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Reproductive Medicine and Biology

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01-01-2014 | Original Article

Simple, sensitive and reliable in vivo assays to evaluate the estrogenic activity of endocrine disruptors

Authors: Kanya Anukulthanakorn, Sukanya Jareonporn, Suchinda Malaivijitnond

Published in: Reproductive Medicine and Biology | Issue 1/2014

Abstract

Purpose

We compared three in vivo assays, determining changes of body weight, and uterotropic and vaginal cytology assays, for the evaluation of estrogenic activity of an estrogen disrupting compound, Pueraria mirifica (PM), in comparison with 17β-estradiol (E).

Methods

Female rats were ovariectomized and gavaged with distilled water, 0.01, 0.1, 1, 10 and 20 mg/kg BW/day of E and 100 and 1,000 mg/kg BW/day of PM for 14 days. Body weights were measured weekly, and vaginal epithelium cells were monitored daily. The uterus was dissected at the end of the treatment period, weighed and examined for histomorphometry.

Results

There were a decrease in body weight and an increase in uterine weight, uterine, endometrium and myometrium areas, uterine gland numbers, and percent of cornified cell which were dependent on doses of E and PM treatments.

Conclusions

Of the three assays proposed, although all are reliable and had critical read-out, measurements of body and uterine weights is likely convenient and simple, but the uterotropic assay needs to kill the animals. Vaginal cytology assay appears most promising for sensitivity and shortening the duration of the assay. Compared to those of E, the estrogenic activity of PM at concentrations of 100 and 1,000 mg/kg BW was in the range of 14 to >20 mg/kg BW.

Propper C. The study of endocrine-disrupting compounds: past approaches and new directions. Integr Comp Biol. 2005;45:194–200.PubMedCrossRef

Gore AC. Endocrine-disrupting chemicals: from basic research to clinical practice. New Jersey: Humana Press; 2007.CrossRef

Soule HD, Vazquez A, Long A, Albert S, Brennan MA. Human cell line from a pleural effusion derived from a breast cancer. J Nat Cancer Inst. 1973;51:1409–13.PubMed

Cherdshewasart W, Traisup V, Picha P. Determination of the estrogenic activity of wild phytoestrogen-rich Pueraria mirifica by MCF-7 proliferation assay. J Reprod Dev. 2008;54:63–7.PubMedCrossRef

Chershewasart W, Cheewasopit W, Picha P. The differential anti-proliferation effect of white (Pueraria mirifica), red (Butea superba), and black (Mucuna collettii) Kwao Krua plants on the growth of MCF-7 cells. J Ethnopharmacol. 2004;93:255–60.CrossRef

Lee YS, Park JS, Cho SD, Son JK, Cherdshewasart W, Kang KS. Requirement of metabolic activation for estrogenic activity of Pueraria mirifica. J Vet Sci. 2002;3:273–7.PubMed

Okamura S, Sawada Y, Satoh T, Sakamoto H, Saito Y, Sumino H, et al. Pueraria mirifica phytoestrogens improve dyslipidemia in postmenopausal women probably by activating estrogen receptor subtypes. Tohoku J Exp Med. 2008;216:341–51.PubMedCrossRef

Boonchird C, Mahapanichkul T, Cherdshewasart W. Differential binding with ERα and ERβ of the phytoestrogen-rich plant Pueraria mirifica. Braz J Med Biol Res. 2010;43:195–200.PubMedCrossRef

Gray LE, Wilson V, Noriega N, Lambright C, Furr J, Stoker TE, et al. Use of the laboratory rat as a model in endocrine disruptor screening and testing. ILAR J. 2004;45:425–37.PubMedCrossRef

10.

Malaivijitnond S, Kiatthaipipat P, Cherdshewasart W, Watanabe G, Taya K. Different effects of Pueraria mirifica, an herb containing phytoestrogens, on LH and FSH secretion in gonadectomized female and male rats. J Pharmacol Sci. 2004;96:428–35.PubMedCrossRef

11.

Malaivijitnond S, Chansri K, Kijkuokul P, Urasopon N, Cherdshewasart W. Using vaginal cytology to assess the estrogenic activity of phytoestrogen-rich herb. J Ethnopharmacol. 2006;107:354–60.PubMedCrossRef

12.

Cherdshewasart W, Kitsamai Y, Malaivijitnond S. Evaluation of the estrogenic activity of the wild Pueraria mirifica by vaginal cornification assays. J Reprod Dev. 2007;53:385–93.PubMedCrossRef

13.

Cherdshewasart W, Sriwatcharakul S, Malaivijitnond S. Variance of estrogenic activity of the phytoestrogen-rich plant. Maturitas. 2008;61:350–7.PubMedCrossRef

14.

Urasopon N, Hamada Y, Asaoka K, Poungmali U, Malaivijitnond S. Isoflavone content of rodent diets and its estrogenic effect on vaginal cornification in Pueraria mirifica-treated rats. Sci Asia. 2008;34:371–6.CrossRef

15.

Sookvanichsilp N, Soonthornchareonnon N, Boonleang C. Estrogenic activity of the dichloromethane extract from Pueraria mirifica. Fitoterapia. 2008;79:509–14.PubMedCrossRef

16.

Siangcham T, Saenphet S, Saenphet K. Estrogen bioassay of Pueraria mirifica Airy Shaw & Suvatabandhu. J Med Plant Res. 2010;4:741–4.

17.

Malaivijitnond S, Tungmunnithum D, Gittarasanee S, Kawin K, Limjunyawong N. Puerarin exhibits weak estrogenic activity in female rats. Fitoterapia. 2010;81:569–76.PubMedCrossRef

18.

Yepuru M, Eswaraka J, Kearbey JD, Barrett CM, Raghow S, Veverka KA, et al. Estrogen receptor-(beta)-selective ligands alleviated high-fat diet- and ovariectomy-induced obesity in mice. J Biol Chem. 2010;285:31292–303.PubMedCrossRef

19.

Tsai YC, Lee YM, Lam KK, Wu YC, Yen MH, Cheng PY. The role of hypothalamic AMP-activated protein kinase in ovariectomy-induced obesity in rats. Menopause. 2010;17:1194–200.PubMedCrossRef

20.

Zhang YB, Zhang Y, Li LN, Zhao XY, Na XL. Soy isoflavone and its effect to regulate hypothalamus and peripheral orexigenic gene expression in ovariectomized rats fed on a high-fat diet. Biomed Environ Sci. 2010;23:68–75.PubMedCrossRef

21.

Chansakaow S, Ishikawa T, Sekine K, Okada M, Higuchi Y, Kudo M, et al. Isoflavonoids from Pueraria mirifica and their estrogenic activity. Planta Med. 2000;66:572–5.PubMedCrossRef

22.

Chansakaow S, Ishikawa T, Seki H, Sekine K, Okada M, Chaichantipyuth C. Identification of deoxymiroestrol as the actual rejuvenating principle of “Kwao Keur”, Pueraria mirifica. The known miroestrol may be an artifact. J Nat Prod. 2000;63:173–5.PubMedCrossRef

23.

Malaivijitnond S. Medical applications of phytoestrogens from Pueraria mirifica Thai herb. Front Med. 2012;6:8–21.PubMedCrossRef

24.

Trisomboon H, Malaivijitnond S, Watanabe G, Taya K. Ovulation block by Pueraria mirifica: a study of its endocrinological effect in female monkeys. Endocrine. 2005;26:33–9.PubMedCrossRef

25.

Trisomboon H, Malaivijitnond S, Watanabe G, Cherdshewasart W, Taya K. The Estrogenic effect of Pueraria mirifica on gonadotrophin levels in aged monkeys. Endocrine. 2006;29:129–34.PubMedCrossRef

26.

Humason GL. Animal tissue techniques. USA: WH Freeman and Company; 1972.

27.

Pederson SB, Fuglsig S, Sjogren P. Identification of steroid receptors in human adipose tissue. Eur J Clin Invest. 1996;26:1051–6.CrossRef

28.

Anwar A, McTernan PG, Anderson LA, Askaa J, Moody CG, Barnett AH, et al. Site-specific regulation of oestrogen receptor-alpha and -beta by oestradiol in human adipose tissue. Diabetes Obes Metab. 2001;3:338–49.PubMedCrossRef

29.

Breton AB, Cockrum RR, Austin KJ, Cammack KM, Ford SP, Hess BW, et al. Hypothalamic expression of genes for appetite regulators and estrogen α estrogen β and leptin receptors in obese dams and their fetuses. Animal. 2011;5:1944–8.PubMedCrossRef

30.

Joyner JM, Hutley LJ, Cameron DP. Estrogen receptors in human preadipocytes. Endocrine. 2001;15:225–30.PubMedCrossRef

31.

Nazz A, Yellayi S, Zakroczymski MA, Bunick D, Doerge DR, Lubahn DB, et al. The soy isoflavone genistein decreases adipose deposition in mice. Endocrinology. 2003;144:3315–20.CrossRef

32.

Silva LE, Castro M, Amaral FC, Antunes-Rodrigues J, Elias LL. Estradiol-induced hypophagia is associated with the differential mRNA expression of hypothalamic neuropeptides. Braz J Med Biol Res. 2010;43:759–66.PubMedCrossRef

33.

Saruhan BG, Ozdemir N. Effect of ovariectomy and of estrogen treatment on the adrenal gland and body weight in rats. Saudi Med J. 2005;26:1705–9.PubMed

34.

Mehasseb MK, Panchal R, Taylor AH, Brown L, Bell SC, Habiba M. Estrogen and progesterone receptor isoform distribution through the menstrual cycle in uteri with and without adenomyosis. Fertil Steril. 2011;95:2228–35.PubMedCrossRef

35.

Kuiper GGJM, Carlsson B, Grandien K, Enmark E, Haggblad J, Nilsson S, et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptor α and β. Endocrinology. 1997;138:863–70.PubMed

36.

Kuiper GGJM, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor β. Endocrinology. 1998;139:4252–63.PubMed

37.

Ashby J, Odum J, Paton D, Lefevre PA, Beresford N, Sumpter JP. Re-evaluation of the first synthetic estrogen, 1-keto-1,2,3,4-tetrahydrophenanthrene, and bisphenol A using both the ovariectomized rat model used in 1933 and additional assays. Toxicol Lett. 2000;115:231–8.PubMedCrossRef

38.

Diel P, Schulz T, Smolnikar K, Strunck E, Vollmer G, Michna H. Ability of xeno- and phytoestrogens to modulate expression of uterotropic activity. J Steroid Biochem Mol Biol. 2000;73:1–10.PubMedCrossRef

39.

Stroheker T, Chagnon MC, Pinnert MF, Berges R, Canivenc-Lavier MC. Estrogenic effects of food wrap packaging xenoestrogens and flavonoids in female Wistar rats: a comparative study. Reprod Toxicol. 2003;17:421–32.PubMedCrossRef

40.

Pessina MA, Hoyt RF Jr, Goldstein I, Traish AM. Differential regulation of the expression of estrogen, progesterone, and androgen receptors by sex steroid hormones in the vagina: immunohistochemical studies. J Sex Med. 2006;3:804–14.PubMedCrossRef

41.

Traish AM, Kim SW, Stankovic M, Goldstein I, Kim NN. Testosterone increases blood flow and expression of androgen and estrogen receptors in the rat vagina. J Sex Med. 2007;4:609–19.PubMedCrossRef

42.

Cornwell T, Cohick W, Raskin I. Dietary phytoestrogens and health. Phytochemistry. 2004;65:995–1016.PubMedCrossRef

43.

Adlercreutz H. Western diet and western diseases: some hormonal and biochemical mechanisms and associations. Scand J Clin Lab Invest. 1990;201(Suppl):3–23.

44.

Ho SC, Chan SG, Yi Q, Wong E, Leung PC. Soy intake and the maintenance of peak bone mass in Hong Kong Chinese women. J Bone Miner Res. 2001;16:1363–9.PubMedCrossRef

45.

Chiechi LM, Secreto G, D’Amore M, Fanelli M, Venturelli E, Cantatore F, et al. Efficacy of a soy rich diet in preventing postmenopausal osteoporosis: the Menfis randomized trial. Maturitus. 2002;42:295–300.CrossRef

46.

File SE, Jarrett N, Fluck E, Duffy R, Casey K, Wiseman H. Eating soya improves human memory. Psychophamacology. 2001;157:430–6.CrossRef

47.

Rose DP, Boyar AP, Wynder EL. International comparisons of mortality rates for cancer of the breast, ovary, prostate, and colon, and per capita food consumption. Cancer. 1986;58:2363–71.PubMedCrossRef

48.

Al-Azzawi F, Wahab M. Effectiveness of phytoestrogens in climacteric medicine. Ann NY Acad Sci. 2010;1205:262–7.PubMedCrossRef

49.

Cherdshewasart W, Sriwatcharakul S. Major isoflavonoid contents of the 1-year-cultivated phytoestrogen-rich herb, Pueraria mirifica. Biosci Biotechnol Biochem. 2007;71:2527–33.PubMedCrossRef

Title: Simple, sensitive and reliable in vivo assays to evaluate the estrogenic activity of endocrine disruptors
Authors: Kanya Anukulthanakorn
Sukanya Jareonporn
Suchinda Malaivijitnond
Publication date: 01-01-2014
Publisher: Springer Japan
Published in: Reproductive Medicine and Biology / Issue 1/2014
Print ISSN: 1445-5781
Electronic ISSN: 1447-0578
DOI: https://doi.org/10.1007/s12522-013-0161-1

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Simple, sensitive and reliable in vivo assays to evaluate the estrogenic activity of endocrine disruptors

Abstract

Purpose

Methods

Results

Conclusions

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Purpose

Methods

Results

Conclusions

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