Distinct roles for Aryl hydrocarbon receptor nuclear translocator and Ah receptor in estrogen-mediated signaling in human cancer cell lines

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Labrecque, Mark P ^b   Takhar, Mandeep K ^b   Hollingshead, Brett D ^a   Prefontaine, Gratien G ^b   Perdew, Gary H ^a   Beischlag, Timothy V ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b SIMON FRASER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 3',4' DIMETHOXY ALPHA NAPHTHOFLAVONE; ALPHA NAPHTHOFLAVONE; AROMATIC HYDROCARBON RECEPTOR; CATHEPSIN D; ESTROGEN; ESTROGEN RECEPTOR ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; PROTEIN PS2; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; MESSENGER RNA;

ARTICLE; CANCER CELL; CELL PROLIFERATION; CELL STRAIN MCF 7; CONTROLLED STUDY; DOWN REGULATION; ECC 1 CELL; GENE REPRESSION; HUMAN; HUMAN CELL; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; UPREGULATION; DRUG EFFECT; GENE SILENCING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PHENOTYPE; TUMOR CELL LINE;

ARYL HYDROCARBON RECEPTOR NUCLEAR TRANSLOCATOR; CELL LINE, TUMOR; CELL PROLIFERATION; ESTROGEN RECEPTOR ALPHA; ESTROGENS; GENE KNOCKDOWN TECHNIQUES; HUMANS; PHENOTYPE; RECEPTORS, ARYL HYDROCARBON; RNA, MESSENGER; SIGNAL TRANSDUCTION; TETRACHLORODIBENZODIOXIN; TRANSCRIPTION, GENETIC;

EID: 84855301572     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0029545     Document Type: Article

References (48)

1. Hankinson O, (1995) The aryl hydrocarbon receptor complex. Annu Rev Pharmacol Toxicol 35: 307-340.
2. Elizondo G, Fernandez-Salguero P, Sheikh MS, Kim GY, Fornace AJ, et al. (2000) Altered cell cycle control at the G(2)/M phases in aryl hydrocarbon receptor-null embryo fibroblast. Mol Pharmacol 57: 1056-1063.
3. Fernandez-Salguero P, Pineau T, Hilbert DM, McPhail T, Lee SS, et al. (1995) Immune system impairment and hepatic fibrosis in mice lacking the dioxin-binding Ah receptor. Science 268: 722-726.
4. Alexander DL, Ganem LG, Fernandez-Salguero P, Gonzalez F, Jefcoate CR, (1998) Aryl-hydrocarbon receptor is an inhibitory regulator of lipid synthesis and of commitment to adipogenesis. J Cell Sci 111 (Pt 22): 3311-3322.
5. Kimura A, Naka T, Nohara K, Fujii-Kuriyama Y, Kishimoto T, (2008) Aryl hydrocarbon receptor regulates Stat1 activation and participates in the development of Th17 cells. Proc Natl Acad Sci U S A 105: 9721-9726.
6. Hollingshead BD, Beischlag TV, Dinatale BC, Ramadoss P, Perdew GH, (2008) Inflammatory signaling and aryl hydrocarbon receptor mediate synergistic induction of interleukin 6 in MCF-7 cells. Cancer Res 68: 3609-3617.
7. Carver LA, Bradfield CA, (1997) Ligand-dependent interaction of the aryl hydrocarbon receptor with a novel immunophilin homolog in vivo. J Biol Chem 272: 11452-11456.
8. Kazlauskas A, Poellinger L, Pongratz I, (1999) Evidence that the co-chaperone p23 regulates ligand responsiveness of the dioxin (Aryl hydrocarbon) receptor. J Biol Chem 274: 13519-13524.
9. Ma Q, Whitlock JP Jr, (1997) A novel cytoplasmic protein that interacts with the Ah receptor, contains tetratricopeptide repeat motifs, and augments the transcriptional response to 2,3,7,8-tetrachlorodibenzo-p-dioxin. J Biol Chem 272: 8878-8884.
10. Pongratz I, Mason GG, Poellinger L, (1992) Dual roles of the 90-kDa heat shock protein hsp90 in modulating functional activities of the dioxin receptor. Evidence that the dioxin receptor functionally belongs to a subclass of nuclear receptors which require hsp90 both for ligand binding activity and repression of intrinsic DNA binding activity. J Biol Chem 267: 13728-13734.
11. Beischlag TV, Perdew GH, (2005) ER alpha-AHR-ARNT protein-protein interactions mediate estradiol-dependent transrepression of dioxin-inducible gene transcription. J Biol Chem 280: 21607-21611.
12. Beischlag TV, Wang S, Rose DW, Torchia J, Reisz-Porszasz S, et al. (2002) Recruitment of the NCoA/SRC-1/p160 family of transcriptional coactivators by the aryl hydrocarbon receptor/aryl hydrocarbon receptor nuclear translocator complex. Mol Cell Biol 22: 4319-4333.
13. Kumar MB, Perdew GH, (1999) Nuclear receptor coactivator SRC-1 interacts with the Q-rich subdomain of the AhR and modulates its transactivation potential. Gene Expr 8: 273-286.
14. Kim JH, Stallcup MR, (2004) Role of the coiled-coil coactivator (CoCoA) in aryl hydrocarbon receptor-mediated transcription. J Biol Chem 279: 49842-49848.
15. Chen YH, Beischlag TV, Kim JH, Perdew GH, Stallcup MR, (2006) Role of GAC63 in transcriptional activation mediated by the aryl hydrocarbon receptor. J Biol Chem 281: 12242-12247.
16. Kollara A, Brown TJ, (2006) Functional interaction of nuclear receptor coactivator 4 with aryl hydrocarbon receptor. Biochem Biophys Res Commun 346: 526-534.
17. Beischlag TV, Taylor RT, Rose DW, Yoon D, Chen Y, et al. (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.
18. Beischlag TV, Luis Morales J, Hollingshead BD, Perdew GH, (2008) The aryl hydrocarbon receptor complex and the control of gene expression. Crit Rev Eukaryot Gene Expr 18: 207-250.
19. Matthews J, Wihlen B, Thomsen J, Gustafsson JA, (2005) Aryl Hydrocarbon Receptor-Mediated Transcription: Ligand-Dependent Recruitment of Estrogen Receptor α to 2,3,7,8-Tetrachlorodibenzo- p-Dioxin-Responsive Promoters. Mol Cell Biol 25: 5317-5328.
20. Ohtake F, Takeyama K, Matsumoto T, Kitagawa H, Yamamoto Y, et al. (2003) Modulation of oestrogen receptor signalling by association with the activated dioxin receptor. Nature 423: 545-550.
21. Tian Y, Ke S, Denison MS, Rabson AB, Gallo MA, (1999) Ah receptor and NF-kappaB interactions, a potential mechanism for dioxin toxicity. J Biol Chem 274: 510-515.
22. Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, et al. (1995) The nuclear receptor superfamily: the second decade. Cell 83: 835-839.
23. Acconcia F, Kumar R, (2006) Signaling regulation of genomic and nongenomic functions of estrogen receptors. Cancer Lett 238: 1-14.
24. Biegel L, Safe S, (1990) Effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) on cell growth and the secretion of the estrogen-induced 34-, 52- and 160-kDa proteins in human breast cancer cells. J Steroid Biochem Mol Biol 37: 725-732.
25. Kharat I, Saatcioglu F, (1996) Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor. Cross-talk between aryl hydrocarbon- and estrogen-mediated signaling. J Biol Chem 271: 10533-10537.
26. Zacharewski TR, Bondy KL, McDonell P, Wu ZF, (1994) Antiestrogenic effect of 2,3,7,8-tetrachlorodibenzo-p-dioxin on 17 beta-estradiol-induced pS2 expression. Cancer Res 54: 2707-2713.
27. Ruegg J, Swedenborg E, Wahlstrom D, Escande A, Balaguer P, et al. (2008) The transcription factor aryl hydrocarbon receptor nuclear translocator functions as an estrogen receptor beta-selective coactivator, and its recruitment to alternative pathways mediates antiestrogenic effects of dioxin. Mol Endocrinol 22: 304-316.
28. Safe S, Wormke M, Samudio I, (2000) Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J Mammary Gland Biol Neoplasia 5: 295-306.
29. Ohtake F, Baba A, Takada I, Okada M, Iwasaki K, et al. (2007) Dioxin receptor is a ligand-dependent E3 ubiquitin ligase. Nature 446: 562-566.
30. Brunnberg S, Pettersson K, Rydin E, Matthews J, Hanberg A, et al. (2003) The basic helix-loop-helix-PAS protein ARNT functions as a potent coactivator of estrogen receptor-dependent transcription. Proc Natl Acad Sci U S A 100: 6517-6522.
31. Castro-Rivera E, Wormke M, Safe S, (1999) Estrogen and aryl hydrocarbon responsiveness of ECC-1 endometrial cancer cells. Mol Cell Endocrinol 150: 11-21.
32. Ricci MS, Toscano DG, Toscano WA Jr, (1999) ECC-1 human endometrial cells as a model system to study dioxin disruption of steroid hormone function. In Vitro Cell Dev Biol Anim 35: 183-189.
33. Murray IA, Krishnegowda G, DiNatale BC, Flaveny C, Chiaro C, et al. (2010) Development of a selective modulator of aryl hydrocarbon (Ah) receptor activity that exhibits anti-inflammatory properties. Chem Res Toxicol 23: 955-966.
34. Murray IA, Flaveny CA, Chiaro CR, Sharma AK, Tanos RS, et al. (2011) Suppression of cytokine-mediated complement factor gene expression through selective activation of the Ah receptor with 3′,4′-dimethoxy-alpha-naphthoflavone. Mol Pharmacol 79: 508-519.
35. Vendrell JA, Magnino F, Danis E, Duchesne MJ, Pinloche S, et al. (2004) Estrogen regulation in human breast cancer cells of new downstream gene targets involved in estrogen metabolism, cell proliferation and cell transformation. J Mol Endocrinol 32: 397-414.
36. Astroff B, Rowlands C, Dickerson R, Safe S, (1990) 2,3,7,8-Tetrachlorodibenzo-p-dioxin inhibition of 17 beta-estradiol-induced increases in rat uterine epidermal growth factor receptor binding activity and gene expression. Mol Cell Endocrinol 72: 247-252.
37. Astroff B, Safe S, (1988) Comparative antiestrogenic activities of 2,3,7,8-tetrachlorodibenzo-p-dioxin and 6-methyl-1,3,8-trichlorodibenzofuran in the female rat. Toxicol Appl Pharmacol 95: 435-443.
38. Gallo MA, Hesse EJ, Macdonald GJ, Umbreit TH, (1986) Interactive effects of estradiol and 2,3,7,8-tetrachlorodibenzo-p-dioxin on hepatic cytochrome P-450 and mouse uterus. Toxicol Lett 32: 123-132.
39. Hoffman EC, Reyes H, Chu FF, Sander F, Conley LH, et al. (1991) Cloning of a factor required for activity of the Ah (dioxin) receptor. Science 252: 954-958.
40. Reyes H, Reisz-Porszasz S, Hankinson O, (1992) Identification of the Ah receptor nuclear translocator protein (Arnt) as a component of the DNA binding form of the Ah receptor. Science 256: 1193-1195.
41. Partch CL, Gardner KH, (2011) Coactivators necessary for transcriptional output of the hypoxia inducible factor, HIF, are directly recruited by ARNT PAS-B. Proc Natl Acad Sci U S A 108: 7739-7744.
42. Nguyen TA, Hoivik D, Lee JE, Safe S, (1999) Interactions of nuclear receptor coactivator/corepressor proteins with the aryl hydrocarbon receptor complex. Arch Biochem Biophys 367: 250-257.
43. Partch CL, Card PB, Amezcua CA, Gardner KH, (2009) Molecular basis of coiled coil coactivator recruitment by the aryl hydrocarbon receptor nuclear translocator (ARNT). J Biol Chem 284: 15184-15192.
44. Arany Z, Huang LE, Eckner R, Bhattacharya S, Jiang C, et al. (1996) An essential role for p300/CBP in the cellular response to hypoxia. Proc Natl Acad Sci U S A 93: 12969-12973.
45. Boitano AE, Wang J, Romeo R, Bouchez LC, Parker AE, et al. (2010) Aryl hydrocarbon receptor antagonists promote the expansion of human hematopoietic stem cells. Science 329: 1345-1348.
46. Perdew GH, Hollingshead BD, Dinatale BC, Morales JL, Labrecque MP, et al. (2010) Estrogen receptor expression is required for low-dose resveratrol-mediated repression of aryl hydrocarbon receptor activity. J Pharmacol Exp Ther 335: 273-283.
47. DiNatale BC, Schroeder JC, Francey LJ, Kusnadi A, Perdew GH, (2010) Mechanistic insights into the events that lead to synergistic induction of interleukin 6 transcription upon activation of the aryl hydrocarbon receptor and inflammatory signaling. J Biol Chem 285: 24388-24397.
48. Hestermann EV, Brown M, (2003) Agonist and chemopreventative ligands induce differential transcriptional cofactor recruitment by aryl hydrocarbon receptor. Mol Cell Biol 23: 7920-7925.