. Braunbeck, C. Bögi et al., “Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds,” Environmental Toxicology and Chemistry, vol. 24, no. 3, pp. 653–664, 2005. View at Publisher · View at Google Scholar · View at Scopus
  22. R. Opitz, G. Levy, I. Lutz, and W. Kloas, “Development of molecular biomarkers to detect thyroid-disrupting activities of environmental chemicals in Xenopus laevis tadpoles,” in Proceedings of the 21st Conference of European Comparative Endocrinologists, R. Keller, H. Dircksen, D. Sedlmeier, and H. Vaudry, Eds., pp. 99–102, Monduzi Editore S.p.A., Bonn, Germany, August 2002.
  23. OECD, OECD Guideline for the Testing of Chemicals—The Amphibian Metamorphosis Assay. In Effects on Biotic Systems Environmental Health and Safety Publications, Paris, France, 2009.
  24. T. Damstra, S. Barlow, A. Bergman, R. Kavlock, and G. Van der Kraak, “Global assessment of the state-of-the-science of endocrine disruptors, International Programme on Chemical Safety, prepared by an expert group on behalf of the World Health Organisation, the International Labour Organisation, and the United Nations Environment Programme,” 2002. View at Google Scholar
  25. D. M. Janz, “Endocrine System,” in The Laboratory Fish, G. K. Ostrander, Ed., chapter 25, Academic Press, San Diego, Calif, USA, 2000. View at Google Scholar
  26. K. Lagler, J. Bardach, R. Miller, and D. Passino, Ichthyology, John Wiley & Sons, New York, NY, USA, 2nd edition, 1977.
  27. M. E. Baker, B. Ruggeri, L. J. Sprague et al., “Analysis of endocrine disruption in southern California coastal fish using an aquatic multispecies microarray,” Environmental Health Perspectives, vol. 117, no. 2, pp. 223–230, 2009. View at Publisher · View at Google Scholar · View at Scopus
  28. L. R. Iwanowicz, V. S. Blazer, S. D. McCormick, P. A. VanVeld, and C. A. Ottinger, “Aroclor 1248 exposure leads to immunomodulation, decreased disease resistance and endocrine disruption in the brown bullhead, Ameiurus nebulosus,” Aquatic Toxicology, vol. 93, no. 1, pp. 70–82, 2009. View at Publisher · View at Google Scholar · View at Scopus
  29. R. D. Moccia, J. F. Leatherland, and R. A. Sonstegard, “Increasing frequency of thyroid goiters in Coho salmon (Oncorhynchus kisutch) in the Great Lakes,” Science, vol. 198, no. 4315, pp. 425–426, 1977. View at Google Scholar · View at Scopus
  30. R. D. Moccia, J. F. Leatherland, and R. A. Sonstegard, “Quantitative interlake comparison of thyroid pathology in Great Lakes coho (Oncorhynchus kisutch) and chinook (Oncorhynchus tschawytscha) salmon,” Cancer Research, vol. 41, no. 6, pp. 2200–2210, 1981. View at Google Scholar · View at Scopus
  31. I. Morgado, M. A. Campinho, R. Costa, R. Jacinto, and D. M. Power, “Disruption of the thyroid system by diethylstilbestrol and ioxynil in the sea bream (Sparus aurata),” Aquatic Toxicology, vol. 92, no. 4, pp. 271–280, 2009. View at Publisher · View at Google Scholar · View at Scopus
  32. J. G. Schnitzler, E. Koutrakis, U. Siebert, J. P. Thomé, and K. Das, “Effects of persistent organic pollutants on the thyroid function of the European sea bass (Dicentrarchus labrax) from the Aegean sea, is it an endocrine disruption?” Marine Pollution Bulletin, vol. 56, no. 10, pp. 1755–1764, 2008. View at Publisher · View at Google Scholar · View at Scopus
  33. A. M. Coimbra and M. A. Reis-Henriques, “Tilapia larvae aroclor 1254 exposure: effects on gonads and circulating thyroid hormones during adulthood,” Bulletin of Environmental Contamination and Toxicology, vol. 79, no. 5, pp. 488–493, 2007. View at Publisher · View at Google Scholar · View at Scopus
  34. H. M. Crane, D. B. Pickford, T. H. Hutchinson, and J. A. Brown, “The effects of methimazole on development of the fathead minnow, Pimephales promelas, from embryo to adult,” Toxicological Sciences, vol. 93, no. 2, pp. 278–285, 2006. View at Google Scholar
  35. O. A. Elsalini and K. B. Rohr, “Phenylthiourea disrupts thyroid function in developing zebrafish,” Development Genes and Evolution, vol. 212, no. 12, pp. 593–598, 2003. View at Google Scholar · View at Scopus
  36. F. Liu, A. Gentles, and C. W. Theodorakis, “Arsenate and perchlorate toxicity, growth effects, and thyroid histopathology in hypothyroid zebrafish Danio rerio,” Chemosphere, vol. 71, no. 7, pp. 1369–1376, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. S. Mukhi and R. Patiño, “Effects of prolonged exposure to perchlorate on thyroid and reproductive function in zebrafish,” Toxicological Sciences, vol. 96, no. 2, pp. 246–254, 2007. View at Publisher · View at Google Scholar · View at Scopus
  38. J. W. Park, C. M. Bradford, J. Rinchard et al., “Uptake, elimination, and relative distribution of perchlorate in various tissues of channel catfish,” Environmental Science and Technology, vol. 41, no. 21, pp. 7581–7586, 2007. View at Publisher · View at Google Scholar · View at Scopus
  39. R. Patiño, M. R. Wainscott, E. I. Cruz-Li et al., “Effects of ammonium perchlorate on the reproductive performance and thyroid follicle histology of zebrafish,” Environmental Toxicology and Chemistry, vol. 22, no. 5, pp. 1115–1121, 2003. View at Publisher · View at Google Scholar · View at Scopus
  40. M. Picard-Aitken, H. Fournier, R. Pariseau, D. J. Marcogliese, and D. G. Cyr, “Thyroid disruption in walleye (Sander vitreus) exposed to environmental contaminants: cloning and use of iodothyronine deiodinases as molecular biomarkers,” Aquatic Toxicology, vol. 83, no. 3, pp. 200–211, 2007. View at Publisher · View at Google Scholar · View at Scopus
  41. L. T. van der Ven, E. J. van den Brandhof, J. H. Vos, D. M. Power, and P. W. Wester, “Effects of the antithyroid agent propylthiouracil in a partial life cycle assay with zebrafish,” Environmental Science and Technology, vol. 40, no. 1, pp. 74–81, 2006. View at Publisher · View at Google Scholar · View at Scopus
  42. R. Kirubagaran and K. P. Joy, “Toxic effects of mercurials on thyroid function of the catfish, Clarias batrachus (L.),” Ecotoxicology and Environmental Safety, vol. 17, no. 3, pp. 265–271, 1989. View at Publisher · View at Google Scholar · View at Scopus
  43. R. N. Ram, “Carbofuran-induced histophysiological changes in thyroid of the teleost fish, Channa punctatus (Bloch),” Ecotoxicology and Environmental Safety, vol. 16, no. 2, pp. 106–113, 1988. View at Publisher · View at Google Scholar · View at Scopus
  44. R. N. Ram and A. G. Sathyanesan, “Histopathological changes in liver and thyroid of the teleost fish, Channa punctatus (Bloch), in response to ammonium sulfate fertilizer treatment,” Ecotoxicology and Environmental Safety, vol. 13, no. 2, pp. 185–190, 1987. View at Google Scholar · View at Scopus
  45. C. A. de Wit, “An overview of brominated flame retardants in the environment,” Chemosphere, vol. 46, no. 5, pp. 583–624, 2002. View at Publisher · View at Google Scholar · View at Scopus
  46. J. Legler and A. Brouwer, “Are brominated flame retardants endocrine disruptors?” Environment International, vol. 29, no. 6, pp. 879–885, 2003. View at Publisher · View at Google Scholar · View at Scopus
  47. P. A. Buffler, M. A. Kelsh, E. C. Lau et al., “Thyroid function and perchlorate in drinking water: an evaluation among California newborns, 1998,” Environmental Health Perspectives, vol. 114, no. 5, pp. 798–804, 2006. View at Publisher · View at Google Scholar · View at Scopus
  48. Y. Yoshiura, Y. C. Sohn, A. Munakata, M. Kobayashi, and K. Aida, “Molecular cloning of the cDNA encoding the β subunit of thyrotropin and regulation of its gene expression by thyroid hormones in the goldfish, Carassius auratus,” Fish Physiology and Biochemistry, vol. 21, no. 3, pp. 201–210, 1999. View at Google Scholar · View at Scopus
  49. J. G. Eales, S. B. Brown, D. G. Cyr, B. A. Adams, and K. R. Finnson, “Deiodination as an index of chemical disruption of thyroid hormone homeostasis and thyroidal status in fish,” in Environmental Toxicology and Risk Assessment: Standardization of Biomarkers for Endocrine Disruption and Environmental Assessment, D. S. Henshel, M. C. Black, and M. C. Harrass, Eds., vol. 8, American Society for Testing and Materials, 1999. View at Google Scholar
  50. J. F. Leatherland, R. W. Hilliard, D. J. Macey, and I. C. Potter, “Changes in serum thyroxine and triiodothyronine concentrations during metamorphosis of the Southern Hemisphere Lamprey Geotria australis, and the effect of propylthiouracil, triiodothyronine and environmental temperature on serum thyroid hormone concentrations of ammocoetes,” Fish Physiology and Biochemistry, vol. 8, no. 2, pp. 167–177, 1990. View at Publisher · View at Google Scholar · View at Scopus
  51. J. G. Eales, “Thyroid function in cyclostomes and fishes,” in Hormones and Evolution, E. J. Barrington, Ed., vol. 1, pp. 341–436, Academic Press, New York, NY, USA, 1979. View at Google Scholar
  52. J. C. Raine, A. Takemura, and J. F. Leatherland, “Assessment of thyroid function in adult medaka (Oryzias latipes) and juvenile rainbow trout (Oncorhynchus mykiss) using immunostaining methods,” Journal of Experimental Zoology, vol. 290, no. 4, pp. 366–378, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. M. A. N. Wabuke-Bunoti and C. E. Firling, “The prehatching development of the thyroid gland of the fathead minnow, Pimephales promelas (Rafinesque),” General and Comparative Endocrinology, vol. 49, no. 2, pp. 320–331, 1983. View at Google Scholar · View at Scopus
  54. B. Alt, O. A. Elsalini, P. Schrumpf et al., “Arteries define the position of the thyroid gland during its developmental relocalisation,” Development, vol. 133, no. 19, pp. 3797–3804, 2006. View at Publisher · View at Google Scholar · View at Scopus
  55. T. Wendl, K. Lun, M. Mione et al., “pax2.1 is required for the development of thyroid follicles in zebrafish,” Development, vol. 129, no. 15, pp. 3751–3760, 2002. View at Google Scholar · View at Scopus
  56. O. A. Elsalini, J. von Gartzen, M. Cramer, and K. B. Rohr, “Zebrafish hhex, nk2.1a, and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors,” Developmental Biology, vol. 263, no. 1, pp. 67–80, 2003. View at Publisher · View at Google Scholar · View at Scopus
  57. M. De Felice and R. Di Lauro, “Thyroid development and its disorders: genetics and molecular mechanisms,” Endocrine Reviews, vol. 25, no. 5, pp. 722–746, 2004. View at Publisher · View at Google Scholar · View at Scopus
  58. N. Le Douarin, J. Fontaine, and C. Le Lievre, “New studies on the neural crest origin of the avian ultimobranchial glandular cells—interspecific combinations and cytochemical characterization of C cells based on the uptake of biogenic amine precursors,” Histochemistry, vol. 38, no. 4, pp. 297–305, 1974. View at Google Scholar · View at Scopus
  59. C. S. Le Lievre and N. M. Le Douarin, “Mesenchymal derivatives of the neural crest: analysis of chimaeric quail and chick embryos,” Journal of Embryology and Experimental Morphology, vol. 34, no. 1, pp. 125–154, 1975. View at Google Scholar · View at Scopus
  60. B. Alt, S. Reibe, N. M. Feitosa, O. A. Elsalini, T. Wendl, and K. B. Rohr, “Analysis of origin and growth of the thyroid gland in zebrafish,” Developmental Dynamics, vol. 235, no. 7, pp. 1872–1883, 2006. View at Publisher · View at Google Scholar · View at Scopus
  61. R. S. Kasper, N. Shved, A. Takahashi, M. Reinecke, and E. Eppler, “A systematic immunohistochemical survey of the distribution patterns of GH, prolactin, somatolactin, beta-TSH, beta-FSH, beta-LH, ACTH, and alpha-MSH in the adenohypophysis of Oreochromis niloticus, the Nile tilapia,” Cell and Tissue Research, vol. 325, no. 2, pp. 303–313, 2006. View at Google Scholar
  62. R. E. Peter, K. L. Yu, T. A. Marchant, and P. M. Rosenblum, “Direct neural regulation of the teleost adenohypophysis,” Journal of Experimental Zoology, vol. 255, no. 4, pp. 84–89, 1990. View at Google Scholar · View at Scopus
  63. D. E. Kime, Endocrine Disruption in Fish, Kluwer Academic Publishers, Boston, Mass, USA, 1998.
  64. F. A. Weltzien, E. Andersson, Ø. Andersen, K. Shalchian-Tabrizi, and B. Norberg, “The brain-pituitary-gonad axis in male teleosts, with special emphasis on flatfish (Pleuronectiformes),” Comparative Biochemistry and Physiology—A Molecular and Integrative Physiology, vol. 137, no. 3, pp. 447–477, 2004. View at Publisher · View at Google Scholar · View at Scopus
  65. A. García Ayala, M. Villaplana, M. P. García Hernández, E. Chaves Pozo, and B. Agulleiro, “FSH-, LH-, and TSH-expressing cells during development of Sparus aurata L. (Teleostei). An immunocytochemical study,” General and Comparative Endocrinology, vol. 134, no. 1, pp. 72–79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. J. L. Leunissen, A. M. de Leeuw, J. Peute, and H. J. Goos, “Immunocytochemistry of gonadotropic cells and identification of cell types in ultrathin cryosections of the pituitary of the rainbow trout, Salmo gairdneri,” Cell and Tissue Research, vol. 226, no. 1, pp. 177–194, 1982. View at Google Scholar · View at Scopus
  67. J. Quesada, M. T. Lozano, A. Ortega, and B. Agulleiro, “Immunocytochemical and ultrastructural characterization of the cell types in the adenohypophysis of Sparus aurata L. (Teleost),” General and Comparative Endocrinology, vol. 72, no. 2, pp. 209–225, 1988. View at Google Scholar · View at Scopus
  68. H. Ueda, G. Young, and Y. Nagahama, “Immunocytochemical identification of thyrotropin (TSH)-producing cells in pituitary glands of several species of teleosts with antiserum to human TSH β subunit,” Cell and Tissue Research, vol. 231, no. 1, pp. 199–204, 1983. View at Google Scholar · View at Scopus
  69. S. Garcia-Navarro, M. M. Malagon, and F. Gracia-Navarro, “Immunohistochemical localization of thyrotropic cells during amphibian morphogenesis: a stereological study,” General and Comparative Endocrinology, vol. 71, no. 1, pp. 116–123, 1988. View at Google Scholar · View at Scopus
  70. L. A. Miranda, D. A. Paz, R. Dezi, and A. Pisanó, “Immunocytochemical and morphometric study on the changes of TSH, PRL, GH and ACTH cells during the development of Bufo arenarum,” Cell and Tissue Research, vol. 283, no. 1, pp. 125–132, 1996. View at Publisher · View at Google Scholar · View at Scopus
  71. K. Ogawa, E. Suzuki, and K. Taniguchi, “Immunohistochemical studies on the development of TSH cells in the pituitary of Xenopus laevis larvae,” The Journal of Veterinary Medical Science, vol. 57, no. 3, pp. 539–542, 1995. View at Google Scholar · View at Scopus
  72. D. S. Cooper, “Antithyroid drugs,” New England Journal of Medicine, vol. 352, no. 9, pp. 905–917, 2005. View at Publisher · View at Google Scholar · View at Scopus
  73. A. Orozco, M. C. Jeziorski, P. J. Linser, R. M. Greenberg, and C. Valverde-R, “Cloning of the gene and complete cDNA encoding a type 2 deiodinase from Fundulus heteroclitus,” General and Comparative Endocrinology, vol. 128, no. 2, pp. 162–167, 2002. View at Publisher · View at Google Scholar · View at Scopus
  74. A. Orozco, P. Villalobos, M. C. Jeziorski, and C. Valverde-R, “The liver of Fundulus heteroclitus expresses deiodinase type 1 mRNA,” General and Comparative Endocrinology, vol. 130, no. 1, pp. 84–91, 2003. View at Publisher · View at Google Scholar · View at Scopus
  75. JO. P. Sanders, S. Van der Geyten, E. Kaptein et al., “Characterization of a propylthiouracil-insensitive type I iodothyronine deiodinase,” Endocrinology, vol. 138, no. 12, pp. 5153–5160, 1997. View at Google Scholar · View at Scopus
  76. J. P. Sanders, S. Van der Geyten, E. Kaptein et al., “Cloning and characterization of type III iodothyronine deiodinase from the fish Oreochromis niloticus,” Endocrinology, vol. 140, no. 8, pp. 3666–3673, 1999. View at Google Scholar · View at Scopus
  77. C. Valverde-R, W. Croteau, G. J. Lafleur Jr., A. Orozco, and D. L. ST. Germain, “Cloning and expression of a 5-iodothyronine deiodinase from the liver of Fundulus heteroclitus,” Endocrinology, vol. 138, no. 2, pp. 642–648, 1997. View at Publisher · View at Google Scholar · View at Scopus
  78. D. S. Cooper and S. A. Rivkees, “Putting propylthiouracil in perspective,” Journal of Clinical Endocrinology and Metabolism, vol. 94, no. 6, pp. 1881–1882, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. N. Momotani, R. Yamashita, F. Makino et al., “Thyroid function in wholly breast-feeding infants whose mothers take high doses of propylthiouracil,” Clinical Endocrinology, vol. 53, no. 2, pp. 177–181, 2000. View at Publisher · View at Google Scholar · View at Scopus
  80. K. C. Grim, M. Wolfe, T. Braunbeck et al., “Thyroid histopathology assessments for the amphibian metamorphosis assay to detect thyroid-active substances,” Toxicologic Pathology, vol. 37, no. 4, pp. 415–424, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. R. Opitz, S. Hartmann, T. Blank, T. Braunbeck, I. Lutz, and W. Kloas, “Evaluation of histological and molecular endpoints for enhanced detection of thyroid system disruption in Xenopus laevis tadpoles,” Toxicological Sciences, vol. 90, no. 2, pp. 337–348, 2006. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Opitz, F. Schmidt, T. Braunbeck, S. Wuertz, and W. Kloas, “Perchlorate and ethylenethiourea induce different histological and molecular alterations in a non-mammalian vertebrate model of thyroid goitrogenesis,” Molecular and Cellular Endocrinology, vol. 298, no. 1-2, pp. 101–114, 2009. View at Publisher · View at Google Scholar · View at Scopus
  83. B. Romeis, Mikroskopische Technik, Urban und Schwarzenberg, 1989.
  84. G. Grandi and M. Chicca, “Early development of the pituitary gland in Acipenser naccarii (Chondrostei, Acipenseriformes): an immunocytochemical study,” Anatomy and Embryology, vol. 208, no. 4, pp. 311–321, 2004. View at Google Scholar · View at Scopus
  85. M. J. Karnovsky, “Use of ferrocyanide-reduced osmium tetroxide in electron microscopy,” The Journal of Cell Biology, vol. 51, p. 146A, 1971. View at Google Scholar
  86. A. R. Spurr, “A low-viscosity epoxy resin embedding medium for electron microscopy,” Journal of Ultrasructure Research, vol. 26, no. 1-2, pp. 31–43, 1969. View at Google Scholar · View at Scopus
  87. K. C. Richardson, L. Jarett, and E. H. Finke, “Embedding in epoxy resins for ultrathin sectioning in electron microscopy,” Stain technology, vol. 35, pp. 313–323, 1960. View at Google Scholar · View at Scopus
  88. E. S. Reynolds, “The use of lead citrate at high pH as an electron-opaque stain in electron microscopy,” The Journal of Cell Biology, vol. 17, pp. 208–212, 1963. View at Google Scholar · View at Scopus
  89. J. M. Connors, L. J. Huffman, and G. A. Hedge, “Effects of thyrotropin on the vascular conductance of the thyroid gland,” Endocrinology, vol. 122, no. 3, pp. 921–929, 1988. View at Google Scholar · View at Scopus
  90. J. M. Connors, L. J. Huffman, M. Michalkiewicz, B. S. Chang, R. D. Dey, and G. A. Hedge, “Thyroid vascular conductance: differential effects of elevated plasma thyrotropin (TSH) induced by treatment with thioamides or TSH-releasing hormone,” Endocrinology, vol. 129, no. 1, pp. 117–125, 1991. View at Google Scholar · View at Scopus
  91. W. L. Goleman, L. J. Urquidi, T. A. Anderson, E. E. Smith, R. J. Kendall, and J. A. Carr, “Environmentally relevant concentrations of ammonium perchlorate inhibit development and metamorphosis in Xenopus laevis,” Environmental Toxicology and Chemistry, vol. 21, no. 2, pp. 424–430, 2002. View at Google Scholar · View at Scopus
  92. K. Yamasaki, Y. Tago, K. Nagai, M. Sawaki, S. Noda, and M. Takatsuki, “Comparison of toxicity studies based on the draft protocol for the ‘Enhanced OECD Test Guideline no. 407’ and the research protocol of ‘Pubertal Development and Thyroid Function in Immature Male Rats’ with 6-n-propyl-2-thiouracil,” Archives of Toxicology, vol. 76, no. 9, pp. 495–501, 2002. View at Publisher · View at Google Scholar · View at Scopus
  93. B. Pradet-Balade, C. Burel, S. Dufour et al., “Thyroid hormones down-regulate thyrotropin β mRNA level in vivo in the turbot (Psetta maxima),” Fish Physiology and Biochemistry, vol. 20, no. 3, pp. 193–199, 1999. View at Google Scholar · View at Scopus
  94. N. R. Farid and M. W. Szkudlinski, “Minireview: structural and functional evolution of the thyrotropin receptor,” Endocrinology, vol. 145, no. 9, pp. 4048–4057, 2004. View at Publisher · View at Google Scholar · View at Scopus
  95. D. S. MacKenzie, R. A. Jones, and T. C. Miller, “Thyrotropin in teleost fish,” General and Comparative Endocrinology, vol. 161, no. 1, pp. 83–89, 2009. View at Publisher · View at Google Scholar · View at Scopus
  96. B. B. Rees, F. A. Sudradjat, and J. W. Love, “Acclimation to hypoxia increases survival time of zebrafish, Danio rerio, during lethal hypoxia,” Journal of Experimental Zoology, vol. 289, no. 4, pp. 266–272, 2001. View at Publisher · View at Google Scholar · View at Scopus
  97. R. Strecker, T. B. Seiler, H. Hollert, and T. Braunbeck, “Oxygen requirements of zebrafish (Danio rerio) embryos in embryo toxicity tests with environmental samples. Comparative biochemistry and physiology,” Toxicology & Pharmacology, vol. 153, no. 3, pp. 318–327, 2011. View at Google Scholar
  98. J. D. Via, G. Vandenthillart, O. Cattani, and A. de Zwaan, “Influence of long-term hypoxia exposure on the energy metabolism of Solea solea. 2. Intermediary metabolism in blood, liver and muscle,” Marine Ecology Progress Series, vol. 111, no. 1-2, pp. 17–27, 1994. View at Google Scholar · View at Scopus
  99. J. C. Rankin and F. B. Jensen, Fish Ecophysiologyl, Chapman & Halll, Boca Raton, Fla, USA, 1993.
  100. H. M. Crane, D. B. Pickford, T. H. Hutchinson, and J. A. Brown, “Effects of ammonium perchlorate on thyroid function in developing fathead minnows, Pimephales promelas,” Environmental Health Perspectives, vol. 113, no. 4, pp. 396–401, 2005. View at Publisher · View at Google Scholar · View at Scopus
  101. A. Anderberg, S. Enestrom, and J. Gillquist, “Protein composition in single follicles, homogenates and fine-needle aspiration biopsies from normal and diseased human thyroid,” Acta Endocrinologica, vol. 96, no. 3, pp. 328–334, 1981. View at Google Scholar
  102. B. Anderberg, S. Enestrom, J. Gillquist, and S. Smeds, “Protein composition of the thyroid colloid in patients with hyperthyroidism,” Journal of Endocrinology, vol. 86, no. 3, pp. 443–449, 1980. View at Google Scholar · View at Scopus
  103. V. Pitsiavas, P. Smerdely, MU. Li, and S. C. Boyages, “Amiodarone induces a different pattern of ultrastructural change in the thyroid to iodine excess alone in both the BB/W rat and the Wistar rat,” European Journal of Endocrinology, vol. 137, no. 1, pp. 89–98, 1997. View at Publisher · View at Google Scholar · View at Scopus
  104. E. M. Allen, “The effect of iodine on lipid peroxidation and ultrastructure in the thyroids of BB/Wor rats,” Journal of Endocrinological Investigation, vol. 15, no. 7, pp. 519–523, 1992. View at Google Scholar · View at Scopus
  105. R. C. A. Onderwater, J. N. M. Commandeur, E. J. Groot, A. Sitters, W. M. P. B. Menge, and N. P. E. Vermeulen, “Cytotoxicity of a series of mono- and di-substituted thiourea in freshly isolated rat hepatocytes: a preliminary structure-toxicity relationship study,” Toxicology, vol. 125, no. 2-3, pp. 117–129, 1998. View at Publisher · View at Google Scholar · View at Scopus
  106. P. C. Adams, G. J. Gibson, and A. R. Morley, “Amiodarone pulmonary toxicity: clinical and subclinical features,” Quarterly Journal of Medicine, vol. 59, no. 229, pp. 449–471, 1986. View at Google Scholar
  107. J. G. Eales and S. B. Brown, “Measurement and regulation of thyroidal status in teleost fish,” Reviews in Fish Biology and Fisheries, vol. 3, no. 4, pp. 299–347, 1993. View at Publisher · View at Google Scholar · View at Scopus
  108. L. A. Miranda, A. Pisanó, and V. Casco, “Ultrastructural study on thyroid glands of Bufo arenarum larvae kept in potassium perchlorate solution,” Biocell, vol. 20, no. 2, pp. 147–153, 1996. View at Google Scholar · View at Scopus
  109. W. L. Goleman, J. A. Carr, and T. A. Anderson, “Environmentally relevant concentrations of ammonium perchlorate inhibit thyroid function and alter sex ratios in developing Xenopus laevis,” Environmental Toxicology and Chemistry, vol. 21, no. 3, pp. 590–597, 2002. View at Google Scholar · View at Scopus
  110. R. J. Handa and R. B. Chiasson, “Comparative effects of three goitrogenic treatments on White Leghorn chickens,” Avian Diseases, vol. 24, no. 4, pp. 916–929, 1980. View at Google Scholar · View at Scopus
  111. J. G. Pierce and T. F. Parsons, “Glycoprotein hormones: structure and function,” Annual Review of Biochemistry, vol. 50, pp. 465–495, 1981. View at Google Scholar · View at Scopus
  112. J. C. O'Connor, S. R. Frame, L. G. Davis, and J. C. Cook, “Detection of thyroid toxicants in a Tier I screening battery and alterations in thyroid endpoints over 28 days of exposure,” Toxicological Sciences, vol. 51, no. 1, pp. 54–70, 1999. View at Publisher · View at Google Scholar · View at Scopus
  113. W. Mellert, K. Deckardt, J. Walter, S. Gfatter, and B. Van Ravenzwaay, “Detection of endocrine-modulating effects of the antithyroid acting drug 6-propyl-2-thiouracil in rats, based on the “Enhanced OECD Test Guideline 407”,” Regulatory Toxicology and Pharmacology, vol. 38, no. 3, pp. 368–377, 2003. View at Publisher · View at Google Scholar · View at Scopus
  114. D. M. Power, L. Llewellyn, M. Faustino et al., “Thyroid hormones in growth and development of fish,” Comparative Biochemistry and Physiology—C Toxicology and Pharmacology, vol. 130, no. 4, pp. 447–459, 2001. View at Publisher · View at Google Scholar · View at Scopus
  115. P. P. Morin, T. J. Hara, and J. G. Eales, “Thyroid hormone deiodination in brain, liver, gill, heart and muscle of atlantic salmon (Salmo salar) during photoperiodically-induced parr-smolt transformation. I. Outer- and inner-ring thyroxine deiodination,” General and Comparative Endocrinology, vol. 90, no. 2, pp. 142–156, 1993. View at Publisher · View at Google Scholar · View at Scopus
  116. T. Braunbeck, V. Storch, and H. Bresch, “Species-specific reaction of liver ultrastructure in Zebrafish (Brachydanio rerio) and trout (Salmo gairdneri) after prolonged exposure to 4-chloroaniline,” Archives of Environmental Contamination and Toxicology, vol. 19, no. 3, pp. 405–418, 1990. View at Google Scholar
  117. M. Benyounes, C. Sempoux, C. Daumerie, J. Rahier, and A. P. Geubel, “Propylthiouracyl-induced severe liver toxicity: an indication for alanine aminotransferase monitoring?” World Journal of Gastroenterology, vol. 12, no. 38, pp. 6232–6234, 2006. View at Google Scholar · View at Scopus
  118. D. S. Cooper, “The side effects of antithyroid drugs,” Endocrinologist, vol. 9, no. 6, pp. 457–467, 1999. View at Google Scholar · View at Scopus
  119. W. A. Parker, “Propylthiouracil-induced hepatotoxicity,” Clinical Pharmacology, vol. 1, no. 5, pp. 471–474, 1982. View at Google Scholar
  120. R. Deidiker and D. E. Demello, “Propylthiouracil-induced fulminant hepatitis: case report and review of the literature,” Pediatric Pathology and Laboratory Medicine, vol. 16, no. 5, pp. 845–852, 1996. View at Publisher · View at Google Scholar · View at Scopus