Molecular mechanisms of 2, 3′, 4, 4′, 5-pentachlorobiphenyl-induced thyroid dysfunction in FRTL-5 cells

PLoS ONE

Volumn 10, Issue 3, 2015, Pages

  Yang, Hui ^a   Chen, Huanhuan ^a   Guo, Hongwei ^a   Li, Wen ^a   Tang, Jinmei ^a   Xu, Bojin ^a   Sun, Minne ^a   Ding, Guoxian ^a   Jiang, Lin ^a   Cui, Dai ^a   Zheng, Xuqin ^a   Duan, Yu ^a  

^a NANJING MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

2,3',4,4',5 PENTACHLOROBIPHENYL; BIPHENYL DERIVATIVE; MESSENGER RNA; PROTEIN KINASE B; SODIUM IODIDE SYMPORTER; TRANSCRIPTION FACTOR FKHRL1; UNCLASSIFIED DRUG; 2,3',4,4',5-PENTACHLOROBIPHENYL; COTRANSPORTER; DIMETHYL SULFOXIDE; FORKHEAD TRANSCRIPTION FACTOR; FOXO3A PROTEIN, RAT; PHOSPHATIDYLINOSITOL 3 KINASE; POLYCHLORINATED BIPHENYL; SMALL INTERFERING RNA;

ANIMAL CELL; APOPTOSIS ASSAY; ARTICLE; CELL COUNTING; CELL LEVEL; CELL LINE; CELL VIABILITY; CONCENTRATION RESPONSE; CONTROLLED STUDY; GENETIC TRANSCRIPTION; MOLECULAR MECHANICS; NONHUMAN; PROTEIN EXPRESSION; RAT; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; REPORTER GENE; SIGNAL TRANSDUCTION; THYROID DISEASE; WESTERN BLOTTING; ANIMAL; ANTAGONISTS AND INHIBITORS; APOPTOSIS; CYTOLOGY; DOWN REGULATION; DRUG EFFECTS; GENETICS; METABOLISM; PHOSPHORYLATION; PROMOTER REGION; THYROID GLAND; UPREGULATION;

ANIMALIA; MAMMALIA; RATTUS;

ANIMALS; APOPTOSIS; CELL LINE; DIMETHYL SULFOXIDE; DOWN-REGULATION; FORKHEAD TRANSCRIPTION FACTORS; PHOSPHATIDYLINOSITOL 3-KINASES; PHOSPHORYLATION; POLYCHLORINATED BIPHENYLS; PROMOTER REGIONS, GENETIC; PROTO-ONCOGENE PROTEINS C-AKT; RATS; RNA, MESSENGER; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; SYMPORTERS; THYROID GLAND; UP-REGULATION;

EID: 84925436682     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120133     Document Type: Article

References (50)

1. Arnold DL, Bryce F, McGuire PF, Stapley R, Tanner JR, Wrenshall E, et al. Toxicological consequences of aroclor 1254 ingestion by female rhesus (Macaca mulatta) monkeys. Part 2. Reproduction and infant findings. Fd Chem Toxic.1995; 33: 457-474.
2. Golden R, Kimbrough R. Weight of evidence evaluation of potential human cancer risks from exposure to polychlorinated biphenyls: an update based on studies published since 2003. Crit Rev Toxicol.2009; 39: 299-331. doi: 10.1080/10408440802291521 PMID: 19514916
3. Portigal CL, Cowell SP, Fedoruk MN, Butler CM, Rennie PS, Nelson CC. Polychlorinated biphenyls interfere with androgen-induced transcriptional activation and hormone binding. Toxicol Appl Pharmacol. 2002; 179: 185-194. PMID: 11906248
4. Zhao G, Wang Z, Zhou H, Zhao Q. Burdens of PBBs, PBDEs, and PCBs in tissues of the cancer patients in the e-waste disassembly sites in Zhejiang, China. Sci Total Environ. 2009; 407: 4831-4837. doi: 10.1016/j.scitotenv.2009.05.031 PMID: 19539352
5. Rolland RM. A review of chemically induced alterations in thyroid and vitamin A status from field studies of wildlife and fish. Journal of Wildlife Diseases. 2000; 36: 615-635. PMID: 11085423
6. Tang JM, Li W, Xie YC, Guo HW, Cheng P, Chen HH, et al. Morphological and functional deterioration of the rat thyroid following chronic exposure to low-dose PCB118. Exp Toxicol Pathol. 2013; 65: 989-994. doi: 10.1016/j.etp.2013.02.001 PMID: 23557935
7. Ishihara A, Sawatsubashi S, Yamauchi K. Endocrine disrupting chemicals: interference of thyroid hormone binding to transthyretins and to thyroid hormone receptors. Mol Cell Endocrinol. 2003; 199: 105-117. PMID: 12581883
8. Boas M, Feldt-Rasmussen U, Skakkebaek NE, Main KM. Environmental chemicals and thyroid function. Eur J Endocrinol. 2006; 154: 599-611. PMID: 16645005
9. Brown SB, Adams BA, Cyr DG, Eales JG. Contaminant effects on the teleost fish thyroid. Environ Toxicol Chem. 2004; 23: 1680-1701. PMID: 15230321
10. Dohan O, De la Vieja A, Paroder V, Riedel C, Artani M, Reed M, et al. The sodium/iodide Symporter (NIS): characterization, regulation, and medical significance. Endocr Rev. 2003; 24: 48-77. PMID: 12588808
11. Kogai T, Taki K, Brent GA. Enhancement of sodium/iodide symporter expression in thyroid and breast cancer. Endocr Relat Cancer. 2006; 13: 797-826. PMID: 16954431
12. Serrano-Nascimento C, da Silva Teixeira S, Nicola JP, Nachbar RT, Masini-Repiso AM, Nunes MT. The acute inhibitory effect of iodide excess on sodium/iodide symporter expression and activity involves the PI3K/Akt signaling pathway. Endocrinology. 2014; 155: 1145-1156. doi: 10.1210/en.2013-1665 PMID: 24424051
13. Bauer TM, Patel MR, Infante JR. Targeting PI3 kinase in cancer. Pharmacol Ther. 2014; 8. Available: http://dx.doi.org/10.1016/j.pharmthera.2014.09.006.
14. Dal Col J, Zancai P, Terrin L, Guidoboni M, Ponzoni M, Pavan A, et al. Distinct functional significance of Akt and mTOR constitutive activation in mantle cell lymphoma. Blood. 2008; 111: 5142-5151. doi: 10.1182/blood-2007-07-103481 PMID: 18339899
15. Laia Rosich AM, Xargay-Torrent S, López-Guerra M, Roldán J, Aymerich M, Salaverria I, et al. Dual PI3K-mTOR inhibition is required to effectively impair microenvironment survival signals in mantle cell lymphoma. Oncotarget. 2014; 5:6788-6800. PMID: 25216518
16. Rodon J, Dienstmann R, Serra V, Tabernero J. Development of PI3K inhibitors: lessons learned from early clinical trials. Nat Rev Clin Oncol. 2013; 10: 143-153. doi: 10.1038/nrclinonc.2013.10 PMID: 23400000
17. Manning BD, Cantley LC. AKT/PKB signaling: navigating downstream. Cell. 2007; 129: 1261-1274. PMID: 17604717
18. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, et al. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell. 1999; 96: 857-868. PMID: 10102273
19. Medema RH, Kops GJ, Bos JL, Burgering BM. AFX-like Forkhead transcription factors mediate cellcycle regulation by Ras and PKB through p27kip1. Nature. 2000; 404: 782-787. PMID: 10783894
20. Luo X, Puig O, Hyu J, Bohmann D, Jasper H. Foxo and Fos regulate the decision between cell death and survival in response to UV irradiation. Embo J. 2007; 26: 380-390. PMID: 17183370
21. Olmos Y, Valle I, Borniquel S, Tierrez A, Soria E, Lamas S, et al. Mutual dependence of Foxo3a and PGC-1alpha in the induction of oxidative stress genes. J Biol Chem. 2009; 284: 14476-14484. doi: 10.1074/jbc.M807397200 PMID: 19324885
22. Kops GJ, Dansen TB, Polderman PE, Saarloos I, Wirtz KW, Coffer PJ, et al. Forkhead transcription factor FOXO3a protects quiescent cells from oxidative stress. Nature. 2002; 419: 316-321. PMID: 12239572
23. Van Der Heide LP, Hoekman MF, Smidt MP. The ins and outs of FoxO shuttling: mechanisms of FoxO translocation and transcriptional regulation. Biochem J. 2004; 380: 297-309. PMID: 15005655
24. Guerrieri F, Piconese S, Lacoste C, Schinzari V, Testoni B, Valogne Y, et al. The sodium/iodide symporter NIS is a transcriptional target of the p53-family members in liver cancer cells. Cell Death Dis. 2013; 4: e807. doi: 10.1038/cddis.2013.302 PMID: 24052075
25. Sastre-Perona A, Santisteban P. Wnt-Independent Role of beta-Catenin in Thyroid Cell Proliferation and Differentiation. Mol Endocrinol. 2014; 28: 681-695. doi: 10.1210/me.2013-1377 PMID: 24645679
26. Medina DL, Santisteban P. Thyrotropin-dependent proliferation of in vitro rat thyroid cell systems. Eur J Endocrinol. 2000; 143: 161-178. PMID: 10913934
27. Weidinger C, Krause K, Mueller K, Klagge A, Fuhrer D. FOXO3 is inhibited by oncogenic PI3K/Akt signaling but can be reactivated by the NSAID sulindac sulfide. J Clin Endocrinol Metab. 2011; 96: E1361-E1371. doi: 10.1210/jc.2010-2453 PMID: 21752881
28. Zheng XQ, Cui D, Xu SH, Brabant G, Derwahl M. Doxorubicin fails to eradicate cancer stem cells derived from anaplastic thyroid carcinoma cells: Characterization of resistant cells. International Journal of Oncology. 2010; 37:307-315. PMID: 20596658
29. Lan L, Cui D, Nowka K, Derwahl M. Stem cells derived from goiters in adults form spheres in response to intense growth stimulation and require thyrotropin for differentiation into thyrocytes. J Clin Endocrinol Metab. 2007; 92: 3681-3688. PMID: 17609303
30. Kawashima A, Tanigawa K, Akama T, Wu H, Sue M, Yoshihara A, et al. Fragments of genomic DNA released by injured cells activate innate immunity and suppress endocrine function in the thyroid. Endocrinology. 2011; 152: 1702-1712. doi: 10.1210/en.2010-1132 PMID: 21303947
31. Liu X, Zhang B, Guo Y, Liang Q, Wu C, Wu L, et al. Down-regulation of AP-4 inhibits proliferation, induces cell cycle arrest and promotes apoptosis in human gastric cancer cells. PLOS ONE. 2012; 7: e37096. doi: 10.1371/journal.pone.0037096 PMID: 22615908
32. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C (T)) Method. Methods. 2001; 25: 402-408. PMID: 11846609
33. Ohashi E, Miyajima N, Nakagawa T, Takahashi T, Kagechika H, Mochizuki M, et al. Retinoids induce growth inhibition and apoptosis in mast cell tumor cell lines. J Vet Med Sci. 2006; 68: 797-802. PMID: 16953078
34. McFarland VA, Clarke JU. Environmental occurrence, abundance, and potential toxicity of polychlorinated biphenyl congeners: considerations for a congener-specific analysis. Environ Health Perspect. 1989; 81:225-239. PMID: 2503374
35. Tarkowski S. Environmental health in Europe. A WHO perspective. Int J Occup Med Environ Health. 1996; 9: 1-6. PMID: 8776147
36. Bloom MS, Weiner JM, Vena JE, Beehler GP. Exploring associations between serum levels of select organochlorines and thyroxine in a sample of New York state sportsmen: the New York State Angler Cohort Study. Environ Res. 2003; 93: 52-66. PMID: 12865048
37. Wassermann M, Wassermann D, Cucos S, Miller HJ. World PCBs map: storage and effects in man and his biologic environment in the 1970s. Ann N Y Acad Sci. 1979; 320: 69-124. PMID: 110205
38. Al-Anati L, Hogberg J, Stenius U. Non-dioxin-like PCBs interact with benzo[a]pyrene-induced p53-responses and inhibit apoptosis. Toxicol Appl Pharmacol. 2010; 249: 166-177. doi: 10.1016/j.taap.2010.09.004 PMID: 20840854
39. Venkatesha VA, Kalen AL, Sarsour EH, Goswami PC. PCB-153 exposure coordinates cell cycle progression and cellular metabolism in human mammary epithelial cells. Toxicol Lett. 2010; 196: 110-116. doi: 10.1016/j.toxlet.2010.04.005 PMID: 20394812
40. Howard A. Polychlorinated biphenyls induce caspase-dependent cell death in cultured embryonic rat hippocampal but not cortical neurons via activation of the ryanodine receptor. Toxicology and Applied Pharmacology. 2003; 190: 72-86. PMID: 12831785
41. Merritt RL, Foran CM. Influence of persistent contaminants and steroid hormones on glioblastoma cell growth. J Toxicol Environ Health A. 2007; 70: 19-27. PMID: 17162496
42. Sanchez-Alonso JA, Lopez-Aparicio P, Recio MN, Perez-Albarsanz MA. Apoptosis-mediated neurotoxic potential of a planar (PCB 77) and a nonplanar (PCB 153) polychlorinated biphenyl congeners in neuronal cell cultures. Toxicol Lett. 2003; 144: 337-349. PMID: 12927351
43. Rankouhi TR, Sanderson JT, van Holsteijn I, van Leeuwen C, Vethaak AD, van den Berg M. Effects of natural and synthetic estrogens and various environmental contaminants on vitellogenesis in fish primary hepatocytes: comparison of bream (Abramis brama) and carp (Cyprinus carpio). Toxicol Sci. 2004; 81: 90-102. PMID: 15159526
44. Pocar P, Klonisch T, Brandsch C, Eder K, Frohlich C, Hoang-Vu C, et al. AhR-agonist-induced transcriptional changes of genes involved in thyroid function in primary porcine thyrocytes. Toxicol Sci. 2006; 89: 408-414. PMID: 16291828
45. Kato Y, Ikushiro S, Haraguchi K, Yamazaki T, Ito Y, Suzuki H, et al. A possible mechanism for decrease in serum thyroxine level by polychlorinated biphenyls in Wistar and Gunn rats. Toxicol Sci. 2004; 81: 309-315. PMID: 15254343
46. Zaballos MA, Garcia B, Santisteban P. Gbetagamma dimers released in response to thyrotropin activate phosphoinositide 3-kinase and regulate gene expression in thyroid cells. Mol Endocrinol. 2008; 22: 1183-1199. doi: 10.1210/me.2007-0093 PMID: 18202153
47. Kogai T, Sajid-Crockett S, Newmarch LS, Liu YY, Brent GA. Phosphoinositide-3-kinase inhibition induces sodium/iodide symporter expression in rat thyroid cells and human papillary thyroid cancer cells. J Endocrinol. 2008; 199: 243-252. doi: 10.1677/JOE-08-0333 PMID: 18762555
48. Liu YY, Zhang X, Ringel MD, Jhiang SM. Modulation of sodium iodide symporter expression and function by LY294002, Akti-1/2 and Rapamycin in thyroid cells. Endocr Relat Cancer. 2012; 19: 291-304. doi: 10.1530/ERC-11-0288 PMID: 22355179
49. Liu Z, Xing M. Induction of sodium/iodide symporter (NIS) expression and radioiodine uptake in nonthyroid cancer cells. PLOS ONE. 2012; 7: e31729. doi: 10.1371/journal.pone.0031729 PMID: 22359623
50. Downward J. Mechanisms and consequences of activation of protein kinase B/Akt. Curr Opin Cell Biol. 1998; 10: 262-267. PMID: 9561851