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Volume 2015 (2015), Article ID 594656, 11 pages
http://dx.doi.org/10.1155/2015/594656
Review Article

Modulation of Aromatase by Phytoestrogens

Department of Physiology and Developmental Biology and The Neuroscience Center, Brigham Young University, Provo, UT 84602, USA

Received 1 October 2015; Revised 31 October 2015; Accepted 17 November 2015

Academic Editor: J. Paul G. Malthouse

Copyright © 2015 Edwin D. Lephart. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. G. Di Nardo and G. Gilardi, “Human aromatase: perspectives in biochemistry and biotechnology,” Biotechnology and Applied Biochemistry, vol. 60, no. 1, pp. 92–101, 2013. View at Publisher · View at Google Scholar · View at Scopus
  2. R. J. Santen, H. Brodie, E. R. Simpson, P. K. Siiteri, and A. Brodie, “History of aromatase: saga of an important biological mediator and therapeutic target,” Endocrine Reviews, vol. 30, no. 4, pp. 343–375, 2009. View at Publisher · View at Google Scholar · View at Scopus
  3. C. Stocco, “Tissue physiology and pathology of aromatase,” Steroids, vol. 77, no. 1-2, pp. 27–35, 2012. View at Publisher · View at Google Scholar · View at Scopus
  4. C. Taxvig, A. Elleby, K. Sonne-Hansen et al., “Effects of nutrition relevant mixtures of phytoestrogens on steroidogenesis, aromatase, estrogen, and androgen activity,” Nutrition and Cancer, vol. 62, no. 1, pp. 122–131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. H. Adlercreutz, C. Bannwart, K. Wähälä et al., “Inhibition of human aromatase by mammalian lignans and isoflavonoid phytoestrogens,” Journal of Steroid Biochemistry and Molecular Biology, vol. 44, no. 2, pp. 147–153, 1993. View at Publisher · View at Google Scholar · View at Scopus
  6. H. Adlercreutz and W. Mazur, “Phyto-oestrogens and Western diseases,” Annals of Medicine, vol. 29, no. 2, pp. 95–120, 1997. View at Publisher · View at Google Scholar · View at Scopus
  7. P. De Cremoux and Y. Jacquot, “Isoflavones and human estrogen receptor: when plants synthesis mammalian hormone minetics,” in Isoflavones: Chemistry, Analysis, Function and Effects, V. R. Preedy, Ed., pp. 157–178, The Royal Society of Chemistry, Cambridge, UK, 2013. View at Google Scholar
  8. S. Karkola and K. Wähälä, “The binding of lignans, flavonoids and coumestrol to CYP450 aromatase: a molecular modelling study,” Molecular and Cellular Endocrinology, vol. 301, no. 1-2, pp. 235–244, 2009. View at Publisher · View at Google Scholar · View at Scopus
  9. D. Ingram, K. Sanders, M. Kolybaba, and D. Lopez, “Case-control study of phyto-oestrogens and breast cancer,” The Lancet, vol. 350, no. 9083, pp. 990–994, 1997. View at Publisher · View at Google Scholar · View at Scopus
  10. C. L. Smith, “Estrogens, overview,” in Encyclopedia of Reproduction, E. Knobil and J. D. Neill, Eds., vol. 2, pp. 119–126, Academic Press, New York, NY, USA, 1999. View at Google Scholar
  11. A. S. Meyer, “Conversion of 19-hydroxy-Δ4-androstene-3,17-dione to estrone by endocrine tissue,” Biochimica et Biophysica Acta, vol. 17, pp. 441–442, 1955. View at Publisher · View at Google Scholar · View at Scopus
  12. A. S. Meyer, M. Hayano, M. C. Lindberg, M. Gutt, and O. G. Rogers, “The conversion of δ4-androstene-3,17-dione-4-C14 and dehydroepiandrosterone by bovine adrenal homogenate preparations,” Acta Endocrinologica, vol. 18, no. 2, pp. 148–168, 1955. View at Google Scholar · View at Scopus
  13. K. J. Ryan, “Biological aromatization of steroids,” The Journal of Biological Chemistry, vol. 234, no. 2, pp. 268–272, 1959. View at Google Scholar · View at Scopus
  14. E. A. Thompson Jr. and P. K. Siiteri, “The involvement of human placental microsomal cytochrome P-450 in aromatization,” The Journal of Biological Chemistry, vol. 249, no. 17, pp. 5373–5378, 1974. View at Google Scholar · View at Scopus
  15. J. M. Grodin, P. K. Siiteri, and P. C. MacDonald, “Source of estrogen production in postmenopausal women,” The Journal of Clinical Endocrinology & Metabolism, vol. 36, no. 2, pp. 207–214, 1973. View at Publisher · View at Google Scholar · View at Scopus
  16. D. L. Hemsell, C. D. Edman, J. F. Marks, P. K. Siiteri, and P. C. MacDonald, “Massive extraglandular aromatization of plasma androstenedione resulting in feminization of a prepubertal boy,” The Journal of Clinical Investigation, vol. 60, no. 2, pp. 455–464, 1977. View at Publisher · View at Google Scholar · View at Scopus
  17. W. C. Boon, J. D. Y. Chow, and E. R. Simpson, “The multiple roles of estrogens and the enzyme aromatase,” Progress in Brain Research, vol. 181, pp. 209–232, 2010. View at Publisher · View at Google Scholar · View at Scopus
  18. D. Ghosh, J. Griswold, M. Erman, and W. Pangborn, “Structural basis for androgen specificity and oestrogen synthesis in human aromatase,” Nature, vol. 457, no. 7226, pp. 219–223, 2009. View at Publisher · View at Google Scholar · View at Scopus
  19. A. Kamat, M. M. Hinshelwood, B. A. Murry, and C. R. Mendelson, “Mechanisms in tissue-specific regulation of estrogen biosynthesis in humans,” Trends in Endocrinology and Metabolism, vol. 13, no. 3, pp. 122–128, 2002. View at Publisher · View at Google Scholar · View at Scopus
  20. E. D. Lephart, “A review of brain aromatase cytochrome P450,” Brain Research Reviews, vol. 22, no. 1, pp. 1–26, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. R. A. Lobo, S. R. Davis, T. J. De Villiers et al., “Prevention of diseases after menopause,” Climacteric, vol. 17, no. 5, pp. 540–556, 2014. View at Publisher · View at Google Scholar · View at Scopus
  22. D. A. Marsh, H. J. Brodie, W. Garrett, C.-H. Tsai-Morris, and A. M. H. Brodie, “Aromatase inhibitors. Synthesis and biological activity of androstenedione derivatives,” Journal of Medicinal Chemistry, vol. 28, no. 6, pp. 788–795, 1985. View at Publisher · View at Google Scholar · View at Scopus
  23. J. L. Olin and M. St. Pierre, “Aromatase inhibitors in breast cancer prevention,” Annals of Pharmacotherapy, vol. 48, no. 12, pp. 1605–1610, 2014. View at Publisher · View at Google Scholar · View at Scopus
  24. E. R. Simpson, C. Clyne, G. Rubin et al., “Aromatase—a brief overview,” Annual Review of Physiology, vol. 64, pp. 93–127, 2002. View at Publisher · View at Google Scholar · View at Scopus
  25. C. Manach, G. Williamson, C. Morand, A. Scalbert, and C. Rémésy, “Bioavailability and bioefficacy of polyphenols in humans. I. Review of 97 bioavailability studies,” The American Journal of Clinical Nutrition, vol. 81, no. 1, pp. 230S–242S, 2005. View at Google Scholar · View at Scopus
  26. C. Manach, A. Scalbert, C. Morand, C. Rémésy, and L. Jiménez, “Polyphenols: food sources and bioavailability,” The American Journal of Clinical Nutrition, vol. 79, no. 5, pp. 727–747, 2004. View at Google Scholar · View at Scopus
  27. E. K. Cheruiyot, L. M. Mumera, W. K. Ng'etich, A. Hassanali, and F. Wachira, “Polyphenols as potential indicators for drought tolerance in tea (Camellia sinensis L.),” Bioscience, Biotechnology and Biochemistry, vol. 71, no. 9, pp. 2190–2197, 2007. View at Publisher · View at Google Scholar · View at Scopus
  28. N. Salah, N. J. Miller, G. Paganga, L. Tijburg, G. P. Bolwell, and C. Rice-Evans, “Polyphenolic flavanols as scavengers of aqueous phase radicals and as chain-breaking antioxidants,” Archives of Biochemistry and Biophysics, vol. 322, no. 2, pp. 339–346, 1995. View at Publisher · View at Google Scholar · View at Scopus
  29. J. P. E. Spencer, M. M. Abd El Mohsen, A.-M. Minihane, and J. C. Mathers, “Biomarkers of the intake of dietary polyphenols: strengths, limitations and application in nutrition research,” British Journal of Nutrition, vol. 99, no. 1, pp. 12–22, 2008. View at Publisher · View at Google Scholar · View at Scopus
  30. C.-M. Liu, C.-Y. Chen, and Y.-W. Lin, “Estimation of tea catechin levels using micellar electrokinetic chromatography: a quantitative approach,” Food Chemistry, vol. 150, pp. 145–150, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. M. S. Butt, A. Imran, M. K. Sharif et al., “Black tea polyphenols: a mechanistic treatise,” Critical Reviews in Food Science and Nutrition, vol. 54, no. 8, pp. 1002–1011, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. M. Meydani and S. T. Hasan, “Dietary polyphenols and obesity,” Nutrients, vol. 2, no. 7, pp. 737–751, 2010. View at Publisher · View at Google Scholar · View at Scopus
  33. S. Khurana, K. Venkataraman, A. Hollingsworth, M. Piche, and T. C. Tai, “Polyphenols: benefits to the cardiovascular system in health and in aging,” Nutrients, vol. 5, no. 10, pp. 3779–3827, 2013. View at Publisher · View at Google Scholar · View at Scopus
  34. S. Wang, N. Moustaid-Moussa, L. Chen et al., “Novel insights of dietary polyphenols and obesity,” The Journal of Nutritional Biochemistry, vol. 25, no. 1, pp. 1–18, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. J. A. Evans and E. J. Johnson, “The role of phytonutrients in skin health,” Nutrients, vol. 2, no. 8, pp. 903–928, 2010. View at Publisher · View at Google Scholar · View at Scopus
  36. M. J. Takaoka, “Of the phenolic substances of white hellebore (Veratrum gandiflorum Loes. fil.),” Journal of the Faculty of Science, Hokkaido University, vol. 3, pp. 1–16, 1940. View at Google Scholar
  37. S. Nonomura, H. Kanagawa, and A. Makimoto, “Chemical constituents of polygonaceous plants. I. Studies on the components of Koj O-Kon. (Polygonum Cuspidatum Sieb. Et Zucc.),” Yakugaku Zasshi, vol. 83, pp. 988–990, 1963. View at Google Scholar
  38. E. H. Siemann and L. L. Creasy, “Concentration of the phytoalexin resveratrol in wine,” American Journal of Enology and Viticulture, vol. 43, pp. 49–52, 1992. View at Google Scholar
  39. A. A. E. Bertelli, L. Giovannini, D. Giannessi et al., “Antiplatelet activity of synthetic and natural resveratrol in red wine,” International Journal of Tissue Reactions, vol. 17, no. 1, pp. 1–3, 1995. View at Google Scholar · View at Scopus
  40. M. Jang, L. Cai, G. O. Udeani et al., “Cancer chemopreventive activity of resveratrol, a natural product derived from grapes,” Science, vol. 275, no. 5297, pp. 218–220, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. J. Tomé-Carneiro, M. Larrosa, A. González-Sarrías, F. A. Tomás-Barberán, M. T. García-Conesa, and J. C. Espín, “Resveratrol and clinical trials: the crossroad from in vitro studies to human evidence,” Current Pharmaceutical Design, vol. 19, no. 34, pp. 6064–6093, 2013. View at Publisher · View at Google Scholar · View at Scopus
  42. J. M. Pezzuto, “The phenomenon of resveratrol: redefining the virtues of promiscuity,” Annals of the New York Academy of Sciences, vol. 1215, no. 1, pp. 123–130, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. Y. Y. Lam, C. M. Peterson, and E. Ravussin, “Resveratrol and calorie restriction: data from rodents to humans,” Experimental Gerontology, vol. 48, no. 10, pp. 1018–1024, 2013. View at Publisher · View at Google Scholar · View at Scopus
  44. B. Turan, E. Tuncay, and G. Vassort, “Resveratrol and diabetic cardiac function: focus on recent in vitro and in vivo studies,” Journal of Bioenergetics and Biomembranes, vol. 44, no. 2, pp. 281–296, 2012. View at Publisher · View at Google Scholar · View at Scopus
  45. J. K. Bhatt, S. Thomas, and M. J. Nanjan, “Resveratrol supplementation improves glycemic control in type 2 diabetes mellitus,” Nutrition Research, vol. 32, no. 7, pp. 537–541, 2012. View at Publisher · View at Google Scholar · View at Scopus
  46. J. P. Crandall, V. Oram, G. Trandafirescu et al., “Pilot study of resveratrol in older adults with impaired glucose tolerance,” The Journals of Gerontology A: Biological Sciences & Medical Sciences, vol. 67, no. 12, pp. 1307–1312, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. E.-J. Park and J. M. Pezzuto, “The pharmacology of resveratrol in animals and humans,” Biochimica et Biophysica Acta, vol. 1852, pp. 1071–1113, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. K. D. R. Setchell and C. Clerici, “Equol: history, chemistry, and formation,” The Journal of Nutrition, vol. 140, no. 7, pp. 1355s–1362s, 2010. View at Publisher · View at Google Scholar · View at Scopus
  49. E. D. Lephart, “Isoflavones and prenatal exposure to equol,” in Isoflavones: Chemistry, Analysis, Function and Effects, V. R. Preedy, Ed., pp. 480–499, The Royal Society of Chemistry, Cambridge, UK, 2013. View at Google Scholar
  50. T. D. Lund, C. Blake, L. Bu, A. N. Hamaker, and E. D. Lephart, “Equol an isoflavonoid: potential for improved prostate health, in vitro and in vivo evidence,” Reproductive Biology and Endocrinology, vol. 9, article 4, 2011. View at Publisher · View at Google Scholar · View at Scopus
  51. R. Gopaul, H. E. Knaggs, and E. D. Lephart, “Biochemical investigation and gene analysis of equol: a plant and soy-derived isoflavonoid with antiaging and antioxidant properties with potential human skin applications,” Biofactors, vol. 38, no. 1, pp. 44–52, 2012. View at Publisher · View at Google Scholar · View at Scopus
  52. E. D. Lephart, “Protective effects of equol and their polyphenolic isomers against dermal aging: microarray/protein evidence with clinical implications and unique delivery into human skin,” Pharmaceutical Biology, vol. 51, no. 11, pp. 1393–1400, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. B. R. Goldin, H. Adlercreutz, J. T. Dwyer, L. Swenson, J. H. Warram, and S. L. Gorbach, “Effect of diet on excretion of estrogens in premenopausal and post-menopausal women,” Cancer Research, vol. 9, pp. 3771–3773, 1981. View at Google Scholar
  54. B. R. Goldin, H. Adlercreutz, S. L. Gorbach et al., “Estrogen excretion patterns and plasma levels in vegetarian and omnivorous women,” The New England Journal of Medicine, vol. 307, no. 25, pp. 1542–1547, 1982. View at Publisher · View at Google Scholar · View at Scopus
  55. H. Aldercreutz, “Does fiber-rich food containing animal lignan precursors protect against both colon and breast cancer? An extension of the ‘fiber hypothesis’,” Gastroenterology, vol. 86, no. 4, pp. 761–764, 1984. View at Google Scholar · View at Scopus
  56. B. R. Goldin, H. Adlercreutz, A. S. L. Gorbach et et al., “The relationship between estrogen levels and diets of Caucasian American and Oriental immigrant women,” The American Journal of Clinical Nutrition, vol. 44, no. 6, pp. 945–953, 1986. View at Google Scholar · View at Scopus
  57. M. Axelson, J. Sjovall, B. E. Gustaffson, and K. D. R. Setchell, “Soya—a dietary source of the non-steroidal oestrogen equol in man and animals,” Journal of Endocrinology, vol. 102, no. 1, pp. 49–56, 1984. View at Publisher · View at Google Scholar · View at Scopus
  58. K. D. R. Setchell, S. P. Borriello, P. Hulme, D. N. Kirk, and M. Axelson, “Nonsteroidal estrogens of dietary origin: possible roles in hormone-dependent disease,” The American Journal of Clinical Nutrition, vol. 40, no. 3, pp. 569–578, 1984. View at Google Scholar · View at Scopus
  59. H. Adlercreutz, “Diet, breast cancer, and sex hormone metabolism,” Annals of the New York Academy of Sciences, vol. 595, pp. 281–290, 1990. View at Publisher · View at Google Scholar · View at Scopus
  60. J. T. Kellis Jr. and L. E. Vickery, “Inhibition of human estrogen synthetase (aromatase) by flavones,” Science, vol. 225, no. 4666, pp. 1032–1034, 1984. View at Publisher · View at Google Scholar · View at Scopus
  61. D. R. Campbell and M. S. Kurzer, “Flavonoid inhibition of aromatase enzyme activity in human preadipocytes,” Journal of Steroid Biochemistry and Molecular Biology, vol. 46, no. 3, pp. 381–388, 1993. View at Publisher · View at Google Scholar · View at Scopus
  62. C. F. Wang, T. Mäkelä, T. Hase, H. Adlercreutz, and M. S. Kurzer, “Lignans and flavonoids inhibit aromatase enzyme in human preadipocytes,” Journal of Steroid Biochemistry and Molecular Biology, vol. 50, no. 3-4, pp. 205–212, 1994. View at Publisher · View at Google Scholar · View at Scopus
  63. C. Pelissero, M. J. P. Lenczowski, D. Chinzi, B. Davail-Cuisset, J. P. Sumpter, and A. Fostier, “Effects of flavonoids on aromatase activity, an in vitro study,” Journal of Steroid Biochemistry and Molecular Biology, vol. 57, no. 3-4, pp. 215–223, 1996. View at Publisher · View at Google Scholar · View at Scopus
  64. J. C. Le Bail, T. Laroche, F. Marre-Fournier, and G. Habrioux, “Aromatase and 17β-hydroxysteroid dehydrogenase inhibition by flavonoids,” Cancer Letters, vol. 133, no. 1, pp. 101–106, 1998. View at Publisher · View at Google Scholar · View at Scopus
  65. H.-J. Jeong, Y. G. Shin, I.-H. Kim, and J. M. Pezzuto, “Inhibition of aromatase activity by flavonoids,” Archives of Pharmacal Research, vol. 22, no. 3, pp. 309–312, 1999. View at Publisher · View at Google Scholar · View at Scopus
  66. A.-R. Ibrahim and Y. J. Abul-Hajj, “Aromatase inhibition by flavonoids,” Journal of Steroid Biochemistry and Molecular Biology, vol. 37, no. 2, pp. 257–260, 1990. View at Publisher · View at Google Scholar · View at Scopus
  67. J.-P. Basly and M.-C. C. Lavier, “Dietary phytoestrogens: potential selective estrogen enzyme modulators?” Planta Medica, vol. 71, no. 4, pp. 287–294, 2005. View at Publisher · View at Google Scholar · View at Scopus
  68. J. D. Brooks and L. U. Thompson, “Mammalian lignans and genistein decrease the activities of aromatase and 17β-hydroxysteroid dehydrogenase in MCF-7 cells,” Journal of Steroid Biochemistry and Molecular Biology, vol. 94, no. 5, pp. 461–467, 2005. View at Publisher · View at Google Scholar · View at Scopus
  69. J. A. van Meeuwen, N. Korthagen, P. C. de Jong, A. H. Piersma, and M. van den Berg, “Antiestrogenic effects of phytochemicals on human primary mammary fibroblasts, MCF-7 cells and their co-cultures,” Toxicology and Applied Pharmacology, vol. 221, no. 3, pp. 372–383, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. S. Rice, H. D. Mason, and S. A. Whitehead, “Phytoestrogens and their low dose combinations inhibit mRNA expression and activity of aromatase in human granulosa-luteal cells,” Journal of Steroid Biochemistry and Molecular Biology, vol. 101, no. 4-5, pp. 216–225, 2006. View at Publisher · View at Google Scholar · View at Scopus
  71. Y. Wang, W. M. Gho, F. I. Chan, S. Chen, and L. K. Leung, “The red clover (Trifolium pratense) isoflavone biochanin A inhibits aromatase activity and expression,” British Journal of Nutrition, vol. 99, no. 2, pp. 303–310, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. S. I. Khan, J. Zhao, I. A. Khan, L. A. Walker, and A. K. Dasmahapatra, “Potential utility of natural products as regulators of breast cancer-associated aromatase promoters,” Reproductive Biology and Endocrinology, vol. 9, article 91, 2011. View at Publisher · View at Google Scholar · View at Scopus
  73. R. J. Santen, L. M. Demers, H. Adlercreutz et al., “Inhibition of aromatase with CGS-16949A in postmenopausal women,” Journal of Clinical Endocrinology and Metabolism, vol. 68, no. 1, pp. 99–106, 1989. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Masamura, H. Adlercreutz, H. Harvey et al., “Aromatase inhibitor development for treatment of breast cancer,” Breast Cancer Research and Treatment, vol. 33, no. 1, pp. 19–26, 1995. View at Publisher · View at Google Scholar · View at Scopus
  75. X. Xu, A. M. Duncan, B. E. Merz, and M. S. Kurzer, “Effects of soy isoflavones on estrogen and phytoestrogen metabolism in premenopausal women,” Cancer Epidemiology Biomarkers and Prevention, vol. 7, no. 12, pp. 1101–1108, 1998. View at Google Scholar · View at Scopus
  76. M. J. Messina, “Soy foods and soybean isoflavones and menopausal health,” Nutrition in Clinical Care, vol. 5, no. 6, pp. 272–282, 2002. View at Google Scholar · View at Scopus
  77. J. P. White and J. S. Schilling, “Postmenopausal hormone replacement: historical perspectives and current concerns,” Clinical Excellence for Nurse Practitioners, vol. 4, no. 5, pp. 277–285, 2000. View at Google Scholar · View at Scopus
  78. J. E. Rossouw, G. L. Anderson, R. L. Prentice et al., “Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the women's health initiative randomized controlled trial,” The Journal of the American Medical Association, vol. 288, no. 3, pp. 321–333, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. L. A. Fitzpatrick, “Soy isoflavones: hope or hype?” Maturitas, vol. 44, pp. S21–S29, 2003. View at Publisher · View at Google Scholar · View at Scopus
  80. H. Adlercreutz, “Phyto-oestrogens and cancer,” The Lancet Oncology, vol. 3, no. 6, pp. 364–373, 2002. View at Publisher · View at Google Scholar · View at Scopus
  81. H. Adlercreutz, “Phytoestrogens and breast cancer,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 83, no. 1–5, pp. 113–118, 2002. View at Publisher · View at Google Scholar · View at Scopus
  82. R. Mackey and R. M. Evans, “Phytoestrogens and the menopause,” Climacteric, vol. 1, no. 4, pp. 302–308, 1995. View at Google Scholar
  83. M. Messerer, S.-E. Johansson, and A. Wolk, “Sociodemographic and health behaviour factors among dietary supplement and natural remedy users,” European Journal of Clinical Nutrition, vol. 55, no. 12, pp. 1104–1110, 2001. View at Publisher · View at Google Scholar · View at Scopus
  84. S. Karkola, H.-D. Höltje, and K. Wähälä, “A three-dimensional model of CYP19 aromatase for structure-based drug design,” Journal of Steroid Biochemistry and Molecular Biology, vol. 105, no. 1–5, pp. 63–70, 2007. View at Publisher · View at Google Scholar · View at Scopus
  85. J. T. Sanderson, J. Hordijk, M. S. Denison, M. F. Springsteel, M. H. Nantz, and M. van den Berg, “Induction and inhibition of aromatase (CYP19) activity by natural and synthetic flavonoid compounds in H295R human adrenocortical carcinoma cells,” Toxicological Sciences, vol. 82, no. 1, pp. 70–79, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. S. Paoletta, G. B. Steventon, D. Wildeboer, T. M. Ehrman, P. J. Hylands, and D. J. Barlow, “Screening of herbal constituents for aromatase inhibitory activity,” Bioorganic & Medicinal Chemistry, vol. 16, no. 18, pp. 8466–8470, 2008. View at Publisher · View at Google Scholar · View at Scopus
  87. Y. E. Wang, T. Y. Wong, F. L. Chan, S. Chen, and L. K. Leung, “Assessing the effect of food mycotoxins on aromatase by using a cell-based system,” Toxicology in Vitro, vol. 28, no. 4, pp. 640–646, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. J.-C. Le Bail, Y. Champavier, A.-J. Chulia, and G. Habrioux, “Effects of phytoestrogens on aromatase, 3β and 17β-hydroxysteroid dehydrogenase activities and human breast cancer cells,” Life Sciences, vol. 66, no. 14, pp. 1281–1291, 2000. View at Publisher · View at Google Scholar · View at Scopus
  89. M. B. M. van Duursen, S. M. Nijmeijer, E. S. de Morree, P. C. de Jong, and M. van den Berg, “Genistein induces breast cancer-associated aromatase and stimulates estrogen-dependent tumor cell growth in in vitro breast cancer model,” Toxicology, vol. 289, no. 2-3, pp. 67–73, 2011. View at Publisher · View at Google Scholar · View at Scopus
  90. M. B. M. van Duursen, E. E. J. W. Smeets, J. C. W. Rijk, S. M. Nijmeijer, and M. van den Berg, “Phytoestrogens in menopausal supplements induce ER-dependent cell proliferation and overcome breast cancer treatment in an in vitro breast cancer model,” Toxicology and Applied Pharmacology, vol. 269, no. 2, pp. 132–140, 2013. View at Publisher · View at Google Scholar · View at Scopus
  91. D. U. Richter, I. Mylonas, B. Toth et al., “Effects of phytoestrogens genistein and daidzein on progesterone and estrogen (estradiol) production of human term trophoblast cells in vitro,” Gynecological Endocrinology, vol. 25, no. 1, pp. 32–38, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. U. Tiemann, F. Schneider, J. Vanselow, and W. Tomek, “In vitro exposure of porcine granulosa cells to the phytoestrogens genistein and daidzein: effects on the biosynthesis of reproductive steroid hormones,” Reproductive Toxicology, vol. 24, no. 3-4, pp. 317–325, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. S. Bolca, M. Urpi-Sarda, P. Blondeel et al., “Disposition of soy isoflavones in normal human breast tissue,” The American Journal of Clinical Nutrition, vol. 91, no. 4, pp. 976–984, 2010. View at Publisher · View at Google Scholar · View at Scopus
  94. X. M. Kang, Q. Y. Zhang, S. H. Wang, X. Huang, and S. Jin, “Effect of soy isoflavones on breast cancer recurrence and death for patients receiving adjuvant endocrine therapy,” Canadian Medical Association Journal, vol. 182, no. 17, pp. 1857–1862, 2010. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Rice and S. A. Whitehead, “Phytoestrogens oestrogen synthesis and breast cancer,” The Journal of Steroid Biochemistry and Molecular Biology, vol. 108, no. 3–5, pp. 186–195, 2008. View at Publisher · View at Google Scholar · View at Scopus
  96. F. Chi, R. Wu, Y.-C. Zeng, R. Xing, Y. Liu, and Z.-G. Xu, “Post-diagnosis soy food intake and breast cancer survival: a meta-analysis of cohort studies,” Asian Pacific Journal of Cancer Prevention, vol. 14, no. 4, pp. 2407–2412, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. M. M. Liu, Y. Huang, and J. Wang, “Developing phytoestrogens for breast cancer prevention,” Anti-Cancer Agents in Medicinal Chemistry, vol. 12, no. 10, pp. 1306–1313, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. A. V. Sirotkin and A. H. Harrath, “Phytoestrogens and their effects,” European Journal of Pharmacology, vol. 741, pp. 230–236, 2014. View at Publisher · View at Google Scholar · View at Scopus
  99. M. Minatoya, G. Kutomi, S. Asakura et al., “Equol, adiponectin, insulin levels and risk of breast cancer,” Asian Pacific Journal of Cancer Prevention, vol. 14, no. 4, pp. 2191–2199, 2013. View at Publisher · View at Google Scholar · View at Scopus
  100. E. D. Lephart, “Review: anti-oxidant and anti-aging properties of equol in prostate health (BPH),” Open Journal of Endocrine and Metabolic Diseases, vol. 4, pp. 1–12, 2014. View at Publisher · View at Google Scholar
  101. V. Z. Ajdžanović, I. M. Medigović, J. B. Pantelić, and V. L. Milošević, “Soy isoflavones and cellular mechanics,” Journal of Bioenergetics and Biomembranes, vol. 46, no. 2, pp. 99–107, 2014. View at Publisher · View at Google Scholar
  102. M. J. Kim, Y. J. Park, K. H. Chung, and S. M. Oh, “The inhibitory effects of the standardized extracts of Ginkgo biloba on aromatase activity in JEG-3 human choriocarcinoma cells,” Phytotherapy Research, vol. 27, no. 12, pp. 1756–1762, 2013. View at Publisher · View at Google Scholar · View at Scopus
  103. G. Celik, H. Akca, and A. Sen, “Investigation of aromotase inhibition by several dietary vegetables in human non-small cell lung cancer cell lines,” Turkish Journal of Biochemistry, vol. 38, no. 2, pp. 207–217, 2013. View at Publisher · View at Google Scholar · View at Scopus
  104. L. Ye, M. Y. Chan, and L. K. Leung, “The soy isoflavone genistein induces estrogen synthesis in an extragonadal pathway,” Molecular and Cellular Endocrinology, vol. 302, no. 1, pp. 73–80, 2009. View at Publisher · View at Google Scholar · View at Scopus