Red clover isoflavones biochanin A and formononetin are potent ligands of the human aryl hydrocarbon receptor

Journal of Steroid Biochemistry and Molecular Biology

Volumn 108, Issue 1-2, 2008, Pages 171-177

  Medjakovic, S ^a,b   Jungbauer, A ^a,b  

^a UNIVERSITY OF NATURAL RESOURCES AND LIFE SCIENCES   (Austria)

^b INSTITUTE FOR MICROELECTRONICS   (Austria)

Author keywords

AhR; Aryl hydrocarbon receptor; Biochanin A; Formononetin; Indole compounds; Isoflavones

Indexed keywords

3 INDOLEMETHANOL; BIOCHANIN A; ESTROGEN RECEPTOR ALPHA; FORMONONETIN; HYDROCARBON RECEPTOR; INDOLE DERIVATIVE; ISOFLAVONE DERIVATIVE; LIGAND; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CANCER PREVENTION; CANCER THERAPY; CELL CYCLE; CONTROLLED STUDY; MENOPAUSAL SYNDROME; NONHUMAN; RECEPTOR INTRINSIC ACTIVITY; RED CLOVER;

DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ESTROGENS; GENISTEIN; HUMANS; ISOFLAVONES; LIGANDS; PHYTOESTROGENS; RECEPTORS, ARYL HYDROCARBON; SACCHAROMYCES CEREVISIAE; TRIFOLIUM;

TRIFOLIUM PRATENSE;

EID: 38649111292     PISSN: 09600760     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsbmb.2007.10.001     Document Type: Article

References (49)

1. Poland A., Glover E., and Kende A.S. Stereospecific, high affinity binding of 2,3,7,8-tetrachlorodibenzo-p-dioxin by hepatic cytosol: evidence that the binding species is receptor for induction of aryl hydrocarbon hydroxylase. J. Biol. Chem. 251 16 (1976) 4936-4946
2. Adachi J., Mori Y., Matsui S., Takigami H., Fujino J., Kitagawa H., Matsuda T., Miller Iii C.A., Kato T., and Saeki K. Indirubin and indigo are potent aryl hydrocarbon receptor ligands present in human urine. J. Biol. Chem. 276 34 (2001) 31475
3. Heath-Pagliuso S., Rogers W.J., Tullis K., Seidel S.D., Denison M.S., Cenijn P.H., and Brouwer A. Activation of the Ah receptor by tryptophan and tryptophan metabolites. Biochemistry 37 33 (1998) 11508
4. Miller Iii C.A. Expression of the human aryl hydrocarbon receptor complex in yeast. Activation of transcription by indole compounds. J. Biol. Chem. 272 52 (1997) 32824
5. Oesch-Bartlomowicz B., Huelster A., Wiss O., Antoniou-Lipfert P., Dietrich C., Arand M., Weiss C., Bockamp E., and Oesch F. Aryl hydrocarbon receptor activation by cAMP vs. dioxin: divergent signaling pathways. Proc. Natl. Acad. Sci. U.S.A. 102 26 (2005) 9218
6. Rannug U., Rannug A., Sjoberg U., Li H., Westerholm R., and Bergman J. Structure elucidation of two tryptophan-derived, high affinity Ah receptor ligands. Chem. Biol. 2 12 (1995) 841-845
7. Savouret J.F., Antenos M., Quesne M., Xu J., Milgrom E., and Casper R.F. 7-Ketocholesterol is an endogenous modulator for the arylhydrocarbon receptor. J. Biol. Chem. 276 5 (2001) 3054-3059 Epub 2000 October 3020
8. Song J., Clagett-Dame M., Peterson R.E., Hahn M.E., Westler W.M., Sicinski R.R., and DeLuca H.F. A ligand for the aryl hydrocarbon receptor isolated from lung. Proc.Natl. Acad. Sci. U.S.A. 99 23 (2002) 14694
9. Vasquez A., Atallah-Yunes N., Smith F.C., You X., Chase S.E., Silverstone A.E., and Vikstrom K.L. A role for the aryl hydrocarbon receptor in cardiac physiology and function as demonstrated by AhR knockout mice. Cardiovas. Toxicol. 3 2 (2003) 153-163
10. Harstad E.B., Guite C.A., Thomae T.L., and Bradfield C.A. Liver deformation in Ahr-null mice: evidence for aberrant hepatic perfusion in early development. Mol. Pharmacol. 69 5 (2006) 1534-1541
11. Schmidt J.V., Su G.H.T., Reddy J.K., Simon M.C., and Bradfield C.A. Characterization of a murine Ahr null allele: involvement of the Ah receptor in hepatic growth and development. Proc.Natl. Acad. Sci. U.S.A. 93 13 (1996) 6731-6736
12. Benedict J.C., Lin T.M., Loeffler I.K., Peterson R.E., and Flaws J.A. Physiological role of the aryl hydrocarbon receptor in mouse ovary development. Toxicol. Sci. 56 2 (2000) 382-388
13. Gonzalez F.J., Fernandez-Salguero P., Lee S.S.T., Pineau T., and Ward J.M. Xenobiotic receptor knockout mice. Toxicol. Lett. 82/83 (1995) 117-121
14. Baba T., Mimura J., Nakamura N., Harada N., Yamamoto M., Morohashi K.I., and Fujii-Kuriyama Y. Intrinsic function of the aryl hydrocarbon (dioxin) receptor as a key factor in female reproduction. Mol. Cell. Biol. 25 22 (2005) 10040-10051
15. Pocar P., Fischer B., Klonisch T., and Hombach-Klonisch S. Molecular interactions of the aryl hydrocarbon receptor and its biological and toxicological relevance for reproduction. Reproduction 129 4 (2005) 379-389
16. Puga A., Xia Y., and Elferink C. Role of the aryl hydrocarbon receptor in cell cycle regulation. Chem. Biol. Inter. 141 1/2 (2002) 117-130
17. Zaher H., Fernandez-Salguero P.M., Letterio J., Sheikh M.S., Fornace Jr. A.J., Roberts A.B., and Gonzalez F.J. The involvement of aryl hydrocarbon receptor in the activation of transforming growth factor-b and apoptosis. Mol. Pharmacol. 54 2 (1998) 313-321
18. Amakura Y., Tsutsumi T., Sasaki K., Maitani T., and Yoshida T. Screening of the inhibitory effect of vegetable constituents on the aryl hydrocarbon receptor-mediated activity induced by 2,3,7,8-tetrachlorodibenzo-p-dioxin. Biol. Pharm. Bull. 26 12 (2003) 1754
19. Amakura Y., Tsutsumi T., Sasaki K., Maitani T., Nakamura M., Kitagawa H., Fujino J., Toyoda M., and Yoshida T. Activation of the aryl hydrocarbon receptor by some vegetable constituents determined using in vitro reporter gene assay. Biol. Pharm. Bull. 26 4 (2003) 532
20. Zhang S., Qin C., and Safe S.H. Flavonoids as aryl hydrocarbon receptor agonists/antagonists: effects of structure and cell context. Environ. Health Perspect. 111 16 (2003) 1877
21. Ashida H. Suppressive effects of flavonoids on dioxin toxicity. BioFactors 12 1-4 (2000) 201
22. Revel A., Raanani H., Younglai E., Xu J., Han R., Savouret J.F., and Casper R.F. Resveratrol, a natural aryl hydrocarbon receptor antagonist, protects sperm from DNA damage and apoptosis caused by benzo(a)pyrene. Reprod. Toxicol. 15 5 (2001) 479-486
23. Singh S.U.N., Casper R.F., Fritz P.C., Sukhu B., Ganss B., Girard Jr. B., Savouret J.F., and Tenenbaum H.C. Inhibition of dioxin effects on bone formation in vitro by a newly described aryl hydrocarbon receptor antagonist, resveratrol. J. Endocrinol. 167 1 (2000) 183-195
24. Chen I., McDougal A., Wang F., and Safe S. Aryl hydrocarbon receptor-mediated antiestrogenic and antitumorigenic activity of diindolylmethane. Carcinogenesis 19 9 (1998) 1631-1639
25. Baumgart A., Schmidt M., Schmitz H.J., and Schrenk D. Natural furocoumarins as inducers and inhibitors of cytochrome P450 1A1 in rat hepatocytes. Biochem. Pharmacol. 69 4 (2005) 657-667
26. Safe S., Wormke M., and Samudio I. Mechanisms of inhibitory aryl hydrocarbon receptor-estrogen receptor crosstalk in human breast cancer cells. J. Mammary Gland Biol. Neoplasia 5 3 (2000) 295
27. Hayes C.L., Spink D.C., Spink B.C., Cao J.Q., Walker N.J., and Sutter T.R. 17β-Estradiol hydroxylation catalyzed by human cytochrome P450 1B1. Proc. Natl. Acad. Sci. U.S.A. 93 18 (1996) 9776-9781
28. Michnovicz J.J., Adlercreutz H., and Bradlow H.L. Changes in levels of urinary estrogen metabolites after oral indole-3- carbinol treatment in humans. J. Natl. Cancer Ins. 89 10 (1997) 718-723
29. Niwa T., Swaneck G., and Bradlow H.L. Alterations in estradiol metabolism in MCF-7 cells induced by treatment with indole-3-carbinol and related compounds. Steroids 59 9 (1994) 523-527
30. Bemanian V., Male R., and Goksøyr A. The aryl hydrocarbon receptor-mediated disruption of vitellogenin synthesis in the fish liver: cross-talk between AHR- and ERa-signalling pathways. Comp. Hepatol. 3 (2004)
31. Wormke M., Castro-Rivera E., Chen I., and Safe S. Estrogen and aryl hydrocarbon receptor expression and crosstalk in human Ishikawa endometrial cancer cells. J. Steroid Biochem. Mol. Biol. 72 5 (2000) 197
32. Kharat I., and Saatcioglu F. Antiestrogenic effects of 2,3,7,8-tetrachlorodibenzo-p-dioxin are mediated by direct transcriptional interference with the liganded estrogen receptor: cross-talk between aryl hydrocarbon- and estrogen-mediated signaling. J.Biol. Chem. 271 18 (1996) 10533-10537
33. Chedraui P., Hidalgo L., San Miguel G., Morocho N., and Ross S. Red clover extract (MF11RCE) supplementation and postmenopausal vaginal and sexual health. Int. J. Gynaecol. Obstet. 95 3 (2006) 296-297 Epub 2006 September 2027
34. Hidalgo L.A., Chedraui P.A., Morocho N., Ross S., and San Miguel G. The effect of red clover isoflavones on menopausal symptoms, lipids and vaginal cytology in menopausal women: a randomized, double-blind, placebo-controlled study. Gynecol. Endocrinol. 21 5 (2005) 257-264
35. Imhof M., Gocan A., Reithmayr F., Lipovac M., Schimitzek C., Chedraui P., and Huber J. Effects of a red clover extract (MF11RCE) on endometrium and sex hormones in postmenopausal women. Maturitas 55 1 (2006) 76-81 Epub 2006 March 2002
36. Miller III C.A. A human aryl hydrocarbon receptor signaling pathway constructed in yeast displays additive responses to ligand mixtures. Toxicol. Appl. Pharmacol. 160 3 (1999) 297-303
37. Kippert F. A rapid permeabilization procedure for accurate quantitative determination of beta-galactosidase activity in yeast cells. FEMS Microbiol. Lett. 128 2 (1995) 201-206
38. Jungbauer A., and Beck V. Yeast reporter system for rapid determination of estrogenic activity. J. Chromatogr. B: Anal. Technol. Biomed. Life Sci. 777 1/2 (2002) 167
39. Safe S., and Wormke M. Inhibitory aryl hydrocarbon receptor-estrogen receptor a cross-talk and mechanisms of action. Chem. Res. Toxicol. 16 7 (2003) 807-816
40. Kawanishi M., Sakamoto M., Kishi K., Yagi T., and Ito A. Construction of reporter yeasts for mouse aryl hydrocarbon receptor ligand activity. Mutat. Res. Gen. Toxicol. Environ. Mutagen. 540 1 (2003) 99
41. Duncan A.M., Merz-Demlow B.E., Xu X., Phipps W.R., and Kurzer M.S. Premenopausal equol excretors show plasma hormone profiles associated with lowered risk of breast cancer. Cancer Epidemiol. Biomarkers Prev. 9 6 (2000) 581-586
42. Han E.H., Ji Y.K., and Hye G.J. Effect of biochanin A on the aryl hydrocarbon receptor and cytochrome P450 1A1 in MCF-7 human breast carcinoma cells. Arch. Pharm. Res. 29 7 (2006) 570-576
43. Sakakibara H., Viala D., Ollier A., Combeau A., and Besle J.M. Isoflavones in several clover species and in milk from goats fed clovers. BioFactors (Oxford England) 22 1-4 (2004) 237
44. Kostelac D., Briviba K., and Rechkemmer G. Phytoestrogens modulate binding response of estrogen receptors a and b to the estrogen response element. J. Agric. Food Chem. 51 26 (2003) 7632
45. Promberger A., Schmid E.R., Dornstauder E., Frühwirth C., and Jungbauer A. Determination of estrogenic activity in beer by biological and chemical means. J. Agric. Food Chem. 49 2 (2001) 633
46. Shen P., Liu M.H., Ng T.Y., Chan Y.H., and Yong E.L. Differential effects of isoflavones, from Astragalus membranaceus and Pueraria thomsonii, on the activation of PPARa, PPARg, and adipocyte differentiation in vitro. J. Nutr. 136 4 (2006) 899-905
47. Lee Y.S., Seo J.S., Chung H.T., and Jang J.J. Inhibitory effects of biochanin A on mouse lung tumor induced by benzo(a)pyrene. J. Kor. Med. Sci. 6 4 (1991) 325
48. Cassady J.M., Zennie T.M., Chae Y.H., Ferin M.A., Portuondo N.E., and Baird W.M. Use of a mammalian cell culture benzo(a)pyrene metabolism assay for the detection of potential anticarcinogens from natural products: inhibition of metabolism by biochanin A, an isoflavone from Trifolium pratense L. Cancer Res. 48 22 (1988) 6257-6261
49. Safe S., and McDougal A. Mechanism of action and development of selective aryl hydrocarbon receptor modulators for treatment of hormone-dependent cancers (review). Int. J. Oncol. 20 6 (2002) 1123