Liver X receptor alpha mediated genistein induction of human dehydroepiandrosterone sulfotransferase (hSULT2A1) in Hep G2 cells

Toxicology and Applied Pharmacology

Volumn 268, Issue 2, 2013, Pages 106-112

  Chen, Yue ^a   Zhang, Shunfen ^a   Zhou, Tianyan ^b   Huang, Chaoqun ^a   McLaughlin, Alicia ^a   Chen, Guangping ^a  

^a OKLAHOMA STATE UNIVERSITY   (United States)

^b PEKING UNIVERSITY HEALTH SCIENCE CENTER   (China)

Author keywords

Gene regulation; Genistein; Liver X receptor; Sulfotransferase; SULT2A1

Indexed keywords

ANDROSTERONE DERIVATIVE; GENISTEIN; LIVER X RECEPTOR ALPHA; LUCIFERASE; MESSENGER RNA; PHYTOESTROGEN; PRASTERONE SULFOTRANSFERASE; UNCLASSIFIED DRUG;

ARTICLE; CELL STRAIN CACO 2; CELL STRAIN HEPG2; CHROMATIN IMMUNOPRECIPITATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; ENZYME INDUCTION; GENE CONTROL; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PROMOTER REGION; PROTEIN FUNCTION; RECEPTOR BINDING; REPORTER GENE; RNA INTERFERENCE; WESTERN BLOTTING;

CHROMATIN IMMUNOPRECIPITATION; ENZYME INDUCTION; GENISTEIN; HEP G2 CELLS; HUMANS; HYDROCARBONS, FLUORINATED; ORPHAN NUCLEAR RECEPTORS; PROMOTER REGIONS, GENETIC; SULFONAMIDES; SULFOTRANSFERASES;

EID: 84875023712     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.01.006     Document Type: Article

References (66)

1. Adams S.M., Aksenova M.V., Aksenov M.Y., Mactutus C.F., Booze R.M. Soy isoflavones genistein and daidzein exert anti-apoptotic actions via a selective ER-mediated mechanism in neurons following HIV-1 Tat(1-86) exposure. PLoS One 2012, 7:e37540.
2. Allred C.D., Allred K.F., Ju Y.H., Goeppinger T.S., Doerge D.R., Helferich W.G. Soy processing influences growth of estrogen-dependent breast cancer tumors. Carcinogenesis 2004, 25:1649-1657.
3. Boyd K.E., Farnham P.J. Coexamination of site-specific transcription factor binding and promoter activity in living cells. Mol. Cell. Biol. 1999, 19:8393-8399.
4. Chawla A., Repa J.J., Evans R.M., Mangelsdorf D.J. Nuclear receptors and lipid physiology: opening the X-files. Science 2001, 294:1866-1870.
5. Chen X., Baker S.M., Chen G. Methotrexate induction of human sulfotransferases in Hep G2 and Caco-2 cells. J. Appl. Toxicol. 2005, 25:354-360.
6. Chen X., Maiti S., Zhang J., Chen G. Nuclear receptor interactions in methotrexate induction of human dehydroepiandrosterone sulfotransferase (hSULT2A1). J. Biochem. Mol. Toxicol. 2006, 20:309-317.
7. Chen W., Chen G., Head D.L., Mangelsdorf D.J., Russell D.W. Enzymatic reduction of oxysterols impairs LXR signaling in cultured cells and the livers of mice. Cell Metab. 2007, 5:73-79.
8. Chen X., Zhang J., Baker S.M., Chen G. Human constitutive androstane receptor mediated methotrexate induction of human dehydroepiandrosterone sulfotransferase (hSULT2A1). Toxicology 2007, 231:224-233.
9. Chen Y.-C., Nagpal M.L., Stocco D.M., Lin T. Effects of genistein, resveratrol, and quercetin on steroidogenesis and proliferation of MA-10 mouse Leydig tumor cells. J. Endocrinol. 2007, 192:527-537.
10. Chen Y., Huang C., Zhou T., Chen G. Genistein induction of human sulfotransferases in HepG2 and Caco-2 cells. Basic Clin. Pharmacol. Toxicol. 2008, 103:553-559.
11. Coughtrie M.W. Sulfation through the looking glass-recent advances in sulfotransferase research for the curious. Pharmacogenomics J. 2002, 2:297-308.
12. Dong D., Ako R., Wu B. Crystal structures of human sulfotransferases: insights into the mechanisms of action and substrate selectivity. Expert Opin. Drug Metab. Toxicol. 2012, 8:635-646.
13. Duanmu Z., Locke D., Smigelski J., Wu W., Dahn M.S., Falany C.N., Kocarek T.A., Runge-Morris M. Effects of dexamethasone on aryl (SULT1A1)- and hydroxysteroid (SULT2A1) -sulfotransferase gene expression in primary cultured human hepatocytes. Drug Metab. Dispos. 2002, 30:997-1004.
14. Duffel M.W., Marshal A.D., McPhie P., Sharma V., Jakoby W.B. Enzymatic aspects of the phenol (aryl) sulfotransferases. Drug Metab. Rev. 2001, 33:369-395.
15. Echchgadda I., Song C.S., Oh T.S., Cho S.H., Rivera O.J., Chatterjee B. Gene regulation for the senescence marker protein DHEA-sulfotransferase by the xenobiotic-activated nuclear pregnane X receptor (PXR). Mech. Ageing Dev. 2004, 125:733-745.
16. Echchgadda I., Song C.S., Oh T., Ahmed M., De La Cruz I.J., Chatterjee B. The xenobiotic-sensing nuclear receptors pregnane x receptor, constitutive androstane receptor, and orphan nuclear receptor hepatocyte nuclear factor 4{alpha} in the regulation of human steroid-/bile acid-sulfotransferase. Mol. Endocrinol. 2007, 21:2099-2111.
17. Echchgadda I., Song C.S., Oh T., Ahmed M., De La Cruz I.J., Chatterjee B. The xenobiotic-sensing nuclear receptors pregnane X receptor, constitutive androstane receptor, and orphan nuclear receptor hepatocyte nuclear factor 4alpha in the regulation of human steroid-/bile acid-sulfotransferase. Mol. Endocrinol. 2007, 21:2099-2111.
18. Falany C.N., Wilborn T.W. Biochemistry of cytosolic sulfotransferases involved in bioactivation. Adv. Pharmacol. 1994, 27:301-329.
19. Ferraris M., Flora A., Chiesara E., Fornasari D., Lucchetti H., Marabini L., Frigerio S., Radice S. Molecular mechanism of the aryl hydrocarbon receptor activation by the fungicide iprodione in rainbow trout (Oncorhynchus mykiss) hepatocytes. Aquat. Toxicol. 2005, 72:209-220.
20. Galijatovic A., Otake Y., Walle U.K., Walle T. Extensive metabolism of the flavonoid chrysin by human Caco-2 and Hep G2 cells. Xenobiotica 1999, 29:1241-1256.
21. Gamage N., Barnett A., Hempel N., Duggleby R.G., Windmill K.F., Martin J.L., McManus M.E. Human sulfotransferases and their role in chemical metabolism. Toxicol. Sci. 2006, 90:5-22.
22. Gong H., Guo P., Zhai Y., Zhou J., Uppal H., Jarzynka M.J., Song W.C., Cheng S.Y., Xie W. Estrogen deprivation and inhibition of breast cancer growth in vivo through activation of the orphan nuclear receptor liver X receptor. Mol. Endocrinol. 2007, 21:1781-1790.
23. Han E.H., Kim J.Y., Jeong H.G. Effect of biochanin A on the aryl hydrocarbon receptor and cytochrome P450 1A1 in MCF-7 human breast carcinoma cells. Arch. Pharm. Res. 2006, 29:570-576.
24. Hengstler J.G., Arand M., Herrero M.E., Oesch F. Polymorphisms of N-acetyltransferases, glutathione S-transferases, microsomal epoxide hydrolase and sulfotransferases: influence of cancer susceptibility. Recent Results Cancer Res. 1998, 154:47-85.
25. Huang Y.H., Lee C.Y., Tai P.J., Yen C.C., Liao C.Y., Chen W.J., Liao C.J., Cheng W.L., Chen R.N., Wu S.M., Wang C.S., Lin K.H. Indirect regulation of human dehydroepiandrosterone sulfotransferase family 1A member 2 by thyroid hormones. Endocrinology 2006, 147:2481-2489.
26. Huang C., Zhou T., Chen Y., Sun T., Zhang S., Chen G. Estrogen-related receptor ERRalpha-mediated downregulation of human hydroxysteroid sulfotransferase (SULT2A1) in Hep G2 cells. Chem. Biol. Interact. 2011, 192:264-271.
27. Ishimi Y., Yoshida M., Wakimoto S., Wu J., Chiba H., Wang X., Takeda K., Miyaura C. Genistein, a soybean isoflavone, affects bone marrow lymphopoiesis and prevents bone loss in castrated male mice. Bone 2002, 31:180-185.
28. Jacobs M.N., Lewis D.F. Steroid hormone receptors and dietary ligands: a selected review. Proc. Nutr. Soc. 2002, 61:105-122.
29. Kirk E., Sutherland P., Wang S.A., Chait A., LeBoeuf R.C. Dietary isoflavones reduce plasma cholesterol and atherosclerosis in C57BL/6 mice but not LDL receptor-deficient mice. J. Nutr. 1998, 128:954-959.
30. Klaassen C.D., Boles J.W. Sulfation and sulfotransferases 5: the importance of 3'-phosphoadenosine 5'-phosphosulfate (PAPS) in the regulation of sulfation. FASEB J. 1997, 11:404-418.
31. Klein C.B., King A.A. Genistein genotoxicity: critical considerations of in vitro exposure dose. Toxicol. Appl. Pharmacol. 2007, 224:1-11.
32. Kousidou O., Tzanakakis G.N., Karamanos N.K. Effects of the natural isoflavonoid genistein on growth, signaling pathways and gene expression of matrix macromolecules by breast cancer cells. Mini Rev. Med. Chem. 2006, 6:331-337.
33. Lee J.H., Gong H., Khadem S., Lu Y., Gao X., Li S., Zhang J., Xie W. Androgen deprivation by activating the liver X receptor. Endocrinology 2008, 149:3778-3788.
34. Maiti S., Chen G. Methotrexate is a novel inducer of rat liver and intestinal sulfotransferases. Arch. Biochem. Biophys. 2003, 418:161-168.
35. Maiti S., Chen X., Chen G. All-trans retinoic acid induction of sulfotransferases. Basic Clin. Pharmacol. Toxicol. 2005, 96:44-53.
36. Maubach J., Bracke M.E., Heyerick A., Depypere H.T., Serreyn R.F., Mareel M.M., De Keukeleire D. Quantitatiion of soy-derived phytoestrogens in human breast tissue and biological fluids by high-performance liquid chromatography. J. Chromatogr. B Biomed. Sci. Appl. 2003, 784:137-144.
37. Mezei O., Chou C.N., Kennedy K.J., Tovar-Palacio C., Shay N.F. Hepatic cytochrome p450-2A and phosphoribosylpyrophosphate synthetase-associated protein mRNA are induced in gerbils after consumption of isoflavone-containing protein. J. Nutr. 2002, 132:2538-2544.
38. Mezei O., Banz W.J., Steger R.W., Peluso M.R., Winters T.A., Shay N. Soy isoflavones exert antidiabetic and hypolipidemic effects through the PPAR pathways in obese Zucker rats and murine RAW 264.7 cells. J. Nutr. 2003, 133:1238-1243.
39. Miodini P., Fioravanti L., Di Fronzo G., Cappelletti V. The two phyto-oestrogens genistein and quercetin exert different effects on oestrogen receptor function. Br. J. Cancer 1999, 80:1150-1155.
40. Mitchell J.H., Duthie S.J., Collins A.R. Effects of phytoestrogens on growth and DNA integrity in human prostate tumor cell lines: PC-3 and LNCaP. Nutr. Cancer 2000, 38:223-228.
41. Mitchell J.H., Duthie S.J., et al. Effects of phytoestrogens on growth and DNA integrity in human prostate tumor cell lines: PC-3 and LNCaP. Nutr. Cancer 2000, 38:223-228.
42. Nakajima D., Kim C.S., Oh T.W., Yang C.Y., Naka T., Igawa S., Ohta F. Suppressive effects of genistein dosage and resistance exercise on bone loss in ovariectomized rats. J. Physiol. Anthropol. Appl. Human Sci. 2001, 20:285-291.
43. Otterness D.M., Her C., Aksoy S., Kimura S., Wieben E.D., Weinshilboum R.M. Human dehydroepiandrosterone sulfotransferase gene: molecular cloning and structural characterization. DNA Cell Biol. 1995, 14:331-341.
44. Otterness D.M., Her C., Aksoy S., Kimura S., Wieben E.D., Weinshilboum R.M. Human dehydroepiandrosterone sulfotransferase gene: molecular cloning and structural characterization. DNA Cell Biol. 1995, 14:331-341.
45. Paik M., Lee H.O., Chung H.S., Yang S.O., Kim J.H., Om A.S. Genistein may prevent cadmium-induced bone loss in ovariectomized rats. J. Med. Food 2003, 6:337-343.
46. Repa J.J., Mangelsdorf D.J. The liver X receptor gene team: potential new players in atheosclerosis. Nat. Med. 2002, 8:1243-1248.
47. Ricketts M.L., Moore D.D., Banz W.J., Mezei O., Shay N.F. Molecular mechanisms of action of the soy isoflavones includes activation of promiscuous nuclear receptors. A review. J. Nutr. Biochem. 2005, 16:321-330.
48. Runge-Morris M., Kocarek T.A. Regulation of sulfotransferases by xenobiotic receptors. Curr. Drug Metab. 2005, 6:299-307.
49. Safford B., Dickens A., Halleron N., Briggs D., Carthew P., Baker V. A model to estimate the oestrogen receptor mediated effects from exposure to soy isoflavones in food. Regul. Toxicol. Pharmacol. 2003, 38:196-209.
50. Scatena R., Martorana G.E., Bottoni P., Giardina B. Mitochondrial dysfunction by synthetic ligands of peroxisome proliferator activated receptors (PPARs). IUBMB Life 2004, 56:477-482.
51. Seo Y.K., Chung Y.T., Kim S., Echchgadda I., Song C.S., Chatterjee B. Xenobiotic- and vitamin D-responsive induction of the steroid/bile acid-sulfotransferase Sult2A1 in young and old mice: the role of a gene enhancer in the liver chromatin. Gene 2007, 386:218-223.
52. Setchell K.D., Cassidy A. Dietary isoflavones: biological effects and relevance to human health. J. Nutr. 1999, 129:758-767.
53. Shwed J.A., Walle U.K., Walle T. Hep G2 cell line as a human model for sulphate conjugation of drugs. Xenobiotica 1992, 22:973-982.
54. Song W.C. Biochemistry and reproductive endocrinology of estrogen sulfotransferase. Ann. N. Y. Acad. Sci. 2001, 948:43-50.
55. Song C.S., Jung M.H., Kim S.C., Hassan T., Roy A.K., Chatterjee B. Tissue-specific and androgen-repressible regulation of the rat dehydroepiandrosterone sulfotransferase gene promoter. J. Biol. Chem. 1998, 273:21856-21866.
56. Song C.S., Echchgadda I., Baek B.S., Ahn S.C., Oh T., Roy A.K., Chatterjee B. Dehydroepiandrosterone sulfotransferase gene induction by bile acid activated farnesoid x receptor. J. Biol. Chem. 2001, 276:42549-42556.
57. Song C.S., Echchgadda I., Seo Y.K., Oh T., Kim S., Kim S.A., Cho S., Shi L., Chatterjee B. An essential role of the CAAT/enhancer binding protein-alpha in the vitamin D-induced expression of the human steroid/bile acid-sulfotransferase (SULT2A1). Mol. Endocrinol. 2006, 20:795-808.
58. Sonoda J., Xie W., Rosenfeld J.M., Barwick J.L., Guzelian P.S., Evans R.M. Regulation of a xenobiotic sulfonation cascade by nuclear pregnane X receptor (PXR). Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13801-13806.
59. Suetsugi M., Su L., Karlsberg K., Yuan Y.C., Chen S. Flavone and isoflavone phytoestrogens are agonists of estrogen-related receptors. Mol. Cancer Res. 2003, 1:981-991.
60. Suzuki T., Miki Y., Nakamura Y., Ito K., Sasano H. Steroid sulfatase and estrogen sulfotransferase in human carcinomas. Mol. Cell. Endocrinol. 2011, 340:148-153.
61. Uppal H., Saini S.P., Moschetta A., Mu Y., Zhou J., Gong H., Zhai Y., Ren S., Michalopoulos G.K., Mangelsdorf D.J., Xie W. Activation of LXRs prevents bile acid toxicity and cholestasis in female mice. Hepatology 2007, 45:422-432.
62. Wilson A.A., Wang J., Koch P., Walle T. Stereoselective sulphate conjugation of fenoterol by human phenolsulphotransferases. Xenobiotica 1997, 27:1147-1154.
63. Wiseman H., Casey K., Bowey E.A., Duffy R., Davies M., Rowland I.R., Lloyd A.S., Murray A., Thompson R., Clarke D.B. Influence of 10 wk soy consumption on plasma concentrations and excretion of isoflavonoids and on gut microflora in healthy adults. Am. J. Clin. Nutr. 2004, 80:692-699.
64. Xiang H., Schevzov G., et al. A comparative study of growth-inhibitory effects of isoflavones and their metabolites on human breast and prostate cancer cell lines. Nutr. Cancer 2002, 42:224-232.
65. Xiao L., Xie X., Zhai Y. Functional crosstalk of CAR-LXR and ROR-LXR in drug metabolism and lipid metabolism. Adv. Drug Deliv. Rev. 2010, 62:1316-1321.
66. Yongfeng Shang X.H., DiRenzo James, Lazar Mitchell A., Brown Myles Cofactor dynamics and sufficiency in estrogen receptor-regulated transcription. Cell 2000, 103:843-852.