Sex-dependent changes in cerebellar thyroid hormone-dependent gene expression following perinatal exposure to thimerosal in rats

Journal of Physiology and Pharmacology

Volumn 63, Issue 3, 2012, Pages 277-283

  Khan, A ^a   Sulkowski, Z L ^a   Chen, T ^a   Zavacki, A M ^a   Sajdel Sulkowska, Elizabeth M ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Brain derived neurotrophic factor; Cerebellum; Reelin; Suppressor of white apricot 1 (swap 1); Thimerosal; Thyroid hormone

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DEIODINASE 2; DEIODINASE 3; MEMBRANE PROTEIN; MESSENGER RNA; PREALBUMIN; REELIN; SUPPRESSOR OF WHITE APRICOT 1; THIOMERSAL; THYROID HORMONE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA SYNTHESIS; FEMALE; GENE; GENE EXPRESSION REGULATION; HYPOTHYROIDISM; MALE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERINATAL DRUG EXPOSURE; PERINATAL PERIOD; RAT; RNA SPLICING; SEX DIFFERENCE; SWAP 1 GENE;

ANIMALS; ANIMALS, NEWBORN; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL ADHESION MOLECULES, NEURONAL; CELL DIFFERENTIATION; CELL PROLIFERATION; CEREBELLUM; EXTRACELLULAR MATRIX PROTEINS; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK PROTEINS; IODIDE PEROXIDASE; MALE; NERVE TISSUE PROTEINS; NEURONS; PREALBUMIN; RATS; RATS, INBRED SHR; SERINE ENDOPEPTIDASES; SEX FACTORS; THIMEROSAL; THYROID HORMONES;

EID: 84864018794     PISSN: 08675910     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Koibuchi N. The role of thyroid hormone on cerebellar development. Cerebellum 2008; 7: 530-533. 282
2. Watanabe C, Yoshida K, Kasanuma Y, Kun Y, Satoh H. In utero methylmercury exposure differentially affects the activities of selenoenzymes in the fetal mouse brain. Environ Res 1999; 80: 208-214.
3. Mori K, Yoshida K, Tani J, Hoshikawa S, Ito S, Watanabe C. Methylmercury inhibits type II 5'-deiodinase activity in NB41A3 neuroblastoma cells. Toxicol Lett 2006; 161: 96-101.
4. Mori K, Yoshida K, Nakagawa Y, et al. Methylmercury inhibits type II 5'-deiodinase activity resulting in a decrease in growth hormone production in GH3 cells. Toxicology 2007; 237: 203-209.
5. Sulkowski ZL, Chen T, Midha S, Zavacki AM, Sajdel-Sulkowska EM. Maternal thimerosal exposure results in aberrant cerebellar oxidative stress, thyroid hormone metabolism, and motor behavior in rat pups; sex-and strain-dependent effects. Cerebellum 2012; 11: 575-586.
6. Crantz FR, Silva JE, Larsen PR. An analysis of the sources and quantity of 3,5,3'-triiodothyronine specifically bound to nuclear receptors in rat cerebral cortex and cerebellum. Endocrinology 1982; 110: 367-375.
7. Morte B, Ceballos A, Diez D, et al. Thyroid hormone-regulated mouse cerebral cortex genes are differentially dependent on the source of the hormone: a study in monocarboxylate transporter-8-and deiodinase-2-deficient mice. Endocrinology 2010; 151: 2381-2387.
8. Hornig M, Chian D, Lipkin WI. Neurotoxic effects of postnatal thimerosal are mouse strain dependent. Mol Psychiatry 2004; 9: 833-845.
9. Burbacher TM, Shen DD, Liberato N, Grant KS, Cernichiari E, Clarkson T. Comparison of blood and brain mercury levels in infant monkeys exposed to methylmercury or vaccines containing thimerosal. Environ Health Perspect 2005; 113: 1015-1021.
10. Olczak M, Duszczyk M, Mierzejewski P, Majewska MD. Neonatal administration of a vaccine preservative, thimerosal, products lasting impairment of nociception and apparent activation of opioid system in rats. Brain Res 2009; 1301: P143-P151.
11. http://www.fda.gov/cber/vaccine/thimerosal.htm#+3
12. Orct T, Blanusa M, Lazarus M, Varnai VM, Kostial K. Comparison of organic and inorganic mercury distribution in suckling rat. J Appl Toxicol 2006; 26: 536-539.
13. Eccles CU, Annau Z. Prenatal methyl mercury exposure: I. Alterations in neonatal activity. Neurobehav Tocicol Teratol 1982; 4: 371-376.
14. Zavacki AM, Ying H, Christoffolete MA, et al. Type 1 iodothyronine deiodinase is a sensitive marker of peripheral thyroid status in the mouse. Endocrinology 2005; 146: 1568-1575.
15. Cuadrado A, Bernal J, Munoz A. Identification of the mammalian homolog of the splicing regulator suppressor-of-white-apricot as a thyroid hormone regulated gene. Brain Res Mol Brain Res 1999; 71: 332-340.
16. Padhi BK, Pelletier G, Williams A, et al. Gene expression profiling in rat cerebellum following in utero and lactational exposure to mixtures of methylmercury, polychlorinated biphenyls and organochlorine pesticides. Toxicol Lett 2008; 176: 93-103.
17. Gereben B, Zavacki AM, Ribich S, et al. Cellular and molecular basis of deiodinase-regulated thyroid hormone signaling. Endocr Rev 2008; 29: 898-938.
18. Dong H, Wade M, Williams A, Lee A, Douglas GR, Yauk C. Molecular insight into the effects of hypothyroidism on the developing cerebellum. Biochem Biophys Res Commun 2005; 330: 1182-1193.
19. Royland JE, Parker JS, Gilbert ME. A genomic analysis of subclinical hypothyroidism in hippocampus and neocortex of the developing rat brain. J Neuroendocrinol 2008; 20: 1319-1338.
20. Takahashi M, Negishi T, Tashiro T. Identification of genes mediating thyroid hormone action in the developing mouse cerebellum. J Neurochem 2008; 104: 640-652.
21. Li Y, Li S, Zhao R, et al. Effects of methylmercury on embryonic cell behavior and expression of related gene. Zhoghua Yu Fang Yi Xue Za Zhi 1999; 33: 81-84.
22. Glover CN, Zheng D, Jayashankar S, Sales GD, Hogstrand C, Lundebye AK. Methylmercury speciation influences brain gene expression and behavior in gestetionally-exposed mice pups. Toxicological Sciences 2009; 110: 389-400.
23. Minami T, Miyata E, Sakamoto Y, Kohama A, Yamazaki H, Ichida S. Expression of metallothionein mRNAs on mouse cerebellum microglia cells by thimerosal and its metabolites. Toxicology 2009; 261: 25-32.
24. Minami T, Miyata E, Sakamoto Y, Yamazaki H, Ichida S. Induction of metallothionein in mouse cerebellum and cerebrum with low-dose thimerosal injection. Cell Biol Toxicol 2010; 26: 143-152.
25. Galton VA, Wood ET, St. Germain EA, et al. Thyroid hormone homeostasis and action in the type 2 deiodinase-deficient rodent brain during development. Endocrinology 2007; 148: 3080-3088.
26. Donai H, Murakami T, Amano T, Sogawa Y, Yamauchi T. Induction and alternative splicing of delta isoform of Ca(2+)/camodulin-dependent protein kinase II during neural differentiation of P19 embryonal carcinoma cells and during brain development. Brain Res Mol Brain Res 2000; 85: 189-199.
27. Ghafouri-Fard S, Abbasi A, Moslehi H, et al. Elevated expression levels of testis-specific genes TEX101 and SPATA19 in basal cell carcinoma and their correlation with clinical and pathological features. Br J Dermatol 2010; 162: 772-779.
28. Galton VA. The roles of the iododthyronine deiodinases in mammalian development. Thyroid 2005; 15: 823-834.
29. Richardson SJ. Cell and molecular biology of transthyretin and thyroid hormones. Int Rev Cytol 2007; 258: 137-193.
30. Visser WE, Friesema EC, Visser TJ. Minireview: thyroid hormone transporters: the knowns and the unknowns. Mol Endocrinol 2011; 25: 1-14.
31. Alvarez-Dolado M, Cuadrado A, Navarro-Yuberro C, et al. Regulation of the L1 cell adhesion molecule by thyroid hormone in the developing brain. Mol Cell Neurosci 2000; 16: 499-514.
32. Guan J, Luo Y, Denker BM. Purkinje cell protein-2 (Pcp2) stimulates differentiation in PC12 cells by Gbetagamma-mediated activation of Ras and p38 MAPK. Biochem J 2005; 392: 389-397.
33. Anderson GW, Hagen SG, Larson RJ, et al. Purkinje cell protein-2 cis elements mediate repression of T3-dependent transcriptional activation. Mol Cell Endocrinol 1997; 131: 79-87.
34. Tu HM, Legradi G, Bartha T, Salvatore D, Lechan RM, Larsen PR. Regional expression of the type 3 iodothyronine deiodinase messenger ribonucleic acid in the rat central nervous system and its regulation by thyroid hormone. Endocrinology 1999; 140: 784-790.
35. Koibuchi N, Yamaoka S, Chin WW. Effect of altered thyroid status on neurotrophin gene expression during postnatal development of the mouse cerebellum. Thyroid 2001; 11: 205-210.
36. Camboni D, Roskoden T, Schwegler H. Effect of early thyroxine on brain-derived neurotrophic factor mRNA expression and protein amount in the rat medial septum/diagonal band of Broca. Neurosci Lett 2003; 350: 141-144. 283
37. Pathak A, Sinha RA, Mohan V, Mitra K, Godbole MM. Maternal thyroid hormone before the onset of fetal thyroid function regulates reelin and downstream signaling cascade affecting neocortical neuronal migration. Cereb Cortex 2011; 21: 11-21.
38. Takahashi H, Takahashi K, Liu FC. FOXP genes, neural development, speech and language disorders. Adv Exp Med Biol 2009; 665: 117-129.
39. Inoue N, Watanabe M, Morita M, et al. Association of functional polymorphism related to the transcriptional level of FoxP3 with prognosis of autoimmune thyroid diseases. Clin Exp Immunol 2010; 162: 402-406.
40. Cuesta I, Zaret KS, Santisteban P. The forkhead factor FoxE1 binds to the thyroperoxidase promoter during thyroid cell differentiation and modifies compacted chromatin structure. Mol Cell Biol 2007; 27: 7302-7314.
41. Tam WY, Leung CK, Tong KK, Kwan KM. FoxP4 is essential in maintenance of Purkinje cell dendritic arborization in the mouse cerebellum. Neuroscience 2011; 172: 562-571.
42. Gao Y, Yan CH, Tian Y, et al. Prenatal exposure to mercury and neurobehavioral development of neonates in Zhoushan City, China. Environ Res 2007; 105: 390-399.
43. Sobutskii MP, Kovan'ko EG, Liutinskii SI, Ivanov SD. Effect of age and gender on genotoxic and biochemical indexes in animal blood after low doses of radiation-mercury exposure. Adv Gerontol 2007; 20: 91-96.
44. Branch DR. Gender-selective toxicity to thimerosal. Exp Toxicol Pathol 2009; 61: 133-136.
45. Ekstrand J, Nielsen JB, Havarinasab S, Zalups RK, Soderkvist P. Mercury toxicokinetics-dependency on strain and gender. Toxicol Appl Pharmacol 2010; 243: 283-291.
46. Wyrembek P, Szczuraszek K, Majewska MD, Mozrzymas JW. Intermingled modulatory and neurotoxic effects of thimerosal and mercuric ions on electrophysiological responses to GABA and NMDA in hippocampal neurons. J Physiol Pharmacol 2010; 61: 753-758.
47. Liu W, Wang X, ZhangR, ZhouY. Effects of postnatal exposure to methylmercury on spatial learning and memory and brain NMDA receptor mRNA expression in rats. Toxicol Lett 2009; 188: 230-235.
48. Lee S, Mian MF, Lee HJ, et al. Thimerosal induces oxidative stress in HeLa S epithelial cells. Environ Toxicol Pharmacol 2006; 22: 194-199.
49. Hagele TJ, Mazerik JN, Gregory A, et al. Mercury activates vascular endothelial cell phospholipase D through thiols and oxidative stress. Int J Toxicol 2007; 26: 57-69.
50. Madri JA. Modeling the neurovascular niche: implications for recovery from CNS injury. J Physiol Pharmacol 2009; 60(Suppl. 4): 95-104.
51. Fonnum F, Lock EA. Cerebellum as a target of toxic substances. Toxicol Lett 2000; 112-113: 9-16.