Suppression of thyroid hormone receptor-mediated transcription and disruption of thyroid hormone-induced cerebellar morphogenesis by the polybrominated biphenyl mixture, BP-6

NeuroToxicology

Volumn 32, Issue 4, 2011, Pages 400-409

  Ibhazehiebo, Kingsley ^a   Iwasaki, Toshiharu ^a   Okano Uchida, Takayuki ^a   Shimokawa, Noriaki ^a   Ishizaki, Yasuki ^a   Koibuchi, Noriyuki ^a  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

BP 6; Granule cell; Purkinje cell; Thyroid hormone; Thyroid hormone receptor; Thyroid hormone response element; Transcription

Indexed keywords

BP 6; POLYBROMINATED BIPHENYL; THYROID HORMONE RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; CELL AGGREGATION; CELL CULTURE; CELL DAMAGE; CELL DEATH; CELL GROWTH; CELL MATURATION; CEREBELLUM; CONTROLLED STUDY; FEMALE; GRANULE CELL; HOMEOSTASIS; NEURITE; NONHUMAN; PRIORITY JOURNAL; PURKINJE CELL; RAT; RECEPTOR BINDING;

ANIMALS; ANIMALS, NEWBORN; BINDING SITES; CELL LINE; CERCOPITHECUS AETHIOPS; CEREBELLUM; DENDRITES; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; FLAME RETARDANTS; NEURITES; NEUROGENESIS; POLYBROMINATED BIPHENYLS; PURKINJE CELLS; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RESPONSE ELEMENTS; THYROID HORMONE RECEPTORS BETA; THYROXINE; TRANSCRIPTION, GENETIC; TRANSFECTION; TRIIODOTHYRONINE;

MAMMALIA; RATTUS;

EID: 79955077295     PISSN: 0161813X     EISSN: 18729711     Source Type: Journal    
DOI: 10.1016/j.neuro.2011.02.008     Document Type: Article

References (79)

1. Adams N.C., Tomoda T., Cooper M., Dietz G., Hatten M.E. Mice that lack astrotactin have slowed neuronal migration. Development 2002, 129:965-972.
2. Allen-Rowland C.F., Castracane V.D., Hamilton M.G., Seifter J. Effects of polybrominated biphenyls (PBB) on the pituitary-thyroid axis of the rat. Proc Soc Exp Biol Med 1981, 166:506-514.
3. Alvarez-Lloret P., Lind P.M., Nyberg I., Orberg J., Rodriguez-Navarro A.B. Effects of 3,3′,4,4′,5-pentachlorobiphenyl (PCB126) on vetebral bone mineralization and on thyroxin and vitamin D levels in Sprague-Dawley rats. Toxicol Lett 2009, 187:63-68.
4. Anderson H.A., Lilis R., Selikoff I.J., Rosenman K.D., Valciukas J.A., Freedman S. Unanticipated prevalence of symptoms among dairy farmers in Michigan and Wisconsin. Environ Health Perspect 1978, 23:217-226.
5. Aust S.D., Millis C.D., Holocomb L. Relationship of basic research in toxicology to environmental standard setting: the case of polybrominated biphenyls in Michigan. Arch Toxicol 1987, 60:229-237.
6. Blanck H.M., Marcus M., Hertzberg V., Tolbert P.E., Rubin C., Henderson A.K., et al. Determinants of polybrominated biphenyl serum decay among women in the Michigan PBB cohort. Environ Health Perspect 2000, 108:147-152.
7. Blanck H.M., Marcus M., Rubin C., Tolbert P.E., Hertzberg V.S., Henderson A.K., et al. Growth in girls exposed in utero and postnatally to polybrominated biphenyls and polychlorinated biphenyls. Epidermiology 2002, 13:205-210.
8. Blanck H.M., Marcus M., Tolbert P.E., Schuch C., Rubin C., Henderson A.K., et al. Time to menopause in relation to PBBs, PCBS, and smoking. Maturitas 2004, 49:97-106.
9. Bradley D.J., Young W.S., Weinberger C. Differential expression of α and β thyroid hormone receptor genes in rat brain and pituitary. Proc Natl Acad Sci USA 1989, 86:7250-7254.
10. Bradley D.J., Towle H.C., Young W.S. Spatial and temporal expression of α- and β-thyroid hormone receptor mRNAs, including the β2 subtype, in the developing mammalian nervous system. J Neurosci 1992, 12:2288-2302.
11. Brilliant L.B., VanAmburg G., Isbister J., Humphrey H., Wilcox K., Eyster J., et al. Breast-milk monitoring to measure Michigan's contamination with polybrominated biphenyls. Lancet 1978, 2:643-646.
12. Brown W.J., Verity M.A., Smith R.L. Inhibition of cerebellar dendrite development in neonatal thyroid deficiency. Neuropathol Appl Neurobiol 1976, 2:191-207.
13. Bushnell P.J., Moser V.C., MacPhail R.C., Oshiro W.M., Derr-Yellin E.C., Philips P.M., et al. Neurobehavioral assessments of rats perinatally exposed to a commercial mixture of polychlorinated biphenyls. Toxicol Sci 2002, 68:109-120.
14. Byrne J.J., Carbone J.P., Hanson E.A. Hypothyroidism and abnormalities in the kinetics of thyroid hormone metabolism in rats treated chronically with polychlorinated biphenyl and polybrominated biphenyl. Endocrinology 1987, 121:520-527.
15. Davis S.I., Blanck H.M., Hertzberg V.S., Tolbert P.E., Rubin C., Cameron L.L., et al. Menstrual function among women exposed to polybrominated biphenyls: a follow-up prevalence study. Environ Health 2005, 9:4-15.
16. Di Carlo F.J., Seifter J., DeCarlo V.J. Assessment of the hazards of polybrominated biphenyls. Environ Health Perspect 1978, 23:351-365.
17. Dobbing J., Sands J. Comparative aspects of the brain growth spurt. Early Hum Dev 1979, 3:79-83.
18. Domino E.F., Fivenson D.P., Domino S.E. Differential tissue distribution of various polybrominated biphenyls of firemaster FF-1 in male rats. Drug Metab Dispos 1980, 8:332-336.
19. Domino L.E., Domino S.E., Domino E.F. Toxicokinetics of 2,2′,4,4′,5,5′-hexabromobiphenyl in the rat. J Toxicol Environ Health 1982, 9:815-833.
20. Eyster J.T., Humphrey H.E., Kimbrough R.D. Partitioning of polybrominated biphenyls (PBBs) in serum, adipous tissues, breast milk, placenta, cord blood, biliary fluid, and feces. Arch Environ Health 1983, 38:47-53.
21. Fisher J.W., Campbell J., Muralidhara S., Bruckner J.V., Ferguson D., Mumtaz M., et al. Effects of PCB126 on hepatic metabolism of thyroxine and perturbations in the hypothalamic-pituitary-thyroid axis in rat. Toxicol Sci 2006, 90:87-95.
22. Gao W.-Q., Zheng J.L., Karihaloo M. Neurotrophin-4/5 (NT-4/5) and brain-derived neurotrophic factor (BDNF) acts at later stages of cerebellar granule cell differentiation. J Neurosci 1995, 15:2656-2667.
23. Geller I., Hartman R.J., Garcia C., Seifter J. Effects of polybrominated biphenyls on a discrimination task in rats. Neurobehav Toxicol 1979, 1:263-267.
24. Geller I., Gause E.M., Leal B.Z., Hartman R.J., Seifter J. Behavioral effects of drugs as a function of maternal polybrominated biphenyl body burden. Toxicol Lett 1985, 24:229-234.
25. Gladen B.C., Rogan W.J. Effects of perinatal polychlorinated biphenyls and dichlorodiphenyl dichloroethane on later development. J Pediatr 1991, 119:58-63.
26. Haddow J.E., Palomoki G.E., Allan W.C., Williams J.R., Knight G.J., Gagnon J., et al. Maternal thyroid deficiency during pregnancy and subsequent development of the child. New Engl J Med 1999, 341:549-555.
27. Hass J.R., McConnell E.E., Haran D.J. Chemical and toxicologic evaluation of Firemaster BP-6. J Agric Food Chem 1978, 26:94-99.
28. Henck J.W., Rech R.H. Effect of perinatal polybrominated biphenyl exposure on acquisition and performance of an auto-shaping paradigm. Neurotoxicology 1986, 7:655-658.
29. Henck J.W., Mattsson J.L., Rezabek D.H., Carlson C.L., Rech R.H. Developmental neurotoxicity of polybrominated biphenyls. Neurotoxicol Teratol 1994, 16:391-399.
30. Henderson A.K., Rosen D., Miller G.L., Figgs L.W., Zahm S.H., Sieber S.M., et al. Breast cancer among women exposed to polybrominated biphenyls. Epidemiology 1995, 6:544-546.
31. Hoque A., Sigurdson A.J., Burau K.D., Humphrey H.E., Hess K.R., Sweeney A.M. Cancer among a Michigan cohort exposed to polybrominated biphenyls in 1973. Epidemiology 1998, 9:373-378.
32. IARC. Polychlorinated biphenyls and polybrominated biphenyls. (Monographs on the evaluation of the carcinogenic risk of chemical to humans, vol. 18. Lyon: IARC;1978. p. 107-24.
33. Ito M. Historical review of the significance of the cerebellum and the role of Purkinje cells in motor learning. Ann NY Acad Sci 2002, 978:273-288.
34. Iwasaki T., Chin W.W., Ko L. Identification and characterization of RRM-containing coactivator activator (CoAA) as TRBP-interacting protein and its splice variant as a coactivator modulator (CoAM). J Biol Chem 2001, 276:33375-33383.
35. Iwasaki T., Miyazaki W., Takeshita A., Kuroda Y., Koibuchi N. Polychlorinated biphenyls suppress thyroid hormone-induced transactivation. Biochem Biophys Res Commun 2002, 299:384-388.
36. Iwasaki T., Miyazaki W., Rokutanda N., Koibuchi N. Liquid chemiluminescent DNA pull-down assay to measure nuclear receptor-DNA binding in solution. BioTechniques 2008, 45:445-448.
37. Jacobson J.L., Fein G.G., Jacobson S.W., Schwartz P.M., Dowler J.K. The transfer of polychlorinated biphenyls (PCBs) and polybrominated biphenyls (PBBs) across the human placenta and into maternal milk. Am J Public Health 1984, 74:378-379.
38. Jacobson J.L., Jacobson S.W. Intellectual impairment in children exposed to polychlorinated biphenyls in utero. New Engl J Med 1996, 335:783-789.
39. Jiang D., Sulllivan P.G., Sensi S.L., Steward O., Wiess J.H. Zn (2+) induces permeability transition pore opening and release of pro-apoptotic peptides from neuronal membrane. J Biol Chem 2001, 276:47524-47529.
40. Kaiser R., Marcus M., Blanck H.M., Naughton M., Zhang R.H., Henderson K.A., et al. Polybrominated biphenyl exposure and benign breast disease in a cohort of US women. Ann Epidemiol 2003, 13:16-23.
41. Kimura-Kuroda J., Nagata I., Kuroda Y. Hdroxylated metabolites of polychlorinated biphenyls inhibit thyroid-hormone-dependent extension of cerebellar Purkinje cell dendrites. Dev Brain Res 2005, 154:259-263.
42. Koibuchi N., Liu Y., Fukuda H., Takeshita A., Yen P.M., Chin W.W. ROR alpha augments thyroid hormone receptor-mediated transcriptional activation. Endocrinology 1999, 140:1356-1364.
43. Koibuchi N., Chin W.W. Thyroid hormone action and brain development. Trends Endocrinol Metab 2000, 11:123-128.
44. Koibuchi N., Yamaoka S., Chin W.W. Effects of altered thyroid status on neurotrophin gene expression during postnatal development of the mouse cerebellum. Thyroid 2001, 11:205-210.
45. Koibuchi N. The role of thyroid hormone on cerebellar development. Cerebellum 2008, 7:530-533.
46. Lilis R., Anderson H.A., Valciukas J.A., Freedman S., Selikoff I.J. Comparison of findings among residents on Michigan dairy farms and consumers of produce purchased on these farms. Environ Health Perspect 1978, 23:105-165.
47. Lindholm D., Castren E., Tsoulfas P., kolbeck R., Berzaghi Mda P., Leingartner A., et al. Neurotrophin-3 induced by tri-iodothyronine in cerebellar granule cells promotes Purkinje cell differentiation. J Cell Biol 1993, 122:443-450.
48. Matthews H.B., Kato S., Morales N.N., Tuey D.B. Distribution and excretion of 2,4,5,2′,4′,5′-hexabromobiphenyl, the major component of fireMaster BP-6. J Toxicol Environ Health 1977, 3:599-605.
49. Miceli J.N., Nolan D.C., Marks B., Hariharan M. Persistence of polybrominated biphenyls (PBB) in human post-mortem tissue. Environ Health Perspect 1985, 60:399-403.
50. Miyazaki W., Iwasaki T., Takeshita A., Kuroda Y., Koibuchi N. Polychlorinated biphenyls suppress thyroid hormone receptor-mediated transcription through a novel mechanism. J Biol Chem 2004, 279:18195-18202.
51. Miyazaki W., Iwasaki T., Takeshita A., Tohyama C., Koibuchi N. Identification of the functional domain of thyroid hormone receptor responsible for polychlorinated biphenyls-mediated suppression of its action in vitro. Environ Health Perspect 2008, 116:1231-1236.
52. Moore R.W., Aust S.D. Purification and characterization of polybrominated biphenyl congeners. Biochem Biophys Res Commun 1978, 84:936-942.
53. Moriyama K., Tagami T., Akamizu T., Usui T., Saijo M., Kanamoto N., et al. Thyroid hormone action is disrupted by bisphenol A as an antagonist. J Clin Endocrinol Metab 2002, 87:5185-5190.
54. Neveu I., Arenas E. Neurotrophins promote the survival and development of neurons in the cerebellum of hypothyroid rats in vivo. J Cell Biol 1996, 133:631-646.
55. Nicholson J.L., Altman J. Synaptogenesis in the rat cerebellum: effects of early hypo- and hyperthyroidism. Science 1972, 176:530-532.
56. Nicholson J.L., Altman J. The effects of early hypo- and hyperthyroidism on development of rat cerebellar cortex. I. Cell proliferation and differentiation. Brain Res 1972, 44:13-23.
57. Okano-Uchida T., Himi T., Komiya Y., Ishizaki Y. Cerebellar granule cell precursors can differentiate into astroglial cells. Proc Natl Acad Sci USA 2003, 101:1211-1216.
58. Oppenheimer J.H., Schwartz H.L. Molecular basis of thyroid hormone-dependent brain development. Endocr Rev 1997, 18:462-475.
59. Poterfield S.P. Thyroid dysfunction and environmental chemicals-potential impact on brain development. Environ Health Perspect 2000, 108:433-438.
60. Preache M.M., Cagen S.Z., Gibson J.E. Perinatal toxicity in mice following maternal dietary exposure to polybrominated biphenyls. Toxicol Appl Pharmacol 1976, 37:171.
61. Reich M.R. Environmental politics and science: the case of PBB contamination in Michigan. Am J Public Health 1983, 73:302-313.
62. Rickert D.W., Dent J.G., Cagen S.Z., McCormack K.M., Melrose P., Gibson J.E. Distribution of polybrominated biphenyls after dietary exposure in pregnant and lactating rats and their offspring. Environ Health Perspect 1978, 23:63-66.
63. Rosen D.H., Flanders W.D., Friede A., Humphrey H.E., Sinks T.H. Half-life of polybrominated biphenyl in human sera. Environ Health Perspect 1995, 103:272-274.
64. Safe S.H. Polychlorinated biphenyls (PCBs): environmental impact, biochemical and toxic responses, and implication for risk assessment. Crit Rev Toxicol 1994, 24:87-149.
65. Schantz S.L., Bowman R.E. Persistent locomotor hyperactivity in offspring of rhesus monkeys exposed to polychlorinated or polybrominated biphenyls. Soc Neurosci Abst 1983, 9:423.
66. Schwartz E.M., Rae W.A. Effects of polybrominated biphenyls (PBB) on developmental abilities in children. Am J Public Health 1983, 73:277-281.
67. Seagull E.A.W. Developmental abilities of children exposed to polybrominated biphenyls (PBB). Am J Public Health 1983, 73:281-285.
68. Seegal R.F. Epidermiological and laboratory evidence of PCB-induced neurotoxicity. Crit Rev Toxicol 1996, 26:709-737.
69. Strait K.A., Schwartz H.L., Seybold V.S., Ling N.C., Oppenheimer J.H. Immunofluorescence localization of thyroid hormone receptor protein β1 and variant α2 in selected tissues cerebellar Purkinje cells as a model for β1 receptor-mediated developmental effects of thyroid hormone in brain. Proc Natl Acad Sci USA 1991, 88:3887-3891.
70. Sweeney A.M., Symanski E. The influence of age at exposure to PBBs on birth outcomes. Environ Res 2007, 105:370-379.
71. Takeshita A., Yen P.M., Ikeda M., Cardona G.R., Liu Y., Koibuchi N., et al. Thyroid hormone response elements differentially modulate the interactions of thyroid hormone receptor with two receptor binding domain in the steroid receptor coactivator-1. J Biol Chem 1998, 273:21554-21562.
72. Takeshita A., Taguchi M., Koibuchi N., Ozawa Y. Putative role of the orphan nuclear receptor SXR (steroid and xenobiotic receptor) in the mechanism of CYP3A4 inhibition by xenobiotics. J Biol Chem 2002, 277:32453-32458.
73. Terrel M.L., Berzen A.K., Small C.M., Cameron L.L., Wirth J.J., Marcus M. A cohort study of the association between secondary sex ratio and parental exposure to polybrominated biphenyl (PBB) and polychlorinated biphenyl (PCB). Environ Health 2009, 8:35.
74. Tilson H.A., Cabe P.A. Studies on the neurobehavioral effects of polybrominated biphenyls in rats. Ann N Y Acad Sci 1979, 320:325-336.
75. Tilson H.A., Jacobson J.L., Rogan W.J. Polychlorinated biphenyls and the developing nervous system: cross species comparisons. Neurotoxicol Teratol 1990, 12:239-248.
76. Tilson H.A., Kodavanti P.R. Neurochemical effects of polychlorinated biphenyls: an overview and identification of research needs. Neurotoxicology 1997, 18:727-743.
77. Valciukas J.A., Lilis R., Wolff M.S., Anderson H.A. Comparative neurobehavioral study of a polybrominated biphenyl-exposed population in Michigan and a nonexposed group in Wisconsin. Environ Health Perspect 1978, 23:199-210.
78. Vasiliu O., Cameron I., Gardiner J., Deguire P., Karmaus W. Polybrominated biphenyls, polychlorinated biphenyls, body weight, and incidence of adult-onset diadetes mellitus. Epidemiology 2006, 17:352-359.
79. Yen P.M. Physiological and molecular basis of thyroid hormone action. Physiol Rev 2001, 81:1097-1142.