Differential and directional estrogenic signaling pathways induced by enterolignans and their precursors

PLoS ONE

Volumn 12, Issue 2, 2017, Pages

  Zhu, Yun ^a,b   Kawaguchi, Kayoko ^a   Kiyama, Ryoiti ^a  

^a NATIONAL INSTITUTE OF ADVANCED INDUSTRIAL SCIENCE AND TECHNOLOGY AIST   (Japan)

^b Scinet Company   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; ENTERODIOL; ENTEROLACTONE; ESTRADIOL; FULVESTRANT; MATAIRESINOL; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHATIDYLINOSITOL 3 KINASE; PINORESINOL; PROTEIN KINASE B; SESAMIN; 1,3 DIOXOLANE DERIVATIVE; 2,3-BIS(3'-HYDROXYBENZYL)BUTANE-1,4-DIOL; 2,3-BIS(3'-HYDROXYBENZYL)BUTYROLACTONE; ESTROGEN; FURAN DERIVATIVE; GAMMA BUTYROLACTONE; LIGNAN;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BREAST CANCER CELL LINE; CELL CYCLE PROGRESSION; CELL PROLIFERATION; CELL TRANSPORT; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG MECHANISM; ENZYME ACTIVATION; ESTROGEN ACTIVITY; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; CELL CYCLE; DNA MICROARRAY; DRUG EFFECTS; MCF-7 CELL LINE; METABOLISM;

4-BUTYROLACTONE; CELL CYCLE; DIOXOLES; ESTROGENS; FURANS; GENE EXPRESSION PROFILING; HUMANS; LIGNANS; MCF-7 CELLS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION;

EID: 85011376163     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0171390     Document Type: Article

References (48)

1. Raffaelli B, Hoikkala A, Leppala E, Wahala K. Enterolignans. J Chromatogr B Analyt Technol Biomed Life Sci. 2002; 777(1-2):29-43. PMID: 12270198.
2. Lampe JW, Atkinson C, Hullar MA. Assessing exposure to lignans and their metabolites in humans. J AOAC Int. 2006; 89(4):1174-1181. PMID: 16915861.
3. Clavel T, Dore J, Blaut M. Bioavailability of lignans in human subjects. Nutr Res Rev. 2006; 19(2):187- 196. doi:10.1017/S0954422407249704 PMID: 19079885.
4. Wang LQ. Mammalian phytoestrogens: Enterodiol and enterolactone. J Chromatogr B Analyt Technol Biomed Life Sci. 2002; 777(1-2):289-309. PMID: 12270221.
5. Adlercreutz H. Lignans and human health. Crit Rev Clin Lab Sci. 2007; 44(5-6):483-525. doi:10.1080/10408360701612942 PMID: 17943494.
6. Sonestedt E, Wirfalt E. Enterolactone and breast cancer: Methodological issues may contribute to conflicting results in observational studies. Nutr Res. 2010; 30(10):667-77. doi:10.1016/j.nutres.2010.09.010 PMID: 21056282.
7. Saarinen NM, Warri A, Airio M, Smeds A, Makela S. Role of dietary lignans in the reduction of breast cancer risk. Mol Nutr Food Res. 2007; 51(7):857-866. doi:10.1002/mnfr.200600240 PMID: 17576639.
8. Dar AA, Arumugam N. Lignans of sesame: purification methods, biological activities and biosynthesis a review. Bioorg Chem. 2013; 50:1-10. doi:10.1016/j.bioorg.2013.06.009 PMID: 23933354.
9. Deroo BJ, Korach KS. Estrogen receptors and human disease. J Clin Invest. 2006; 116(3):561-570. doi:10.1172/JCI27987PMID: 16511588.
10. Kiyama R, Wada-Kiyama Y. Estrogenic endocrine disruptors: Molecular mechanisms of action. Environ Int. 2015; 83:11-40. doi:10.1016/j.envint.2015.05.012 PMID: 26073844.
11. Kiyama R, Zhu Y. DNA microarray-based gene expression profiling of estrogenic chemicals. Cell Mol Life Sci. 2014; 71(11):2065-2082. doi:10.1007/s00018-013-1544-5 PMID: 24399289.
12. Kiyama R. Biological effects induced by estrogenic activity of lignans. Trends Food Sci Tech. 2016; 54:186-196.
13. Welshons WV, Murphy CS, Koch R, Calaf G, Jordan VC. Stimulation of breast cancer cells in vitro by the environmental estrogen enterolactone and the phytoestrogen equol. Breast Cancer Res Treat. 1987; 10(2):169-175. PMID: 3427225.
14. Mousavi Y, Adlercreutz H. Enterolactone and estradiol inhibit each other's proliferative effect on MCF-7 breast cancer cells in culture. J Steroid Biochem Mol Biol. 1992; 41(3-8):615-619. PMID: 1562532.
15. Sathyamoorthy N, Wang TT, Phang JM. Stimulation of pS2 expression by diet-derived compounds. Cancer Res. 1994; 54(4):957-961. PMID: 8313386.
16. Aehle E, Muller U, Eklund PC, Willfor SM, Sippl W, Drager B. Lignans as food constituents with estrogen and antiestrogen activity. Phytochemistry. 2011; 72(18):2396-2405. doi:10.1016/j.phytochem.2011.08.013 PMID: 21889775.
17. Jin JS, Lee JH, Hattori M. Ligand binding affinities of arctigenin and its demethylated metabolites to estrogen receptor alpha. Molecules. 2013; 18(1):1122-1127. doi:10.3390/molecules18011122 PMID: 23325100.
18. Dong S, Furutani Y, Suto Y, Furutani M, Zhu Y, Yoneyama M, et al. Estrogen-like activity and dual roles in cell signaling of an Agaricus blazei Murrill mycelia-dikaryon extract. Microbiol Res. 2012; 167 (4):231-237. doi:10.1016/j.micres.2011.09.003 PMID: 22015258.
19. Dong S, Furutani Y, Kimura S, Zhu Y, Kawabata K, Furutani M, et al. Brefeldin A is an estrogenic, Erk1/2-Activating component in the extract of Agaricus blazei mycelia. J Agric Food Chem. 2013; 61(1):128- 136. doi:10.1021/jf304546a PMID: 23215459.
20. Terasaka S, Aita Y, Inoue A, Hayashi S, Nishigaki M, Aoyagi K, et al. Using a customized DNA microarray for expression profiling of the estrogen-responsive genes to evaluate estrogen activity among natural estrogens and industrial chemicals. Environ Health Perspect. 2004; 112(7):773-781. PMID: 15159206.
21. Inoue A, Seino Y, Terasaka S, Hayashi S, Yamori T, Tanji M, et al. Comparative profiling of the gene expression for estrogen responsiveness in cultured human cell lines. Toxicol In Vitro. 2007; 21(4):741- 752. doi:10.1016/j.tiv.2007.01.014 PMID: 17369015.
22. Kiyama R, Zhu Y, Kawaguchi K, Iitake N, Wada-Kiyama Y, Dong S. Estrogen-responsive genes for environmental studies. Environ Technol Innov. 2014; 1-2, 16-28.
23. Foster JS, Henley DC, Ahamed S, Wimalasena J. Estrogens and cell-cycle regulation in breast cancer. Trends Endocrinol Metab. 2001; 12(7):320-327. PMID: 11504672.
24. Arnold A, Papanikolaou A. Cyclin D1 in breast cancer pathogenesis. J Clin Oncol. 2005; 23(18):4215- 4224. doi:10.1200/JCO.2005.05.064 PMID: 15961768.
25. Prall OW, Sarcevic B, Musgrove EA, Watts CK, Sutherland RL. Estrogen-induced activation of Cdk4 and Cdk2 during G1-S phase progression is accompanied by increased cyclin D1 expression and decreased cyclin-dependent kinase inhibitor association with cyclin E-Cdk2. J Biol Chem. 1997; 272 (16):10882-10894. PMID: 9099745.
26. Skildum AJ, Mukherjee S, Conrad SE. The cyclin-dependent kinase inhibitor p21WAF1/Cip1 is an antiestrogen- regulated inhibitor of Cdk4 in human breast cancer cells. J Biol Chem. 2002; 277(7):5145- 5152. doi:10.1074/jbc.M109179200 PMID: 11741909.
27. Martynowicz H, Janus A, Nowacki D, Mazur G. The role of chemokines in hypertension. Adv Clin Exp Med. 2014; 23(3):319-325. PMID: 24979502.
28. Li S, Lu J, Chen Y, Xiong N, Li L, Zhang J, et al. MCP-1-induced ERK/GSK-3β/Snail signaling facilitates the epithelial-mesenchymal transition and promotes the migration of MCF-7 human breast carcinoma cells. Cell Mol Immunol. 2016; in press.
29. Peñalvo JL, LoÂpez-Romero P. Urinary enterolignan concentrations are positively associated with serum HDL cholesterol and negatively associated with serum triglycerides in U.S. adults. J Nutr. 2012; 142 (4):751-756. doi:10.3945/jn.111.150516 PMID: 22378329.
30. Reger MK, Zollinger TW, Liu Z, Jones J, Zhang J. Urinary phytoestrogens and cancer, cardiovascular, and all-cause mortality in the continuous National Health and Nutrition Examination Survey. Eur J Nutr. 2016; 55(3):1029-1040. doi:10.1007/s00394-015-0917-y PMID: 25943648.
31. Frankenfeld CL. Cardiometabolic risk factors are associated with high urinary enterolactone concentration, independent of urinary enterodiol concentration and dietary fiber intake in adults. J Nutr. 2014; 144 (9):1445-1453. doi:10.3945/jn.114.190512 PMID: 24966407.
32. Azrad M, Vollmer RT, Madden J, Dewhirst M, Polascik TJ, Snyder DC, et al. Flaxseed-derived enterolactone is inversely associated with tumor cell proliferation in men with localized prostate cancer. J Med Food. 2013; 16(4):357-360. doi:10.1089/jmf.2012.0159 PMID: 23566060.
33. Touillaud MS, ThieÂbaut AC, Fournier A, Niravong M, Boutron-Ruault MC, Clavel-Chapelon F. Dietary lignan intake and postmenopausal breast cancer risk by estrogen and progesterone receptor status. J Natl Cancer Inst. 2007; 99(6):475-486. doi:10.1093/jnci/djk096 PMID: 17374837.
34. Buck K, Zaineddin AK, Vrieling A, Linseisen J, Chang-Claude J. Meta-Analyses of lignans and enterolignans in relation to breast cancer risk. Am J Clin Nutr. 2010; 92(1):141-153. doi:10.3945/ajcn.2009.28573 PMID: 20463043.
35. Buck K, Vrieling A, Zaineddin AK, Becker S, Husing A, Kaaks R, et al. Serum enterolactone and prognosis of postmenopausal breast cancer. J Clin Oncol. 2011; 29(28):3730-3738. doi:10.1200/JCO.2011.34.6478 PMID: 21900115.
36. Mabrok HB, Klopfleisch R, Ghanem KZ, Clavel T, Blaut M, Loh G. Lignan transformation by gut bacteria lowers tumor burden in a gnotobiotic rat model of breast cancer. Carcinogenesis. 2012; 33(1):203-208. doi:10.1093/carcin/bgr256 PMID: 22080573.
37. Kuijsten A, Arts IC, Hollman PC, van't Veer P, Kampman E. Plasma enterolignans are associated with lower colorectal adenoma risk. Cancer Epidemiol Biomarkers Prev. 2006; 15(6):1132-1136. doi:10.1158/1055-9965.EPI-05-0991 PMID: 16775171.
38. Clavel T, Henderson G, Alpert CA, Philippe C, Rigottier-Gois L, Dore J, et al. Intestinal bacterial communities that produce active estrogen-like compounds enterodiol and enterolactone in humans. Appl Environ Microbiol. 2005; 71(10):6077-6085. doi:10.1128/AEM.71.10.6077-6085.2005 PMID: 16204524.
39. Jansen GH, Arts IC, Nielen MW, Muller M, Hollman PC, Keijer J. Uptake and metabolism of enterolactone and enterodiol by human colon epithelial cells. Arch Biochem Biophys. 2005; 435(1):74-82. doi:10.1016/j.abb.2004.12.015 PMID: 15680909.
40. Penttinen P, Jaehrling J, Damdimopoulos AE, Inzunza J, Lemmen JG, van der Saag P, et al. Dietderived polyphenol metabolite enterolactone is a tissue-specific estrogen receptor activator. Endocrinology. 2007; 148(10):4875-4886. doi:10.1210/en.2007-0289 PMID: 17628008.
41. Carreau C, Flouriot G, Bennetau-Pelissero C, Potier M. Enterodiol and enterolactone, two major dietderived polyphenol metabolites have different impact on ERalpha transcriptional activation in human breast cancer cells. J Steroid Biochem Mol Biol. 2008; 110(1-2):176-185. doi:10.1016/j.jsbmb.2008.03.032 PMID: 18457947.
42. Kiyama R. Endocrine disruptor actions through receptor crosstalk. Environ. Biotechnol. 2016; in press.
43. van der Schouw YT, de Kleijn MJ, Peeters PH, Grobbee DE. Phyto-oestrogens and cardiovascular disease risk. Nutr Metab Cardiovasc Dis. 2000; 10(3):154-167. PMID: 11006924.
44. Tanji M, Kiyama R. Expression profiling of estrogen responsive genes using genomic and proteomic techniques for the evaluation of endocrine disruptors. Cur Pharmacogenom. 2004; 2, 255-266.
45. Damdimopoulou P, Nurmi T, Salminen A, Damdimopoulos AE, Kotka M, van der Saag P, et al. A single dose of enterolactone activates estrogen signaling and regulates expression of circadian clock genes in mice. J Nutr. 2011; 141(9):1583-1589. doi:10.3945/jn.111.140277 PMID: 21753063.
46. Takić MM, Jovanović VB, Pavićević ID, Uzelac TN, Aćimović JM, Ristić-Medić DK, et al. Binding of enterolactone and enterodiol to human serum albumin: increase of cysteine-34 thiol group reactivity. Food Funct. 2016; 7(2):1217-1226. doi:10.1039/c5fo01346a PMID: 26838610.
47. Miguel V, Otero JA, Garcõa-Villalba R, Tomas-Barberan F, Espõn JC, Merino G, et al. Role of ABCG2 in transport of the mammalian lignan enterolactone and its secretion into milk in Abcg2 knockout mice. Drug Metab Dispos. 2014; 42(5):943-946. doi:10.1124/dmd.113.055970 PMID: 24568887.
48. Nishihara T, Nishikawa J-I, Kanayama T, Dakeyama F, Saito K, Imagawa M, et al. Estrogenic activities of 517 chemicals by yeast two-hybrid assay. J Health Sci. 2000; 46(4):282-298.