JNK pathway decreases thyroid hormones via TRH receptor: A novel mechanism for disturbance of thyroid hormone homeostasis by PCB153

Toxicology

Volumn 302, Issue 1, 2012, Pages 68-76

  Liu, Changjiang ^a   Ha, Mei ^b   Cui, Yushan ^c   Wang, Chengmin ^a   Yan, Maosheng ^a   Fu, Wenjuan ^a   Quan, Chao ^a   Zhou, Jun ^a   Yang, Kedi ^a  

^a HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

^b WUHAN UNIVERSITY   (China)

^c TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

JNK pathway; PCB153; Thyroid hormone homeostasis; TRH receptor

Indexed keywords

2,2',4,4',5,5' HEXACHLOROBIPHENYL; GLUTATHIONE PEROXIDASE; LIOTHYRONINE; MALONALDEHYDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PROTIRELIN; PROTIRELIN RECEPTOR; STRESS ACTIVATED PROTEIN KINASE; SUPEROXIDE DISMUTASE; THYROID HORMONE; THYROTROPIN; THYROXINE;

ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FREE LIOTHYRONINE INDEX; FREE THYROXINE INDEX; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; LIOTHYRONINE BLOOD LEVEL; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; THYROID GLAND; THYROTROPIN BLOOD LEVEL; THYROXINE BLOOD LEVEL;

ANIMALS; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; HOMEOSTASIS; HUMANS; INJECTIONS, INTRAPERITONEAL; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MALE; POLYCHLORINATED BIPHENYLS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, THYROID HORMONE; THYROTROPIN-RELEASING HORMONE; THYROXINE; TRIIODOTHYRONINE;

ANIMALIA; RATTUS;

EID: 84865982169     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.07.016     Document Type: Article

References (34)

1. Belgardt B.F., Mauer J., Wunderlich F.T., Ernst M.B., Pal M., Spohn G., Brönneke H.S., Brodesser S., Hampel B., Schauss A.C., Brüning J.C. Hypothalamic and pituitary c-Jun N-terminal kinase 1 signaling coordinately regulates glucose metabolism. Proc. Natl. Acad. Sci. U.S.A. 2010, 107:6028-6033.
2. Bennett B.L., Sasaki D.T., Murray B.W., O'Leary E.C., Sakata S.T., Xu W., Leisten J.C., Motiwala A., Pierce S., Satoh Y., Bhagwat S.S., Manning A.M., Anderson D.W. SP600125, an anthrapyrazolone inhibitor of Jun N-terminal kinase. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:13681-13686.
3. Boas M., Feldt-Rasmussen U., Skakkebaek N.E., Main K.M. Environmental chemicals and thyroid function. Eur. J. Endocrinol. 2006, 154:599-611.
4. Cao J., Lin Y., Guo L.H., Zhang A.Q., Wei Y., Yang Y. Structure-based investigation on the binding interaction of hydroxylated polybrominated diphenyl ethers with thyroxine transport proteins. Toxicology 2010, 277:20-28.
5. Chauhan K.R., Kodavanti P.R., McKinney J.D. Assessing the role of ortho-substitution on polychlorinated biphenyl binding to transthyretin, a thyroxine transport protein. Toxicol. Appl. Pharmacol. 2000, 162:10-21.
6. Cheek A.O., Kow K., Chen J., McLachlan J.A. Potential mechanisms of thyroid disruption in humans: interaction of organochlorine compounds with thyroid receptor, transthyretin, and thyroid-binding globulin. Environ. Health Perspect. 1999, 107:273-278.
7. Conde de la Rosa L., Schoemaker M.H., Vrenken T.E., Buist-Homan M., Havinga R., Jansen P.L., Moshage H. Superoxide anions and hydrogen peroxide induce hepatocyte death by different mechanisms: involvement of JNK and ERK MAP kinases. J. Hepatol. 2006, 44:918-929.
8. Craft E.S., DeVito M.J., Crofton K.M. Comparative responsiveness of hypothyroxinemia and hepatic enzyme induction in Long-Evans rats versus C57BL/6J mice exposed to TCDD-like and phenobarbital-like polychlorinated biphenyl congeners. Toxicol. Sci. 2002, 68:372-380.
9. Davies T., Marians R., Latif R. The TSH receptor reveals itself. J. Clin. Invest. 2002, 110:161-164.
10. Davis R.J. Signal transduction by the JNK group of MAP kinases. Cell 2000, 103:239-252.
11. De Miguel M., Fernández-Santos J.M., Utrilla J.C., Carrillo-Vico A., Borrero J., Conde E., Guerrero J.M., Martín-Lacave I. Thyrotropin-releasing hormone receptor expression in thyroid follicular cells: a new paracrine role of C-cells?. Histol. Histopathol. 2005, 20:713-718.
12. Fisher J.W., Campbell J., Muralidhara S., Bruckner J.V., Ferguson D., Mumtaz M., Harmon B., Hedge J.M., Crofton K.M., Kim H., Almekinder T.L. Effect of PCB 126 on hepatic metabolism of thyroxine and perturbations in the hypothalamic-pituitary-thyroid axis in the rat. Toxicol. Sci. 2006, 90:87-95.
13. Gauger K.J., Giera S., Sharlin D.S., Bansal R., Iannacone E., Zoeller R.T. Polychlorinated biphenyls 105 and 118 form thyroid hormone receptor agonists after cytochrome P4501A1 activation in rat pituitary GH3 cells. Environ. Health Perspect. 2007, 115:1623-1630.
14. Hallgren S., Darnerud P.O. Polybrominated diphenyl ethers (PBDEs), polychlorinated biphenyls (PCBs) and chlorinated paraffins (CPs) in rats-testing interactions and mechanisms for thyroid hormone effects. Toxicology 2002, 177:227-243.
15. Hennig B., Hammock B.D., Slim R., Toborek M., Saraswathi V., Robertson L.W. PCB-induced oxidative stress in endothelial cells: modulation by nutrients. Int. J. Hyg. Environ. Health 2002, 205:95-102.
16. Ibhazehiebo K., Iwasaki T., Kimura-Kuroda J., Miyazaki W., Shimokawa N., Koibuchi N. Disruption of thyroid hormone receptor-mediated transcription and thyroid hormone-induced Purkinje cell dendrite arborization by polybrominated diphenyl ethers. Environ. Health Perspect. 2011, 119:168-175.
17. Khan M.A., Lichtensteiger C.A., Faroon O., Mumtaz M., Schaeffer D.J., Hansen L.G. The hypothalamo-pituitary-thyroid (HPT) axis: a target of nonpersistent ortho-substituted PCB congeners. Toxicol. Sci. 2002, 65:52-61.
18. Khan M.A., Hansen L.G. Ortho-substituted polychlorinated biphenyl (PCB) congeners (95 or 101) decrease pituitary response to thyrotropin releasing hormone. Toxicol. Lett. 2003, 144:173-182.
19. Kim B.Y., Han M.J., Chung A.S. Effects of reactive oxygen species on proliferation of Chinese hamster lung fibroblast (V79) cells. Free Radic. Biol. Med. 2001, 30:686-698.
20. Knerr S., Schrenk D. Carcinogenicity of " non-dioxinlike" polychlorinated biphenyls. Crit. Rev. Toxicol. 2006, 36:663-694.
21. Li M.H., Hsu P.C., Guo Y.L. Hepatic enzyme induction and acute endocrine effects of 2,2',3,3',4,6'-hexachlorobiphenyl and 2,2',3,4',5',6-hexachlorobiphenyl in prepubertal female rats. Arch. Environ. Contam. Toxicol. 2001, 41:381-385.
22. Liu C., Wang C., Yan M., Quan C., Zhou J., Yang K. PCB153 disrupts thyroid hormone homeostasis by affecting its biosynthesis, biotransformation, feedback regulation, and metabolism. Horm. Metab. Res. 2012, 10.1055/s-0032-1311569.
23. Liu J., Song E., Liu L., Ma X., Tian X., Dong H., Song Y. Polychlorinated biphenyl quinone metabolites lead to oxidative stress in HepG2 cells and the protective role of dihydrolipoic acid. Toxicol. In Vitro 2012, 26:841-848.
24. Minutoli L., Altavilla D., Marini H., Passaniti M., Bitto A., Seminara P., Venuti F.S., Famulari C., Macrì A., Versaci A., Squadrito F. Protective effects of SP600125 a new inhibitor of c-Jun N-terminal kinase (JNK) and extracellular-regulated kinase (ERK1/2) in an experimental model of cerulein-induced pancreatitis. Life Sci. 2004, 75:2853-2866.
25. Morse D.C., Wehler E.K., Wesseling W., Koeman J.H., Brouwer A. Alterations in rat brain thyroid hormone status following pre- and postnatal exposure to polychlorinated biphenyls (Aroclor 1254). Toxicol. Appl. Pharmacol. 1996, 136:269-279.
26. Nussey S., Whitehead S. Endocrinology: An Integrated Approach 2001, Bios Scientific Publishers Ltd., Oxford.
27. Radice S., Chiesara E., Fucile S., Marabini L. Different effects of PCB101, PCB118, PCB138 and PCB153 alone or mixed in MCF-7 breast cancer cells. Food Chem. Toxicol. 2008, 46:2561-2567.
28. Ramadass P., Meerarani P., Toborek M., Robertson L.W., Hennig B. Dietary flavonoids modulate PCB-induced oxidative stress, CYP1A1 induction, and AhR-DNA binding activity in vascular endothelial cells. Toxicol. Sci. 2003, 76:212-219.
29. Roux P.P., Blenis J. ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 2004, 68:320-344.
30. Sabio G., Cavanagh-Kyros J., Barrett T., Jung D.Y., Ko H.J., Ong H., Morel C., Mora A., Reilly J., Kim J.K., Davis R.J. Role of the hypothalamic-pituitary-thyroid axis in metabolic regulation by JNK1. Genes Dev. 2010, 24:256-264.
31. Santini F., Vitti P., Ceccarini G., Mammoli C., Rosellini V., Pelosini C., Marsili A., Tonacchera M., Agretti P., Santoni T., Chiovato L., Pinchera A. In vitro assay of thyroid disruptors affecting TSH-stimulated adenylate cyclase activity. J. Endocrinol. Invest. 2003, 26:950-955.
32. Sharma N., Deshmukh R., Bedi K.L. SP600125, a competitive inhibitor of JNK attenuates streptozotocin induced neurocognitive deficit and oxidative stress in rats. Pharmacol. Biochem. Behav. 2010, 96:386-394.
33. Vaishnav D., Jambal P., Reusch J.E., Pugazhenthi S. SP600125, an inhibitor of c-Jun N-terminal kinase, activates CREB by a p38 MAPK-mediated pathway. Biochem. Biophys. Res. Commun. 2003, 307:855-860.
34. Zhou T., Ross D.G., DeVito M.J., Crofton K.M. Effects of short-term in vivo exposure to polybrominated diphenyl ethers on thyroid hormones and hepatic enzyme activities in weanling rats. Toxicol. Sci. 2001, 61:76-82.