Evaluation of Estrogenic Activity of Licorice Species in Comparison with Hops Used in Botanicals for Menopausal Symptoms

PLoS ONE

Volumn 8, Issue 7, 2013, Pages

  Hajirahimkhan, Atieh ^a   Simmler, Charlotte ^a   Yuan, Yang ^a   Anderson, Jeffrey R ^a   Chen, Shao Nong ^a   Nikolić, Dejan ^a   Dietz, Birgit M ^a   Pauli, Guido F ^a   van Breemen, Richard B ^a   Bolton, Judy L ^a  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

8 PHENYLNARINGENIN; ALKALINE PHOSPHATASE; ESTROGEN; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; GLYCYRRHIZA GLABRA EXTRACT; GLYCYRRHIZA INFLATA EXTRACT; GLYCYRRHIZA URALENSIS EXTRACT; HUMULUS LUPULUS EXTRACT; ISOLIQUIRITIGENIN; LIQUIRITIGENIN; MESSENGER RNA; PHYTOESTROGEN; PLANT EXTRACT; UNCLASSIFIED DRUG; XANTHOHUMOL;

ARTICLE; BINDING AFFINITY; CANCER CELL; CELL STRAIN MCF 7; COMPARATIVE STUDY; CONCENTRATION RESPONSE; CONTROLLED STUDY; DRUG MECHANISM; DRUG RECEPTOR BINDING; DRUG SCREENING; DRUG SELECTIVITY; DRUG STRUCTURE; ENDOMETRIUM CANCER; ENZYME ACTIVITY; ENZYME INDUCTION; ESTROGEN ACTIVITY; ESTROGEN RESPONSIVE ELEMENT; GENE; GENE INDUCTION; GLYCYRRHIZA; GLYCYRRHIZA GLABRA; GLYCYRRHIZA INFLATA; GLYCYRRHIZA URALENSIS; HUMULUS LUPULUS; IC 50; IN VITRO STUDY; ISOMERIZATION; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MENOPAUSAL SYNDROME; NONHUMAN; PLANT ROOT; TREFOIL FACTOR 1 GENE;

ALKALINE PHOSPHATASE; CELL DEATH; CELL LINE, TUMOR; CHALCONES; CHROMATOGRAPHY, LIQUID; ENZYME INDUCTION; FEMALE; FLAVANONES; GENE EXPRESSION REGULATION, NEOPLASTIC; GLYCYRRHIZA; HUMANS; HUMULUS; LIGANDS; LUCIFERASES; MASS SPECTROMETRY; MENOPAUSE; PHYTOESTROGENS; PLANT EXTRACTS; PLANT PREPARATIONS; PROTEIN BINDING; RECEPTORS, ESTROGEN; RNA, MESSENGER; TUMOR SUPPRESSOR PROTEINS; ULTRAFILTRATION;

EID: 84880080675     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0067947     Document Type: Article

References (60)

1. Minino AM (2011) Death in the United States, 2009. NCHS Data Brief: 1-8.
2. Barlow DH, (1997) Who understands the menopause? Br J Obstet Gynaecol 104: 879-880.
3. Shaver JL, Giblin E, Paulsen V, (1991) Sleep quality subtypes in midlife women. Sleep 14: 18-23.
4. Kronenberg F, (1994) Hot Flashes - Phenomenology, Quality-of-Life, and Search for Treatment Options. Experimental Gerontology 29: 319-336.
5. Shumaker SA, Legault C, Rapp SR, Thal L, Wallace RB, et al. (2003) Estrogen plus progestin and the incidence of dementia and mild cognitive impairment in postmenopausal women: the Women's Health Initiative Memory Study: a randomized controlled trial. JAMA 289: 2651-2662.
6. Wassertheil-Smoller S, Hendrix SL, Limacher M, Heiss G, Kooperberg C, et al. (2003) Effect of estrogen plus progestin on stroke in postmenopausal women - The Women's Health Initiative: A randomized trial. Jama-J Am Med Assoc 289: 2673-2684.
7. Rossouw JE, Anderson GL, Prentice RL, LaCroix AZ, Kooperberg C, et al. (2002) Risks and benefits of estrogen plus progestin in healthy postmenopausal women: principal results from the Women's Health Initiative randomized controlled trial. JAMA 288: 321-333.
8. Hajirahimkhan A, Dietz BM, Bolton JL (2013) Botanical modulation of menopausal symptoms: Mechanisms of action. Planta Med. In Press.
9. Salter S, Brownie S, (2010) Treating primary insomnia - the efficacy of valerian and hops. Aust Fam Physician 39: 433-437.
10. Blumenthal M, German Federal Institute for Drugs and Medical Devices, Commission E (2000) Herbal medicine: expanded Commission E monographs. Newton, MA: Integrative Medicine Communications. 519 p.
11. Overk CR, Guo J, Chadwick LR, Lantvit DD, Minassi A, et al. (2008) In vivo estrogenic comparisons of Trifolium pratense (red clover) Humulus lupulus (hops), and the pure compounds isoxanthohumol and 8-prenylnaringenin. Chem Biol Interact 176: 30-39.
12. Overk CR, Yao P, Chadwick LR, Nikolic D, Sun Y, et al. (2005) Comparison of the in vitro estrogenic activities of compounds from hops (Humulus lupulus) and red clover (Trifolium pratense). J Agric Food Chem 53: 6246-6253.
13. Liu J, Burdette JE, Xu H, Gu C, van Breemen RB, et al. (2001) Evaluation of estrogenic activity of plant extracts for the potential treatment of menopausal symptoms. J Agric Food Chem 49: 2472-2479.
14. Hemachandra LP, Madhubhani P, Chandrasena R, Esala P, Chen SN, et al. (2012) Hops (Humulus lupulus) inhibits oxidative estrogen metabolism and estrogen-induced malignant transformation in human mammary epithelial cells (MCF-10A). Cancer Prev Res 5: 73-81.
15. Dietz BM, Kang YH, Liu G, Eggler AL, Yao P, et al. (2005) Xanthohumol isolated from Humulus lupulus inhibits menadione-induced DNA damage through induction of quinone reductase. Chem Res Toxicol 18: 1296-1305.
16. Basly JP, Lavier MC, (2005) Dietary phytoestrogens: potential selective estrogen enzyme modulators? Planta Med 71: 287-294.
17. Roelens F, Heldring N, Dhooge W, Bengtsson M, Comhaire F, et al. (2006) Subtle side-chain modifications of the hop phytoestrogen 8-prenylnaringenin result in distinct agonist/antagonist activity profiles for estrogen receptors alpha and beta. J Med Chem 49: 7357-7365.
18. Diel P, Thomae RB, Caldarelli A, Zierau O, Kolba S, et al. (2004) Regulation of gene expression by 8-prenylnaringenin in uterus and liver of Wistar rats. Planta Med 70: 39-44.
19. Bolca S, Li J, Nikolic D, Roche N, Blondeel P, et al. (2010) Disposition of hop prenylflavonoids in human breast tissue. Mol Nutr Food Res 54: S284-294.
20. Wang ZY, Nixon DW, (2001) Licorice and cancer. Nutr Cancer 39: 1-11.
21. Geller SE, Studee L, (2005) Botanical and dietary supplements for menopausal symptoms: what works, what does not. J Womens Health 14: 634-649.
22. Taylor M, (2012) Complementary and alternative medicine preparations used to treat symptoms of menopause. Men Med 20: S1-S8.
23. Ju YH, Doerge DR, Helferich WG, (2008) A dietary supplement for female sexual dysfunction, Avlimil, stimulates the growth of estrogen-dependent breast tumors (MCF-7) implanted in ovariectomized athymic nude mice. Food Chem Toxicol 46: 310-320.
24. Costello CH, Lynn EV, (1950) Estrogenic substances from plants; glycyrrhiza. J Am Pharm Assoc Am Pharm Assoc 39: 177-180.
25. Mersereau JE, Levy N, Staub RE, Baggett S, Zogovic T, et al. (2008) Liquiritigenin is a plant-derived highly selective estrogen receptor beta agonist. Mol Cell Endocrinol 283: 49-57.
26. Maggiolini M, Statti G, Vivacqua A, Gabriele S, Rago V, et al. (2002) Estrogenic and antiproliferative activities of isoliquiritigenin in MCF7 breast cancer cells. J Steroid Biochem Mol Biol 82: 315-322.
27. Kondo K, Shiba M, Nakamura R, Morota T, Shoyama Y, (2007) Constituent properties of licorices derived from Glycyrrhiza uralensis, Glycyrrhiza glabra, or Glycyrrhiza inflata identified by genetic information. Biol Pharm Bull 30: 1271-1277.
28. Possemiers S, Bolca S, Grootaert C, Heyerick A, Decroos K, et al. (2006) The prenylflavonoid isoxanthohumol from hops (Humulus lupulus L.) is activated into the potent phytoestrogen 8-prenylnaringenin in vitro and in the human intestine. J Nutr 136: 1862-1867.
29. Possemiers S, Heyerick A, Robbens V, De Keukeleire D, Verstraete W, (2005) Activation of proestrogens from hops (Humulus lupulus L.) by intestinal microbiota; conversion of isoxanthohumol into 8-prenylnaringenin. J Agric Food Chem 53: 6281-6288.
30. Chadwick LR, Nikolic D, Burdette JE, Overk CR, Bolton JL, et al. (2004) Estrogens and congeners from spent hops (Humulus lupulus). J Nat Prod 67: 2024-2032.
31. Pauli GF, Jaki BU, Lankin DC, (2007) A routine experimental protocol for qHNMR illustrated with Taxol. J Nat Prod 70: 589-595.
32. Littlefield BA, Gurpide E, Markiewicz L, McKinley B, Hochberg RB, (1990) A simple and sensitive microtiter plate estrogen bioassay based on stimulation of alkaline phosphatase in Ishikawa cells: estrogenic action of delta 5 adrenal steroids. Endocrinology 127: 2757-2762.
33. Hata H, Holinka CF, Pahuja SL, Hochberg RB, Kuramoto H, et al. (1987) Estradiol metabolism in Ishikawa endometrial cancer cells. J Steroid Biochem 26: 699-704.
34. Pisha E, Pezzuto JM, (1997) Cell-based assay for the determination of estrogenic and anti-estrogenic activities. Methods Cell Sci 19: 37-43.
35. Gherezghiher TB, Michalsen B, Chandrasena RE, Qin Z, Sohn J, et al. (2012) The naphthol selective estrogen receptor modulator (SERM), LY2066948, is oxidized to an o-quinone analogous to the naphthol equine estrogen, equilenin. Chem-Biol Interact 196: 1-10.
36. Sun Y, Gu C, Liu X, Liang W, Yao P, et al. (2005) Ultrafiltration tandem mass spectrometry of estrogens for characterization of structure and affinity for human estrogen receptors. J Am Soc Mass Spectrom 16: 271-279.
37. Obourn JD, Koszewski NJ, Notides AC, (1993) Hormone- and DNA-binding mechanisms of the recombinant human estrogen receptor. Biochemistry 32: 6229-6236.
38. Catherino WH, Jordan VC, (1995) Increasing the number of tandem estrogen response elements increases the estrogenic activity of a tamoxifen analogue. Cancer Lett 92: 39-47.
39. Johnson BM, Nikolic D, van Breemen RB, (2002) Applications of pulsed ultrafiltration-mass spectrometry. Mass Spectrom Rev 21: 76-86.
40. Choi SY, Ha TY, Ahn JY, Kim SR, Kang KS, et al. (2008) Estrogenic activities of isoflavones and flavones and their structure-activity relationships. Planta Med 74: 25-32.
41. Kupfer R, Swanson L, Chow S, Staub RE, Zhang YL, et al. (2008) Oxidative in vitro metabolism of liquiritigenin, a bioactive compound isolated from the Chinese herbal selective estrogen beta-receptor agonist MF101. Drug Metab Dispos 36: 2261-2269.
42. Simmler C, Hajirahimkhan A, Lankin DC, Bolton JL, Jones T, et al. (2013) Dynamic residual complexity of the isoliquiritigenin-liquiritigenin interconversion during bioassay. J Agric Food Chem (in press).
43. Dong S, Inoue A, Zhu Y, Tanji M, Kiyama R, (2007) Activation of rapid signaling pathways and the subsequent transcriptional regulation for the proliferation of breast cancer MCF-7 cells by the treatment with an extract of Glycyrrhiza glabra root. Food Chem Toxicol 45: 2470-2478.
44. Lutomski J, (1983) [Chemistry and therapeutic use of licorice (Glycyrrhiza glabra L.)]. Pharm Unserer Zeit 12: 49-54.
45. Simons R, Vincken JP, Mol LA, The SA, Bovee TF, et al. (2011) Agonistic and antagonistic estrogens in licorice root (Glycyrrhiza glabra). Anal Bioanal Chem 401: 305-313.
46. Kensler TW, Wakabayashi N, (2010) Nrf2: friend or foe for chemoprevention? Carcinogenesis 31: 90-99.
47. Yuan X, Zhang B, Chen N, Chen XY, Liu LL, et al. (2012) Isoliquiritigenin treatment induces apoptosis by increasing intracellular ROS levels in HeLa cells. J Asian Nat Prod Res 14: 789-798.
48. Zhou GS, Song LJ, Yang B, (2013) Isoliquiritigenin inhibits proliferation and induces apoptosis of U87 human glioma cells in vitro. Mol Med Rep 7: 531-536.
49. Dietz BM, Bolton JL, (2011) Biological reactive intermediates (BRIs) formed from botanical dietary supplements. Chem Biol Interact 192: 72-80.
50. Cuendet M, Oteham CP, Moon RC, Pezzuto JM, (2006) Quinone reductase induction as a biomarker for cancer chemoprevention. J Nat Prod 69: 460-463.
51. Eggler AL, Liu G, Pezzuto JM, van Breemen RB, Mesecar AD, (2005) Modifying specific cysteines of the electrophile-sensing human Keap1 protein is insufficient to disrupt binding to the Nrf2 domain Neh2. Proc Natl Acad Sci USA 102: 10070-10075.
52. Calliste CA, Le Bail JC, Trouillas P, Pouget C, Habrioux G, et al. (2001) Chalcones: structural requirements for antioxidant, estrogenic and antiproliferative activities. Anticancer Res 21: 3949-3956.
53. Cuendet M, Guo J, Luo Y, Chen S, Oteham CP, et al. (2010) Cancer chemopreventive activity and metabolism of isoliquiritigenin, a compound found in licorice. Cancer Prev Res 3: 221-232.
54. Cisak A, Mielczarek C, (1992) Practical and theoretical aspects of flavanone chalcone isomerizations. J Chem Soc Perk T 2: 1603-1607.
55. Nudelman NS, Furlong JJP, (1991) Conversion of flavanones into chalcones in alkaline-medium - kinetic and spectroscopic studies. J Phys Org Chem 4: 263-270.
56. Andujar SA, Filippa MA, Ferretti FH, Blanco SE, (2003) Isomerization of 4′-methoxy-flavanone in alkaline medium. Determination of the enolate formation constant. J Mol Struc-Theochem 636: 157-166.
57. Yamin LJ, Blanco SE, Luco JM, Ferretti FH, (1997) Theoretical study of cyclization of 2′-hydroxychalcone. Theochem-J Mol Struc 390: 209-215.
58. Kang HE, Sohn SI, Baek SR, Lee JW, Lee MG, (2011) Effects of acute renal failure induced by uranyl nitrate on the pharmacokinetics of liquiritigenin and its two glucuronides, M1 and M2, in rats. J Pharm Pharmacol 63: 49-57.
59. Gustafsson JA, (1999) Estrogen receptor beta - a new dimension in estrogen mechanism of action. J Endocrinol 163: 379-383.
60. MacGregor JI, Jordan VC, (1998) Basic guide to the mechanisms of antiestrogen action. Pharmacol Rev 50: 151-196.