Hexabromocyclododecane facilitates FSH activation of ERK1/2 and AKT through epidermal growth factor receptor in rat granulosa cells

Archives of Toxicology

Volumn 88, Issue 2, 2014, Pages 345-354

  Fa, Svetlana ^a   Samardzija, Dragana ^a   Odzic, Ljubica ^a   Pogrmic Majkic, Kristina ^a   Kaisarevic, Sonja ^a   Kovacevic, Radmila ^a   Andric, Nebojsa ^a  

^a UNIVERSITY OF NOVI SAD   (Serbia)

Author keywords

AKT; EGFR; ERK1 2; Granulosa; HBCDD; Lhr

Indexed keywords

ANIMALS; BUTADIENES; CELLS, CULTURED; FEMALE; FOLLICLE STIMULATING HORMONE; GENE EXPRESSION REGULATION; GRANULOSA CELLS; HYDROCARBONS, BROMINATED; MAP KINASE SIGNALING SYSTEM; NITRILES; PHOSPHORYLATION; PROTO-ONCOGENE PROTEINS C-AKT; QUINAZOLINES; RATS; RATS, WISTAR; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, LH; TOXICITY TESTS; TYRPHOSTINS;

EID: 84893945549     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-013-1133-2     Document Type: Article

References (41)

1. Andric N, Ascoli M (2006) A delayed gonadotropin-dependent and growth factor-mediated activation of the extracellular signal-regulated kinase 1/2 cascade negatively regulates aromatase expression in granulosa cells. Mol Endocrinol 20(12):3308-3320. doi: 10.1210/me.2006-0241
2. Andric N, Thomas M, Ascoli M (2010) Transactivation of the epidermal growth factor receptor is involved in the lutropin receptor-mediated down-regulation of ovarian aromatase expression in vivo. Mol Endocrinol 24(3):552-560. doi: 10.1210/me.2009-0450
3. Arkhipov A, Shan Y, Das R et al (2013) Architecture and membrane interactions of the EGF receptor. Cell 152(3):557-569. doi: 10.1016/j.cell.2012. 12.030
4. Campbell KL (1979) Ovarian granulosa cells isolated with EGTA and hypertonic sucrose: cellular integrity and function. Biol Reprod 21(4):773-786
5. Chen S, Liu X, Segaloff DL (2000) A novel cyclic adenosine 3′,5′-monophosphate-responsive element involved in the transcriptional regulation of the lutropin receptor gene in granulosa cells. Mol Endocrinol 14(9):1498-1508
6. Christen V, Crettaz P, Oberli-Schrammli A, Fent K (2010) Some flame retardants and the antimicrobials triclosan and triclocarban enhance the androgenic activity in vitro. Chemosphere 81(10):1245-1252. doi: 10.1016/j.chemosphere.2010.09.031
7. Conneely OM (2010) Progesterone receptors and ovulation. Handb Exp Pharmacol 198:37-44. doi: 10.1007/978-3-642-02062-9-3
8. Cottom J, Salvador LM, Maizels ET et al (2003) Follicle-stimulating hormone activates extracellular signal-regulated kinase but not extracellular signal-regulated kinase kinase through a 100-kDa phosphotyrosine phosphatase. J Biol Chem 278(9):7167-7179. doi: 10.1074/jbc.M203901200
9. Covaci A, Gerecke AC, Law RJ et al (2006) Hexabromocyclododecanes (HBCDs) in the environment and humans: a review. Environ Sci Technol 40(12):3679-3688
10. Dingemans MM, Heusinkveld HJ, de Groot A, Bergman A, van den Berg M, Westerink RH (2009) Hexabromocyclododecane inhibits depolarization-induced increase in intracellular calcium levels and neurotransmitter release in PC12 cells. Toxicol Sci 107(2):490-497. doi: 10.1093/toxsci/kfn249
11. Dorosh A, Ded L, Elzeinova F, Peknicova J (2011) Assessing oestrogenic effects of brominated flame retardants hexabromocyclododecane and tetrabromobisphenol A on MCF-7 cells. Folia Biol 57(1):35-39
12. Dufau ML, Liao M, Zhang Y (2010) Participation of signaling pathways in the derepression of luteinizing hormone receptor transcription. Mol Cell Endocrinol 314(2):221-227. doi: 10.1016/j.mce.2009.05.005
13. Ema M, Fujii S, Hirata-Koizumi M, Matsumoto M (2008) Two-generation reproductive toxicity study of the flame retardant hexabromocyclododecane in rats. Reprod Toxicol 25(3):335-351. doi: 10.1016/j.reprotox.2007.12.004
14. Fa S, Pogrmic-Majkic K, Dakic V et al (2013a) Acute effects of hexabromocyclododecane on Leydig cell cyclic nucleotide signaling and steroidogenesis in vitro. Toxicol Lett 218(1):81-90. doi: 10.1016/j.toxlet.2013. 01.009
15. Fa S, Pogrmic-Majkic K, Samardzija D et al (2013b) Involvement of ERK1/2 signaling pathway in atrazine action on FSH-stimulated LHR and CYP19A1 expression in rat granulosa cells. Toxicol Appl Pharmacol. doi: 10.1016/j.taap.2013.03.031
16. Fan HY, Liu Z, Shimada M et al (2009) MAPK3/1 (ERK1/2) in ovarian granulosa cells are essential for female fertility. Science 324(5929):938-941. doi: 10.1126/science.1171396
17. Fitzpatrick SL, Carlone DL, Robker RL, Richards JS (1997) Expression of aromatase in the ovary: down-regulation of mRNA by the ovulatory luteinizing hormone surge. Steroids 62(1):197-206
18. Gonzalez-Robayna IJ, Alliston TN, Buse P, Firestone GL, Richards JS (1999) Functional and subcellular changes in the A-kinase-signaling pathway: relation to aromatase and Sgk expression during the transition of granulosa cells to luteal cells. Mol Endocrinol 13(8):1318-1337. doi: 10.1210/me.13.8.1318
19. Hsieh M, Lee D, Panigone S et al (2007) Luteinizing hormone-dependent activation of the epidermal growth factor network is essential for ovulation. Mol Cell Biol 27(5):1914-1924. doi: 10.1128/MCB.01919-06
20. Hunzicker-Dunn ME, Lopez-Biladeau B, Law NC, Fiedler SE, Carr DW, Maizels ET (2012) PKA and GAB2 play central roles in the FSH signaling pathway to PI3K and AKT in ovarian granulosa cells. Proc Natl Acad Sci USA 109(44):E2979-E2988. doi: 10.1073/pnas.1205661109
21. Ibhazehiebo K, Iwasaki T, Xu M, Shimokawa N, Koibuchi N (2011) Brain-derived neurotrophic factor (BDNF) ameliorates the suppression of thyroid hormone-induced granule cell neurite extension by hexabromocyclododecane (HBCD). Neurosci Lett 493(1-2):1-7. doi: 10.1016/j.neulet.2011.01.062
22. Kayampilly PP, Menon KM (2009) Follicle-stimulating hormone inhibits adenosine 5′-monophosphate-activated protein kinase activation and promotes cell proliferation of primary granulosa cells in culture through an Akt-dependent pathway. Endocrinology 150(2):929-935. doi: 10.1210/en.2008-1032
23. Kwintkiewicz J, Giudice LC (2009) The interplay of insulin-like growth factors, gonadotropins, and endocrine disruptors in ovarian follicular development and function. Semin Reprod Med 27(1):43-51. doi: 10.1055/s-0028-1108009
24. Mariussen E, Fonnum F (2003) The effect of brominated flame retardants on neurotransmitter uptake into rat brain synaptosomes and vesicles. Neurochem Int 43(4-5):533-542
25. Mukherjee A, Park-Sarge OK, Mayo KE (1996) Gonadotropins induce rapid phosphorylation of the 3′,5′-cyclic adenosine monophosphate response element binding protein in ovarian granulosa cells. Endocrinology 137(8):3234-3245
26. Park JY, Su YQ, Ariga M, Law E, Jin SL, Conti M (2004) EGF-like growth factors as mediators of LH action in the ovulatory follicle. Science 303(5658):682-684. doi: 10.1126/science.10924631092463
27. Park MA, Hwang KA, Lee HR, Yi BR, Jeung EB, Choi KC (2012) Cell growth of BG-1 ovarian cancer cells is promoted by di-n-butyl phthalate and hexabromocyclododecane via upregulation of the cyclin D and cyclin-dependent kinase-4 genes. Mol Med Rep 5(3):761-766. doi: 10.3892/mmr.2011.712
28. Penov Gasi KM, Miljkovic DA, Medic Mijacevic LD et al (2003) Synthesis, X-ray crystal structures and biological activity of 16-amino-17-substituted-D- homo steroid derivatives. Steroids 68(7-8):667-676
29. Pogrmic K, Fa S, Dakic V, Kaisarevic S, Kovacevic R (2009) Atrazine oral exposure of peripubertal male rats downregulates steroidogenesis gene expression in Leydig cells. Toxicol Sci 111(1):189-197. doi: 10.1093/toxsci/kfp135
30. Robker RL, Richards JS (1998) Hormone-induced proliferation and differentiation of granulosa cells: a coordinated balance of the cell cycle regulators cyclin D2 and p27Kip1. Mol Endocrinol 12(7):924-940
31. Saegusa Y, Fujimoto H, Woo GH et al (2009) Developmental toxicity of brominated flame retardants, tetrabromobisphenol A and 1,2,5,6,9,10- hexabromocyclododecane, in rat offspring after maternal exposure from mid-gestation through lactation. Reprod Toxicol 28(4):456-467. doi: 10.1016/j.reprotox.2009.06.011
32. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9(7):671-675
33. Shimada M, Hernandez-Gonzalez I, Gonzalez-Robayna I, Richards JS (2006) Paracrine and autocrine regulation of epidermal growth factor-like factors in cumulus oocyte complexes and granulosa cells: key roles for prostaglandin synthase 2 and progesterone receptor. Mol Endocrinol 20(6):1352-1365. doi: 10.1210/me.2005-0504
34. Shkolnik K, Tadmor A, Ben-Dor S, Nevo N, Galiani D, Dekel N (2011) Reactive oxygen species are indispensable in ovulation. Proc Natl Acad Sci USA 108(4):1462-1467. doi: 10.1073/pnas.1017213108
35. Thomsen C, Molander P, Daae HL et al (2007) Occupational exposure to hexabromocyclododecane at an industrial plant. Environ Sci Technol 41(15):5210-5216
36. van der Ven LT, Verhoef A, van de Kuil T et al (2006) A 28-day oral dose toxicity study enhanced to detect endocrine effects of hexabromocyclododecane in Wistar rats. Toxicol Sci 94(2):281-292. doi: 10.1093/toxsci/kfl113
37. van der Ven LT, van de Kuil T, Leonards PE et al (2009) Endocrine effects of hexabromocyclododecane (HBCD) in a one-generation reproduction study in Wistar rats. Toxicol Lett 185(1):51-62. doi: 10.1016/j.toxlet.2008.12.003
38. Wayne CM, Fan HY, Cheng X, Richards JS (2007) Follicle-stimulating hormone induces multiple signaling cascades: evidence that activation of Rous sarcoma oncogene, RAS, and the epidermal growth factor receptor are critical for granulosa cell differentiation. Mol Endocrinol 21(8):1940-1957. doi: 10.1210/me.2007-0020
39. Williams AL, DeSesso JM (2010) The potential of selected brominated flame retardants to affect neurological development. J Toxicol Environ Health B 13(5):411-448. doi: 10.1080/10937401003751630
40. Zeleznik AJ, Saxena D, Little-Ihrig L (2003) Protein kinase B is obligatory for follicle-stimulating hormone-induced granulosa cell differentiation. Endocrinology 144(9):3985-3994. doi: 10.1210/en.2003-0293
41. Zhang X, Yang F, Xu C, Liu W, Wen S, Xu Y (2008) Cytotoxicity evaluation of three pairs of hexabromocyclododecane (HBCD) enantiomers on Hep G2 cell. Toxicol In Vitro 22(6):1520-1527. doi: 10.1016/j.tiv.2008.05.006