Effects of the natural endocrine disruptor equol on the pituitary function in adult male rats

Toxicology

Volumn 304, Issue , 2013, Pages 69-75

  Loutchanwoot, Panida ^a,b   Srivilai, Prayook ^a   Jarry, Hubertus ^c  

^a MAHASARAKHAM UNIVERSITY   (Thailand)

^b BURAPHA UNIVERSITY   (Thailand)

^c UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Endocrine disruptor; Equol; Male rat; MRNA expression; Pituitary

Indexed keywords

ANDROGEN; ANTIANDROGEN; EQUOL; ESTROGEN; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; FLUTAMIDE; GONADORELIN RECEPTOR; LUTEINIZING HORMONE; LUTEINIZING HORMONE BETA SUBUNIT; MESSENGER RNA; OLIVE OIL; PROLACTIN; TRUNCATED ESTROGEN RECEPTOR PRODUCT 1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DRUG EXPOSURE; ESTROGEN ACTIVITY; GENE EXPRESSION; HORMONE BLOOD LEVEL; HYPOPHYSIS FUNCTION; IN VIVO STUDY; MALE; NONHUMAN; PRIORITY JOURNAL; RADIOIMMUNOASSAY; RAT; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADMINISTRATION, ORAL; ANIMALS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENDOCRINE DISRUPTORS; EQUOL; FLUTAMIDE; GENE EXPRESSION REGULATION; LUTEINIZING HORMONE; MALE; PITUITARY GLAND; PITUITARY HORMONES; PROLACTIN; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, ANDROGEN; RECEPTORS, ESTROGEN; REPRODUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER;

ANIMALIA; RATTUS;

EID: 84871817647     PISSN: 0300483X     EISSN: 18793185     Source Type: Journal    
DOI: 10.1016/j.tox.2012.11.017     Document Type: Article

References (56)

1. Acerini C.L., Hughes I.A. Endocrine disrupting chemicals: a new and emerging public health problem?. Arch. Dis. Child. 2006, 91:633-641.
2. Andrews P., Freyberger A., Hartmann E., Eiben R., Loof I., Schmidt U., Temerowski M., Becka M. Feasibility and potential gains of enhancing the subacute rat study protocol (OECD test guideline no. 407) by additional parameters selected to determine endocrine modulation. A pre-validation study to determine endocrine-mediated effects of the antiandrogenic drug flutamide. Arch. Toxicol. 2001, 75:65-73.
3. Andrews P., Freyberger A., Hartmann E., Eiben R., Loof I., Schmidt U., Temerowski M., Folkerts A., Stahl B., Kayser M. Sensitive detection of the endocrine effects of the estrogen analogue ethinylestradiol using a modified enhanced subacute rat study protocol (OECD test guideline no. 407). Arch. Toxicol. 2002, 75:194-202.
4. Bovee T.F., Schoonen W.G., Hamers A.R., Bento M.J., Peijnenburg A.A. Screening of synthetic and plant-derived compounds for (anti)estrogenic and (anti)androgenic activities. Anal. Bioanal. Chem. 2008, 390:1111-1119.
5. Bowey E., Adlercreutz H., Rowland I. Metabolism of isoflavones and lignans by the gut microflora: a study in germ-free and human flora associated rats. Food Chem. Toxicol. 2003, 41:631-636.
6. Brown N.M., Belles C.A., Lindley S.L., Zimmer-Nechemias L., Witte D.P., Kim M., Setchell K.D.R. Mammary gland differentiation by early life exposure to enantiomers of the soy isoflavone metabolite equol. Food Chem. Toxicol. 2010, 48:3042-3050.
7. Christoffel J., Rimoldi G., Wuttke W. Effects of 8-prenylnaringenin on the hypothalamo-pituitary-uterine axis in rats after 3-month treatment. J. Endocrinol. 2006, 188:397-405.
8. Dalkin A.C., Haisenleder D.J., Ortolano G.A., Ellis T.R., Marshall J.C. The frequency of gonadotropin-releasing-hormone stimulation differentially regulates gonadotropin subunit messenger ribonucleic acid expression. Endocrinology 1989, 125:917-924.
9. Dalkin A.C., Burger L.L., Aylor K.W., Haisenleder D.J., Workman L.J., Cho S., Marshall J.C. Regulation of gonadotropin subunit gene transcription by gonadotropin-releasing hormone: measurement of primary transcript ribonucleic acids by quantitative reverse transcription-polymerase chain reaction assays. Endocrinology 2001, 142:139-146.
10. Friend K.E., Resnick E.M., Ang L.W., Shupnik M.A. Specific modulation of estrogen receptor mRNA isoforms in rat pituitary throughout the estrous cycle and in response to steroid hormones. Mol. Cell. Endocrinol. 1997, 131:147-155.
11. Giguere V., Meunier H., Veilleux R., Labrie F. Direct effects of sex steroids on prolactin release at the anterior pituitary level: interactions with dopamine, thyrotropin-releasing hormone, and isobutylmethylxanthine. Endocrinology 1982, 111:857-862.
12. Hedlund T.E., Johannes W.U., Miller G.J. Soy isoflavonoid equol modulates the growth of benign and malignant prostatic epithelial cells in vitro. Prostate 2003, 54:68-78.
13. Hedlund T.E., van Bokhoven A., Johannes W.U., Nordeen S.K., Ogden L.G. Prostatic fluid concentrations of isoflavonoids in soy consumers are sufficient to inhibit growth of benign and malignant prostatic epithelial cells in vitro. Prostate 2006, 66:557-566.
14. Jarry H., Christoffel J., Rimoldi G., Koch L., Wuttke W. Multi-organic endocrine disrupting activity of the UV screen benzophenone 2 (BP2) in ovariectomized adult rats after 5 days treatment. Toxicology 2004, 205:87-93.
15. Jordan V.C., Lieberman M.E. Estrogen-stimulated prolactin synthesis in vitro. Classification of agonist, partial agonist, and antagonist actions based on structure. Mol. Pharmacol. 1984, 26:279-285.
16. Ju Y.H., Fultz J., Allred K.F., Doerge D.R., Helferich W.G. Effects of dietary daidzein and its metabolite, equol, at physiological concentrations on the growth of estrogen-dependent human breast cancer (MCF-7) tumors implanted in ovariectomized athymic mice. Carcinogenesis 2006, 27:856-863.
17. Kaiser U.B., Jakubowiak A., Steinberger A., Chin W.W. Differential effects of gonadotropin-releasing hormone (GnRH) pulse frequency on gonadotropin subunit and GnRH receptor messenger ribonucleic acid levels in vitro. Endocrinology 1997, 138:1224-1231.
18. Kelce W.R., Wilson E.M. Environmental antiandrogens: developmental effects, molecular mechanisms, and clinical implications. J. Mol. Med. (Berl.) 1997, 75:198-207.
19. Kolle S.N., Melching-Kollmuss S., Krennrich G., Landsiedel R., van Ravenzwaay B. Assessment of combinations of antiandrogenic compounds vinclozolin and flutamide in a yeast based reporter assay. Regul. Toxicol. Pharmacol. 2011, 60:373-380.
20. Kubota K., Ohsako S., Kurosawa S., Takeda K., Qing W., Sakaue M., Kawakami T., Ishimura R., Tohyama C. Effects of vinclozolin administration on sperm production and testosterone biosynthetic pathway in adult male rat. J. Reprod. Dev. 2003, 49:403-412.
21. Kunimatsu T., Yamada T., Miyata K., Yabushita S., Seki T., Okuno Y., Matsuo M. Evaluation for reliability and feasibility of the draft protocol for the enhanced rat 28-day subacute study (OECD guideline 407) using androgen antagonist flutamide. Toxicology 2004, 200:77-89.
22. Larionov A., Krause A., Miller W. A standard curve based method for relative real time PCR data processing. BMC Bioinformatics 2005, 6:62.
23. Lehmann L., Esch H.L., Wagner J., Rohnstock L., Metzler M. Estrogenic and genotoxic potential of equol and two hydroxylated metabolites of Daidzein in cultured human Ishikawa cells. Toxicol. Lett. 2005, 158:72-86.
24. Leonhardt S., Shahab M., Luft H., Wuttke W., Jarry H. Reduction of luteinizing hormone secretion induced by long-term feed restriction in male rats is associated with increased expression of GABA-synthesizing enzymes without alterations of GnRH gene expression. J. Neuroendocrinol. 1999, 11:613-619.
25. Lieberman M.E., Maurer R.A., Claude P., Wiklund J., Wertz N., Gorski J. Regulation of pituitary growth and prolactin gene expression by estrogen. Adv. Exp. Med. Biol. 1981, 138:151-163.
26. Liu H., Du J., Hu C., Qi H., Wang X., Wang S., Liu Q., Li Z. Delayed activation of extracellular-signal-regulated kinase 1/2 is involved in genistein- and equol-induced cell proliferation and estrogen-receptor-alpha-mediated transcription in MCF-7 breast cancer cells. J. Nutr. Biochem. 2010, 21:390-396.
27. Loutchanwoot P., Wolfgang W., Hubertus J. Effects of a 5-day treatment with vinclozolin on the hypothalamo-pituitary-gonadal axis in male rats. Toxicology 2008, 243:105-115.
28. Lund T.D., Munson D.J., Haldy M.E., Setchell K.D., Lephart E.D., Handa R.J. Equol is a novel anti-androgen that inhibits prostate growth and hormone feedback. Biol. Reprod. 2004, 70:1188-1195.
29. Lund T.D., Blake C., Bu L., Hamaker A.N., Lephart E.D. Equol an isoflavonoid: potential for improved prostate health, in vitro and in vivo evidence. Reprod. Biol. Endocrinol. 2011, 9:4-9.
30. Mitchner N.A., Garlick C., Ben-Jonathan N. Cellular distribution and gene regulation of estrogen receptors alpha and beta in the rat pituitary gland. Endocrinology 1998, 139:3976-3983.
31. Molina-Molina J.M., Hillenweck A., Jouanin I., Zalko D., Cravedi J.P., Fernandez M.F., Pillon A., Nicolas J.C., Olea N., Balaguer P. Steroid receptor profiling of vinclozolin and its primary metabolites. Toxicol. Appl. Pharmacol. 2006, 216:44-54.
32. Morton M.S., Arisaka O., Miyake N., Morgan L.D., Evans B.A. Phytoestrogen concentrations in serum from Japanese men and women over forty years of age. J. Nutr. 2002, 132:3168-3171.
33. Muthyala R.S., Ju Y.H., Sheng S., Williams L.D., Doerge D.R., Katzenellenbogen B.S., Helferich W.G., Katzenellenbogen J.A. Equol, a natural estrogenic metabolite from soy isoflavones: convenient preparation and resolution of R- and S-equols and their differing binding and biological activity through estrogen receptors alpha and beta. Bioorg. Med. Chem. 2004, 12:1559-1567.
34. Nedvidkova J., Haluzik M., Pacak K., Schreiber V., Starka L. Estrogenic effect of estradiol-sulfamate on the male rat anterior pituitary. J. Steroid Biochem. Mol. Biol. 1998, 67:359-362.
35. Neri R. Pharmacology and pharmacokinetics of flutamide. Urology 1989, 34:19-21. discussion 46-56.
36. Neumann F., Topert M. Pharmacology of antiandrogens. J. Steroid Biochem. 1986, 25:885-895.
37. Norwitz E.R., Jeong K.H., Chin W.W. Molecular mechanisms of gonadotropin-releasing hormone receptor gene regulation. J. Soc. Gynecol. Investig. 1999, 6:169-178.
38. O'Connor J.C., Cook J.C., Slone T.W., Makovec G.T., Frame S.R., Davis L.G. An ongoing validation of a Tier I screening battery for detecting endocrine-active compounds (EACs). Toxicol. Sci. 1998, 46:45-60.
39. O'Connor J.C., Frame S.R., Biegel L.B., Cook J.C., Davis L.G. Sensitivity of a Tier I screening battery compared to an in utero exposure for detecting the estrogen receptor agonist 17 beta-estradiol. Toxicol. Sci. 1998, 44:169-184.
40. O'Connor J.C., Frame S.R., Ladics G.S. Evaluation of a 15-day screening assay using intact male rats for identifying antiandrogens. Toxicol. Sci. 2002, 69:92-108.
41. Ohsako S., Kubota K., Kurosawa S., Takeda K., Qing W., Ishimura R., Tohyama C. Alterations of gene expression in adult male rat testis and pituitary shortly after subacute administration of the antiandrogen flutamide. J. Reprod. Dev. 2003, 49:275-290.
42. Rachoń D., Vortherms T., Seidlová-Wuttke D., Wuttke W. Effects of dietary equol on the pituitary of the ovariectomized rats. Horm. Metab. Res. 2007, 39:256-261.
43. Rachoń D., Vortherms T., Seidlová-Wuttke D., Menche A., Wuttke W. Uterotropic effects of dietary equol administration in ovariectomized Sprague-Dawley rats. Climacteric 2007, 10:416-426.
44. Roth C., Schricker M., Lakomek M., Strege A., Heiden I., Luft H., Munzel U., Wuttke W., Jarry H. Autoregulation of the gonadotropin-releasing hormone (GnRH) system during puberty: effects of antagonistic versus agonistic GnRH analogs in a female rat model. J. Endocrinol. 2001, 169:361-371.
45. Sathyamoorthy N., Wang T.T. Differential effects of dietary phyto-oestrogens daidzein and equol on human breast cancer MCF-7 cells. Eur. J. Cancer 1997, 33:2384-2389.
46. Scippo M.L., Argiris C., Van De Weerdt C., Muller M., Willemsen P., Martial J., Maghuin-Rogister G. Recombinant human estrogen, androgen and progesterone receptors for detection of potential endocrine disruptors. Anal. Bioanal. Chem. 2004, 378:664-669.
47. Selvaraj V., Zakroczymski M.A., Naaz A., Mukai M., Ju Y.H., Doerge D.R., Katzenellenbogen J.A., Helferich W.G., Cooke P.S. Estrogenicity of the isoflavone metabolite equol on reproductive and non-reproductive organs in mice. Biol. Reprod. 2004, 71:966-972.
48. Setchell K.D.R., Clerici C. Equol: history, chemistry, and formation. J. Nutr. 2010, 140:1355S-1362S.
49. Setchell K.D.R., Clerici C. Equol: pharmacokinetics and biological actions. J. Nutr. 2010, 140:1363S-1368S.
50. Sonnenschein C., Soto A.M. An updated review of environmental estrogen and androgen mimics and antagonists. J. Steroid Biochem. Mol. Biol. 1998, 65:143-150.
51. Tena-Sempere M., Barreiro M.L., Gonzalez L.C., Pinilla L., Aguilar E. Differential neonatal imprinting and regulation by estrogen of estrogen receptor subtypes alpha and beta and of the truncated estrogen receptor product (TERP-1) mRNA expression in the male rat pituitary. Neuroendocrinology 2001, 74:347-358.
52. Tena-Sempere M., Gonzalez L.C., Pinilla L., Huhtaniemi I., Aguilar E. Neonatal imprinting and regulation of estrogen receptor alpha and beta mRNA expression by estrogen in the pituitary and hypothalamus of the male rat. Neuroendocrinology 2001, 73:12-25.
53. Tong Y., Simard J., Labrie C., Zhao H.F., Labrie F., Pelletier G. Inhibitory effect of androgen on estrogen-induced prolactin messenger ribonucleic acid accumulation in the male rat anterior pituitary gland. Endocrinology 1989, 125:1821-1828.
54. Wood C.E., Appt S.E., Clarkson T.B., Franke A.A., Lees C.J., Doerge D.R., Cline J.M. Effects of high-dose soy isoflavones and equol on reproductive tissues in female cynomolgus monkeys. Biol. Reprod. 2006, 75:477-486.
55. Yu W.J., Lee B.J., Nam S.Y., Ahn B., Hong J.T., Do J.C., Kim Y.C., Lee Y.S., Yun Y.W. Reproductive disorders in pubertal and adult phase of the male rats exposed to vinclozolin during puberty. J. Vet. Med. Sci. 2004, 66:847-853.
56. Yuan J.P., Wang J.H., Liu X. Metabolism of dietary soy isoflavones to equol by human intestinal microflora - implications for health. Mol. Nutr. Food Res. 2007, 51:765-781.