Exposure to PCB 77 induces tissue-dependent changes in iodothyronine deiodinase activity patterns in the embryonic chicken

General and Comparative Endocrinology

Volumn 148, Issue 3, 2006, Pages 327-335

  Beck, Veerle ^a   Roelens, Simon A ^a   Darras, Veerle M ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Chicken; Development; Iodothyronine deiodinase; Polychlorinated biphenyl (PCB); Thyroid hormone (TH)

Indexed keywords

LIOTHYRONINE; POLYCHLORINATED BIPHENYL; THYROXINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELLULAR DISTRIBUTION; CEREBELLUM; CONTROLLED STUDY; DEVELOPMENTAL STAGE; EMBRYO; EMBRYO DEVELOPMENT; ENVIRONMENTAL EXPOSURE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INACTIVATION; HATCHING; LIVER; NONHUMAN; PRIORITY JOURNAL; TELENCEPHALON; THYROID HORMONE BLOOD LEVEL; TISSUE DISTRIBUTION;

EID: 33747829621     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2006.04.003     Document Type: Article

References (57)

1. Adams, C., Lans, M.C., Klasson-Wehler, E., Van Engelen, J.G.M., Visser, T.J., Brouwer, A., 1990. Hepatic thyroid hormone 5′-deiodinase, another target-protein for monohydroxy metabolites of 3,3′,4,4′-tetrachlorobiphenyl. In: Proceedings of Dioxin 90, The Tenth International Conference on Organohalogen Compounds 1, 51-54.
2. Allen J.R., Carstens L.A., and Barsotti D.A. Residual effects of short-term low-level exposure of non-human primates to polychlorinated biphenyls. Toxicol. Appl. Pharmacol. 30 (1974) 440-451
3. Becker K.B., Stephens K.C., Davey J.C., Schneider M.J., and Galton V.A. The type 2 and type 3 iodothyronine deiodinases play important roles in coordinating development in Rana catesbeiana tadpoles. Endocrinology 13 7 (1997) 2989-2997
4. Beetstra J.B., van Engelen J.G., Karels P., van der Hoek H.J., de Jong M., Docter R., Krenning E.P., Hennemann G., Brouwer A., and Visser T.J. Thyroxine and 3,3′,5-triiodothyronine are glucuronidated in rat liver by different uridine diphosphate-glucuronyltransferases. Endocrinology 12 2 (1991) 741-746
5. Bernal J. Action of thyroid hormone in brain. J. Endocrinol. Invest. 2 3 (2002) 268-288
6. Bernal J., Guadaño-Ferraz A., and Morte B. Perspectives in the study of thyroid hormone action on brain development and function. Thyroid 1 11 (2003) 1005-1012
7. Berry M.J., Kates A.-L., and Larsen P.R. Thyroid hormone regulates type I deiodinase messenger RNA in rat liver. Mol. Endocrinol. 4 (1990) 743-748
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72 (1976) 248-254
9. Brouwer A., Ahlborg U.G., Van den Berg M., Birnbaum L.S., Boersma E.R., Bosveld B., Denison M.S., Gray L.E., Hagmar L., Holene E., Huisman M., Jacobson S.W., Jacobson J.L., Koopman-Esseboom C., Koppe J.G., Kulig B.M., Morse D.C., Muckle G., Peterson R.E., Sauer P.J.J., Seegal R.F., Smits-van Prooije A.E., Touwen B.C.L., Weisglas-Kuperus N., and Winneke G. Functional aspects of developmental toxicity of polyhalogenated aromatic hydrocarbons in experimental animals and human infants. Eur. J. Pharmacol. 293 (1995) 1-40
10. Brouwer A., Morse D.C., Lans M.C., Schuur A.G., Murk A.J., Klasson-Wehler E., Bergman A., and Visser T.J. Interactions of persistent environmental organohalogens with the thyroid hormone system: mechanisms and possible consequences for animal and human health. Toxicol. Ind. Health 1 1-2 (1998) 59-84
11. Campos-Barros A., Meinhold H., Walzog B., and Behne D. Effects of selenium and iodine deficiency on thyroid hormone concentrations in the central nervous system of the rat. Eur. J. Endocrinol. 136 (1997) 316-323
12. Coimbra A.M., Reis-Henriques M.A., and Darras V.M. Circulating thyroid hormone levels and iodothyronine deiodinase activities in Nile tilapia (Oreochromis niloticus) following dietary exposure to Endosulfan and Aroclor 1254. Comp. Biochem. Physiol. C Toxicol. Pharmacol. 14 1 (2005) 8-14
13. Crantz F.R., Silva J.E., and Larsen P.R. An analysis of the sources and quantity of 3,5,3′-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum. Endocrinology 11 2 (1982) 367-375
14. Darras V.M., Kotanen S.P., Geris K.L., Berghman L.R., and Kühn E.R. Plasma thyroid hormone levels and iodothyronine deiodinase activity following an acute glucocorticoid challenge in embryonic compared to posthatch chickens. Gen. Comp. Endocrinol. 104 (1996) 203-212
15. Darras V.M., Visser T.J., Berghman L.R., and Kühn E.R. Ontogeny of type I and type III deiodinase activities in embryonic and posthatch chicks: relationship with changes in plasma triiodothyronine and growth hormone levels. Comp. Biochem. Physiol. A 10 1 (1992) 131-136
16. DiStefano J.J., Jang M., Malone T.K., and Broutman M. Comprehensive kinetics of triiodothyronine production, distribution, and metabolism in blood and tissue pools of the rat using optimized blood-sampling protocols. Endocrinology 11 1 (1982) 198-213
17. Faber R.A., and Hickey J.J. Eggshell thinning, chlorinated hydrocarbons, and mercury in inland aquatic bird eggs, 1969 and 1970. Pestic. Monit. J. 7 1 (1973) 27-36
18. Feirabend H.K.P. Development of longitudinal patterns in the cerebellum of the chicken (Gallus domesticus): a cytoarchitectural study on the genesis of cerebellar modules. Eur. J. Morphol. 2 2-4 (1990) 169-223
19. Gould J.C., Cooper K.R., and Scanes C.G. Effects of polychlorinated biphenyl mixtures and three specific congeners on growth and circulating growth-related hormones. Gen. Comp. Endocrinol. 10 2 (1997) 221-230
20. Gould J.C., Cooper K.R., and Scanes C.G. Effects of polychlorinated biphenyls on thyroid hormones and liver type I monodeiodinase in the chick embryo. Ecotoxicol. Environ. Saf. 43 (1999) 195-203
21. Guadaño-Ferraz A., Escámez M.J., Rausell E., and Bernal J. Expression of type 2 iodothyronine deiodinase in hypothyroid rat brain indicates an important role of thyroid hormone in the development of specific primary sensory systems. J. Neurosci. 1 9 (1999) 3430-3439
22. Harris A.R., Fang S.L., Vagenakis A.G., and Braverman L.E. Effect of starvation, nutriment replacement, and hypothyroidism on in vitro hepatic T4 to T3 conversion in the rat. Metabolism 2 11 (1978) 1680-1690
23. Hart LaVail J., and Cowan W.M. The development of the chick tectum. I. Normal morphology and cytoarchitectonic development. Brain Res. 28 (1971) 391-419
24. Heyers D., Kovjanic D., and Redies C. Cadherin expression coincides with birth dating patterns in patchy compartments of the developing chicken telencephalon. J. Comp. Neurol. 46 2 (2003) 155-166
25. Huang T.S., Beredo A., Solomon D.H., and Chopra I.J. The inner ring (5-) monodeiodination of thyroxine (T4) in cerebral cortex during fetal, neonatal, and adult life. Metabolism 3 3 (1986) 272-277
26. Kaplan M.M., McCann U.D., Yaskoski K.A., Larsen P.R., and Leonard J.L. Anatomical distribution of phenolic and tyrosyl ring iodothyronine deiodinases in the nervous system of normal and hypothyroid rats. Endocrinology 10 2 (1981) 397-402
27. Karmarkar M.G., Prabarkaran D., and Godbole M.M. 5′-Monodeiodinase activity in developing human cerebral cortex. Am. J. Clin. Nutr. 5 2 Suppl. (1993) 291S-294S
28. Klaassen C.D., and Hood A.M. Effects of microsomal enzyme inducers on thyroid follicular cell proliferation and thyroid hormone metabolism. Toxicol. Pathol. 2 1 (2001) 34-40
29. Lans M.C., Spiertz C., Brouwer A., and Koeman J.H. Different competition of thyroxine binding to transthyretin and thyroxine-binding globulin by hydroxy-PCBs, PCDDs and PCDFs. Eur. J. Pharmacol. 270 (1994) 129-136
30. Larsen P.R., Silva J.E., and Kaplan M.M. Relationships between circulating and intracellular thyroid hormones: physiological and clinical implications. Endocr. Rev. 2 1 (1981) 87-102
31. Morse D.C., Groen D., Veerman M., Van Amerongen C.J., Koëter H.B.W.M., Smits Van Prooije A.E., Visser T.J., Koeman J.H., and Brouwer A. Interference of polychlorinated biphenyls in hepatic and brain thyroid hormone metabolism in fetal and neonatal rats. Toxicol. Appl. Pharmacol. 122 (1993) 27-33
32. Morse D.C., Wehler E.K., Wesseling W., Koeman J.H., and Brouwer A. Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (aroclor 1254). Toxicol. Appl. Pharmacol. 136 (1996) 269-279
33. Reyns G.E., Janssens K.A., Buyse J., Kühn E.R., and Darras V.M. Changes in thyroid hormone levels in chicken liver during fasting and refeeding. Comp. Biochem. Physiol. B Biochem. Mol. Biol. 13 1 (2002) 239-245
34. Reyns G.E., Venken K., Morreale de Escobar G., Kühn E.R., and Darras V.M. Dynamics and regulation of intracellular thyroid hormone concentrations in embryonic chicken liver, kidney, brain, and blood. Gen. Comp. Endocrinol. 13 1 (2003) 80-87
35. Roelens S.A., Beck V., Maervoet J., Aerts G., Reyns G.E., Schepens P., and Darras V.M. The dioxin-like PCB 77 but not the ortho-substituted PCB 153 interferes with chicken embryo thyroid hormone homeostasis and delays hatching. Gen. Comp. Endocrinol. 14 1 (2005) 1-9
36. Roelens S.A., Beck V., Clerens S., Vanden Bergh G., Arckens L., Darras V.M., and Van der Geyten S. Neurotoxicity of polychlorinated biphenyls (PCBs) by disturbance of thyroid hormone-regulated genes. Ann. NY Acad. Sci. 1040 (2005) 454-456
37. Romanoff A.L. The avian embryo (1960), The Macmillan company, New York p. 1305
38. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implications for risk assessment. Crit. Rev. Toxicol. 2 2 (1994) 87-149
39. Santini F., Hurd R.E., Lee B., and Chopra I.J. Thyromimetic effects of 3,5,3′-triiodothyronine sulfate in hypothyroid rats. Endocrinology 13 1 (1993) 105-110
40. Schantz S.L. Developmental neurotoxicity of PCBs in humans: what do we know and where do we go from here?. Neurotoxicol. Teratol. 1 3 (1996) 217-227
41. Schuur A.G., Legger F.F., van Meeteren M.E., Moonen M.J.H., van Leeuwen-Bol I., Bergman A., Visser T.J., and Brouwer A. In vitro inhibition of thyroid hormone sulfation by hydroxylated metabolites of halogenated aromatic hydrocarbons. Chem. Res. Toxicol. 1 9 (1998) 1075-1081
42. Silva J.E., Gordon M.B., Crantz F.R., Leonard J.L., and Larsen P.R. Qualitative and quantitative differences in the pathways of extrathyroidal triiodothyronine generation between euthyroid and hypothyroid rats. J. Clin. Invest. 7 4 (1984) 898-907
43. Silva J.E., and Larsen P.R. Comparison of iodothyronine 5′-deiodinase and other thyroid-hormone-dependent enzyme activities in the cerebral cortex of hypothyroid neonatal rat. Evidence for adaptation to hypothyroidism. J. Clin. Invest. 7 5 (1982) 1023-1110
44. Silva J.E., and Matthews P.S. Production rates and turnover of triiodothyronine in rat-developing cerebral cortex and cerebellum. Responses to hypothyroidism. J. Clin. Invest. 7 3 (1986) 1035-1049
45. Spear P.A., and Moon T.W. Low dietary iodine and thyroid anomalies in ring doves, streptopelia-risoria, exposed to 3,4,3′,4′-tetrachlorobiphenyl. Arch. Environ. Contam. Toxicol. 1 5 (1985) 547-553
46. Striedter G.F., and Beydler S. Distribution of radial glia in the developing telencephalon of chicks. J. Comp. Neurol. 38 3 (1997) 399-420
47. Tilson H.A., and Kodavanti P.R.S. Neurochemical effects of polychlorinated biphenyls: an overview and identification of research needs. Neurotoxicology 1 3 (1997) 727-744
48. Tu H.M., Legradi G., Bartha T., Salvatore D., Lechan R.M., and Larsen P.R. Regional expression of the type 3 iodothyronine deiodinase messenger ribonucleic acid in the rat central nervous system and its regulation by thyroid hormone. Endocrinology 14 2 (1999) 784-790
49. Van den Berg M., Craane B.L.H.J., Sinnige T., Vanmourik S., Dirksen S., Boudewijn T., Vandergaag M., Lutkeschipholt I.J., Spenkelink B., and Brouwer A. Biohemical and toxic effects of polychlorinated biphenyls (PCBs), dibenzo-p-dioxins (PCDDs) and dibenzofurans (PCDFs) in the cormorant (Phalacrocorax-carbo) after in ovo exposure. Environ. Toxicol. Chem. 1 5 (1994) 803-816
50. Van der Geyten S., Sanders J.P., Kaptein E., Darras V.M., Kühn E.R., Leonard J.L., and Visser T.J. Expression of chicken hepatic type I and type III iodothyronine deiodinases during embryonic development. Endocrinology 13 12 (1997) 5144-5152
51. Van der Geyten S., Van den Eynde I., Segers I.B., Kühn E.R., and Darras V.M. Differential expression of iodothyronine deiodinases in chicken tissues during the last week of embryonic development. Gen. Comp. Endocrinol. 12 1 (2002) 65-73
52. Verhoelst C.H., Darras V.M., Doulabi B.Z., Reyns G., Kuhn E.R., and Van der Geyten S. Type I iodothyronine deiodinase in euthyroid and hypothyroid chicken cerebellum. Mol. Cell. Endocrinol. 21 1-2 (2004) 97-105
53. Visser T.J. Importance of deiodination and conjugation in the hepatic metabolism of thyroid hormone. In: Greer M.A. (Ed). The Thyroid Gland (1990), Raven Press, NY 255-269
54. Visser T.J., Kaplan M.M., Leonard J.L., and 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. 71 (1983) 992-1002
55. Visser T.J., Kaptein E., van Toor H., Van Raaij J.A.G.M., Van den Berg K.J., Tjong Tjin Joe C., Van Engelen J.G.M., and Brouwer A. Glucuronidation of thyroid hormone in rat liver: effects of in vitro treatment with microsomal enzyme inducers and in vitro assay conditions. Endocrinology 13 5 (1993) 2177-2186
56. Wassermann M., Wassermann D., Cucos S., and Miller H.J. World PCBs map: storage and effects in man and his biologic environment in the 1970s. Ann. NY Acad. Sci. 320 (1979) 69-124
57. Zoeller R.T. Polychlorinated biphenyls as disruptors of thyroid hormone action. In: Robertson L.W., and Hansen L.G. (Eds). PCBs. Recent advances in environmental toxicology and health effects (2001), The University Press of Kentucky 265-269