A single prenatal exposure to the endocrine disruptor 2,3,7,8-tetrachlorodibenzo-p-dioxin alters developmental myelination and remyelination potential in the rat brain

Journal of Neurochemistry

Volumn 115, Issue 4, 2010, Pages 897-909

  Fernandez M ^a   Paradisi, M ^a   D'Intino, G ^a   Del Vecchio, G ^a   Sivilia, S ^a   Giardino, L ^a   Calza L ^a  

^a UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

2,3,7,8 tetrachlorodibenzo p dioxin; Myelin basic protein; Neural stem cells; Oligodendrocyte precursor cells

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; BIOLOGICAL MARKER; MESSENGER RNA; MYELIN BASIC PROTEIN; PLATELET DERIVED GROWTH FACTOR ALPHA RECEPTOR; POLYCHLORINATED BIPHENYL; THYROID HORMONE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL LINEAGE; CELL MATURATION; CELL PROLIFERATION; CEREBELLUM; CONTROLLED STUDY; DIENCEPHALON; EX VIVO STUDY; FEMALE; GESTATIONAL AGE; MALE; MEDULLA OBLONGATA; MILK; MYELINATION; NONHUMAN; OLIGODENDROGLIA; PLACENTA; PRENATAL EXPOSURE; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REMYELINIZATION; SIGNAL TRANSDUCTION; TELENCEPHALON; THYROID HORMONE METABOLISM;

ANIMALS; ANIMALS, NEWBORN; BRAIN; CELL PROLIFERATION; CELLS, CULTURED; ENDOCRINE DISRUPTORS; FEMALE; GROWTH INHIBITORS; MALE; NERVE FIBERS, MYELINATED; OLIGODENDROGLIA; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; RATS; TETRACHLORODIBENZODIOXIN;

ANIMALIA; RATTUS;

EID: 77958601277     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2010.06974.x     Document Type: Article

References (70)

1. Ahmed O. M., El-Gareib A. W., El-Bakry A. M., Abd El-Tawab S. M. and Ahmed R. G. (2008) Thyroid hormones states and brain development interactions. Int. J. Dev. Neurosci. 26, 147-209.
2. Baas D., Bourbeau D., Sarliève L. L., Ittel M. E., Dussault J. H. and Puymirat J. (1997) Oligodendrocyte maturation and progenitor cell proliferation are independently regulated by thyroid hormone. Glia 19, 324-32.
3. Baas D., Legrand C., Samarut J. and Flamant F. (2002) Persistence of oligodendrocyte precursor cells and altered myelination in optic nerve associated to retina degeneration in mice devoid of all thyroid hormone receptors. Proc. Natl Acad. Sci. USA 99, 2907-2911.
4. Beischlag T. V., Taylor R. T., Rose D. W., Yoon D., Chen Y., Lee W. H., Rosenfeld M. G. and Hankinson O. (2004) Recruitment of thyroid hormone receptor/retinoblastoma-interacting protein 230 by the aryl hydrocarbon receptor nuclear translocator is required for the transcriptional response to both dioxin and hypoxia. J. Biol. Chem. 279, 54620-54628.
5. Bell D. R., Clode S., Fan M. Q. et al. (2007a) Toxicity of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in the developing male Wistar(Han) rat. I: No decrease in epididymal sperm count after a single acute dose. Toxicol. Sci. 99, 214-231.
6. Bell D. R., Clode S., Fan M. Q. et al. (2007b) Toxicity of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in the developing male Wistar(Han) rat. II: Chronic dosing causes developmental delay. Toxicol. Sci. 99, 224-233.
7. Bell D. R., Clode S., Fan M. Q. et al. (2010) Interpretation of studies on the developmental reproductive toxicology of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin in male offspring. Food Chem. Toxicol. 48, 1439-1447.
8. Bernal J. (2005) Thyroid hormones and brain development. Vitam. Horm. 71, 95-122.
9. Bernal J. (2007) Thyroid hormone receptors in brain development and function. Nat. Clin. Pract. Endocrinol. Metab. 3, 249-259.
10. Bernal J. and Guadaño-Ferraz A. (2002) Analysis of thyroid hormone-dependent genes in the brain by in situ hybridization. Methods Mol. Biol. 202, 71-90.
11. Boas M., Main K. M. and Feldt-Rasmussen U. (2009) Environmental chemicals and thyroid function: an update. Curr. Opin. Endocrinol. Diabetes Obes. 16, 385-391.
12. Boggs J. M. (2006) Myelin basic protein: a multifunctional protein. Cell. Mol. Life Sci. 63, 1945-1961.
13. Bradl M. and Lassmann H. (2010) Oligodendrocytes: biology and pathology. Acta Neuropathol. 119, 37-53.
14. Calzà L., Fernández M. and Giardino L. (2010) Cellular approaches for stimulating CNS remyelination: Thyroid hormone to promote myelin repair via endogenous stem and precursor cells. J. Mol. Endo. 44, 13-23.
15. Casey B. (2005) Environmental contaminants and maternal thyroid function. Am. J. Obstet. Gynecol. 193, 1889-1890.
16. Ceballos A., Belinchon M. M., Sanchez-Mendoza E., Grijota-Martinez C., Dumitrescu A. M., Refetoff S., Morte B. and Bernal J. (2009) Importance of monocarboxylate transporter 8 for the blood-brain barrier-dependent availability of 3, 5, 3'-triiodo-l-thyronine. Endocrinology 150, 2491-2496.
17. Crofton K. M. and Zoeller R. T. (2005) Mode of action: neurotoxicity induced by thyroid hormone disruption during development - hearing loss resulting from exposure to PHAHs. Crit. Rev. Toxicol. 35, 757-769.
18. Darras V. M. (2008) Endocrine disrupting polyhalogenated organic pollutants interfere with thyroid hormone signalling in the developing brain. Cerebellum 7, 26-37.
19. Domingo J. L., Bocio A., Nadal M., Schuhmacher M. and Llobet J. M. (2002) Monitoring dioxins and furans in the vicinity of an old municipal waste incinerator after pronounced reductions of the atmospheric emissions. J. Environ. Monit. 4, 395-399.
20. Durand B. and Raff M. (2000) A cell-intrinsic timer that operates during oligodendrocyte development. Bioessays 22, 64-71.
21. Emond C., Birnbaum L. S. and DeVito M. J. (2004) Physiologically based pharmacokinetic model for developmental exposures to TCDD in the rat. Toxicol. Sci. 80, 115-133.
22. Fernández M., Pirondi S., Manservigi M., Giardino L. and Calzà L. (2004) Thyroid hormone participates in the regulation of neural stem cells and oligodendrocyte precursor cells in the central nervous system of adult rat. Eur. J. Neurosci. 20, 2059-2070.
23. Fernández M., Paradisi M., Giardino L. and Calzà L. (2006) To know neural stem properties from diseased brains: a critical step for brain repair, in Neural Stem Cell Research (Greer E. V., ed.), pp. 77-97. Nova Science Publishers Inc, New York.
24. Fernández M., Paradisi M., Del Vecchio G., Giardino L. and Calzà L. (2009) Thyroid hormone induces glial lineage of primary neurospheres derived from non-pathological and pathological rat brain: implications for remyelination-enhancing therapies. Int. J. Dev. Neurosci. 27, 769-778.
25. Fritsche E., Cline J. E., Nguyen N. H., Scanlan T. S. and Abel J. (2005) Polychlorinated biphenyls disturb differentiation of normal human neural progenitor cells: clue for involvement of thyroid hormone receptors. Environ. Health Perspect. 113, 871-876.
26. Giacomini S. M., Hou L., Bertazzi P. A. and Baccarelli A. (2006) Dioxin effects on neonatal and infant thyroid function: routes of perinatal exposure, mechanisms of action and evidence from epidemiology studies. Int Arch Occup Environ Health 79, 396-404.
27. Guadaño-Ferraz A., Obregón M. J., St Germain D. L. and Bernal J. (1997) The type 2 iodothyronine deiodinase is expressed primarily in glial cells in the neonatal rat brain. Proc. Natl Acad. Sci. USA 94, 10391-10396.
28. Haarmann-Stemmann T. and Abel J. (2006) The arylhydrocarbon receptor repressor (AhRR): structure, expression, and function. Biol. Chem. 9, 1195-1199.
29. Hall J. M., Barhoover M. A., Kazmin D., McDonnell D. P., Greenlee W. F. and Thomas R. S. (2010) Activation of the aryl-hydrocarbon receptor inhibits invasive and metastatic features of human breast cancer cells and promotes breast cancer cell differentiation. Mol. Endocrinol. 24, 359-369.
30. Hirako M., Aoki M., Kimura K., Hanafusa Y., Ishizaki H. and Kariya Y. (2005) Comparison of the concentrations of polychlorinated dibenzo-p-dioxins, dibenzofurans, and dioxin-like polychlorinated biphenyls in maternal and fetal blood, amniotic and allantoic fluids in cattle. Reprod. Toxicol. 20, 247-254.
31. Hurst C. H., DeVito M. J., Setzer R. W. and Birnbaum L. S. (2000) Acute administration of 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) in pregnant Long Evans rats: association of measured tissue concentrations with developmental effects. Toxicol. Sci. 53, 411-420.
32. Ishihara K., Warita K., Tanida T., Sugawara T., Kitagawa H. and Hoshi N. (2007) Does paternal exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) affect the sex ratio of offspring? J. Vet. Med. Sci. 69, 347-352.
33. Jagannathan N. R., Tandon N., Raghunathan P. and Kochupillai N. (1998) Reversal of abnormalities of myelination by thyroxine therapy in congenital hypothyroidism: localized in vivo proton magnetic resonance spectroscopy (MRS) study. Brain Res. Dev. Brain Res. 109, 179-86.
34. Jana N. R., Sarkar S., Ishizuka M., Yonemoto J., Tohyama C. and Sone H. (1999) Cross-talk between 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin and testosterone signal transduction pathways in LNCaP prostate cancer cells. Biochem. Biophys. Res. Commun. 256, 462-468.
35. Kakeyama M., Sone H., Miyabara Y. and Tohyama C. (2003) Perinatal exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin alters activity-dependent expression of BDNF mRNA in the neocortex and male rat sexual behavior in adulthood. Neurotoxicology 24, 207-217.
36. Kuil C. W., Brouwer A., Van Der Saag P. T. and Van Der Burg B. (1998) Interference between progesterone and dioxin signal transduction pathways. Different mechanisms are involved in repression by the progesterone receptor A and B isoforms. J. Biol. Chem. 273, 8829-8834.
37. Li B., Liu H. Y., Dai L. J., Lu J. C., Yang Z. M. and Huang L. (2006) The early embryo loss caused by 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin may be related to the accumulation of this compound in the uterus. Reprod. Toxicol. 21, 301-306.
38. Ligon K. L., Kesari S., Kitada M., Sun T., Arnett H. A., Alberta J. A., Anderson D. J., Stiles C. D. and Rowitch D. H. (2006) Development of NG2 neural progenitor cells requires Olig gene function. Proc. Natl Acad. Sci. USA 103, 7853-7858.
39. Lowry O. H., Rosebrough N. J., Farr A. L. and Randall R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275.
40. Ma C., Marlowe J. L. and Puga A. (2009) The aryl hydrocarbon receptor at the crossroads of multiple signaling pathways. EXS. 99, 231-257.
41. Marshall N. B. and Kerkvliet N. I. (2010) Dioxin and immune regulation: emerging role of aryl hydrocarbon receptor in the generation of regulatory T cells. Ann. N Y Acad. Sci. 1183, 25-37.
42. Matthews J., Wihlén B., Thomsen J. and Gustafsson J. A. (2005) Aryl hydrocarbon receptor-mediated transcription: ligand-dependent recruitment of estrogen receptor alpha to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin-responsive promoters. Mol. Cell. Biol. 25, 5317-5328.
43. Miller R. H. and Mi S. (2007) Dissecting demyelination. Nat. Neurosci. 10, 1351-1354.
44. Morrow D., Qin C., Smith R., III and Safe S. (2004) Aryl hydrocarbon receptor-mediated inhibition of LNCaP prostate cancer cell growth and hormone-induced transactivation. J. Steroid Biochem. Mol. Biol. 88, 27-36.
45. Nagayama J., Kohno H., Kunisue T., Kataoka K., Shimomura H., Tanabe S. and Konishi S. (2007) Concentrations of organochlorine pollutants in mothers who gave birth to neonates with congenital hypothyroidism. Chemosphere 68, 972-976.
46. Nicolay D. J., Doucette J. R. and Nazarali A. (2007) Transcriptional control of oligodendrogenesis. Glia 55, 1287-1299.
47. Nishimura N., Yonemoto J., Miyabara Y., Sato M. and Tohyama C. (2003) Rat thyroid hyperplasia induced by gestational and lactational exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Endocrinology 144, 2075-2083.
48. Nishimura N., Yonemoto J., Nishimura H., Ikushiro S. and Tohyama C. (2005) Disruption of thyroid hormone homeostasis at weaning of Holtzman rats by lactational but not in utero exposure to 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin. Toxicol. Sci. 85, 607-614.
49. Obregon M. J., Calvo R. M., Del Rey F. E. and De Escobar G. M. (2007) Ontogenesis of thyroid function and interactions with maternal function. Endocr. Dev. 10, 86-98.
50. Ohtake F., Takeyama K., Matsumoto T. et al. (2003) Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423, 545-550.
51. O'Shea P. J. and Williams G. R. (2002) Insight into the physiological actions of thyroid hormone receptors from genetically modified mice. J. Endocrinol. 175, 553-570.
52. Pallud S., Lennon A. -M., Ramauge M., Gavaret J.-M., Croteau W., Pierre M., Courtin F. and St. Germain D. L. (1997) Expression of the Type II Iodothyronine Deiodinase in Cultured Rat Astrocytes Is Selenium-dependent. J. Biol. Chem 272, 18104-18110.
53. Polito A. and Reynolds R. (2005) NG2-expressing cells as oligodendrocyte progenitors in the normal and demyelinated adult central nervous system. J. Anat. 207, 707-716.
54. Rice D. and Barone S., Jr (2000) Critical periods of vulnerability for the developing nervous system: evidence from humans and animal models. Environ. Health Perspect. 108, 511-533.
55. Rodríguez-Peña A. (1999) Oligodendrocyte development and thyroid hormone. J. Neurobiol. 40, 497-512.
56. Rogister B., Ben-Hur T. and Dubois-Dalcq M. (1999) From neural stem cells to myelinating oligodendrocytes. Mol. Cell. Neurosci. 14, 287-300.
57. Schoonover C. M., Seibel M. M., Jolson D. M., Stack M. J., Rahman R. J., Jones S. A., Mariash C. N. and Anderson G. W. (2004) Thyroid hormone regulates oligodendrocyte accumulation in developing rat brain white matter tracts. Endocrinology 145, 5013-5020.
58. Seo B. W., Li M. H., Hansen L. G., Moore R. W., Peterson R. E. and Schantz S. L. (1995) Effects of gestational and lactational exposure to coplanar polychlorinated biphenyl (PCB) congeners or 2, 3, 7, 8-tetrachlorodibenzo-p-dioxin (TCDD) on thyroid hormone concentrations in weanling rats. Toxicol. Lett. 78, 253-262.
59. Sharlin D. S., Bansal R. and Zoeller R. T. (2006) Polychlorinated biphenyls exert selective effects on cellular composition of white matter in a manner inconsistent with thyroid hormone insufficiency. Endocrinology 147, 846-858.
60. Singh K. P., Casado F. L., Opanashuk L. A. and Gasiewicz T. A. (2009) The aryl hydrocarbon receptor has a normal function in the regulation of hematopoietic and other stem/progenitor cell populations. Biochem. Pharmacol. 77, 577-587.
61. Suzuki G., Nakano M. and Nakano S. (2005) Distribution of PCDDs/PCDFs and Co-PCBs in human maternal blood, cord blood, placenta, milk, and adipose tissue: dioxins showing high toxic equivalency factor accumulate in the placenta. Biosci. Biotechnol. Biochem. 69, 1836-1847.
62. Thundiyil J. G., Solomon G. M. and Miller M. D. (2007) Transgenerational exposures: persistent chemical pollutants in the environment and breast milk. Pediatr. Clin. North Am. 54, 81-101.
63. Vehlow J., Bergfeldt B. and Hunsinger H. (2006) PCDD/F and related compounds in solid residues from municipal solid waste incineration - a literature review. Waste Manag. Res. 24, 404-420.
64. Wang S. L., Su P. H., Jong S. B., Guo Y. L., Chou W. L. and Päpke O. (2005) In utero exposure to dioxins and polychlorinated biphenyls and its relations to thyroid function and growth hormone in newborns. Environ. Health Perspect. 113, 1645-1650.
65. Watanabe M., Sakurai Y., Ichinose T., Kotani M. and Itoh K. (2006) Monoclonal antibody Rip specifically recognizes 2', 3'-cyclic nucleotide 3'-phosphodiesterasi in oligodendrocytes. Neurosci. Res. 84, 525-533.
66. Wilhelm M., Wittsiepe J., Lemm F. et al. (2008) The Duisburg birth cohort study: influence of the prenatal exposure to PCDD/Fs and dioxin-like PCBs on thyroid hormone status in newborns and neurodevelopment of infants until the age of 24 months. Mutat. Res. 659, 83-92.
67. Yamada-Okabe T., Aono T., Sakai H., Kashima Y. and Yamada-Okabe H. (2004) 2, 3, 7, 8-Tetrachlorodibenzo-p-dioxin augments the modulation of gene expression mediated by the thyroid hormone receptor. Toxicol. Appl. Pharmacol. 194, 201-210.
68. Zoeller R. T. and Crofton K. M. (2005) Mode of action: developmental thyroid hormone insufficiency - neurological abnormalities resulting from exposure to propylthiouracil. Crit. Rev. Toxicol. 35, 771-781.
69. Zoeller R. T. and Rovet J. (2004) Timing of thyroid hormone action in the developing brain: clinical observations and experimental findings. J. Neuroendocrinol. 16, 809-818.
70. Zoeller R. T., Dowling A. L. and Vas A. A. (2000) Developmental exposure to polychlorinated biphenyls exerts thyroid hormone-like effects on the expression of RC3/neurogranin and myelin basic protein messenger ribonucleic acids in the developing rat brain. Endocrinology 141, 181-189.