Perchlorate and ethylenethiourea induce different histological and molecular alterations in a non-mammalian vertebrate model of thyroid goitrogenesis

Molecular and Cellular Endocrinology

Volumn 298, Issue 1-2, 2009, Pages 101-114

  Opitz, R ^a   Schmidt, F ^b   Braunbeck, T ^b   Wuertz, S ^a   Kloas, W ^a,c  

^a LEIBNIZ INSTITUTE OF FRESHWATER ECOLOGY AND INLAND FISHERIES   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c HUMBOLDT UNIVERSITY   (Germany)

Author keywords

Gene expression; Goiter; Thyroid gland; Thyroid stimulating hormone; Xenopus

Indexed keywords

2 IMIDAZOLIDINETHIONE; PERCHLORATE; THYROID HORMONE;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL CYCLE; CELL PROLIFERATION; CELLULAR STRESS RESPONSE; CONTROLLED STUDY; DNA REPLICATION; GENE EXPRESSION; GOITER; GROWTH RETARDATION; HISTOPATHOLOGY; HORMONE INHIBITION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEIN SYNTHESIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; THYROID HORMONE METABOLISM; THYROID HORMONE RELEASE; THYROID HORMONE SYNTHESIS; UNINDEXED SEQUENCE; UPREGULATION; XENOPUS LAEVIS;

ANIMALS; ANTITHYROID AGENTS; BRAIN; DISEASE MODELS, ANIMAL; ENDOCRINE DISRUPTORS; ETHYLENETHIOUREA; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GOITER; LIFE CYCLE STAGES; PERCHLORIC ACID; THYROID GLAND; THYROTROPIN; VERTEBRATES; XENOPUS LAEVIS;

EID: 57749207038     PISSN: 03037207     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mce.2008.08.020     Document Type: Article

References (75)

1. Adler V., Yin Z., Fuchs S.Y., Benezra M., Rosario L., Tew K.D., Pincus M.R., Sardana M., Henderson C.J., Wolf C.R., Davis R.J., and Ronai Z. Regulation of JNK signaling by GSTp. EMBO J. 18 (1999) 1321-1334
2. Arvan P., Kim P.S., Kuliawat R., Prabakaran D., Muresan Z., Yoo S.E., and Abu H.S. Intracellular protein transport to the thyrocyte plasma membrane: potential implications for thyroid physiology. Thyroid 7 (1997) 89-105
3. Baris O., Savagner F., Nasser V., Loriod B., Granjeaud S., Guyetant S., Franc B., Rodien P., Rohmer V., Bertucci F., Birnbaum D., Malthiery Y., Reynier P., and Houlgatte R. Transcriptional profiling reveals coordinated up-regulation of oxidative metabolism genes in thyroid oncocytic tumors. J. Clin. Endocrinol. Metab. 89 (2004) 994-1005
4. Baryshev M., Sargsyan E., Wallin G., Lejnieks A., Furudate S., Hishinuma A., and Mkrtchian S. Unfolded protein response is involved in the pathology of human congenital hypothyroid goiter and rat non-goitrous congenital hypothyroidism. J. Mol. Endocrinol. 32 (2004) 903-920
5. Bidey S.P., Hill D.J., and Eggo M.C. Growth factors and goitrogenesis. J. Endocrinol. 160 (1999) 321-332
6. Bradford C.M., Rinchard J., Carr J.A., and Theodorakis C. Perchlorate affects thyroid function in eastern mosquitofish (Gambusia holbrooki) at environmentally relevant concentrations. Environ. Sci. Technol. 39 (2005) 5190-5195
7. Bruhat A., Averous J., Carraro V., Zhong C., Reimold A.M., Kilberg M.S., and Fafournoux P. Differences in the molecular mechanisms involved in the transcriptional activation of the CHOP and asparagine synthetase genes in response to amino acid deprivation or activation of the unfolded protein response. J. Biol. Chem. 277 (2002) 48107-48114
8. Buckingham M.B. Effects of TSH and thiourea upon thyroid function in the lizard, Xantusia henshawi. Gen. Comp. Endocrinol. 14 (1970) 178-183
9. Calebiro D., de Filippis T., Lucchi S., Martinez F., Porazzi P., Trivellato R., Locati M., Beck-Peccoz P., and Persani L. Selective modulation of protein kinase A I and II reveals distinct roles in thyroid cell gene expression and growth. Mol. Endocrinol. 20 (2006) 3196-3211
10. Coleman R., Evennett P.J., and Dodd J.M. The ultrastructural localization of acid phosphatase, alkaline phosphatase and adenosine triphosphatase in induced goitres of Xenopus laevis Daudin tadpoles. Histochemie 10 (1967) 33-43
11. Das B., Cai L., Carter M.G., Piao Y.L., Sharov A.A., Ko M.S., and Brown D.D. Gene expression changes at metamorphosis induced by thyroid hormone in Xenopus laevis tadpoles. Dev. Biol. 291 (2006) 342-355
12. De Felice M., Postiglione M.P., and Di Lauro R. Thyrotropin receptor signaling in development and differentiation of the thyroid gland: insights from mouse models and human diseases. Endocrinology 145 (2004) 4062-4067
13. Denef J.F. Experimental goiter formation. Bull Mem. Acad. R. Med. Belg. 144 (1989) 313-318
14. Denef J.F., Haumont S., Cornette C., and Beckers C. Correlated functional and morphometric study of thyroid hyperplasia induced by iodine deficiency. Endocrinology 108 (1981) 2352-2358
15. Denver R.J., Pavgi S., and Shi Y.B. Thyroid hormone-dependent gene expression program for Xenopus neural development. J. Biol. Chem. 272 (1997) 8179-8188
16. Doerge D.R., and Takazawa R.S. Mechanism of thyroid peroxidase inhibition by ethylenethiourea. Chem. Res. Toxicol. 3 (1990) 98-101
17. - symporter (NIS) mediates electroneutral active transport of the environmental pollutant perchlorate. Proc. Natl. Acad. Sci. U.S.A. 104 (2007) 20250-20255
18. Dorak T. Real-Time PCR. Advanced Methods Series (2006), Taylor & Francis, Oxford
19. Dumont J.E., Lamy F., Roger P., and Maenhaut C. Physiological and pathological regulation of thyroid cell proliferation and differentiation by thyrotropin and other factors. Physiol. Rev. 72 (1992) 667-697
20. Dumont J.E., Maenhaut C., and Lamy F. Control of thyroid cell proliferation and goitrogenesis. Trends Endocrinol. Metab. 3 (1992) 12-17
21. Dunn J.T., and Dunn A.D. Update on intrathyroidal iodine metabolism. Thyroid 11 (2001) 407-414
22. Elsalini O.A., von Gartzen J., Cramer M., and Rohr K.B. Zebrafish hhex, nk2.1a, and pax2.1 regulate thyroid growth and differentiation downstream of Nodal-dependent transcription factors. Dev. Biol. 263 (2003) 67-80
23. Eng P.H., Cardona G.R., Fang S.L., Previti M., Alex S., Carrasco N., Chin W.W., and Braverman L.E. Escape from the acute Wolff-Chaikoff effect is associated with a decrease in thyroid sodium/iodide symporter messenger ribonucleic acid and protein. Endocrinology 140 (1999) 3404-3410
24. Furlow J.D., and Neff E.S. A developmental switch induced by thyroid hormone: Xenopus laevis metamorphosis. Trends Endocrinol. Metab. 17 (2006) 40-47
25. Gereben B., Salvatore D., Harney J.W., Tu H.M., and Larsen P.R. The human, but not rat, dio2 gene is stimulated by thyroid transcription factor-1 (TTF-1). Mol. Endocrinol. 15 (2001) 112-124
26. Glatt C.M., Ouyang M., Welsh W., Green J.W., Connor J.O., Frame S.R., Everds N.E., Poindexter G., Snajdr S., and Delker D.A. Molecular characterization of thyroid toxicity: anchoring gene expression profiles to biochemical and pathologic end points. Environ. Health Perspect. 113 (2005) 1354-1361
27. Grommen S.V., Taniuchi S., Janssen T., Schoofs L., Takahashi S., Takeuchi S., Darras V.M., and De Groef B. Molecular cloning, tissue distribution, and ontogenic thyroidal expression of the chicken thyrotropin receptor. Endocrinology 147 (2006) 3943-3951
28. Handa R.J., and Chiasson R.B. Comparative effects of three goitrogenic treatments on White Leghorn chickens. Avian Dis. 24 (1980) 916-929
29. Helbing C.C., Bailey C.M., Ji L., Gunderson M.P., Zhang F., Veldhoen N., Skirrow R.C., Mu R., Lesperance M., Holcombe G.W., Kosian P.A., Tietge J., Korte J.J., and Degitz S.J. Identification of gene expression indicators for thyroid axis disruption in a Xenopus laevis metamorphosis screening assay. Part 1. Effects on the brain. Aquat. Toxicol. 82 (2007) 227-241
30. Kameda Y. Dog thyroid glands after chronic administration of antithyroid drugs. Am. J. Pathol. 117 (1984) 316-325
31. Kimura T., Van Keymeulen A., Golstein J., Fusco A., Dumont J.E., and Roger P.P. Regulation of thyroid cell proliferation by TSH and other factors: a critical evaluation of in vitro models. Endocr. Rev. 22 (2001) 631-656
32. Kloas W. Amphibians as a model for the study of endocrine disruptors. Int. Rev. Cytol. 216 (2002) 1-57
33. Kohrle J., Jakob F., Contempre B., and Dumont J.E. Selenium, the thyroid, and the endocrine system. Endocr. Rev. 26 (2005) 944-984
34. Krause K., Karger S., Schierhorn A., Poncin S., Many M.C., and Fuhrer D. Proteomic profiling of cold thyroid nodules. Endocrinology 148 (2007) 1754-1763
35. Krohn K., Fuhrer D., Bayer Y., Eszlinger M., Brauer V., Neumann S., and Paschke R. Molecular pathogenesis of euthyroid and toxic multinodular goiter. Endocr. Rev. 26 (2005) 504-524
36. Lalli E., and Sassone-Corsi P. Thyroid-stimulating hormone (TSH)-directed induction of the CREM gene in the thyroid gland participates in the long-term desensitization of the TSH receptor. Proc. Natl. Acad. Sci. U.S.A. 92 (1995) 9633-9637
37. Leatherland J.F. Environmental physiology of the teleostean thyroid gland: a review. Environ. Biol. Fish. 7 (1982) 83-110
38. Lee M.C., and Miller E.A. Molecular mechanisms of COPII vesicle formation. Semin. Cell Dev. Biol. 18 (2007) 424-434
39. Lutz I., Kloas W., Springer T.A., Holden L.R., Wolf J.C., Krueger H.O., and Hosmer A.J. Development, standardization and refinement of procedures for evaluating effects of endocrine active compounds on development and sexual differentiation of Xenopus laevis. Anal. Bioanal. Chem. 390 (2008) 2031-2048
40. Maier J., van Steeg H., van Oostrom C., Paschke R., Weiss R.E., and Krohn K. Iodine deficiency activates antioxidant genes and causes DNA damage in the thyroid gland of rats and mice. Biochim. Biophys. Acta 1773 (2007) 990-999
41. Manzon R.G., and Denver R.J. Regulation of pituitary thyrotropin gene expression during Xenopus metamorphosis: negative feedback is functional throughout metamorphosis. J. Endocrinol. 182 (2004) 273-285
42. McNabb F.M. The hypothalamic-pituitary-thyroid (HPT) axis in birds and its role in bird development and reproduction. Crit. Rev. Toxicol. 37 (2007) 163-193
43. Miranda L.A., Pisano A., and Casco V. Ultrastructural study on thyroid glands of Bufo arenarum larvae kept in potassium perchlorate solution. Biocell 20 (1996) 147-153
44. Nieuwkoop P.D., and Faber J. Normal Table of Xenopus laevis (Daudin) (1994), Garland Publishing Inc., New York
45. Olen E. The fine structure of experimentally induced hyperplastic and colloid goiter in the hamster. Lab. Invest. 21 (1969) 336-346
46. Opitz R., Braunbeck T., Bogi C., Pickford D.B., Nentwig G., Oehlmann J., Tooi O., Lutz I., and Kloas W. Description and initial evaluation of a Xenopus metamorphosis assay for detection of thyroid system-disrupting activities of environmental compounds. Environ. Toxicol. Chem. 24 (2005) 653-664
47. Opitz R., Hartmann S., Blank T., Braunbeck T., Lutz I., and Kloas W. Evaluation of histological and molecular endpoints for enhanced detection of thyroid system disruption in Xenopus laevis tadpoles. Toxicol. Sci. 90 (2006) 337-348
48. Opitz R., Trubiroha A., Lorenz C., Lutz I., Hartmann S., Blank T., Braunbeck T., and Kloas W. Expression of sodium-iodide symporter mRNA in the thyroid gland of Xenopus laevis tadpoles: developmental expression, effects of antithyroidal compounds, and regulation by TSH. J. Endocrinol. 190 (2006) 157-170
49. 4 in propylthiouracil-hypothyroid rats. Acta Endocrinol. 103 (1983) 81-87
50. Oyadomari S., and Mori M. Roles of CHOP/GADD153 in endoplasmic reticulum stress. Cell Death Differ. 11 (2004) 381-389
51. Pedraza P.E., Obregon M.J., Escobar-Morreale H.F., del Rey F.E., and de Escobar G.M. Mechanisms of adaptation to iodine deficiency in rats: thyroid status is tissue specific. Its relevance for man. Endocrinology 147 (2006) 2098-2108
52. Pomerance M., Carapau D., Chantoux F., Mockey M., Correze C., Francon J., and Blondeau J.P. CCAAT/enhancer-binding protein-homologous protein expression and transcriptional activity are regulated by 3′,5′-cyclic adenosine monophosphate in thyroid cells. Mol. Endocrinol. 17 (2003) 2283-2294
53. Regard E. Cytophysiology of the amphibian thyroid gland through larval development and metamorphosis. Int. Rev. Cytol. 52 (1978) 81-118
54. Ron D., and Walter P. Signal integration in the endoplasmic reticulum unfolded protein response. Nat. Rev. Mol. Cell Biol. 8 (2007) 519-529
55. Ruscoe J.E., Rosario L.A., Wang T., Gate L., Arifoglu P., Wolf C.R., Henderson C.J., Ronai Z., and Tew K.D. Pharmacologic or genetic manipulation of glutathione S-transferase P1-1 (GSTpi) influences cell proliferation pathways. J. Pharmacol. Exp. Ther. 298 (2001) 339-345
56. Sargsyan E., Baryshev M., and Mkrtchian S. The physiological unfolded protein response in the thyroid epithelial cells. Biochem. Biophys. Res. Commun. 322 (2004) 570-576
57. Sato K., Yamazaki K., Shizume K., Kanaji Y., Obara T., Ohsumi K., Demura H., Yamaguchi S., and Shibuya M. Stimulation by thyroid-stimulating hormone and Grave's immunoglobulin G of vascular endothelial growth factor mRNA expression in human thyroid follicles in vitro and flt mRNA expression in the rat thyroid in vivo. J. Clin. Invest. 96 (1995) 1295-1302
58. Scipioni A., Ferretti E., Soda G., Tosi E., Bruno R., Costante G., Meringolo D., Arturi F., Durante C., Amorosi A., Foschini M.P., Nardi F., Russo D., and Filetti S. hNIS protein in thyroid: the iodine supply influences its expression and localization. Thyroid 17 (2007) 613-618
59. Shi Y.B. Amphibian Metamorphosis. From Morphology to Molecular Biology (1999), John Wiley & Sons, New York
60. Srisomsap C., Subhasitanont P., Otto A., Mueller E.C., Punyarit P., Wittmann-Liebold B., and Svasti J. Detection of cathepsin B up-regulation in neoplastic thyroid tissues by proteomic analysis. Proteomics 2 (2002) 706-712
61. Stoker T.E., Ferrell J.M., Laws S.C., Cooper R.L., and Buckalew A. Evaluation of ammonium perchlorate in the endocrine disruptor screening and testing program's male pubertal protocol: ability to detect effects on thyroid endpoints. Toxicology 228 (2006) 58-65
62. Tietge J.E., Holcombe G.W., Flynn K.M., Kosian P.A., Korte J.J., Anderson L.E., Wolf D.C., and Degitz S.J. Metamorphic inhibition of Xenopus laevis by sodium perchlorate: effects on development and thyroid histology. Environ. Toxicol. Chem. 24 (2005) 926-933
63. - symporter mRNAs in dog thyroid. Mol. Cell. Endocrinol. 131 (1997) 195-203
64. Van der Geyten S., Van den Eynde I., Segers I.B., Kuhn E.R., and Darras V.M. Differential expression of iodothyronine deiodinases in chicken tissues during the last week of embryonic development. Gen. Comp. Endocrinol. 128 (2002) 65-73
65. van Staveren W.C., Solis D.W., Delys L., Venet D., Cappello M., Andry G., Dumont J.E., Libert F., Detours V., and Maenhaut C. Gene expression in human thyrocytes and autonomous adenomas reveals suppression of negative feedbacks in tumorigenesis. Proc. Natl. Acad. Sci. U.S.A. 103 (2006) 413-418
66. van Staveren W.C., Detours V., Dumont J.E., and Maenhaut C. Negative feedbacks in normal cell growth and their suppression in tumorigenesis. Cell Cycle 5 (2006) 571-572
67. Vassart G., and Dumont J.E. The thyrotropin receptor and the regulation of thyrocyte function and growth. Endocr. Rev. 13 (1992) 596-611
68. Viglietto G., Romano A., Manzo G., Chiappetta G., Paoletti I., Califano D., Galati M.G., Mauriello V., Bruni P., Lago C.T., Fusco A., and Persico M.G. Upregulation of the angiogenic factors PlGF, VEGF and their receptors (Flt-1, Flk-1/KDR) by TSH in cultured thyrocytes and in the thyroid gland of thiouracil-fed rats suggest a TSH-dependent paracrine mechanism for goiter hypervascularization. Oncogene 15 (1997) 2687-2698
69. Wolff J. Perchlorate and the thyroid gland. Pharmacol. Rev. 50 (1998) 89-105
70. Wynford-Thomas D., Stringer B.M., and Williams E.D. Desensitisation of rat thyroid to the growth-stimulating action of TSH during prolonged goitrogen administration. Persistence of refractoriness following withdrawal of stimulation. Acta Endocrinol. 101 (1982) 562-569
71. Wynford-Thomas D., Stringer B.M., and Williams E.D. Goitrogen-induced thyroid growth in the rat: a quantitative morphometric study. J. Endocrinol. 94 (1982) 131-140
72. Xia C., Hu J., Ketterer B., and Taylor J.B. The organization of the human GSTP1-1 gene promoter and its response to retinoic acid and cellular redox status. Biochem. J. 313 (1996) 155-161
73. Yamada E., Yamazaki K., Takano K., Obara T., and Sato K. Iodide inhibits vascular endothelial growth factor-A expression in cultured human thyroid follicles: a microarray search for effects of thyrotropin and iodide on angiogenesis factors. Thyroid 16 (2006) 545-554
74. Yen P.M. Physiological and molecular basis of thyroid hormone action. Physiol. Rev. 81 (2001) 1097-1142
75. Zambon A.C., Zhang L., Minovitsky S., Kanter J.R., Prabhakar S., Salomonis N., Vranizan K., Dubchak I., Conklin B.R., and Insel P.A. Gene expression patterns define key transcriptional events in cell-cycle regulation by cAMP and protein kinase A. Proc. Natl. Acad. Sci. U.S.A. 102 (2005) 8561-8566