Phytoestrogenic potential of cyclopia extracts and polyphenols

Planta Medica

Volumn 79, Issue 7, 2013, Pages 580-590

  Louw, Ann ^a   Joubert, Elizabeth ^a,b   Visser, Koch ^a  

^a STELLENBOSCH UNIVERSITY   (South Africa)

^b AGRICULTURAL RESEARCH COUNCIL   (South Africa)

Author keywords

Cyclopia; E screen; ER binding; ERE promoter reporter assay; Fabaceae; phytoestrogen; uterotrophic assay

Indexed keywords

BENZALDEHYDE DERIVATIVE; BENZOPHENONE; CALYCOSIN; CHALCONE DERIVATIVE; CYCLOPIA EXTRACT; CYCLOPIA SUBTERNATA EXTRACT; DIHYDROCHALCONE; DIOSMETIN; ERIOCITRIN; ERIODICTYOL; ESTRADIOL; FLAVANOL DERIVATIVE; FLAVANONE; FLAVONE; FLAVONOL; FORMONONETIN; HESPERETIN; ISOFLAVONE; LUTEOLIN; MANGIFERIN; NARINGENIN; NARIRUTIN; ONONIN; OROBOL; PHYTOESTROGEN; PLANT EXTRACT; POLYPHENOL; PRUNIN; UNCLASSIFIED DRUG; UNINDEXED DRUG; XANTHONE 4 ACETIC ACID;

AQUEOUS SOLUTION; CHEMICAL COMPOSITION; CYCLOPIA (GENUS); CYCLOPIA SUBTERNATA; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG RESEARCH; ESTROGEN ACTIVITY; HORMONE RECEPTOR INTERACTION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; MENOPAUSAL SYNDROME; NONHUMAN; PHYTOCHEMISTRY; PLANT LEAF; REVIEW;

CYCLOPIA PLANT; FEMALE; HUMANS; PHYTOESTROGENS; PHYTOTHERAPY; PLANT EXTRACTS; POLYPHENOLS; SOUTH AFRICA;

CYCLOPIA (ANGIOSPERM); FABACEAE;

EID: 84877876326     PISSN: 00320943     EISSN: 14390221     Source Type: Journal    
DOI: 10.1055/s-0032-1328463     Document Type: Review

References (106)

1. Joubert E., Gelderblom W. C., Louw A., de Beer D. South African herbal teas: Aspalathus linearis, Cyclopia spp. and Athrixia phylicoides - a review. J Ethnopharmacol: 2008; 119 376 412
2. Schutte A. Systematics of the genus Cyclopia Vent. (Fabaceae, Podalyrieae). Edinburgh J Bot: 1997; 54 125 170 (Pubitemid 127479339)
3. Joubert E., Joubert M. E., Bester C., de Beer D., De Lange J. H. Honeybush (Cyclopia spp.): From local cottage industry to global markets - the catalytic and supporting role of research. S Afr J Bot: 2011; 77 887 907
4. Watt J. M., Breyer-Brandwijk M. G. The medicinal and poisonous plants of southern and eastern Africa. London E. & S. Livingstone: 1962
5. Ferreira D., Kamara B. I., Brandt E. V., Joubert E. Phenolic compounds from Cyclopia intermedia (honeybush tea). 1. J Agric Food Chem: 1998; 46 3406 3410 (Pubitemid 128488141)
6. Kamara B. I., Brandt E. V., Ferreira D., Joubert E. Polyphenols from honeybush tea (Cyclopia intermedia). J Agric Food Chem: 2003; 51 3874 3879
7. Kamara B. I., Brand D. J., Brandt E. V., Joubert E. Phenolic metabolites from honeybush tea (Cyclopia subternata). J Agric Food Chem: 2004; 52 5391 5395
8. Joubert E., Richards E. S., Van der Merwe J. D., De Beer D., Manley M., Gelderblom W. C. An effect of species variation and processing on phenolic composition and in vitro antioxidant activity of aqueous extracts of Cyclopia spp. (honeybush tea). J Agric Food Chem: 2008; 56 954 963 (Pubitemid 351300269)
9. Hubbe M. E. Evaluation of antioxidant and free radical scavenging activities of honeybush tea (Cyclopia). Stellenbosch Stellenbosch University: 2000
10. Marnewick J., Joubert E., Joseph S., Swanevelder S., Swart P., Gelderblom W. Inhibition of tumour promotion in mouse skin by extracts of rooibos (Aspalathus linearis) and honeybush (Cyclopia intermedia), unique South African herbal teas. Cancer Lett: 2005; 224 193 202 (Pubitemid 40725841)
11. Sissing L., Marnewick J., de Kock M., Swanevelder S., Joubert E., Gelderblom W. Modulating effects of rooibos and honeybush herbal teas on the development of esophageal papillomas in rats. Nutr Cancer: 2011; 63 600 610
12. Muller C. JF, Joubert E., Gabuza K., de Beer D., Louw J., Fey S. J. Assessment of the antidiabetic potential of an aqueous extract of honeybush (Cyclopia intermedia) in streptozotocin and obese insulin resistant wistar rats. In: Rasooli I. ed. Phytochemicals - bioactivities and impact on health. Rijeka In Tech: 2011; 313 332
13. Mose Larsen P., Fey S. J., Louw J., Joubert L. Anti-diabetic extract of honeybush. US Patent 20110045108: 2012
14. Rood B. Uit die veldapteek. Kaapstad Tafelberg: 1994
15. Kokotkiewicz A., Luczkiewicz M., Sowinski P., Glod D., Gorynski K., Bucinski A. Isolation and structure elucidation of phenolic compounds from Cyclopia subternata Vogel (honeybush) intact plant and in vitro cultures. Food Chem: 2012; 133 1373 1382
16. de Beer D., Joubert E. Development of HPLC method for Cyclopia subternata phenolic compound analysis and application to other Cyclopia spp. J Food Comp Anal: 2010; 23 289 297
17. De Beer D., Schulze A. S., Joubert E., De Villiers A., Malherbe C. J., Stander M. A. Food ingredient extracts of Cyclopia subternata (honeybush): variation in phenolic composition and antioxidant capacity. Molecules: 2012; 17 14602 14624
18. Hattori M., Shu Y. Z., El-Sedawy A. I., Namba T., Kobashi K., Tomimori T. Metabolism of homoorientin by human intestinal bacteria. J Nat Prod: 1988; 51 874 878
19. Sanugul K., Akao T., Li Y., Kakiuchi N., Nakamura N., Hattori M. Isolation of a human intestinal bacterium that transforms mangiferin to norathyriol and inducibility of the enzyme that cleaves a C-glucosyl bond. Biol Pharm Bull: 2005; 28 1672 1678 (Pubitemid 41324131)
20. Nakamura K., Nishihata T., Jin J. S., Ma C. M., Komatsu K., Iwashima M., Hattori M. The C-glucosyl bond of puerarin was cleaved hydrolytically by a human intestinal bacterium strain PUE to yield its aglycone daidzein and an intact glucose. Chem Pharm Bull (Tokyo): 2011; 59 23 27
21. Shanle E. K., Xu W. Endocrine disrupting chemicals targeting estrogen receptor signaling: identification and mechanisms of action. Chem Res Toxicol: 2011; 24 6 19
22. Heldring N., Pike A., Andersson S., Matthews J., Cheng G., Hartman J., Tujague M., Strom A., Treuter E., Warner M., Gustafsson J. A. Estrogen receptors: how do they signal and what are their targets. Physiol Rev: 2007; 87 905 931 (Pubitemid 47084672)
23. Kortenkamp A., Martin O., Faust M., Evans R., McKinley R., Orton F., Rosivatz E. State of the art assessment of endocrine disruptors. Final Rep: 2011; 2011 1 135
24. EDSTAC Endocrine disruptor screening and testing advisory committee final report, 1998. Washington US Environmental Protection Agency: 1998
25. Saarinen N. M., Bingham C., Lorenzetti S., Mortensen A., Makela S., Penttinen P., Sorensen I. K., Valsta L. M., Virgili F., Vollmer G., Warri A., Zierau O. Tools to evaluate estrogenic potency of dietary phytoestrogens: a consensus paper from the EU Thematic Network "Phytohealtho" (QLKI-2002-2453). Genes Nutr: 2006; 1 143 158
26. Soto A. M., Maffini M. V., Schaeberle C. M., Sonnenschein C. Strengths and weaknesses of in vitro assays for estrogenic and androgenic activity. Best Pract Res Clin Endocrinol Metab: 2006; 20 15 33 (Pubitemid 43323762)
27. Dobbins L. L., Brain R. A., Brooks B. W. Comparison of the sensitivities of common in vitro and in vivo assays of estrogenic activity: application of chemical toxicity distributions. Environ Toxicol Chem: 2008; 27 2608 2616
28. Fang H., Tong W., Perkins R., Soto A. M., Prechtl N. V., Sheehan D. M. Quantitative comparisons of in vitro assays for estrogenic activities. Environ Health Perspect: 2000; 108 723 729
29. Patisaul H. B., Jefferson W. The pros and cons of phytoestrogens. Front Neuroendocrinol: 2010; 31 400 419
30. Verhoog N. JD, Joubert E., Louw A. Screening of four Cyclopia (honeybush) species for putative phyto-oestrogenic activity by oestrogen receptor binding assays. S Afr J Sci: 2007; 103 13 21 (Pubitemid 46999510)
31. de Cremoux P., This P., Leclercq G., Jacquot Y. Controversies concerning the use of phytoestrogens in menopause management: bioavailability and metabolism. Maturitas: 2010; 65 334 339
32. Verhoog N. J., Joubert E., Louw A. Evaluation of the phytoestrogenic activity of Cyclopia genistoides (honeybush) methanol extracts and relevant polyphenols. J Agric Food Chem: 2007; 55 4371 4381 (Pubitemid 46932632)
33. Liu L., Xu D. M., Cheng Y. Y. Distinct effects of naringenin and hesperetin on nitric oxide production from endothelial cells. J Agric Food Chem: 2008; 56 824 829 (Pubitemid 351300251)
34. Promberger A., Dornstauder E., Frühwirth C., Schmid E. R., Jungbauer A. Determination of estrogenic activity in beer by biological and chemical means. J Agric Food Chem: 2001; 49 633 640 (Pubitemid 32172604)
35. Guo D., Wang J., Wang X., Luo H., Zhang H., Cao D., Chen L., Huang N. Double directional adjusting estrogenic effect of naringin from Rhizoma drynariae (Gusuibu). J Ethnopharmacol: 2011; 138 451 457
36. Breinholt V., Larsen J. C. Detection of weak estrogenic flavonoids using a recombinant yeast strain and a modified MCF7 cell proliferation assay. Chem Res Toxicol: 1998; 11 622 629 (Pubitemid 28285587)
37. Han D. H., Denison M. S., Tachibana H., Yamada K. Relationship between estrogen receptor-binding and estrogenic activities of environmental estrogens and suppression by flavonoids. Biosci Biotechnol Biochem: 2002; 66 1479 1487 (Pubitemid 39246853)
38. Reiter E., Beck V., Medjakovic S., Mueller M., Jungbauer A. Comparison of hormonal activity of isoflavone-containing supplements used to treat menopausal complaints. Menopause: 2009; 16 1049 1060
39. Tang J. Y., Li S., Li Z. H., Zhang Z. J., Hu G., Cheang L. C., Alex D., Hoi M. P., Kwan Y. W., Chan S. W., Leung G. P., Lee S. M. Calycosin promotes angiogenesis involving estrogen receptor and mitogen-activated protein kinase (MAPK) signaling pathway in zebrafish and HUVEC. PLoS One: 2010; 5 e11822
40. Beck V., Unterrieder E., Krenn L., Kubelka W., Jungbauer A. Comparison of hormonal activity (estrogen, androgen and progestin) of standardized plant extracts for large scale use in hormone replacement therapy. J Steroid Biochem Mol Biol: 2003; 84 259 268 (Pubitemid 36514843)
41. Mu H., Bai Y. H., Wang S. T., Zhu Z. M., Zhang Y. W. Research on antioxidant effects and estrogenic effect of formononetin from Trifolium pratense (red clover). Phytomedicine: 2009; 16 314 319
42. Chen J., Liu L., Hou R., Shao Z., Wu Y., Chen X., Zhou L. Calycosin promotes proliferation of estrogen receptor-positive cells via estrogen receptors and ERK1/2 activation in vitro and in vivo. Cancer Lett: 2011; 308 144 151
43. Zhu J. T., Choi R. C., Chu G. K., Cheung A. W., Gao Q. T., Li J., Jiang Z. Y., Dong T. T., Tsim K. W. Flavonoids possess neuroprotective effects on cultured pheochromocytoma PC12 cells: a comparison of different flavonoids in activating estrogenic effect and in preventing beta-amyloid-induced cell death. J Agric Food Chem: 2007; 55 2438 2445 (Pubitemid 46556236)
44. Mfenyana C., De Beer D., Joubert E., Louw A. Selective extraction of Cyclopia for enhanced in vitro phytoestrogenicity and benchmarking against commercial phytoestrogen extracts. J Steroid Biochem Mol Biol: 2008; 112 74 86
45. Kitalong C., El-Halawany A., El-Dine R., Ma C., Hattori M. Phenolics from Phaleria nisidai with estrogenic activity. Records Nat Prod: 2012; 6 296 300
46. Collins-Burow B. M., Burow M. E., Duong B. N., McLachlan J. A. Estrogenic and antiestrogenic activities of flavonoid phytochemicals through estrogen receptor binding-dependent and -independent mechanisms. Nutr Cancer: 2000; 38 229 244 (Pubitemid 32762024)
47. Wagner H., Ulrich-Merzenich G. Synergy research: approaching a new generation of phytopharmaceuticals. Phytomedicine: 2009; 16 97 110
48. Geller S. E., Studee L. Botanical and dietary supplements for menopausal symptoms: what works, what does not. J Womens Health (Larchmt): 2005; 14 634 649 (Pubitemid 41508708)
49. Nilsson S., Mäkelä S., Treuter E., Tujague M., Thomsen J., Andersson G., Enmark E., Pettersson K., Warner M., Gustafsson J. Å. Mechanisms of estrogen action. Physiol Rev: 2001; 81 1535 1565 (Pubitemid 32951806)
50. Yager J. D., Davidson N. E. Estrogen carcinogenesis in breast cancer. N Engl J Med: 2006; 354 270 282
51. Humphries K. H., Gill S. Risks and benefits of hormone replacement therapy: the evidence speaks. Can Med Assoc J: 2003; 168 1001 1010 (Pubitemid 36513129)
52. Rymer J., Wilson R., Ballard K. Making decisions about hormone replacement therapy. Br Med J: 2003; 326 322 326 (Pubitemid 36205169)
53. Glazier M. G., Bowman M. A. A review of the evidence for the use of phytoestrogens as a replacement for traditional estrogen replacement therapy. Arch Intern Med: 2001; 161 1161 1172 (Pubitemid 32691512)
54. Rossouw J., Anderson G., Prentice R., LaCroix A. Z., Kooperberg C., Stefanick M., Jackson R. D., Beresford S. A., Howard B. V., Johnson K. C. Writing Group for the Womens Health Initiative Investigators. Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Womens Health Initiative randomized controlled trial. JAMA: 2002; 288 321 333 (Pubitemid 34761611)
55. Farquhar D. Postmenopausal hormone replacement therapy for chronic disease prevention: results from the Womens Health Initiative trial. CMAJ: 2002; 167 377 378
56. Van Leeuwen F. E., Rookus M. A. Breast cancer and hormone-replacement therapy: the Million Women Study. The Lancet: 2003; 362 1330
57. Warren M. P., Halpert S. Hormone replacement therapy: controversies, pros and cons. Best Pract Res Clin Endocrinol Metab: 2004; 18 317 332 (Pubitemid 38992414)
58. Santen R. J., Allred D. C., Ardoin S. P., Archer D. F., Boyd N., Braunstein G. D., Burger H. G., Colditz G. A., Davis S. R., Gambacciani M. Postmenopausal hormone therapy: an Endocrine Society scientific statement. J Clin Endocrinol Metab: 2010; 95 s1 s66
59. Scheiber M. D., Rebar R. W. Isoflavones and postmenopausal bone health: a viable alternative to estrogen therapy? Menopause: 1999; 6 233
60. Russell L., Hicks G. S., Low A. K., Shepherd J. M., Brown C. A. Phytoestrogens: a viable option? Am J Med Sci: 2002; 324 185 188
61. Mackey R., Eden J. Phytoestrogens and the menopause. Climacteric: 1998; 1 302 308 (Pubitemid 128691313)
62. Adlercreutz H., Mazur W. Phyto-oestrogens and Western diseases. Ann Med: 1997; 29 95 120 (Pubitemid 27226319)
63. Magee P. J., Rowland I. R. Phytoestrogens, their mechanism of action: current evidence for a role in breast and prostate cancer. Br J Nutr: 2004; 91 513 531 (Pubitemid 38584776)
64. Amin A., Buratovich M. The anti-cancer charm of flavonoids: a cup-of-tea will do. Recent Pat Anticancer Drug Discov: 2007; 2 109 117 (Pubitemid 46957317)
65. Setchell K. Phytoestrogens: the biochemistry, physiology, and implications for human health of soy isoflavones. Am J Clin Nutr: 1998; 68 1333S 1346S (Pubitemid 28550909)
66. Palmieri C., Cheng G., Saji S., Zelada-Hedman M., Weihua Z., Van Noorden S., Wahlstrom T., Coombes R., Warner M., Gustafsson J. Estrogen receptor beta in breast cancer. Endocr Relat Cancer: 2002; 9 1 13 (Pubitemid 34302928)
67. Hartman J., Ström A., Gustafsson J. Å. Estrogen receptor beta in breast cancer-diagnostic and therapeutic implications. Steroids: 2009; 74 635 641
68. Maximov P. Y., Lee T. M., Jordan V. C. The discovery and development of Selective Estrogen Receptor Modulators (SERMs) for clinical practice. Curr Clin Pharmacol: 2013; 8 135 155
69. Ververidis F., Trantas E., Douglas C., Vollmer G., Kretzschmar G., Panopoulos N. Biotechnology of flavonoids and other phenylpropanoid-derived natural products. Part I: Chemical diversity, impacts on plant biology and human health. Biotechnol J: 2007; 2 1214 1234 (Pubitemid 350047840)
70. Cornwell T., Cohick W., Raskin I. Dietary phytoestrogens and health. Phytochemistry: 2004; 65 995 1016 (Pubitemid 38542736)
71. Usui T. Pharmaceutical prospects of phytoestrogens. Endocr J: 2006; 53 7 20
72. Rice S., Whitehead S. A. Phytoestrogens oestrogen synthesis and breast cancer. J Steroid Biochem Mol Biol: 2008; 108 186 195 (Pubitemid 351179632)
73. Tempfer C. B., Bentz E. K., Leodolter S., Tscherne G., Reuss F., Cross H. S., Huber J. C. Phytoestrogens in clinical practice: a review of the literature. Fertil Steril: 2007; 87 1243 1249 (Pubitemid 46829161)
74. Messina M., Hughes C. Efficacy of soyfoods and soybean isoflavone supplements for alleviating menopausal symptoms is positively related to initial hot flush frequency. J Med Food: 2003; 6 1 11 (Pubitemid 36576609)
75. Boucher B. A., Cotterchio M., Anderson L. N., Kreiger N., Kirsh V. A., Thompson L. U. Use of isoflavone supplements is associated with reduced postmenopausal breast cancer risk. Int J Cancer: 2013; 132 1439 1450
76. Fink B. N., Steck S. E., Wolff M. S., Britton J. A., Kabat G. C., Gaudet M. M., Abrahamson P. E., Bell P., Schroeder J. C., Teitelbaum S. L. Dietary flavonoid intake and breast cancer survival among women on Long Island. Cancer Epidemiol Biomarkers Prev: 2007; 16 2285 2292 (Pubitemid 351196361)
77. Wu A., Yu M., Tseng C., Pike M. Epidemiology of soy exposures and breast cancer risk. Br J Cancer: 2008; 98 9 14
78. Shu X. O., Zheng Y., Cai H., Gu K., Chen Z., Zheng W., Lu W. Soy food intake and breast cancer survival. JAMA: 2009; 302 2437 2443
79. Lee S. A., Shu X. O., Li H., Yang G., Cai H., Wen W., Ji B. T., Gao J., Gao Y. T., Zheng W. Adolescent and adult soy food intake and breast cancer risk: results from the Shanghai Womens Health Study. Am J Clin Nutr: 2009; 89 1920 1926
80. Travis R. C., Allen N. E., Appleby P. N., Spencer E. A., Roddam A. W., Key T. J. A prospective study of vegetarianism and isoflavone intake in relation to breast cancer risk in British women. Int J Cancer: 2008; 122 705 710 (Pubitemid 350308968)
81. Hooper L., Madhavan G., Tice J. A., Leinster S. J., Cassidy A. Effects of isoflavones on breast density in pre- and post-menopausal women: a systematic review and meta-analysis of randomized controlled trials. Hum Reprod Update: 2010; 16 745 760
82. Mersereau J. E., Levy N., Staub R. E., Baggett S., Zogric T., Chow S., Ricke W. A., Tagliaferri M., Cohen I., Bjeldanes L. F. Liquiritigenin is a plant-derived highly selective estrogen receptor β agonist. Mol Cell Endocrinol: 2008; 283 49 57
83. Leitman D. C., Christians U. MF101: a multi-component botanical selective estrogen receptor beta modulator for the treatment of menopausal vasomotor symptoms. Expert Opin Investig Drugs: 2012; 21 1031 1042
84. Rhomberg L. R., Goodman J. E., Foster W. G., Borgert C. J., Van Der Kraak G. A critique of the European Commission Document, "State of the Art Assessment of Endocrine Disrupterso" Crit Rev Toxicol: 2012; 42 465 473
85. Bock C., Waldmann K. H., Ternes W. Mangiferin and hesperidin metabolites are absorbed from the gastrointestinal tract of pigs after oral ingestion of a Cyclopia genistoides (honeybush tea) extract. Nutr Res: 2008; 28 879 891
86. Bock C., Ternes W. The phenolic acids from bacterial degradation of the mangiferin aglycone are quantified in the feces of pigs after oral ingestion of an extract of Cyclopia genistoides (honeybush tea). Nutr Res: 2010; 30 348 357
87. Efferth T., Koch E. Complex interactions between phytochemicals. The multi-target therapeutic concept of phytotherapy. Curr Drug Targets: 2011; 12 122 132
88. Kong D. X., Li X. J., Zhang H. Y. Where is the hope for drug discovery? Let history tell the future. Drug Discov Today: 2009; 14 115 119
89. Patwardhan B., Mashelkar R. A. Traditional medicine-inspired approaches to drug discovery: can Ayurveda show the way forward? Drug Discov Today: 2009; 14 804 811
90. Katiyar C., Gupta A., Kanjilal S., Katiyar S. Drug discovery from plant sources: An integrated approach. AYU (An international quarterly journal of research in Ayurveda): 2012; 33 10 19
91. Gertsch J. Botanical drugs, synergy, and network pharmacology: forth and back to intelligent mixtures. Planta Med: 2011; 77 1086 1089
92. Joubert E., Manley M., Maicu C., de Beer D. Effect of pre-drying treatments and storage on color and phenolic composition of green honeybush (Cyclopia subternata) herbal tea. J Agric Food Chem: 2010; 58 338 344
93. Zava D. T., Blen M., Duwe G. Estrogenic activity of natural and synthetic estrogens in human breast cancer cells in culture. Environ Health Perspect: 1997; 105 03 637 645 (Pubitemid 27246429)
94. Zava D. T., Duwe G. Estrogenic and antiproliferative properties of genistein and other flavonoids in human breast cancer cells in vitro. Nutr Cancer: 1997; 27 31 40 (Pubitemid 26424313)
95. Hwang S. L., Yen G. C. Effect of hesperetin against oxidative stress via ER- and TrkA-mediated actions in PC12 cells. J Agric Food Chem: 2011; 59 5779 5785
96. Lee S., Chung H., Maier C. G., Wood A. R., Dixon R. A., Mabry T. J. Estrogenic Flavonoids from Artemisia vulgaris L. J Agric Food Chem: 1998; 46 3325 3329 (Pubitemid 128478903)
97. Poon C. H., Wong T. Y., Wang Y., Tsuchiya Y., Nakajima M., Yokoi T., Leung L. K. The citrus flavanone naringenin suppresses CYP1B1 transactivation through antagonising xenobiotic-responsive element binding. Br J Nutr advance online publication 31 August 2012; 10.1017/S0007114512003595
98. Zand R. S., Jenkins D. J., Diamandis E. P. Steroid hormone activity of flavonoids and related compounds. Breast Cancer Res Treat: 2000; 62 35 49 (Pubitemid 30609562)
99. Overk C. R., Yao P., Chadwick L. R., Nikolic D., Sun Y., Cuendet M. A., Deng Y., Hedayat A. S., Pauli G. F., Farnsworth N. R., van Breemen R. B., Bolton J. L. Comparison of the i n vitro estrogenic activities of compounds from hops (Humulus lupulus) and red clover (Trifolium pratense). J Agric Food Chem: 2005; 53 6246 6253 (Pubitemid 41169368)
100. Shemesh M., Lindner H. R., Ayalon N. Affinity of rabbit uterine oestradiol receptor for phyto-oestrogens and its use in a competitive protein-binding radioassay for plasma coumestrol. J Reprod Fertil: 1972; 29 1 9
101. Ji Z. N., Zhao W. Y., Liao G. R., Choi R. C., Lo C. K., Dong T. T., Tsim K. W. In vitro estrogenic activity of formononetin by two bioassay systems. Gynecol Endocrinol: 2006; 22 578 584 (Pubitemid 44888806)
102. Matsumoto T., Kobayashi M., Moriwaki T., Kawai S., Watabe S. Survey of estrogenic activity in fish feed by yeast estrogen-screen assay. Comp Biochem Physiol C Toxicol Pharmacol: 2004; 139 147 152 (Pubitemid 39535799)
103. Chemler J. A., Lim C. G., Daiss J. L., Koffas M. AG. A versatile microbial system for biosynthesis of novel polyphenols with altered estrogen receptor binding activity. Chem Biol: 2010; 17 392 401
104. Murata M., Midorikawa K., Koh M., Umezawa K., Kawanishi S. Genistein and daidzein induce cell proliferation and their metabolites cause oxidative DNA damage in relation to isoflavone-induced cancer of estrogen-sensitive organs. Biochemistry: 2004; 43 2569 2577 (Pubitemid 38327852)
105. Sotoca A. M., Bovee T. FH, Brand W., Velikova N., Boeren S., Murk A. J., Vervoort J., Rietjens I. M. Superinduction of estrogen receptor mediated gene expression in luciferase based reporter gene assays is mediated by a post-transcriptional mechanism. J Steroid Biochem Mol Biol: 2010; 122 204 211
106. Zych M., Folwarczna J., Trzeciak H. I. Natural phenolic acids may increase serum estradiol level in ovariectomized rats. Acta Biochim Pol: 2009; 56 503 507